ENVIRONMENTAL SCIENCE, ENGINEERING AND TECHNOLOGY

LAGOONS: BIOLOGY, MANAGEMENT

AND ENVIRONMENTAL IMPACT

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 ENVIRONMENTAL SCIENCE, ENGINEERING
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 ENVIRONMENTAL SCIENCE, ENGINEERING AND TECHNOLOGY

LAGOONS: BIOLOGY, MANAGEMENT

AND ENVIRONMENTAL IMPACT

ADAM G. FRIEDMAN
EDITOR

Nova Science Publishers, Inc.

New York
Copyright © 2011 by Nova Science Publishers, Inc.

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LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA

Lagoons : biology, management, and environmental impact / editor, Adam G.
Friedman.
p. cm.
Includes index.
ISBN 978-1-61122-086-5 (eBook)
1. Lagoons. I. Friedman, Adam G.
GB2203.2.L34 2010
551.46'18--dc22
2010033077

Published by Nova Science Publishers, Inc. † New York

 CONTENTS

Preface vii
Chapter 1 Metabolic and Structural Role of Major Fish Organs as an Early
Warning System in Population Assessment 1
C. Fernandes , A. Afonso and M.A. Salgado
Chapter 2 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns
and Biomonitoring Implications 39
F. Frontalini, E. Armynot du Châtelet, J.P. Debenay, R. Coccioni
and G. Bancalà
Chapter 3 Coastweb, a Foodweb Model Based on Functional Groups for
Coastal Areas Including a Mass-Balance Model for Phosphorus 73
Lars Håkanson and Dan Lindgren
Chapter 4 Form and Functioning of Micro Size Intermittent Closed Open
Lake Lagoons (ICOLLs) in NSW, Australia 119
W. Maher, K. M. Mikac, S. Foster, D. Spooner and D. Williams
Chapter 5 Waterbirds as Bioindicators in Coastal Lagoons: Background,
Potential Value and Recent Research in Mediterranean Areas 153
Francisco Robledano Aymerich and Pablo Farinós Celdrán
Chapter 6 How Important are Local Nutrient Emissions to Eutrophication in
Coastal Areas Compared to Fluxes from the Outside Sea? A Case-
Study Using Data from the Himmerfjärden Bay in the Baltic Proper 185
Lars Håkanson and Maria I. Stenström-Khalili
Chapter 7 Environmental Consequences of Innovative Dredging in Coastal
Lagoon for Beach Restoration 219
Emmanuel Lamptey
vi Contents

Chapter 8 State of Knowledge of the Trophic State of Worldwide Lagoon

Ecosystems: Leading Fields and Perspectives 249
Monia Renzi, Antonietta Specchiulli, Raffaele D’Adamo
and Silvano E. Focardi
Chapter 9 Treatment of Contaminated Sediments by Chemical Oxidation 279
Sabrina Saponaro, Alessandro Careghini, Kevin Gardner
and Scott Greenwood
Chapter 10 Reconstruction of the Eutrophication in the Gulf of Finland Using a
Dynamic Process-Based Mass-Balance Model 301
Lars Håkanson
Chapter 11 Environmental Management and Sustainable Use of Coastal
Lagoons Ecosystems 333
Rutger de Wit, Behzad Mostajir, Marc Troussellier
and Thang Do Chi
Chapter 12 Involvement of Local Users is the Overlooked Background
Information for Improving Implementation of
Conservation Solutions in Coastal Lagoon
Management: The Case of the Ichkeul
National Park (Tunisia) 351
Caterina Casagranda
Chapter 13 Birth, Evolution and Death of a Lagoon: Late Pleistocene to
Holocene Palaeoenvironmental Reconstruction of the Doñana
National Park (SW Spain) 371
F. Ruiz,, M. Pozo, M. I. Carretero, M. Abad
M. L. González-Regalado, J. M. Muñoz, J. Rodríguez-Vidal,
L. M. Cáceres, J. G. Pendón, M. I. Prudêncio and M. I. Dias
Chapter 14 The Alvarado Lagoon – Environment, Impact, and Conservation 397
Jane L. Guentzel, Enrique Portilla-Ochoa,
Alejandro Ortega-Argueta, Blanca E. Cortina-Julio
and Edward O. Keith
Chapter 15 Adaptive Lagoon Fishery Development through Sustainable
Livelihoods Approach: A Case Study of Chilika Lagoon, India 417
Shimpei Iwasaki
Chapter 16 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 435
Yoko Niimura, Hiroaki Saito, and Satoru Taguchi
Chapter 17 The Evaluation of Some Limnological Features of the Lagoon
Lakes in European Part of Turkey 457
Belgin Çamur-Elipek and Timur Kırgız
Index 475
 PREFACE

Coastal lagoons are particularly complex environments in which the transition between
marine and continental waters is gradual, due to the continuity of the aquatic habitat. They are
characterized by major fluctuations in chemical and physical parameters, which reflect
multiple interactions between the distance to the sea, water depth, the nature of the sediment,
organic matter quality, hydrodynamic turnover time, tidal currents, wind forced currents,
volume lost by evaporation, and gravitational circulation. This book presents current research
from across the globe in the study of lagoons, their biology, management and environmental
impact.
Chapter 1- There are thousands of pollutants that affect aquatic environment and their
effects have long been a concern and cause of research. This number grows annually since
new compounds and formulations are synthesized. At present the concept of pollution
involves knowledge of environmental fate and effects of chemical pollutants and their
impacts on both, ecosystems and on social and economic development.
Some aquatic environments are vital because of their critical ecological and economic
importance. There are numerous lakes, lagoons and coastal lagoons playing a social and
economic role on adjacent human populations, as they support fishing and recreational
activities, and an ecological role, as they also support a characteristic flora and fauna,
becoming important habitats. Additionally, several of these fresh waters reservoirs become a
vital supply of potable water.
In many cases, even in sub-lethal concentrations, aquatic pollutants affect structure and
normal functioning of natural populations as they can cause impacts at multiple levels of
organization, including cells, tissues, organs, individuals and community level. Several
aquatic species can be used to study these issues and fish has been proved to be a suitable
test-organism. Fish organs, such as liver, spleen and kidney can be very helpful to understand
the response mechanisms to pollutant exposure. Fish liver is the main target organ of dietary
route and the central metabolic organ, where detoxification mechanisms occur; spleen is
involved in development of circulating blood cells, as well as immunity; and kidney is
involved with excretion and thus, with electrolyte balance and acid-base regulation.
Moreover, the anterior part of kidney supports the main pool of several fish leukocyte types.
Assessment of coastal and shallow lagoon waters is a top priority among environmental
monitoring activities, due to high ecological and economical importance of these relevant
resources. In particular in enclosed communities, such as lakes and lagoons, this issue is
enhanced according to the abundance and diversity of wildlife and increased need for water
quality. Fish are relatively sensitive to changes in the environment and toxic effects of
viii Adam G. Friedman

pollutants may start to occur in the cell and in metabolic pathways, before significant
alterations in behaviour or morphology can be identified.
The knowledge of normal metabolic processes of these major fish organs and alterations
induced by exposure to pollutants can be a tool for an early warning system in the evaluation
and analysis of the wealth of a fish population and their natural environment.
Chapter 2- Coastal lagoons are particularly complex environments in which the transition
between marine and continental waters is gradual, due to the continuity of the aquatic habitat.
They are characterized by major fluctuations in chemical and physical parameters, which
reflect multiple interactions between the distance to the sea, water depth, the nature of the
sediment, organic matter quality, hydrodynamic turnover time, tidal currents, wind forced
currents, volume lost by evaporation, and gravitational circulation. Moreover, these
ecosystems are often subjected to a great deal of anthropogenic impact, which further
complicates our understanding of these habitats. Comparative studies of lagoonal
environments essentially require the utilization of organisms that are distributed worldwide
and occur in high density populations in most of the benthic niches. This is certainly the case
for foraminifers which, as lower trophic level members, are crucial to the biological
community and ideal candidates for comprehensive habitat assessment. Some widespread
paralic benthic foraminiferal species are present from temperate macrotidal estuaries to
tropical microtidal lagoons, thus enabling comparative studies of environmental conditions to
be conducted.
Since lagoons are increasingly affected by environmental stress and degradation due to
pollution and other anthropogenic factors, there is a pressing need to develop a set of
indicators and monitoring approaches with which to assess their health.
A large number of research programs have addressed these issues within various regions,
and studies of foraminiferal assemblages have produced very useful, comprehensive datasets
on environmental and biotic conditions.
This paper is a review of what is known about the foraminiferal assemblages living in
lagoons, including their distribution according to environmental parameters and their value
when it comes to assessing environmental quality in these ecosystems.
Chapter 3- It is important to develop tools to get realistic predictions of how, e.g., the
loading of contaminants and future climate changes may affect the structure and function of
aquatic ecosystems. The CoastWeb-model presented in this work in meant as such a tool.
CoastWeb is a process-based mechanistic foodweb model for coastal areas (the ecosystem
scale) and includes a mass-balance model (CoastMab) for phosphorus. The model is based on
ordinary differential equations and gives monthly calculations of production and biomasses
for ten functional groups (phytoplankton, benthic algae, macrophytes, bacterioplankton,
herbivorous and predatory zooplankton, zoobenthos, jellyfish, prey and predatory fish).
CoastMab calculates in- and outflow, sedimentation, diffusion, resuspension, up- and
downward mixing, biouptake and retention of phosphorus in biota. There are algorithms for,
e.g., migration of fish and plankton between the given coastal area and the sea and the
influence of exposure on macrophyte cover . The paper presents case-studies on
eutrophication, overfishing and toxic contamination illustrating the potential of CoastWeb as
a tool for sustainable coastal management. Increased nutrient loading will cause several
changes to the foodweb characteristics of the studied coastal area. Some of these could be
expected without a model, but here they have been quantified using a general foodweb model.
The model accounts for different compensatory effects that are difficult to quantify without a
 Preface ix

model. The case-study on overfishing indicates that increased fishing will likely affect the
studied coastal system marginally because the migration of fish from the sea is large in the
studied coastal area. The case-study on toxic contamination shows that a reduction of
zoobenthos biomass will have clear effects of fish production and biomass in the studied
coastal area.
Chapter 4- ICOLLs are considered to be one of the most ecologically productive
ecosystems on earth. Similar to other coastal water bodies, ICOLLs lie at the interface of
marine, freshwater and terrestrial systems and therefore represent highly dynamic transition
zones between river/creek catchments and near-shore coastal waters. ICOLLs often act as net
sinks of land derived sediments and nutrients; mature systems are believed to act as a source
of organic material and nutrients to the adjacent sea. Suzuki et al., (1998) describes ICOLLs
as having unique structural and functional characteristics as a consequence of their position in
the landscape, thus having large spatial and temporal variability in their environmental and
(consequently their dependant) biological variables.
The focus for this chapter is micro size ICOLLs, classified as any coastal water body that
has:
(i) the presence of barrier beach, spit or series of barrier islands that can restrict oceanic
exchange;
(ii) a surface water area of less than 0.5 km2
(iii) the retention of all or the majority of the water mass within the lagoon during low
tide in the adjacent sea; and
(iv) the capacity of to remain brackish to fully saline either by percolation through and/or
overtopping through inlet/outlet channels.
ICOLLs can be viewed in a hierarchical manner, with the ocean and catchment
influencing other smaller scale processes. Characteristics of the catchment and oceanic
regimes influence water quality, tidal regime, stream flow, sediment delivery and seston
within an ICOLL. Flow regimes and sediment loads in turn affect ICOLL morphology and
sediment composition, such as nutrient status and organic matter composition. Alterations in
catchment flow can either increase the residence time of water within an ICOLL increasing
the susceptibility to eutrophication or decrease the residence time possibly leading to nutrient
limiting conditions. In turn, these attributes determine the biological diversity and functioning
of these systems.
Chapter 5- Among the biological components of estuarine systems and other transitional
coastal waters, waterbirds are probably the group that has been monitored more intensively
and throughout longer time series, especially due to the use of citizen science. Moreover,
several authors have reviewed, organized and analyzed critically the role and potential use of
waterbirds as bioindicators. Recently, academic research has encouraged more intensive
monitoring of waterbirds in the context of bioindication in wetlands and coastal waters.
However, in the particular case of coastal lagoons, birds have received little attention
compared to research efforts directed to other taxa, ignoring their important role as top
predators and underestimating their contribution to various ecological processes. Few studies
have included waterbirds as integral components of the food webs in lagoons, relating them to
other biota. However, recent studies show that waterbirds respond to changes imposed by a
variety of stressors, constituting warning signals against undesirable changes. Waterbirds can
be used as bioindicators both at suborganismic and at population-community-ecosystem
levels. Either approach requires that the relationships birds establish with habitats and with
x Adam G. Friedman

the ensemble of the lagoon‘s biocoenosis are clarified. As these relationships and the
bioindicator role of waterbirds are established in more detail, stands out their usefulness as
indicators of impairment in coastal lagoons of similar characteristics, subject to similar
impacts with time lags. Studies on the waterbird community of the Mar Menor Lagoon (SE
Spain) show the long-term response of populations to variables related to eutrophication and
biological changes (proliferations of jellyfish and changes in fish stocks). Studies based on
community variation in relation to internal environmental gradients of the lagoon, show
spatial responses that can be mapped, and provide a basis for building indices of integrity.
This is a relevant issue given the paucity of studies that explore and apply the indicator value
of birds in conservation and environmental evaluation, particularly in the Mediterranean and
elsewhere in temperate latitudes. Recent studies that integrate the monitoring of different
physico-chemical and biotic variables of the lagoon with waterbird numbers and distribution,
and research on waterbird trophic ecology based on stable isotope analysis, aim at clarifying
the role of waterbirds as top-down controllers in the food webs of coastal lagoons. A role
whose monitoring is also important from an applied perspective, given the potential of some
waterbirds like cormorants to become conflicting species (through their interaction with
fisheries). The application of these monitoring schemes to other Mediterranean lagoons
emerges as a valuable tool for assessing and preventing changes in the ecological status of
these systems with respect to relatively undisturbed, reference conditions.
Chapter 6- The basic aim of this work has been to present a general approach to quantify
how coastal systems are likely to respond to changes in nutrient loading. The conditions in
most coastal areas depend on nutrients emissions from points sources, diffuse sources, river
input and the exchange of nutrients and water between the given coast and the outside sea, but
all these fluxes can not be of equal importance to the conditions in the given coastal area, e.g.,
for the water clarity, primary production and concentration of harmfull algae (such as
cyanobacteria). This work describes how a general process-based mass-balance
model (CoastMab) has been applied for the case-study area, the Himmerfjärden Bay on the
Swedish side of the Baltic Proper. The model has previously been extensively tested and
validated for salt, phosphorus, suspended particulate matter, radionuclides and metals in
several lakes and coastal areas. The transport processes quantified in this model are general
and apply for all substances in all aquatic systems, but there are also substance-specific parts
(mainly related to the particulate fraction and the criteria for diffusion). This is not a model
where the user should make any tuning or change model constants. The idea is to have a
model based on general and mechanistically correct algorithms describing the transport
processes (sedimentation, resuspension, diffusion, mixing, etc.) at the ecosystem scale and to
calculate the role of the different transport processes and how a given system would react to
changes in inflow related to natural variations and anthropogenic reductions of water
pollutants. The results presented in this work indicate that the conditions in the
Himmerfjärden Bay are dominated by the water exchange between the bay and the outside
sea. The theoretical surface-water retention time is about 19 days, as determined using the
mass-balance model for salt, which is based on comprehensive and reliable empirical data.
This means that although this bay is quite enclosed, it is still dominated by the water
exchange towards the sea. Local emissions of nutrients to the Himmerfjärden Bay are small
compared to the nutrient fluxes from the sea. If the conditions in this, and many similar bays,
are to be improved, it is very important to lower the nutrient concentrations in the outside sea.
 Preface xi

Chapter 7- Evidence suggests that hydraulic dredging is accompanied by considerable

adverse environmental impacts on the receiving ecosystem especially on the benthos and
water quality. Recently, innovative dredging is designed to minimise environmental impacts
and enhance the ecological settings. Evaluations of environmental consequences of such
innovative dredging are essential to quantify the ecological benefits and the associated
impacts to ensure good environmental management. Congruently, innovative dredging
(‗design with nature‘ principle) in a large tropical coastal lagoon in Ghana (Keta lagoon),
West Africa, was assessed Before, During and After dredging operations on spatio-temporal
scales to ascertain the environmental impacts on the macrobenthic fauna, shorebirds and
water quality. A total of 9091 million cubic meter of sediment was removed from the 8m
stretch of the lagoon for beach nourishment, land reclamation and creation of habitat islands.
The macrobenthic fauna was sampled once in 2000 (Before), 2001 (During) and 2002 (After)
along seven stations (A-0 to G-0 of 1-km interval) in the dredged channel. Water quality was
assessed at the subsurface and bottom layers quarterly from June, 2001 to September, 2002.
The shorebirds community abundance were quantified monthly from August 2000 to 2002,
but only parallel data from August-December (peak periods of shorebirds abundance) of each
year (2000-2002) was used for statistical analyses.
The results demonstrate that dredging had initial adverse effects on numerical abundance
of macrobenthic fauna but with evidence of recovery a year after the dredging (2002). Species
recorded in 2001(During Dredging) and 2002 (After Dredging) were very similar in terms of
composition particularly in the wet periods, suggesting the influence of seasonal
environmental factors. The abundance of the species showed significant spatio-temporal
variations (p<0.05). The macrobenthic fauna was dominated by opportunistic species of the
family Capitellidae. Although, Nepthys lyrochaeta revealed higher frequency of occurrence
(52%), there was significant (p<0.05) decrease in abundance after dredging (2002).
Conversely, Notomastus cf. latericeus depicted significant (p<0.05) increase (recovery) after
dredging (2002).
There was no apparent impact on coastal avifauna although numerical abundance of
wader group decreased from 78% in 2000; 69% in 2001 to 51% in 2002. Conversely, terns
showed increased abundance from 17% in 2000, 21% in 2001 and 47% in 2002 indicating
positive impact. The shorebirds placed in the ‗others‘ category experienced peak and trough
between the period (6% in 2000; 10% in 2001, and 2% in 2002). In general mean numerical
abundance of the shorebirds increased from 8.8% in 2000 (Before) to 81.5% in 2002 (After)
of the periods.
Temporal and spatial variability occurred in the physicochemical parameters measured
(e.g., salinity, total dissolved solids, total suspended solids and sulfate). However, elevated
turbidity occurred in localised areas along the fetch during the dredging operation. The results
of the analysis presented are pertinent to several questions, such as what are the expected
ecological benefits of innovative dredging and adverse impacts on the receiving ecosystem.
Chapter 8- In the latest years, the environmental research has focused on studying the
water quality of marine-coastal ecosystems and on the main consequences of human activities
within these environments, their surroundings and catchments. Among aquatic water systems,
coastal lagoons are particularly vulnerable to water-quality deterioration, due to their
restricted water exchange. In addition, they are used as nursery areas for aquaculture and
fisheries exploitations, which represent the main economic relevance for local inhabitants.
Protection of the ecological status of worldwide lagoons has to be the key purpose of the
xii Adam G. Friedman

International directives, as coastal lagoons are naturally stressed ecosystems which suffer
from frequent environmental disturbances and fluctuations related to their geomorphologic
characteristics, general hydrodynamics, abiotic and biological parameters. The main keys of
ecological research studies in coastal lagoons are represented by the need to improve the
general knowledge on system dynamics focusing on the leading aspects useful to develop
eco-compatible management plans which allow us to preserve their productivity avoiding
losses of biodiversity related to the increase of bioavailabile nutrients. The increasing number
of ecosystems exhibiting frequently a progressive decline of water quality has led
environmental researchers and managers to identify eutrophication as a major worldwide
problem. The development of simple and not expensive well calibrated indices of
eutrophication represents one of the most actual ecological fields in which researchers are
involved. Many European countries have developed within the Water Framework Directive
(CE 2000/60), an environmental quality classification scheme in order to assess the trophic
state and water quality through the use of specific indices based on environmental factors.
Our aim is to evaluate nowadays the state of knowledge related to eutrophication of
worldwide lagoon ecosystems, highlighting the main fields of interest and major problems.
Leading problems are related to the choise of useful indices, their calibration, their efficiency
in describing dynamics of lagoons characterized by different trophic levels and the selection
of the opportune pristine ecosystem as reference for lagoon classifications related to water
quality.
Chapter 9- A number of different approaches can be used when managing contaminated
sediments depending on site-specific conditions, sediment characteristics, mix of conta-
minants in the sediment and local regulations. Ex situ management options can include
landfill disposal or, more generally, the application of remediation treatments for beneficial
reuse, which may improve the economics of management and/or be required to meet
regulatory requirements.
Chemical oxidation involves the use of chemical additives to remediate sediments
contaminated by organic compounds. Due to electron transfers between two (or more)
compounds, pollutants are degraded into less toxic or biologically available chemical forms.
Chemical oxidation also changes the pH and redox conditions of the treated system, which
may also alter the mobility of the target and other compounds and elements.
Several different oxidizing agents are available that result in different effectiveness on
different pollutants. The most commonly used oxidants are Fenton-like reagents (hydrogen
peroxide catalyzed by bivalent iron ions), ozone, permanganate, and persulfate. Recent
laboratory studies have also shown good results in peroxy-acid systems (an organic acid
mixed with hydrogen peroxide) to degrade compounds such as Polycyclic Aromatic
Hydrocarbons (PAHs).
Oxidation is a non-selective process. Therefore, the oxidizable material within the
sediment (natural organic matter, detritus, etc.), which may be a significant percentage of the
sediment mass, can consume the oxidizing agent. Moreover, many different reactions can
occur (acid/base reactions, sorption/desorption, dissolution, hydrolysis, ion exchange,
oxidation/reduction, precipitation, etc.). Pollutant removal efficiency strictly depends on the
contamination (pollutants, concentrations) and the sediment being treated (physical-chemical
properties and composition). Laboratory tests are always necessary to evaluate the feasibility
of the treatment to select the best oxidizer and the proper treatment configuration.
 Preface xiii

This chapter reports on laboratory batch tests conducted on sediments from Porto
Marghera (Italy) and New York/New Jersey Harbor (NY, USA). Porto Marghera sediments
were treated with Fenton-like reagents to remove total petroleum hydrocarbons, PAHs, and
polychlorinated biphenyls. Different oxidizers (Fenton-like reagents, persulfate, and peroxy-
acid) were used for the New York City sediments polluted by PAHs. For the latter sediments,
the leachability of metals in the treated sediments and filtration resistance were also assessed
to understand potential unintended consequences of treatment on metal availability and
sediment dewatering operations.
Chapter 10- The Gulf of Finland is a large bay in the Baltic Sea where major changes
have taken place during the last 100 years. The Secchi depth has, for example, decreased from
more than 7 m to about 5 m. The basic aim of this work has been to try to reconstruct the
development that has taken place in this bay during the last 100 years. Since the conditions in
the Gulf of Finland depend very much on both the river input of nutrients directly to the bay
and the exchange of nutrients and water between the bay and the Baltic Proper, this work has
focused on such interactions. The work describes how a general process-based mass-balance
model (CoastMab) has been applied for the Baltic Proper and the Gulf of Finland. The model
has previously been extensively tested and validated for phosphorus, suspended particulate
matter, radionuclides and metals in several lakes and coastal areas. The transport processes
quantified in this model are general and apply for all substances in all aquatic systems, but
there are also substance-specific parts (mainly related to the particulate fraction and the
criteria for diffusion). This is not a model where the user should make any tuning or change
model constants. The idea is to have a model based on general and mechanistically correct
algorithms describing the monthly transport processes (sedimentation, resuspension,
diffusion, missing, etc.) at the ecosystem scale and to calculate the role of the different
transport processes and how a given system would react to changes in inflow related to
natural changes and anthropogenic reductions of water pollutants. The results presented in
this work indicate that it is possible to remediate the Gulf of Finland and the Baltic Proper to
the conditions that characterized the system 100 years ago. About 7000 tons of phosphorus
(including 1800 tons from the tributaries to the Gulf of Finland) must then be removed on an
annual basis from the present annual tributary load of about 30000 tons to the Baltic Proper.
The trophic conditions in the Baltic Proper have varied relatively little during the last 25-30
years. The most marked changes in Secchi depth in the Gulf of Finland took place between
1920 and 1980.
Chapter 11- This chapter illustrates some of the major issues for the management and use
of coastal lagoons using two examples from the South of France. These are the mesotidal
Bassin d‘Arcachon on the Atlantic coast and the microtidal Etang de Thau on the
Mediterranean (see Figure 1). Oyster-farming is a major use in both lagoons. Coastal lagoons
are part of a coastal landscape and are therefore typical transition zones between the continent
and the sea, characterised by gradients and ecotones. Thus, it is most important to consider
the coastal lagoon ecosystems in the context of the coastal zone and consider their links both
with the ocean as well as with the hinterland. The latter requests a thorough knowledge of the
watershed of the lagoon. Coastal areas, which are commonly defined as the interface or the
transition area between land and sea, are diverse in function, form and dynamics. In general,
these systems are not well defined by strict spatial boundaries and include low lands,
intertidal zones, salt marshes, wetlands, lagoons and their watersheds. From the development
and management point of view, the coastal areas are characterised by the economical
xiv Adam G. Friedman

activities that they support and by the impact of these activities on the environment.
Accordingly, the coastal areas are characterised by i) the production of living resources, ii)
highly diverse human uses including urban development, exploitation of sediments, shipping
and harbours, commercial and sport fishing, aquaculture, tourism, and as a receptacle of
industrial and agricultural waste, iii) their role in providing protection against flooding and by
iv) their biodiversity and role in the functioning of the ecosystems at different spatial levels.
Chapter 12- The Garaet El Ichkeul in Northern Tunisia has long been recognized as one
of the four major wetland areas in the Western Mediterranean basin (MAB Reserve in 1977,
World Heritage and Ramsar site in 1980). The Ichkeul lagoon and its marshes perform
essential ecological functions which are the basis of multiple services that contribute to the
wellbeing and economy of the local community. The villagers living within the core area and
the buffer zone have used to make a living off the land that did not seem to pose any threat to
the functions and services of these ecosystems. However, the construction of dams on the
rivers which provide water for the lake and marshes, as planned by the Tunisian Ministry of
Agriculture for the purposes of agricultural, urban and industrial development, has had an
impact on the ecological character of the site.
The Tunisian authorities, aware of the impact of these dams on the natural environment at
Ichkeul, founded a National Park. Unfortunately, the Park regulations were introduced
without taking properly into account the reality of the socio-economic conditions of local
residents. The lack of rehabilitation measures forced the villagers to exploit the resources in a
non-selective way, which in turn further aggravated the existing pressure on the Park and the
precarious social conditions in which the families survive.
An international multidisciplinary study of all biotic and non-biotic aspects of the
National Park drew up an integrated management plan which was designed to take into
account the socio-economic development of the region. Since then, a number of conservation
measures have been adopted by the Tunisian authorities. They mainly take into account the
flora and fauna but without consultation of the people affected by these measures – a fact that
possibly explains the limited implementation of the management plan proposed by the
multidisciplinary study.
The question is of more than local interest, since similar problems arise throughout the
Mediterranean and elsewhere, i.e. conservation measures have been introduced but the
legislation is not respected in practice. When stakeholders are not involved initially or are
brought into the process at a later date, without the opportunity to provide input, they are
seldom supportive of the policy outcome. This is due in large part to the continued reluctance
of natural scientists and developers to learn from local community practices, as opposed to
management systems established on the basis of scientific facts. However, recent studies on
traditional ways of living off the land claim that the local communities have developed
elaborate processes for sustainably exploiting their resources. Such practices can provide an
important information base for integrated resource management. The goal is: (1) to promote
recognition of the traditional resource practices and the accumulated wisdom as important
features within ecological research, and (2) to stimulate debate about whether their input will
have significance for improving environmental management policy.
Chapter 13- A multidisciplinary study of sediment cores from Doñana National Park (SW
Spain), a broad region of wetlands in SW Spain, provides the base for the reconstruction of
the main palaeoenvironmental changes that occurred in the Guadalquivir estuary since OIS 3.
The facies analysis differentiates six main facies, deposited in freshwater pond and marsh
 Preface xv

(FA-1: laminated silt), brackish marsh or the periphery of a brackish lagoon (FA-2: greyish
silt), a shallow lagoon (FA-3: green silt and clay), the marine connection of this lagoon (FA-
4: yellow silt) or sandy spit (FA-6: yellow sand), whereas FA-5 includes bioclastic silt and
sand with a tsunamigenic origin.
The vertical arrangement of these facies, their dates and a detailed comparison with
previous works permit to delimitate ten phases in the Late Pleistocene to Holocene evolution
of this lowland. In the oldest phase (OIS 3), this area was occupied by freshwater marshes.
Phase 2 (OIS 2) was characterized by the alternation of freshwater and brackish marshes,
partly enclosed by aeolian units. During the third phase (Early Holocene), the brackish
marshes constituted the northern limit of a broad lagoon that extended along the present-day
inner shelf. The sea-level highstand of the Present Interglacial (Flandrian transgression, phase
4: ~6.5 cal BP) caused the inundation of this area, occupied by an open lagoon. Between 6.5
and 4.6 cal ka (phase 5), incipient brackish marshes emerged along the margins of this lagoon
and a first tsunamigenic event (5100-4800 cal BP) eroded partially the Doñana spit. The
following phase (4.6-3.7 cal ka) was relatively quiet, with predominance of infilling
processes. This calm scenario was interrupted by a new period of instability (phase 7: 3.7-3
cal ka), with two new high-energy events. The progressive infilling is the main feature of
phase 8 (3-2.2 cal ka), with the emersion of new brackish marshes and a decreasing depth in
the adjacent lagoon. The first historical tsunamis (phase 9: 2.2-1.9 cal ka) induced the
creation of washover fans and bioclastic ridges overlying the previous marshes. Since 1.9 cal
ka (phase 10), the growing of the Doñana spit and the fluvial-tidal sediment inputs caused an
important filling of the Guadalquivir estuary (Doñana National Park), only interrupted by new
tsunami records (~1.8-1.5 cal ka).
Chapter 14- The Alvarado Lagoon System (ALS) in south-central Veracruz State,
Mexico, is a mangrove dominated coastal wetland formed by the confluence of the Acula,
Blanco, Limon and Papaloapan rivers. The ALS has a maximum width of 4.5 km, a mean
surface area of 62 km2, and is connected to the Camaronera Lagoon by a narrow channel and
to the Gulf of Mexico (GOM) via a 0.4 km wide sea channel. Water samples were collected
during the wet (September 2005) and dry (March 2003 and 2005) seasons. Salinity ranged
from 1-25.5 psu and pH was slightly alkaline (7.6-8.6). Levels of total organic carbon (TOC),
total mercury (Hg), and total suspended solids (TSS) ranged from 3.9-20.9 mg C/L, 0.92-26.1
ng Hg/L, and 1-39.2 mg TSS/L, respectively. The strong correlation (R2=0.71; P=0.001)
between total mercury and TSS in the water column suggests that particulate matter is a
carrier phase for mercury within the Alvarado and Camaronera Lagoons.
The ALS is one of the most productive estuarine-lagoon systems in the Mexican GOM.
Model studies suggest that primary production by sea grasses provides more energy input to
the ecosystem than detritus, which is contrary to most other Mexican GOM lagoons and
estuaries. In 2004 the ALS was nominated Ramsar site no. 1355 because of its important
biodiversity, ecological attributes, and high resource production. Over 100 fish species have
been collected from the ALS, representing four ecological guilds: marine stenohaline, marine
euryhaline, estuarine, and freshwater fishes. These assemblages have not experienced
significant changes over the past 40 years, but there has been a recent decline in diversity.
Antillean manatees (Trichechus manatus manatus) historically have occurred in the ALS but
were reduced in the 1970s and 1980s by hunting and are now considered endangered. The
rescue of 6 orphan calves between 1998 and 2000 suggests that manatees are reinhabiting the
ALS as a result of conservation measures. Manatees are most commonly sighted in the
xvi Adam G. Friedman

Alvarado Lagoon, Acula River and adjacent lagoons, and are rarely sighted in the Limon
River and adjacent lagoons. To protect the manatees and their habitat an educational program
was developed in 1998 and an assessment of their current status and critical habitat in the
ALS was conducted. Our manatee conservation efforts were recognized in 2001 when
September 7th was officially declared the ―National Day of the Manatee‖ in Mexico. Almost
350 species of birds occur in the ALS, including the Mexican Duck (Anas diazi), which is
undergoing a slow but marked decline due to habitat destruction and overhunting. The largest
threats to the ALS include unsustainable sugar cane cultivation, cattle-ranching, coastal urban
development, oil and gas exploration and exploitation, water pollution by urban waste and
agricultural runoff, and increases in port and tourism industries. Despite the establishment of
government policy and measures to protect the coastal wetlands of ALS, the identified threats
continue to menace the important biodiversity and human well-being of the region.
Chapter 15- Fishery resource in the lagoon environment is the primary form of livelihood
for survival and affects lives in different ways. For centuries, fishermen used to keep a certain
harmony with fishery resources in a traditional manner but they have been faced with various
vulnerabilities in managing fishery resources and their related livelihoods. This chapter
presents a case study of fishing communities in Chilika Lagoon (India) with emphasis on
adaptive capacity to respond to changes in the lagoon environment. It explores pressing
constraints and positive strengths of lagoon fishery development by applying the concept of
Sustainable Livelihoods Approach (SLA).
The research is based on five livelihood assets analysis developed by DFID with due
consideration of vulnerability assessment and institutional contexts. Drawing on Chilika
Lagoon experience, the study revealed that vulnerabilities to fishery livelihoods are affected
by climatic and environmental dimensions as well as by socio-economic and cultural values.
The range of pressing constraints for fishing communities covers not just fishing but also
marketing, schooling, social relations, social infrastructure and environmental and disaster
prevention awareness. This exposure posed grave threats in lowering the capability of people
in the choice of lagoon fishery development, leading to less income generation and its
associated byproducts.
In contrast, the study identified several attempts to cope with the underlying root causes
of failure in resource-based development. The Chilika Development Authority (CDA), for
instance, implemented hydrological interventions in 2000, resulting to fisheries enhancement
with a spectacular increase in fish landings. The elaborations undertaken by CDA also made
great contributions to institutional arrangements for watershed management with a concept of
participatory micro-watershed management that has enabled the upper communities to
upgrade their socio-economic status as well as mitigate the impacts of siltation. Importantly,
innovative activities which are considered to be positive strengths of lagoon fishery
development have been commonly associated with the involvement of various stakeholders to
adjust to the ecological-social-economic system in response to actual or expected impacts.
Finally, this chapter draws some suggestions on adaptive strategies for fishery
development in Chilika Lagoon and potential implications to other lagoons all over the world.
The findings in Chilika Lagoon fisheries provide answers to the enquiry on holistic and
integrated measures to sustain lagoon fisheries by putting forward the principle of SLA.
Chapter 16- A seasonal variability in the vertical flux of ice algae was examined with a
multiple sediment trap during seasonal ice coverage in SaromaKo Lagoon, Hokkaido, Japan.
The multiple sediment traps were moored at 4 m below the water surface and 5 m above the
 Preface xvii

bottom to collect suspended materials at 7 dayintervals for 64 days from February 4 to April
8, 1999. Community structure of ice algae and water column phytoplankton collected with the
sediment traps was determined in terms of both cell abundance and cell volume. For the ice
algal community, Odontella aurita was the most dominant in cell volume, followed by
Pleurosigma spp., Achnanthes spp., Detonula confervacea, Bacteriaosira fagilis, Fragil-
ariopsis spp., and Navicula spp. while Fragilariopsis spp. and Achnanthes spp. were dominant
numerically. Water column phytoplankton were dominant in descending order of cell volume
by Membraneis spp. Thalassiosira spp. Campylodiscus sp., Chaetoceros spp., Amphora spp.,
and Dictyocha speculum, and Alexandrium sp. Mean cell volume ratio of ice algae to total
algae with one standard deviation was 0.30 ± 0.28 and highly variable although a similar ratio
based on cell number was 0.72 ± 0.06. The vertical fluxes of chlorophyll a (Chl a) was
estimated from the volume ratio, and the mean with one standard deviation was 0.90 ± 0.42
mg Chl a m−2 d−1. This suggests that the ecological role of ice algae in a small embayment
should be considered separately from ecosystem in the high latitudes although a total release
of ice algal carbon from the sea ice into a water column could be similar to one in the high
latitudes and only 3 g C m2 in 65 day ice season. Even during the ice coverage, due to a
lateral transport of phytoplankton through two channels from the Sea of Okhotsk, where ice
coverage was always incomplete, the community structure of released ice algae under the sea
ice was modified significantly. A combination of laterally transported water column
phytoplankton and vertically released ice algae into the underlying water column may play a
significant role in the energy transfer to the successful aquaculture of scallops and oysters as
well as other benthos in the shallow coastal water ecosystem.
Chapter 17- Lagoons have perfect hydrodynamic perspective and very sensitive
structures. First of all, the human activities on lagoons have become a major environmental
concern. Any artificial influence to these sensitive areas may cause the destruction of the
natural balance of them.
Turkish coasts have more than 70 lagoon lakes which are formed on about 60 000 ha.
area. European part of Turkey which is also named as ―Turkish Thrace‖ is surrounded by
three different seas: The Marmara Sea, The Black Sea, and The Aegean Sea. The region has a
lot of lagoon lakes (such as Lakes Mert and Erikli are located on the coasts of The Black Sea
in Kırklareli province; Lakes Terkos, Küçükçekmece, and Büyükçekmece are located on the
coasts of The Marmara Sea in İstanbul province; and Lakes Gala, Dalyan, Taşaltı, Işık, Vakıf,
and Tuzla are located on the coasts of The Aegean Sea in Edirne province) which are formed
at different types. Therefore, Turkish Thrace may be considered as a rich area in terms of
lagoon lakes. Furthermore, some lakes are important parts of some National Parks in Turkey.
In this chapter, some limnological features of some lagoon lakes located in European part
of Turkey were evaluated. With this aim, both the results of the previous limnological studies
performed by different researchers (by the authors and/or the others) since 1987 in some
lagoons in the region and the results of the present data on the lakes which were visited on
different dates by the authors at the years 2008 and 2009 for sampling were evaluated.
According to the all data (both from the previous studies and from the present study) some
physicochemical features, salinity levels, some biological data of the lagoons were gathered
in this chapter. Furthermore, rather roughly trophy levels of the lagoons were determined by
the available features which are used to determine the trophy level of the lakes. In conclusion,
this study aimed to gather all data on the lagoons in European part of Turkey by making a
comparison of their former and present status.
xviii Adam G. Friedman

Consequently, the results from the previous limnological studies performed in some
lagoons in the region (a review); the results from the present data on some features of some
lagoons (a research); limnological evaluation on all of the lagoons in the region (an
evaluation) were provided in the present chapter. Thus, it was provided the whole
limnological documents which have been gathered from the lakes at separate times since
1987.
In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 1-38 © 2011 Nova Science Publishers, Inc.

Chapter 1

METABOLIC AND STRUCTURAL ROLE OF MAJOR

FISH ORGANS AS AN EARLY WARNING SYSTEM IN
POPULATION ASSESSMENT

C. Fernandes 1*, A. Afonso 2 and M.A. Salgado 2

1
IPB - Instituto Politécnico de Bragança, CIMO - Centro de Investigação de Montanha,
Campus de Santa Apolónia, Apartado 1038, 5301-854 Bragança, Portugal
2
ICBAS - Instituto de Ciências Biomédicas de Abel Salazar, CIIMAR - Centro
Interdisciplinar de Investigação Marinha e Ambiental, Rua dos Bragas,
289, 4050-123, Porto, Portugal

ABSTRACT
There are thousands of pollutants that affect aquatic environment and their effects
have long been a concern and cause of research. This number grows annually since new
compounds and formulations are synthesized. At present the concept of pollution
involves knowledge of environmental fate and effects of chemical pollutants and their
impacts on both, ecosystems and on social and economic development.
Some aquatic environments are vital because of their critical ecological and
economic importance. There are numerous lakes, lagoons and coastal lagoons playing a
social and economic role on adjacent human populations, as they support fishing and
recreational activities, and an ecological role, as they also support a characteristic flora
and fauna, becoming important habitats. Additionally, several of these fresh waters
reservoirs become a vital supply of potable water.
In many cases, even in sub-lethal concentrations, aquatic pollutants affect structure
and normal functioning of natural populations as they can cause impacts at multiple
levels of organization, including cells, tissues, organs, individuals and community level.
Several aquatic species can be used to study these issues and fish has been proved to be a
suitable test-organism. Fish organs, such as liver, spleen and kidney can be very helpful
to understand the response mechanisms to pollutant exposure. Fish liver is the main target
organ of dietary route and the central metabolic organ, where detoxification mechanisms

* Corresponding author: E-mail: conceicao.fernandes@ipb.pt. Fax: +351 273 325 405.

2 C. Fernandes, A. Afonso and M. A. Salgado

occur; spleen is involved in development of circulating blood cells, as well as immunity;

and kidney is involved with excretion and thus, with electrolyte balance and acid-base
regulation. Moreover, the anterior part of kidney supports the main pool of several fish
leukocyte types.
Assessment of coastal and shallow lagoon waters is a top priority among
environmental monitoring activities, due to high ecological and economical importance
of these relevant resources. In particular in enclosed communities, such as lakes and
lagoons, this issue is enhanced according to the abundance and diversity of wildlife and
increased need for water quality. Fish are relatively sensitive to changes in the
environment and toxic effects of pollutants may start to occur in the cell and in metabolic
pathways, before significant alterations in behaviour or morphology can be identified.
The knowledge of normal metabolic processes of these major fish organs and
alterations induced by exposure to pollutants can be a tool for an early warning system in
the evaluation and analysis of the wealth of a fish population and their natural
environment.

1. INTRODUCTION
There are thousands of pollutants that affect aquatic environment and their effects have
long been a concern and cause of research. This number grows annually since new
compounds and formulations are synthesized. At present the concept of pollution involves
knowledge of environmental fate and effects of chemical pollutants and their impacts on both,
ecosystems and on social and economic development.
Some aquatic environments are vital because of their critical ecological and economic
importance. There are numerous lakes, lagoons and coastal lagoons playing a social and
economic role on adjacent human populations, as they support fishing and recreational
activities, and an ecological role, as they support a characteristic flora and fauna, becoming
important habitats. Additionally, several of these fresh waters reservoirs become a vital
supply of potable water.
Assessment of coastal and shallow lagoon waters is a top priority among environmental
monitoring activities, due to high ecological and economical importance of relevant
resources. In particular in enclosed communities, such as lakes and lagoons, this issue is
enhanced according to the total and the diversity of wildlife and increased need for water
quality.
Fish, compared with invertebrates, are more sensitive to many toxicants and are the
convenient test-objects for water quality assessment and toxicological effects. They are
exposed to pollutants via two main routes, waterborne and dietary and, fish can develop early
signs of toxic effects, even with low contamination levels. Depending on time of exposure,
bioavailability and chemical speciation of pollutants in water, as well as several biotic and
abiotic factors, and synergistic or antagonistic effects, aquatic pollutants can cause impacts on
natural fish populations at multiple levels of organization, including cells, tissues, organs,
individuals and community.
Several biomarker evaluations can be used to monitor environmental activities. Toxicants
body burden in fish tissues can be a helpful indicator of contaminant exposure however it
depends on chemical type and speciation, and metabolic processes such as absorption,
redistribution and compartmentalization into specific tissues and it is not easy to interpret,
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 3

when there are several contaminants involved. On the other hand, the variety of highly
sensitive physiologic mechanisms in fish, together with multiple contaminants exposure, may
lead to an integrated stress response, beyond to their toxic effects at the cell and tissue levels.
The ideal bioaccumulation marker of exposure is one that is chemical-specific, accurately
measurable in trace quantities, measurable in easily sampled biological tissues or by non-
invasive techniques, and correlates well with exposure history (Van der Ost, 2003). However
several biomarker responses have been tested on limited number of compounds, ecosystems,
and for relatively short periods of time. The complementary use of non-specific biomarkers
could bring a wider range of application on environmental monitoring, related to broad-
spectrum of contamination.
Fish organs, such as liver, spleen and kidney can be helpful to evaluate the impact and
understand the response mechanisms to toxic exposure and so can be used as useful
biomarkers in monitoring environmental quality. Fish liver is the main target organ of dietary
route and the central metabolic organ, where detoxification mechanisms occur; spleen is
involved in development of circulating blood cells, as well as immunity; and kidney is
involved with excretion and thus, with electrolyte balance and acid-base regulation.
Moreover, kidney is the major hematopoietic organ and its anterior part (pronefros) supports
the main pool of several fish leukocyte types. The knowledge of normal metabolic processes
of these major fish organs and alterations induced by exposure to pollutants can be a tool for
an early warning system in the evaluation and analysis of the quality of aquatic environment
and fish population wealth.
Biochemical responses to contaminant exposure can include changes in hematologic
parameters and in plasma electrolytes concentrations, as well as histopathologic alterations in
several organs including liver, kidney and spleen.
It is also useful, from both economic and public health points of view, to assess the effect
of chemical pollutants on the fish immune system, and on their vulnerability to infection.

2. LIVER, ITS ROLE IN METABOLISM, ACCUMULATION

AND REGULATION OF XENOBIOTIC COMPOUNDS

Fish liver, the largest visceral organ, plays a major role in metabolism, namely
detoxification, protein and hormone synthesis, glycogen storage and lipid metabolism. It
produces bile, an alkaline compound which aids in digestion, via the emulsification of lipids.
It also performs and regulates a wide variety of biochemical reactions requiring highly
specialized tissues, including the synthesis and breakdown of small and complex molecules,
many of which are necessary for normal vital functions (Wolf and Wolfe, 2005). Liver has
also a key role in regulating vertebrate homeostasis, including reproductive cycle (Rocha et
al., 2003).
There are two general basic types of livers: those that contain pancreatic tissue vs. those
that do not. Fish livers with exocrine pancreatic tissue are often called ―hepatopancreas‖
(Bruslé and Anadon, 1996; Rocha and Monteiro, 1999). Reports on the morphology of fish
liver reflect the structural non-lobulation of the hepatic parenchyma, quite different from
traditional lobulation as reported in the mammalian liver.
4 C. Fernandes, A. Afonso and M. A. Salgado

The liver major vascular organization consist of afferent blood vessels entering by the
hilum – hepatic artery and portal vein – and efferent veins - hepatic vein(s) - emerging at the
anterior surface of the organ, which is not always a single vessel. It is consensual that
hepatocytes are the main component of the fish liver and the most important structural
element of the hepatic parenchyma. Covering the liver, there is a thin (Glisson) capsule that
can bridge through the submesothelial connective tissue with the intrahepatic interstitial one.
The more numerous liver cells are hepatocytes and usually 3 structures appear evidenced:
dense bodies - that include primary and secondary lysosomes and residual bodies -, lipid
droplets and glycogen. Hepatocyte morphology depends on the quantity of storage products,
such as lipid and glycogen, and also on the reproductive cycle, in particular the estrogen-
induced state of vitellogenesis in spawning females (Vethaak, 1993).
Hepatic organization is not exactly the same in all fish species (Robertson and Bradley,
1992) and variations with age, nutritional status, temperature and sexual maturation normally
occurs (Van Bohemen et al., 1981; Storch et al., 1984; Barni et al., 1985). The endocrine
influences, which are strongly connected with the environmental regulation breeding status,
also affect hepatic structure (Rocha and Monteiro, 1999).

Histopathology

Histopathology of fish liver is a monitoring tool that can provide an assessment of the
effects of environmental stressors on fish populations, and it has been considered one of the
most reliable indicators of health impairment on aquatic animals due to anthropogenic
activities (Hinton and Laurén 1990; Stentiford et al. 2003).
Despite some morphological differences among species, liver is essentially similar in all
vertebrates. There are more similarities than differences between fish and mammals in terms
of their macro- and microanatomy, physiological and biochemical characteristics, and
pathologic responses to hepatotoxic substances (Wolf and Wolfe, 2005).
In terms of anatomical differences, fish have a relatively lower liver to body weight ratio,
they have 1/4 to 1/2 less liver perfusion than mammals (Klassen and Plaa, 1967; Gingerich,
1984). But it is however, the hepatocyte architecture one of the relevant features of fish liver
anatomy. The relation of hepatocytes and the blood ductules and canaliculi draining into
them, make the basal and basolateral aspects of hepatocytes the only ones to be directly
exposed to sinusoidal perfusion. Consequently the uptake of some chemicals may be lower.
On the other hand, the blood flow through fish hepatic sinusoids is relatively slower,
increasing the time of uptake, which may partially compensate for the reduced hepatocyte
exposure (Hinton, et al. 2001, Gingerich, 1982).
Liver histopathology has been used as an indicator of environmental stress since it
provides a definite biological end-point of historical exposure (Stentiford et al. 2003), and the
kind of injury is often dependent upon time of exposure to pollutants, such as metals (Yang
and Chen 2003; Au 2004; Olojo et al. 2005). Although, liver histopathological alterations are
not specific to pollutants, several studies have established a causal relationship between metal
concentrations and fish liver lesions (Au 2004).
Because the liver is so important in detoxification, exposure to contaminants can lead to
an increase in liver size from hypertrophy (an increase in size), hyperplasia (an increase in
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 5

number) of hepatocytes (Goede and Barton 1990; Hinton and Lauren 1990), or both.
Significant higher Zn- and Cu-liver content associated with extensive hepatic heterogeneous
parenchyma, with large spectrum of vacuolization, observed in mullet (Liza saliens) suggest
that these abnormalities could be a response to metal chronic exposure (Fernandes et al.,
2008c).
Ultrastructural changes induced by toxicant exposure may include increased numbers of
organelles such as myelinated bodies, mitochondria, glycogenosomes, peroxisomes, and
lysosomes, and changes in rough endoplasmic reticulum (increased amount, vesiculation, and
dilatation). Physiologic hypertrophy of hepatocytes can be observed in reproductively active
female fish, or in male fish that have been exposed to exogenous estrogenic compounds, since
estrogens stimulate hepatocyte metabolism for vitellogenin (yolk lipoprotein) production
(Wester et al., 2003). These phenomena however can have a physiologic or toxicologic cause.
Cytoplasmic and nuclear enlargement (megalocytosis), are others histologic alterations
observed in cases of algal toxicity in farmed Atlantic salmon (Kent et al., 1988; Andersen et
al., 1993; Stephen et al., 1993).
Other types of nuclear changes, such as enlarged, binucleate, or bizarre nuclei, are seen
occasionally, most often in the repair stages of toxicosis (Ferguson, 1989). A common and
certainly pathologic, response of the fish liver to toxins is hepatocyte necrosis. The most
characteristic reaction to toxicity is an apoptotic type of single cell death (Ferguson, 1989;
Boorman et al., 1997). Typically, a random pattern of necrosis rather than a zonal pattern can
be seen in fish liver, although occasionally a perivenous distribution of necrosis is observed
(Casillas, et al., 1983). Necrosis of the biliary epithelium can also be induced in rainbow trout
experimentally exposed to the toxin alpha-naphthylisothiocyanate (Metcalfe, 1998). Unlike
mammals, cirrhosis is rarely seen in the fish liver as a sequel to hepatocellular necrosis
(Ferguson, 1989).
Piscine cholangiofibrosis may be accompanied by bile duct hyperplasia, increased
numbers of bile ductule and/or oval cells, and nonneoplastic proliferation of the biliary
epithelium (Boorman et al., 1997).
Neoplasia, in fish liver collected from natural waters, has been one of the histologic
biomarkers used in many research studies, to assess the hepatotoxicity of pollutants. There is
now solid evidence, however, that fish should also be recognised as valid models for
assessing other nonneoplastic biomarkers, in terms of both field and laboratory-based
research (Wolf and Wolfe, 2005).

Glycogen and Lipid Reserves

A common morphologic response of the fish liver to toxicity is a loss of hepatic glycogen
and/or lipid (Ferguson, 1989). Macroscopically, affected fish have small, dark livers;
microscopically, decrease of hepatocellular vacuolization, and size alterations of hepatocytes.
Loss of glycogen or lipid can occur as a direct effect of intoxication, or it may occur
secondary to decreased body condition, caused by inanition, stress, or concurrent disease. The
latter is probably more typical.
However, accumulation of fat or glycogen in the liver has also been observed in Japanese
medaka (Oryzias latipes) (Wester et al., 1988) and guppies (Poecilia reticulate) (Wester and
6 C. Fernandes, A. Afonso and M. A. Salgado

Canton, 1987), as a result of organotins exposure. The hypothesis to explain such results was
that glycogen accumulation was due to decreased glycogen breakdown in consequence of
hepatocellular toxicity.
Liver of fish stores large amounts of lipids (triglyceride), but unfortunately this feature
can hardly be used as a biomarker of hepatotoxicity since there are no accepted criteria for the
diagnosis of hepatic lipidosis. Different percentages of lipid concentrations can be
accumulated by different fish species (McLelland et al., 1995), so that the concentration
above which lipid accumulation would be pathologic, would rather vary, however there are
several reasons to use this alteration with some precaution as a reliable biomarker of
contamination.
Hepatic lipidosis in extreme may result in the fusion of the fat globules from
neighbouring hepatocytes, but even though may not be detrimental or irreversible in all fish.
In addition it may be nutritionally induced (Penrith et al., 1994) by an excessively energy-rich
diet or caused by lipid peroxidation associated with diets rich in polyunsaturated fats and/or
by the suppression of vitamin E (Ferguson, 1989).
Lipid peroxidation in fish may also be toxicant-induced. The induction of hepatic lipid
peroxidation caused by chronic dietary exposure to Cu was confirmed in grey mullet (Chelon
labrosus) (Baker et al., 1998) and in mullet (Liza saliens) chronically exposed to Cu
(Fernandes et al., 2008b). Sediment contaminated with polyaromatic hydrocarbons,
polychlorinated biphenyls (PCBs), and metals have been described as lipid peroxidation
inducters in channel catfish (Di Gulio et al., 1993) and in juvenile grey mullet Liza ramada
exposed to atrazine (Biagianti-Risbourg and Bastide, 1995).
Lipid or glycogen vacuolization can cause an increase in the size of hepatocytes;
however, Hinton et al., (1992) identified 3 additional potential causes of hepatocellular
enlargement: organelle proliferation (hypertrophy); the failure of sublethally-injured
hepatocytes to mitotically divide (megalocytosis); and vacuolar swelling of the endoplasmic
reticulum cisternae (hydropic degeneration). Hepatocyte hypertrophy was observed in
rainbow trout that was simultaneously exposed to endosulfan and disulfoton (Arnold et al.,
1995).

Biotransformation System of Xenobiotics

In terms of physiology, the liver of fish, as the liver of mammals, is responsible for the
same basic metabolic functions: processing, and storage of nutrients, enzyme and cofactors
synthesis, bile formation and excretion, and the metabolism of xenobiotic compounds. A
complex multienzyme family, normally referred as the biotransformation system,
accomplishes the biotransformation of xenobiotics in fish. This system metabolizes both,
endogenous and foreign compounds, through a series of reactions, which can be divided in
two steps: Phase I that often produces reactive or toxic metabolites, and phase II where larger
groups are conjugated with the oxygenated xenobiotic into polar, water-soluble and less-
reactive end-products and thus can be excreted from the organism.
Fish have many of the same microsomal and cytosolic enzymes as mammals (Cowey and
Walton, 1989). The cytochrome P450 (CYP) monooxygenase system comprise a family of
enzymes that catalyse phase I monooxygenation reactions and among them, the CYP1A,
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 7

which can be found in hepatocytes, biliary epithelial cells, and endothelial cells (Stegeman et
al., 1979; Stegeman and Hahn, 1994; Hinton et al., 2001). The activity of this enzyme has
been demonstrated to vary according to the type of inducer, the exposure route, and the fish
species (Hinton et al., 2001).
Fish also have an enterohepatic cycling mechanism (Gingerich, 1982) to process the
substances that were not metabolized during their first pass through the liver. This
enterohepatic cycling may increase the efficacy of xenobiotic removal (Gingerich, 1982;
deBethizy and Hayes, 2001).
The induction of the CYP1A system has become an important tool for monitoring
environmental exposure of fish to organic compounds (Hodson et al., 1991) and has been
extensively used as a biomarker of aquatic contamination by different pollutants in freshwater
as well as in marine environments (Narbonne et al., 1991; Parente et al., 2004). The CYP1A
is a sensitive indicator to different environmental contaminants, such as polycyclic aromatic
hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), and pesticides, in mammalian as
well as in fish (Haasch et al., 1993).
In this context, the cytochrome P450-dependent monooxygenase induction, measured as
ethoxyresorufin O-deethylase (EROD) activity, has been used as an indicator of exposure to
pollutants (Setegman and Lech, 1991; Stegeman and Hahn, 1994; Whyte et al., 2000;
Pacheco and Santos, 2002; Ferreira et al., 2004). The expression of hepatic CYP1A and its
evaluation by increases in EROD activity has been used in field and laboratory studies to
assess the pollutants exposure in different fish species (Narbonne et al., 1991; Goksøyr and
Förlin, 1992; Ferreira et al., 2004; Miller et. al 2004; Lee and Anderson, 2005; Bacanskas et.
al, 2005).
Nevertheless, there are a number of essential physiologic differences between
mammalian and fish livers, some of which may affect the rate, pattern, and/or extent of
toxicity that occurs in a fish following chemical exposure. One of the most important
differences is that fish appear to have a relatively homogenous distribution of biotransforming
enzymes in their livers (Gingerich, 1982; Schar et al., 1985; Metcalfe, 1998; Hinton et al.,
2001) that is, there is generally no preferential location for these enzymes within anatomical
structures, such as central veins. The significance of this dissimilarity will be addressed
shortly.
Another difference is that fish monooxygenases like CYP1A may be refractory to some
classic cytochrome inducers such as phenobarbital (Ferguson, 1989), or variably responsive
to other inducers such as 3-methylcholanthrene (Di Gulio et al., 1995) or resistant in cases
where fish has been chronically exposed to heavy pollution. A PAH-resistant population of
killifish has been identified in a creosoto contaminated site (Van Veld and Westbrook, 1995)
However in the same site, CYP1A was environmental induced on both hepatic and
extrahepatic tissues at certain times of the year. The variability in resistance among different
populations of chemically impacted killifish suggests that such a resistance can occur through
different mechanisms depending on the type of toxicant, and the genetic variability of the
population (Bello et al., 2001).
Fish liver is more tolerant to hepatotoxins than the liver of mammals, which means that
the same hepatic changes are only observed in fish exposed to greater concentrations of
toxicant (Gingerich, 1984). This tolerance of fish to hepatotoxins could be attributed to some
of the mentioned above factors, such as the lower perfusion rate of the fish liver, the
8 C. Fernandes, A. Afonso and M. A. Salgado

limitation of toxic exposure to the basal hepatocyte membrane, the homogenous distribution
of biotransforming enzymes, and the fact that some enzymes are not readily inducible.
Another important propensity of the fish liver is that the lesion distribution, following
toxic exposure, tends to be random, without the zonal pattern that is common to sublethal
intoxications in mammals (Ferguson, 1989; Boorman et al., 1997; Hinton et al., 2001). Again,
this trait has been attributed to the homogenous distribution of biotransforming enzymes in
the fish liver, and the fact that the zonal architecture is not apparent.

Transaminases

Many enzymes of intermediary metabolism of fish as plasma transaminases are affected

by exposure to chemicals. Alanine aminotransferase (AlaAT) and aspartate aminotransferase
(AspAT) are indicators of liver damage. They are both mitochondrial and cytosolic and are a
very sensitive measure of hepatotoxicity and histophathalogic changes that can be assessed
within a shorter time (Balint et al., 1997). These intracellular enzymes are involved in
catabolism of amino acids, transferring amino groups to α-keto acids.
Usually they are present at very low amounts in serum or plasma. Their increase in
plasma may mean liver damage, resulting in their liberation and raising plasma levels (Rao,
2006). For this reason transaminases have been used as indicators of tissue damage (Oluah,
1998, 1999; De la Torre et al. 2000; Das et al., 2004).
The increase in (AlaAT), and (AspAT) activities has been observed in fish
experimentally exposed to various chemicals including phenols (Hori et al., 2006),
organophosphorus insecticide (Rao, 2006) and metals (Varanka et al., 2001) resulting in
metabolic alterations at various levels and tissues and hepatic ultrastructure changes. In field
studies, where fish has been chronically exposed to environmental metals (Cu and Zn) an
increase of plasma AspAT was found suggesting a change in protein metabolism (Fernandes
et al. 2008c).

Metal-Binding Proteins

Metallothioneins (MTs), are cysteine-rich metal-binding proteins which are believed to

play an essential role in regulating the intracellular concentration of the ionic forms of zinc
and copper and in protecting cells from the deleterious effects of harmful heavy metals, such
as cadmium and mercury (Kaegi et al. 1981; Kaegi and Schaffer 1988; Kaegi 1993). They
have an additional role in reducing the toxicity of other metals such as Ag, Cd and Hg in
contaminated environments since they also bind elements from groups Ib and IIb of the
periodic table (Livingstone, 1993).
The relationship between metal levels in the environment and MTs concentrations in
animal tissues has led to their use for monitoring the biological effects of metal exposure
(Hylland et al., 1992; Livingstone, 1993). The mechanism of metal detoxification by MTs
occurs via metal-initiated transcriptional activation of MT genes, resulting in an increase in
MT synthesis, and subsequent binding to the free metals (Hogstrand and Haux, 1991)
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 9

In teleost fish, there are marked variations in the inductive response between different
species and there are a number of environmental and animal conditions that influence MTs
synthesis, as season, temperature, salinity, dietary status and reproductive steroids (Olsson et
al., 1995, 1996; Hylland et al., 1998). Interpretation of the results and consequently its use as
biomarker of environmental contamination is therefore limited (Rotchell et al., 2001).

3. THE LYMPHOHEMOPOIETIC TISSUES IN FISH

In vertebrates, the hemopoietic system is one of the primary targets to several insults. As
fish do not have bone marrow or lymph nodes, the hematopoiesis and lymphopoiesis must
occur in different fish organs (Agius and Roberts, 2003). In teleosts, hemopoiesis is mainly
located within the stroma of the spleen and in the kidney interstitium (Kranz and Peters, 1984;
Fänge and Nilsson, 1985; Agius and Roberts, 2003). To a lesser extent, hemopoiesis may also
occur in the peri-portal areas of the liver, in the intestinal sub-mucosa and in the thymus
(Kranz and Peters, 1984; Agius and Roberts, 2003; Tort et al., 2003) and there are also reports
of their occasional occurrence in gills, brain and gonads (Agius and Roberts, 2003).
Teleost fish species do not have lymph nodes, thus mature lymphocytes are dependent of
hemopoietic tissues, such as the spleen. The thymus, kidney and spleen are the major
lymphoid organs in fish (Fänge and Nilsson, 1985; Agius and Roberts, 2003; Tort et al.,
2003; Zapata et al., 2006) and, to a lesser extent, mucosa-associated lymphoid tissues can
occur, including in the skin and gills (Tort et al., 2003; Huttenhius et. al., 2006).
The amount of lymphoid tissue in spleen of distinct vertebrates reflects the pattern of
blood circulation and/or occurrence of other peripheral lymphoid organs (Zapata et al., 1996;
Agius and Roberts, 2003). Therefore, teleosts splenic lymphoid tissue is poorly developed
(Zapata et al., 1996); Fänge and Nilsson, 1985), with diffuse layers of lymphoid tissue
showing a tendency to accumulate around blood vessels and macrophage aggregates, as well
as scattered lymphocytes within the whole spleen parenchyma (Lamers and De Haas, 1985;
Fänge and Nilsson, 1985). On the contrary elasmobranchs, because they loose their renal
lymphoid tissue in adult life, show an important splenic lymphoid contribution (Zapata et al.,
1996).
The major teleost lymphoid organs appeared in the following sequence: kidney, spleen,
and thymus, as it has been earlier observed in fish, like Senegalese sole (Solea senegalensis),
turbot (Scophthalmus maximus) and Japanese flounder (Paralichthys olivaceus) (Padrós and
Crespo, 1996; Cunha et al., 2003), becoming soon the spleen rich in blood capillaries, red
blood cells and thrombocytes (Padrós and Crespo, 1996). In freshwater species, but not in
marine teleosts, the spleen is the last organ to become lymphoid (Zapata et al., 2006).

3.1. The Spleen

Fish spleen is an organ with multiplicity of functions and, depending on fish species, can
present high structural complexity.
Spleen is surrounded by a connective tissue capsule, which is frequently a thin structure,
as it has been shown in rainbow trout (Kita and Itazawa, 1994) and carp (Lamers and De
10 C. Fernandes, A. Afonso and M. A. Salgado

Haas, 1985). Blood vessels organization in the spleen showed that visceral arteries originate
the arterial blood supply and the hepatic portal system comprises the splenic veins (Fänge and
Nilsson, 1985). The parenchyma includes grossly: blood vessels, ellipsoids, macrophages and
white pulp that correspond to lymphoid tissue, showing a reticular area without definite
lymphoid centers, and red pulp, showing predominantly erythrocytes (Fänge and Nilsson,
1985; Sailendri and Muthukkaruppan, 2005). However, red and white pulp is less clearly
defined in poikilothermics than in the homeothermic vertebrates (Fänge and Nilsson, 1985).
The ellipsoids are the terminal arterial capillaries and in carp they are surrounded by a cuff of
cells (mainly macrophages) (Lamers and De Haas, 1985). Ellipsoids have been suggested to
be involved in immune response, by trapping antigens, or through formation of antigen-
antibody complexes (Fänge and Nilsson, 1985; Lamers and De Haas, 1985). Within the
spleen, macrophage aggregates usually occur close to the blood vessels and, in certain
species, they are surrounded by a lymphoid sheath (Kranz and Peters, 1984; De Vico et al.,
2008).
The spleen of teleost fish, compared with those of elasmobranchs, is usually smaller. In
teleosts spleen weight ranges 0,05-0,86 % of the body weight comparing with elasmobranchs
that could range between 0,1 to 4,0 % (Fänge and Nilsson, 1985).
In fish, the spleen is involved in the development of circulating blood cells, as well as
immunity. Functions of fish spleen comprise blood cell formation, their storage and release,
and also destruction of aged or defective blood cells and foreign agents by cells of the non-
specific immune response (Fänge and Nilsson, 1985; Spazier et al., 1992). Rapid expulsion of
stored blood cells by contraction of the fish spleen can occur after severe exercise (Franklin et
al., 1993; Kita and Itazawa, 1994). The spleen also serves as a filter, retaining and eliminating
effete or aged blood cells and foreign particles (Fänge and Nilsson, 1985; Kita and Itazawa,
1994).
The white pulp, lymphoid tissue, is mainly related to immune response, by processes
involving macrophages and lymphocytes, and although species differences may exist, it has
been suggested that the spleen is also involved in anti-body production. Along with other
lymphohemopoietic tissues, such as the pronephros, the spleen probably is an important
source of immunoglobulins in elasmobranchs and teleosts (Fänge and Nilsson, 1985).

3.2. The Kidney

Fish is the oldest, largest and most variable group of vertebrates on Hearth. So, it is not
surprising that this obligate aquatic animal has a multifunctional kidney, which is reflected on
its complex tissue organization.
Originated from mesoderm, development of kidney is a gradual process that occurs
during the embryonic period and reaches various degrees of differentiation in different
groups. That differentiation happens always from the head to the caudal region in a concept of
a kidney triplicate organization (i.e. pronefros, mesomefros and metanefros). Because it forms
within the intermediate mesoderm located in the dorsal and posterior body wall, modern fish
kidney is a retroperitoneal organ (Hildebrand and Goslow, 2001; Kardong, 2002).
The kidney ontogenetic development in teleost species stops at the opistonefros phase.
This organ has two distinct segments: an anterior pronefretic segment (the head kidney) and a
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 11

posterior segment mesonefretic, with contribution of some metanefros components (the trunk
kidney). Although both segments hare lymphoemopoietic, it is more intense in the anterior
part because this part is not involved in excretory function. The head kidney parenchyma is
dispersed between the sinusoid system that is supported by the stroma. The stroma supports
the hemopoietic tissue and has an important role in nonspecific immunity traping and
clearance of debris and damaged cells mainly from blood (reviewed by Press and Evensen,
1999).
It appears, from studies in various teleost species, that the anterior kidney is the first
lymphoid organ to possess Ig+ cells during ontogenesis (Kaattari and Irwin, 1985; Castillo et
al., 1993; Koumans-van Diepen et al., 1994; Breuil et al., 1997; Romano et al., 1997;
Schroder et al., 1998). Moreover, Kaattari and Irwin (1985) suggested that this organ also
serves as a secondary lymphoid organ.
The functions assigned to each part of the organ, throughout its development, will vary
and, in some cases, after a transient development, a complete regression can happen, or other
function can be assigned to the remaining structures. For example, in several bony fishes the
archinefretic ducts are shared in urine and sperm release. In other cases they have testicular
ducts. (Hildebrand and Goslow, 2001; Kardong, 2002).
Fish kidney shows morphological and physiological variations between and within
groups. For example, Chondrichthyes have particular arrangements - i.e. Leydig organ-
(Zapata et al., 1996) and within teleosts there are aglomerular species (McDonald and
Grosell, 2006). Furthermore, in contrast to higher vertebrates, most fish species hatch these
organs at embryonic stage, so becoming free-living organisms. The adult fish kidney, often
situated along the dorsal wall of the body cavity, is for most species an opistonefros divided
into anterior pronefric region (head or cranial) and posterior (trunk or caudal) sections
(Kardong 2002).
The anterior kidney is one of the primary hemopoietic organ in adult teleosts (Press and
Evensen, 1999). Together with the blood, anterior kidney has the largest amount and the
greatest variety of fish leucocytes. In fact, anterior kidney is the larger lymphomieloid organ
in most teleosts (Zapata and Cooper, 1990; Zapata et al., 1996). So, it is usually the supplier
of leukocytes for in vitro studies.
The interest seen over the recent few decades by the fish kidney functions is not
surprising. In fact, all vertebrates have that retroperitoneal organ (the kidney) that is
responsible for several vital functions. Removal of nitrogenous waste products and other
circulating harmful substances is the most commonly known, because this function is general
through all vertebrate groups. Osmoregulation and water balance are also vertebrate kidney
general functions (Varsamos et al., 2005; Evans, 2008). The other two functions of fish
kidney are reflected in the endocrine tissues, that include medullar and cortical adrenal
homologs, the chromaffin tissue, or chromaffin bodies, and the interregnal tissue, or
interregnal bodies, that produce catecholamines (Reid et al., 1998) and corticosteroid
hormones (McCormick, 2001; Martinez-Porchas, 2009), respectively; and the last to be
addressed, but not least important, is an hemopoiesis and immunological functions (Ellis
1977; 1999; Secombes 1993).
Kidney plays a key role in maintaining body homeostasis, by blood filtration and critical
electrolyte and acid–base balance and maintenance of intracellular fluid volume. As part of its
blood filtering function, kidney remove wastes and toxicants from blood and discharges those
through urine, while conserving essential ions, amino acids, and glucose. Other kidney crucial
12 C. Fernandes, A. Afonso and M. A. Salgado

function is the absorption and deposition of calcium. The kidney also produces essential
hormones, including renin and erythropoietin (Bernier et al., 1999).

Kidney and Its Role in Electrolyte Balance

The knowledge on osmoregulation and its implications in growth is vital to understand

fish survival. The water salinity has great impact in fish physiology, namely the various
salinity regimes that occur in estuaries where it is of particular importance to several fish
species. Freshwater environments display a diversity of low ionic types and ratios and
typically have substantially lower levels of total dissolved electric charged particles (ions)
than marine or brackish waters. On the other hand, in marine environment, ions occur in
stable ratios, comparatively with absolute concentrations. Even though, teleosts may live in
waters which exhibit wide ranges of salinity, since they are capable of maintaining relatively
stable plasma and tissue ion concentrations (Evans et al., 2004; Evans, 2008).
Osmoregulation is the mechanism for maintaining constant internal ionic concentrations
relative to external or environmental ionic concentrations. The osmoregulatory mechanisms
maintain at almost constant or only slightly variable blood osmolality, between 280 and 360
mOsm kg -1 (Varsamos et al., 2005).
From the point of view of hydromineral regulation, the main function of kidney, in
freshwater fish, is the excretion of large volumes of osmotically accumulated water and the
elimination of surplus ions extracted from the food, mainly K+, sulfate, and phosphate. In the
limit, if renal losses of valuable ions via urine occurs, intensive reabsorption of Na+, Cl–,
Mg2+ and Ca2+ takes place, by transporting enzymes and exchangers in epithelial cells lining
the nephronic tubules, collective tubules, and bladder (Beyenbach, 1995), depending on the
external salinity.
In marine environments loss of water from fish tissues is dramatic as exposure occurs
over the entire body surface and the major function of fish kidney is excretion of divalent ions
taken up by drinking. Water excretion has to be reduced as much as possible in a
hyperosmotic environment, and this is achieved mainly by reduction of the glomerular
filtration rate (Beyenbach, 1995).
Few studies are available on the physiological aspects of renal hydromineral function,
such as urine flow and renal ion excretion rates. Technical drawbacks as collection of such
fluids require cannulation that is complicated and extremely stressful to fish, often interfering
with results. Thus, a proper evaluation of the effects of toxic chemicals on the kidney is even
more complicated than in others organs.

4. THE IMPACT OF WATER CONTAMINATION ON RENAL FUNCTION

Because it is the main route of elimination of hydrophilic toxicant metabolites, kidney is
also an important organ in toxicology. The high volumes processed in kidney lead to high
levels of exposure particularly toxicants, with concomitant deposition of these toxic
substances and eventual damage.
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 13

A number of substances have been implicated in kidney damage. As Au (2004),

mentioned, histochemical techniques can be used as biomarkers, of general health condition
of fish and of toxic organic contaminant exposure. However, both histopathological and
morphological analysis showed moderate sensitivity to pollution when compared with other
techniques (Van der Oost et al., 2003).
Toxicological studies have revealed extensive histopathological alterations in kidney as a
result of fish exposure to heavy metals and organic chemicals. Generally, proximal tubules
appear to be the first affected, but damage progresses to the posterior segments and glomeruli,
following both, chronic exposure, or high concentration of the toxicant (Au, 2004; Wendelaar
Bonga and Lock, 2008).
Some metals, including cadmium, lead, mercury, nickel, and chromium, particularly
abundant in some contaminated aquatic environments, are severely nephrotoxic. Also,
halogenated hydrocarbons, including bromobenzene, chloroform, carbon tetrachloride and
tetrafluoroethylene, that are transported to the kidney as cysteine S-conjugate, have
nephrotoxic action (Wendelaar Bonga and Lock, 2008). The herbicide paraquat, diquat, and
2,4,5-trichlorophenoxyacetate have also toxic effects on the kidney (Parvez and Raisuddin,
2006).
Histopathological effects vary from slight disruption of the proximal tubular cells,
increased numbers of phagosomes and lysosomes, and abnormal mitochondria, to rupture of
cell membranes, swelling and vacuolization, increased cell death by necrosis and apoptosis,
and large lesions in the tubular epithelia (Hisar et al., 2009; Kosai et al., 2009; Vinodhini and
Narayanan, 2009).
Although kidney has been used as nonspecific cellular biomarker, for cadmium it is well
known its affinity for renal tissue, as a site of accumulation, here the highest concentrations of
this metal are usually found, after exposure (Bentley, 1991; McCoy et al., 1995; Van
Campenhout et al., 2009). As a consequence, cadmium is able to produce severe
histopathological alterations (Gill et al., 1989; Hallare et al., 2005). Copper has no specific
affinity for the kidneys, but it can also produce significant structural damage to both
glomeruli and renal tubules (Vinodhini and Narayanan, 2009). A study on mercury chloride
effects on head kidney macrophage function and integrity of sea bass (Dicentrarchus labrax)
and their dependence on macrophage activating factor(s) (MAF) for the production of
reactive oxygen species (ROS), showed a decrease in ROS production as compared to cells
incubated with medium alone. MAF activation of the macrophages phagocytic activity was
also impaired by HgCl2 addition. Mercury chloride induced macrophages apoptosis and MAF
addition prevented this effect (Sarmento et al., 2005).
Among the many organic chemicals producing similar effects are paraquat (Molck and
Friis, 1997), TCDD (Henry et al., 1997) and atrazine (Fischer-Scherl et al., 1991).
It is clear that the lesion severity of renal functions, including hydromineral regulation, is
affected by the concentration and length of exposure. Relatively few studies deals with renal
functions, however inhibitory effects of silver on K+- dependent of p-nitrophenol phosphatase
(Bury, 2005), of cadmium and chromium (Venugopal and Reddy, 1993), of copper and
mercury (Singh and Sivalingam, 1982; Lan et al., 1993), as well as on renal tubular Na+/K+-
ATPase, Ca2+-ATPase, and Na+/Ca+ exchange activity were reported (Wright and Welbourn,
1993).
Most organic pollutants may be responsible for a reduced activity of renal ion transport,
in a less specific way. The reduction of Na+/K+-ATPase activity induced by paraquat has been
14 C. Fernandes, A. Afonso and M. A. Salgado

related to the disruption of this chemical on mitochondrial electron chain transfer (Molck and
Friis, 1997).
Decrease in renal Na+ efflux was found in freshwater rainbow trout following exposure to
waterborne copper (Li et al., 1996). As copper has a strong inhibitory action upon Na+/K+-
ATPase activity, the opposite effect was expected, i.e. an increased tubular reabsorption of
Na+, for which Na+/K+-ATPase is a driving force. A physiological response of the kidney to
compensate the impairment of branchial Na+ uptake was the explanation for this phenomenon
(Grosell et al., 1998).

Endocrine Kidney Response to Stressors

Fish kidney participates also through several endocrine mechanisms, during exposure to a
wide range of internal and environmental stress factors. Cortisol is the principal corticoid
secreted by the interrenal tissue located in the head-kidney of teleost fish. It is released by the
activation of the hypothalamus-pituitary-interrenal axis (Mommsen et al., 1999). The
hypothalamus releases corticotropin-releasing factor (CRF) toward blood circulation and this
polypeptide further stimulates secretion of adrenocorticotropic hormone (ACTH) from the
anterior pituitary gland (Fryer and Lederis, 1986), which induces the release of cortisol by the
kidney interrenal tissue (Balm and Pottinger, 1995; Mommsen et al., 1999). More important
in freshwater fish is prolactin, the hormone controlling the permeability to water and ions in
the gills, intestine, and renal tubules (Sakamoto and McCormick, 2006).
The interference of toxic agents with neuroendocrine control processes in fish involving
osmoregulation has been documented (Hontela et al., 1992). Prolactin cells, adreno-
corticotropic hormone (ACTH) cells and the interrenal cortisol producing cells were those
that received major attention in order to investigate the potential use as biomarkers (Ramesh
et al., 2009).
Activation of prolactin cells has been frequently observed in fish exposed to toxic agents
and has been generally interpreted as a compensatory response to the disturbance in the
permeability of these epithelia by toxicants (reviewed by Wendelaar Bonga and Pang, 1989).
Cortisol is one of the primary stress hormones in fish and also an important stimulator of
Na+/K+- ATPase activity in gills, intestine, and kidney. The multiple functions of this
hormone clearly demonstrate the intimate relationship between the stress response and
osmoregulation in fish (Wendelaar Bonga, 1997; Reid et al., 1998; Barton, 2002).
Endocrine dysfunction was also found in fish from water naturally contaminated with a
mixture of pollutants, including heavy metals and PCBs, when compared with fish from an
unpolluted reference site (Hontela et al., 1992; Hontela et al., 1997; Wendelaar Bonga and
Lock, 2008). Hypothalamo–pituitary–interrenal (HPI) axis of wild brown trout is activated in
fish from sites contaminated with cadmium and zinc. Histological analyses revealed that
interrenal cells are more stimulated, exhibiting both hypertrophy and hyperplasia (Norris et
al., 1997). These results suggest that the hypothalamo-pituitary-interrenal (HPI) axis of fish
living in metal-contaminated water may be susceptible to chronic stimulation.
A study of effects of endosulfan, an organochlorine pesticide, on cortisol secretion in
vitro revealed that the head kidney cells of rainbow trout, (Oncorhynchus mykiss) exposed to
endosulfan, decreased ACTH- or dbcAMP-stimulated cortisol secretion and cell viability in a
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 15

concentration-dependent pattern and the doses required to disrupt cortisol secretion were
significantly lower than lethal doses to the head kidney cells (Leblond et al., 2001).
The interrenal tissue of yellow perch, from a site contaminated by a mixture of heavy
metals and organic contaminants, secreted significantly less cortisol in response to a
standardized pulse of ACTH than those from an unpolluted site (Brodeur et al., 1998) .
Given the cortisol importance for osmoregulation in fish, any interference with the
secretion of cortisol and its stimulant hormone (ACTH) may be expected to have an effect on
osmoregulation (McDonald and Milligan, 1997); however, the actual impact of the disruptive
effects of some toxic chemicals on this process remains to be established. Currently, the use
of cortisol as a biomarker has to be done carefully. For proper use of cortisol as biomarker, an
evaluation has to be done in each case (species, contaminant compounds and environmental
conditions).

5. IMMUNE SYSTEM IN FISH

The main source of pollution in aquatic environment is the growing human population
and their demanding needs that may affect both, fish and human health.
Degradation of environmental conditions, due to pollution, can disturb fish immune
process and consequently fish health. Consequences of exposure to pollutants on fish immune
system can range from suppression/inhibition or even enhancement of a specific immune
response. According to Agius and Roberts (2003), fish inhabiting polluted environments can
respond to environmental conditions altering the nonspecific defence activities.
In fact, toxic effects on the immune system may serve as an excellent biomarker to
monitor pollution and water quality, since most environmental pollutants are known to alter
immune system function, even at doses that do not cause histopathological toxicity (Agbede
et al., 2005).

5.1. Non-Specific Defence Mechanisms

As in all jawed vertebrates, fish species possess a complex mechanisms system that
provide homeostasis and fight against infection. The complexity and the type of these
mechanisms led to a division in innate (non-specific) and an acquired (adaptive or specific)
immunity. Indeed, the system is unique and their parts are interdependent, with several
molecules and cells working together in both, innate and acquired system. Both types have
the participation of both, cellular and humoral factors. However, as the term humoral was first
applied to activities involving antibodies, humoral innate components are just referred as
soluble components.
As previously stated, the innate immunity is generally subdivided into two parts, the
cellular and humoral defense responses (Köllner et al, 2002; Aoki et al., 2008). Cellular
responses include physical barriers, such as mucus and epithelial tissues in skin, gills and
stomach (Aoki et al., 2008), and cells, like monocytes/macrophages, and granulocytes, mainly
involved in phagocytosis (Agbede et al., 2005; Aoki et al., 2008). Humoral responses involve
16 C. Fernandes, A. Afonso and M. A. Salgado

a variety of proteins and glycoproteins capable of destroying or inhibiting growth of

infectious microorganisms (Aoki et al., 2008).
The non-specific immunity, in fish, is the primary line of defence and represents a
considerable part of the immune response, since activation of leucocytes is one of the first
reactions in every immune response (Agbede et al., 2005; Aoki et al., 2008). This mechanism
is characterised by being non-specific and therefore not depending upon previous recognition
of the invader (Tort et al., 2003). Depending on the antigen leukocyte, certain subpopulations
are activated and proliferate. However, it has been shown in different fish species that some
circulating sub-populations are able to act in immune defence without prior activation
(Köllner et al, 2002). The nonspecific immunity in fish primarily depends on the phagocytic
activity of sub-populations of monocytes/macrophages and neutrophilic granulocytes (Köllner
et al, 2002; Agbede et al., 2005).
Phagocytosis, killing and degradation of invading microorganisms by professional
phagocytes, is a crucial process in the mechanisms of defense of vertebrates against some
infections (Mackaness, 1969; Ellis, 1977; Adams and Hamilton, 1984; Edwards and
Kilkpatrick, 1986; Lehrer et al., 1988; Hine, 1992; Brown, 1995). It is interesting that
mammals, teleosts and other higher eukaryotes utilize two types of professional phagocytic
cells -neutrophils and macrophages- in the defense against infection (Rowley and Ratcliffe,
1988; Secombes and Fletcher, 1992; Brown, 1995). Data from studies conducted on the
behavior of each of the two professional mammals phagocytes in inflammation, including that
due to infectious situations, can be summarized as follows (Lehrer et al., 1988; Haslett et al.,
1989; Silva et al., 1989; Densen et al., 1995; Kubicka et al., 1996; van Furth 1992).
Macrophages are present in all body compartments being in a quiescent state. Therefore,
when superficial barriers are breached by an invading microorganism, it encounters this
phagocyte. Neutrophils are present in large numbers in blood and hemopoietic organ pools as
a reserve, and, under normal conditions, are rare in the tissues and body cavities. These
granulocytes migrate to the infection focus just when mobilized by chemotactic molecules,
including those released by macrophages (Afonso et al., 1998a; Afonso et al., 1998b).
Although phagocytic system in fish involves resident macrophages present in all organs
and tissues of the body (Agbede et al., 2005), spleen has an important role in this mechanism,
developed by macrophages and granular leucocytes inside parenchyma. This is not surprising
since it is known that phagocytosis is the principal function of macrophages in teleosts fish
(Agius and Roberts, 2003; Agbede et al., 2005), and the response of splenic macrophages to
foreign substances is the subsequent elimination by phagolysosomes. Therefore macrophages
aggregates have been considered as metabolic dumps (Kranz and Peters, 1984).

Macrophage Aggregates

Macrophages are mononuclear cells derived from circulating blood monocytes,

terminally differentiated, that have been studied in a variety of fish species (Secombes and
Fletcher, 1992; Enane et al., 1993; Secombes, 1993). Several distinct macrophages
subpopulations seem to exist in fish (Afonso et al., 1998a; Neumann et al., 2000). Described
long ago by Metchnikoff (1887), phagocytosis is one of the most ancient cellular immune
mechanisms and the term ―macrophage‖ came first of these observations. Several
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 17

immunoregulatory molecules such as macrophage-activating factor (MAF), TNF-, TGF-,

-glucans, growth hormone, and neurotransmitters have been implicated in the modulation of
fish macrophage phagocytosis (Secombes, 1994; Secombes et al., 1996).
Temperature can affect nonspecific immune responses in fish. Studies on the effect of
environmental temperature, on fish nonspecific defences, revealed greater effectiveness of
phagocytosis at low environmental temperature in several species (Morvan et al., 1998).
Dispersed or aggregated, macrophages are pigmented populations with particular interest.
Macrophage aggregates (MAs), or melanomacrophage centers, are structures normally
located in the stroma of the hemopoietic tissue of spleen and kidney, although in some fish,
they are also found in liver (Fringe and Nilsson, 1985; Kranz, 1989; Montero et al., 1999;
Agius and Roberts, 2003). MAs vary between the different hemopoietic organs. Splenic MAs
exist in all teleosts fish (Lamers and De Haas, 1985) and for most fish species they are more
abundant and larger than those in the liver (Kranz and Peters, 1984), and compared to kidney,
they are more variable in pigmentation and show a closer degree of aggregation (Kranz,
1989).
As stated before, polluted environments may induce changes in fish nonspecific defence
activity. Macrophage aggregates have been used as nonspecific cellular biomarkers of
physiological stress following exposure to chemical pollutants. Changes in MAs number and
structure could be a sensitive biomarker, which could be of great value as an early sign of
environmental contamination (Montero et al., 1999; Fournie et al., 2001; Agius and Roberts,
2003; Facey et al., 2005; Jordanova et al., 2006).
General functions of these centres have been described as storage, destruction or
detoxification of exogenous and endogenous substances, and iron metabolism and recycling
(Montero et al., 1999; Agius and Roberts, 2003; Jordanova et al., 2006). They have also been
implicated in the immune response, including inflammatory and humoral responses (Montero
et al., 1999). MAs often exist as complex discrete centres, containing lymphocytes and
macrophages, and may be primitive analogues of the germinal centres of lymph nodes of
higher vertebrates (Kranz and Peters, 1984; Kranz, 1989; Agius and Roberts, 2003). It is
thought that the MAs might be involved in the response of fish to infectious agents, by acting
as focal depositories of resistant pathogens and also as antigen processors in immune
responses (Lamers and De Haas, 1985; Agius and Roberts, 2003).
Different types of pigments have been identified, frequently even within the same cell
(Agius and Roberts, 2003), which seems to be species-specific (Jordanova et al., 2006).
Melanin is not observed in MAs of carp, being the, hemosiderin and lipofuscin the main
pigments (Lamers and De Haas, 1985). At least 3 types of pigments have been identified in
the macrophages aggregates e.g. melanin, lipofuscin/ceroid and the hematogenous pigment
hemosiderin (Fringe and Nilsson, 1985; Agius and Roberts, 2003; Jordanova et al., 2006).
These pigments are associated to different biochemical roles, and their levels could be
indicative of fish unbalance physiology.

Splenic MAs

Macrophage aggregates increase in size, frequency or in pigment patterns in conditions of

environmental stress and have been suggested as reliable biomarkers of water quality (Agius
18 C. Fernandes, A. Afonso and M. A. Salgado

and Roberts, 2003). Furthermore, Hinton et al. (1992) have suggested MAs as histologic
biomakers of contaminant exposure or environmental stress.
Histochemical properties of splenic MAs vary considerably between healthy and diseased
fish and increases in pigment content are suggestive of catabolic, infectious or toxic exposure
(Agius and Roberts, 2003; De Vico et al., 2008). The accumulation of iron appears to be a
characteristic feature of splenic MAs, but not of those in the liver, leading to conclude that
one of their main functions is the digestion of degraded red blood cells (Kranz and Peters,
1984). Hemosiderin, related with iron storage and recycling (Fringe and Nilsson, 1985;
Montero et al., 1999), is usually detectable in little amounts in the MAs of spleen and
increased storage should be considered as a pathological event (De Vico et al., 2008). The
increase hemosiderin in splenic MAs, in some infectious diseases, occurs manly due to high
rates of erythrocyte destruction or/and high iron sequestering in centers to prevent them from
bacterial growth (Kranz, 1989). Also Khan and Nag (1993), reported an increase in splenic
hemosiderin in fish exposed to crude oil.
According Agius and Roberts (2003) lipofuscin is the pigment that accumulates with age
and tissue destruction and is the most widespread pigment in the MAs of many fish species.
Increase of lipofuscin is derived from cell peroxidation (Kranz, 1989; Agius and Roberts,
2003). Lipofuscin in splenic MAs, has been predominantly related to high levels of tissue
catabolism and degenerative chronic disorders (De Vico et al., 2008).
Although changes in splenic MAs can be considered in toxicological studies as a
sensitive biomarker, since they are nonspecific, their abundance and structure can be affected
by many factors and so these etiologies must be considered in toxicological studies. Increase
of splenic MAs has been associated with starvation (Agius and Roberts, 1981; Fänge and
Nilsson, 1985), with ulcerous infection (Kranz, 1989), with parasitic infection (De Vico et al.,
2008), with nutritional imbalances and high fish stocking density (Montero et al., 1999). It
has also been observed that these centres increase in size and number, at least in a number of
fish species, as fish grow older and tissues degenerate (Agius and Roberts, 2003). In addition,
normal fluctuations occur, since MAs could undergo seasonal and breeding dependent
variations. It is established that the amount of pigmented MAs in spleen was significantly
increased in wild Ohrid trout females, during and/or after spawning (Jordanova et al., 2006).
Thus, for biomonitoring purposes, normal fluctuations of a pollution biomarker must be
excluded to achieve reliable responses. Data control could be made by comparisons between
contaminated and reference sites, with fish of similar age and captured at the same season.
Besides, a quantitative study, an assessment of spleen and liver MAs in broun trout (Salmo
truta) during an entire gonadal cycle performed by Jordanova et al. (2006), was required since
it provides a basis for future evaluation of normal versus altered levels of MAs induced by
pollution, to be applied at least in the same group of fish.
Although non-specific, MAs in fish has been proven to be a sensitive indicator of
exposure to environmental contaminants (Au, 2004). Splenic MAs are effective biotic
indicators for discrimination between fish exposed to degraded and non-degraded
environments. However comparative studies, on the incidence of MAs in the spleen, kidneys
and liver of fish exposed to toxic chemicals, have shown an opposite trend. A reduction in
number and size of these structures in fish living in polluted water is probably due to a
pollutant-induced immunosuppression (De Vico et al., 2008). The spleen of the eel (Anguilla
anguilla), exposed to a chemical spill, showed alterations such as necrosis, lacking of MAs
and a reduced number of macrophages dispersed throughout the reticulum, compared to
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 19

controls (Spazier et al., 1992). Normally, the phagocytic capacity of the spleen in eel and
other species is mainly associated with number and extent of MAs (Spazier et al., 1992), and
according to these authors a decreased ability of macrophages phagocytic function, is
possibly due to a toxicant-induced reduction of chemotactic activity.
Metals may disturb ionic metabolic, balance and cell division of immunocompetent cells.
It was found in vivo that copper causes, in a dose-dependent manner, a depressed phagocytic
activity of catfish spleen macrophages (Saxena and Saxena, 2008).
The utility of splenic MAs has been assumed as a general indicator of fish exposure to
contaminated environments and has been used in monitoring programs, such as the
Environmental Monitoring and Assessment Program–Estuaries (EMAP-E). This study, using
image analysis, has proved that MAs densities greater than 40/mm2 can be correlated with
exposure, to hypoxic conditions or chemical contamination in sediments (Fournie et al.,
2001). Also, utilizing image analysis, an increase in splenic hemosiderin was observed in
longhorn sculpin (Myoxocephalus octodecemspinosus), yellowfin sole (Limanda aspersa),
quillback rockfish (Sebastes maliger) and kelp greenling (Hexagrammos decagrammus)
exposed to crude oil (Khan and Nag, 1993).
An environmental study in Calcasieu Estuary, Louisiana, showed that the frequency of
MAs in spotted trout (Cynoscion nebulosus) spleen was significantly higher in contaminated
sites, than reference sites (Jenkins, 2004). According to Kranz and Peters (1984), the MAs in
spleen and liver of ruffe (Gymnocephalus cernua) from the polluted Elbe River, augmented
during the development of several histopathological abnormalities of these organs.
It also is well established an association between erythrocyte damage and spleen toxicity,
after exposure to aniline and other aromatic amines. According to Monteiro et al. (2006) after
96 h of exposure to aromatic amine 3,4-dichloroaniline spleen histological alterations and
deposition of hemosiderin granules, in a dose-dependent manner, were observed in juveniles
of common goby (Pomatoschistus microps), compared to control groups.
Besides, splenic MAs hyperplasia was generally reported in a variety of fish species
inhabiting degraded environments, such as exposed to pulp mill effluent and areas with
elevated levels of xenobiotic chemicals (Au, 2004).
It has been shown that heavy metals exposure cause significant pathological changes in
fish lymphoid organs and fish mortality. Histopathology of spleen tissues of common carp
(Cyprinus carpio carpio) after metals exposure revealed congestion, haemorrhage,
lymphocytic infiltration and degenerative changes with loss of cellular architecture (Saxena
and Saxena, 2008). In laboratory conditions, frequency and size of splenic MAs were
significantly increased in Tilapia mossambica after median lethal exposure to heavy metal
cadmium chloride (Suresh, 2009). Osman et al. (2009), found splenic histopathological
changes in Oreochromis nilotica under copper sulfate and lead acetate laboratory exposure.
Fish spleen showed congestion of vessels, depletion of lymphoid follicles, excessive
hemosiderosis and hyper activation of MAs, associated with increase of pollutants
concentration and time of exposure. Also MAs sizes, in male pike (Esox lucius) and longnose
sucker (Catostomus catostomus), have increased with mercury contamination (Hinck et al.,
2004).
A long-term effect of small concentrations of the dioxin TCDD introduced in the diet of
rainbow trout (Oncorhynchus mykiss), was evaluated by Walter et al. (2000). The increased
numbers of macrophages and pigmented macrophages with intracytoplasmic hemosiderin
20 C. Fernandes, A. Afonso and M. A. Salgado

observed suggested a link with increased degeneration of lymphocytes and, possibly also,
erythrocytes.
Chronic (32 weeks) exposure of rainbow trout (O. mykiss) to sewage treatment plant
(STP) effluent showed effects on spleen leucocytes and on the integrity of spleen tissue.
Spleen tissue of exposed fish appeared to have less structural integrity and infiltration of
stimulated monocytes/macrophages, as compared to control (Hoeger et al., 2004).
These results are in agreement with the general idea that the increase in size, frequency
and pigments variation on MAs of fish spleen, in conditions of environmental stress, is a
reliable biomarker for water chemical pollution.
In addition, utility of splenic MAs as biomarkers could be extended to evaluation of
ecosystems recovery. Significant decreases in splenic MAs area were also used to suggest
decreased exposure to contaminants on a fish population (Facey et al., 2005). Results of
rainbow trout (O. mykiss) exposure to sublethal concentrations of the pesticide endosulfan
showed splenic abnormalities, after 21 days of exposure, including exudate, necrosis and
scattered MAs throughout the spleen, compared to control; whereas after 30 days of recovery,
lesions were no longer seen (Altinok and Capkin, 2007).
According to Jordanova et al. (2006), changes in MAs relative volume can be a non-
expensive and sensitive biomarker, which should be of great value as a first-line evaluator of
early signs of aquatic environmental degradation. The histologic analyses of spleen could
include the assessment of morphometric parameters, such as mean MAs profile area and
number per square millimetre of spleen tissue (De Vico et al., 2008). Also, image analyses
that select and quantify pigmented area are proved to be an objective way of MAs evaluation
in salmonid spleen (Schwindt et al., 2006). This method is less time-consuming and was
shown to be very accurate. Other studies that have used area occupied by MAs, noted
increased splenic hemosiderin in several fish exposed to crude oil (Khan and Nag, 1993) and
in dab with ulcers (Kranz, 1989). Using image analysis of splenic MA Fournie et al. (2001)
also proved the utility of this technique as effective discriminator between fish exposed to
degraded and nondegraded environments.
These approaches can provide data that is easily analysed statistically, resulting in less
controversial conclusions and reinforces the importance of using splenic MAs as histologic
biomarker of contaminant exposure.

6. ORGANO-SOMATIC INDICES
Organo-somatic indices reflect the status of organs within the whole body, which may
change in size due to environmental factors more rapidly than organism weights and lengths
increase or decrease. Although several factors could increase or decrease the sizes of a few
organs, the organo-somatic indices have been used widely in fish health and population
assessments.
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 21

The Splenosomatic Index (SSI)

Spleen size is considered a useful diagnostic factor because, as previously seen, this
organ plays a highly important role in hemopoiesis and immune reactivity of fish and the use
of relative spleen weight could provide information about fish health.
The splenosomatic index (SSI) is the weight of the spleen expressed as a percentage of
total body weight, and alterations in this index could indicate an abnormal condition in the
spleen (Dethloff and Schmitt, 2000). Commitment in immune defence could be measured by
spleen size, moreover the use of spleen size is also recommended in ecotoxicological studies
as a standard measure of immunocompetence on fish (Šimková et al., 2008; Van der Ost et
al., 2003).
There is evidence that immune system of fish reacts to various environmental factors,
including anthropogenic ones, and, therefore, the immune responses (either stimulation or
suppression) have to be considered as an unspecific indicator of environmental stress.
Phagocytic activity is an important immunological function in the study of bacterial infections
in fish and contaminants can affect spleen directly and change their normal function within
the immune system. These facts, together with contaminant exposure, could facilitate
development of infectious and/or non-infectious diseases and in this way resulting in different
disease prevalence and incidence. Pollution of the natural aquatic environment, with
industrial or agricultural sewage, is an important immuno-suppressing factor, resulting in
higher susceptibility of fish to infectious diseases (Köllner et al, 2002).
For that reason, this issue is also of relevance for environmental monitoring programmes
and useful, from both points of view, economic and public health.
Enlargement of the spleen is considered to be indicative of disease or immune system
problems (Dethloff and Schmitt, 2000). Parasitic infections, can lead to an increase in spleen
volume (Durborow, 2003; Khan, 2009), usually by development of leucocyte reactions
(Lizama et al., 2006). However, when relative spleen size is used as reflecting an immune
investment against parasites or pathogens, large spleen can be interpreted either as an
improving ability to respond to parasite exposure or an indication of high immunological
activity from already established infection. (Šimková et al., 2008).
Often the occurrence of MAs mainly around parasite larvae has been noticed in infected
liver and spleen (Dezfuli et al., 2007). In rainbow trout (O. mykiss) a positive association
between spleen size and resistance to bacterial disease was also found (Hadidi et al., 2008).
Histological, and morphometric modifications of splenic macrophage aggregates in sea
breams (Sparus aurata), infected by an ectoparasite in the gills, revealed a dramatic increase
in the size and number of MAs in fish (De Vico et al., 2008).
Increase splenosomatic index could be dependent on parasitic load. According to Lizama
et al. (2006), the infestations in fish Prochilodus lineatus, by acantocephalan, increase SSI,
while the infestation with metacercariae, due to the lower intensity of this infection, resulted
in SSI decrease.
Environmental alterations, due to contamination can also alter the SSI. Fish chronically
exposed to a bleached Kraft mill effluent (BKME) showed a tendency for high SSI (Adams et
al., 1992). Jenkins (2004) also found in black drum (Pogonias cromis), a splenosomatic index
significantly higher in fish from contaminated sites than in fish from reference sites.
Decrease in SSI is commonly found following contaminants exposure. Fish exposed to
organic contaminants, alone or in combination with metal, have shown decrease SSI (Hinck
22 C. Fernandes, A. Afonso and M. A. Salgado

et al., 2004). Exposure of fish to lead for up to 183 days was reported to produce a reduction
in spleen size, with an increase in leukocyte number (Saxena and Saxena , 2008). Decreased
SSI was also recorded in fish exposed to petroleum and polluted waters, with PCBs, PAHs,
metals (Dethloff and Schmitt, 2000). These findings are consistent with the use of SSI as a
sensitive end point biomarker.
A complex pattern of effects of paper mill effluents in fish physiology was observed.
Some results indicate that in-stream exposure to elemental-chlorine-free pulp and paper mill
effluents the SSI decreases. An experiment of 35 days exposure to surface water of up- and
downstream, from a pulp and paper mill treatment-effluent discharge, showed that SSI was
significantly decreased in fish downstream, compared to fish upstream, along with a transfer
from lymphocytes to neutrophils in peripheral blood (Baer et al., 2009).
The effects of paper mill effluents on free-ranging and captive largemouth bass
(Micropterus salmoides) were assessed by Sepúlveda et al., (2004). Fish in outdoor tank,
exposed to increasing full strength effluent for 28 or 56 days, showed that SSI was not
affected; whereas free-ranging bass sampled from effluent-dominated sites showed a
decreased in both SSI and number of splenic macrophage aggregates, in relation to reference
streams. Besides a decline on the weight of the spleen, results also showed hematological
changes, such as reductions in the number of red blood cells, probably caused by alterations
in the hemopoietic capacity of the spleen and/or head kidney. These authors also suggested
that the decrease number of splenic MAs is due to the decreased spleen weights since bass
with larger spleens and livers tend to have more MAs. Also an important issue addressed in
this study is that, although many of the physiological parameters measured were statistically
different from control or reference fish, they fell within normal physiological ranges when
compared to reports on largemouth bass and other freshwater species.
Based on that, it is evident that different responses could arise between laboratory and
field biomarker assessments, and also conclusions about significant trends observed must be
distinguished from normal physiological ranges.
As an unspecific indicator, also certain endogenous factors are known to affect the SSI.
The range of spleen sizes varies among fishes and populations of the same species. Relative
spleen weight may also differ with age, gender and gonad development (Dethloff and
Schmitt, 2000). Seasonal changes of the spleen size have long been known to occur in the
salmon (Salmo salar) and other salmonids. Before and after spawning the spleen is large and
hyperemic, but at spawning it shrinks and becomes anemic, maybe related to blood storage
rather than lymphoid or hemopoietic activities (Fänge and Nilsson, 1985). However, in BEST
fish monitoring program, in the Yukon River Basin, the SSI of longnose sucker (C.
catostomus), was not influenced by gender (Hinck et al., 2004).
Nonspecific stressors can also ending into altered spleen morphology. Several studies
have shown that fish under hypoxic conditions or severe exercise, reveals spleen contraction
and then decrease in size (Fänge and Nilsson, 1985; Dethloff and Schmitt, 2000). Rainbow
trout, generally considered to be a hypoxia-sensitive species, showed, during hypoxia
exposure, a decrease in SSI and an increase in blood hemoglobin. Splenic contraction and the
subsequent red blood cell release, accounts for decrease in SSI (Lai et al., 2006). Exercise at a
speed great enough to cause exhaustion also contributed to the increase in hematocrit of
Pagothenia borchgrevinki (Franklin et al., 1993).
Based on these considerations and according to Dethloff and Schmitt (2000), in addition
to histological data, that show a relation between cellular changes in the spleen and exposure
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 23

to contaminants, the SSI is a relevant indicator of spleen dysfunction and a useful biomarker
of fish health.

The Hepato-Somatic Index (HSI)

Alterations in liver size due to environmental stressors are of interest since liver plays
vital functions such as energy storage and metabolism. Evaluation of the hepato-somatic
index (HIS) must consider the endogenous, sometimes cyclic variations as well as the
exogenous factors associated with toxicant exposure.
The HSI varies with seasonal cycles (Delahunty and de Vlaming, 1980; Slooff et al.,
1983; Beamish et al., 1996; Saborowski and Buchholz, 1996). Nutritional quality and regimes
are main factors that affect relative liver size (Daniels and Robinson, 1986; Heidinger and
Crawford, 1977; Foster et al., 1993). Gonadal development and sex of fish make the HSI to
vary along the reproductive cycle (Fabacher and Baumann, 1985; Förlin and Haux, 1990;
Grady et al., 1992). In females, the HSI may change due to the synthesis of vitellogenin in
liver (Scott and Pankhurst, 1992).
Nevertheless, the HSI is the organo-somatic index most measured to assess pollution
exposure (Adams and McLean, 1985; Goede and Barton, 1990). Several investigators have
suggested that relative liver enlargement in fish indicates exposure to environmental
carcinogens or other toxic chemicals.
Studies evaluating the relative liver size of fish from contaminated and reference sites
often utilize the HSI, which expresses liver size as a percentage of total body weight (Facey et
al., 1999). The rock bass Ambloplites rupestris collected from a sediment contaminated
harbor showed a significant increase of splenic tissue occupied by macrophage aggregates
and greater HSI than fish from reference sites (Facey, 2005). In this study macrophage
aggregates and HIS were also used to evaluate the recovery of the fish population in a 7-year
period after remediation has been implemented.
An increase of HSI in brown bullheads (Ameiurus nebulosus) has been reported
associated with polycyclic aromatic hydrocarbons (PAHs) contamination (Fabacher and
Baumann, 1985; Gallagher and Di Giulio, 1989). Several other species (Atlantic cod, winter
flounder, redbreast sunfish, striped bass, hard-head catfish and European plaice) exposed to
different chemicals or mixtures of chemicals PAHs, PCBs, in natural or industrial waters, all
had enlarged livers (Poels et al., 1980; Fletcher et al., 1982; Buckley et al., 1985; Kiceniuk
and Khan, 1987; Adams et al., 1989; Everaarts et al., 1993; Secombes et al., 1995). This
enlargement of fish liver seems to be due to the increase of xenobiotic metabolism rather than
the increase of detoxification enzyme activities (Fabacher and Baumann, 1985; Gallagher and
Di Guilio, 1989). In a coastal lagoon, contaminated with metals, condition indices (K and
HSI) of mullets (Liza saliens) that bioaccumulated high concentrations of Cu and Zn in their
liver were higher compared to mullets from the sea, suggesting abnormal condition in the
lagoon population (Fernandes, 2008a).
In contrast with these results several other studies described a decrease of liver size
following exposure to contaminants (Chambers, 1979; Larsson et al., 1984; Hickie and Dixon
1987; Ruby et al., 1987; Hoque et al., 1998). The decrease of HSI may reflect glycogen loss
to produce energy (Barton et al., 1987) but histopathological alterations including hepatocyte
24 C. Fernandes, A. Afonso and M. A. Salgado

damage and degeneration may also result in decrease of liver size (Ram and Singh, 1988).
Other explanations attribute lower HSI to altered carbohydrate metabolism (Adams et al.,
1992a).
The use of SSI and HSI is very challenging since they respond to several affecting factors
that need to be recognized and avoided or accounted for, when possible. Organo-somatic
indices should only be compared within species, or at least between similar species, of the
same classes of age. In addition it is preferable a separation by gender, to avoid gender effect.
The sampling procedure must be quick and effective to avoid fish handling stress that can
provoke recruitment of erythrocytes from the spleen, and tissue alterations. Comparisons
between polluted and natural environments must be performed with fish caught at same
season. And finally, according to Dethloff and Schmitt (2000), organ size is better expressed
relative to fish size excluding the gonads weight.

CONCLUSION
Aquatic toxicology is part of a general trend in a world of increasing contaminant risks
and it is clear that confined waters are among great concern. Coastal and shallow lagoon
waters are still ecological and economical relevant resources that justify the study and
development of early warning systems for evaluation of aquatic environment and fish
population health. They are vital for implementation of effective recovery measures. This
chapter contributes to the knowledge of liver, kidney and spleen metabolic processes and their
alterations induced by pollutants exposure.
The fact that contaminants usually appear in the environment as complex mixtures that
can cause interactive effects, underlines the necessity of using a range of different biomarkers
when attempting to evaluate environmental impact. The use of liver, kidney and spleen as an
early warning system in population assessment, has the advantage of looking at different
metabolic and anatomic biomarkers levels and thus offering an integrated approach of toxic
effects.
Biochemical responses to contaminant exposure can include changes in neuroendocrine
control of osmoregulation, plasma electrolytes concentrations, EROD and plasmatic
transaminases activities, metallothioneins synthesis in liver and hematologic parameters in
spleen. Ultrastructural changes induced by toxicant exposure also occur in liver, kidney and
spleen depending on the concentration and length of exposure. Changes in histochemical
properties of splenic MAs are linked to fish exposure to contaminated environments. Besides,
organo-somatic indices variations, as a measure of immune defence and as well as energy
storage and metabolism, they reflect well fish toxic exposure.
 Metabolic and Structural Role of Major Fish Organs as an Early Warning System… 25

Figure 1. Diagram of the major fish organs involved in the regulation, hemopoietic, immune and
detoxification processes, and the evaluation of their responses to be used as fish biomarkers of
stress/injury.

The suite of methods that should be applied to each organ depends on sensitivity, cost-
effectiveness, the ability of the methods to detect the contaminants and requires expertise. In
addition, the experimental design should take into account the potential confounding factors
that may occur for each of the described biomarkers.
Regarding structural aspects, the knowledge of the normal organ microanatomy is
fundamental to properly evaluate abnormal physiologic and histological changes. The fact
that toxic agents can act as stressors also implies that their effects are partially additive with
those of other stressors. As outlined in this manuscript, the structure of the organs normally
varies in direct connection with gender, age, nutritional status, or temperature. Moreover, a
solid baseline data on the normal morphology and physiologic range is essential to establish
associations with toxic induced changes.
Concerning fish, long-term toxic exposure can instigate several adaptive responses
therefore is essential to know such variations for correct discrimination between structural
adaptations and lesions caused by pollutants.
The weight-of-evidence for the utility of analysing these organs, as an early warning
system, is that it can be useful for detecting toxic diffuse effects, such as those arising from
poor accumulation in fish. Similarly, more than one autochthon fish species is useful for
accurately assess the presence of environmental contaminants, given that metabolic pathways
in different species can show diverse sensitivity and behavior to respond against toxic
exposure.
This approach contributes to a realistic understanding of the implications and extent of
aquatic pollution and thus to choose wisely remediation strategies to achieve a sustainable
management.
26 C. Fernandes, A. Afonso and M. A. Salgado

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 39-72 © 2011 Nova Science Publishers, Inc.

Chapter 2

BENTHIC FORAMINIFERA IN COASTAL

LAGOONS: DISTRIBUTIONAL PATTERNS
AND BIOMONITORING IMPLICATIONS

F. Frontalini,1 E. Armynot du Châtelet2, J.P. Debenay3,

R. Coccioni1 and G. Bancalà1
1
DiSUAN, Urbino University, Campus Scientifico, Localita' Crocicchia,
61029, Urbino, Italy
2
CNRS, UMR 8157, UFR des Sciences de la Terre, Laboratoire Géosystèmes,
Université de Lille-1, bâtiment SN5, 59655 Villeneuve d‘Ascq cedex, France
3
IRD, Unité 182 LOCEAN, BP A5, 98848 Nouméa cedex,
Nouvelle-Calédonie, France

ABSTRACT
Coastal lagoons are particularly complex environments in which the transition
between marine and continental waters is gradual, due to the continuity of the aquatic
habitat. They are characterized by major fluctuations in chemical and physical
parameters, which reflect multiple interactions between the distance to the sea, water
depth, the nature of the sediment, organic matter quality, hydrodynamic turnover time,
tidal currents, wind forced currents, volume lost by evaporation, and gravitational
circulation. Moreover, these ecosystems are often subjected to a great deal of
anthropogenic impact, which further complicates our understanding of these habitats.
Comparative studies of lagoonal environments essentially require the utilization of
organisms that are distributed worldwide and occur in high density populations in most of
the benthic niches. This is certainly the case for foraminifers which, as lower trophic
level members, are crucial to the biological community and ideal candidates for
comprehensive habitat assessment. Some widespread paralic benthic foraminiferal
species are present from temperate macrotidal estuaries to tropical microtidal lagoons,
thus enabling comparative studies of environmental conditions to be conducted.
40 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

Since lagoons are increasingly affected by environmental stress and degradation due
to pollution and other anthropogenic factors, there is a pressing need to develop a set of
indicators and monitoring approaches with which to assess their health.
A large number of research programs have addressed these issues within various
regions, and studies of foraminiferal assemblages have produced very useful,
comprehensive datasets on environmental and biotic conditions.
This paper is a review of what is known about the foraminiferal assemblages living
in lagoons, including their distribution according to environmental parameters and their
value when it comes to assessing environmental quality in these ecosystems.

1. INTRODUCTION
A lagoon is ‗a body of shallow sea water or brackish water separated from the sea by
some form of barrier‘, which excludes isolated inland saline water bodies. In reality, lagoons
are complex ecotones located between continental and marine systems. They are also highly
heterogeneous due to: 1) strong variations in physical, chemical and biological characteristics
over space and time, and 2) multiple exchanges with the limiting continental and marine
systems, the atmosphere, and sediments. Located at the transition between the continental and
the marine realms, lagoons belong to paralic habitats. The term paralic was defined by
Naumann (1854) for fossil environments and was first used by a sedimentary geologist. Later,
the notion was adapted to apply to recent ecosystems comprising estuaries, coastal lagoons,
marshes, and coastal zones under high freshwater input (Guélorget and Perthuisot, 1983,
1992). This term is more precise than the traditional phrase ‗margino marine‘ and is
increasingly used to refer to modern environments.
For the purpose of this study, we restricted our survey to clastic lagoons separated from
the ocean by a depositional land barrier, excluding coral reef lagoons. We also used the
physiography of clastic lagoons as clarified by Kjerfve (1986), who distinguished between
restricted, choked and leaky lagoons (Figure 1). In particular, restricted lagoons are
characterized by two or more entrance channels or inlets as well as well-defined tidal
circulation.

Figure 1. Schematic representations of restricted, choked and leaky lagoons, after Kjerfve (1986)
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 41

Like other paralic environments (e.g. marsh, mangrove, estuary, fjord and delta), lagoons
exhibit a balance between an enhanced freshwater input and an evaporation loss, which
determines a salinity gradient within the continuity of the aquatic habitat. Transition
processes are much more complex in sheltered lagoons with high water retention times than
in large well-flushed estuaries. On the basis of the triple influence of fluvial input, exchanges
with the sea, and climate, the gradation can be either horizontal and/or vertical, and moves
from brackish to hypersaline environments. These general conditions are complicated by a
complex interplay of an array of parameters that include: (1) local climatic conditions (i.e.
temperature, insolation, evaporation-rainfall balance); (2) horizontal salinity distribution,
which also controls plant distribution; (3) vertical mixing between hypo- and hypersaline
water, thus affecting water stratification; (4) hydrodynamic turnover time; (5) the energy of
wind-forced currents and wave action; (6) the nature of the bottom; (7) the occurrence of
seaweed or seagrass meadows; (8) the quality and quantity of suspended sediment (turbidity),
nutrients, and dissolved and particulate organic matter; (9) the physical-chemical
characteristics of the water (mainly oxygen content and pH); and (10) aperiodic crises, such
as anoxia, drought, storms, or frost (Debenay et al., 2000; Debenay and Guillou, 2002).
These multiple factors lead to a major internal patchiness and heterogeneity, as well as
environmental fluctuations which occur at a variety of time scales ranging from daily to
seasonal to years/decades, and which are further influenced by multiple impacts of
anthropogenic activities. These can be the result of: pollution from industrial, domestic,
agricultural, and mining work; dredging and spoil dumping; salinization; siltation and
sedimentation from land clearance; forestry; and the destruction of habitat. Agricultural
runoffs may be enriched in nutrients and pesticide residues, the former of which can lead to
eutrophication, the deterioration of water quality and, ultimately, anoxic conditions (Wilson et
al., 1993; Moss, 1996). However, nutrients are not the only chemicals affecting the
ecosystems; trace elements and other organic and inorganic chemicals are also ubiquitous
contaminants of the aquatic environment.
There is, therefore, a need to develop a set of indicators and monitoring approaches for
use in these shallow transitional waters which are increasingly affected by environmental
stress that is naturally and, above all, anthropogenically induced. This requirement is made
more difficult by the complexity of these environments, which can often influence and
complicate the application of the most common indicators and indices of environmental
quality and health status.
A large number of research programs have addressed these problems within various
coastal regions, and have produced extremely valuable and comprehensive datasets on the
environmental and biotic conditions within these systems. A growing number of new tools
and methods for assessing the health of these systems have thus emerged, and of these
foraminifera are of primary importance.
Foraminifera (class Foraminifera: d‘Orbigny, 1826; phylum Granuloreticulata) are
single-celled organisms (protists), which play a significant role in global, biogeochemical
cycles of inorganic and organic compounds, making them one of the most important animal
groups on earth (Haynes, 1981; Lee and Anderson, 1991; Yanko et al., 1999). Furthermore,
many foraminiferal taxa secrete a carbonate shell, which is readily preserved and so records
evidence of environmental stresses and changes over time. They are commonly small and
abundant compared to other hard-shelled taxa and are easy to collect, meaning that a highly
reliable database for statistical analysis can be obtained, even when only small sample
42 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

volumes are available. Because of their: widespread distribution; short life and reproductive
cycles (from a few weeks for small taxa to one year for some larger forms: Boltovskoy, 1965,
and Murray, 1991, 2006); high biodiversity; and specific ecological requirements,
foraminifera respond rapidly to environmental changes. Benthic foraminifera are particularly
sensitive, and can be successfully utilized for their value as bio-indicators of environmental
change in a wide range of marine environments (e.g. Alve, 1991, 1995; Yanko et al., 1999;
Coccioni, 2000; Debenay et al., 2001, 2005; Murray and Alve, 2002; Armynot du Châtelet et
al., 2004; Frontalini and Coccioni, 2008; Frontalini et al., 2009, 2010; Coccioni et al., 2009;
Debenay et al., 2009a; Armynot du Châtelet and Debenay, 2010).
The aim of this paper is to review the recent advances and achievements when it comes to
understanding the processes controlling the distribution of foraminiferal assemblages within
lagoons. The main findings in relation to an array of parameters will also be summarized and
emphasized. The article will also discuss the significance and influence of anthropogenic
activities on benthic foraminifera in these sensitive, but environmentally valuable, areas.

2. MATERIAL AND METHODS

Samples were collected either with a grab sampler or by snorkelling in subtidal
environments. At intertidal stations, the samples were obtained by scraping off the upper five
millimeters of sediment. The collections were made at several points over a surface of about 1
m2 using a pseudoreplication strategy (Hurlbert, 1984) to limit the bias due to patchy
distribution. In such heterogeneous environments, field experience shows that the standard
collection of samples over a 10 cm2 surface (e.g. Wells, 1971) does not provide reliable data,
while the time consuming study of replicates (e.g. Murray, 2006) is justified only for detailed
studies of living assemblages. Samples can be preserved in alcohol (ethanol), which allows
Rose Bengal staining (Walton, 1952) to be used to help identify living individuals. Only
superficial samples are considered because, even though foraminifera can live at depths of 30
cm in the sediment (e.g. Goldstein et al., 1995; Ozarko et al., 1997), the greatest numbers of
living creatures, which produce the accumulation of living and empty tests, are found in the
surface layer <1 cm (review in Alve and Murray, 2001). Collecting sediment from greater
depths would also include tests deposited over a long period of time.
At the laboratory, a subsample of 50 cm3 was extracted from each sample after
homogenization and then washed through 315 and 50/63 μm sieves. After drying, the
microfauna were separated from sand grains by flotation on trichloroethylene (d=1.465) or
carbon tetrachloride (d=1.594). Observations were carried out under a stereo microscope and:
(1) the total number of tests in 50 cm3 of sediment was examined; (2) 100 to 300 individuals,
depending on the total number of species, were counted (Fatela and Taborda, 2002); and (3)
whole samples were checked for rare species which were not found during counting. When
the population density was lower than 100, all of the individuals were counted. Rose Bengal
stained (living?) individuals were noted separately to provide information on living, dead and
total (stained + empty tests) assemblages. However, the reliability of Rose Bengal staining for
determining living individuals is still the subject of some debate (discussion in Debenay et al.,
2009b, p. 253-254), and the study of living assemblages in highly dynamic environments,
such as lagoons, might be more appropriate for time series studies.
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 43

3. FORAMINIFERA LIVING IN LAGOONAL ENVIRONMENTS

Complicated by tidal and seasonal cycles, the physicochemical characteristics of lagoonal
environments can change drastically in relation to hydrodynamic turnover time (itself a
function of freshwater input), tidal currents, wind forced currents, and volume lost by
evaporation and gravitational circulation. Benthic organisms living in such environments
must adapt to this instability and are generally euryhaline and eurythermal. For example, the
cosmopolitan Ammonia tepida tolerates salinities ranging from 0.2 to 100 (Bradshaw, 1957;
Reddy and Rao, 1984; Debenay, 1990; Almogi-Labin et al., 1992; Wennrich et al., 2007).
However, only a few species can tolerate such ecological conditions, and the foraminiferal
assemblages in lagoons are poorly diversified and display high levels of dominance. Despite
the fact that endemic species which characterize specific areas can be found, there is an
overall species similarity in lagoonal environments. The foraminiferal assemblages are
generally dominated by Rotaliina in moderately restricted environments, the most
cosmopolitan species being Ammonia parkinsoniana (d‘Orbigny, 1839), Ammonia tepida
(Cushman, 1826), Elphidium gunteri (Cole, 1931), Haynesina germanica (Herenberg, 1840),
and Quinqueloculina seminula (Linné, 1758) (Figure 2). On the other hand, the agglutinated
species Ammobaculites exiguus Cushman and Brönnimann, 1984, Ammotium salsum
(Cushman and Brönnimann, 1984), Arenoparella mexicana (Kornfeld, 1931), Gaudryna
exilis Cushman Brönnimann, 1984, Haplophragmodes wilberti Andersen, 1953,
Pseudoclavulina sp. and Trochammina spp. are the dominant species in restricted to highly
restricted environments (Figure 2). Low salinity habitats are dominated by Miliammina fusca
(Brady, 1870), Astrammina sphaerica (Heron-Allen and Earland, 1932) and Polysaccammina
ipohalina Scott, 1976 (Figure 2).
Ammonia tepida and Q. seminula are considered to be quite tolerant of environmental
stress (Debenay et al., 2000; Debenay and Guillou, 2002), and these two species have been
regarded as the primary pioneers in several paralic environments (Debenay et al., 2009b). For
example, in the hypersaline Araruama Lagoon (Brazil) and Lake Qarun (Egypt), they
comprise 70% of the total foraminiferal assemblage (Debenay et al., 2001; Abu-Zied et al.,
2007). Ammonia beccarii (tepida?), which is associated with Cribroelphidium articulatum,
was also reported as being present in the hypersaline Coorong Lagoon (Cann et al., 2000). It
is also well represented in the Santo André Lagoon, Portugal, in association with H.
germanica, Elphidium oceanensis and Q. seminula (Cearreta et al., 2002); in Lake lllawarra,
Australia, where it is associated with Cribrononion sydneyensis (Yassini and Jones, 1989)
and in small coastal lagoons located along the coast of West Africa (Debenay, 1990). In
Croatia, A. tepida lives in low-oxygen, slightly hypersaline lagoons, typically in association
with Haynesina depressula Walker and Jacob, 1798, Elphidium crispum (Linné, 1758), and
Quinqueloculina spp. (Vanicek et al., 2000). However, a great deal of confusion still exists
about the variety of forms and the taxonomy of the genus, despite numerous attempts to
clarify these issues (e.g. Hayward et al., 2004). It is, therefore, highly probable that several
different species are present in lagoons.
44 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

Figure 2. Benthic foraminiferal species in lagoon environments: 1. Polysaccammina ipohalina, 2.

Trochammina inflata, 3. Pseudoclavulina sp., 4. Ammobaculites exiguus, 5. Ammotium salsum lateral
and apertural views, 6. Miliammina earlandi apertural and lateral views, 7. Miliammina fusca lateral
and apertural views, 8. Caronia exilis lateral and apertural views, 9. Quinqueloculina seminula, 10.
Arenoparrella mexicana spiral, apertural, and umbilical views, 11. Haplophragmoides wilberti lateral
and apertural views, 12. Eponides repandus apertural and spiral views, 13. Discorbinella bertheloti
spiral, umbilical, and lateral views, 14. Bolivina striatula, 15. Porosononion granosum, 16. Nonionella
turgida, 17. Discorinopsis agayoi umbilical and spiral views, 18. Pararotalia cananeiaensis spiral,
lateral and umbilical views, 19. Ammonia parkinsoniana umbilical view, 20. Ammonia tepida umbilical
views, 21. Elphidium gunteri, 22. Cribroelphidium excavatum, 23. Haynesina germanica, 24.
Haynesina depressula, 25. Elphidium crispum. Scale bars are 100µm
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 45

The geographic distribution of these paralic species covers spectacularly wide latitudinal
and longitudinal ranges (e.g. Sen Gupta, 1999; Debenay and Guillou, 2002), and their
worldwide distribution supposes powerful dispersion processes. Aerial transport, over short
or great distances, is often mentioned, since foraminifera may occasionally survive on the
muddy feet or feathers of migratory seabirds, whose landfalls are mostly intertidal mud and
sand flats (e.g. Resig, 1974; Lessard, 1980; Patterson et al., 1997; Hayward and Hollis, 1994;
Almogi-Labin et al., 1995; Wennrich et al., 2007). Transport by fish is also possible if they
move from one area to another during feeding and defecation (Daniels and Lipps, 1978;
Langer and Lipps, 2006; Debenay et al., in press). The transplantation of marine fish or
shellfish may also play a part in the introduction of new foraminifera (Arnal, 1954; Bouchet
et al., 2007). Travel over short distances may similarly affect embryonic juveniles, which are
easily transported thanks to a density that is similar to that of seawater (Goubert, 1997; Alve,
1999; Hayward et al., 1999). Accordingly, incoming tidal currents probably introduce many
coastal species to the lagoons, but only those that can adapt, grow and reproduce in the new
environment survive.
In shallow paralic environments, the most successful colonizer is A. tepida in both
brackish (Wennrich et al., 2007) and hypersaline (Almogi- Labin et al., 1992) waters. Indeed,
during interglacial intervals in the Quaternary, it colonized lakes along the Mediterranean
(Usera et al., 2002). It also populated shrimp ponds, which are associated with Q. seminula,
with its fast reproduction rates rapidly increasing the density of live specimens and the
accumulation of empty tests (Debenay et al., 2009b).

4. DISTRIBUTION OF FORAMINIFERA IN
LAGOONAL ENVIRONMENTS

4.1. Common Pattern

Numerous studies of benthic foraminiferal assemblages have been carried out in lagoons,
(e.g. Closs, 1963; Closs and Madeira, 1968; Schafer and Sen Gupta, 1969; Murray, 1971;
Madeira-Falceta, 1974; Suguio et al., 1975; Scott, 1976a,b; Zaninetti et al., 1977, 1979; Scott
and Medioli, 1980; Zaninetti, 1982; Beurlen and Hilterman, 1983; Boltovskoy and Martinez,
1983; Debenay, 1990, 1991; Albani et al., 1991; Debenay et al., 1993; Alve and Murray,
1994a; Hayward et al., 1996; Redois and Debenay, 1996; Vanicek et al., 2000; Coccioni,
2000; Cearreta et al., 2002; Serandrei Barbero et al., 2004). A common pattern is their general
distribution along a marine-continental gradient, with diverse assemblages, including
calcareous forms closest to the ocean, changing landwards into oligospecific-to-monospecific
assemblages in both hyposaline and hypersaline environments (Debenay et al., 2000;
Debenay and Guillou, 2002). Low diversity assemblages present in the areas closest to
freshwater input contain only agglutinated species (e.g. Serandrei Barbero et al., 1997; Lloyd
and Evans, 2002)
As stated by Nichols (1974) and reported in numerous studies, this pattern suggests that
salinity is the major controlling factor for the presence of foraminiferal assemblages in paralic
environments. However, their distribution is often more complex, reflecting multiple
interactions between the distance to the sea, water depth, the nature of the sediment,
46 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

hydrodynamic turnover time, tidal currents, wind forced currents, and gravitational
circulation etc. It also depends on the great variety of foraminiferal behaviour, namely mode
of nutrition, tolerance to oxygen depletion, steno- or euryhalinity, steno- or eurythermy, epi-
or endofaunal mode of life, and free or attached mode of life. Among the major parameters
identified as having a strong influence on foraminiferal distribution are: exposure during tidal
cycles (Hayward and Hollis, 1994; De Rijk, 1995; Horton et al., 1999); pH (Wang, 1992);
organic matter content; and grain size of the sediment (Scott et al., 1979; Zaninetti, 1982;
Petrucci et al., 1983; Albani et al., 1991; Jennings and Nelson, 1992; Coccioni 2000).
Consequently, foraminiferal assemblages may change considerably from one lagoon to
another, depending on local characteristics.
As a result of the complexity of interpreting entire assemblages, biocenotic indices, such
as the diversity index or the dominance index, are often used for the characterization of the
community structure and, subsequently, environmental conditions. However, attempts to use
the Fisher diversity index revealed that values vary irregularly between 2 and 8 inside the
lagoons, without any clear ecological significance (Zaninetti et al., 1977; Debenay, 1990;
Debenay et al., 1998). This is probably the result of a replacement of fauna (hyaline species
replaced by agglutinated ones), rather than a simple faunal change. Moreover, biocenotic
indices neither take into account the role of the species in the community, nor their potential
interest as bioindicators. Accordingly, they are of lesser value than the methods based on the
presence/absence of bioindicator species (Caquet and Lagadic, 1998).
Instead of such biocenotic indices, the ―Confinement Index‖, or Ic, which is based on the
relative abundance of species identified as being characteristic of environmental conditions,
has been defined in the estuaries and lagoons of West Africa (Debenay, 1990). It was later
adapted, with slight modifications, for utilization in Brazilian lagoons (Debenay et al., 1996),
a Mediterranean lagoon (Debenay et al., 2005), and in the Mekong estuary (Debenay and
Luan, 2006). The species used for the calculation of the Ic are listed in Table 1.
The following selected examples were studied separately by one of us. They are grouped
together here to illustrate the particular conditions that can prevail in some representative
lagoonal environments.

Figure 3. Locations map of some of the presented lagoons

 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 47

Table 1. The Confinement Index and the species considered

for its calculation in different worldwide areas

Group A, species related to
strong marine influence:
Mediterranean Elphidium crispum,
(Kalloni) Gavelinopsis praegeri,
Lobatula lobatula, Nonionella
turgida, Quinqueloculina
stelligera, Rosalina bradyi, R.
floridensis, R. globularis,
Triloculina adriatica
Vietnam Asterorotalia dentata,
(Mekong Asterorotalia pulchella,
delta) Brizalina striatula,
Cribroelphidium cf. incertum,
Rosalina sp.
Brazil (coastal Bolivina striatula, Elphidium
lagoons) gunteri, Pararotalia sp.,
Rosalina spp.
Africa Elphidium fichtelianum,
(coastal Pararotalia sp., Bolivina
lagoons and striatula, Rosalina spp.
estuaries)
Western coast Brizalina strialula, Brizalina
of France variabilis, Cribroelphidium
excavatum, Elphidium
pulvereum, Quinqueloculina
stelligera, Rosalina spp.
Ic = (C /(B + C) - A /(A + B) + 1)/2Ic = 1 if assemblage III is the only one represented (A + B = 0);
Ic = 0 if assemblage I is the only one represented (B + C = 0). Ic<0.4 indicates low confinement;
0.4<Ic<0.7 indicates moderate confinement; Ic>0.9 indicates an extreme confinement
Group B, species from paralic
environments subjected to
noticeable marine influence:
Aubignyna planidorso,
Brizalina striatula, B.
variabilis, Eggerelloides
scaber, Elphidium jenseni,
Porosononion granosum
Ammonia spp., Brizalina cf.
variabilis, Haynesina sp.,
Miliammina spp.,
Quinqueloculina seminula
Ammonia spp., Bolivina
variabilis, Elphidium
galvestonense, Haynesina
germanica, Quinqueloculina
seminula, Quinqueloculina
poeyana
Eggerelloides scaber,
Quinqueloculina poeyana, Q.
seminula, Haynesina
germanica, Elphidium
gunteri, E. limosum, Bolivina
variabilis, Ammonia spp.
Ammonia tepida, Elphidium
gunteri, Haynesina
germanica, Quinqueloculina
seminula
Group C, euryhaline species
living in more restricted areas:
Ammonia tepida, A. convexa,
Cribroelphidium translucens,
Haynesina depressula
simplex, Haynesina sp.,
Quinqueloculina seminula
Ammobaculites formosensis,
Ammotium cf. salsum,
Arenoparrella asiatica,
Haplophragmoides wilberti,
Jadammina macrescens,
Siphotrochammina lobata,
Trochammina spp.
Ammobaculites exiguus,
Ammotiumsalsum,
Arenoparrella mexicana,
Gaudryina exilis,
Haplophragmoides wilberti,
Miliammina spp.,
Trochammina spp.,
Siphotrochammina spp.
Ammobaculites exiguus,
Ammotium salsum,
Arenoparella mexicana,
Gaudryina exilis,
Haplophragmoides wilberti,
Miliammina spp.,
Trochammina spp.,
Siphotrochammina lobata
Jadammina macrescens,
Miliammina spp.,
Paratrochammina spp.,
Trochammina spp.

4.2. Choked Stratified Lagoon

Example: Lagoa da Conceição, Brazil, latitude ≈ 27°3 S (Debenay et al., 1998; Figures 3
and 4).

Morphology
The lagoon is elongated, about 13.5 km in length, with a total surface area of about 19
km2 (Knoppers et al., 1984; Muehe and Caruso-Gomes, 1989). It communicates with the sea
via a narrow, 2 m deep and 2 km long channel (Odebrecht and Caruso-Gomes, 1987; Sierra
de Ledo and Klingebiel, 1993). The lagoon is longitudinally divided into three zones, with a
maximum water depth of about 8 m, and is separated by shallows and/or narrowings. The
48 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

dunes extend into shallow sandbanks on the east side, while a deep channel is present on the
west side (Figure 4).

Hydrodynamics
The long and shallow entrance channel reduces water exchanges with the ocean, while
fresh water enters the lagoon through runoff from the western granitic reliefs, the João
Gualberto River discharge in the northern zone, and groundwater seepage from the sand
dunes in the southern zone (Odebrecht and Caruso-Gomes, 1987). During the rainy season,
the high freshwater input is responsible for strong water stratification, with brackish
superficial water (≈18‰) and saline bottom waters (> 30‰) being trapped in the depressions
and becoming anoxic. During the dry season, the stratification is weakened and the bottom
waters can be renewed.

Sediments
The sediments in the depressions are organic-rich muds, while fine to medium grained
sands, with numerous fragments of euryhaline Pelecypods, make up the sand banks.

Figure 4. Conceição Lagoon on Santa Catarina island. A. Horizontal distribution of the main
foraminiferal species showing the dominance of agglutinated species on sand banks while hyaline
species dominate in deeper areas; B. Vertical distribution of the main foraminiferal species showing the
impact of the halocline on the dominant species. C. Distribution of Ic values with depth showing the
impact of the halocline on foraminiferal assemblages (after Debenay et al., 1998)
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 49

Foraminiferal Assemblages
The density of tests in 50 cm3 of sediment (D50) varies from zero to 800 inside the
lagoon, reaching 5000 in the outer part of the entrance channel. Thirty-three species are
found. The assemblages reveal little horizontal change, except for a higher percentage of
Miliammina (70%), which is under the direct influence of freshwater input. Vertically, they
change abruptly at about the halocline: shallow sand banks (<1.5 m) are dominated by
agglutinated species, mainly Ammotium salsum, which is associated with A. exiguus,
Pseudoclavulina sp., G. exilis, and Miliammina earlandi. Depressions, on the other hand, are
characterized by less restricted foraminiferal taxa, such as A. tepida and E. gunteri (Figure 4
A-B). This deeper microfauna only develops during periods of bottom water renewal (dry
season), while only empty tests are found during anoxic conditions (rainy season).
Pararotalia cananeiaensis, which is characteristic of a stronger marine influence, is found
only in the outer part of the channel.
The diagram of the Ic vs. depth clearly shows the distribution of the two assemblages,
which are separated from each other at the depth corresponding to the halocline (Figure 4C).
The Ic index, which is between 0.4 and 0.7 in most parts of the depressions, indicates a
moderate confinement, while a strong confinement is suggested in the shallow areas.
Stratification is also observed in the choked, hyposaline Ebrie Lagoon (Ivory Coast;
Debenay et al., 1987). Ammotium salsum is the dominant species, and is associated with A.
tepida near the entrance channel. A high proportion of Miliammina spp. occurs near the
mouth of the main tributary. Neither foraminifera nor other microorganisms are found in the
deep anoxic depressions.

4.3. Restricted Lagoon with Salt Wedge

Example: Cananéia-Iguape Lagoon, Brazil, latitude ≈ 25° S (Eichler et al., 1995;

Debenay et al., 1998; Figures 3 and 5)

Morphology
The Cananéia-Iguape Lagoon is made up of channels that run parallel to the coastline and
are separated from the sea by a sand spit, which is more than 70 km long. The study area in
the south-eastern part of the lagoon consists of two channels that are 6 to 10 m deep (Mar de
Cubatão and Mar de Cananéia), and are connected southwards with the Baia de Trapandé (10
m deep), which is wide open to the sea through a 13 m deep inlet (Figure 5). Mangroves are
well developed on the edges of the lagoon.

Hydrodynamics
The characteristics of the mixohaline waters depend on sea-water inputs during semi-
diurnal microtidal tides (mean amplitude about 0.8 m) and seasonal cycles of freshwater input
from small coastal rivers (Miyao et al., 1986). The resulting pattern is an inclined salinity
gradient (salt wedge), which is related to gravitational circulation (Kjerfve, 1986; Kjerfve and
Magill, 1989) (Figure 5B).
50 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

Figure 5. Cananéia-Iguape Lagoon. A. Horizontal distribution of the main foraminiferal species

showing changes from hyaline species near the inlet to agglutinated species landward. B. Distribution
of salinity values with depth and distance to the sea showing the salt wedge. B. Distribution of Ic values
with depth and distance to the sea where the influence of the salt wedge can be seen. Anomalous values
of Ic are found in areas subjected to pollution (after Eichler et al., 1995; Debenay et al., 1998)

Sediments
The sediments are mostly muddy sands, with mud in restricted areas, sand near the inlet
where the tidal currents are stronger, and coarse sand and gravel in estuaries where there are
strong currents during the rainy season.

Foraminiferal Assemblages
The density (D50) varies from 20 to 3000, reaching a maximum at Baia de Trapandé. The
microfauna are comprised of about 100 species. Near the lagoon entrance, under marine
influence, the assemblage is dominated by calcareous species, particularly P. cananeiaensis,
which is associated with Brizalina striatula, E. gunteri, and Pseudononion atlanticum (Figure
5A). This assemblage progressively changes landwards, with an increasing proportion of
agglutinated species, such as A. salsum and G. exilis, becoming dominant in restricted areas.
In low salinity areas, the assemblages become oligospecific, with the M. earlandi
predominating. The progressiveness in the transition means that it is not possible to subdivide
the lagoon into clearly distinct zones.
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 51

The Ic index increases progressively landwards, reflecting the gradual transition in

foraminiferal assemblages. It increases more rapidly in the shallow waters (Ic D 0:4 about 10
km from the sea) than in the deep bottom waters of the channel (Ic D 0:4 about 18 km from
the sea), revealing a weaker marine influence in the shallower areas in relation to the salt
wedge (Figure 5C).

4.4. Choked Non-Stratified Hypersaline Lagoon

Example: the Lagoon of Araruama, Brazil, latitude ≈ 23° S (Debenay et al., 2001, Figures
3 and 6)

Morphology
The Lagoon of Araruama is one of the largest hypersaline lagoons in the world (Kjerfve
et al., 1996). It is about 47 km long, with a surface area of 210 km2 and an additional 65 km2
of adjacent salt-producing ponds. Its average depth is about 3 m up to a maximum of 17 m. It
has only limited water exchanges with the sea through a narrow and shallow entrance channel
(less than 4 m deep) located at its eastern extremity. Sand spits, constructed by wind driven
circulation cells, extend into sand banks and partially divide the lagoon into several basins.

Hydrodynamics
The deficit in the water balance: average rainfall ≈700 mm/y, average evaporation ≈1400
mm/y (Kjerfve et al., 1996), results in permanently hypersaline conditions. The mean salinity
may exceed 65‰ (average 52‰; André et al., 1979), lowering only in the entrance channel
and the eastern-most basin. In the salt-producing ponds it exceeds 100‰. Only two
tributaries, located in the north-western part of the lagoon, have permanent runoffs. Other
freshwater inputs result from rainfall, runoffs, small river occasional discharges, and domestic
sewage, which are estimated to be 0.7 m3/s (Kjerfve et al., 1996). The increase in the
superficial water density, which results from intense evaporation, induces mixing in the water
column and prevents water stratification. The tidal range (0.8 m to 1.3 m in the open ocean)
rapidly weakens in the lagoon, where it becomes negligible (14 km inside) (Lessa, 1990). The
circulation processes are dominated by clockwise wind driven circulation cells.

Sediments
The input of fluvial sediments is noticeable in the western part of the lagoon where fine
organic rich sediments accumulate (Azevedo, 1984; Barroso, 1987). The finest sediments,
which are comprised of up to 98% of silt and clay, are mainly present in the deepest, central
part of the lagoon and in the shallow, eastern-most lagoon cell. They are black and reduced,
except for a thin surface layer. The sediments of the shallower northern and southern parts of
the lagoon are shelly sands with a thick oxidized layer. The western-most lagoon cell often
has accumulations of organic remains (plant fragments, dead fish or various domestic
effluents). The maximum concentrations of organic carbon, phosphorus, and nitrogen are
found near to human activities (Campos et al., 1979; Debenay et al., 2001).
52 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

Figure 6. Araruama Lagoon. The dominance of Ammonia tepida is related to enrichment in

anthropogenic nutrients along the northern shore and eastern part of the lagoon assemblages (after
Debenay et al., 2001)

Foraminiferal Assemblages
The density (D50) varies from 50 to about 50,000 inside the lagoon, reaching 500,000 in
adjacent areas. A total of seventy-four species are found, with the species richness of the
samples ranging between 5 and 27. Very few specimens were alive. The D50 is highest along
the northern coast and in the central part of the lagoon, while it is less than 1000 near to the
main urban areas, Araruama City and Cabo Frio. In the entire lagoon, the assemblages are
dominated by three species: A. tepida, Q. seminula (first identified as Triloculina oblonga)
and the less abundant Cribroelphidium excavatum var. selseyense. Ammonia tepida is
dominant (50%-92% of the assemblages) along the northern shore and at the eastern end of
the lagoon, while Q. seminula is dominant at the other stations (Figure 6). This has been
attributed to the input of wastewaters and the enrichment in anthropogenic nutrients along the
northern shore and eastern part of the lagoon. Only a few species that are indicative of marine
influence are present in the outermost stations of the entrance channel (e.g. Eponides
repandus, Discorbinella bertheloti, Pseudononion atlanticum, Quinqueloculina lamarckiana
and P. cananeiaensis). In adjacent areas, Q. seminula is frequently dominant, and is
associated with A. tepida and species that are absent or rare in the lagoon, such as
Discorinopsis aguayoi. Textulariidae are nearly absent, even in the hyposaline estuaries of the
tributaries. No correlation was observed between the abundance of common species and any
of the sedimentary parameters. The Ic index is about 0.5 in almost the entire lagoon, except
near the entrance and in the estuaries of the tributaries.

4.5. Restricted, Non-Stratified Lagoon, with Roughly Normal Saline Waters

Example: Gulf of Kalloni, Lesvos Island, Greece, latitude ≈ 39°05‘ N, longitude ≈ 26°10‘
E (Debenay et al., 2005; Figures 3 and 7)
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 53

Morphology
The Gulf of Kalloni is essentially a lagoon that is about 20 km long, with a surface area
of about 130 km2. It communicates with the sea through a narrow inlet, which is less than 2
km wide, at its south-western end. The depth of about 25 m at the inlet decreases steadily
north-eastwards, while the gulf progressively widens, ending up in a wider and shallower
north-eastern part.

Hydrodynamics
During the dry season (May-September), weak freshwater input and strong wind-induced
evaporation lead to higher salinity (38‰) in the north-eastern end of the gulf. During the
rainy season (October-April), freshwater input from small intermittent rivers lowers the
salinity, the seasonal range being about 5‰ (Lefebvre, 1993). No vertical salinity
stratification was observed, other than temporary stratification during strong rainfalls.
According to Kjerfve and Magill (1989), the horizontal salinity gradient demonstrates that the
flushing rate is relatively long in the north-eastern part of the gulf.
Water exchange with the Aegean Sea depends on tidal flow (maximum tidal range of 23
cm) and wind-forced currents (Millet and Lamy, 2002; Debenay et al., 2005). When northern
winds dominate (June to September), the marine waters penetrate through the central part of
the gulf, reaching its north-east end in less than five days; the ebb tidal flow moves along the
shores. In contrast, when the southern winds blow (October to March), the marine waters
penetrate along the shores, particularly the southern shore. The seawards ebb tidal flow
moves through the central part of the gulf. North-westerly and south-easterly winds, which
only blow for limited periods, induce clockwise gyratory currents that limit the inflow of
marine water to the south-western part of the gulf and enhance the confinement in the north-
eastern part (Millet and Lamy, 2002).

Sediments
The bottom sediments are sand, muddy sand or sandy mud, with a greater proportion of
mud (up to 93%) in the low energy, deepest areas. These are mostly of terrigenous origin,
with a greater contribution of carbonate biogenic production in the shallower sandy areas.
They are enriched in organic matter near a fish farm and a small town to the south. The
concentration of Cu is low in most of the gulf (around 14 ng/g), revealing the absence of
noticeable chemical contamination, except in the vicinity of the town of Skala Kalloni (53
ng/g) (Angelidis et al., 2001).

Foraminiferal Assemblages
The density (D50) varies from 160 to about 40,000, with the maximum being near the
inlet. The lower values are in the central axis of the gulf and in two areas of high organic
input near a fish farm and a town. A total of 147 species is found, which is quite high
compared to the shallow choked lagoons of the western Mediterranean (69 in the Thau
Lagoon, France (Kurk, 1961) and 47 in the Prévost Lagoon, France) (Favry et al., 1998), but
considerably lower than in Mediterranean open gulfs: 222 species in the Gulf of Policastro,
Italy (Sgarrella et al., 1985) and 366 in the Gulf of Naples (Sgarrella and Moncharmont-Zei,
1993). With respect to foraminiferal assemblages, the Gulf of Kalloni has an intermediate
position between choked lagoons and the gulfs that are wide open to the sea. The species
54 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

richness ranges between 11 and 81, with decreasing values from the inlet towards the north-
eastern end of the gulf and from the shores towards the deeper, central part. The six dominant
species are Haynesina sp., Aubignyna planidorso, A. beccarii, A. tepida, Porosononion
granosum and Nonionella turgida. Ammonia tepida and Haynesina sp. achieve their
maximum relative abundances in the north-eastern part of the gulf and in the two areas of
high organic input. A. planidorso and P. granosum reach their highest relative abundance
along the central axis of the gulf, where water energy is lower in the depression of the
southern axial zone, and in the centre of the gyratory currents affecting the north-eastern part
of the gulf. The lower density and species richness in the two areas of high organic input may
result from low-oxygen stress. At these two stations the dominant species A. tepida and
Haynesina sp. Owing to the weak freshwater influence, the agglutinated species used for
calculating the Ic in previous studies are extremely rare or are not found in the Gulf of
Kalloni
The distribution of the Ic reflects the decreasing marine influence north-eastwards; values
are higher than 6.5 in the north-eastern part of the gulf (Figure 7), indicating more restricted
conditions. The values of the Ic are also high in the two areas of high organic input,
highlighting that organic matter accumulation can have the same impact on this index as
decreasing marine influence does.

Figure 7. Gulf of Kalloni. Values indicated on this figure were measured in September 1993. The Ic
values show increasing confinement with distance to the sea and the impact of both the fish farm and
the town of Skala Polychnitos. The density of foraminiferal assemblages shows a decrease with
increasing distance to the sea, mainly in the central part of the gulf. The species diversity is higher
along the southeastern shore of the lagoon indicating the penetration of marine water along the shore
during most of the year (after Debenay et al., 2005)
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 55

4.6. Choked Hyposaline Lagoon

Example: Lake Nokoué, Bénin, latitude ≈ 6°26‘ N, longitude ≈ 2°27‘ E (Debenay et al.,
1993; Figures. 3 and 8)

Morphology
This coastal lagoon extends over about 160 km2 (20 km long from west to east). It is
closed by a sand spit, which is about 5 km wide, and is directly connected to the sea via a
narrow channel through Cotonou. Another connection to the sea exists to the east of the
lagoon, through a channel and the lagoons of Nigeria. The Cotonou channel can close during
low-water periods. The south coast is sandy while the north coast, where the main tributaries
flow into the lagoon, is marshy. The lagoon is shallow (<3 m) except near the entrance
channel (9 m).

Hydrodynamics
The main water circulation pattern is a general clockwise, wind driven current around the
lagoon, with several smaller circulation cells (Colleuil, 1984; Millet et al., 1991). Tidal
currents are sensitive only during low water periods, and are mainly located near the entrance
channel. Freshwater inputs are generally produced by rain and runoffs during the great rainy
season (March - July) and by the main tributary, the Oueme River, during the small rainy
season (September – November). When the Oueme River is in spate (September –
December), almost the entire lagoon is filled with fresh water, with a salinity of about 0.2‰.
At the beginning of the low water period, oceanic waters penetrate the lagoon through the
Cotonou channel and are pushed westwards by the clockwise current, inducing a west-east
zonation. Maximum salinity can then reach 33‰. Later, the entrance channel closes naturally,
due to long-shore sediment input, and the salinity lowers, with a gradient from 10‰ (west) to
5‰ (east). No vertical water stratification was observed.

Sediments
The sediments are of terrigenous origin, and are typically organic rich muds, with some
sand banks deposited by the wind driven currents.

Foraminiferal Assemblages
The foraminiferal assemblages collected in Lake Nokoué are poor and dominated by the
euryhaline A. salsum. However, near the Cotonou channel, and under oceanic influence, they
are more diversified, with A. parkinsoniana, A. tepida and E. gunteri present. The samples
collected from the organic-rich-sediment in the estuaries of the tributaries contain A.
mexicana and H. wilberti, while the brackish eastern area contains M. earlandi and M. fusca.
The distribution of the confinement index, the Ic, fit well with the hydrological
characteristics of the area (Figure 8). Values lower than 0.4 are limited to the vicinity of the
Cotonou channel, highlighting the weakness of the marine influence. Both the westwards
extension of the area, where the Ic is less than 0.7, and its north-eastern extension are the
result of the combined effects of: i) freshwater input from the Ouémé River; and ii) the
clockwise rotation of the water masses. The south-eastern extension of this area is probably
due to the influence of the eastern channel.
56 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

Figure 8. Lake Nokoué. The distribution of the confinement index Ic is related to the input of marine
water through the entrance channel and to the circulation of these waters pushed by wind-forced
currents assemblages (after Debenay et al., 1993)

4.7. Generalization

Living at the bottom of areas of water, benthic foraminifera are subjected to all kinds of
changes in the characteristics of water masses, ranging from the scale of the tidal to seasonal
cycles. They therefore represent the average conditions prevailing at the site of sampling,
which is of primary interest in these highly changing environments. The selected examples of
coastal clastic lagoons reveal that the main distribution pattern of foraminiferal assemblages
is primarily related to the balance between marine and continental influence, thus reflecting
the various water masses. The sensitivity of foraminifera is such that they can indicate the
influence of salt wedges, such as in the Cananéia-Iguape Lagoon. The impact of marine water
has often been emphasized in the literature, and a good example is the Santo André coastal
lagoon, where Cearreta et al. (2002) reported that the absolute abundance of foraminiferal
assemblages greatly increases when the inlet periodically opens. Salinity certainly plays a
prominent role in the impact of the balance between marine and continental water masses, as
is attested to by the presence of foraminifera in inland saline lakes. The selected examples
also reveal that the gradient of marine influence is not necessarily a direct function of the
distance to the inlet, and that this primary distributional pattern may be complicated by
secondary parameters, such as water stratification. Consequently, a simple horizontal
mapping of foraminiferal assemblages has no significance in a stratified lagoon, such as the
Lagoa da Conceiçao, and could lead to misinterpretations.
In areas of almost stable salinity, the assemblages are controlled by secondary
parameters, which are no longer obscured by the marine/continental balance. In the Araruama
Lagoon, for example, local conditions, such as anthropogenic inputs, clearly affect the
foraminiferal assemblages. Albani (1978) reported the same phenomenon in estuarine
environments, where assemblages reflected the marine and fluvial water masses in areas of
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 57

variable conditions, while in areas of more stable salinity the major parameters became water
depth and tidal activity.
In the study examples, no clear relationship could be established between foraminiferal
assemblages and the nature of the sediment. However, such a link could be evidenced in Lake
lllawarra, Australia (Yassini and Jones, 1989), and in the Bassin d'Arcachon, a restricted
lagoon on the Atlantic coast of France, where Le Campion (1970) recognized a number of
sub-environments with different foraminiferal assemblages related to the nature of the
sediment. Generally, muddier sediments, usually accompanied by higher nutrient conditions,
tend to contain a greater density of foraminifera than sandier sediments, as seen in the
Gippsland Lakes, Australia (Apthorpe, 1980) and the Goro Lagoon, Italy (Coccioni, 2000).
The agglutinated species collected in the selected lagoons are always related to low
salinity and are always associated with low pH conditions. However, when considering these
species and their significance for environmental conditions, it is necessary to make the
distinction between organic-cemented species, which mainly live in low salinity and low pH
conditions, and calcite-cemented species, which are abundant in fully marine reefal
environments and coral reef lagoons. The species that lives in the less saline areas is M. fusca,
and is always found near fluvial input sites. This species is often reported to be present in the
same type of environments and also seems to prefer the quieter conditions prevailing in
shallow, subtidal sheltered waters (Lewis, 2006).
The great variety of lagoonal functioning illustrated by the selected examples reveals that
it is impossible to establish a universal model for foraminiferal distribution in lagoons.
However, these assemblages may be used as a key indicator in lagoonal environments, either
for understanding the functioning of the lagoon, as was the case in Lagoa da Conceiçao
(Debenay et al., 1998), or for exploring the favourable, average conditions for man‘s activity,
such as aquaculture. For example, it was demonstrated in the Nokoue Lagoon that the
distribution of the confinement index, the Ic, fits well with macrobenthic zonation (Debenay
et al., 1993). The Ic index is also a powerful tool for comparing various lagoonal
environments and other paralic habitats, typically estuaries. Moreover, the Ic also gives a
helpful indication of organic matter input and serves as a useful tool for a quick
characterization of the environment, including the detection of any anthropogenic impact.

5. USING FORAMINIFERA FOR ASSESSING WATER

AND SEDIMENT QUALITY IN LAGOONS

5.1. Use of Foraminifera

Coastal areas have traditionally been places of human settlement, with the accompanying
development of cities, industries and other human-related activities possibly having an impact
on aquatic ecosystems and modifying their health quality and local biota. Although human-
induced disturbances may take many forms, the most deleterious impact typically occurs in
paralic environments, where the effects generally overlap with the stress conditions which
tend to be induced by drastic changes in water characteristics. At present, there is clearly an
increasing need to monitor the ecosystem response to different types of disturbance. Despite
the complex interplay of natural vs. anthropogenic induced stress, biological organisms like
58 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

foraminifera can be used to provide an early warning of the presence or absence of pollution
(biological monitoring). Like the biotic indices that have already been developed for
macrofaunal organisms, foraminiferal monitoring procedures are also beginning to be
formalized, and considerable effort has been made to develop new methodologies for the
biological monitoring of different contaminants. Moreover, because of our increased
knowledge of the biology of foraminifera, it is clear that benthic foraminifera have great
potential as indicators of stress, thereby providing one of the most sensitive and inexpensive
markers of environmental strain in both naturally and anthropogenically stressed locations
(Murray and Alve, 2002).
Benthic foraminifera generally respond to adverse ecological conditions, mainly by
undergoing: i) local extinctions; ii) compositional biocenosis changes; iii) assemblage
modifications, which include changes in abundance and diversity; iv) dwarfism (Lilliput
effect); v) prolocular morphology; vi) reproduction capability; and vii) the development of
test abnormalities (e.g. Alve 1991, 1995; Yanko et al., 1994; Geslin, 1999; Frontalini et al.,
2009).
Over the last few years, many studies of benthic foraminiferal assemblages have been
carried out in different parts of the world in areas exposed to different kinds of marine
pollution, which has generally included a) increased organic matter, b) hydrocarbons-oil and
c) trace elements.

5.2. The Effect of Organic Matter on Benthic Foraminifera

The input of organic matter has deleterious effects on marine ecosystems and their
benthic community by inducing high nutrient levels which can ultimately lead to oxygen
deficiency. The influence of organic material on the benthic community is not only controlled
by its quantity, but also by its quality. Although organic matter is composed of a wide range
of compounds, it can be divided into two main groups. The first includes the material that is
more easily biodegradable and ―naturally‖ produced. This encompasses organic compounds
from agriculture (e.g. fertilizers) and aquaculture, as well as domestic sewage, which is
readily metabolized by marine organisms. In contrast, the effluents of pulp/paper mills, which
are composed primarily of cellulose, lignin and other wood fibers, are rather resistant and
difficult to metabolize.
According to Alve (1995), the increase in organic matter from both sources in the so-
called defined ―hyper-trophic‖ zone may stimulate the growth of large populations of benthic
foraminifera. However, an excess of organic material may negatively influence the benthic
community. In fact, most studies have revealed that around areas of organic matter supply
(e.g. outfall and pipe), an abiotic zone might occur in response to the development of anoxic
conditions. Changes in density are not the only response by benthic foraminifera to organic
matter, with a lowering in species diversification also being documented in the vicinity of
many outfalls (e.g. Resig, 1960; Schafer, 1973).
Although the Index of confinement (Ic) is used to define a marine-to-confined water
gradient, it can be also utilized to unravel the influence of freshwater discharges and detect
anthropogenic impact (Debenay et al., 1998, 2005). This is the case in the Cananéia-Iguape
Lagoon, which exhibits salinity gradients due to the mixing of freshwater input from local
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 59

rivers with marine waters, and where anomalous values of the Ic and the dominance of
Miliammina spp., in correspondence with freshwater input, have been documented by
Debenay et al. (1998). Although the environmental quality of the Gulf of Kalloni has been
reported as good, higher organic matter contents have been noted in the vicinity of a fish farm
and in correspondence to the town of Skala Polychnitos (Figure 7). This is due to local
pollution sources, which include urban effluents and agricultural land runoffs (Panayotidis et
al., 1999). The enhanced organic matter input appears to be responsible for a lowering in
density and species diversity as well as a higher Ic index and abundances of A. tepida and
Haynesina sp. (Debenay et al., 2005). In the hypersaline Lagoon of Araruama, the strong
contrast of foraminiferal assemblage distributions between the north-eastern part of the
lagoon, which is dominated by A. tepida, and the southern part, where T. oblonga dominates
(Figure 6), has been related to organic-rich wastewater input along the north-eastern coast of
the lagoon (Debenay et al., 2001). Ammonia tepida has usually been found in shallow marine
environments, lagoons and deltaic zones (Jorissen, 1988; Almogi-Labin et al., 1992;
Coccioni, 2000; Abu-Zied et al., 2007; Frontalini et al., 2009), and is known for its great
tolerance to chemical and thermal pollution, fertilizing products, and hydrocarbons (e.g.
Yanko and Flexer, 1991; Coccioni, 2000). It was even capable of supporting very polluted
environments and high concentrations of trace elements (e.g. Ferraro et al., 2006). Yanko et
al. (1994) found that megalospheric forms of A. tepida were dominant at stations where toxic
trace metal pollution was prevalent. Similarly, H. germanica has been regarded by Stubbles
(1993) and Armynot du Châtelet et al. (2004) as a species that is tolerant to pollution, and its
increasing dominance is an indicator of stressed environmental conditions.
Enrichments of organic matters have also been considered to be responsible for
increasing the proportions of abnormal tests (FAI). In particular, in shrimp ponds in New
Caledonia, Debenay et al. (2009a) documented a strongly positive correlation between the
FAI and (1) the quantity of easily oxidized material (EOM) deposited at the bottom of the
ponds, and (2) the sediment oxygen demand. This is corroborated by the poorly diversified
assemblages that are mainly dominated by A. tepida and Q. seminula, indicating very
restricted conditions and major environmental stress. It has also been suggested that a very
high FAI could be a potential indicator of great accumulations of native organic matter,
leading to a high sediment oxygen demand.
In their multi-proxy study on intertidal estuaries in New Zealand, Hayward et al. (2004,
2006) found that stepwise shifts in dominance from calcareous to agglutinated forms, which
are usually related to increasing continental influence, were also associated with the arrival
and establishment in the area of humans. These major faunal changes probably resulted from
the increased freshwater runoffs associated with forest clearance and an increase of nutrient
inputs. Clear foraminiferal faunal zones have been documented by Takata et al. (2006) in the
organic-rich brackish-water Lagoon of Saroma (Japan). This faunal distribution appears to be
controlled by the dissolved oxygen content of the bottom water and a combination of organic
enrichment and mud content in the substrate in front of river mouths. In particular, these
authors reported a river-mouth fauna dominated by Elphidium excavatum, which is probably
adapted to organic-rich sediment. Previous studies have reported the presence of E.
excavatum in highly organic substrates; Schafer (1973) noted that the Elphidium
incertum/Elphidium clavatum Group (probably related to E. excavatum) was particularly
abundant around sewage outfalls in Chaleur Bay, Canada, while Alve and Murray (1999)
inferred that E. excavatum can live in substrates characterized by highly variable grain size
60 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

and TOC content. Major changes in foraminiferal assemblages over both time and space have
also been reported in the Osaka Bay (which can be regarded as a restricted lagoon) by
Tsujimoto et al. (2006a, b). Using living foraminiferal assemblages, these researchers
documented an inner area of the bay which was mainly related to eutrophication and
dominated by agglutinated forms (Trochammina hadai and Eggerella advena). Moreover,
they also highlighted marked foraminiferal assemblages present over the past 50 years, where
the dominance of agglutinants, which was linked to the increase of eutrophication from the
1960s to the 1970s, was followed by a decrease of these forms in response to the imposition
of improved environmental regulations. A similar approach has been used in the northern
sector of the Lagoon of Venice by Albani et al. (2007), who compared foraminiferal
assemblages from samples collected in 1983 and 2001, thus documenting unchanged
conditions for 50% of the lagoon. On the basis of these results, these authors have been able
to document both the effectiveness of the purification plant, which has been operating since
1980s, and improvements in the water quality in the area near Porto Marghera.

5.3. The Effect of Hydrocarbon-Oil on Benthic Foraminifera

The effect of hydrocarbons on benthic foraminiferal assemblages in field and

experimental studies has been the subject of only a few papers (e.g. Vénec-Peyre, 1981;
Yanko et al., 1994; Alve, 1995; Bernhard et al., 2001; Morvan et al., 2004; Ernst et al., 2006;
Sabean et al., 2009). Increased mortality and abnormality and decreased density and diversity
are among the effects on benthic foraminiferal assemblages induced by hydrocarbon
pollution. In particular, and in order to address the response of benthic foraminifera to
pollution as a result of the ―Erika‖ oil spill, Morvan et al. (2004) evaluated a site situated on
the tidal mudflat along the southern Bay of Bourgneuf (France) at monthly/bimonthly
intervals. Although a clear link between FAI and oil pollution was not found, impoverished
fauna in terms of density and species richness was highlighted, confirming the potential
sensitivity of foraminifera to this pollutant, and suggesting a direct impact either by the oil
spill itself or by the strong disturbance of the environment resulting from cleaning activities.

5.4. The Effect of Trace Elements on Benthic Foraminifera

Although most trace elements are biologically essential at very low concentrations, they
become potentially toxic to marine and estuarine organisms above a specific threshold
(Kennish, 1992). Over the last four decades, many studies from different environmental
settings have focused on the response of benthic foraminifera to pollution by trace elements
(Alve, 1991, 1995; Sharifi et al., 1991; Yanko et al., 1994 1998, 1999; Coccioni, 2000; Geslin
et al., 2000, 2002; Samir, 2000; Samir and El-Din, 2001; Elberling et al., 2003; Armynot du
Châtelet et al., 2004; Coccioni et al., 2003, 2005, 2009; Coccioni and Marsili, 2005; Ferraro
et al., 2006; Frontalini and Coccioni, 2008; Frontalini et al., 2009, 2010). Most of these
studies documented a lowering in species diversity and density, and a high incidence of
abnormality, megalospheric and dwarfed forms, and changes in assemblage composition.
 Benthic Foraminifera in Coastal Lagoons: Distributional Patterns and… 61

The benthic foraminiferal response to trace element pollution was investigated by Samir
(2000) in two Egyptian Nile Delta lagoons (Manzalah and Edku). The high level of pollution
reported in the Manzalah was believed to be lethal to foraminifera and, indeed, only one
species of Ostracoda (Cyprideis torosa) was found to be able to survive in this environment.
On the other hand, the Edku Lagoon, which had trace element concentrations close to the
natural baseline level, yielded living foraminifera. On the basis of total assemblages, the
Manzalah Lagoon exhibited lower foraminiferal diversification and higher percentages of
both megalospheric forms of A. tepida and abnormality.
A similar response, in terms of very impoverished foraminiferal assemblages, has been
documented in different Italian lagoons (e.g. Santa Gilla, Venice, Orbetello and Lesina) by
Frontalini et al. (2009, 2010) and Coccioni et al. (2009). In particular, reduced foraminiferal
diversification and high percentages of abnormal forms have been reported close to the most
polluted industrial zone of Porto Marghera (Coccioni et al., 2009). The same authors reported
a biocenosis (living assemblages) dominated by A. tepida, H. germanica and E. oceanensis.
These assemblages are comparable to the Ammonia associations with H. germanica that are
characteristic of lagoons along the Mediterranean coast (see Murray, 1991, 2006).
High concentrations of trace elements (e.g. Hg values up to 10 times higher than the
background level) were found in the Santa Gilla lagoon, the innermost part of which is
comprised of the industrial complex at Macchiareddu. Indeed, the trace element concentration
values were generally higher than the USEPA ER–L and ER-M levels (Frontalini et al.,
2009). The same authors documented an oligotipic assemblage and the occurrence of
abnormalities, particularly in the innermost part of the lagoon, testifying to an important
chemical stress in this area. In contrast, higher diversity values and lower percentages of
abnormalities were recognized in the outermost part, which is probably favoured by faster
water renewal and the reduced influence of urban discharge. This reflects a limited influence
of trace element concentrations in the sediment.
On the basis of trace element analysis of the biogenic carbonate of porcelanaceous
foraminifera, Frontalini et al. (2009) also found higher concentrations than those reported in
unpolluted environments. The same results were achieved by Madkour and Youssef Ali
(2008), who found high concentrations of Fe and Mn in benthic foraminiferal tests from
several Egyptian Red Sea lagoons (e.g. Umm al-Huwayat).

7. CONCLUSION
Lagoons, like other transitional marine environments, are areas where biological,
chemical, and physical processes overlap over both time and space. Our understanding of
them might be improved by knowledge of the behaviour of the organisms evolving and living
in these complex systems. Benthic foraminifera are highly suitable and sensitive biological
organisms through which our comprehension of lagoon environments can be further explored.
Since the early 1900s, plenty of studies have documented the ability of benthic foraminifera
to synthetically reflect a great variety of complex processes. Despite of the general conditions
are complicated by a complex interplay of an array of parameters in lagoon environments,
this work highlights that foraminiferal assemblages are distributed along major gradients (i.e.,
salinity). Benthic foraminifera have been also proven to be particularly sensitive
62 F. Frontalini, E. Armynot du Châtelet, J.P. Debenay et al.

microrganisms and they have been successfully utilized for their value as bio-indicators of
environmental change in a wide range of marine environments including lagoon ecosystems.
In this context, the ―Confinement Index‖ gives a helpful indication of organic matter input
and serves as a useful tool for a quick characterization of the environment, including the
detection of any anthropogenic impact. Although the separation of natural and
anthropogenically-induced stress is sometimes hampered by environmental complexity,
benthic foraminifera are ideal and reliable candidate for environmental monitoring program
and management of lagoonal ecosystems.

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 73-117 © 2011 Nova Science Publishers, Inc.

Chapter 3

COASTWEB, A FOODWEB MODEL BASED ON

FUNCTIONAL GROUPS FOR COASTAL AREAS
INCLUDING A MASS-BALANCE MODEL FOR
PHOSPHORUS

Lars Håkanson* and Dan Lindgren

Department of Earth Sciences, Uppsala University, Uppsala, Sweden

ABSTRACT
It is important to develop tools to get realistic predictions of how, e.g., the loading of
contaminants and future climate changes may affect the structure and function of aquatic
ecosystems. The CoastWeb-model presented in this work in meant as such a tool.
CoastWeb is a process-based mechanistic foodweb model for coastal areas (the
ecosystem scale) and includes a mass-balance model (CoastMab) for phosphorus. The
model is based on ordinary differential equations and gives monthly calculations of
production and biomasses for ten functional groups (phytoplankton, benthic algae,
macrophytes, bacterioplankton, herbivorous and predatory zooplankton, zoobenthos,
jellyfish, prey and predatory fish). CoastMab calculates in- and outflow, sedimentation,
diffusion, resuspension, up- and downward mixing, biouptake and retention of
phosphorus in biota. There are algorithms for, e.g., migration of fish and plankton
between the given coastal area and the sea and the influence of exposure on macrophyte
cover . The paper presents case-studies on eutrophication, overfishing and toxic
contamination illustrating the potential of CoastWeb as a tool for sustainable coastal
management. Increased nutrient loading will cause several changes to the foodweb
characteristics of the studied coastal area. Some of these could be expected without a
model, but here they have been quantified using a general foodweb model. The model
accounts for different compensatory effects that are difficult to quantify without a model.
The case-study on overfishing indicates that increased fishing will likely affect the
studied coastal system marginally because the migration of fish from the sea is large in
the studied coastal area. The case-study on toxic contamination shows that a reduction of

*
Corresponding author: Email: Lars.Hakanson@geo.uu.se., tel: +46 184713897; fax: +46 184712737.
74 Lars Håkanson and Dan Lindgren

zoobenthos biomass will have clear effects of fish production and biomass in the studied
coastal area.

Keywords: coastal areas, eutrophication, foodweb modelling, functional groups, mass-

balance modelling, overfishing, phosphorus, toxic contamination, climate change

INTRODUCTION
At any modelling scale, the complexity of natural ecosystems always exceeds the
complexity and size of any model, so simplifications are always needed. The ultimate goal in
achieving predictive power and general validity for a model is to find the most appropriate
simplifications (Monte, 1995, 1996; Monte et al., 1999; Peters, 1991). Different models for
biota focus on different targets and scales. Fundamentally different approaches may be used
in, e.g., physiological models, models for individual species and models for functional
groups, approaches using different time scales (hours to years), different spatial scales (from
sites to ecosystems), different driving variables (climatological data or map parameters) and
approaches using statistical methods or models based on ordinary differential equations (box
models) or partial differential equations (2- or 3-dimensional models), see Monte (1996),
Mace (2001).
The CoastWeb-model presented in this work is meant as a tool for coastal sciences and
management to study how changes in nutrient inflow, fishing, water temperature and
contamination by toxins could influence the structure and function of coastal ecosystems.
CoastWeb is basically a combination of a foodweb model for lakes (LakeWeb, Håkanson and
Boulion, 2002), a process-based dynamic mass-balance model for phosphorus (CoastMab,
Håkanson and Eklund, 2007) and several adjustments needed to bring these two models
together into a comprehensive unit. An important feature of this model, and a pre-requisite for
its practical use, is that it can be run by a few driving variables readily accessible from
standard maps and monitoring programs.
CoastWeb is based on ordinary differential equations, works at the ecosystem scale and
gives monthly predictions, but it does not address the finer details related to individual
species or changes among sites within coastal systems. LakeWeb, has been positively tested
against comprehensive empirical data for lakes and by sensitivity and uncertainty analyses
(Håkanson and Boulion, 2002). LakeWeb was used for the Baltic Sea as a tool to set fish
quotas (Håkanson and Gyllenhammar, 2005) by calculating the fish production potential and
how it depends on environmental conditions (salinity, temperature and phosphorus loading)
as well as on fishing and overfishing. Håkanson and Gyllenhammar (2005) compared
LakeWeb with other models, e.g., Ecopath/Ecosim (Christensen et al., 2000; Walters et al.,
1997, 2000; Sandberg et al., 2000; Harvey et al., 2003) and that comparison will not be
repeated here. However, it should be stressed that CoastWeb provides a new dimension to
understand and simulate the factors regulating aquatic ecosystem structure, including the fish
production. Ecopath/Ecosim and CoastWeb/LakeWeb are complementary and both can
calculate production and biomasses, but CoastWeb/LakeWeb has a separate sub-model to
calculate inflow, outflow and internal processes (sedimentation, resuspension, etc.) of
nutrients so that the nutrient concentration can be related to the nutrient loading and used to
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 75

calculate chlorophyll (phytoplankton biomass). Ecopath/Ecosim is designed to handle more

detailed foodweb interactions than CoastWeb/LakeWeb.
Most of the algorithms used in the mass-balance model for phosphorus (CoastMab) have
been critically tested and shown to predict well, but only for coastal areas within a fairly
limited salinity range. It would be very interesting to test CoastWeb/CoastMab for more
saline systems, e.g., in the Mediterranean, along the Atlantic coast or in the Black Sea. The
case-studies presented here merely illustrate the potential use of this modelling related to
eutrophication, toxic contamination and overfishing – each case-study could easily grow into
a large book. So, this paper is ―not the end, nor the beginning of the end, but rather the end of
the beginning‖.

Figure 1. Illustration of the steps to define the boundary lines of a coastal area (step 1) at the
topographical bottlenecks defined by the ratio between the section area (At) and the enclosed coastal
area (A) where the exposure (Ex) attains a minimum value. Once the boundary lines for the coastal area
are defined, steps 2 and 3 illustrate how to calculate important coastal parameters (such as
morphometric size, form and special parameters, the theoretical surface and deep water retention times
and where areas of fine sediment accumulation prevails)
76 Lars Håkanson and Dan Lindgren

The text has been divided into the following parts:

First, the basic structure of the foodweb model is described, including the approach to
define the geographical boundary conditions for coastal areas, the approach to define
―normal‖ biomasses for the functional groups, migration into and out from coastal
areas and an outline of the new sub-model for jellyfish.
Then, there is a section related to the different roles of macrophytes in coastal systems
and how these roles and functions can be modelled using CoastWeb.
The third main part gives results related to the three case-studies and how CoastWeb may
be used as a tool to analyse how very complicated and important environmental
problems may be handled in a structured and quantitative manner.
The appendix gives a list of minor modifications done to transform the lake model into a
model for coastal areas.

METHODS – THE MODELLING APPROACH

Coastal Ecosystem Boundaries

It is easy to define what a lake is or a stretch of river. It is more difficult to draw the
borderlines toward the sea and/or adjacent coast to define a given coastal area. The positions
of such borders are essential for mass-balance calculations since arbitrary borderlines
generate arbitrary volumes, which reduce the predictive power of the mass-balance model
(Håkanson, 1999). CoastWeb requires that the coastal area is defined according to the
topographical bottleneck approach (Figure 1). The boundaries should be drawn at the
topographical bottlenecks using Geographical Information Systems (GIS) techniques so that
the exposure (Ex = 100·At/A) attains a minimum value when different alternatives for
defining the boundary lines are tested (At = section area; A = enclosed coastal area; Pilesjö et
al., 1991). Once the coastal area is defined, other key variables for mass-balance calculations
may also be defined, such as the water volume. This method also makes it possible to use
simple models to estimate the theoretical surface-water retention time (Persson et al., 1994),
the deep-water exchange (Håkanson and Karlsson, 2004) and the bottom dynamic conditions
(Håkanson, 2006) from morphometrical parameters. Such simple models are important since
establishing an empirical value of the theoretical water retention time from field
measurements can be costly. CoastWeb may be used for the main coast types, tidal coasts,
open coasts, archipelago coasts and bays (Håkanson, 2000).

The Foodweb Model

The main aim of the LakeWeb-model is to quantitatively describe characteristic foodweb

interactions so that production, biomasses and predation can be determined for the functional
groups in the model: the three primary producers, phytoplankton, benthic algae and
macrophytes, the five secondary producers, herbivorous zooplankton, predatory zooplankton,
zoobenthos, prey fish and predatory fish, and one decomposer, bacterioplankton. Jellyfish is
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 77

added as a functional group to adapt the model to coastal conditions. The group ―predatory
fish‖ does the work of eating ―prey fish‖, which in turn eats zooplankton (herbivorous and
predatory) and zoobenthos. Other organisms, like benthic bacteria and fungi are not treated
individually but are included in the flux called ―zoobenthos production from other sediment
sources‖. Such simplifications are necessary to keep the model as small as possible, to keep
the driving variables as few and as accessible as possible and to be able to critically test the
model using empirical data. The idea is not to include everything, but to focus on key
functional groups and fundamental abiotic/biotic relationships (see Figure 2 for an overview
of the LakeWeb model). CoastWeb is meant to cover a wide range in temperature, water
basin morphometry, trophic state and salinity. Since the model can be run from few and
readily accessible driving variables (see Table 1), it is evident that the aim is to model general
conditions. This modelling is intended to handle feedbacks among the functional groups, but
biotic/abiotic feedbacks also are included.

Table 1. Data needed to run the CoastWeb-model for the studied coastal areas (data
from Wallin et al., 1992 and Håkanson et al., 2007). The water exchange between
Ringkobing Fjord and the sea is regulated by a sluice

Area Country Lati- Water Catch- Dmax Dm At Chl Sal- Ca- CTP Sec
tude area ment area inity conc. #
(°N) (km2) (km2) (m) (m) (km2) (µg/l) (mg/l) (µg/l) (m)
Ringkobing Denmark 56 300 3 500 5.1 1.9 sluice 52/9,1* 7.8/9.6 30 130/56 0.6/1.6
Ronneby S. Swed. 56 11.0 633 17.6 4.3 0.0176 2.1 6.5 25 21 4
Gräsmarö C. Swed. 58 13.8 0 46.9 14 0.0825 2.6 6.6 15 17 4.3
Haverö Finland 61 2.3 0 22.5 8.6 0.0172 2.1 6.5 15 27 3.4
Gävle N. Swed. 61 17.1 2 600 17.0 8.4 0.0063 3.5 4.2 9 23 3.6
Dmax = maximum depth; Dm = mean depth; At = section area; Chl = concentration of chlorophyll-a; CTP
= TP-concentration; Sec = Secchi depth; *) mean values from all existing data 1990/93 and
2000/2003, respectively; #) estimated values

Predatory fish
Secondary producers

Prey fish
Jellyfish
Predatory zooplankton
Zoobenthos
Herbivorous zooplankton
Sediments Benthic algae Macrophytes

Primary producers Bacterioplankton

Phytoplankton

Decomposer
Figure 2. Illustration of a coastal foodweb including ten groups of organisms (phytoplankton,
bacterioplankton, benthic algae, macrophytes, herbivorous zooplankton, predatory zooplankton,
jellyfish, zoobenthos, prey fish and predatory fish)
78 Lars Håkanson and Dan Lindgren

Figure 3. Illustration of general and fundamental transport processes to, within and from coastal
systems used in the mass-balance model for phosphorus in the CoastWeb-model. ―ET-sediments‖ in the
figure refer to erosion and transportation areas where fine sediments and particulate forms of nutrients
are resuspended. ―Active A-sediments‖ are biologically active sediment areas where fine sediments are
continuously being deposited (accumulation areas)

Mass-balance modelling of nutrients is important in aquatic ecology (Vollenweider,

1968; OECD, 1982) and by including a mass-balance model for nutrients in the foodweb
model, it is possible to calculate the uptake and retention of phosphorus in biota.
Basically, CoastWeb consists of two parts: the foodweb model, which is driven by
chlorophyll and calculates production (kg ww/month) and biomass (kg ww) of the functional
groups, and the mass-balance model for phosphorus (CoastMab; Håkanson and Eklund, 2007)
based on transport processes that appear in most systems (Figure 3) and apply to most
substances (nutrients, suspended particulate matter (= SPM), radionuclides, etc.).
Key concepts in this modelling are (Table 2): (1) Consumption rates - ―how large a
fraction of the prey biomass is consumed per time unit by the predator?‖ (2) Metabolic
efficiency ratios for each compartment - ―how much of the food consumed will increase the
biomass of the consumer?‖ (3) Turnover or retention rates for each compartment - ―how long
is the mean, characteristic lifespan of the group?‖ (4) Food choices - ―if there is a food
choice, how much is consumed of each food type?‖ (5) Migration rates - ―how large a
fraction of the group will leave and enter the system per unit of time?‖ These concepts will be
described briefly below for jellyfish. Håkanson and Boulion (2002) give more information on
the different concepts.
This modelling uses a simple general system to assign weights to food choices and adjust
the consumption to the number of food choices. Figure 4 gives an overview of the food
choice panel. If there are more than two food choices, they are first differentiated by a
distribution coefficient (DC1) that separates between the primary and the other food types. A
second distribution coefficient (DC2) separates the second most popular food type from the
rest, etc.
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 79

Table 2. Metabolic efficiency ratios for key functional groups (MER = PR/CON,
dimensionless). The MER-value is calculated from the mass-balance equation, CON =
PR + RES + FAE, where CON = consumption, PR = production, RES = respiration, FAE
= unassimilated food (faeces), all dimensionless, and T = turnover time (= BM/PR, days;
BM = biomass). The actual consumption rate constant, CR, expresses reduction of prey
organism biomass per unit of time. The jellyfish values on PR, RES and FAE are from
Schneider (1989) while the corresponding values for the other functional groups mainly
are from Winberg (1985) and Håkanson and Boulion (2002)

CON PR RES FAE MER T CR Consumes Consumed by

Zooherb 100 24 36 40 0.24 6.0 0.17 Phytopl., Prey fish,
Bacteriopl.Zoo Jellyfish
pred,
Zoopred 100 32 48 20 0.32 11.0 0.091 Zooherb Prey fish,
Jellyfish
Zoobenthos 100 15 35 50 0.15 65 0.015 Macrophytes, Prey fish
Benthic algae
Prey fish 100 16 64 20 0.16 300 0.016 Zoobent., Pred. fish
Zooherb,
Zoopred
Predatory 100 25 55 20 0.25 450 0.0013- Prey fish Pred. fish
fish 0.02
Jellyfish 100 22 56 20 0.22 120 0.008 Zoopred, None
Zooherb

Predatory
fish

DC = 1

Prey fish
DC = DC =
1-0.5·Ysec 0.5·Ysec
Zoo- Zoo- Jelly-
benthos plankton DC = fish
0.5
DC = DC = DC = DC =
0.5 0.5 0.75 0.25 DC =
Benthic Organic Pred. zoo- Herb. zoo- 0.5
plants sediments plankton plankton
DC = DC = DC = DC =
0.75 0.25 0.5 0.5
Benthic Macro- Phyto- Bacterio-
algae phytes plankton plankton

Secchi depth Phosphorus SPM

and
morphometry

Figure 4. Food choice panel for the default set-up used for the CoastWeb-model

Table 3. Gives a compilation of abbreviations used in this modelling.

80 Lars Håkanson and Dan Lindgren

Table 3. Abbreviations and dimensions of the most commonly used concepts and
variables in this modelling. Note that we have tried to use as simple and self-explanatory
abbreviations as possible. Greek letters have been banned

A. Organisms
BA = Benthic algae
BE = Zoobenthos
BP = Bacterioplankton
JE = Jellyfish
MA = Macrophytes
PD = Predatory fish
PH = Phytoplankton
PY = Prey fish
ZH = Zooplankton, herbivours
ZP = Zooplankton, predators
B. Driving variables
Area = Coastal area (m2)
Dm = Mean depth (m)
Dmax = Maximum depth (m)
SWT = Surface-water temperature (°C)
TP = Total phosphorus (μg/l)
C. Foodweb interactions
BM = Biomass (kg ww), e.g., BMBP
CON = Consumption (kg ww/week), e.g., CONPHZH (of PH eaten by ZH)
CR = Actual consumption rate (1/week), e.g., CRZPPY (ZP eaten by PY)
EL = Elimination (kg ww/week), e.g., ELZP
IPR = Initial production (kg ww/week), e.g., IPRZHZP (ZH eaten by ZP)
NBM = Normal biomass (kg ww), e.g., NBMBE
NCR = Normal consumption rate (1/week), e.g., NCRPY
MER = Metabolic efficiency ratio (dim. less), e.g., MERPYPD (PY eaten by PD)
NR = Number of first order food choices (dim. less), e.g., NRZH
PR = Production (kg ww/week), e.g., PRPD (PR defined by the ratio BM/T)
T = Turnover time (weeks), e.g., TPH
D. Mass-balance for phosphorus (= CoastMab)
ASec = Area above Secchi depth (m2)
BL = Biota with long turnover times
BS = Biota with short turnover times
C = Concentration, e.g., of phosphorus CTP (μg/l)
DF = Dissolved fraction of phosphorus (dim. less)
DP = Dissolved phosphorus (μg/l)
DR = Dynamic ratio (dim. less)
ET = Areas of fine sediment erosion and transport (dim. less)
F = Flux of phosphorus (g/week), e.g., FETA (from ET to A)
M = Mass of phosphorus (g), e.g., MET
PF = Particulate fraction of phosphorus (dim. less)
R = Rate (1/week)
SW = Surface water
Vd = Volume development (= form factor, dim. less)
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 81

Table 3. (Continued)
Y = Dimensionless moderator
E. Other abbreviations
Chl = Chlorophyll-a concentration (μg/l)
dw = Dry weight
IG = Sediment organic content (= loss on ignition, % dw)
PrimP = Primary phytoplankton production
Prec = Mean annual precipitation (mm/yr)
SPM = Suspended particulate matter (mg/l)
Sec = Secchi depth (m)
W = Sediment water content (% ww)
ww = Wet weight

Table 4. Many biological variables, whose determination normally require extensive and
expensive field and laboratory work, may be estimated from lake TP (in µg/l = mg/m3).
From Håkanson and Peters (1995) and Håkanson and Boulion (2002). PrimP = primary
production (in g ww / m2 yr), Maccov = Macrophyte cover of lake bed (in % lake area),
SecMV = mean annual Secchi depth (in m), Dm = mean lake depth (in m), Col = lake
colour (mg Pt/l), DC = distribution coefficient (dimensionless), n = number of lakes used
in the regression, ww = wet weight and dw = dry weight

y-value Equation Range for r2 n Units

x
Equations based on phosphorus used as norms in LakeWeb:
Chlorophyll =0.28·TP0.96 2.5-100 0.77 77 mg ww/m3
(summer mean)
Chlorophyll =0.64·TP1.05 2.5-100 0.81 50 mg ww/m3
(summer max.)
Max. prim. prod. =20·TP-71 7-200 0.95 38 mg C/m3·d
(TP>10)
Max. prim. prod. =0.85·TP1.4 mg C/m3·d
(TP<10)
Mean prim. prod. =10·TP-79 7-200 0.94 38 m C/m3·d
(TP>10)
Mean prim. prod. =0.85·TP1.4 mg C/m3·d
(TP<10)
Phytoplankton =30·TP1.4 3-80 0.88 27 mg ww/m3
Bacterioplankton =0.90·TP0.66 3-100 0.83 12 mill./ml
Zooplankton, =0.77·38·TP0.64 3-80 0.86 12 mg ww/m3
herbivores
Zooplankton, =0.23·38·TP0.64(the distr. coeff. is mg ww/m3
predators 0.77)
Zoobenthos =810·TP0.71 3-100 0.48 38 mg ww/m2
Fish =590·TP0.71 10-550 0.75 18 mg ww/m2
Fish yield =7.1·TP 8-550 0.87 21 mg
ww/m2·yr
Other equations used as norms in LakeWeb:
Bacterioplankton =10(0.973·(0.27·log(Chl)+0.19)-0.438) mg ww/m3
82 Lars Håkanson and Dan Lindgren

Table 4. (Continued)
y-value Equation Range for r2 n Units
x
Fish yield =0.0023·PrimP0.9 170-14 000 0.64 66 mg
ww/m2·yr
Prey fish =DC·fish biomass (default DC=0.73) mg ww/m2
Predatory fish =(1-DC)·fish biomass mg ww/m2
Macrophyte = 0.50·( SecMV/Dm) 229%
cover
Macrophytes =1.37·log(Maccov)+3.58 g ww/m2·yr
0.86
Zooplankton, =0.15·(PrimP·1000) 13-15 000 0.61 42 g ww/m2·yr
herbivores
Zooplankton, =0.076·(PrimP·1000)0.84 2-3 000 0.43 42 g ww/m2·yr
predators
Examples of local, regional and general relationships that may be used in the CoastWeb-model to
predict chlorophyll-a concentrations from TP
Local (for Chl =
Ringkobing SMTH(((SWT+0.1)/9),12,60)·10^(-
Fjord): 1.86+1.72·log(CTP))
Regional (Baltic Chl = ((SWT+0.1)/20)·10^(-
coastal areas): 1.59+1.56·log(CTP))
General: Chl =
(1/YCa)·YDRchl·Ytemp·Ysal·(0.28·CTP·0.56
/PF)0.96

Predictions of Normal Biomasses

In LakeWeb and CoastWeb ―normal‖ (= norms = characteristic) biomasses of all

functional groups are needed for calculations of consumption and migration. All normal
biomasses and production values for the functional groups should ideally be calculated from
empirical regressions yielding a high coefficient of determination (r2). Such general
regressions are not, to the best of our knowledge, available for coastal areas, but many such
empirical regressions are available for lakes (see Table 4). This is a major problem, not just to
obtain good predictive power using CoastWeb, but also more generally in coastal ecology, to
know what the ―normal‖ conditions are, given a set of standard abiotic regulating variables,
such as TP-concentration for lakes. For coastal areas, the salinity is important for the Secchi
depth (see Håkanson, 2006) and also for the relationship between chlorophyll and nutrient
concentrations (Figure 5). Since there are no empirical relationships available for coastal
areas that predict normal biomasses (norms), and since normal biomasses are essential in this
modelling, the approach here is to modify and adjust the normal biomasses used in the
LakeWeb-model and given in Table 4.
Salinity influences the relationship between Chl and TP – the higher the salinity the lower
chlorophyll relative to TP (Figure 5). If the primary production becomes lower at higher
salinities, so will the secondary production. Hence, the first step in the approach to estimate
coastal norms is to calculate a correction factor (Ychl) that describes the difference between
chlorophyll in lakes (Chllake) and in coastal areas (Chlcoast) at the same TP, eq. 1.
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 83

50
1. Lakes, mean summer values; salinity = 0
45 2. Brackish coastal areas, salinities 2- 20; mean salinity - 11
3. Marine coastal areas, mean salinity - 23.5
4. Marine sites, mean salinity - 36
40

Chlorophyll-a concentration (µg/l)

Chl=(1/YCa)·YDRchl·Ytemp·Ysal·(0.28·TP·0.56/PF)^0.96
35
If Ca-conc. < 10 mg/l then YCa =1 else YCa = (1+0.23·(Ca/10-1))
If DR > 2.45 then YDRchl=1 else YDRchl=DR/2.45
30 Ytemp = ((SWT+0.1)/20); SWT = surface-water temperature; °C
Ysal = (1-0.75·Sal/36); Sal = salinity
25
PF = the particulate fraction of P (calculated in the CoastWeb-model) 1

20
2
15
3
10

5 4

0
0 10 20 30 40 50 60 70 80 90 100
TP-concentration (µg/l)

Figure 5. The relationship between median total phosphorus concentrations (TP) in surface water and
median concentrations of chlorophyll-a from the summer period (months 6, 7 and 8) for lakes, brackish
water systems, marine coastal areas and open marine sites covering a salinity range from 0 to 36. DR is
the dynamic ratio = √Area/Dm (Area = coastal area in km2; Dm = mean depth in m) (modified from
Håkanson et al., 2005)

Ychl = Chlcoast/Chllake (1)

Chlcoast may be calculated from a regression between TP and Chl as explained in Figure
5; Chllake is derived from Table 4. Hence, Ychl is 1 for lakes and less than 1 for coastal areas
that have lower Chl-values than lakes at the same TP. To get the norms for the different
functional groups, the corresponding norms in LakeWeb (Table 4) are multiplied with this
correction factor.
The normal biomasses for herbivorous zooplankton (NBMZH), predatory zooplankton
(NBMZP), prey fish (NBMPY) and predatory fish (NBMPD) are calculated as:

NBMZH = Ychl·(DCZHZP)·10-6·Vol·38·CTP0.64 (2)

DCZHZP is set to 0.77 as a default value (Håkanson and Boulion, 2002); Vol is the coastal
volume (m3).

NBMZP = Ychl·(1-DCZHZP)·10-6·Vol·38·CTP0.64 (3)

The normal biomass for fish (prey plus predatory fish) is given by:
84 Lars Håkanson and Dan Lindgren

NBMfish = Ychl·10-6·(Area·590·CTP0.71) (4)

NBMPY = (DCPYPD)·SMTH(NBMfish,TPY,NBMfish) (5)

NBMPD = (1-DCPYPD)·SMTH(NBMfish,TPD,NBMfish) (6)

TPY and TPD are the turnover times for prey and predatory fish. The smoothing function
(SMTH; see Håkanson, 1999, for more information on smoothing function) is used to adjust
the temporal variability in TP to the turnover time of prey fish.
The distribution coefficient regulating the fraction of prey fish is given by eq. 7. The
more eutrophic the system, the higher the fraction of prey fish. This means that in relatively
low-productive systems with TP = CTP = 15 µg/l, DCPYPD = (15/(15+22))0.4 = 0.70; and 70%
of the fish biomass would be prey fish.

DCPYPD = (CTP/(CTP +22))0.4 (7)

In LakeWeb, the normal biomass of zoobenthos (NBMZB) is calculated from Table 4 as

810·(CTP0.71). In CoastWeb, this has been modified to take into account that the biomass of
zoobenthos primarily should depend on the sedimentation of organic matter and the bottom
area above the Secchi depth, which regulate the production of benthic algae and macrophytes.
The approach to predict NBMZB in CoastWeb is:

If CTP < 100 µg/l then NBMZB = YChlZB·10-6·Area·810·(CTP0.71) else

NBMZB = YChlZB·10-6·Area·810·(CTP0.71)·(1-0.5·(CTP/100-1)) (8)

Area is the coastal area (m2), CTP is the modelled TP-concentration. The normal biomass
of phytoplankton is given by:

NBMPH = Ychl·(10-6)·Vsec·(30·CTP1.4) (9)

(30·TP1.4) is the normal biomass of phytoplankton in lakes (Table 4) and Vsec (or VsecSW)
the water volume above the Secchi depth (Sec), calculated from:

Vsec = V-(A-Asec)·Vd·(Dmax-Sec)/3 (10)

Vd is the form factor (Vd = 3·Dm/Dmax) and Asec is the bottom area shallower than the
Secchi depth.
The normal biomass of benthic algae (NBMBA) is calculated from the normal production
of benthic algae (NPRBA) and the turnover time of benthic algae (TBA) by:

NBMBA = NPRBA·TBA (11)

Where

NPRBA = 0.63·(Asec/A)·PRPH·(YsalSW) (12)

 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 85

Asec/A is the part of the bottom area shallower than the Secchi depth; PRPH is the
production of phytoplankton (PRPH = BMPH/TPH). The equation in CoastWeb is the same as in
LakeWeb, except for YsalSW, which is a salinity moderator for how the salinity influences the
water clarity, which in turn influences the production of benthic algae (if SalSW < 1 then
YsalSW = 1 else YsalSW = SalSW/1).
The normal biomass of bacterioplankton (NBMBP) is estimated from a lake regression
based on TP and Chl (Table 4), and modified by a moderator for SPM (YSPMBP) – the higher
the amount of degradable organic suspended matter, the higher the normal biomass of
bacterioplankton.

NBMBP =YSPMBP·0.001·Vol·10(0.973·(0.27·log(Chl)+0.19)-0.438) (13)

YSPMBP is given by:

YSPMBP = SPMSWcoast/SPMSWlake (14)

So, if there is a difference in SPM between a coast and a similar lake, this would
influence the normal biomass of bacterioplankton in the coast. The SPM-concentrations in the
surface water in the coast (SPMSWcoast) and in a corresponding lake (SPMSWlake) are calculated
from the respective TP-concentrations and the regression between TP and SPM (from
Håkanson, 2006).
The same approach is used to estimate normal biomasses of the functional groups in the
sea outside the given coastal area (NBMsea), which are used to calculate immigration. NBMsea
is estimated from:

NBMsea = NBMcoast·Ychlsea (15)

Ychlsea is Chlsea/Chlcoast. For phytoplankton in the sea outside the given coastal area, the
normal biomass is:

NBMPHsea = Ychlsea·(30·CTPsea1.4) (16)

For herbivorous and predatory zooplankton, the normal biomasses in the sea (NBMZHsea
and NBMZPsea) are calculated as Ychlsea·NBMZH and Ychlsea·NBMZP. This is also the case for
the normal biomasses for prey and predatory fish (Ychlsea·NBMPY and Ychlsea·NBMPD). For
bacterioplankton, we have:

NBMBPsea = NBMBP·YSPMsea (17)

YSPMsea is SPMsea/SPMcoast and SPMsea is calculated from (SPMsea = 10(1.56·log(TPsea)-1.64)).

The TP-concentration in the sea outside the given coast (TPsea = CTPsea in µg/l) is an
obligatory driving variable.
Immigration and emigration are not calculated for benthic algae, macrophytes and
zoobenthos since these groups are assumed to be largely stationary. Migration of the other
functional groups is described in the following section. We will be show how these
algorithms work using data from real coastal areas.
86 Lars Håkanson and Dan Lindgren

Table 5. Compilation of equations used to quantify immigration and emigration of

predatory fish, prey fish, jellyfish, predatory zooplankton, herbivorous zooplankton,
phytoplankton and bacterioplankton. There is no in- and emigration for benthic algae
or zoobenthos (or macrophytes) in the model

Ychlsea = Chlsea/Chlcoast
The chlorophyll concentration in the sea and the coast may be given either by empirical data
or by local, regional or global regressions based on TP and SWT (SWT = surface-water
temp, °C)
Predatory fish (PD); immigration:
If BMPD/NBMPD < 1 then FinmigPD = Yseason ·RmigPD·NBMPDsea else FinmigPD = 0.5·Yseason
·RmigPD·NBMPDsea
Migration rate: RmigPD = (1/TSW) [this is the theoretical surface water retention rate]
Dimensionless seasonal moderator for migration: Yseason
If (YseasonA -YseasonB) ≥ 0 then Yseason = ((YseasonA+YseasonB)/2)·(Lat/63) else Yseason =
((YseasonA+YseasonB)/2)·(63/Lat,
where YseasonB = SMTH(YsaeasonA, AV, 0.12)
NBMPDsea = NBMPDlake ·Ychlsea
Ychlsea = Chlsea/Chlcoast
Predatory fish (PD); emigration
If BMPD/NBMPD < 1 then FoutmigPD = 0.5·Yseason ·RmigPD·BMPD else FoutmigPD = Yseason
·RmigPD·BMPD
Prey fish (PY) immigration:
If BMPDY/NBMPY < 1 then FinmigPY = Yseason ·RmigPY·NBMPYsea else FinmigPY = 0.5·Yseason
·RmigPY·NBMPYsea
Migration rate: RmigPY = (0.33·1/TSW)
NBMPYsea = NBMPYlake ·Ychlsea
Prey fish (PY); emigration
If BMPY/NBMPY < 1 then FoutmigPY = 0.5·Yseason ·RmigPY·BMPY else FoutmigPD = Yseason
·RmigPD·BMPD
Jellyfish (JE)
Migration rate: RmigJE = RmigPY
Immigration: FinmigJE = RmigJE·NBMJEsea
NBMJEsea = NBMJE ·Ychlsea
NBMJE (kg ww) is assumed to be 10 times the normal biomass of predatory zooplankton
(NBMZP, see below).
Emigration: FoutmigJE = RmigJE·BMJE
Predatory zooplankton (ZP)
Migration rate: RmigZP = 1/TSW
Immigration: FinmigZP = RmigZP·NBMZPsea
NBMZPsea = NBMZPlake ·Ychlsea
Emigration: FoutmigZP = RmigZP·BMZP
Herbivorous zooplankton (ZH)
Migration rate: RmigZH = RmigZP
Immigration: FinmigZH = RmigZH·NBMZH
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 87

Table 5. (Continued)
NBMZHsea = NBMZHlake ·Ychlsea
Emigration: FoutmigZH = RmigZH·BMZH
Phytoplankton (PH)
Migration rate: RmigPH = 0.5·RmigZP
Immigration: FinmigPH = RmigPH·NBMPHsea
NBMPHsea = NBMPHlake ·Ychlsea
Emigration: FoutmigPH = RmigPH·BMPH
Bacterioplankton (BP)
Migration rate: RmigBP = RmigPH
Immigration: FinmigBP = RmigBP·NBMBPsea
NBMBPsea = NBMBPlake ·Ychlsea
Emigration: FoutmigBP = RmigBP·BMBP

Migration

LakeWeb accounts for immigration and emigration of fish. Coastal areas have a much
more dynamic exchange of water than lakes (a typical theoretical surface-water retention time
for Baltic Sea coastal areas is 4-6 days; and a typical water retention time for a lake is about 1
year; see Håkanson, 2000), which affects the immigration and emigration of fish to and from
the area. Migration of fish is a complicated issue (Levinton, 2001), but it has to be quantified
in CoastWeb where the aim is to obtain realistic predictions of fish biomass. Not only prey
and predatory fish migrate, but also jellyfish, zooplankton, bacterioplankton and
phytoplankton. New algorithms for immigration and emigration are used for all these
functional groups (Table 5). They are based on the following principles:

1. The migration rate (Rmig, per month) in LakeWeb is related to the surface water (SW)
retention rate (Rmig =1/TSW). This is meant to account for the physical possibilities
for the organisms to migrate: if there is no inflow or outflow of water, no organisms
will migrate in and out of the system. This approach is also used in CoastWeb for
plankton that travel with the water rather than in the water, but not for fish and
jellyfish. Plankton is mainly transported by water currents, as given by the SW-
exchange (TSW). The deep-water (DW) exchange is generally smaller than the SW-
exchange and the focus here is on the water exchange for the productive SW-layer.
2. It is assumed that big predatory fish will move more than smaller prey fish (the
default assumption is that the migration rate is a factor of 3 lower for prey fish than
for predatory fish, all else being constant); jellyfish and prey fish are assumed to
have similar migration rates but jellyfish is likely to drift more passively in the water
than prey fish. Vertical movements of jellyfish are achieved through contraction of
the bell (Moen and Svensen, 2004).
3. Fish can migrate in and out of coastal areas for a number of reasons: as a part of their
life cycle, to spawn, mate, etc. (Levinton, 2001) or more seasonally in search for
food. This behaviour is different for different species. Knowledge of the dominating
species in a region should be used to define an optimum migration behaviour for the
88 Lars Håkanson and Dan Lindgren

prey and predatory fish in the given region. For example, in Baltic Sea systems,
Baltic herring (Clupea harengus) is likely to migrate into the coast in great numbers
during the spawning in the spring (Axenrot and Hansson, 2004), which implies that
the predatory fish feeding on herring also will migrate into the coast, and that the fish
biomass in the coast will increase. To account for such regional migration patterns,
CoastWeb uses a dimensionless moderator (Yseason), which could be adjusted to the
prevailing conditions in different regions. This moderator is multiplied with the
default migration rate (Rmig). As in LakeWeb, it is also assumed that the immigration
or emigration of fish depend on the relationship between the actual biomass in the
coastal area and the normal biomass (the BM/NBM-ratio). The migration may also
sometimes be temperature dependent. Fish eat and grow faster in species-specific
temperature ranges (Larsson and Berglund, 2005). This temperature influence could
also be accounted for in the Yseason-moderator. An algorithm has been added to take
into account that the latitude (Lat in °N) probably influences the seasonal migration
patterns for fish. One should expect a more pronounced seasonal variation in light
and temperature at high latitudes than at low latitudes and hence also in migration of
fish searching for food. This has been handled in the following manner:
If Lat > 63°N then AV = 1 else AV = (63-Lat); AV is an averaging function used in
the smoothing function (SMTH) below:

YseasonB = SMTH(YsaeasonA, AV, 0.12) (18)

YseasonA is the seasonal moderator used for all coasts at latitudes ≥ 63°N (for which
AV = 1; this is an assumed boundary latitude for the given algorithm). At lower
latitudes, the function will smooth this curve (Figure 6A). The general moderator for
migration is given by:
If (YseasonA -YseasonB) ≥ 0 then Yseason = ((YseasonA+YseasonB)/2)·(Lat/63) else

Yseason = ((YseasonA+YseasonB)/2)·(63/Lat) (19)

Yseason is the default dimensionless moderator. It is shown in Figure 6A for four

different latitudes (≥ 63, 56, 45 and 35°N). With this setup, the moderator attains
high values in the spring at high latitudes reflecting regions with strong migrations
related to the spawning and feeding of the dominating fish species. This is a
suggestion for a general approach that can be used if no information is available on
regional migratory patterns of fish. If such information is available, it should
preferably be used.
4. It would require a very extensive sea-model (similar to and compatible with
CoastWeb) to predict the amount of fish or plankton available for immigration
outside any given coastal area. CoastWeb estimates the potentially available fish
biomass for immigration using an estimated normal fish biomass in the sea outside
the given coastal area, which is calculated from chlorophyll in the sea outside the
coastal area. The immigration of predatory fish is then calculated as:
If BMPD/NBMPD < 1 then FinmigPD = Yseason·RmigPD·NBMPDsea else

FinmigPD = 0.5·Yseason·RmigPD·NBMPDsea (20)

 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 89

RmigPD is the default migration rate for predatory fish (= 1/TSW). If the theoretical
SW-retention time, TSW, is 6 days, the surface water is exchanged 5 times each
month. Since there are no general migration rates to/from coastal areas available in
the literature (to the best of our knowledge), the value of the default migration rate is
our estimate based on calibrations using information from the studied coastal areas.
To quantify this more accurately is an important task for the future. NBMPDsea is the
normal biomass of predatory fish in the sea outside the given coastal area calculated
from the normal biomass of predatory fish in lakes, NBMPDlake (Table 4) and a
chlorophyll moderator, Ychlsea. Figure 6B illustrates the migration rate (Rmig) for
predatory and prey fish for the Ronneby coastal area (latitude 56°N; Table 1). An
Rmig-value of 0.75 means that 75% of the fish biomass may migrate either in or out of
the coastal area.
5. Emigration of predatory fish is calculated in a similar way, i.e.:
If BMPD/NBMPD < 1 then FoutmigPD = 0.5·Yseason·RmigPD·BMPD else

FoutmigPD = Yseason·RmigPD·BMPD (21)

Figure 6. A. Illustration of the seasonal moderator for immigration and emigration, Yseason, for four
different latitudes (≥ 63, 56, 45 and 35 °N) and
B. The default migration rates for prey and predatory fish (RmigPY and RmigPD, respectively) using data
for the Ronneby coastal area (latitude 56 °N)
90 Lars Håkanson and Dan Lindgren

Table 5 gives a compilation of all equations quantifying immigration and emigration. It

shows that the basic set-up is applied to all functional groups. Note that CoastWeb does not
account for cannibalism (feeding within the functional group). Cannibalism exists in aquatic
systems among fish (Menshutkin, 1971), but to gain simplicity, the model calculates net
production of fish (and zooplankton and zoobenthos).
Table 6 gives all calculated monthly fluxes of predatory fish, i.e., immigration and
emigration, initial production (IPR), production (BM/T), fishing and elimination, for the
Ronneby coastal area (Table 1). Table 6 and the following four tables give results
exemplifying the magnitude of these fluxes. Evidently, uncertainties in major fluxes are more
decisive for the predictions than uncertainties in minor fluxes. So, it is important to identify
the major fluxes and use algorithms that quantify these as correctly as possible. One can note:

The biomass of predatory fish in this coast varies between 2.5 and 4 t wet weight during
the year.
The initial production is relatively high during summer and fall with a yearly total of 3.2
t/y; the production values are about 3 t/y.
Immigration and emigration are significant; immigration 16 t/y and emigration 10 t/y. So,
there is a net immigration of predatory fish to this area.
The annual fishing of predatory fish under default conditions is 5 t/y.
The loss of predatory fish (death, etc.) is 4 t/y.

Table 7. gives the corresponding values for prey fish.

The biomass of prey fish is about a factor 5 times higher than for predatory fish; the
biomass varies between 12 and 20 t during the year.
The initial production is 63 t/y and the production about 20 t/y.
Immigration is 12 t/y and emigration 25 t/y, which means a significant net outflow of
prey fish.

Table 6. Calculated monthly and annual values of predatory fish biomass

and fluxes of predatory fish in the Ronneby coastal area (southern Baltic Proper)

Month Biomass IPRPD ElimPD FishingPD InmigPD OutmigPD Production

(BMPD) (kg ww/m) (kg ww/m) (kg ww/m) (kg ww/m) (kg ww/m) (BMPD/TPD)
(kg ww) (kg ww/m)
Jan 3 811 294 365 128 513 480 258
Feb 3 646 277 348 283 622 432 246
Mar 3 187 240 318 653 798 525 215
Apr 2 647 166 260 1 442 2 096 1 100 179
May 3 426 178 285 1 010 3 329 1 434 231
Jun 3 606 229 332 303 2 056 1 470 244
Jul 3 828 264 347 121 1 422 995 259
Aug 4 030 308 369 91 1 222 869 272
Sep 4 155 329 383 385 1 798 1 234 281
Oct 3 977 319 381 331 1 060 846 269
Nov 4 002 306 374 139 772 539 270
Dec 3 977 304 375 147 661 468 269
Annual 3 214 4 137 5 033 16 349 10 392 2 993
values:
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 91

Table 7. Calculated monthly and annual values of prey fish biomass

and fluxes in the Ronneby coastal area

From PY to PD

(BMPY/TPY)
(kg ww/m)

(kg ww/m)

(kg ww/m)

(kg ww/m)

(kg ww/m)

(kg ww/m)

(kg ww/m)

(kg ww/m)

(kg ww/m)
Production
OutmigPY
FishingPY
Biomass

(kg ww)

IPRZHPY

InmigPY
IPRZBPY

IPRZPPY
(BMPY)

ElimPY
Month

Jan 17 024 3 906 17 12 1 177 2 447 287 318 1 161 1 727

Feb 16 057 3 946 29 18 1 107 2 316 627 341 1 252 1 628
Mar 14 516 4 063 43 24 960 2 136 1 460 438 1 552 1 472
Apr 12 025 3 907 52 28 663 1 776 3 282 1 782 2 539 1 220
May 12 900 4 573 95 56 713 1 752 2 088 3 236 2 533 1 308
Jun 14 338 5 902 150 94 916 1 911 582 1 586 2 887 1 454
Jul 16 979 7 147 151 100 1 056 2 198 256 1 041 2 288 1 722
Aug 19 388 7 502 130 84 1 233 2 566 211 882 2 179 1 966
Sep 19 366 6 767 102 65 1 315 2 738 916 1 241 3 230 1 964
Oct 18 823 5 912 67 37 1 278 2 696 783 676 2 479 1 909
Nov 18 643 5 172 36 21 1 222 2 644 326 457 1 673 1 891
Dec 17 845 4 291 14 10 1 216 2 569 336 379 1 372 1 810
Annual 63 088 886 549 12 856 27 749 11 154 12 377 25 145 20 071
values:

Zoobenthos is the most dominating and important food for prey fish. The prey fish
production from zoobenthos consumption is 63 t/y, compared to 1 t/y from
consumption of herbivorous zooplankton and 0.5 t/yr from consumption of predatory
zooplankton.
The annual fishing of prey fish is 11 t/y.
The loss of prey fish (death, etc.) is 28 t/y.

Table 8. gives the results for predatory zooplankton.

The biomass varies very much during the year, from 120 kg ww during the winter to
almost 1.6 t during the summer.
The initial production from eating herbivorous zooplankton is over 27 t/yr and the
production about 21 t/yr.
Immigration is 49 t/y and emigration 40 t/y, i.e., a net inflow from the sea.
The elimination is 29 t/y.

Table 9 shows the same results for zoobenthos, which feed on benthic algae (430 t/y),
macrophytes (24 t/y), but most of all on ―sediments‖ (1000 t/y) since zoobenthos mainly are
detrivores.

The biomass of zoobenthos varies between 45 and 100 t during the year and is about a
factor of 6 higher than the biomass of prey fish.
Immigration and emigration are zero (zoobenthos are largely stationary within the given
coastal area).
The elimination of zoobenthos is about 1000 t/y.
92 Lars Håkanson and Dan Lindgren

Table 8. Calculated monthly and annual values of biomass and

fluxes for predatory zooplankton in the Ronneby coastal area

Month Biomass IPRZP ElimZP From ZP From ZP InmigZP OutmigZP Production

(BMZP) (kg (kg to JE to PY (kg (kg (BMZP/TZP)
(kg ww) ww/m) ww/m) (kg (kg ww/m) ww/m) (kg ww/m)
ww/m) ww/m)
Jan 117 135 456 0 147 1 066 626 323
Feb 160 150 501 0 165 1 248 688 442
Mar 252 300 790 0 259 1 926 1 084 696
Apr 340 527 1 134 0 350 2 600 1 556 940
May 607 933 1 569 0 399 3 455 2 153 1 678
Jun 1 159 3 224 3 309 0 814 5 994 4 542 3 203
Jul 1 594 6 769 5 568 0 1 375 8 249 7 641 4 405
Aug 1 285 6 676 5 617 0 1 466 7 808 7 709 3 551
Sep 917 4 399 4 182 0 1 222 6 376 5 739 2 534
Oct 681 2 787 3 037 0 944 5 125 4 168 1 882
Nov 347 1 051 1 750 0 540 3 307 2 402 959
Dec 146 464 987 0 306 1 983 1 355 403
Annual 27 415 28 900 0 7 987 49 137 39 663 21 017
values:

Table 9. Calculated monthly and annual values of biomass

and fluxes for zoobenthos in the Ronneby coastal area

Month Biomass (BMZB) IPRBAZB IPRsedZB IPRMAZB From ZB to PY ElimZB Production

(kg ww) (kg ww/m) (kg ww/m) (kg ww/m) (kg ww/m) (kg ww/m) (BMZB/TZB)
(kg ww/m)
Jan 45 501 6 284 73 156 1 034 24 374 58 168 10 808
Feb 48 373 10 099 75 203 1 001 24 720 58 711 11 490
Mar 53 841 15 137 76 514 1 069 26 935 60 316 12 789
Apr 64 705 22 908 77 983 1 260 33 436 57 851 15 369
May 80 396 49 432 84 312 1 723 52 251 67 525 19 096
Jun 100 518 78 805 91 251 2 510 66 358 86 086 23 876
Jul 103 515 84 256 95 216 3 247 75 697 104 025 24 588
Aug 90 509 68 794 96 027 3 298 71 336 109 788 21 499
Sep 77 495 49 825 94 897 2 876 60 968 99 645 18 407
Oct 69 738 28 632 89 079 2 371 40 650 87 189 16 565
Nov 57 531 15 390 81 274 1 862 34 077 76 656 13 665
Dec 47 569 6 157 73 798 1 280 27 314 63 882 11 299
Annual values: 435 719 1 008 710 23 531 538 116 929 844 199 451

These simulations indicate that zoobenthos is an important food for fish in this coastal
area and that threats to the production of zoobenthos would be serious to the fish production.
Immigration and emigration of fish and zooplankton are important processes. There is
generally no jellyfish in the Ronneby coastal area. The next section focuses on jellyfish.

An Outline of the Sub-Model for Jellyfish

Jellyfish (JE) can appear in great numbers and are able to consume substantial amounts of
mainly zooplankton, which can influence on fish production (Schneider and Behrends, 1994;
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 93

Brodeur et al., 2002; Purcell, 2003). This makes them an important part of coastal foodwebs
and they have been included as a secondary production unit in CoastWeb for areas where the
salinity is high enough (the default threshold value in this model is set to 10; Lucas (2001)
gave a value of 14 for a common jellyfish, Aurelia aurita). Jellyfish is a predatory
zooplankton and could belong to the predatory zooplankton group in the model. However, the
medusae-stage, i.e., what we generally mean by jellyfish, is so different compared to other
predatory zooplankton concerning size, abundance, etc. that it has been assigned its own
group in CoastWeb.
Figure 7 illustrates the jellyfish sub-model and Table 10 gives all equations. Although
this is a new sub-model, it is built in the same way as all other sub-models. This section will
give an outline of this building block.
Since jellyfish mainly eat zooplankton (Larson, 1987; Mills, 1995; Hansson, 2006), there
is only one food choice between predatory and herbivorous zooplankton. So, the number of
first order food choices for jellyfish is NRJE = 2, separated by DCZPZH. Jellyfish are also
known to consume ichthyoplankton (fish eggs and larvae; Cowan et al., 1996; Suchman and
Brodeur, 2005). However, this is not considered in the model since ichthyoplankton is not
included as a functional group.

Table 10. Basic differential equation for production and biomass of jellyfish (JE)

BMJE(t) = BMJE(t - dt) + (IPRZHJE + IPRZPJE + InmigJE - ElimJE - OutmigJE)·dt

IPRZHJE = YsalJE· (1- DCZPZH)·FZHJE· MERZP·Ytemp0.5 [initial production of JE from eating ZH]
IPRZPJE = YsalJE· DCZPZH·FZPJE· MERZP·Ytemp0.5 [initial production of JE from eating ZP]
InmigJE = RmigJE·NBMJEsea [immigration of JE]
ElimJE = BMJE·1.386/TJE [elimination of JE]
OutmigJE = RmigJE·BMJE [emigration of JE]
FZHJE = BMJE·CRJE [flux from ZH to JE]
FZPJE = BMJE·CRJE [flux from ZP to JE]
Ychlsea = Chlsea/Chlcoast [correction factor for biomasses in the sea and in the coast related to
chlorophyll]
CRJE = (NCRJE+NCRJE·(BMJE/NBMJE-1)) [consumption rate for JE; if NBMJE = 0, then CRJE = 0]
DCZPZH = 0.5 [distribution coefficient for JE eating ZP or ZH]
MERZP = 0.32 [metabolic efficiency ratio for JE eating ZP or ZH]
RmigJE = RmigPY = RmigPD·0.33 [basic migration rates for PY, JE and PD]
NJE = 2 [number of first order food choices]
NBMJE = 10·NBMZP = 50·Ychlsea·(1-DCZHZP)·10-6·SMTH((V·38·CTP 0.64),TZP,(V·38·CTP 0.64)) [normal
biomass of JE]
NCRJE = NJE/TJE [normal consumption rate for JE]
SalSW = Surface-water salinity [= 6.5 in the Ronneby coastal area]
TJE = 120/30.42 [turnover time for JE in months]
YsalJE = if SalSW < 10 then 0 else 1 [assumed threshold salinity for JE production]
Ytemp = (SWT+0.1)/9 [dimensionless moderator for temperature influences on bioproduction]
94 Lars Håkanson and Dan Lindgren

Outline of the sub-model for jellyfish

From ZH to JE, FZHJE

MERZP
YSWT

IPR ZHJE T JE

InmigJE Jellyfish biomass

BMJE
Elim JE

RmigJE

IPR ZPJE OutmigJE

From ZP to JE,
FZPJE
CRJE
DCZPZH
NCR JE

NJE YsalJE

NBM ZP
NBM JE SalSW

Figure 7. An outline of the new sub-model for jellyfish

The consumption of biomass from grazing is calculated in kg ww/month. The total

consumption is given by FZPJE = BMZP·CRJE. BMZP is the available biomass of predatory
zooplankton and CRJE is the actual consumption rate (jellyfish eating its prey):

CRJE = (NCRJE+NCRJE·(BMJE/NBMJE-1)) (22)

NCRJE is the normal consumption rate, BMJE is the actual biomass of jellyfish and
NBMJE is the normal biomass. This means that the model quantifies changes in the actual
consumption of the prey unit related to changes in the biomass of the consumer: more animals
in the secondary unit (higher BMJE) means a higher actual consumption rate, CRJE. If the
actual biomass of the predator is equal to the normal biomass of the predator, BMJE/NBMJE =
1, and CRJE = NCRJE. If the actual biomass of the predator is twice the normal biomass, then
CRJE = 2·NCRJE. So, the model gives a linear increase in consumption with increase in
biomass of the secondary unit. Lacking reliable empirical data, it is assumed that NBMJE may
be set to be 10 times higher than the normal biomass of predatory zooplankton and depend on
salinity. This gives:

NBMJE = 10·NBMZP·YsalJE (23)

By using a boundary condition, NBMJE can never be less than 0. The normal
consumption rate, NCRJE, is NCRJE = 2/TJE. TJE is the turnover time of jellyfish (i.e., of the
medusae stage). According to Lucas (2001), medusae of the common jellyfish, Aurelia aurita,
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 95

generally live for 4 to 8 months. In the model, 120 days is used as a default value of turnover
time for Jellyfish. The initial production (IPR) of jellyfish (JE) from eating predatory
zooplankton (ZP) is given by:

IPRJE = YsalJE·DCZPZH·FZPJE·MERZP·Ytemp0.5 (24)

The distribution coefficient, DCZPZH, gives the fraction of predatory zooplankton versus
herbivorous zooplankton consumed by jellyfish.
The MER-value is the amount of the total consumption (FZPJE) that will increase the
biomass of the consumer, here jellyfish. The jellyfish digestion/consumption of its prey is
temperature dependent (Martinussen and Båmstedt, 1999). This is accounted for by a
dimensionless moderator Ytemp0.5 (Ytemp = ((SWT+0.1)/9); SWT = the SW-temperature in °C).
YsalJE is a salinity moderator, which works in the following way: If the SW-salinity (salSW) is
lower than 10, then YsalJE = 0 else YsalJE = salSW/10. Jellyfish can in some cases be consumed
by fish and turtles (Legović, 1987) and they can also be consumed by other jellyfish
(Martinussen and Båmstedt, 1999). However, this is not accounted for in the default set-up of
the model. Jellyfish are removed from the coastal system by two processes: elimination,
related to the turnover time of jellyfish and emigration.
Immigration and emigration of jellyfish are calculated from:

FinmigJE = RmigPY·NBMJEsea·YsalJE (25)

FoutmigJE = RmigPY·BMJE (26)

The migration rate for jellyfish is set equal to the migration rate for prey fish and the
normal biomass of jellyfish in the sea outside the given coastal area is calculated from
NBMJEsea = NBMJE·Ychl. The actual biomass of jellyfish in the coastal area, BMJE, is
calculated automatically in the model and Ychl is defined by eq. 1. Elimination, i.e. the loss of
biomass (ELJE) is given as:

ELJE = BMJE·1.386/TJE (27)

Where 1.386 is the halflife constant (-ln(0.5)/0.5 = (0.693/0.5; see Håkanson and Peters,
1995).

THE ROLE OF MACROPHYTES

Macrophyte Cover

The sub-model used in LakeWeb to predict the macrophyte cover is shown in eq. 28.

MAcovlake = (10.49+1.502·(Sec /Dm)-1.993·(90/(90-Lat))-0.

422·(√Dmax)+0.490·log(A1·10-6))2 (28)
96 Lars Håkanson and Dan Lindgren

In CoastWeb, it has been modified by an energy factor (Yex1) taking into account that
coasts are open and affected by wind/wave action from the sea. This moderator quantifies that
in coasts, where the wind/wave energy is high and the water exchange fast, it would be more
difficult for the roots of the macrophytes to develop which would lower the macrophyte cover
(MAcov in % of the coastal area). The macrophyte cover is calculated as:

MAcov = MAcovlake· (1/Yex10.75) (29)

If Ex < 0.003 (lower boundary condition for the exposure; see Figure 1) then Yex1 = 1
else Yex1 = (Ex/0.003)0.25
If Ex > 10 (upper boundary condition for the exposure) then Yex1 = 10 else Yex1 =
(Ex/0.003)0.25
So, if the exposure (Ex) is very limited (< 0.003), the equation will calculate the same
macrophyte cover as for a lake. If Ex is very high (> 10) for open coasts, (1/Yex10.75) will be
0.18 and the macrophyte cover will be only 18% of the corresponding value for a lake. A
typical Ex-value for Baltic coastal areas is about 0.1 (Håkanson, 2006) which gives Yex =
0.52 and a macrophyte cover that is 52% of what would be expected in a lake with the same
Secchi depth (Sec in m), the same area above a water depth of one meter (A1 in km2), the
same mean depth (Dm in m) and maximum depth (Dmax in m). The macrophyte cover is used
to calculate macrophyte production and biomass; the higher the macrophyte cover, the higher
the fish biomass (if everything else is constant), since the macrophytes provide a protected
environment for small fish (Sogard and Able, 1991).
Different macrophyte species prefer different salinities (Boston et al., 1989; King and
Garey, 1999) and have different tolerance to changes in salinity (Rout and Shaw, 1998, 2001).
A relatively constant salinity is desirable for the macrophytes to abound. Figure 8 shows that
the increase in salinity in the middle of the 1990s in Ringkobing Fjord (see Table 1) likely
caused the observed reduction in macrophyte cover. There has been a slight change in
dominance from sago pondweed Potemogeton pectinatus towards the more salt tolerant ditch
grass Ruppia cirrhosa in recent years. This example is included to stress that Coast Web does
not include any consideration to the fact that there can be changes in the abundance of single
macrophyte species with a higher or lower tolerance to changes in salinity. The overall
correspondence between the predicted values for the macrophyte cover during the period
when the salinity was lower than 9.5 is good (see Håkanson, 2006), but when the salinity
reached a threshold value of 9.5 (Håkanson et al., 2007), there was an initial reduction in
macrophytes, which is not captured by the model. This is because when the salinity increases,
the Secchi depth will also iincrease, which means that the model will predict an increased
macrophyte cover. However, Figure 8 shows that the opposite has happened in Ringkobing
Fjord. This indicates that the effect of the changes in salinity on single macrophyte species is
even more pronounced than indicated by looking just at the macrophyte cover for the initial
period. The actual change should be related to the curve predicted by CoastWeb since these
predictions describe what would normally be expected under given conditions related to the
factors accounted for in CoastWeb (eq. 28).
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 97

Figure 8. Illustration of how the mean annual macrophyte cover and the mean annual salinity have
varied in Rinkobing Fjord between 1980 and 2004, and how the macrophyte cover is predicted by the
modified CoastWeb-model

Macrophytes and Macroalgae and Their Influence on Fish Production

Macrophytes and macroalgae constitute a good environment for some species of

predatory fish, e.g., for pike to make an ambush (Savino and Stein, 1989). The beds of
macrophytes constitute a ―nursery‖ for young fish (Sogard and Able, 1991), which help to
sustain a high fish biomass. Macrophytes and macroalgae are generally not important food for
most fish (Barnes and Hughes, 1988; except for herbivores), but they provide shelter (Persson
and Eklöv, 1995; Duarte, 2000) and can reduce the predation pressure (Nelson and Bonsdorff,
1990; Winfield, 2004), especially on small fish. In LakeWeb, this is handled by a
dimensionless moderator, YMA:

YMA = (1-0.2·(Maccov/25-1)) (30)

Maccov is the macrophyte cover (%). Macroalgae are expected to play a larger role in
saline systems than in lakes for two reasons. Firstly, when the water clarity increases, the
depth of the photic zone increases. This increases the production of benthic algae and
macrophytes, which can cause a shift from a dominance of pelagic primary production to
benthic primary production. Secondly, in marine systems such a shift would likely lead to a
higher percentage of large macroalgae compared to smaller benthic algae. These macroalgae
will influence the structure of the coastal ecosystem in ways similar to the macrophytes. In
LakeWeb, the macrophytes influence the fish production mainly by providing a safe haven
for the small fish. This is accounted for by lowering the predation pressure (from man,
mammals or birds) on the fish. In CoastWeb, the influence of macroalgae and macrophytes on
production and survival of prey and predatory fish is accounted for by a modification of the
dimensionless moderator (YMA) in eq. 30. This gives a new moderator YMAcoast, eq. 31, that
should reduce the predation pressure on prey and predatory fish in the same manner as YMA
does in LakeWeb.
98 Lars Håkanson and Dan Lindgren

YMAcoast = YMA/YBAmacro (31)

YBAmacro is the ratio between the actual biomass of benthic algae in coastal areas and the
normal biomass of benthic algae in lakes (YBAmacro = BMBA/NBMBAlake). This ratio reflects
the prevalence of macroalgae in coastal areas compared to lakes and is generally higher
than 1.
In LakeWeb, the loss of prey fish from fishing and predation, is given by a constant
default rate. In CoastWeb, the corresponding default rate is modified by two dimensionless
moderators meant to make the loss of prey fish from fishing more realistic. The loss of prey
fish from fishing is given by FfishPY (in kg ww/month):

FfishPY = YMAcoast·BMPY·RfishPY (32)

BMPY is the biomass of prey fish and RfishPY is the fishing rate of the prey fish. RfishPY is
defined as:

RfishPY =Ysec·Yseason ·0.5 (33)

0.5 (1/month) is a default fishing rate used in LakeWeb (derived from extensive
calibrations), which is affected by two dimensionless moderators that account for influence of
Secchi depth (Ysec) and seasonal migration pattern to and from the coastal area (Yseason). If
empirical data are available on fishing of prey fish, such data should be used instead of the
default fishing rate of 0.5.
If the Secchi depth in a corresponding lake (Seclake) is larger than the Secchi depth in the
coast (Seccoast = Sec), then Ysec =1 else Ysec = Sec/Seclake. So, if the water clarity in the coast
is larger than in a corresponding lake, the predation pressure on prey fish is assumed to be
higher than in a lake. This is quantified by this simple dimensionless moderator. Yseason is the
dimensionless moderator for seasonal migration (see eq. 19).
The loss from all types of predation on predatory fish (FfishPD in kg ww/month) is given in
a similar way by:

FfishPD = YMAcoast·BMPD·2·RfishPY (34)

The default assumption is that the rate for fishing and predation is higher for predatory
fish than for prey fish based on the fact that large fish are more attractive for professional and
recreational fishermen (given by the factor 2). Figure 9 illustrates how the prey fish biomass,
the predatory fish biomass and the elimination of prey fish depend on the new algorithm
given in eq. 31. In these simulations, the new algorithm was used after month 26, before the
algorithm in eq. 30 was used. One should note the effects that the macroalgae would have on
the predation of prey fish (Figure 9C). The effect is due to an increase in prey fish biomass,
which is compensated for by a significant increase in the food available for predatory fish and
hence also in predation pressure of predatory fish on prey fish. The net effect is a relatively
small change in prey fish biomass (Figure 9B) and in predatory fish biomass (Figure 9A).
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 99

Figure 9. Simulations to illustrate the role of macroalgae for the fish production and biomass in coastal
areas. In these simulations, the dimensionless moderator expressing how macroalgae influence
elimination of prey fish was used from month 26 (the curves ―Accounting for macroalgae‖) compared
to a situation when this moderator is not used. Using data from the Ronneby coastal area, S. Sweden,
(A) gives the results for predatory fish, (B) for prey fish and (C) for the predation/fishing of prey fish

RESULTS
This section presents case-studies to illustrate the potential use of CoastWeb to quantify
how three major threats to coastal systems are likely to influence the structure and function of
coastal foodwebs and this section will also give results from sensitivity analyses to illustrate
how the model works along a latitude/temperature gradient and a salinity gradient. The first
case-study focuses on eutrophication, the second on overfishing and the third on toxic
contamination.

Eutrophication

The idea here is to study how hypothetical stepwise (3-year steps) increases in TP in the
sea outside a coast would likely influence the coast. Here, data from the Haverö coastal area
are used (Finland; Table 1). The results are presented in Figure 10. The actual (default) TP-
concentration in the sea is 24 µg/l, and tests have been done of how values of 0.75·24, 24,
1.5·24 and 2·24 would change modelled values of TP in the coastal water (A), chlorophyll
(B), Secchi depth (C), the oxygen saturation in the deep-water zone, O2Sat (D), the normal
and actual biomasses of zoobenthos (E), herbivorous zooplankton (F), prey fish (G) and
predatory fish (H). Modelled values of TP, chlorophyll, Secchi depth and O2Sat are also
100 Lars Håkanson and Dan Lindgren

compared with empirical data and uncertainty bands for the empirical data. The main results
and conclusions of the simulations are:

There is generally good correspondence between modelled and empirical data for the TP-
concentration (Figure 10A), chlorophyll (Figure 10B), Secchi depth (Figure 10C) and
O2Sat (Figure 10D). Note that the empirical chlorophyll value is a mean value for the
entire summer period.
There is also a close and logical correspondence between the actual and normal
biomasses for zoobenthos, herbivorous zooplankton, prey fish and predatory fish.
Note that the actual biomasses accounts for seasonal variations and predation more
realistically than the normal biomasses, which are basically empirical reference
values.
The increased hypothetical eutrophication of the sea outside the coastal area will
drastically increase TP also in the coast (which is logical because the water retention
time in this area is 3-5 days, Persson et al., 1994) (Figure 10E). This leads to higher
Chl-values (Figure 10B), reduced Secchi depths (Figure 10C) and lower O2Sat
(Figure 10D), which will influence zoobenthos (Figure 10E) living in the sediments
more than zooplankton in the more oxygenated surface water (Figure 10F).
Since there is much more zoobenthos in the system than zooplankton (about 50 t ww
compared to about 3-5 t ww), zoobenthos is an important source of food for
omnivorous prey fish and changes in zoobenthos will have clear effects on the prey
fish (Figure 10G), and changes in prey fish biomass will in turn influence the
predatory fish who feed on prey fish (Figure 10H).
The zoobenthos within the accumulation areas (A-areas) will die if O2Sat is lower than
20%, but the oxygenation of the sediments on the erosion and transport areas (ET-
areas) will maintain a low biomass of zoobenthos in the more shallow parts of the
coastal area.

To conclude: The increased eutrophication in the sea will imply several changes to the
water quality and foodweb characteristics of the studied coastal area. Many of these changes
could be expected without a model, but the point here is that they have been quantitatively
predicted using a general comprehensive foodweb model which includes a dynamic mass-
balance model for phosphorus. This modelling accounts for many abiotic and biotic
interactions and feedbacks and it is meant to give the ―normal‖ response of the system to the
given change in the TP-concentration in the sea. The model accounts for different types of
compensatory effects (such as increasing eutrophication leading to a higher primary
phytoplankton production, which leads to more suspended particulate matter in the water and
a lower Secchi depth, which leads to a smaller depth of the photic zone, which leads to a
lower primary phytoplankton production). Such effects are difficult to quantify without a
model. As stated, CoastWeb simulates functional groups and hence does not include
responses related to single species.
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 101

Figure 10. Case-study on coastal eutrophication using data from the Haverö coastal area. There are
changes in 3-year steps in the TP-concentration in the sea adjacent to the coastal area. The default TP-
concentration in the sea is 24 µg l-1 and this value has been set to 0.75·24, 24, 1.5·24 and 2·24 (i.e., 18,
24, 36 and 48 µg l-1) and the consequences calculated for (A) the TP-concentration in the given coastal
area, (B) chlorophyll, (C) Secchi depth, (D) oxygen saturation in the deep-water zone (all compared to
empirical mean values and inherent uncertainties in the mean values; the chlorophyll mean value is for
the summer period) and actual and normal biomasses of (E) zoobenthos (F) herbivorous zooplankton,
(G) prey fish and (H) predatory fish. MV: Mean values, SD: Standard deviation

Overfishing

Extensive fishing or fishing more than the permitted quota, is, unfortunately, a common
practice in most parts of the world and an issue of intensive debate in many countries (Eagle
102 Lars Håkanson and Dan Lindgren

and Thompson Jr., 2003; Hilborn et al., 2003). The idea with this case study is to illustrate
how CoastWeb can be used to address this issue. Here, data from the Gävle coastal area
(northern Sweden; Table 1) have been used. We will show how changes in fishing would
influence the structure of this coastal ecosystem. The scenario is defined in Figure 11A. First,
there is a ―normal‖ period of three years, then a period of one year when ten times the normal
amount of prey and predatory fish is taken out of the system, followed by a recovery period of
two years, then another period of intensive fishing with 20 times the default fishing for a
period of two years, followed by a recovery period. Note that this is also a sensitivity analysis
since no other changes than fishing have been made.
In Figure 11, the consequences for TP-concentration (A), Secchi depth (B), chlorophyll
(C) and the actual biomasses with and without this extensive fishing for herbivorous and
predatory zooplankton (D, E), zoobenthos (F), prey fish (G) and predatory fish (H) are
presented. The main results and conclusions of the simulation are:

Also for this coastal area, there is generally a good correspondence between modelled
and empirical data for TP (Figure 11A), Secchi depth (Figure 11B) and chlorophyll
(Figure 11C). One can also note from these three figures that the changes in fishing
in this coastal area would not affect the three water variables very much.
There are no clear changes for herbivorous zoolankton (Figure 11D), but increases in the
biomass of predatory zooplankton as a response to the lower predatory pressure from
a declining biomass of prey fish related to the extensive fishing (Figure 11E and
11G).
The lower predation pressure on zoobenthos from a reduced biomass of benthivorous
prey fish is evident (Figure 11F).
Note that this coastal system will recover quickly. As long as there is fish in the sea
outside the coast, immigration of fish will continue, and the system will return to a
dynamic steady state, as given by the algorithms for migration in the model.

To conclude: The increased fishing will likely only affect the given coastal system
marginally and mostly so during the period of the intensive fishing. The immigration of fish
from the sea, especially in the springtime, is very large. However, if this kind of fishing were
done also in the outside sea, the results would be different. This scenario also shows that it is
essential to use as accurate values as possible on immigration and emigration in the model.

Toxic Contamination

The final case-study concerns the effects of toxic substances. Our aim is to demonstrate
the potential of CoastWeb for making calculations to obtain realistic expectations of the
consequences that contaminants can have on the coastal foodweb. We will examine what
might happen if a hypothetical contaminant would drastically reduce the biomass of a
functional group. Large ecosystem effects should be expected if there are major changes in
groups with large biomasses. For that reason, zoobenthos have been selected and data from
the Ronneby coastal area have been used. There is also another reason to focus on
zoobenthos, related to the fact that many toxic substances show a high affinity for particles in
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 103

aquatic systems (Håkanson, 1999; Mackay, 2001). This means that high concentrations of
such substances may appear in sediments, the habitat for zoobenthos.

Figure 11. Case-study on extensive fishing (or overfishing) using data from the Gävle coastal area. First
there is a tenfold increase in the default fishing/predation rate on prey and predatory fish for one year,
and then the fishing rate is increased by a factor of 20 for two consecutive years (see Figure A). The
consequences of these events are calculated for (A) TP-concentration, (B) Secchi depth and (C)
chlorophyll (all compared to empirical data, mean values and uncertainties in the mean values; the
chlorophyll mean value is for the summer period). Figures D to H gives a comparison of how this
extensive fishing would influence the actual biomasses of (D) herbivorous zooplankton, (E) predatory
zooplankton, (F) zoobenthos, (G) prey fish and (H) predatory fish. MV: Mean values, SD: Standard
deviation
104 Lars Håkanson and Dan Lindgren

Figure 12. Case-study on toxic contamination using data from the Ronneby coastal area. It is assumed
that there is first a contamination that eliminates 90% of the zoobenthos months 7 and 8, then a
contamination that kills 99% of the zoobenthos for a whole year, and, finally, total extinction of
zoobenthos (see Figure A). The consequences of these events are calculated for the actual and normal
biomasses of (B) phytoplankton, (C) benthic algae, (D) bacterioplankton, (E) herbivorous zooplankton,
(F) predatory zooplankton, (G) prey fish and (H) predatory fish. MV: Mean values, SD: Standard
deviation

Figure 12A presents the scenario. First, 90% of the zoobenthos biomass is reduced (killed
by contamination) months 7 and 8, year 4. Then, after a two year recovery period, 99% of the
zoobenthos biomass is reduced for an entire year. Finally, after another period of recovery, all
zoobenthos are killed. Figure 12 shows how this would influence the actual and normal
biomasses of zoobenthos (A), phytoplankton (B), benthic algae (C), bacterioplankton (D),
herbivorous zooplankton (E), predatory zooplankton (F), prey fish (G) and predatory fish (H).
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 105

Initially, there is a good correspondence between actual and normal biomasses also in this
area for all the eight functional groups shown in Figure 12.
The changes in zoobenthos (Figure 12A) will not affect phytoplankton (Figure 12B),
benthic algae (Figure 12C) and bacterioplankton (Figure 12D).
Since there is much more zoobenthos in the system than herbivorous and predatory
zooplankton (about 100 t ww compared to about 5 and 1 t ww, respectively),
zoobenthos is an important food source for omnivorous prey fish and reductions or
changes in zoobenthos will have clear effects on prey fish and hence also on
predatory fish (compare Figure 12A to Figure 12G and H).

To conclude: This case-study shows that a reduction of zoobenthos biomass will have
clear effects of fish production and biomass in the given coastal area. This scenario may not
be realistic in the sense that nothing but zoobenthos has been affected by the contamination.
However, more realistic simulations can be made with the model. The model can, e.g., also be
used to simulate non-lethal effects of toxic substances, such as reduced production. The idea
here is just to briefly demonstrate its potential.

Sensitivity Analysis – Latitude/Temperature

This section first presents a sensitivity analysis along a latitude (temperature) gradient.
The latitude for the Gräsmarö coastal area (see Table 1; latitude = 58°N) has been changed in
3-year steps to 40, 50, 58 and 70°N. Results are given in Figure 13 for Secchi depth, TP,
O2Sat, chlorophyll (using the general approach in Table 4) and actual and normal biomasses
of benthic algae, zoobenthos, prey fish and predatory fish. Figure 13A gives the driving
variable, the latitude gradient. The main results and conclusions of the simulation are:

The change in latitude will cause clear changes in predicted surface-water temperatures
(Figure 13A).
There is a good correspondence between modelled and empirical chlorophyll (Figure
13B); the figure gives empirical mean values (MV) and MV plus two standard
deviations (SD).
There is a good correspondence also between modelled values for sedimentation on
accumulation areas and empirical data, as determined from sediment traps (Figure
13C).
Figure 14D to H give values of the actual and normal biomasses for phytoplankton,
benthic algae, bacterioplankton, zoobenthos and predatory fish. The actual biomasses
should give representative values since these values account for predation and
several factors that are not included in the calculation of the normal biomasses. In
general, however, there is a good correspondence between the two measures
indicating that the model works as expected.
It is also interesting to compare the biomasses: in this test, the biomass of benthic algae
(Figure 13E) is higher than the biomass of bacterioplankton (Figure 13F), which is
higher than the biomass of phytoplankton (Figure 13D); the biomass of zoobenthos
106 Lars Håkanson and Dan Lindgren

(Figure 13G) is about 20 times higher than the biomass of predatory fish (Figure
13H).

Figure 13. Testing the model along a latitude gradient using data from the Gräsmarö coastal area. The
default latitude (58°N) has been changed in 3-year steps by 40, 50, 58 and 70°N and the consequences
have been calculated for (A) the surface-water temperature, (B) chlorophyll-a, (C) sedimentation on
accumulation areas (as compared to empirical maximum and minimum data from sediment traps), and
modelled actual and normal biomasses of (D) phytoplankton, (E) benthic algae, (F) bacterioplankton,
(G) zoobenthos and (H) predatory fish. MV: Mean values, SD: Standard deviation
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 107

Sensitivity Analysis - Salinity

This section presents a sensitivity analysis along a salinity gradient. Figure 14 uses data
from the Ronneby coastal area (see Table 1). The default salinity inside and outside this area
has been increased in 3-year steps from 6.5 to 13, 19.5 and 26 and the consequences
calculated for all functional groups and bioindicators while all other factors have been kept
constant at the default conditions. Figure 14 gives results for Secchi depth, TP, O2Sat,
chlorophyll (using the general approach in Table 4) and actual and normal biomasses of
benthic algae, jellyfish, prey fish and predatory fish. Figure 14A gives the driving variable,
the salinity gradient. The main results and conclusions are:

The increase in salinity will cause a distinct increase in Secchi depth and in water clarity
(Figure 14A).
There is a good correspondence between modelled and empirical Secchi depths also in
this coastal area. Whenever data are available, Figure 14 also gives empirical mean
values (MV) and standard deviations for the empirical data (SD) as a measure of the
inherent uncertainty in the empirical data.
There is a good correspondence between modelled and empirical TP. TP will decrease
somewhat along the salinity gradient (Figure 14B).
There is also a fine correspondence between modelled and empirical O2Sat, which will
decrease with increasing salinity because a high salinity will increase flocculation
and sedimentation of suspended particulate matter and particulate phosphoprus. In
this open and shallow area, the deep-water turnover time is about 6 days and the
deep-water volume is small. This means that the coastal area is well oxygenated
(Figure 14C).
There is also a relatively good correspondence between modelled and empirical
chlorophyll (Figure 14D). Chlorophyll decreases with increasing salinity (see Figure
5) and with lower TP.
The biomass of benthic algae (Figure 14E) increases along the salinity gradient because a
higher salinity means an increased water clarity and therefore photosynthetic activity.
Also the Jellyfish biomass increases (Figure 14F). However, there are no empirical
data on biomasses available for comparison.
Also the biomass of zoobenthos increases, meaning more food for prey fish and a higher
biomass of prey fish along the salinity gradient. More prey fish also means more
food for the predatory fish and an increase in predatory fish biomass (Figure 14G and
H). The changes in salinity would also influence the migration of fish and the
consumption rates since the salinity influences the normal biomasses of both prey
and predatory fish.

In reality, individual species can be sensitive to changes in salinity and would not survive
the big changes in salinity that was used in this example. However, the model does not
simulate individual species, but functional groups and a salinity that is non-optimal for one
species may be optimal for another species in the same functional group.
108 Lars Håkanson and Dan Lindgren

Figure 14. Testing the CoastWeb-model using data from the Ronneby coastal area along a salinity
gradient. The default salinity (6.5) has been increased in 3-year steps by a factor of 1, 2, 3 and 4 and the
consequences calculated for (A) Secchi depth, (B) TP-concentration, (C) oxygen saturation in the deep-
water zone, (D) chlorophyll-a concentration using the general model (all compared to empirical mean
values and inherent uncertainties in the mean values; the chlorophyll mean value is for the summer
period) and actual and normal biomasses of (E) benthic algae, (F) jellyfish, (G) prey fish and (H)
predatory fish

DISCUSSION AND COMMENTS

The overall framework for this modelling is that science and management need
practical, operational tools to predict how coastal ecosystems would likely respond to
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 109

different threats so that the best possible remedial actions can be taken. The model presented
in this work in meant as a tool to address such issues. This is exemplified by the case-studies
and sensitivity analyses discussed in this paper
We have presented a first version of CoastWeb, a coastal foodweb model that simulates
ten functional groups and includes a mass-balance model for phosphorus. CoastWeb is an
adaptation of a foodweb model for lakes and its underlying structure and main algorithms
have been extensively tested. However, this is a first adaptation of the model to coastal
conditions and there are several parts that could and should be improved if, and when, better
data become available from more coastal areas covering a wide functional domain. At
present, the lack of data is most evident for more saline coastal areas.
A major deficiency in CoastWeb compared to LakeWeb concerns the empirical models to
predict normal biomasses for the functional groups. In this respect, limnology, where good
empirical models exist for almost all functional groups, is ahead of coastal ecology. This
highlights the importance of getting better data and knowledge on the role of the salinity to
predict chlorophyll from phosphorus and/or nitrogen in costal areas. It is also important to
seek better knowledge on the processes regulating nitrogen fluxes in marine systems to be
able to include a mass-balance model of nitrogen in CoastWeb in the future.
In CoastWeb, jellyfish has been introduced as a functional group. The model structure for
this group is the same as for all other functional groups. Empirical data have been used for
jellyfish model parameterisation, when available. However, in this first version, several
estimates have been used that may need to be changed when more and better data become
available in the future. Mass occurrence (blooms) of jellyfish also needs to be addressed in
future versions of CoastWeb.
Due to the high variability that coastal fish show concerning food habits, migratory
patterns, etc., it is difficult to develop general algorithms for fish that give good predictions
over a wide range of areas. The regional seasonal moderator (Yseason) that handles migration
of fish used in this work is only meant as a template and is mainly intended to reflect
prevailing conditions in Baltic Sea coastal areas. Similar regional moderators should be
developed for other coastal regions. This is especially important since the performed tests
show that migration of fish is of major importance for coastal fish biomasses. It is essential to
stress that the model simulates functional groups and not individual species.
In the presented sensitivity analyses and case-studies, several water variables show good
correspondence with existing and available empirical data. The calculated biomasses seem
reasonable, but no or few empirical biomasses data have been available to perform
independent validations. This is desirable for the future, although it is very hard to get
comprehensive, time- and area compatible data on biomasses and abiotic variables from the
same area for functional groups of organisms.

ACKNOWLEDGMENTS
This work has been carried out within the framework of the Thresholds-project, an
integrated EU project (no., 003933-2), and we would like to acknowledge the financial
support from EU and the constructive cooperation within the project. Special thanks to prof.
Carlos Duarte, the scientific coordinator of the project.
110 Lars Håkanson and Dan Lindgren

APPENDIX: MINOR MODIFICATIONS

1. Salinity is of paramount importance for the number of different species: freshwater
species dominate at salinities lower than 5 (psu), brackish water species at salinities
from 5 to 20 and saltwater species at higher salinities than 20 (Remane, 1934). The
salinity also influences the settling velocity of SPM, and hence water clarity (Secchi
depth): the higher the salinity, the greater the aggregation, and the higher the
sedimentation (Kranck, 1973, 1979). In CoastMab, this is expressed by a
dimensionless moderator for salinity (Ysal) operating on the settling velocity. The
effect of salinity is of special importance in estuaries where fresh and saltwater meet
and a zone of maximum turbidity occurs (Gebhardt et al., 2005). A new algorithm
relating the Secchi depth to SPM and salinity (from Håkanson, 2006) has also been
incorporated into CoastWeb.
2. SPM-values are used to calculate the Secchi depth, which in turn is important to
predict macrophyte cover and production of benthic algae. In the original CoastMab-
model for total phosphorus (TP) (Håkanson and Eklund, 2007), SPM is calculated by
a dynamic SPM-model. For simplicity, and because there is a close relationship
between SPM and TP, this version of CoastWeb has omitted the dynamic SPM-
model and uses a regression to predict SPM from dynamically modelled TP-
concentrations (Figure 15). It is based on annual data from 51 systems (data from
Lindström et al., 1999; Håkanson, 2006) and gives a high coefficient of
determination (r2 = 0.895). However, this regression is based on data from systems
with salinities lower than 15 so it may provide limited predictive power for systems
with higher salinities.

y = 1.561x - 1.639; r2 = 0.895; n = 51; p < 0.001

1.75

1.5

1.25

1
log(SPM) [mg l-1]

.75

.5

.25

-.25
lake data, salinity 0
-.5
coastal data, salinity 5-15
-.75
.6 .8 1 1.2 1.4 1.6 1.8 2 2.2 2.4

log(TP) [µg l-1]

Figure 15. The regression between annual SPM and TP-concentrations based on data from 51 coastal
areas and lakes
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 111

3. The chlorophyll-a concentration (Chl) is important in CoastWeb since Chl is needed

to predict phytoplankton biomass. If the aim is to use only CoastWeb, the simplest
approach is to use empirical data of Chl. However, if the aim is to study how changes
in phosphorus loading affect the foodweb, CoastMab should be linked to CoastWeb.
Calculating chlorophyll from nutrients is a fundamental concern in aquatic sciences.
Generally, Chl-values are predicted from temperature or light and nutrient
concentrations (Dillon and Rigler, 1974; Smith, 1979; Riley and Prepas, 1985; Evans
et al., 1996).
In this work, regressions relating monthly TP to monthly chlorophyll are used. A
local relationship (Håkanson et al., 2007) between chlorophyll and TP has been used
for Ringkobing Fjord, Denmark (see Table 4 and Figure 16, with and without a
smoothing function SMTH; see Håkanson, 1999). Note that modelled values are not
compared to the empirical mean values, but to uncertainty bands calculated as
median monthly values ± the uncertainty in the mean empirical value.
The regional regression in Table 4 is from Håkanson and Eklund (2007);
(SWT+0.1)/20) is the temperature moderator where 20°C is the summer mean
temperature for this regression. If no local or regional relationships are available, the
general approach in Table 4 may be used. This is an adaptation of a basic regression
for lakes [(0.28·CTP)0.96; from OECD (1982)], which is modified by a four
moderators. The calcium moderator (YCa) takes into account that systems with Ca-
concentrations > 10 mg/l are likely to have lower Chl-values relative to TP than
systems with lower Ca-concentrations (Håkanson et al., 2005). The morphometry
moderator, YDRchl, quantifies how the dynamic ratio (DR = √Area/Dm; Area in km2
and mean depth, Dm, in m) influences the relationship between TP and Chl. Systems
with DR > 2.45, are dominated by resuspension events of fine sediments (Håkanson
and Jansson, 1983). In such systems, benthic algae may be resuspended and included
in the water sample used for the chlorophyll analysis. YDRchl is given by:

If DR < 2.45 then YDRchl = 1 else YDRchl = DR/2.45 (35)

The temperature moderator [Ytemp= ((SWT+0.1)/20)] has already been mentioned.

The salinity moderator, Ysal, takes into account that the salinity influences the
distribution coefficient between dissolved and particulate P in a similar way as
calcium: the higher the salinity the lower the slope of the regression line between TP
and chlorophyll (Figure 5; Håkanson et al., 2007).
The relationship between Chl and phosphorus is also affected by the particulate
fraction of phosphorus (PF). In LakeWeb, monthly PF was set to 0.56 as a reference
value (Håkanson and Eklund, 2007), but in CoastWeb PF is affected by the
biouptake and retention of phosphorus in functional groups, eq. 36.

If SWT > 9 °C then PF = 0.56·(MSW + Mshort + Mlong)/MSW

else PF = 0.56·MSW/(MSW+ Mshort + Mlong) (36)

MSW, Mshort, Mlong are the amounts of TP [g] in the surface water, in functional
groups with short turnover times and with long turnover times. So, in CoastWeb,
112 Lars Håkanson and Dan Lindgren

dynamically modelled TP-concentrations can be used to predict chlorophyll using the

best available empirical regressions.
4. The volume of the deep-water (DW) zone, VDW, is not calculated from Awb·(Dmax-
Dwb)/3 (Awb = the area below the theoretical wave base in m2; Dmax = the maximum
depth in m; Dwb = the depth of the theoretical wave base in m), as it was in LakeWeb,
but from:

VDW = Awb·Vd·(Dmax-Dwb)/3 (37)

The previous expression works well for systems where the DW-zone has the form of
a cone, but for systems that are more U-shaped with Vd-values higher than 1, the
correction using the form factor (Vd = 3·Dm/Dmax) will provide a more realistic
estimate of VDW.
5. The moderator, YEh1, is used to express the oxygen stress on zoobenthos in
LakeWeb. In CoastWeb, it has been replaced by a more tested approach, which is
also used to quantify diffusion of phosphorus from sediments (Håkanson and Eklund,
2007):

If O2Sat > 50% then YEh1 = (2-1·(O2Sat/50-1)) else

YEh1 = (2-3000·(CTPA/1)·(O2Sat/50-1)) (38)

Figure 16. Modelling chlorophyll in Ringkobing Fjord, from modelled monthly TP-concentrations
(actual data and smoothed data) using the CoastMab-model (within CoastWeb) and the regression given
in eq. 2, compared to uncertainty bands based on median monthly values ± the uncertainty in the
empirical annual mean values (see Håkanson et al., 2007)
 Coastweb, a Foodweb Model Based on Functional Groups for Coastal… 113

CTPA is the modelled TP-concentration is accumulation-area (A) sediments. If CTPA is

higher than 1 mg/g dw, the dimensionless amplitude value (3000) increases, and
hence also the diffusion; if CTPA is lower than 1, the amplitude value decreases. The
following smoothing function has also been applied to provide realistic temporal
changes in the moderator for zoobenthos:

YEh = SMTH(1/YEh1, TZB, 1/YEh1) (39)

TZB is the turnover time for zoobenthos (Table 2). YEh is never permitted to attain
values < 0.

6. The dimensionless moderator expressing how low oxygen saturation in the DW-zone
(O2Sat in %) would influence the survival of zoobenthos in areas of erosion and
transport (ET-areas) has been modified from YEh10.25 to YEh10.5. This means that a low
O2Sat will more clearly reflect lower oxygen conditions also in the surface water.
7. The distribution coefficient regulating the prey fish consumption of either
zooplankton or zoobenthos has been changed from 0.5 in LakeWeb to DCZPZB =
0.5·Ysec0.2. For coasts, which generally have a higher water clarity than lakes, the
basic DC-value is modified by a Secchi depth moderator (Ysec;, eq. 40), that
compares the Secchi depth in the coast Secchicoast with that of a corresponding lake,
Secchilake.

If Secchilake > Secchicoast then Ysec = 1 else Ysec = Secchicoast/Secchilake (40)

Which, e.g., gives 0.5·20.2 = 0.57 (a diet of 57% zooplankton and 43% zoobenthos
consumed by prey fish) if Ysec is 2. The power (0.2) has been derived by calibration.
8. The moderator used in LakeWeb to reduce the predation pressure in very turbid lakes
(Yfish) has been set to 1, since Secchi depths lower than 1 m are rare in coastal areas
on a monthly basis (the ecosystem scale).
9. The amount of food (―sediment pool‖, FsedZB in kg ww/month) available for the
zoobenthos is not calculated in the same manner as in LakeWeb, but from
sedimentation of particulate phosphorus recalculated into sedimentation of organic
matter as food for the zoobenthos. This is done accordingly:

FsedZB = FAET·(1000/2)·1000·(100/(1-W))·0.67 (41)

FAET is the sedimentation of TP on ET- and A-areas in g dw/month (calculated

automatically in CoastMab from eq. 42). FAET is calculated from a function which
gives an annual smoothing of the monthly sedimentation on ET-areas and A-areas
(FSWET and FDWA in g TP/month):

FAET = SMTH((FSWET+FDWA), 12, (FSWET+FDWA)) (42)

From Håkanson (2006) it is assumed that SPM deposited on ET- and A-areas on
average has a TP-concentration of 2 mg/g dw. Multiplication with 1000 gives SPM
in kg dw/month. W is the water content of SPM (= 100·(g ww-g dw)/g ww) of SPM
114 Lars Håkanson and Dan Lindgren

calculated from eq. 43. Multiplication with (100/(1-W)) gives the amount of SPM in
kg ww/month. It is also assumed that 2/3 of the deposited SPM is available as food
for zoobenthos.

W = (1-0.0375·(ET/0.15-1))·75 (43)

When the fraction of ET-areas is 15%, W is 75% which is used as the default water
content of ET- and A-sediments in coastal areas (Håkanson et al., 1984). If the
fraction of ET-areas (with coarser materials), is higher, the calculated water content
of the SPM should be lower, which is given by eq. 43. If ET is 0.9, W is 61%.

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aurita medusae in the Kiel Bight and western Baltic. J. Mar. Sci., 51, 359-367.
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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 119-151 © 2011 Nova Science Publishers, Inc.

Chapter 4

FORM AND FUNCTIONING OF MICRO SIZE

INTERMITTENT CLOSED OPEN
LAKE LAGOONS (ICOLLS) IN NSW, AUSTRALIA

W. Maher1, K. M. Mikac2, S. Foster1,

D. Spooner1 and D. Williams1
1
Ecochemistry Laboratory, Institute for Appled Ecolgy,
University of Canberra, Bruce, ACT, Australia.
2
Institute for Conservation Biology and Environmental Management,
University of Wollongong, Wollongong, NSW, Australia.

ABSTRACT
ICOLLs are considered to be one of the most ecologically productive ecosystems on
earth. Similar to other coastal water bodies, ICOLLs lie at the interface of marine,
freshwater and terrestrial systems and therefore represent highly dynamic transition zones
between river/creek catchments and near-shore coastal waters. ICOLLs often act as net
sinks of land derived sediments and nutrients; mature systems are believed to act as a
source of organic material and nutrients to the adjacent sea. Suzuki et al., (1998)
describes ICOLLs as having unique structural and functional characteristics as a
consequence of their position in the landscape, thus having large spatial and temporal
variability in their environmental and (consequently their dependant) biological variables.
The focus for this chapter is micro size ICOLLs, classified as any coastal water
body that has:

(i) the presence of barrier beach, spit or series of barrier islands that can restrict oceanic
exchange;
(ii) a surface water area of less than 0.5 km2
(iii) the retention of all or the majority of the water mass within the lagoon during low
tide in the adjacent sea; and
(iv) the capacity of to remain brackish to fully saline either by percolation through and/or
overtopping through inlet/outlet channels.
120 W. Maher, K. M. Mikac, S. Foster et al.

ICOLLs can be viewed in a hierarchical manner, with the ocean and catchment
influencing other smaller scale processes. Characteristics of the catchment and oceanic
regimes influence water quality, tidal regime, stream flow, sediment delivery and seston
within an ICOLL. Flow regimes and sediment loads in turn affect ICOLL morphology
and sediment composition, such as nutrient status and organic matter composition.
Alterations in catchment flow can either increase the residence time of water within an
ICOLL increasing the susceptibility to eutrophication or decrease the residence time
possibly leading to nutrient limiting conditions. In turn, these attributes determine the
biological diversity and functioning of these systems.

1. INTRODUCTION AND DEFINITION

Intermittently Closed and Open Lake Lagoons (ICOLLs) are a common feature of the
NSW coastline, occupying approximately 92 % of all New South Wales estuarine waters
(Williams et al., 1998). ICOLLs are coastal bodies of saline water (Figure 1), either wholly or
partially separated from the adjacent sea, by one or more restricted inlets (Bird, 1967a, b,
1994; Mee, 1978). They are characterised as having largely varying salinities e.g. hyposaline
to hypersaline (Kjerfve, 1986, 1994; Bamber, 1998), and often as being stagnant and brackish
(ie: 5-20ppt) in nature (Ward and Ashley, 1989; Tagliapietra et al., 2009).
ICOLLs are considered to be one of the most ecologically productive ecosystems on
earth (Boynton et al., 1996). Similar to other coastal water bodies, ICOLLs lie at the interface
of marine, freshwater and terrestrial systems and therefore represent highly dynamic
transition zones between river/creek catchments and near-shore coastal waters (Edgar and
Barrett, 2000). ICOLLs often act as net sinks of land derived sediments and nutrients; mature
systems are believed to act as a source of organic material and nutrients to the adjacent sea
(Kjerfve and Magill, 1989; Cognetti and Maltagliati, 2000). Suzuki et al., (1998) describes
ICOLLs as having unique structural and functional characteristics as a consequence of their
position in the landscape, thus having large spatial and temporal variability in their
environmental and (consequently their dependant) biological variables. On the south eastern
coast of NSW they provide a habitat for commercially important fish stocks (Griffiths, 2001),
and are sanctuaries for many migrating demersal nektonic species (e.g. shrimps, crabs, spots,
flounders) that depend on shallow lagoonal habitats as nursery areas for early development
(Boynton et al., 1996).
Of all the systems that are inherent to the coastal environments, ICOLLs have the greatest
potential to become eutrophic (Comin and Valiela, 1993; Boynton et al., 1996; Menendez and
Comin, 2000). Reduced flushing, shallow waters, and often silt/clay sediment composition all
contribute to accelerate eutrophication. NSW coastal lakes are under immense pressure, and
almost all have been modified with approximately 60% classified as degraded and in need of
comprehensive or significant protection (HRC, 2002). One of the main problems associated
with this assessment was the lack of data for micro size ICOLLs along the south coast of
NSW, which highlight the requirement for future research priority.
To provide the focus for this chapter a micro size ICOLL will be classified as any coastal
water body that has:
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 121

(i) the presence of barrier beach, spit or series of barrier islands that can restrict oceanic
exchange;
(ii) a surface water area of less than 0.5 km2
(iii) the retention of all or the majority of the water mass within the lagoon during low
tide in the adjacent sea; and
(iv) the capacity of to remain brackish to fully saline either by percolation through and/or
overtopping through inlet/outlet channels.

Figure 1. Morphology and sediment facies of micro-size ICOLLs. A: Brackish Creeks (Wimbie Creek);
B: Broad Basins (Kianga Lake); C: Floodplain brackish creeks (Congo Creek)
122 W. Maher, K. M. Mikac, S. Foster et al.

Figure 2. Hierarchical effects in ICOLLs

ICOLLs can be viewed in a hierarchical manner; with the ocean and catchment
influencing other smaller scale processes (see Figure 2). Characteristics of the catchment and
oceanic regimes influence water quality, tidal regime, stream flow, sediment delivery and
plankton within an ICOLL (Kench 1999; Loneragan and Bunn 1999; Roshanka and
Pattiaratchi 1999; Cooper 2001; Roy et al. 2001). Flow regimes and sediment loads in turn
affect ICOLL morphology and sediment composition, such as nutrient status and organic
matter composition (Harris 2001b). In turn, these attributes determine the biological diversity
and functioning of these systems. Alterations in catchment flow can either increase the
residence time of water within an ICOLL increasing the susceptibility to eutrophication or
decrease the residence time possibly leading to nutrient limiting conditions (Cooper 2001).

2. PHYSICAL FEATURES
ICOLLs are located at the transitional zone between rivers and oceans and often act as
net sinks of land derived sediment and nutrient inputs (Kennish, 1986; Kjerfve, 1994).
ICOLLs may have one or multiple entrances to the sea that are intermittently open or closed
to the ocean (Kench, 1999). These shallow systems are often found behind barrier islands and
sand spits and are conspicuous physiographic features of continental land margin around the
world (Boynton et al., 1996).
The movement of sediment into these water bodies is part of an evolutionary process and
changes the morphology and bathometry of the ICOLL basin (Kennish, 1986). Accelerated
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 123

infilling caused by increased catchment sediment loads can sometimes ‗in fill‘ coastal
ICOLLs, although the isolation of the water body from the ocean is the true cause of their
demise (Hodgkin, 1998). The different stages of isolation of ICOLLs to the ocean have also
been attributed to differences in ICOLL volume and varying catchment discharges (i.e.
sporadic or consistent) (Hodgkin, 1998).
The location of the ICOLL entrance in relation to the inherent coastal features that shelter
them from prevailing wind and ocean waves is also an important physical aspect of ICOLLs
(Hodgkin, 1998). The formation of the barrier that restricts oceanic exchange is reliant on
shoreline drift of marine sands that accumulate at the entrance of the ICOLL (Kennish, 1986).
During high river discharges the barrier can be breached allowing tidal inflow and exchange.
Understanding of the ecological and hydrological consequences of these breaches within
south eastern Australian ICOLLs are limited (Pollard, 1994; Wiecek and Floyd, 2006; Gale et
al., 2007).
In Australia, ICOLLs are found where high wave energy, microtides (ie: tidal amplitude
<2 m), low fluvial discharge and low coastal relief dominate (Bayly, 1971; Digby et al.,
1999). These oceanographic and terrestrial forces act synchronously to produce ICOLLs
(Bird, 1967a, 1994; Digby et al., 1999). In Australia, ICOLLs are noticeably absent on
coastlines characterised by high retreating cliffs e.g. Great Australian Bight, and where
macrotides dominate e.g. Northern Australia (Bird, 1994; Digby et al., 1999). Bird (1967a)
demonstrated that ICOLLs are well represented throughout the southern seaboard of
Australia, and although a great variation in lagoon morphology occurs, similar general
physico-chemical and biological processes operate in most south eastern Australian ICOLLs.

3. MORPHOLOGY
ICOLLs display high morphological variability (Figure 1 and 3), and have been
previously described as either brackish creeks (Stanton et al. 1999), or barrier lagoons (Bird
1994; Kjerfve 1994; Cooper 2001). Brackish creeks are typically narrow creeks with a single
entrance to the ocean, usually with a sand bar built up to around the high tide level (Stanton et
al. 1999). Brackish creeks are also usually narrow shallow channels that have a small surface
area (Stanton et al. 1999; Mikac et al. 2007). Barrier lagoons on the other hand can have
single or multiple entrances with a narrow entrance opening out to a larger shallow
lagoon/lake (Kjerfve 1994).
Digby et al. (1999) and Gregory and Petrie (1994) described numerous physical
characteristics that can be easily measured to define the morphology of estuaries, some of
which are pertinent to ICOLLs (e.g. Haines et al. 2006). The morphological features that best
classify micro sized ICOLLs on the south east coast of New South Wales are:

Cross sectional ratio – ratio of average width of the ICOLL to the average width of the
mouth. Describes the general shape of the lagoon i.e. values <1 indicate a narrow
entrance opening out into a wide lagoon, whereas values >1 indicate a wide entrance
narrowing toward the back. ICOLLs with a value <1 would tend to restrict tidal flow
when open while ICOLLs with values >1 would facilitate tidal flushing (Gregory and
Petrie 1994).
124 W. Maher, K. M. Mikac, S. Foster et al.

ICOLL surface area (km2) – Measurement of the surface area of the ICOLL (Digby et al.
1999).
Length to width ratio – length to width ratio is an indicator of the geometry of the ICOLL
i.e. long and narrow to short and wide (Gregory and Petrie 1994).
Fluvial flow – Fluvial flow is a ratio of mean annual rainfall runoff to the volume of the
lagoon. Fluvial flow is an indication of the ICOLLs buffering capacity i.e. ICOLLs
with low fluvial flow have smaller volumes of water entering from the catchment in
comparison with the ICOLLs volume therefore, expected changes in the water
characteristics (salinity) would be attenuated (Digby et al. 1999). Fluvial flow is
calculated using the equation:

FF = (P × A × Ceff) ÷ V

Figure 3. Cross sections of the berm (entrance channel), middle and basin in ICOLLs. A: Brackish
Creeks (Wimbie Creek); B: Broad Basins (Kianga Lake); C: Floodplain brackish creeks (Congo Creek).
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 125

Where FF is fluvial flow; P is the mean annual precipitation; A is the area of the
catchment under a single land use; Ceff is the rainfall runoff coefficient for the land use; V is
the volume of the ICOLL.
Three main morphologies are present in ICOLLs of the southeastern coast of NSW, and
have been classified based on their physical features as brackish creeks, lake lagoons and
floodplain lagoons (Figure 1). The morphology of ICOLLs is a reflection of the topography
of the catchment. Brackish creeks characteristically have high cross sectional ratios and high
fluvial flows, which together with their small water volumes have little capacity to attenuate
inputs from the catchment or the ocean. Brackish creeks have pronounced boom bust cycles
and are highly variable environments in respect to their water quality (Foster, 2002; Mikac et
al. 2007). Brackish creeks tend to occur in coastal environments with steep catchments with
little to no flood plain, these are the most common type of ICOLL occurring on the south east
coast of NSW. Lake lagoons characteristically have large surface areas and high length to
width ratios and low fluvial flows. Lake lagoons are the most stable type of small ICOLL (i.e.
<0.5 km2) in respect to their water quality as they have greater buffering capacity due to their
large water volumes, which acts to attenuate inputs (i.e. smaller oceanward openings in
relation to their body and low fluvial inputs in relation to their volume). Lake lagoons
typically occur in moderately sloped catchments with some flood plain development.
Floodplain lagoons occur in large catchments with low catchment slopes and moderate fluvial
flows. These ICOLLs are long and sinuous along their length and have well defined
floodplains. Floodplain lagoons tend to be flanged with the seaward opening larger than the
ICOLL body, causing greater tidal influence when the ICOLL is open to the ocean.
Many of the processes involved in the geomorphological evolution of ICOLLs are similar
to the processes involved in river systems (i.e. floodplain development) (Vannote et al. 1980).
Lake lagoon ICOLLs would be classified as being in the early to middle stages of
geomorphological evolution and flood plain ICOLLs in the latter stages (Digby et al. 1999).
It would be difficult to place brackish creeks into a geomorphological class due the lack of
floodplain development and depositional features (Digby et al. 1999). Cooper (2001), agues
that scouring during flood events would result in the removal of much of the accumulated
sediments “thus resetting the evolutionary clock”. It can be expected that flood events will
occur with more frequency in steeper catchments (i.e. greater fluvial flow), it would be
anticipated that brackish creeks would tend not to follow the accepted hypothesis of
shallowing with age (Roy et al. 2001).

4. CATCHMENT CHARACTERISTICS AND

HYDROLOGICAL PROCESSES

4.1. The Influence of Catchment Characteristics on ICOLLs

Catchments can be viewed as functional geographic units that integrate a variety of

environmental processes and anthropogenic effects on the landscape (Post and Jakeman 1996;
Aspinall and Pearson 2000). Both Edgar and Barrett (2000) and Harris (2001b) found that
changes in land-use within coastal catchments affected both the quantity and quality of
material entering estuaries. Estuaries form the terminal point in a catchment where all water
126 W. Maher, K. M. Mikac, S. Foster et al.

leaves the river system and enters the ocean (Frissell et al. 1986). In this respect estuaries
form the interface between the terrestrial and oceanic environments (Edgar and Barrett 2000;
Cooper 2001). ICOLLs are often separated from the ocean by a barrier of sand, and during
periods of freshwater input from the catchment, act as sinks for all the products exported (e.g.
sediment, organic matter, nutrients and pollutants) (Kench 1999). As such, catchment exports
play a vital role in the health and function of ICOLLs (Heap and Harris 2002). Changes in the
amount of sediment, organic matter and nutrients will affect the functioning of these
ecosystems, by altering their physical, chemical and biological nature (Hopkinson Jr and
Vallino 1995; Harris 2001a, b; Cooper 2001).
The physical features of a catchment such as slope, land cover, soils types, drainage
density, shape and size of the catchment, as well as urban infrastructure govern the movement
of water and associated constitutes (i.e. sediment, nutrients and organic matter) through the
catchment (Calow and Petts 1994; Post and Jakeman 1996; Harris 2001b; Jennings and
Jarnagin 2002). The volume and velocity of water through the catchment is crucial in
determining the morphology of ICOLLs, such as the shape of the water body, entrance
morphology, internal depositional characteristics and the opening and closing regimes of the
ICOLL (Bell and Edwards 1980; Sklar and Browder 1998; Cooper 2001, Roy et al. 2001).

4.2. Catchment Hydrology

Australia is the driest inhabited continent, with a large variation in runoff compared to the
rest of the world. Many of Australia‘s rivers and streams are ephemeral. Hydrographs often
show a rapid rise in stream level followed by a sharp decline with long periods of little or no
flow (Croke and Jakemen 2001). ICOLLs receive most of their freshwater input during high
rainfall events (Pollard 1994).
As a result of their small catchment areas, ICOLL inlets are often blocked for extended
periods by sand deposited by wave action. They are only open when there is a sufficiently
large storm where storm water inflow raises the water level such that the berm is breached or
when there are large waves overtopping the berm. The unpredictable nature of rainfall on the
South Coast of NSW results in erratic opening of ICOLLs. The frequency and magnitude of
rainfall events determines the frequency of entrance opening. Under low stream flow
conditions, water inputs are balanced by water losses through evaporation and seepage and
the entrance remains closed (Figure 4a). Wave energy will maintain the berm and over
washing will top up lagoons and maintain brackish water conditions. Storm events of
sufficient magnitude will incise a channel and cause the berm to breach (Figure 4b). The
depth of incision will determine how much of the ICOLL is drained. Wave action will
normally re-establish the berm within 1-2 weeks and the lagoon water level will remain low
unless refilled by runoff or tidal exchange (Figure 4c).
Streams and rivers serve as rapid conduits for water and anthropogenic nutrients to
estuarine and coastal marine environments (McMahon, 1998; Smith, 1999). Slope determines
the velocity of the surface runoff that governs the erosive potential and the transport capacity
of the flow (Lepisto et al., 1995; Croke and Jakeman, 2001). Hill slope erosion across
Australia has increased 100-fold in historical times as a result of catchment clearing and
agricultural land use (Prosser, 2001). Smaller catchments are often steeper which tends to
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 127

induce greater sediment movement and subsequent sediment yield. During periods of high
rainfall and runoff, exports of sediment, nutrients and organic matter tend to be higher (Harris
2001a, b). This often causes characteristic sediment plumes from the river into the ocean from
estuaries, however, as ICOLLs are closed for the majority of the time, these sediments and
associated material are trapped within the ICOLL and can have a great affect upon the water
quality and sediment composition within the ICOLL.

Figure 4. ICOLL hydrology. A: ICOLL full; B: Berm breeched; C: Berm rebuilt, ICOLL drained
(Wimbie Creek)
128 W. Maher, K. M. Mikac, S. Foster et al.

5. PHYSIOCHEMICAL FEATURES
The physicochemical composition of ICOLLs is highly variable (Figure 4) depending on
runoff, wave action and whether the ICOLL entrance is open or closed (Mikac, 2001; Foster,
2002). The period of closure will also influence water composition (Wiecek and Floyd, 2006;
Scanes et al., 2007).

5.1. Salinity and pH

Salinity regimes within ICOLLs depend on the ratio of fresh water inflow, overtopping,
tidal exchange and evaporation. If the entrance is closed and stream flow is low, ICOLLs are
generally brackish (15-25 % S) and increase in salinity over time if evaporation exceeds the
fresh water input. ICOLLs can also be stratified with a denser saline layer (36 % S) in deeper
areas. Increased stream flow can result in a surface layer of fresh water or a reduction in
salinity. It is common to find a lens of nearly fresh water (8-10 % S) over a deeper layer of
brackish water (16-25 % S). Once the berm is breached, the ICOLL can become completely
fresh although saline layers in deeper areas will persist. Depending on how long the entrance
is open, tide height and storm activity, salinity can vary from brackish to sea water due to
over washing and tidal exchange. pH will also change with variations in storm water inflows
and salinity. Fresh water pH varies between 5.5-6.5 while brackish water tends to have a
similar pH to sea water (pH 8).

5.2. Temperature

The temperature of the bulk of ICOLL water generally reflects the ambient air
temperature and varies seasonally from 5 - 40 oC. However, overtopping or filling by
seawater can substantially modify water temperature depending on the ambient seawater
temperature. Seawater temperature along the South Coast varies from to 11 -21 oC and
doesn‘t follow a seasonal pattern. Thus ICOLL water temperature will be highly dependent
on if the ICOLL is open or closed. the period of closure and prevailing sea water temperature.
Similarly, water temperature of the deep saline layer, if present, will be also depend on the
ambient seawater temperature. These deep saline layers can be warmer than the overlying
water depending on the seawater temperature, ambient air temperature and decomposition of
organic matter, which generates heat.

5.3. Dissolved Oxygen

Dissolved oxygen concentration is also highly variable depending on the source of the
water, ambient temperature, water stratification and biological activity. Normally if ICOLLs
are open or surface flow is occurring, dissolved oxygen concentrations are 40-100%
saturation. Over washing of seawater raises the oxygen levels, as seawater is generally 100%
saturated with oxygen. Catchment runoff brings water in that is oxygen saturated but also
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 129

brings in organic matter that through respiration lowers oxygen concentrations. On closure,
ICOLLs oxygen concentrations can vary from 0-140 % saturation. Over a 24 hour period,
oxygen concentrations can drop to 0 % saturation at night especially if a deep stratified saline
layer is present, and depending on the presence of algae recover to 50-80 % saturation during
day light hours. Prolonged deoxygenation will led to the mortality of organisms while
hypoxia (< 10% saturation) will effect growth, feeding and metabolic rates (Gray et al. 2002).
Many ICOLLs have extensive mats of benthic attached algae during summer. In shallow, non
turbid ICOLLs, oxygen concentrations can become supersaturated (100-140%) due to algae
photosynthesis.

5.4. Nutrients

As most nutrients enter ICOLLs bound to suspended particulates, the concentration of

dissolved phosphorus (< 1 g/l), dissolved nitrogen (5-10 g/L) and ammonia (2-10 g/L) are
normally low (Mikac, 2001; Foster, 2002; Mikac et al., 2007). Inputs of dissolved nutrients
from septic sewage systems and sewer overflows during periods of high rainfall can result in
short lived elevation of nutrient concentrations (P: 3-5 g/L; N: 20-30 g/L) especially
ammonia (20-90 g/L). Low water column nutrient concentrations limit phytoplankton
growth such that attached benthic algae are the most common algae growth (Nozais et al.
2001).

5.5. Colour

During periods of low flow, ICOLLs are generally non-turbid and highly coloured from
the release of tannins from decomposing organic litter. Together with the low soluble nutrient
concentrations, tannins may limit phytoplankton growth. We have shown in our laboratory
that the growth of algae species such as Chaetamorpha, Oscillatoria and E. ralfsii are
inhibited by highly coloured water derived from tannins (Dalton et al. unpublished).

6. SEDIMENT COMPOSITION

6.1. Grain Size

Patterns of sedimentation in coastal water bodies are highly heterogeneous and vary
according to hydrological processes e.g. river discharge, tidal flow and catchment inputs
(Dyer, 1979). Bird (1994) proposed a general sedimentation model for ICOLLs. This model
suggested that coarser material e.g. sand and gravel, is deposited as the river/creek enters the
lagoon, while the finer sediment e.g. silt/ clay, is carried out into the lagoon and deposited
throughout the central basin.
Sediments enter coastal lagoons from oceanic and fluvial sources (Bird 1967b; Kennish
1986). The terrestrial and coastal geology influence the types of sediments available for
transport (Thornton et al. 1995). A number of factors can affect the transport and spatial
130 W. Maher, K. M. Mikac, S. Foster et al.

distribution of sediments in ICOLLs e.g. salinity, surface runoff, tidal influence (Dyer 1979;
Thornton et al. 1995; Kench 1999). In general, coarse sediments of fluvial sands and gravel
are deposited where the river meets the lagoon, the finer sediments of silt and clay are carried
further and, through the process of flocculation, deposited within the central basin, with wave
action carrying oceanic sand into the mouth of the lagoon (Dyer 1979; Bird 1994). Sediments
are a depository for organic matter, nutrients and contaminants (Thornton et al. 1995).
The sediments in microsize ICOLLs consisted mainly of sand at the seaward end with
increasing silt upstream (Figure 1). This is typical of south eastern Australian coastal lagoons
(e.g. Allan et al., 1985) from which marine sand is transported (and eventually deposited) into
ICOLLs by ocean currents and wave action (Owen, 1978). However, Mikac et al. (2007)
found that the ICOLLs in catchments dominated by urban development had greater %
silt/clay. Silt/clay is a covariate of urbanisation, where % silt/clay increases as urbanisation
increases (Edgar and Barrett, 2000). Hume and McGlone (1986) have shown that the
deforestation of catchments for urban development increases the peakedness and frequency of
catchment high flows and results in an increase in the loads of fine sediment deposited into
coastal water bodies. Once the catchment is developed the soil is stabilised, however, the
peakedness of flows increases further because of the development of sealed areas and
stormwater systems (Hume and McGlone, 1986). Stormwater systems, of urbanised areas in
particular, are known to carry large quantities of fine sediment, organic material, nutrients and
contaminants to coastal water bodies (Dennison and Abal, 1999). In addition, Mikac et al.
(2007) found that an increase in the % silt/clay of sediments was associated with an increase
in sediment total organic carbon, nutrient (total nitrogen and phosphorus) and trace metal
concentrations (lead, copper, cadmium and zinc). It should be noted that concentrations of
these nutrients and trace metals did not exceed benchmark levels as recommended by
Australian water and sediment quality guidelines (ANZECC/ARMCANZ, 2000). Rather, silt
and clay have a large sorption capacity and thus locations with greater % silt/clay have a
greater potential to bind and scavenge organic matter, nutrients and trace metals (Kennish,
1986; Arakel, 1995). In particular, fine sediments have an immense sorption capacity because
of their large surface area to volume ratio and high surface charge to mass ratio (Arakel,
1995). The effects of ICOLL opening and closing on the sediments of the system are vast. If
an ICOLL is closed for extended periods, the system will be subjected to greater influence of
land derived sediments (usually fine sediments) that accumulate in the absence of diurnal
tidal scouring and near coast sand deposition.

6.2. Nitrogen and Phosphorus

Phosphorus and nitrogen are considered macronutrients, as they are essential for
biological processes (Deeley and Paling 1999). Typically in uncontaminated ICOLLs,
nitrogen and phosphorus concentrations vary from 20-100 and 5-80 g/g respectively with
higher concentrations in silt than sand. Nutrients enter ICOLLs attached to sediments, humic
material or in organic matter, either through catchment runoff, inputs from the ocean,
precipitation or the decomposition of biota (Kennish 1986; Thornton et al. 1995). Most
nutrients entering ICOLLs are found in the finer sediments of silt and clay (Thornton et al.
1995; Harris 2001b). Nutrients can be reintroduced into the water column by chemical,
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 131

physical and biological processes such as changes in pH and redox, bioturbation and
bioirrigation (See Section 6.4; Thornton et al. 1995).
Under oxic conditions, phosphorus is usually bound with iron (Fe) in the sediments and
nitrate converted to nitrogen gas through the process of denitrification (Aston 1980; Heggie et
al. 1999). Under low pH and/or anoxic conditions phosphorus can be liberated from
sediments and nitrogen released into the water column as ammonia (Figure 5 and 6) (Aston
1980; Hatcher 1994; Thornton et al. 1995; Heggie et al. 1999). ICOLLs are generally
nitrogen limited, with increases in nitrogen shown to stimulate algal growth (Harris 2001b).
Nutrient concentrations within ICOLLs sediments have been shown to be highly seasonal and
ICOLL specific (e.g. Schallenberg et al., 2010).

6.3. Organic Matter

Organic matter enters estuaries both internally through the decay of fauna and fauna and
externally through inputs from the catchment (leaf litter fall, leaching of soils) and ocean
(seaweed, biota) (Kennish 1986). Typically in uncontaminated ICOLLs, organic carbon
concentrations vary from <0.01-10 % respectively with higher concentrations in silt relative
to sand. Large quantities of organic matter can enter ICOLLs during periods of high fluvial
inputs (Day 1981) and in some ICOLLs the extensive accumulation of dead seaweed also
occurs. Within estuaries organic matter is the primary food source for many benthic
organisms (Morrisey 1995). Large quantities of organic matter can adversely affect water
quality by producing anoxic conditions leading to sulphate reduction and the production of
hydrogen sulphide gas (H2S) (Burton 1976). Hydrogen sulphide per se, should not be viewed
as a problem as some polychaete species eg Capitella sp. require hydrogen sulphide as a
settlement cue (Cuomo, 1985).

6.4. Biogeochemical Nutrient Cycles

Benthic sediments in shallow coastal embayments (i.e. ICOLLs) are the primary site for
the mineralisation of organic matter (Fisher et al., 1982; Jorgensen and Revsbech, 1989;
Heggie, 1999). These processes are primarily mediated by bacteria and contribute, together
with catchment discharges, to the nutrient concentrations in the water column.

6.4.1. Nitrogen
Inorganic nitrogen species NO3- and NH3+ are the most important because they are readily
available for biological uptake (Herbert, 1999). Currently, the consensus is that denitrification
ie the release of nitrogen as nitrogen gas, in closed systems with restricted oceanic exchange,
plays a vital role in regulating, or removing, nitrogen out of the aquatic cycle (Figure 5). This
is especially apparent in shallow Australian coastal systems where denitrification is primarily
a sedimentary based process (Heggie et al., 1999).
132 W. Maher, K. M. Mikac, S. Foster et al.

Figure 5. Nitrogen cycling in response to organic carbon loading

 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 133

Figure 6. Phosphorus cycling in response to organic carbon loading

During the cooler months of the year, or when labile organic matter is unavailable,
bacterial metabolic activity is low, and the water column is well oxygenated. This situation
promotes deep penetration of oxygen into benthic sediments that is utilised by bacteria to
oxidize organic matter (ammonification), which is then oxidized further by nitrifying bacteria
134 W. Maher, K. M. Mikac, S. Foster et al.

to nitrate (nitrification). In the anoxic microzones, which are vertically and horizontally
distributed throughout the sediment profile, denitrifying bacteria reduce the nitrate to nitrogen
gas that is released to the atmosphere (denitrification) (Figure 5a). Under these conditions
biologically available nitrogen concentrations in the water column remain stable, and often
limit phytoplankton and microphyte production.
Once water temperatures increase and a source of organic carbon is available, the
metabolic activity of heterotrophic bacteria increases and oxygen in the sediment profile is
restricted to the surficial zone. Under these conditions, ammonification and nitrification is
reduced and denitrification ceases (Figure 5b). Alternate electron acceptors are employed by
the bacteria to mineralize the organic matter, and sulphate is the most likely source. Sulphate
reduction of organic matter releases ammonia to the water column, which is directly available
for biological uptake (Figure 5c). Large fluxes of ammonia to the overlying water column
occur that support algal blooms and cause fish kills.

6.4.2. Phosphorus
Organic carbon inputs also control the mobilisation of phosphorus from ICOLL
sediments into overlying water. During the cooler months of the year, or when labile organic
matter is unavailable, bacterial activity is low, and the water column is well oxygenated and
little phosphorus is released. Sediments are oxidised and phosphorus complexes with iron.
Thus phosphorus is effectively trapped in sediments (Figure 6a). When ‗fresh‘ labile organic
matter is deposited to marine sediments oxygen is consumed and phosphorus is released from
organic matter and iron oxide phases (Figure 6b). Under anoxic conditions H2S is formed and
reacts with iron-phosphorus complexes. The capacity of the sediment to retain the phosphorus
is drastically reduced and a larger phosphate fluxes occurs (Figure 6c).
The mineralisation of organic matter and desorption from inorganic complexes have been
identified as major sources of phosphorus for phytoplankton production in coastal marine
environments (Nixon, 1981; McComb, 1998).

7. BIOLOGICAL FEATURES

7.1. Food Webs

The biota of brackish ICOLLs comprises relatively few species when compared to stable
marine habitats (Hammond and Synnot, 1994). Salinity is the prime factor in determining the
types of organisms within ICOLLS. Organisms within ICOLLs need to cope with varying
salinity and usually are opportunists such as polychaetes and shrimps, adapted to exploit
space and resources following disturbances ie opening and closing regimes (Boesch, 1977).
Generally, food webs in micro size ICOLLs are detritus based relying on allochthonous inputs
from both terrestrial and marine sources (Hadwen and Arthington, 2006), as phytoplankton
abundance is low because of low water column nutrient concentrations and tannins (see
Section 5.4 and 5.5). Benthic communities dominate micro size ICOLLs with attached algae,
microphytobenthos (Figure 7) and meso- and macro invertebrates being the dominant
organisms (Figure 8). Fish that are mobile and efficient osmoregulators also thrive in ICOLLs
(Figure 9) (Hadwen and Arthington, 2006).
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 135

Figure 7. Typical algae and plants in ICOLLs

7.2. Algae and Plants

As ICOLLs are relatively unstable environments and considerable redistribution of sand

and sediment occurs, it is rare to find extensive seagrass beds or mangroves within microsize
ICOLLs. Where these do occur in ICOLLs, it is in stable areas in which sand or sediment has
accumulated and not remobilised. Fringing vegetation tends to be salt tolerant terrestrial
species such as sedge, Juncus and Salt Bush (Atriplex).
As mentioned in Section 5, phytoplankton abundance is normally low because of the low
water column nutrient concentrations (Nozais et al. 2001) and the presence of tannins.
Phytoplankton abundance tends to be higher in winter months than in summer months.
Phytoplankton species abundance will be a function of ICOLL pH. Although some species
grow well over a wide range of pH (6-10), some species growth rates are significantly
136 W. Maher, K. M. Mikac, S. Foster et al.

influenced by pH (Hinga, 2002) with pH changes of 0.1 units causing observable changes in
phytoplankton community structure. Any freshwater phytoplankton carried into ICOLLs die
at salinities greater than 8% S (McLusky, 1989). Also in some ICOLLs it has been found that
phytoplankton growth is governed by the opening and closing regimes of the system, with
some ICOLLs experiencing greater phytoplankton chlorophyll a concentrations during
closure with the opposite being found for others (Schallenberg et al., 2010). Nitrogen and
phosphorus limitation and/or light limitation were other factors that were found to alter
phytoplankton growth in ICOLLs (Everett et al., 2007; Schallenberg et al., 2010).
Benthic attached filamentous algae such as Enteromorpha sp. form extensive mats in
warmer months and decline in autumn. Microphytobenthos have been reported in the
literature to exhibit strong seasonal fluctuations and not to be inhibited by low water column
nutrient concentrations or light availability (Nozais et al 2001). Large populations of
microphytobenthos (diatoms and other micro algae) also occur in silty-sandy sediments up to
depths of 20 cm. These algae play an important role in maintaining the surface of sediments
and overlying water in an oxygenated state (Peckol and Rivers, 1996) and are an important
food source for macroinvertebrates.
Little information is known about algal recruitment, competition or predation, the effects
of disturbances and changes in pH, salinity and temperature in micro size ICOLLs. All of
these factors are known to cause changes in the distribution and abundance of phytoplankton,
filamentous algae and microphytobenthos (Hamilton et al. 2000). Processes are likely to be
different in different ICOLLs.

7.3. Soft Sediment Macrofauna

Soft-sediment macrofauna are marine invertebrates that live within the sediment bed that
are retained on 1 or 0.5 mm sieves (Snelgrove and Butman, 1994). It has been suggested that
the soft-sediment macrofauna when coupled with an assessment of their habitat parameters
may be used as reliable indicators of anthropogenic or natural disturbance (e.g. Warwick,
1986, 1993; Deeley and Paling, 1999). In the microsize ICOLLs of southeastern Australia,
Mikac et al. (2007) found a total of 20, 253 individuals belonging to 12 marine invertebrate
families (Figure 8). The macrofaunal communities of the five ICOLLs examined consisted of
polychaetes (Capitellidae, Nereididae, Sabellidae, Spionidae and Serpulidae), gastropods
(Haminoeidae and Hydrobiidae), bivalve molluscs (Galeommatidae and Mytilidae) an
amphipod (Melitidae) and isopod crustaceans (Cirolanidae and Sphaeromatidae). The
macrofaunal assemblages of the microsize ICOLLs examined by Mikac et al. (2007) were
typical of meso and macrosize ICOLLs in Australia (e.g. Hodgkin and Clark, 1988; Platell
and Potter, 1996; Edgar et al., 2000b).
The soft-sediment macrofaunal abundance and composition of an ICOLL is usually a
function of its size and opening and closing regime (Hutchings, 1999). Although not directly
examined by Mikac et al. (2007), opening and closing regimes are acknowledged as having a
significant effect on overall taxa richness and assemblage composition. In that, the opening
and closing regime is known to affect the habitat parameters (salinity, dissolved oxygen,
sediment grain size and organic carbon content) of the macrofauna and therefore have an
indirect effect. This is supported by Platell and Potter (1996) who show that not only does the
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 137

closure of Wilson‘s Inlet (a mesosize ICOLL in south-western Western Australia) prevent

recruitment of macrofaunal larvae into the system but also determines the salinity regime of
the water body.

Figure 8. Typical benthic macrofauna in ICOLLs

It is difficult to determine which specific abiotic variable is responsible for the pattern of
macrofaunal assemblages in micro size ICOLLs, however, the habitat parameters found to
best explain soft-sediment macrofaunal composition in large south eastern Australian ICOLLs
include water quality (salinity, dissolved oxygen) and physico-chemical sediment variables
(grain size, organic carbon content) (Weate and Hutchings, 1977; Hutchings et al., 1978;
Powis and Robinson, 1980; Atkinson et al., 1981; Poore, 1982; Robinson et al., 1982; Gibbs,
1986). More recent work conducted by Platell and Potter (1996) and Mikac et al. (2007) have
attempted to single out the habitat parameters of the macrofauna in micro- and meso- sizel
ICOLLs. Platell and Potter (1996) found that a greater number of macrofaunal species were
associated with sediment composition and also the biomass of an aquatic macrophyte Ruppia
megacarpa. In turn, Mikac et al. (2007) found that the macrofauna of five microsize ICOLLs
examined was largely a function of sediment composition. Where fine sediment and sandy
substrata dominated, opportunistic polychaete taxa e.g. spionids, capitellids, nereids, and
138 W. Maher, K. M. Mikac, S. Foster et al.

mollusc taxa e.g. hydrobiids and mytilids were numerically dominant. It is possible that these
opportunistic macrofaunal taxa occur in disturbed locations because of their ability to
reproduce quickly in unrestricted conditions afforded by new unexploited environments
(Grassle and Grassle, 1974; Pearson and Rosenburg, 1978; Barnes, 1989). In ICOLLs, where
large variability in abiotic variables is common, usually due to unpredictable opening and
closing regimes, it is not surprising to find taxa that have life history characteristics e.g. r-
selected species, that enable them to exploit such environments. Mikac et al. (2007)
demonstrated that microsize ICOLLs in NSW have similar macrofaunal taxanomic
assemblages as larger Australian ICOLLs. The macrofaunal assemblages are also governed
by opening and closing regimes, either directly, through macrofaunal recruitment when
ICOLLs are connected to the sea or indirectly, through the effect opening and closing exerts
on abiotic variables (i.e. water quality and physico-sediment quality) or macrofaunal habitat
parameters within these systems.

7.4. Fish

To date there are no publications on the ichthyofauna of micro size ICOLLs in south
eastern Australia. However, the ichthyofauna of meso size ICOLLs have been investigated by
Pollard (1994) and Griffiths (1999) and (2000). Both Pollard (1994) and Griffiths (1999)
found similar species in the six ICOLLs examined by the authors. Both authors show that
greater taxa richness and abundance of fishes occurred in the larger and more open of the
ICOLLs examined. Pollard (1994) studied Lake Conjola, Swan lake and Lake Wollumboola
(meso sized coastal lagoons) and found that the larger of these and the ICOLL that was open
the most (i.e. Lake Conjola) had the most species and also the greatest abundance of these
species. Pollard (1994) found species composition in the ICOLLs examined were similar to
permanently open estuaries in eastern Australia. Griffiths (1999) found that fish abundance
and taxa richness was a function of size and opening and closing regimes. In addition, the
larger of the ICOLLs examined by Griffith (1999; i.e. Lake Illawarra), which was connected
to the ocean more often, had a greater abundance of commercial and non-commercial species
than the smaller and less frequently open ICOLL examined. The most common fish found by
Griffiths (1999) in the three ICOLLs examined were Ambassis jacksoniensis (Lake Illawarra);
Pseudogobius olosium (Shellharbour Lagoon); and Atherinosoma microstoma (Werri
Lagoon). In addition, the commercially important species Mugil cephalus, Acanthopognus
autralis and Myxus elongatus were also found. As well, both Pollard (1994); Griffiths (1999;
2001) showed that ICOLLs are important nursery areas for juvenile fish of both commercial
and non-commercial significance. ICOLLs are also refugia as juvenile fish are protected from
open ocean predators during ICOLL closure.
Griffiths (1999) discusses the consequences of opening and closing of ICOLLs and
suggests that although the consequences of such events are poorly documented in Australian
ICOLLs (regardless of size), there is evidence that species composition and abundance are a
function of the duration, frequency and time of ICOLL opening that may coincide with the
recruitment period of a wide range of species and randomly increase the chance of other
species entering the ICOLLs. As discussed in section 1.1, near shore and land based coastal
processes determine the opening /closing regimes of ICOLLs. If these processes coincide
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 139

with recruitment periods of various fish species then ICOLLs that are connected to the sea are
available to be recruited into. This is supported by Griffiths (2001) who found that the
recruitment of Acanthopagrus australis occurred in marked phases when the ICOLL
examined was connected to the adjacent sea.

Figure 9. Typical fish species in ICOLLs

Consequently the spatial and temporal variability of fish assemblages and their
abundances within ICOLLs is often large because the patterns of assemblages in ICOLLs are
a function of the opening and closing regimes. Not only does an intermittent opening and
closing regime effect recruitment into the lagoon itself but also effects the general water
quality of the lagoon. That is, when the ICOLL is closed from the adjacent sea for extended
periods and freshwater versus saltwater inputs are greater, the resulting changed salinity
140 W. Maher, K. M. Mikac, S. Foster et al.

profile of the ICOLL will favour euryhaline species and be detrimental to stenohaline species.
The inherent variability in opening and closing regimes in ICOLLs is recognised as the
driving force that determines the fish assemblages of ICOLLs, regardless of size, in south
eastern Australia.

8. ANTHROPOGENIC CHANGES
ICOLLs are not isolated ecosystems but intimately connected or nested within adjacent or
larger systems (e.g. Frissell et al., 1986, See Section 4). ICOLLs represent systems that form
part of a continuum from rivers and creeks to lagoons; from lagoons to the sea; and from the
sea to the ocean (e.g. Vannote et al., 1980). These systems are inherently linked and thus a
natural or anthropogenic disturbance or perturbation at one level inevitably has an effect at
various other temporal and spatial scales within the system (Glasby and Underwood, 1996).
Human activity in coastal catchments has been directly correlated with increased rainfall
runoff and sediment loads (Hume and McGlone 1986; Harris 2001b; Jennings and Jarnagin
2002). Water carries particulate and soluble material through the catchment, into the coastal
zone (Petts 1984). Alterations in the physical nature of the catchment can increase or decrease
the amount of particulate and soluble material moving through the catchment, however,
increased movement of material normally occurs (Petts 1984).
The physical variability in ICOLLs is influenced by numerous factors whose effects
coincide with different catchment characteristics that drive this variability (Cooper 2001). The
morphology of ICOLLs increases the susceptibility of ICOLLs to changes in land-use (Heap
and Harris 2002). Due to the presence of a barrier, ICOLLs lack tidal flushing (Cooper 2001;
Heap and Harris 2002). This can lead to the build up of nutrients, sediments and other
contaminants, which in turn can affect the ecological function of the ICOLLs through reduced
sediment and water quality (Heap and Harris 2002).
The morphology of an ICOLL can have a profound effect on the symptoms associated
with eutrophication. The position of the entrance in relation to the shoreline drift can
influence the opening regime; the estero can influence the exchange kinetics between the
ICOLL and the adjacent ocean. Water residence time within the ICOLL influences the
accumulation of organic matter, high water residence time often correspond to increased
potential for eutrophication symptoms. Unlike permanently open estuaries which are flushed
diurnally (Kennish, 1986), ICOLLs are usually closed off from the adjacent sea and thus
susceptible to changes in land use practices in their catchments (Zann, 1995; Inglis and Cross,
2000; Mikac et al., 2007). It is widely accepted that anthropogenic activities effect estuarine
ecosystems and in numerous instances have resulted in large-scale alterations of their natural
communities (Edgar et al., 1998; Edgar and Barrett, 2000). Bucher and Saenger (1991)
showed that 70 % of the 738 coastal water bodies dominating the Australian coastline have
deforested catchments and associated poor water quality, yet they represent habitats with
moderate to high fisheries and conservation value.
More alarming is the recent trend in ICOLL degradation (Edgar et al., 2000; Edgar and
Barrett, 2000). Zann (1995) and Hutchings (1999) reported that mesosized ICOLLs of the
densely populated south eastern and western Australian coastlines are under immense threat
from the adverse effects of urbanisation.
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 141

8.1. Changes in Catchment Land-Use, Hydrology and Water Quality

It is well established that deforestation associated with urban or commercial development

increases the peakedness and frequency of catchment high flows and fine sediment runoff to
estuaries (Hume and McGlone, 1986). Once the catchment is developed the soil is stabilised
and although sediment runoff decreases, the peakedness of flows increases further because of
the development of sealed areas and stormwater systems (Hume and McGlone, 1986). This is
supported by numerous authors who have demonstrated that changes in land use have effects,
usually considered to be adverse, on the receiving system‘s physical, chemical and biological
components (Loughran et al., 1986; Hogg and Norris, 1991; Arakel, 1995; Zann, 1995;
Stromberg et al., 1998; Dennison and Abal, 1999; Foster and Lees, 1999; Harris, 1999).
Stormwater and sewage discharges from urbanised catchments contain fine sediments,
nutrients, organic material, heavy metals, pesticides, oils and hydrocarbons (Deeley and
Paling, 1999). Elevated concentrations of trace metals, toxic to fauna, are readily stored in the
sediments and act as an intermittent source of contamination (Arakel, 1995; Birch, 1996,
2000). Trace metals such as cadmium, lead, copper and zinc have become serious
contaminants throughout Australian coastal water bodies (Birch, 2000). Physical alterations to
catchments as a result of commercial, urban or industrial development e.g. impervious
surfaces, drainage systems etc., are exacerbated by urban non-point source discharges which
aid in the rapid deterioration of water and physico-chemical sediment quality (Aelion et al.,
1997; Corbett et al., 1997; Wahl et al., 1997; Dennison and Abal, 1999).

8.2. Changes in Biological Communities

Both natural and anthropogenic disturbances may affect the overall pattern of
macrofaunal assemblages temporally and spatially in an ICOLL. The habitat parameters
found to explain soft-sediment macrofaunal composition in south eastern Australian ICOLLs
include a combination of water quality and physico-chemical sediment variables (Weate and
Hutchings, 1977; Hutchings et al., 1978; Powis and Robinson, 1980; Atkinson et al., 1981;
Poore, 1982; Robinson et al., 1982; Gibbs, 1986; Mikac et al., 2007). As indicated in
previous sections of this chapter, the water quality and physico-chemical sediment variables
of ICOLLs are a function of opening and closing regimes and catchment activities i.e. land
use.
Numerous biotic indices may be used to summarise the response of organisms to
anthropogenic/natural disturbance and stress. Biotic indicators of anthropogenic or natural
stress or disturbance include ecological measures such as taxa richness, relative taxa
abundance, taxa diversity, biomass and size strata (Deeley and Paling, 1999). Indices of biotic
integrity are most popular for assessing anthropogenic disturbance/stress or ecosystem health
and three biotic metrics are commonly used: (1) taxa richness and composition including
indicator taxa e.g. capitellids, nereids and spionids are usually indicative of disturbed/
contaminated locations; (2) trophic composition or the proportion of taxa belonging to
different feeding groups e.g. the proportion of suspension feeders compared to deposit
feeders; and (3) mean abundance of individuals belonging to a particular taxonomic grouping
or feeding guild (Deeley and Paling, 1999). In microsized ICOLLs in southeastern Australia,
142 W. Maher, K. M. Mikac, S. Foster et al.

Mikac et al. (2007) reported a significant increase in spatial heterogeneity/variability of

macrofauna between control and impact (urban) locations. The author found that in impacted
locations there was a shift towards more opportunistic taxa e.g. polychaetes, compared to the
less opportunistic/conservative taxa found at control locations. Others have found that in
anthropogenically disturbed locations opportunistic polychaete e.g. spionids, capitellids,
nereids, mollusc e.g. hydrobiids (Pearson and Rosenburg, 1978) and mytilid taxa (Grassle and
Grassle, 1974; Desrosiers et al., 1990), numerically dominate.
The combined effects of urban/commercial/industrial development on the macrofauna of
coastal water bodies have been difficult to determine (Edgar and Barrett, 2000; Inglis and
Kross, 2000). However, numerous correlative and descriptive publications have provided
convincing evidence to demonstrate a direct link between changes in community composition
e.g. increase in opportunists usually deposit feeding polychaetes, and reduced water and
physico-chemical sediment quality e.g. organic contamination (Grassle and Grassle, 1974;
Pearson and Rosenburg, 1978) and trace metal contamination (Inglis and Kross, 2000).
The observed decline in suspension feeders and the increase of deposit feeders in organic
and/or contaminant rich sediments is widely accepted (Pearson and Rosenburg, 1978;
Warwick, 1986; Clarke and Warwick, 1994; Inglis and Kross, 2000). That is, there is a
change from large bodied, long-lived, iteroparous k- selected species to r-selected species
(MacArthur and Wilson, 1967; Pianka, 1970). The later are characteristically small bodied,
short-lived species that are able to reproduce quickly and readily colonise disturbed locations
(MacArthur and Wilson, 1967; Pianka, 1970).
The spatial distribution of environmental variables and contaminants within coastal water
bodies is variable, with the foci of accumulation occurring near major sources of
contamination or in depositional environments where fine sediments and organic matter
accumulate (Morrisey et al., 1994; Inglis and Kross, 2000). Inglis and Kross, (2000) proposed
that if contaminants are haphazardly distributed, changes in the soft-sediment macrofauna
will be characterised by an increase in the spatial variability of assemblages from degraded
sites. This tenet is based on work conducted by Caswell and Cohen (1991) who demonstrated
that in patchy environments, disturbance can generate heterogeneity both spatially and
temporally in local macrofaunal community structure (Caswell and Cohen, 1991). In the
absence of disturbance the once patchy and heterogeneous habitats converge to form a
uniform landscape (Caswell and Cohen, 1991). This is supported by Warwick and Clarke
(1993) who found a marked increase in variability among macrofaunal samples from
disturbed/stressed treatments. Therefore, the possible detection of habitat degradation,
identified as increased spatial variability, may be achieved using spatially nested experimental
designs that incorporate measures of variance within and among the effected locations or
habitats (Underwood, 1997, 2000; Krebs, 1999).

9. MANAGEMENT

9.1. Flood Management

Many ICOLLs are surrounded by urban areas and when development was approved often
no consideration of possible inundation during extreme rainfall events was considered.
 Form and Functioning of Micro Size Australian Intermittent Closed Open Lake… 143

Consequently some ICOLLS are artificially opened to prevent flooding of houses and
infrastructure such as roads and sewage pumping stations (Wiecek and Floyd, 2006). In these
situations, ICOLLs would probably have opened naturally, thus artificial opening will make
little difference to the ecology of ICOLLs. As well, flora and fauna found in ICOLLs are
often species that can tolerate natural or anthropogenic disturbances (artificial openings).

9.2. Water Quality

Changed land use in catchments will inevitably lead to increases in suspended solids,
nutrients and altered carbon inputs (see section 8 and 9.3). Most nutrients (excluding sewage
inputs) will be attached to or incorporated into particles and deposited in sediments. Micro
sized ICOLLs, even after severe storm events have low water column dissolved nutrient
concentrations and do not experience many phytoplankton blooms. Sediments are already
relatively rich in nutrients, thus the addition of nutrient rich sediment is unlikely to alter the
natural ecosystem balance. Potentially the greatest threat to ICOLLs is nutrient and reactive
carbon inputs from untreated sewage from leaking septic tanks and sewage overflows.
Reactive organic matter will interfere with the natural nutrient cycling processes in ICOLLs.
Denitrification (see Section 6.4.1) can cease and ammonia released to the water column. As
well, phosphorus can also be released to the water column (see Section 6.4.2). Consequently
dissolved nutrient concentrations will be increased and phytoplankton growth favoured over
the growth of benthic attached algae (Schallenberg et al., 2010). Ammonia is also toxic to
marine organisms especially fish. Deoxygenation caused by decomposition of reactive
organic matter can also lead to fish kills. Most ICOLLs have periods of being odorous due to
hydrogen sulphide production. This is a natural phenomenon, a result of naturally high
sulphide concentrations from sea water inputs and periods of anoxia. Sewage inputs would
lead to longer periods of anoxia and longer periods of excessive hydrogen sulphide
production. Erosion in catchments and mobilisation of sediment is also a threat to ICOLLs as
smothering of habitats and infilling may occur. However, as scouring of ICOLLs often occurs
when ICOLLs open, sediments are probably not as greater a threat as in poorly flushed
marine lake and barrier estuaries. ICOLLs are highly variable in their water quality even
when they are the same type of ICOLL and located in the same geographic area/region,
therefore it is imperative that each ICOLL be managed as a single entity rather than a series
of lagoons from a particular location (Scanes et al., 2007; Chuwen et al., 2009; Schallenberg
et al., 2010).

9.3. Conservation

A potential problem of deforestation of catchments and urbanisation is that the amount

and composition (from eucalypts to introduced grasses and other plant species) of organic
matter entering ICOLLs changes. Detritus based ecosystems such as ICOLLs are adapted to
specific types of organic matter thus fundamental changes in ecology may occur. Broad scale
clearing in catchments should be avoided and revegetation with native species encouraged
preventing drastic changes in organic carbon inputs and composition. Riparian vegetation
144 W. Maher, K. M. Mikac, S. Foster et al.

forms an important habitat in ICOLLs. Urbanisation leads to loss of riparian vegetation with
many ICOLLs having houses built within 5-10 metres of the water body. Reestablishment
and restoration of riparian buffer strips would aid in conserving biodiversity and prevent
erosion of banks and channel widening. As ICOLLs are breeding grounds and refugia for fish,
artificial opening of ICOLLs should be avoided as protection from open water marine
predators is a feature of ICOLLs. Fish seem to survive and thrive in closed ICOLLs as long as
ICOLLs do not become totally devoid of oxygen.

9.4. Amenity

As described in Section 9.2, odours due to hydrogen sulphide formation are often a
problem in ICOLLs. Odours are a natural phenomenon and exacerbated by anoxic conditions.
However, some hydrogen sulphide is required as a settlement cue for polychaetes (Cuomo,
1985). Opening the mouth of ICOLLs to allow flushing to occur can alleviate odours.
However, as mentioned above ICOLLs as refugia can be compromised. The community
probably should be educated as to why odours occur and the trade off between alleviating
odours and compromising biodiversity and breeding habitats. While ICOLLs are closed they
may look like they are in poor condition because of scum build up and algae growth. This is a
natural phenomenon and not a symptom of deterioration. Again, education is needed as to
what the natural states of ICOLLs are.

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Chapter 5

WATERBIRDS AS BIOINDICATORS IN COASTAL

LAGOONS: BACKGROUND, POTENTIAL VALUE AND
RECENT RESEARCH IN MEDITERRANEAN AREAS

Francisco Robledano Aymerich*

and Pablo Farinós Celdrán
Department of Ecology and Hidrology,
University of Murcia, Espinardo, Spain

ABSTRACT
Among the biological components of estuarine systems and other transitional coastal
waters, waterbirds are probably the group that has been monitored more intensively and
throughout longer time series, especially due to the use of citizen science. Moreover,
several authors have reviewed, organized and analyzed critically the role and potential
use of waterbirds as bioindicators. Recently, academic research has encouraged more
intensive monitoring of waterbirds in the context of bioindication in wetlands and coastal
waters. However, in the particular case of coastal lagoons, birds have received little
attention compared to research efforts directed to other taxa, ignoring their important role
as top predators and underestimating their contribution to various ecological processes.
Few studies have included waterbirds as integral components of the food webs in
lagoons, relating them to other biota. However, recent studies show that waterbirds
respond to changes imposed by a variety of stressors, constituting warning signals against
undesirable changes. Waterbirds can be used as bioindicators both at suborganismic and
at population-community-ecosystem levels. Either approach requires that the
relationships birds establish with habitats and with the ensemble of the lagoon‘s
biocoenosis are clarified. As these relationships and the bioindicator role of waterbirds
are established in more detail, stands out their usefulness as indicators of impairment in
coastal lagoons of similar characteristics, subject to similar impacts with time lags.
Studies on the waterbird community of the Mar Menor Lagoon (SE Spain) show the
long-term response of populations to variables related to eutrophication and biological

*
Corresponding author: E-mail: frobleda@um.es
154 Francisco Robledano Aymerich and Pablo Farinós Celdrán

changes (proliferations of jellyfish and changes in fish stocks). Studies based on

community variation in relation to internal environmental gradients of the lagoon, show
spatial responses that can be mapped, and provide a basis for building indices of integrity.
This is a relevant issue given the paucity of studies that explore and apply the indicator
value of birds in conservation and environmental evaluation, particularly in the
Mediterranean and elsewhere in temperate latitudes. Recent studies that integrate the
monitoring of different physico-chemical and biotic variables of the lagoon with
waterbird numbers and distribution, and research on waterbird trophic ecology based on
stable isotope analysis, aim at clarifying the role of waterbirds as top-down controllers in
the food webs of coastal lagoons. A role whose monitoring is also important from an
applied perspective, given the potential of some waterbirds like cormorants to become
conflicting species (through their interaction with fisheries). The application of these
monitoring schemes to other Mediterranean lagoons emerges as a valuable tool for
assessing and preventing changes in the ecological status of these systems with respect to
relatively undisturbed, reference conditions.

1. INTRODUCTION
Among the biota of estuarine systems and other transitional coastal waters (TW),
waterbirds are probably the group that has been monitored more intensively and throughout
longer time series (Crivelli et al., 1996; Delany et al., 1999; Gilissen et al., 2002; Wetlands
International, 2008). The use of citizen science has been crucial in this respect (Kushlan,
1993). However, the application of such datasets to ecological monitoring or bioindication
has been much more limited. Waterbirds have been the main criterion -and for a long time,
virtually the only available- for the designation of internationally important wetlands, with a
prominent role in the implementation of the Ramsar Convention (Morgan, 1982; Green et al.,
2002; Jackson et al., 2004). But quite often, once wetlands have been awarded the label of
Ramsar Sites, waterbird monitoring data have become mere ―success indicators‖ of the type
of management focused at bird populations and their preferred habitats. In most cases, this
success has been measured only in quantitative terms (number of birds). Or, at best, the
monitoring of some specialized bird species has lead to some form of biodiversity and
environmental health indication (Máñez et al., 2010).
Several authors have reviewed, organized and analyzed critically the role and potential
use of waterbirds as bioindicators (e.g. Peakall and Boyd 1987; Adamus 1996; Green and
Figuerola 2003; Gregory et al. 2003; Stolen et al. 2004; Rönkä et al. 2005; Amat and Green,
2010). Recently, academic research has encouraged more intensive monitoring of waterbirds
in the context of bioindication in wetlands and coastal waters (Hubina, 2008; Rönkä et al.
2008). However, in the particular case of coastal lagoons (CLs, hereafter), birds have received
little attention compared to research efforts directed to other taxa, ignoring their important
role as top predators and underestimating their contribution to various ecological processes
(Daborn et al., 1993; Comín and Hernández, 1997; Glassom and Branch, 1997; Steinmetz,
2003; Hahn et al., 2007; Rodríguez-Villafañe et al., 2007). Few studies have included
waterbirds as integral components of the food webs in lagoons, relating them to other biota
(Acuna et al., 1994; Žyydelis and Kontautas, 2008).
Recent studies show that waterbirds respond to changes imposed by a variety of stressors,
constituting warning signals against undesirable changes (Amat and Green, 2010; Mallory et
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 155

al., 2010). Waterbirds can be used as bioindicators both at suborganismic and at population-
community-ecosystem level (Kushlan, 1993). Either approach requires that the relationships
birds establish with habitats and with the ensemble of the lagoon‘s biocoenosis are clarified.
As these relationships and the bioindicator role of waterbirds are established in more detail in
the best studied lagoons, so will improve their usefulness for detecting impairment trends in
other lagoons of similar characteristics, subjected to similar impacts with different time lags.
Among the basic questions to which studies of waterbirds should respond, we will try to
examine to what extent current knowledge and studies in progress in Mediterranean CLs,
shed some light on the following:

Do waterbird metrics or indexes respond in a predictable manner to long-term changes in

the ecological conditions of CLs?
Do such metrics or indices track spatial gradients of ecological impairment inside CLs?
What is the spatial scale (habitat, site, landscape) at which species respond to
environmental changes affecting CLs?
Which combination of suborganismical and population-community-ecosystem level
bioindicators (sensu Kushlan, 1993) will produce the best scheme for waterbird-
based bioindication in CLs?

2. WATERBIRDS AS INDICATORS: POTENTIAL

USES AND RESTRICTIONS
The potential for using of waterbirds for assessing wetland quality is based on several
attributes which allow them to fulfil the properties of good indicators (Roomen et al., 2006;
Everard, 2008). Waterbirds are sensitive to changes in the composition and structure of the
wide range of habitats and landscapes they use; they occupy a high trophic position; they are
conspicuous and easily identifiable to species in the field and hence can be monitored without
greater methodological limitations; they enjoy a wide coverage through routine schemes of
coordinated monitoring (U.S. EPA, 2002; DeLuca et al., 2004; Stolen et al., 2004; Bryce et
al., 2005; Brazner et al., 2007). In particular, waterbirds show a close relationship with the
abiotic characteristics and food webs of inland aquatic ecosystems (Paszkowski and Tonn,
2006), which has spurred their integration in the studies of such systems (Kerekes and
Pollard, 1994 ).
Attributes of waterbird populations or communities (species composition, abundance,
reproductive success, habitat use) can provide information about other ecosystem
characteristics (trophic structure, hidrology, organic or chemical contaminants…) that are
more difficult to monitor (Stolen et al., 2004; Roomen et al., 2006). The use of waterbirds as
biological indicators has been often questioned by the lack of a measurable direct response to
changes in limnological variables (Adamus, 1996; Green and Figuerola, 2003). However,
monitoring waterbird populations, at least in a regional system or a wetland compex
(Adamus, 1996), provides a good signal of environmental change (Martínez et al., 2005). For
instance, several authors have observed a response of waterbird populations to changes in the
supply of nutrients from multiple sources, to both inland and coastal waters (Nilsson, 1985;
Raffaelli, 1999). The interpretation of such changes is complicated because waterbird
156 Francisco Robledano Aymerich and Pablo Farinós Celdrán

responses change depending on the stage within the process of eutrophication (Van Impe,
1985; Raffaelli, 1999; Van Eerden et al., 2005), and sometimes also in a taxon-specific way
(Rönkä et al., 2005).
Among other major limitations for the use of waterbirds as indicators, it can also be
mentioned the frequent lack of concordance or similarity between the diversity of waterbirds
and that of other organisms living in the same aquatic habitats (Amat and Green, 2010), for
which they are expected to act as surrogates (Stolen et al., 2004). High mobility and
instability in numbers within sites at different temporal scales (interanual to daily) can lead to
misleading conclusions about relationships of waterbirds with environmental conditions if
monitoring work does not account for this variability (Dodd and Colwell, 1996; Johnson and
Krohn, 2001; Roomen et al., 2006; Bolduc and Afton, 2008; Amat and Green, 2010).
Despite the limitations exposed, waterbirds have been shown to track environmental
changes at different temporal scales, and at different levels or organization (species,
communities) within ecological systems (Amat and Green, 2010). Basically ornithological
studies searching for trends in waterbird numbers and inferring local habitat changes as
explanatory factors (e.g. Lopes et al., 2005), while coming closer to the indicator approach,
usually lack the environmental dataset needed to support these inferences (Stolen et al.,
2004).

3. THE PARTICULAR CASE OF MEDITERRANEAN

COASTAL LAGOONS
As mentioned earlier, waterbirds have received little attention in CLs compared to
research efforts directed to other taxa (see e.g. Bachelet et al., 2000; Pérez-Ruzafa et al.,
2004; Arvanitidis et al., 2005; Basset et al., 2008), ignoring their important ecological role
and the relevant influence they can exert on ecosystem processes. Mediterranean CLs are not
an exception. This is surprising since Mediterranean wetlands, and especially lagoons, meet
several characteristics that make them particularly suitable for testing the response of
waterbirds to environmental pressures, due to the concentration of human activities and
population along its shores (De Stefano, 2004; Viaroli et al., 2005). Mediterranean CLs
receive through their watersheds the influence of intensively farmed and densely populated
areas, especially during the summer months when this semi-enclosed sea becomes the major
world‘s tourism hotspot (Vogiatzakis et al., 2006).
Although bird-based Indices of Biotic Integrity (IBIs) for terrestrial and aquatic
ecosystems have been developed worldwide during the last decades (O‘Connell et al., 1998,
2000; Canterbury et al., 2000; Bryce et al., 2002; DeLuca et al., 2004; Bishop and Myers,
2005; DeLuca et al., 2004), their application to Mediterranean TWs has been very limited,
and only Paracuellos et al. (2002) get close to the concept of bird-based assessment of
wetland condition, comparing the situation before and after the abandonment of
Mediterranean Salinas.
The European Union (EU) Water Framework Directive (WFD) proposes an indicator
system based on hydromorphological, physico-chemical and biological elements (flora,
invertebrates, fish) but ignores birds, despite being an important macroscopic component of
aquatic ecosystems, for: i) their contribution to their ecological integrity, in terms of
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 157

composition, structure, and functioning; and ii) their role as integrators and detectors of
ecological change. Composite bird indexes of integrity can also help to harmonize the WFD‘s
water-quality objectives with the biodiversity conservation objectives set by other EU
Directives (Birds and Habitats). Such assessment tools can be especially useful in complex
Mediterranean TW areas like CLs and their associated wetlands, where many conservation
and protection regulations overlap. Moreover, multispecies assessments of protected areas can
be a valuable tool, not only for its own zoning or management, but for the investigation of
human impacts on biodiversity at a wide array of scales (Devictor et al., 2007).

4. A TYPICAL MEDITERRANEAN EXAMPLE:

THE MAR MENOR CASE STUDY
Research carried out up to date on the waterbird community of the Mar Menor Lagoon
(SE Spain) shows the long-term response of populations and guilds, to proximate variables
related to eutrophication and other apparent biological changes (proliferations of jellyfish and
changes in fish stocks) whose ultimate causes are the intensification of agriculture and
urbanization (Pérez-Ruzafa et al., 2002; Alvarez-Rogel et al., 2006; García-Pintado et al.,
2007). Besides, recent studies based on community variation in relation to internal
environmental gradients of the lagoon (Farinós and Robledano, in press), display spatial
responses that can be mapped and provide a basis for building indices of integrity. In this
section we report on the main results, whether published or not, of such studies. The issues
dealt with in are relevant, given the scarcity of studies that explore and apply the indicator
value of birds to the conservation and environmental assessment of CLs, particularly in the
Mediterranean and elsewhere in temperate latitudes (some exceptions being, e.g.: Tamisier
and Boudouresque, 1994; Green, 1998; Ntiamoa-Baidu, 1998; Green et al., 2002; Paracuellos
et al., 2002; Hubina, 2008).
Let us first draw an outline of the environmental characteristics of the case study site
(Mar Menor CL), a hypersaline lagoon located in the coast of Murcia Region (Figure 1). At
135 km2, it is the largest CL of the western Mediterranean (Pérez Ruzafa and Marcos, 2003)
and has an average depth of 4 m. It is separated from the Mediterranean Sea by a narrow sand
strip (La Manga) almost completely reclaimed for tourism, and surrounded by an irrigated
agricultural plain of 480 km2 inside a total watershed area of 1.275 km2 also with dense urban
settlements (Figure 1). The waterbird community is one of the most important biological
components of the Mar Menor CL, included in the Ramsar List of Wetlands since 1994
(Robledano, 1998), and designated as EU Bird Specially Protected Area (SPA) and as
Barcelona Convention‘s Specially Protected Area of Mediterranean Importance (SPAMI)
since 2001. The lagoon experienced major physical and hydrological changes in the decade of
1970‘s due to the dredging of one of the inlts (Estacio) communicating it with the sea. This
increased the marine influence, starting a process of ―mediterraneization‖, i.e. smoothing the
sharp differences between the lagoon (hypersalinity, higher temperature, greater confinement)
and the open sea. Until mid 1980‘s the lagoon lacked any permanent watercourses flowing
into, but since then the Albujón Channel started to discharge a permanent flow of agricultural
drainage water, refuse from desalination and untreated urban wastewater (García-Pintado et
al., 2007). Total yearly flow has been recently estimated in 20 Hm3 of water whose
158 Francisco Robledano Aymerich and Pablo Farinós Celdrán

conductivity is usually between 8-11 mS/cm2, a brackish input into the hypersaline (33.6-46.2
p.s.u) main water mass (Lloret et al., 2005). There are also low-salinity inputs through several
minor channels, below-ground seepages and diffuse drainage.
Environmental datasets (predictors) were obtained from several official data, modelling
studies and intensive monitoring campaigns performed by different institutions and research
groups (see e.g. Rodríguez et al., 2005; Martínez et al., 2007). For more detailed information
on sampling procedures and statistical methods we refer to these papers and reports.
The basis of this research work are the winter waterbird census made between 1972 and
2005 in the framework of the International Waterbird Census (IWC), compiled for the Region
of Murcia by Hernández and Robledano (1991), Martínez et al. (2005) and Hernández et al.,
2006), and on more recent waterbird monitoring campaigns running along shorter periods but
with a more intensive coverage (Robledano et al., 2008; Farinós and Robledano, in press).
These datasets represent the source for the main ornithological response variables. Tables 1
and 2 present the most important species, in terms of abundance, included in such studies.

Figure 1. Geographical location of the Mar Menor CL

 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 159

Table 1. Wintering species studied in the Mar Menor CL classified “a priori” on the
basis of their taxonomic, habitat and trophic characteristics. “Habitat specialization”
refers to the degree of restriction of each species to the lagoon main water mass;
“Feeding specialization” summarizes the variety of food types and foraging methods
used by each species. The characterization is based on personal work in the area plus
literature sources (Cramp, 1980). “Trophic guild” follows Ysebaert et al. (2000)

Familiy Species Habitat Feeding Trophic

specialization specialization guild
Common Coot Restricted (rarely
Gruidae Generalist Herbivore
Fulica atra outside lagoon)
Oportunistic (moves
Cormorant around widely to
Phalacrocoracidae Generalist
Phalacrocorax carbo terrestrial, aquatic
and marine habitats)
Great Crested Grebe Restricted (rarely
Specialist
Podiceps cristatus outside lagoon)
Piscivores
Podicipedidae Facultative
Black-necked Grebe (occasional
Generalist
Podiceps nigricollis movements to nearby
wetlands)
Red-breasted Merganser Restricted (rarely
Anatidae Specialist
Mergus serrator outside the lagoon)

Table 2. Species of the Mar Menor CL offshore waterbird community recorded in the
studies covering at least one complete year cycle (occasional species, i.e. those with
abundances ≤ 1 individual in any census, have been excluded). Main phenological status
is also indicated (W= species of the winter community; S=species of the summer
community)

Family Species‘ scientific name Species‘ common name Phenology

Podicipedidae Podiceps cristatus Great-crested Grebe W
Podiceps nigricollis Black-necked Grebe W
Phalacrocoracidae Phalacrocorax carbo Great Cormorant W
Laridae Larus michahellis Yellow-legged Gull W+S
Larus ridibundus Black-headed Gull W+S
Larus genei Slender-billed Gull W+S
Larus audouinii Audouin‘s Gull W+S
Sternidae Sterna sandvicensis Sandwich Tern W
Sterna hirundo Common Tern W+S
Anatidae Mergus serrator Red-breasted Merganser W
Ardeidae Egretta garzetta Little Egret W+S

In the most recent work (Farinós et al., 2009), three groups of environmental variables
were used: descriptors of physico-chemical conditions (nutrients), biological conditions
(ichthyoplankton species composition, total ichthyoplankton abundance and chlorophyll ―a‖),
and variables expressing distances to shelter or disturbance elements (mainly islands and
airports, respectively).
160 Francisco Robledano Aymerich and Pablo Farinós Celdrán

4.1. Long Term Response of Waterbirds to Environmental Changes

Eutrophication is one of the main problems confronted by coastal ecosystems (Caddy and
Bakun, 1995). In the Mar Menor Lagoon, many research initiatives have attempted to gauge
the contribution of various causes and pathways to this process (Esteve and Martínez, 2003;
Delbaere and Nieto-Serradilla, 2004; Jiménez-Cárceles et al., 2005; García Pintado et al.,
2007), but most of them have been carried out on a short time or small spatial scale, and there
is a lack of studies on the long term responses of biodiversity to the biotic changes imposed
by eutrophication.
Martínez et al. (2005), Esteve et al. (2008) and Robledano et al. (in press) analysed the
relationship of waterbirds with locally measured or estimated environmental variables
(nutrient load, fish production, jellyfish blooms) related with the process of eutrophication,
and discussed the potential value of birds as indicators of the trophic status of the wetland.
They used linear regression and GLMs to relate the biomass of the five waterbird species that
compose the bulk of the lagoon‘s waterbird community to these variables. Since local
changes in waterbird numbers can obviously be linked to external influences, affecting their
populations globally, there was a need to collect information on the status of wintering
populations in higher-level biogeographical divisions (Lopes et al., 2005; Roomen et al.,
2006), an important issue when interpreting local trends in waterbird data (see e.g. Rendón et
al., 2008). In the Mar Menor studies, such influences were controlled through the use of a
biogeographical (Western Mediterranean) population index as a predictor, and by comparing
population trends at national and local scales (Martínez et al., 2005, Robledano et al., in
press).
The Red-breasted Merganser was the dominant piscivore during most of the decade of
1970. The Great Cormorant dominated the community most years since then, representing ca.
50% of the biomass except between 1988 and 1996 when other piscivores, including the two
Grebe species (Podiceps cristatus and nigricollis), dominate (Figure 2). Only the Great
Cormorant showed a significant relationship with its Western Mediterranean population index
(explaining almost 50% of the variation in local biomass), an effect that biased the global
positive response of the piscivore guild to nutrient load (NLD). Red-breasted Merganser
appeared relatively insensitive to nutrient enrichment, although it declined in the long-term.
The remaining species responded positively. NLD was a significant predictor of their biomass
when a 2-year lag was allowed, although this variable alone had a low explanatory power,
except for the Coot, for which it accounted for up to 59.5% of the variance. When temporal
phases were defined within the study period (Table 3), grebes (Podicipedidae) could be
identified as early warners of eutrophication, and herbivores (Coot) as a late-stage indicators
(Figure 2). Although eutrophication often causes a marked deterioration of seagrass and
macroalgal communities, apparently not beneficial for herbivores (Noordhuis et al., 2002), it
also can favour opportunistic macroalgae (Krause-Jensen et al., 2008), a source of food for
generalist herbivores like Coot (Perrow et al., 1997; Yallop et al., 2004). The proliferation of
such algae is already observed in some stretches of the lagoon‘s shoreline.
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 161

Figure 2. Top: Changes in the environmental variables that describe changes experienced by the Mar
Menor CL: estimated nutrient load (NLD-2, 2 year lagged), jellyfish numbers (JFGS-2, 2 year lagged)
and fish catch (FISH). The last variable is used as a surrogate index for fish productivity. Bottom:
variation of the relative contribution of different species and guilds to total biomass

Table 3. Main phases identified by the response of waterbirds to environmental

changes in the Mar Menor CL (modified from Robledano et al., in press)

1 2 3 4 5
1972-79 1980-87 1988-1995 1996-(97)-? ?-(1999)-2005
Nutrient Start and Regular Moderate Sharp increase Higher loading
inputs stabilization loading increase (fluctuant)
Fishing High but Very few data Fluctuant at Sharp decline Stable or
catches declining at the (probably intermediate fluctuant at low
end of period fluctuant at levels levels
(overfishing?) intermediate
levels)
Jellyfish Absent Absent Absent Incipient Dramatic
populations increase and
peak numbers
Water Dominance of Dominance of Increase of Decrease of Increase of
birds Mergus serrator Phalacrocorax+ Podicipedidae Podicipedidae herbivores
Low piscivore Mergus (maximum Dominance of (Fulica)
diversity relative Phalacrocorax Partial recovery
contribution) of
Maximum Podicipedidae
piscivore
diversity

The increase of piscivores along a period of declining fish catches could reflect a shift in
fish community composition or structure that favours their feeding preferences. It is possible
162 Francisco Robledano Aymerich and Pablo Farinós Celdrán

that piscivores select prey types or size classes other than those commercially exploited
(Liordos and Goutner, 2007), which in the long term seem to be negatively affected by
eutrophication. This decrease in fish yield can also be a consequence of overfishing, leading
to a dominance of small fish (Van Rijn and Van Eerden, 2003), which creates good feeding
conditions for species like the Great Crested Grebe and the Great Cormorant (Gwiazda, 1997;
Smit et al., 1997; Van Rijn and Van Eerden, 2003). Other species can survive entirely on prey
different than fish (invertebrates), like Black-necked Grebe (Jehl, 2001; Fjeldså, 2004).
Jellyfish, the main top-down agent controlling the food web in the Mar Menor lagoon
(Pérez Ruzafa et al., 2002), seemed to modify the response of waterbirds to nitrogen load
during the years when the surplus of nutrients triggered a bloom of this gelatinous component
of zooplankton (mainly two species of allochtonous scyphomedusae, Rhyzostoma pulmo and
Cotylorhyza tuberculata, recent colonisers of the lagoon). It has also been suggested that
jellyfish not only affect birds through nutrient removal, but also qualitatively modifying the
structure of the food web.

4.2. Spatial Response of Waterbirds along Coastal Lagoon Gradients

From October 2006 to March 2008, Farinós and Robledano (in press) studied the spatio-
temporal structure of the offshore waterbird community of the Mar Menor CL in relation with
environmental gradients, in order to assess the role of waterbirds as integrative indicators of
the lagoon‘s bio-ecological status. Waterbirds were censused in 20 sampling stations
distributed according to an established zonation scheme based on the degree of confinement
(as defined by Guelorget and Perthuisot, 1983) and primary production (Pérez-Ruzafa et al.
2005), which was subsequently modified to match bird use at the landscape level.
Multivariate classification and ordination techniques (MDS and SIMPER) allowed to identify
indicator species and to display their association with relevant environmental vectors. Total
abundance of waterbirds increased latitudinally, southward in winter and vice versa in
summer. Greater abundance and diversity were found in the southern half of the lagoon in
winter, where grebes (62.8%), gulls (22%) and cormorants (15.1%) , and in the northern half
in summer, where gulls (80.1%) and terns (9.3%) where the dominant species.
Taking the sampling sections of figure 3 as an expression of its internal heterogeneity, the
MDS ordination of the samples showed that changes in community structure poorly reflected
the zonation established by Pérez-Ruzafa et al. (2005). A new spatial aggregation of samples
was derived from a ―waterbird zoning‖ classification, based on the level of similarity which
had a more coherent spatial expression (80-85% similarity). The new zones (Figure 3) can be
characterized from a combination of terrestrial influence (direct or indirect, depending on
their relative position regarding incoming channels and internal circulation), marine influence
(inner or outer, in relation to the open sea) and latitudinal position (north or south): IIIN
(indirect influence inner north), DII (direct influence inner), IIIS (indirect influence inner
south), IIOS (indirect influence outer south), IION (indirect influence outer north) and ODS
(other dispersed sampling stations). ―Indirect influence‖ refers to the effect of nutrient inputs
through internal circulation.
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 163

Figure 3. Map of the Mar Menor CL showing the original zonation of Pérez-Ruzafa et al. (2005), and
the sampling stations for the study of the offshore waterbird community and related environmental
characteristics (left). The map on the right displays the zonation based on the level of similarity of the
waterbird community among sampling stations (―waterbirds zoning‖), and the most representative
species of each zone . Modified from Farinós and Robledano (in press)

A distinct latitudinal distribution of particular species was observed (Figure 3), the
northern half of the lagoon‘s basin being characterized by Black-headed Gull (Larus
ridibundus) and the southern half by Great-crested Grebe (Podiceps cristatus) and Great
Cormorant (Phalacrocorax carbo). Such distribution patterns seem to respond to internal
functional gradients of the lagoon, but also to the physical structure of the habitat (e.g.
sheltered areas) and to the influence of human activities (direct disturbance or landscape
modification). Both internal and external factors related with waterbird abundance and
distribution are affected by human activity, as has been shown in other wetland ecosystems,
both at local and landscape scales (Kerekes and Pollard 1994; Noordhuis, et al. 2002;
Paracuellos, 2006; Paszkowski and Tonn, 2006; Hebert et al. 2009). While at community
level winter abundance and diversity seem to respond to gross levels of productivity,
individual species‘ responses are indicative of internal gradients in these and other factors.
The Great-creasted Grebe favours areas indirectly influenced by nutrient inputs over direct
discharge zones, which supports its role of early warner about eutrophication (already
recognized as such in the 1980s; see Hernández and Robledano 1997). The same preference is
shown by the Great Cormorant, proposed as an indicator of waters of intermediate turbidity
(Van Rijn and Van Eerden 2003; Rönkä et al. 2005). However, in the Mar Menor CL the
Great Cormorant should preferably be considered a background indicator of eutrophication,
given its mobility and landscape-scale response to increased productivity and complementary
food sources (irrigation ponds, fish farms). Compared with earlier work in the area
(Hernandez and Robledano, 1997), the main difference revealed by this study, apart from the
164 Francisco Robledano Aymerich and Pablo Farinós Celdrán

decrease of Anatidae, is precisely the increase of cormorants in the winter waterbird

assemblage.
The physical structure and geomorphology of the lagoon can help to explain the
differential use of the water mass by some species, e.g. Great Cormorants, which feed mainly
in the area with more islands where they can perch on small emergent rocky outcrops
(Reymond and Zuchuat 1995; Roycroft et al. 2007). Also, restricted to the island-rich part of
the lagoon is the Red-breasted Merganser, once a characteristic species of the Mar Menor CL
but now undergoing a steady decline in numbers (Martínez et al., 2005). The positive
numerical response of other piscivores in some phases of eutrophication suggests that changes
in the type and quality of food resources might explain the Merganser‘s opposing trend. The
species favouring the northern, island-free part of the lagoon, seem to be more dependent on
the influence of the Mediterranean Sea than on increased productivity of terrestrial origin. An
example is the Black-headed Gull, strictly favouring the more open and oligotrophic waters of
the north basin. This species has increased notably in the Mediterranean during the last
century in response to the increased variety and quantity of resources offered by man,
although this process has occurred at a landscape level (Blondel and Aronson, 1999). In the
Mar Menor CL, the zones favoured by Black-headed gulls do also display the greatest
diversity of trophic resources and are the most suitable for the species‘ foraging techniques
(Lewis et al., 2003).

Figure 4. Density distribution of Sandwich Tern (Sterna sandvicensis) in July 2007 (left graph) and
November 2007 (right graph)
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 165

Figure 5. Density distribution of grebes during 2006-2007 wintering season (left, December; right,
January): upper graphs, Great-creasted Grebe (Podiceps cristatus); lower graphs, Black-necked Grebe
(Podiceps nigricollis)

The results show that waterbirds can be incorporated in a monitoring scheme of the
lagoon, as integrative indicators of spatial gradients of environmental deterioration. As shown
by figures 4 and 5, mapping the densities of waterbird indicator species is a promising tool to
detect changes in the direction and/or intensity of the pressures (whether originated in the
mainland or in the seaward side of the lagoon), since these changes make themselves evident
along the main spatial gradients identified within the water mass. Coastal lagoons are
dynamic, wide open systems, and highly dependent on adjacent terrestrial and marine systems
with which a continuous exchange of materials and energy occurs (Pérez Ruzafa and Marcos
2003). A multitude of anthropogenic changes can modify the natural inputs from their
166 Francisco Robledano Aymerich and Pablo Farinós Celdrán

watersheds (Menéndez and Comín 2000; 2001; Herrera-Silveira et al. 2002; Contreras and
Warner, 2004).
The ecological status of CLs is determined, among other factors, by the confluence of
these opposing forces (terrestrial vs marine influence, natural processes vs anthropogenic
modifiying factors) that explain their heterogeneity, biodiversity and productivity (Tamisier
and Bouduresque 1994; Pérez Ruzafa et al. 2002). A landscape perspective is essential to
build sound conservation programs for waterbird assemblages (Guadagnin, et al., 2005), but
also to assess waterbird indicator potential and to devise associated monitoring schemes.
Hidrology, nutrient status, disturbance levels and other relevant features of the CL, can be
severely modified by actions carried out at the watershed level, in the watercourses and
hydraulic connections of the lagoon with adjacent ecosystems, in the shoreline habitats or its
immediate landscape surroundings, as well as by those occurring in the lagoon‘s littoral and
benthic communities.
The diversity of waterbirds in the Mar Menor lagoon increases with proximity to the
Mediterranean Sea, a trend already found for other animal groups (Rosique 2000) and that
can be attributed to an increased diversity of food resources and feeding habitats. In a
comparative analysis of 40 Atlanto-Mediterranean coastal lagoons Pérez-Ruzafa et al. (2007)
found that fish species richness increased with lagoon volume and the openness parameter,
which characterizes the potential influence of the sea on general lagoon hydrology and is
related to the total transversal area of the inlets connecting the lagoon to the sea. On the other
hand, the number of species decreased exponentially with the phosphate concentration in
water, and fishing yield increased with the chlorophyll a concentration in the water column
and exponentially with shoreline development. Since waterbirds seem to respond well to
changes in these parameters within the lagoon, processes of such importance for the system as
the increase in marine influence (the so-called "mediterraneization") or the eutrophication
caused by discharges of urban origin, can be traced through waterbird monitoring.
In contrast to other biota of these transitional water ecosystems, birds have the capacity to
integrate in their responses the combined effects of purely physical and/or trophic influences,
plus human deterioration of habitats by direct disturbance or through the modification of the
landscape setting (Rosa et al. 2003; McKinney et al. 2006; De Luca et al., 2008). Since
anthropogenic impacts on the lagoon from different spatial scales (watershed, immediate
landscape, shoreline, lagoon sections) act through relatively discrete and well-referenced
paths, the distribution of waterbirds within the lagoon emerges as a potential barometer of the
system‘s internal response to these pressures.
Although biologically meaningful and statistically supported (Erwin and Custer, 2000;
Van Strien et al., 2009) such a distributional response to a complex syndrome of ecological
changes can still be regarded as too general or vague if our interest is to develop a
scientifically sound and practical wildlife indicator (Stolen et al., 2004). The next step needed
is thus to discern the specific CL attributes to be indicated (e.g., nutrient status, habitat
structure, biodiversity), and to state a model of how the proposed waterbird indicator will
respond to perturbations of the lagoon ecological status or functioning. This will allow to
upgrade indicators based on waterbird abundance distribution, or indexes built upon it, to the
types -among those distinguished by Van Strien et al. (2009)- with more strength in the
detection of anthropogenic impacts on the biodiversity of CLs (Figure 6).
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 167

Strong
TYPE 3 TYPE 4

¿How are specific ¿How is biodiversity

taxa responding to a responding to a
driving force? driving force?

Waterbird Multispecies
abundance conservation
Strength distribution value
of link to indexes
a driver Long term trends
in waterbird
populations and
guilds
¿How are specific ¿How is biodiversity
taxa doing? doing?

Weak TYPE 1 TYPE 2

Weak Ability to generalise findings to Strong

trends in biodiversty

Figure 6. Judgements of the examples of bird-based indicators studied in the Mar Menor CL, in the
framework of the tipology sketched by Van Strien et al. (2009). Arrows show the potential for
upgrading indicator types currently under development, along the scales of increasing strength depicted
by the axes

The decisions about urban planning and land arrangement for different uses (agricultural,
residential...), and about the spatial allocation of typical lagoon uses (recreation, transport,
fishing...) have also a direct influence in the levels of potential damage and disturbance to
biological communities (birds being in this sense particularly reactive), and indirectly through
an increased risk of nutrient and contaminants release. In this sense, watebirds ability to
respond quickly to changes in the levels of disturbance (Davidson and Rothwell, 1993;
Burton, 2007), to the spread of potentially harmful structures (fishing nets), to bioaccumulate
toxins or pollutants (Kushlan, 1993; Konstantinou et al., 2000), or to show symptoms of
disease (Newman et al., 2007), makes them irreplaceable monitoring tools.
The use of multispecies and multimetric indexes is another promising application of
research on indicators, to assess both ecological integrity and the interest for conservation of
discrete areas subjected to different levels of disturbance. In a first attempt to apply
waterbird-based indexes to assess the ecological integrity of different sections of the Mar
Menor shoreline, Robledano and Farinós (2007) selected bird metrics through a guild-based
approach, on the basis of shared characteristics of waterbirds‘ life history, distribution,
demography or behaviour. As a first test, composite Waterbird IBIs were calculated in two
contexts: i) an ensemble of littoral sites within a large coastal lagoon, representing a spatial
disturbance gradient; and ii) a series of waterbird records in this same wetland complex,
covering a temporal disturbance gradient. Bird data used were: i) mean waterbird density
calculated from 5 winter counts in 14 sites (500 m of shoreline x 1000 m towards the centre
of the Mar Menor lagoon, Figure 7); ii) winter waterbird census (made in january within the
International Waterbird Census, IWC).
168 Francisco Robledano Aymerich and Pablo Farinós Celdrán

Figure 7. Location of the sampling stations of the Mar Menor CL shoreline compared through the
calculation of waterbird-based Indices of Biotic Integrity (IBIs)

The spatial gradient of disturbance was described through a subjective index (DI-S)
created from a combination of stress factors (artificial/natural uses in the immediate land and
water surroundings, hidrological and/or hidrochemical alterations, presence of mitigation
factors like vegetation buffer zones). To validate it, an independent index of disturbance (DI-
ECELS) was calculated using a procedure adapted from the ECELS index of
hidromorphological and vegetation quality (ACA, 2006), which takes inverse values and is
scaled in the same terms than the DI-S index. The correlation between both indexes was
relatively high and significant (r Spearman = 0.76; p < 0.01).
Waterbird metrics were selected on the basis of the procedures established by Bryce et al.
(2002) and DeLuca et al. (2004). The first authors give scores to the species according to their
vulnerability to disturbance, classifying them as specialists or generalists in different
attributes (feeding habitat, foraging methods, breadth of diet, distribution range, migratory
character) - equaling specialization to greater sensitivity to changes in the wetland. The
second authors test the response of a quartet of metrics (number of species, number of
individuals, % species and % individuals) for each of these same attributes. A metrics is
selected when its response matches the hypothetical ―expected‖ response (i.e., metric values
decrease significantly as the level of disturbance increases.

Two separate indices were calculated based on each of these reference papers.

(a) The Bird IBIBRYCE was calculated from the scores of the selected metrics, multiplied
by 10 and divided by the total number of metrics, to keep it within a scale from 0 to
100.
(b) The Bird IBIDELUCA was obtained from a modification of the author‘s original
formula:
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 169

Table 4. Values of waterbird-based IBIs for different

sampling stations of the Mar Menor CL shoreline

S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 S12 S13 S14

IMBCDELUCA 17.75 17.00 17.19 17.14 17.00 17.83 17.19 16.79 16.40 17.50 15.75 15.75 15.75 19.63
IBIBRYCE 56.05 50.1 42.1 65 52.8 87.6 60.1 44.3 58.56 53.2 46.3 36.2 36.5 90.08
IBIBRYCE (1-6) 4 2 3 3 2 4 3 2 1 2 1 1 1 6
IBIDELUCA (1-6) 3 2 1 4 2 6 3 1 3 3 2 1 1 6

WIMBCI = Σ [(S IMBCI ] –4

/ SN)

Where SN is the total number of species detected in the wetland. The equation represents
the mean score of all the species present. Four is subtracted to ensure a scale that starts at zero
and is constant.
The values obtained for the two Bird IBIS in the different sampling stations shown in
Figure 7 are shown in Table 4.
In the two last rows of the table, the values of the indices have been scaled between 1-6,
considering the total range of variation, and shades of grey used to highlight those stations
better (darker) and negatively rated (lighter). Although not completely concordant, the results
can be interpreted in relation to the characteristics of the sampling stations, particularly the
habitat and landscape characteristics. The results are neither entirely consistent with those
obtained from the study of the community within the water mass of the lagoon (the so-called
"offshore" community). However, some similarities are evident, especially the high value that
reach the sectors most influenced by the connection to the Mediterranean. Sectors which, as
seen in the previous sections, must be considered of great importance for the overall bird
diversity of the lagoon.
When these same indices are applied at a long-term scale to the whole lagoon, the
indexes do not respond to known degradation processes (e.g. increase in nutrient loads or
decrease in fishing yields) that have affected the lagoon during the period in which they were
obtained. In the long run, none of the metrics that make them up seems to show a clear trend
of change, unlike to what happens when the same assessment procedure is applied at the
spatial scale. It seems that an individual species or taxonomic guild approach like that
presented in section 4.1 is best suited to the nature of the waterbird community of the main
water mass of a Mediterranean CL.
Although not implemented in the lagoon, multispecies indexes based in the conservation
value for birds (Pons et al, 2003; Paquet et al, 2006), have proved very useful when applied to
peripheral wetlands of the Mar Menor inner shore (Robledano et al., 2010). Also, a recent test
of such indices in restored coastal salt ponds (Farinós et al., 2009 a) has proven useful to
detect changes in bird conservation value along a process of nutrient enrichment. These
indexes, and some other bird metrics (abundance, diversity) fit bell-shaped response curves,
in apparent response to the initial improvement and subsequent deterioration of ecological
characteristics relevant to birds and other biodiversity of coastal saline habitats. The fact that
these relationships emerge in restored ponds equivalent to the low-salinity compartments of
solar saltworks (from which they have originated), is remarkable. The latter are aquatic
ecosystems sharing common characteristics with natural transitional waters ecosystems (like
CLs), whose study is of special interest to the WFD (Evangelopoulos et al., 2008). Therefore,
170 Francisco Robledano Aymerich and Pablo Farinós Celdrán

coastal lagoons seem an ideal field for the application of these assessment indices, already
tested in small-scale replicates.

4.3. New Approaches: Coupling Waterbird Studies with Other Biological

Monitoring Schemes

Recent studies that integrate the monitoring of different physico-chemical and biotic
variables of the Mar Menor with waterbird numbers and distribution, and research on
waterbird trophic ecology based on stable isotope analyses, are helping to clarify the links
between these top consumers and other trophic components of CLs. The firs studies also
point to the search of concordance among indicators, as a necessary step for the selection of a
suite of indicators to be incorporated into a multi-metric/multi-assemblage index of coastal
wetland condition (Brazner et al., 2007). The second ones will help to clarify the strength of
association of waterbirds with the CL basin versus their use of alternative or complementary
habitats.
In multivariate analyses relating waterbird community metrics (abundance, diversity)
calculated from spatially and temporally segregated counts (monthly census in discrete
sectors), with environmental variables recorded in the same sampling stations (Farinós et al.,
2009 b), some relevant relationships emerged, which deserve further study. In multiple
regression analyses (Table 5), total abundance of waterbirds showed a dependence on
seasonality and on the spatial gradient (positive coefficient with salinity and negative with
temperature). Nitrite had a positive effect on the wintering community diversity. The winter
community abundance showed also a negative relationship with ichthyoplankton (its increase
was associated with a reduction in the density of fish larvae), which indicates that waterbird
populations could regulate this throphic component in the lagoon (top-down control of the
food web).
These results were concordant, in global terms, with the species associations displayed by
a Canonical Correspondence Analysis (CCA) whose first axis (40% explained variance)
seemed to differentiate species based on their foraging and seasonal general preferences (with
piscivorous birds associated with frecuency of fishing nets). The second axis of this same
analysis (20% explained variance) differentiated species based on their specific preferred prey
and the tolerance to disturbance activities or elements.
The waterbird community shows a strong dependence on the seasonal and spatial
variation in the physicochemical properties of the lagoon‘s water mass, which determines its
response to the gradient of continental influence (in combination with the spatially
heterogeneous influence of the surrounding landscape structure and the extent of direct
human disturbance). This is mediated by specific food preferences, as waterbird abundance
seems not to respond directly to primary or secondary productivity (see also Farinós and
Robledano, in press), and waterbird populations could even exert a top-down control of the
food web.
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 171

Table 5. Summary of multiple regression models with waterbird metrics (total

abundance, species diversity) as response variable, and environmental or landscape
variables -recorded in the stations sampled by boat- as predictors

Dependent variable: SHANNON-WIENER DIVERSITY

Waterbird assemblage: All year Multiple adj. R2: 0.630
Predictors: Coef p-value
Distance to the nearest village -0.027 0.078
Salinity 0.030 0.000
Temperature -0.043 0.000
Waterbird assemblage: Winter Multiple adj. R2: 0.685
Predictors: Coef p-value
Stress (Mean weighted record of disturbance events) 0.415 0.000
Nitrite 0.052 0.025
Waterbird assemblage: Summer Multiple adj. R2: 0.240
Predictors: Coef p-value
Distance to main communication channel 0.025 0.000
Waterbird assemblage: All year Multiple adj. R2: 0.550
Predictors: Coef p-value
Nitrite 1.452 0.017
Salinity 0.601 0.000
Temperature -0.921 0.000
Waterbird assemblage: Winter Multiple adj. R2: 0.544
Predictors: Coef p-value
Stress 6.685 0.000
Nitrite 1.042 0.000
Ichthyoplankton -0.003 0.000
Waterbird assemblage: Summer Multiple adj. R2: 0.450
Predictors: Coef p-value
Mean frequency of fishing nets at each sampling -0.901 0.000
station
Distance to the nearest harbour 1.011 0.001
Distance to the nearest village -0.847 0.024
Salinity 0.055 0.000

4.4. Towards a Better Understanding of Waterbird Trophic Ecology in CL

Research on waterbird trophic ecology based on stable isotope analyses, aim at clarifying
the role of waterbirds as top-down controllers suggested by the preliminary research results
outlined in the previous section. Monitoring of such effects of top predators is also important
from an applied perspective, given the potential of piscivorous birds to become conflicting
species, through their interaction with fisheries (Engström, 2001; Carss, 2003; Liordos and
Goutner, 2007). This new approach also intends to determine how the feeding dispersion of
172 Francisco Robledano Aymerich and Pablo Farinós Celdrán

the species studied around the Mar Menor CL and other habitat types, can affect their
indicator value.
In this regard, current work (P. Farinós et al., in preparation) attempts to explore, through
the application of newly standardized methodologies like circular statistics (Post, 2002,
Schmidt et al., 2007) or niche interactions and trophic diversity measures (Layman et al.
2007), the feeding dispersion patterns of cormorants in the Region of Murcia throughout its
potential habitats distributed along the continental-marine gradient (with the Mar Menor
lagoon as ―typical‖ TW habitat).
These studies are primarily focused at three groups of wintering cormorants settled in
three habitat types (freshwater bodies, coastal lagoon and open marine water), and their
potential prey, and are based on detecting trends of change in the isotopic signature of C13 and
N15 among the three areas, exploring the breadth, overlap and packing of food niche occupied
by each group and clarifying the predator-prey relationships. As preliminary results, in Figure
8 is shown the biplot representing the mean and standard deviation of the signal of C13 and
N15 of each trophic group studied. At a first glance, the representation depicts a strong affinity
-from the point of view of the trophic niche and feeding habitats-, between two groups of
wintering birds as distant as freshwater and marine cormorants (the position of the latter
suggesting that their feeding extends to freshwater bodies as well).
In any case, several aspects and issues expressed through circular and other statistical
techniques described above, are still under discussion with regard to other research works that
explore the isotopic signature of different elements in the food webs of the Mar Menor CL
(Marín-Guirao et al. 2008, Lloret and Marín, 2009).

22,00

20,00

18,00
Lake cormorants

16,00 Marine
cormorants
N
δ 15

14,00

Lagoon
12,00 Lake fish cormorants

10,00
Marine fish
8,00 Lagoon fish

6,00
-26,00 -24,00 -22,00 -20,00 -18,00 -16,00 -14,00 -12,00 -10,00 -8,00
13
δ C

Figure 8. Biplot representing the mean and standard deviation of the signal of C13 and N15 of each
trophic group of Great Cormorants studied. ―Lake cormorants (and fish) refer to the group whose
samples were collected in an inland freshwater reservoir; ―Marine‖, to those sampled in open sea
islands; and ―Lagoon‖, to those from the Mar Menor CL
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 173

Finally, eco-toxicological studies have been launched in order to explore the role of the
Great Cormorant as bio-indicator of heavy metals pollution (Burger and Gochfeld, 2001 a), a
process also present in the lagoon as a result of decades of opencast mining in the southern
part of its watershed. These studies draw on the growing number of dead specimens beached
in the lagoon shoreline, as a result of an increasing number of individuals drowned in fishing
nets. The collection of fresh corpses is already yielding further data on the feeding ecology of
this species (stomach contents), in addition to the tissues in which to base the toxicological
analyses. The sampling of various elements of live and dead specimens for monitoring
purposes, will help in future studies on the community of waterbirds and the whole lagoon
ecosystem. Most of the species studied are top predators that integrate food web processes
over time. A feature which, combined with new techniques to conduct retrospective
measurement of chemical and/or biochemical indicators in archived tissue samples, can
inform about temporal changes in food webs (Hebert et al., 2009).

5. SYNTHESIS AND PERSPECTIVES

A main conclusion of this review is that waterbird monitoring activities in CLs should
make a qualitative leap from routine accounting of population changes, towards a more
accurate record of bird metrics, and their combination in meaningful indexes. While the
former has an indisputable value for the compilation of indicators at national or international
scales, studies of regional or local levels are of most interest to detect and, where appropriate,
prevent, trends in habitat degradation. Austin et al. (2000) states that a regional breakdown of
winter indices (based in wader census) increases understanding of national trends and can
potentially act as an early warning system, highlighting possible declines before they become
apparent at a national level. These declines may be indicators of changes in habitat quality
that could have important consequences for conservation. In analogy, local monitoring of
waterbird indicator species in CLs would help to better understand how the processes
operating on this scale are combined and integrated to generate emerging trends.
Ornithological monitoring data are recognized by various authors as cost-effective
components of indicator systems for assessing habitat quality in wetlands (Brazner et al.,
2007; Everard, 2008), and therefore should be investigated further on their consistency with
other metrics and indices developed for the internal assessment of alteration gradients in CLs
(e.g. Salas et al., 2006). At this point, it seems also indisputable the convenience of a multi-
species/multi-metric system of ecological and biological monitoring of CLs based on
waterbirds (Brazner et al., 2007). This system needs to combine the population-community-
ecosystem indicators dealt with in sections 4.1 to 4.3, the suborganismical ones outlined at the
end of section 4.3, and whatever other relevant biological data generated by monitoring
programs.
Schemes like wildlife disease surveillance programs, beached-bird surveys, rehabilitation
center data, and waterbird monitoring programs, all can supply information about a number of
parameters (morbidity and mortality, breeding effort, breeding success, changes in population
sizes) which combined, will provide a potentially robust early warning system for larger scale
perturbations. This has remarkable implications, not only for aquatic bird health, but also for
human health, as aquatic birds are used as sentinels for the alteration of ecosystems (wetlands,
174 Francisco Robledano Aymerich and Pablo Farinós Celdrán

coastal areas) from which people obtain important goods and services (Burger and Gochfeld,
2001 b; Newman et al. 2007).
Ongoing studies will allow in the near future to address key issues raised in the
introduction to this chapter, but they are also opening new questions to be answered by
posing new hypotheses, leading to the correct formulation of indicators (Stolen et al., 2004;
Amat and Green, 2010). From a practical point of view, there remains the question of how to
transfer the knowledge generated to ecologically and geographically related areas, as are
other coastal lagoons in early stages of impairment and/or under still less intense pressures.
Previous studies in closely related CL complexes (e.g. Tamisier and Boudouresque, 1994;
Charco-García et al., 1995; Hernández and Robledano, 1997) show differences in the
composition of their communities of waterbirds, which could be related to a lagged
expression of similar alteration processes (as a consequence of different socio-economic
development contexts, like those found in Northern versus Southern Mediterranean shores).
It is possible, in any case, that waterbird responses found in the Mar Menor CL are site-
specific, as it seems to happen in other Mediterranean sites (Tamisier and Boudouresque,
1994), so comparative studies in similar ecosystems and in other habitat types are urgently
needed. Once tested in Northern Mediterranean CLs, the application of bird bioindication
schemes to less impacted wetlands of the Southern shores (taken as relatively undisturbed
reference sites) appears as a valuable tool for assessing and preventing changes in the
ecological status of these systems. Such comparative studies, coupled with the long term
monitoring data available from CLs of developed countries, will also help to establish
restoration objectives for the latter, with the reference undisturbed stages as most desirable
(though not always achievable) targets.

ACKNOWLEDGMENTS
The studies on which this chapter is based were funded, until 2006, by the European
Union through EC ―Energy, Environment & Sustainable Development Programme‖ (DITTY
Project, Contract EVK3-CT-2002-0084 DITTY). Between 2007-2009 financial support came
from the Spanish Ministry of Education and Science through Project IBISMED- ESTADO
ECOLÓGICO DE LOS HUMEDALES DEL MEDITERRÁNEO SEMIÁRIDO:
PROPUESTA DE INDICADORES PARA SU EVALUACIÓN (CGL 2006-08134). We
thank Asociación de Naturalistas del Sureste (ANSE) for coordinating waterbird censuses in
the Mar Menor Lagoon during the years without public support to this scheme, and many
volunteer ornithologists for carrying them out.
Recent work on the offshore waterbird community of the Mar Menor CL would not have
been possible without the logistical support of Angel Perez Ruzafa and Research Group of
Marine Ecology (in particular, Mari Carmen Mompeán, Victoria Fernández, Jhoni I. Quispe,
Marta García, Mercedes González and Oscar Esparza). The study was supported by the
University of Murcia and Consejería de Agricultura y Agua de la Región de Murcia through
the Agreement ―Red de Control y Vigilancia de la Calidad de las Aguas Litorales de la
Región de Murcia‖.
M. Francisca Carreño assisted in the calculation of some environmental variables with
GRASS and in graphical representations. Jhoni I. Quispe also collaborated in the creation of
 Waterbirds as Bioindicators in Coastal Lagoons: Background, Potential Value… 175

distribution maps, and J. Miñano in the figures. Part of the content of this chapter comes from
the work done by the first author during a stay in 2007 in the ―Unitat d'Ecosistemes Aquatics‖
del IRTA (Centre d'Aqüicultura de Sant Carles de la Ràpita, Catalonia, Spain).

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Chapter 6

HOW IMPORTANT ARE LOCAL NUTRIENT

EMISSIONS TO EUTROPHICATION IN COASTAL
AREAS COMPARED TO FLUXES FROM THE
OUTSIDE SEA? A CASE-STUDY USING DATA FROM
THE HIMMERFJÄRDEN BAY IN THE BALTIC PROPER

Lars Håkanson* and Maria I. Stenström-Khalili

Dept. of Earth Sciences, Uppsala University, Uppsala, Sweden

ABSTRACT
The basic aim of this work has been to present a general approach to quantify how
coastal systems are likely to respond to changes in nutrient loading. The conditions in
most coastal areas depend on nutrients emissions from points sources, diffuse sources,
river input and the exchange of nutrients and water between the given coast and the
outside sea, but all these fluxes can not be of equal importance to the conditions in the
given coastal area, e.g., for the water clarity, primary production and concentration of
harmfull algae (such as cyanobacteria). This work describes how a general process-based
mass-balance model (CoastMab) has been applied for the case-study area, the
Himmerfjärden Bay on the Swedish side of the Baltic Proper. The model has previously
been extensively tested and validated for salt, phosphorus, suspended particulate matter,
radionuclides and metals in several lakes and coastal areas. The transport processes
quantified in this model are general and apply for all substances in all aquatic systems,
but there are also substance-specific parts (mainly related to the particulate fraction and
the criteria for diffusion). This is not a model where the user should make any tuning or
change model constants. The idea is to have a model based on general and
mechanistically correct algorithms describing the transport processes (sedimentation,
resuspension, diffusion, mixing, etc.) at the ecosystem scale and to calculate the role of
the different transport processes and how a given system would react to changes in inflow
related to natural variations and anthropogenic reductions of water pollutants. The results

*
Corresponding author: E-mail: Lars.Hakanson@geo.uu.se, Fax: +46-18-471-2737, Phone: +46-18-471-3897.
186 Lars Håkanson and Maria I. Stenström-Khalili

presented in this work indicate that the conditions in the Himmerfjärden Bay are
dominated by the water exchange between the bay and the outside sea. The theoretical
surface-water retention time is about 19 days, as determined using the mass-balance
model for salt, which is based on comprehensive and reliable empirical data. This means
that although this bay is quite enclosed, it is still dominated by the water exchange
towards the sea. Local emissions of nutrients to the Himmerfjärden Bay are small
compared to the nutrient fluxes from the sea. If the conditions in this, and many similar
bays, are to be improved, it is very important to lower the nutrient concentrations in the
outside sea.

Keywords: coastal waters; nutrients; eutrophication; Baltic Sea; Himmerfjärden Bay; mass-
balance modeling; Secchi depth; chlorophyll, cyanobacteria

1. INTRODUCTION AND AIM

The title of this paper addresses a key issue in coastal management: If investments are
being made to reduce local nutrient emissions to coastal areas, e.g., from industries and other
point sources (such as fish farms), from diffuse sources, by means of changing agricultural
practices, what are the benefits for the local receiving water system? And how much of the
local emissions would be transported out of the local coastal system and contaminate the
outside sea? To answer such questions, it is evident that one needs to quantify all major fluxes
of water and nutrients/contaminants to, within and from the given coastal area to put the
planned reductions into the proper context. This work will use a general mass-balance model
(CoastMab; see Håkanson and Eklund, 2007, for a more thorough model description) in three
different forms:

(1) CoastMab for salt will provide water fluxes to, within and from the given coastal
area and also the basic algorithms for (a) the theoretical water retention times (which
influence the turbulence of the system and hence also sedimentation of particulate
matter), (b) the mixing transport between the surface and the deep-water layers and
(c) diffusion fluxes of dissolved substances (such as salt and dissolved forms of
nutrients).
(2) CoastMab for phosphorus will provide the requested nutrient fluxes and put the
nutrient fluxes from the tributaries and from local emissions into a framework where
also the exchange of nutrients between the given coastal area and the outside sea are
calculated. The main difference between CoastMab for salt and CoastMab for
phosphorus relate to the fact that phosphorus may appear in two different forms, the
particulate fraction (PF), which is subject to gravitational sedimentation, and the
dissolved fraction (DF = 1 – PF), which is subject to biouptake and also that the
phosphorus deposited in the sediments may return to the water phase by means of
advective and diffusive transport processes. The advective fluxes are mainly caused
by wind-induced wave action and slope processes and the diffusive internal loading
mainly by high sedimentation of organic material leading to high oxygen
consumption, low oxygen concentrations and low redox potential in the sediments,
which favors the formation of high levels of dissolved phosphorus in the sediments,
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 187

which trigger a high diffusion of phosphorus from the sediments. These processes are
well known and included in textbooks in recent sedimentology (see, e.g., Håkanson
and Jansson, 1983) and these processes are also included in the CoastMab-model.
(3) CoastMab for suspended particulate matter (see Håkanson, 2006), which also
predicts water clarity (Secchi depth) and sedimentation of matter and how these
factors relate to nutrient fluxes (how the nutrient concentrations regulate the internal
production of suspended particles) and the salinity (which regulates the aggregation
of suspended particles and hence also sedimentation and water clarity).

A central question in coastal management is how a given system would respond to

suggested measures. How long would it take to reach a new steady state? What are the
characteristic new nutrient concentrations in the water? And how would key bioindicators for
eutrophication (see, e.g., Nixon, 1990; Livingston, 2001; Schernewski and Schiewer, 2002;
Schernewski and Neumann, 2005; Moldan and Billharz, 1997; Bortone, 2005), such as
chlorophyll-a concentration, concentration of cyanobacteria, oxygen concentration in the
deep-water zone or Secchi depth change? In short, what is the environmental benefit related
to the remedial costs? Such questions are addressed in this work using a general process-
based quantitative approach which could also be used for other coastal areas than the case-
study area discussed here, the Himmerfjärden Bay in the Baltic Sea.
Eutrophication is ranked as the most severe threat to the Baltic Sea (Savage et al., 2002;
Bernes, 2005). Himmerfjärden was chosen as study area because it has been investigated
intensively since 1976 and long data series on nutrient levels and water quality variables are
available. There has been no proper mass-balance modeling of the bay before this study but
Elmgren and Larsson (1997) and Larsson et al. (2006) stressed the importance of performing
a mass-balance modeling study of Himmerfjärden to determine flows and water retention
times in the bay. Khalili (2007) has presented a literature study on previous eutrophication
research in Himmerfjärden. The research in the bay includes four large-scale nutrient
regulation tests related to the discharges from a water treatment plant, Himmerfjärdsverket.
The results from Himmerfjärden are often cited and used to motivate the benefits of nitrogen
emission reductions. This has been questioned and the debate has been lively (Rabalais, 2002;
Rönnberg and Bonsdorff, 2004; Howarth and Marino, 2006; Boesch et al., 2006).
The following section will present the data used in the mass-balance calculations for salt,
phosphorus and suspended particulate matter (SPM). A central part of this work is to compare
modeled data on the target variables (salinity, phosphorus and nitrogen concentrations, Secchi
depth, chlorophyll and oxygen concentrations) with empirical data. We will also present
model predictions of cyanobacteria, SPM-concentrations, phosphorus concentration in
sediments and sedimentation but in those cases there are no comparable reliable empirical
data accessible to us. The main results concern the dynamic response of the system to
reductions in nutrient loading and the analyses and interpretations of those results.
It should be stresses that the CoastMab-model has previously been extensively tested and
validated with good results for phosphorus from over 20 different coastal areas and more than
40 lakes, for suspended particulate matter in over 20 coastal areas and more than 10 lakes and
for toxic substances (radionuclides and metals) in several lakes and coastal areas.
188 Lars Håkanson and Maria I. Stenström-Khalili

2. INFORMATION ON THE HIMMERFJÄRDEN BAY

2.1. Previous Tests and Studies

Himmerfjärden Bay (see Figure 1), situated about 60 km south of Stockholm at 59° 00‘
N, 17° 45‘, is a narrow bay divided into four sub-basins (Boesch et al., 2006). The basins are
separated by thresholds, and just outside the outer basin, to the south, is the area Hållsfjärden.
Hållsfjärden is commonly used as a reference area for Himmerfjärden and holds a reference
station called B1. There are five sampling stations in Himmerfjärden, H2 to H6.
Himmerfjärden is connected to Lake Mälaren in the north but the freshwater inflow to the bay
is limited to a few short periods when the water levels in the lake are high (Elmgren and
Larsson, 1997). Himmerfjärden has been monitored since the middle of the 1970s when
sewage water from the area southwest of Stockholm was redirected from Lake Mälaren to
Himmerfjärden. In 1974, the treatment plant in Himmerfjärden began to remove phosphorus
and 96% of the phosphorus is, on average, removed today. The treatment plant initially
served about 90 000 people but the population increased rapidly, causing an increase in
primarily nitrogen fluxes. Today, the plant serves 240 000 people (Boesch et al., 2006).
Extensive nitrogen removal has been implemented since the late 1990‘s reaching about 90
percent in 1998 (Larsson and Elmgren, 2001).

Figure 1. Himmerfjärden with the locations of sampling stations and treatment plant
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 189

It must be stressed that it has been assumed that the emissions from the sewage treatment
plant contributes with flows of nitrogen of such significance that the regulation of emissions
would have a clear effect on the eutrophication status in Himmerfjärden. This assumption was
mainly based on the fact that total nitrogen concentration and inorganic concentrations of
nitrogen before the spring bloom at station H4 correlated (r2 = 0.69, n = 16) with the load
from the sewage treatment plant. Changes in eutrophication status have consequently been
interpreted mainly as results of treatment plant regulatory measures (Elmgren and Larsson,
1997; Elmgren and Larsson, 2001; Larsson and Elmgren, 2001).
The first large-scale experiment in Himmerfjärden was performed in 1983 when the
concentration of phosphorus in the treatment plant discharge was allowed to increase to about
fourfold (or twofold as compared to the amount discharged annually in 1983, i.e., 31 tons).
According to Elmgren and Larsson (1997), no increase in primary production was observed
following this increase in phosphorus loading but a slight increase in heterocytes (the nitrogen
fixing cells in cyanobacteria) was noted and this increase occurred mainly at station B1 in the
reference area possibly implying that the growth of cyanobacteria in Himmerfjärden reflects
the growth in the adjacent sea.
The second large-scale experiment started in 1985 when the treatment plant increased its
capacity and began receiving sewage from Eolshälls treatment plant resulting in increased
emissions of nitrogen to Himmerfjärden. The increase was followed by a successive decrease
when nitrogen reduction processes were introduced and became more and more efficient
reaching about 50 percent in 1992. As in the case with the first experiment, no increase in
primary production occurred following increasing nitrogen inputs to the bay. Elmgren and
Larsson (1997) suggested that phosphorus at this time was the main limiting nutrient in
Himmerfjärden and that the excess nitrogen was exported to the adjacent sea causing
increased eutrophication in the outside sea.
As mentioned, Elmgren and Larsson (1997) found no significant correlation between
eutrophication indicators, such as chlorophyll, phytoplankton production (biomass) or Secchi
depth, and varying loads of nitrogen and phosphorus from the sewage treatment plant
following the two first large-scale experiments. They concluded that further removal of
phosphorus would not be meaningful since the emissions from the treatment plant constitute a
small fraction of total loading of phosphorus. They recommended to increase nitrogen
removal efficiency from treatment plant discharge.
Following the recommendations from Elmgren and Larsson (1997) extensive nitrogen
removal (about 90 percent) began in 1998. A third large-scale experiment was performed in
2001-2002 when emissions of nitrogen were deliberately doubled. As in the previous cases,
no increase in chlorophyll a levels was observed by the increase in nitrogen from the sewage
treatment plant (Boesch et al. 2006).
According to Boesch et al. (2006) both the experiment in 1983 and the two experiments
with increased nitrogen emissions may have been too small and or to short to result in clear
changes in primary production in the bay.
From this background, we will present several scenarios where the phosphorus emissions
from the plant are increased and also the TP-fluxes from the sea. The idea is to quantify all
key transport processes (see Figure 2) and see how the given changes, and potential remedial
strategies, would influence not just the phosphorus concentrations in the bay but also key
bioindicators (the Secchi depth, and concentrations of cyanobacteria and chlorophyll).
190 Lars Håkanson and Maria I. Stenström-Khalili

Point source emissions

Precipitation
Inflow from Biouptake and retention in biota Water and TP exchange
catchment between the coast and the sea

Surface water ET-sediments

Mixing Resuspension
Wave base
Deep water Sedimentation Diffusion

Diffusion
Compaction
Active A-sediments

Bioturbation Biopassive A-sediments (geosphere)

Burial

Figure 2. An outline of transport processes (= fluxes) and the structure of the dynamic coastal model for
phosphorus (CoastMab)

2.2. Data and Methods

This work will use morphometric data from Khalili (2007) who made an analysis of the
Himmerfjärden Bay using geographical information systems (GIS). Basin-specific data are
compiled in table 1, which gives information on, e.g., total area; volume; mean depth;
maximum depth; the volume of the surface-water layer and the deep-water layer; the section
area, which defines the cross-sectional area that separates the given coastal area from the
outside sea (Figure 3); the tributary water discharge to the bay; the discharge of water and
phosphorus from the plant; the catchment area; latitude; and mean annual precipitation.
Figure 3 shows the limiting section area which constitutes the boundary between the bay and
the open sea, as determined using the topographical bottleneck method, i.e., so that the
exposure attains a minimum value. From this figure, one can note that the deepest part of the
section area is at 19 m, and this is also the reason for setting the theoretical wave base at 19 m
in the Himmerfjärden Bay; above the theoretical wave base, there should be discontinuous
sedimentation of fine sediments and particulate phosphorus, and areas of fine sediment
erosion and transport; at larger water depths, there should be areas of fine sediment
accumulation.
So, the theoretical wave base separates the transportation areas (T), with discontinuous
sedimentation of fine materials, from the accumulation areas (A), with continuous
sedimentation of fine suspended particles (see Håkanson and Jansson, 1983). The
Himmerfjärden Bay has been divided into two depth intervals:

(1) The surface-water layer (SW), i.e., the water above the theoretical wave base at 19
m.
(2) The deep-water layer (DW) is defined as the volume of water beneath the theoretical
wave base (see table 1).

It should be noted that the theoretical wave base is meant to describe average conditions.
During storm events, the wave base will likely be at greater water depths (see Jönsson, 2005)
and during calm periods at shallower depths. Khalili (2007) has presented a new
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 191

hypsographic curve and a corresponding volume curve for Himmerfjäden and those curves
have been used in this work to calculate the volumes given in table 1. One can note that the
area below the theoretical wave base (Dwb) is 46 km2 and that the SW-volume is 2.6 km3, the
volume of the DW-layers is small (only 0.24 km3) and the entire volume is 2.88 km3. The
boundary lines for the Himmerfjärden Bay used in this work are from Khalili (2007); the total
section area (At), which provides a minimum value of the exposure (Ex=100·At/A; see
Pilesjö et al., 1991, for more information regarding the topographical bottlerneck method to
objectively define the boundary lines for coastal areas) is 45310 m2, which gives an exposure
(Ex) of 0.0194, indicating the enclosed character of the bay.

Table 1. Data on Himmerfjärden Bay (see Kahlili, 2007, for more information)

Catchment area (ADA in km2) 1 268

Annual precipitation (Prec, mm/yr) 460
Area (A in km2) 234
Area below wave base at 19 m (ADwb in km2) 46
Maximum depth (Dmax in m) 52
Wave base (Dwb in m) 19
Dynamic ratio (DR=√A/Dm) 1.24
Areas of fine sediment erosion and transport (ET, dim. less) 0.80
Exposure (Ex=100·At/A) 0.0194
Form factor (Vd=3·Dm/Dmax) 0.71
Land rise (LR, mm/yr) 4
Latitude (Lat, °N) 59
Mean depth (Dm=V/A, m) 12.3
Water flow from plant (Qplant, m3/yr) 35 000 000
Water flow from rivers (Qtrib, m3/yr) 491 600 000
Section area (At, m2) 45 310
TP-emissions from plant (FTPplant, kg/yr) 1 632
Volume of DW-layer (VSW, km3) 0.236
Volume of SW-layer (VDW, km3) 2.642
Total volume (V, km3) 2.878

5
Water depth (m)

0
Section
1000 2000 3000 4000 5000 length (m)
-5

-10

-15

-20

Figure 3. Limiting section area profile between Askö-Torö in the Himmerfjärden Bay
192 Lars Håkanson and Maria I. Stenström-Khalili

Table 2. Monthly data on driving variables (mean monthly number of hours with
daylight), surface-water (SW) salinity in the sea outside of Himmerfjärden Bay
(the Baltic proper, BP), Secchi depth outside the bay, TP in SW and
DW-water outside the bay and SW and DW-temperatures in the bay.
MV = mean value; M50 = median; SD = standard deviation

Month Daylight SalinitySWBP SecchiBP TPSWBP TPDWBP TempSW TempDW

hr/month psu psu µg/l µg/l °C °C
1 9.1 7.18 8.5 30.1 31.2 0.7 1.3
2 11.8 7.12 8.5 27.2 29.3 1.1 1.2
3 14.3 7.01 7.0 22.1 24.3 3.0 2.3
4 17.1 7.01 9.0 18.2 21.2 8.0 4.0
5 18.5 7.06 7.6 18.1 22.4 12.6 5.9
6 18.1 6.96 5.3 16.6 24.5 16.1 7.5
7 15.8 6.96 5.5 17.9 24.8 18.0 8.3
8 13.0 6.93 6.7 19.3 26.0 14.6 8.0
9 10.1 6.92 8.5 23.1 27.1 10.8 8.1
10 7.3 7.00 9.5 25.9 26.9 7.6 7.1
11 6.4 7.09 7.8 30.9 33.3 1.3 2.1
12 6.4 7.09 7.8 30.9 33.3 1.3 2.1
MV 12.3 7.03 7.7 23.4 27.0 7.9 4.8
M50 12.4 7.01 7.8 22.6 26.5 7.8 4.9
SD 4.5 0.08 1.3 5.5 4.0 6.4 2.9

Table 2 shows the driving variables used in this work (calculated from the ongoing
monitoring program for the period 1997 to 2007). This table gives monthly mean values for
the number of hours with daylight (needed to calculate chlorophyll concentration), salinity in
the surface water outside the Himmerfjärden Bay in the Baltic Proper (needed in the mass-
balance calculation of salt inflow from the Baltic Proper), the Secchi depth in the area outside
of Himmerfjärden (needed to calculate the inflow of SPM from the Baltic Proper), the total
phosphorus (TP) concentrations in the SW and DW-layers in the area outside of
Himmerfjärden (needed to calculate the inflow of TP from the Baltic Proper), and the
empirical monthly SW and DW-temperatures in the Himmerfjärden (needed to quantify
mixing).
In the following modeling, we will compare the modeled values for the target variables
mainly to the confidence intervals related to ± 1 standard deviation of the mean monthly
empirical data accessible to us from the bay.

3. THE DYNAMIC COASTWEB-MODEL

The model consists of five compartments: surface water (SW), deep water (DW),
erosion/transportation areas for fine sediments (ET), accumulation areas for fine sediments
below the theoretical wave base (A) and biota with short turnover times (BS; plankton). There
are algorithms for all major internal fluxes of salt, TP and SPM (outflow, TP and SPM from
land uplift, sedimentation of particulate TP and SPM, resuspension of TP and SPM, diffusion
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 193

of salt and dissolved phosphorus, mixing, biouptake of dissolved phosphorus and burial of TP
and SPM and mineralization of the organic fraction of SPM; see Håkanson and Eklund, 2007
and Håkanson, 2006 which give and motivate all equations and model variables). Table 3
gives a compilation of all equations and model variables related to the CoastMab-model for
salt.

Table 3. A compilation of all equations and model variables in the mass-balance model
for salt (CoastMab). Abbreviations: F for flow (kg/month), R for rate (1/month), C or
Sal for concentration (‰ = psu = kg/m3), DC for distribution coefficients
(dimensionless), M for mass (kg salt), D for depth in m, A for area in m2, V for volume
in m3; ET stands for areas with erosion and resuspension (advection) of fine sediments
above the theoretical wave base; T is the theoretical retention time (years); flow from
one compartment (e.g., SW) to another compartment (e.g., DW) is written as FSWDW;
mixing flow is abbreviated as FxDWMW; Q is water discharge (m3/month)

Surface-water layer (SW)

MSW(t) = MSW(t - dt) + (FxMWSW + Ftrib + Fprec + FdDWSW + FInSW +FplantSW - FoutSW - FxSWDW –
Feva)·dt
INFLOWS:
FxDWSW = MDW·RxSWDW·VSW/VDW; mixing from DW to SW (kg/month)
Ftrib = Qtrib·Saltrib; tributary inflow of salt (kg/month)
Fprec = Qprec·Salprec; precipitation of salt (kg/month)
FdDWSW = Qprec·Salprec; precipitation of salt (kg/month)
FdDWSW= MDW·Diffcoeff ·Diffconst; diffusion from DW to SW (kg/month)
FinSW = Qin·SalSWBP; inflow of salt to SW (kg/month)
FplantSW = QplantSW·Salplant; inflow of salt to SW from water purification plant (kg/month)
OUTFLOWS:
FoutSW = QoutSW·SalSW; outflow of salt from SW (kg/month)
FxSWDW = MSW·RxSWDW; mixing from SW to DW (kg/month)
Feva = Qeva·Saleva; evaporation of salt from SW (kg/month)
Deep-water layer (DW)
MDW(t) = MDW(t - dt) + (FxSWDW + FinDW - FxMWSW - FdDWSW – FoutDW)·dt
INFLOWS:
FxSWDW = MSW·RxSWDW; mixing from SW to DW (kg/month)
FinDW = QinDW·SalDWBP; inflow of salt to DW (kg/month)
OUTFLOWS:
FxDWSW = MDW··RxSWDW·VSW/VDW; mixing from DW to SW (kg/month)
FdDWSW = MDW·Diffcoeff ·Diffconst; diffusion from DW to SW (kg/month)
FoutDW = SalDW·QoutDW; outflow of salt from DW (kg/month)
Model variables
Area = 234·106; coastal area (m2)
Area below wave base (AWB) = 46·106; (m2)
Saleva = 0; salinity in evaporating water (psu)
Salplant = 0; salinity in water from plant (psu)
Salprec = 0; salinity in precipitation (psu)
Saltrib= 0; salinity in tributary water (psu)
194 Lars Håkanson and Maria I. Stenström-Khalili

Table 3. (Continued)
Diffconst = 0.05/12; diffusion rate (1/month)
DCSWDW = 0.9; distribution coefficient regulating water inflow from the sea to the SW and
DW layers in the bay
DCSWDWplant = 0.99; distribution coefficient regulating water inflow from the plant to the SW
and DW layers in the bay
Diffcoeff = if SalSW > SalDW then 0 else (SalDW-SalSW); diffusion coefficient
ET = (Area-AWB)/Area; distribution coefficient (fraction of ET-areas)
Exposure (Ex) = (100·At·10-6)/(Area·10-6)
Mean depth (dm) = 12.3: (m)
Rxdef = Strat·ET/12; default mixing rate (1/month)
Rxexp = 2; mixing rate expotent
RxSWDW = if SalDW > SalSW then Rxdef·(1/(1+SalDW-SalSW))^ Rxexp else Rxdef; mixing rate (1/month)
Prec = 460; mean annual precipitation (mm/yr)
Qemp = if SWT < 5 °C then 491.6·106 else (491.6·106-Qplant); annual empirical freshwater
inflow (m3/yr)
Qeva = 0.9·Qprec; water transport related to evaporation (m3/month)
QinSW = DCSWMW·Qin; water inflow to SW from the sea (m3/month)
Qin = 4500·106; total water inflow from the sea (m3/month)
QinDW = Qin·(1-DCSWMW); water inflow to DW from the sea (m3/month)
QmixDWSW = FxDWSW/SalDW; mixing water flow (m3/month)
QoutDW = (QinSW+QinDW+Qtrib+Qprec)-(QoutSW+Qeva)+Qplant/12; outflow of water from DW
(m3/month)
QoutSW = /QinSW+Qprec+Qtrib-Qeva); outflow of water from SW (m3/month)
Qprec = Area·Prec·0.001/12; water flow from precipitation (m3/month)
QplantDW = (1-DCSWDWplant)·35·10^6
QplantSW = DCSWDWplant·35·10^6
Qtrib = (Qemp/12)·YQ
SalDW = MDW/VDW; DW salinity (psu)
SalSW = MSW/VSW; SW salinity (psu) Section area(At) = 45310 (m2)
Strat = if ABS(SWT- DWT) < 4 °C then Strat = (1+1/(1+ABS(SWT- DWT)) else 1/ABS(SWT- DWT;
temperature dependent stratification
SWT = surface water temperatire (°C)
TDW = VDW/(QinDW+QmixMWSW); theoretical deep water retention time (months)
VDW = 0.236·10^9; DW volume (m3)
V = Area·Mean_depth; volume (m3)
VSW = (V-VDW); SW volume (m3)
Wave base = 19 m

To calculate the inflow of salt, TP and SPM to the Himmerfjärden Bay (HI) from the
Baltic Proper (BP), data on the concentrations in the SW and DW-layers in the Baltic Proper
from table 2 have been used. The inflows to the two layers from the Baltic Proper are given
by the water discharges in table 4 (QSWBPHI and QDWBPHI) and the given concentrations. The
empirical Secchi depths in table 2 have been recalculated into SPM-values (the suspended
particles regulate the light scattering in the water and the Secchi depth) by eq. 1 (from
Håkanson, 2006):

SPMSW = 10^(-0.3-2·(log(Sec)-(10^(0.15·log(1+SalSW)+0.3)-1))/
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 195

Table 4. Compilation of calculated monthly data (using the mass-balance for salt) for
water transport (Q in million m3/yr) related to evaporation (Qeva), surface water (SW)
inflow from the Baltic Proper (BP) to Himmersfjärden Bay (HI), deep-water (DW)
inflow from BP to HI, mixing from DW to SW in HI, DW outflow from HI to BP, SW
outflow from HI to BP, water flow related to direct precipitation onto the surface area
of HI (Qprec), inflow of water to SW and DW from the water treatment plant (QSWplant
and QDWplant) and freshwater inflow from tributaries (Qtrib). MV = mean value; M50 =
median; SD = standard deviation.

Month Qeva QSWBPHI QDWBPHI QDWSWx QDWHIBP QSWHIBP Qprec QSWplant QDWplant Qtrib
1 8.1 4050 450 278 453 4104 9.0 2.9 0.03 52.9
2 8.1 4050 450 303 453 4095 9.0 2.9 0.03 44.3
3 8.1 4050 450 248 453 4099 9.0 2.9 0.03 47.9
4 8.1 4050 450 37 453 4110 9.0 2.9 0.03 59.1
5 8.1 4050 450 18 453 4110 9.0 2.9 0.03 59.4
6 8.1 4050 450 13 453 4084 9.0 2.9 0.03 33.2
7 8.1 4050 450 10 453 4078 9.0 2.9 0.03 27.1
8 8.1 4050 450 13 453 4076 9.0 2.9 0.03 25.0
9 8.1 4050 450 151 453 4078 9.0 2.9 0.03 26.7
10 8.1 4050 450 276 453 4081 9.0 2.9 0.03 30.3
11 8.1 4050 450 243 453 4097 9.0 2.9 0.03 46.4
12 8.1 4050 450 256 453 4097 9.0 2.9 0.03 46.4
MV 8.1 4050 450 154 453 4092 9 2.9 0.03 42
M50 8.1 4050 450 197 453 4096 9 2.9 0.03 45
SD 0 0 0 125 0 13 0 0 0 13

((10^(0.15·log(1+ SalSW)+0.3)-1)+0.5)) (1)

So, SPM-values (in mg/l) are calculated from measured Secchi depths (in m) and the
salinity of the SW-layer in the area outside Himmerfjärden (SalSW in psu). The higher the
salinity, the higher the aggregation and the higher the Secchi depth.
Figure 4 A and B give comparisons between modeled salinities and measured values
(instead of using the mean or median empirical data, we prefer to give the uncertainty bands
related to ± 1 standard deviation). The idea is that the modeled values should lie in-between
these uncertainty bands. This is one main way of controlling the model predictions, another
way is shown in table 5. From extensive measurements in many coastal areas (see Håkanson
et al., 1986), one can conclude that typical water velocities in limiting section areas generally
range between 1 and 15 cm/s for coastal areas in the Baltic Sea. Lower mean velocities than 1
cm/s would be rather unrealistic on a monthly basis. The water velocity in the section area has
been calculated for the total outflow (m3/yr) divided by half the section area since there is also
inflow of water to maintain a given water level ((m3/yr)·(1/(0.5·m2). These calculations give
an average velocity in the section area of 7.7 cm/s, which is in the middle of the expected
range.
Another way to check the modeled water fluxes between the coast and the sea is to
compare these model predictions from the mass-balance for salt with data from an
empirically-tested model for the theoretical water retention time. It has been shown (Persson
et al., 1994) that TSW can be predicted very well (r2 = 0.95) with the regression in eq. 2, which
is based on the exposure (Ex), which, in turn is a function of section area (At) and coastal area
(Area). The range of this model for TSW is given by the minimum and maximum values for
196 Lars Håkanson and Maria I. Stenström-Khalili

Ex of 0.002 < Ex < 1.3; Ex = 0.0194 for Himmerfjärden Bay is well within this range. The
model should not be used without complementary algorithms if the tidal range is > 20 cm/day
or for coastal areas dominated by fresh water discharges. For open coasts, i.e., when Ex > 1.3,
TSW may be calculated not by this equation but from a model based on coastal currents
(Håkanson, 2006) .

ln(TSW) = (-4.33·(√Ex) + 3.49) (2)

From table 5, one can note the good correspondence between TSW-values calculated using
the mass-balance for salt (mean value = 0.62 months) and with eq. 2 (mean value = 0.59
months). One can also see from table 5 that the theoretical deep-water retention time, TDW, is
short (0.41 months on average) because the volume of the DW-layer is small and TDW is
defined from the ratio between the volume of the DW-layer and the total water flux to the
DW-layer.

Table 5. Modeled monthly values the flow velocity of water in the section area,
the theoretical surface-water (SW) retention time calculated from the mass-balance
for salt (TSW), and from the empirical morphometrical formula based on the
exposure (Ex) (TSWEx) and for the deep-water (DW) according to the mass-balance
for salt (TDW). MV = mean value; M50 = median; SD = standard deviation

Month Monthly flow Theor. wat. Theor. wat. Theor. wat.

velocity ret. time ret. time ret. time
uAt, cm/s TSWEx, months TSW, months TDW, months
1 7.66 0.59 0.60 0.32
2 7.66 0.59 0.59 0.31
3 7.66 0.59 0.60 0.34
4 7.66 0.59 0.63 0.48
5 7.66 0.59 0.63 0.50
6 7.66 0.59 0.64 0.51
7 7.66 0.59 0.64 0.51
8 7.66 0.59 0.64 0.51
9 7.66 0.59 0.62 0.39
10 7.66 0.59 0.60 0.33
11 7.66 0.59 0.60 0.34
12 7.66 0.59 0.60 0.33
MV 7.66 0.59 0.62 0.41
M50 7.66 0.59 0.62 0.39
SD 0 0 0.02 0.09
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 197

Figure 4. Comparison between modeled values and uncertainty bands for the empirical mean values
representing ± 1 standard deviation for A. SW-salinity, B. DW-salinity, C. TP-concentration in SW, D.
TP-concentration in DW, E. Chlorophyll, F. Secchi depth, G. O2-concentration in DW, H. modeled TP-
concentration in accumulation area sediments in relation to minimum and maximum reference values, I.
modeled TN-concentration in relation to ±1 standard deviations for the empirical mean values, J.
modeled TN/TP-ratios in relation to the Redfield ratio (7.2 in g) and the Threshold ratio (15 in g), K.
modeled values of cyanobacteria, and L. modeled SPM-concentrations in the SW and DW-layers
198 Lars Håkanson and Maria I. Stenström-Khalili

Also note that there has been no calibration or tuning regarding the water fluxes given in
table 4 and that these fluxes are used also to calculate the TP and SPM-fluxes. The monthly
data on tributary water discharge used in the modeling have been calculated from the
empirical average annual value using the dimensionless moderator for this purpose (from
Abrahamsson and Håkanson, 1998). When empirical data from 119 rivers were compared to
modeled values, the r2-value was 0.84. This model has also been described and successfully
used in many previous contexts (see, e.g., Håkanson, 2006).This moderator is based on data
on the size of the catchment area, mean annual precipitation and latitude (see table 1). Since
we do not have access to reliable empirical monthly data on tributary water discharge for the
study period (1997 to 2007), it should be stressed that this modeling concerns average,
characteristic conditions on a monthly basis for this period of time and not the actual
sequence of months.
The theoretical water retention times in the two layers from the basic mass-balance for
salt (see table 4) are used together with the temperature-dependent mixing rate in the mass-
balance model as indicators of how the turbulent mixing influences the settling velocity for
particulate phosphorus and SPM – the faster the water renewal, the more turbulence, the
lower the settling velocity. The mixing rate regulating the monthly transport of water, salt and
nutrients between the surface and the deep-water layers depends on the difference in
temperature and salinity between the two layers and the form of the basin, as given by the
areas of fine sediment erosion and transport (ET) (see Table 3). The small TP-input from
precipitation onto the water surface of the Himmerfjärden Bay has been estimated from the
characteristic annual precipitation of 460 mm and a TP-concentration in the rain of 5 µg/l (see
Håkanson and Eklund, 2007).
The internal processes are: sedimentation of particulate phosphorus from surface water to
deep water (FTPSWDW), sedimentation from SW to areas of erosion and transportation
(FTPSWET), sedimentation from DW to accumulation areas (FTPDWA), resuspension (advection)
from ET-areas (including TP from land uplift, FTPLU) either back to the surface water
(FTPETSW) or to the deep water (FTPETDW), diffusion of dissolved phosphorus from
accumulation area sediments to the DW-layer (FTPADWd), diffusion from DW-water to SW-
water (FTPDWSWd), upward and downward mixing between SW and DW (FTPDWSWx and
FTPSWDWx) and biouptake and elimination of phosphorus from biota (FTPSWBS and FTPBSSW).
When there is a partitioning of a flux from one compartment to two compartments, this is
handled by a distribution coefficient (DC).

1. The DCs regulating the amount of phosphorus in particulate and dissolved fractions
in the SW and DW-layers. These DCs are called particulate fractions (PF). By
definition, only the particulate fraction of a substance is subject to gravitational
sedimentation and only the dissolved fraction (DF = 1 – PF) may be taken up by
biota. Table 6 gives a compilation of calculated PF-values for the SW and DW-
compartments. The CoastMab-model uses an algorithm to calculate the PF-value for
phosphorus in the surface-water layer based on the biouptake of dissolved P (the
higher the biouptake of dissolved P, the higher the PF-value) and the resuspension of
particulate P (which depends on the stratification; the more homothermal the water,
the more resuspension and the higher the PF-value). The default PF-value is 0.56,
which is a general, average empirical value based on extensive data from many
aquatic systems (see Håkanson and Boulion, 2002; Håkanson and Bryhn, 2008a, b).
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 199

So, the default PF-value is modified by the two dimensionless moderators for
biouptake and stratification/resuspension, as explained in Håkanson and Eklund
(2007). The PF-value for the deep-water layer is also calculated from
resuspension/stratification, the resuspended fraction of phosphorus in the deep-water
layer (which is calculated automatically in the model) and the monthly temperature
of the deep-water layer, which regulates the bacterial decomposition of organic
material, and hence also the oxygen consumption and the dissolved fraction of
phosphorus (see Håkanson and Eklund (2007).
One can note that the PF-values in the SW-compartment vary between 0.2 and 0.87
depending on season of the year (and how much TP is bound in biota) and that the
PF-values in the DW-compartment are low during stratified conditions (when most
phosphorus appear in dissolved form). The mean PFSW-value is 0.51 (see table 6).
2. The DC regulating sedimentation of particulate phosphorus either to areas of fine
sediment erosion and transport (FTPSWET) or to the DW-areas beneath the theoretical
wave base (FTPSWDW). The ET-value is 0.80 (i.e., 80% of the total area of the bay are
dominated by areas with fine sediment erosion and transport).
3. The DC describing the resuspension flux from ET-areas back either to the surface
water (FTPETSW) or to the DW-compartment (FTPETDW), as regulated by the form
factor (Vd, where DC=Vd/3, Vd = 3·Dm/Dmax, Dm = the mean depth, Dmax = the
maximum depth).
4. The DC describing how much of the TP in the water that has been resuspended
(DCres) and how much that has never been deposited and resuspended (1-DCres) in
the SW and DW-layers. The resuspended fraction settles out faster than the materials
that have not been deposited.

Table 6. Modeled monthly values related to accumulation area sediments 0-10 cm; bulk
density, organic content (= loss on ignition), water content, sedimentation and fall
velocities of suspended particulate matter and particulate phosphorus. MV = mean
value; M50 = median; SD = standard deviation

Month Bulk Organic Water Sedimentation Sedimentation Fall Fall Particulate Particulate
density content content velocity velocity fraction fraction
bg IG W SedDW SedDW vSW vDW PFDW PFSW
g ww/cm3 g/g dw % ww µg/cm2·d cm/yr m/month m/month
1 1.17 6.3 75 12.1 0.01 2.4 2.3 0.22 0.22
2 1.17 6.3 75 11.2 0.01 2.4 2.3 0.23 0.20
3 1.17 6.3 75 10.8 0.01 2.4 2.2 0.23 0.26
4 1.17 6.3 75 14.6 0.02 2.5 2.2 0.02 0.81
5 1.17 6.3 75 17.8 0.02 2.4 2.2 0.01 0.82
6 1.17 6.3 75 19.5 0.02 2.4 2.3 0.01 0.86
7 1.17 6.3 75 21.6 0.03 2.4 2.3 0.01 0.87
8 1.17 6.3 75 18.6 0.02 2.4 2.3 0.02 0.80
9 1.17 6.3 75 11.8 0.01 2.5 2.3 0.53 0.46
10 1.17 6.3 75 12.3 0.02 2.5 2.2 0.37 0.31
11 1.17 6.3 75 13.2 0.02 2.5 2.3 0.18 0.27
12 1.17 6.3 75 12.6 0.02 2.5 2.3 0.20 0.23
MV 1.17 6.3 75 14.7 0.018 2.4 2.3 0.17 0.51
M50 1.17 6.3 75 12.9 0.020 2.4 2.3 0.19 0.39
SD 0 0 0 3.7 0.0062 0.051 0.036 0.17 0.29
200 Lars Håkanson and Maria I. Stenström-Khalili

Land uplift (FLU) is a special case. Land uplift is a main contributor of TP to the Baltic
Proper (Håkanson and Bryhn, 2008b). From the map illustrating the spatial variation in land
uplift (see Voipio, 1981), one can calculate that the mean land uplift in the Himmerfjärden
Bay is about 4 mm/yr and this value has been used in these calculations. Land uplift has been
discussed in many contexts (Voipio, 1981; Jonsson et al., 1990; Jonsson, 1992) and the
algorithm to quantify how land uplift influences the fluxes of TP and SPM has been given by
Håkanson and Bryhn (2008b). The total area above the theoretical wave base in the
Himmerfjärden is about 188 km2 and the sediments in this area will be exposed to increased
erosion by wind/wave action due to the land uplift. The sediments in the shallower parts,
which may have been deposited more than 1000 years ago, will be more consolidated than the
recent materials close to the theoretical wave base. The calculation of the TP-flux from land
uplift uses (1) modeled data on the TP-concentration in the accumulation area sediments from
the DW-zone, (2) a water content of the sediments exposed to increased erosion set to be 15%
lower than the modeled water content of the recent sediments and (3) the total volume of
sediments above the theoretical wave base lifted each year.
To calculate the TP-uptake and retention in biota, this modeling uses a similar approach
as presented by Håkanson and Boulion (2002). This means that the uptake and retention in
biota depends on concentration of dissolved P, daylight, temperature and the turnover time of
the modeled organisms. It is given by:

MBSTP(t) = MBSTP(t - dt) + (FTPbioup - FTPbioret)·dt (3)

MBSTP(t) = The mass (amount) of TP in biota with short turnover times (plankton) (g).
FTPbioup = MSWTP·YSWT·(30/TBL)·(DayL/12.3)·(DFSW/0.44); the biouptake of TP in biota
(g/month).
FTPbiore = MBLTP·30/TBL; the retention (= outflow) of TP from biota (g/month).
YSWT = (SWT/11.85); the dimensionless moderator regulating the temperature dependent
biouptake of TP. TBS = the average turnover time for the functional groups included
in biota (phytoplankton 3.2 days, bacterioplankton = 2.8 days and herbivorous
zooplankton = 6 days).
SWT = The surface water temperature (°C); 11.85 = the mean surface water temperature
for the growing season (°C).
DFSW = the dissolved particulate fraction of phosphorus in surface water (dim. less); 0.44
is a standard reference value for DF (see Håkanson and Boulion, 2002).
DayL= the number of days with daylight (see table 2); 12.3 is the mean annual value; so,
this is a dimensionless moderator for the influence of light on the primary
production.

3.1. Regressions between Modeled TP-Values versus Total-N and Different

Bioindicators

It is well established (Redfield et al., 1963) that plankton cells have a typical atomic
composition of C106N16P, which means that 16 times as many atoms (and 7.2 times as many
grams) are needed of N than of P to produce phytoplankton. This means that one generally
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 201

finds a marked co-variation between phosphorus and nitrogen concentrations in aquatic

systems (see Wallin et al., 1992) and in this work total nitrogen (TN) concentrations have
been predicted from dynamically modeled monthly TP-concentrations using a regression
from Håkanson and Eklund, 2007). The regression is:

log(TN) = 0.70·log(TP) + 1.61 (4)

(r2 = 0.88; n = 58 coastal systems)

There are several reasons why we have not done any dynamic, process-based mass-
balance modeling for nitrogen. To the best of our knowledge, there are no general algorithms,
which could be used within the framework of existing general mass-balance models that can
quantify nitrogen fixation either from the atmosphere or from sources within a given aquatic
systems in a reliable manner. The main reason for this is the lack of well-tested, practically
useful approaches to predict the concentration of nitrogen fixing bluegreen algae. Studies
have shown (Rahm et al., 2000) that atmospheric nitrogen fixation may be very important in
contexts of mass-balance calculations for nitrogen in the Baltic Sea. Lacking empirically
well-tested algorithms to quantify atmospheric and internal nitrogen fixation, crucial
questions related to the effectiveness of remedial measures to reduce nutrient discharges to
aquatic systems cannot be properly evaluated. It also means that it is generally very difficult
to understand, model and predict changes in measured TN-concentrations in the water phase,
since such changes in concentrations are always mechanistically governed by mass-balances,
i.e., the quantification of the most important transport processes regulating the given
concentrations. The problem to understand and predict TN-concentrations in marine systems
is accentuated by the fact that there are no (to the best of our knowledge) practically useful
models to quantify the particulate fraction for nitrogen in saltwater systems (but such
approaches are available for phosphorus in lakes and brackish systems, see Håkanson and
Eklund, 2007). In mass-balance modeling, it is imperative to have a reliable algorithm for the
particulate fraction of nitrogen, since the particulate fraction (PF) is the only fraction that by
definition can settle out due to gravity. From previous modeling work (see, e.g., Floderus,
1989), one can conclude that it is also very difficult to quantify denitrification. Denitrification
depends on sediment red-ox conditions, i.e., on sedimentation of degradable organic matter
and the oxygen concentration in the deep-water zone, but also on the frequency of
resuspension events, on the presence of mucus-binding bacteria, on the conditions for
zoobenthos and bioturbation. Given this complexity, it is easy to understand why empirically
well-tested algorithms to quantify denitrification on a monthly basis do not exist to the best of
our knowledge. The atmospheric wet and dry deposition of nitrogen may be very large (in the
same order as the tributary inflow) and patchy (Wulff et al., 2001), which means that for, e.g.,
large coastal areas and relatively smaller systems far away from measurement stations, the
uncertainty in the value for the atmospheric deposition is also generally very large.
Total phosphorus is since long recognized as generally the most crucial limiting nutrient
for lake primary production (Schindler, 1977, 1978; Chapra, 1980; Boers et al., 1993; Wetzel,
2001). Nitrogen is regarded as a key nutrient in some marine areas (Redfield, 1958; Ryther
and Dunstan, 1971; Nixon and Pilson, 1983; Howarth and Cole, 1985; Howarth, 1988; Hecky
and Kilham, 1988; Ambio, 1990; Nixon, 1990). Håkanson et al. (2007) demonstrated from a
very comprehensive comparative study that only 9 systems out of 533 covering a very wide
size and salinity domain were nitrogen limited in the sense that the TN/TP-ratios were lower
202 Lars Håkanson and Maria I. Stenström-Khalili

than 7.2 for the growing season and 34% of the systems had TN/TP-ratios lower than 15.
They also demonstrated that there is an increasing risk for harmful algal blooms (of
cyanobacteria) when the TN/TP-ratio is below 15. One should note that also Guildford and
Hecky (2000) stressed that long-term nutrient limitation is generally governed by phosphorus
and not by nitrogen in both lakes and marine systems. This is a good reason for the mass-
balance modeling for phosphorus discussed in this work. There are also clearly increasing
risks of harmful algal blooms if the water temperature is above 15 °C (Edler, 1979;
Wasmund, 1997; Håkanson et al., 2007).
In this work, the modeling is done on a monthly basis and in the CoastMab-model there
is information on the dissolved fraction of phosphorus. This means that the basic approach for
the mean conditions during the growing season (ChlGS in µg/l; eq. 5) has been modified to
predict the requested mean monthly chlorophyll values (Chl). These calculations use simple
dimensionless moderators to account for seasonal/monthly changes in the light conditions
(DayL; mean monthly number of hours with daylight in the Himmerfjärden Bay; from
standard tables) and in the amount of bioavailable/dissolved phosphorus (DFSW). This means
the chlorophyll-a concentration are predicted from:

Chl = (DayL/12.3)·(DFSW/0.44)·ChlGS (5)

Where the basic model between the TP-concentration in the SW-layer (TPSW in µg/l,
modeled), the salinity in the SW-layer (SalSW, modeled) and ChlGS is given in table 7A.
(DayL/12.3) is a dimensionless moderator based on the ratio between the monthly DayL-
values divided by the mean annual number of hours with daylight (12.3) at this latitude (59
°N). The modeled monthly values of the dissolved fraction in the SW-layer (DFSW) have been
transformed into a dimensionless moderator by division with the average DF-value of 0.44 for
phosphorus in surface water conditions. This means that the predicted chlorophyll values are
low if DF is low, the number of hours with daylight low and the modeled TP-values low. The
small variations in salinity (see Figure 4A and B) will not influence the predicted Chl-values
very much, but such variations are also accounted for.
The basic model to predict mean chlorophyll-a concentrations for the growing season
from TP-concentrations was tested by Håkanson and Eklund (2007) and gave an average
error when empirical data were compared to modeled data of 0.06; the standard deviation for
the 21 tested coastal areas was 0.55, which corresponds to the 95% confidence interval for the
uncertainty in the empirical data. This means that it is probably not possible to predict better
than this. However, the range in the empirical data only covered coastal areas from the Baltic
Sea.
The empirically-based model to predict the total concentration of cyanobacteria
(Håkanson et al., 2007) is given in table 7B. The following simulations will use dynamically
modeled monthly TP-concentrations in the SW-layer, empirical mean monthly SW-
temperatures, dynamically modeled SW-salinities and modeled monthly TN-concentrations in
the SW-layer (see eq. 4) to predict monthly values of cyanobacteria in the SW-layer. Note
that there are no empirical data available to us to test the predicted values for cyanobacteria,
but these values are basically predicted from an empirical approach which yielded an r2-value
of 0.78 (coefficient of determination), which is close to the maximum possible predictive
power for cyanobacteria because of the inherently very high coefficient of variation (CV) for
cyanobacteria (see Håkanson et al., 2007). Nitrogen fixation by different species of
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 203

cyanobacteria counteracts long-term nitrogen deficits, and the N-fixation rate depends on the
TP-concentration, water temperature and the TN/TP-ratio (see Figure 4).
When the mean O2-concentration is lower than about 2 mg/l, and the mean oxygen
saturation (O2Sat in %) lower than about 20%, many key functional benthic groups are extinct
(Pearson and Rosenber, 1976). Empirical data on the amount of material deposited in deep-
water sediment traps (1 m above the bottom; SedDW in g dw/m2·day) were used in deriving
the model for oxygen used in this modeling (see eq. 6, from Håkanson, 2006). This empirical
model for oxygen is put into the dynamic SPM-model and the empirical data on
sedimentation in the deep-water zone (SedDW) will be replaced by modeled values of SedDW
from the dynamic SPM-model. The values for the O2-concentration (mg/l) calculated in this
manner for the growing season will be compared to empirical oxygen data from the
Himmerfjärden Bay.

O2=0.1·(101-10^(0.47+0.643·log(SedDW)+0.323·Dm^0.5-

0.118·(100·ET)^0.5+(1/QFS)·0.301·log(1+TDW)))) (6)

Of all the many factors that could, potentially, influence the O2-concentration in the DW-
zone, the following were shown (using stepwise multiple regression analysis using data from
23 Baltic Sea coastal areas) to be most important:

1. Sedimentation in the deep-water layer (SedDW); the more oxygen-consuming matter

in the deep-water zone, the lower O2.
2. The prevailing bottom dynamic conditions in the coastal area (ET, i.e., the erosion
and transport areas). If variations among coastal areas in ET are accounted for. If ET
is high (say 0.95), the oxygenation is also likely high and O2 high, and vice versa.
3. The theoretical deep-water retention time (TDW); variations in mean O2 among
coastal areas can also be statistically related to variations in TDW; the longer TDW, the
lower O2. This is logical and mechanistically understandable.
4. The mean depth (Dm); the mechanistic reason for this is not so easy to disclose since
Dm influences different factors, e.g., (1) resuspension, (2) the volume and hence all
SPM-concentrations, (3) stratification and mixing, and (4) the depth of the photic
zone and, hence, primary production. However, coastal areas with small mean depths
generally have clear water, little SPM, low sedimentation and high O2. Fine
suspended particles in open coastal areas will be transported out of the area and not
be entrapped in the same manner as in closed lagoons or lakes. If variations among
coastal areas in Dm are accounted for, the r2 value was 0.80 when tested for 23 Baltic
coastal areas (data from Wallin et al., 1992).
5. The oxygen model was basically derived using data from coastal areas without
freshwater inflow. For coastal areas with freshwater inflow, the factor QFS will
account for tributary influences (Qtrib) in the following way:

If Qtrib = 0 then QFS = 1 else QFS = ((Qtrib+Qsalt)/Qsalt)^(120/(1+TDW))) (6)

Where the theoretical deep-water retention time (TDW) is given in days. Dimictic
coastal areas in the Baltic Sea (i.e., coastal areas which become homothermal in the
204 Lars Håkanson and Maria I. Stenström-Khalili

spring and in the fall) rarely have longer characteristics TDW-values than 120 days.
Qsalt is the total inflow (QSW plus QDW) of saline water from the outside sea. This
means that if TDW is 12.3 days as it is in the Himmerfjärden Bay, if Qtrib is 1% of Qsalt
(see table 4), QFS is 2.2 and the predicted O2-concentration 7.3 mg/l and not 6.5 mg/l
as it would have been expected if the coastal area did not have any tributary inflow.

This oxygen model should not be used for coastal areas dominated by tides.

The following section will demonstrate how this modeling predicts the salinities in the
two layers, the TP-concentrations, Secchi depths, cyanobacteria and nitrogen concentrations
and also other variables of interest, such as TP-concentrations in sediments (0-10 cm) below
the theoretical wave base (the accumulation-area sediments), sedimentation in the two layers,
settling velocities for particulate phosphorus (and suspended particulate matter) and the
particulate fractions (PF = 1-DF). Whenever possible, the modeled values will be compared
to empirical data and to the uncertainty bands related to the empirical data. All calculated TP-
fluxes in Himmerfjärden Bay and all calculated TP-amounts (= where would one find the
TP?) will be given.

Table 7A. The model for chlorophyll-a (from Håkanson and Eklund, 2007).
The model predicts median summer values for chlorophyll
in surface water from total phosphorus and salinity

Chl = Ysal·TP
Ysal = if Y3 <0.012 then 0.012 elseY3
Y1 = if salinity < 2.5 then (0.20-0.1·(salinity/2.5-1)) else (0.20+0.02·(salinity/2.5-1))
Y2 = if salinity< 12.5 then Y1 else (0.28-0.1·(salinity/12.5-1))
Y3 = if salinity> 40 then (0.06-0.1·(salinity/40-1)) else Y2
Chl = chlorophyll-a concentration in μg/l; TP = TP-concentration in surface water in μg/l;
salinity in psu
Ysal = dimensionless moderator for the influence of salinity on chlorophyll
B. The model for cyanobacteria (from Håkanson et al., 2007). The model predicts median
summer values for total cyanobacteria in surface water from total phosphorus, total nitrogen,
salinity and surface-water temperatures.
CB = ((5.85·log(TP)-4.01)4)·YTNTP·YSWT·Ysal
YTNTP = if TN/TP < 15 then (1-3·(TN/TP/15-1)) else 1
YSWT = if SWT ≥ 15 then (0.86+0.63·((SWT/15)1.5-1)) else (1+1·((SWT/15)3-1))
Ysal = if salinity <10 then (2.1+1.1·((salinity/10)2-1)) else (2.1-115·((salinity/10)0.01-1))
CB in μg ww/l; salinity in psu; SWT= Surface water temperature in °C; Total-N (TN) in
μg/l; Total-P (TP) in μg/l
Model domain: 4 < TP < 1300; 165 < TN < 6830; 0 < salinity < 40; 8 < SWT < 25
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 205

4. RESULTS

4.1. Modeled Values versus Empirical Data

Figure 4 shows modeled values compared to the standard deviations for the mean
empirical values monthly data for the period 1997 to 2007. If the model yields values close to
the empirical mean value and in-between these two uncertainty bands, the predictions should
be regarded as good. For all these comparisons between modeled and empirical data, it should
be noted that:

1. The monthly tributary inflows of water, phosphorus and SPM have not been
calculated using actual monthly inflow data (since no such data are available to us).
This will explain some of the differences between the modeled and the measures
monthly values.
2. The monthly calculations of the inflow of water, salt, SPM and phosphorus from the
Baltic Proper use mean values for the SW and the DW-compartments not in the
inflowing water from the area outside the Himmerfjärden Bay, which would have
been more appropriate, but values from a single station meant to reflect the
conditions outside the bay in the Baltic Proper (see Figure 1). This likely also further
explains some of the differences between the modeled and the measured monthly
values.

With these reservations, one can note from Figure 4 that:

The TP-concentrations in the SW and DW-layer (Figure 4C and D) are within the defined
uncertainty bands of the empirical data.

1. The modeled chlorophyll concentrations give the ―twin-peak pattern‖ as indicated by

the empirical data but the predicted values are somewhat higher than the measured
data in connection to the two peaks but within the given uncertainty bands for the
main part of the growing season and for the winter period. It should be stressed that
the chlorophyll concentrations are predicted from a regression based on dynamically
modeled TP-concentrations in the surface water, the predicted salinities in the SW-
layer and a dimensionless moderator for the average light conditions at this latitude.
A simple and typical form of a dimensionless moderator is, e.g., the ratio between a
mean monthly value, MM, and a mean annual value, AM. In traditional mass-balance
models, one would multiply an amount (kg) by a rate (1/month) to get a flux (i.e.,
amount·rate or amount·rate·1). In this model, one multiplies kg·(1/month)·Y (=
amount·rate·mod), where Y is a dimensionless moderator quantifying how an
environmental variable influences the given flux (e.g., sedimentation of particulate
phosphorus). Instead of building a large mechanistic sub-model for how
environmental factors influence given rates, this technique uses a simple, general
algorithm for the moderator. Empirical data can be used for the calibration of the
moderator. The modeled values also account for biouptake in biota with short
turnover times, but they do not include any considerations to the biouptake and
retention of phosphorus in biota with long turnover times (such as fish, zoobenthos,
206 Lars Håkanson and Maria I. Stenström-Khalili

macrophytes). Given the limitations of the modeling for chlorophyll, one can
conclude that the overall correspondence is relatively good.
2. The predicted Secchi depths are also quite close to the empirical values and the
temporal patterns agree quite well.
3. The oxygen concentrations in the DW-layer (Figure 4G) are within the defined
uncertainty bands of the empirical data for the growing season.
4. The predicted TP-concentrations in the accumulation areas sediments (0-10 cm; 0.61
mg/g dw; dw = dry weight) below the wave base of 19 m (Figure 4H) are within the
minimum and maximum lines defined for Baltic Sea coastal sediments (see
Håkanson and Eklund, 2007) of 0.5 to 2.5 mg/g dw.
5. The TN-concentrations are predicted from a regression (eq. 4) using dynamically
modeled TP-concentrations in the SW-compartment. There is a relatively good
correspondence between modeled and measured TN-concentrations (Figure 4I).
6. The TN/TP-ratios based on modeld values are given in Figure 4J in relation to the
Redfield-ratio of 7.2 (in g) and the Threshold-ratio of 15 for cyanobacterial (see
Håkanson et al., 2007). The monthly TN/TP-ratios are clearly higher than 7.2 all
months, and higher than 15 most summer months. Given the situation in the
Himmerfjärden Bay, as revealed by these data, a lowering of the TN/TP-ratio will
imply greater risks for blooming of cyanobacteria. So, to reduce the nitrogen
concentration is useless when the TN/TP-ratio is higher than 15, and harmful when
the TN/TP-ratio is lower than 15, since this would stimulated the growth of
cyanobacteria, which should be avoided. The focus should instead be set on
reductions of the major anthropogenic fluxes of phosphorus to the Baltic Proper.
7. The predicted concentrations of cyanobacteria in Himmerfjärden under default
conditions are given in Figure 4K. Under calm conditions when these algae will float
to the surface, the concentrations in the upper meter of water may be many times
higher than the mean values for the entire SW-layer shown in Figure 4K.
8. The modeled SPM-concentrations in the SW and DW-compartments are shown in
Figure 4L. These values will, together with the modeled salinities in Figure 4A and
D, determine the values for the Secchi depth given in Figure 4F. For the open Baltic
Sea, a default value of 3 mg/l (from Pustelnikov, 1977) has often been used.
Håkanson and Eckhell (2005) have presented more data on SPM-concentrations in
the Baltic Proper and those data also indicate that typical values in the SW-layer are
between 0.1 and 14 mg/l with a mean value of about 2 mg/l. The predicted values in
Himmerfjärden Bay agree quite well with the empirical data from those studies.

From Figure 4, one can conclude that the CoastMab-model predicts the target variables
quite well given the factual limitations in the seasonal patterns in the driving variables for
tributary water discharge (since this pattern in the modeling is not based on measured data for
the modeled period) and in the seasonal pattern for the TP and SPM-concentrations outside
Himmersfjärden Bay. Note that there has been no tuning of the model to achieve these
predictions and that the basic model has been shown to describe the transport processes for
phosphorus very well for many other coastal areas (see Håkanson and Eklund, 2007). This
should lend credibility to the following simulations.
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 207

Table 8. A ranking of the annual fluxes (t/yr), as calculated using the CoastMab-model
based on the monthly fluxes (t/month) of TP to, in and out of the Himmerfjärden Bay.
The key fluxes for remedial measures are bolded. F = flux, SW = surface water, DW =
deep water, HI = Himmerfjärden Bay, BP = Baltic Proper, trib = tributary, d = diffusive
flux, x = mixing flux, LU = land uplift, ET = erosion and transport areas for fine
sediments, A = accumulation areas for fine sediments, BS = biota with short turnover
times, bur = burial

Month 1 2 3 4 5 6 7 8 9 10 11 12 Annual
FTPBSSW 13.6 26.3 99.2 216.2 151.9 142.9 139.9 141.8 249.1 209.8 109.7 20.0 1521
FTPSWBS 12.3 28.8 109.1 67.5 151.5 141.5 140.5 142.1 260.1 197.7 96.1 20.0 1367
FTPSWHIBP 136.3 130.0 114.2 95.8 77.9 70.2 69.2 74.2 111.5 128.4 126.5 135.1 1269
FTPSWBPHI 122.1 110.4 89.7 73.8 73.2 67.1 72.6 78.2 93.4 104.9 109.6 125.0 1120
FTPETSW 14.1 14.1 12.1 2.5 3.9 4.8 5.8 10.3 61.7 28.0 15.7 13.5 187
FTPDWHIBP 15.5 14.8 13.0 11.4 11.3 12.2 12.8 14.0 19.3 15.6 14.3 15.6 170
FTPDWBPHI 14.0 13.2 11.0 9.6 10.1 11.0 11.2 11.7 12.2 12.1 13.7 15.0 145
FTPLU 10.4 10.3 10.3 10.3 10.3 10.3 10.2 10.2 10.2 10.3 10.4 10.4 124
FTPSWET 7.5 6.7 6.8 8.0 8.5 9.6 10.3 12.8 17.8 10.7 7.0 7.7 113
FTPDWSWx 9.5 9.9 7.1 0.9 0.5 0.3 0.3 0.4 6.4 9.4 10.1 8.8 64
FTPETDW 4.4 4.4 3.8 0.8 1.2 1.5 1.8 3.2 19.1 8.7 4.9 4.2 58
FTPSWDWx 9.0 9.2 5.7 0.5 0.2 0.1 0.1 0.1 2.2 5.7 8.1 8.2 49
FTPMWSWd 3.8 3.4 2.3 1.5 1.5 1.9 2.2 2.9 7.5 3.9 3.1 4.0 38
FTPSWDW 1.8 1.6 1.7 2.0 2.1 2.3 2.5 3.1 4.3 2.6 1.7 1.9 28
FTPtrib 2.8 2.3 2.5 3.1 3.1 1.8 1.4 1.3 1.4 1.6 2.1 2.5 26
FTPplantSW 1.6 1.6 1.6 1.6 1.6 1.6 1.6 1.6 1.6 1.6 1.6 1.6 19
FTPDWA 0.7 0.8 0.7 0.0 0.0 0.0 0.0 0.1 4.6 1.8 0.8 0.7 10.3
FTPbur 1.0 1.0 0.8 0.7 0.8 0.7 0.7 0.8 0.7 0.7 0.8 0.9 9.6
FTPprec 0.04 0.04 0.04 0.04 0.04 0.04 0.04 0.04 0.04 0.04 0.04 0.04 0.54
FTPplantDW 0.02 0.02 0.02 0.02 0.02 0.02 0.02 0.02 0.02 0.02 0.02 0.02 0.20
FTPADWd 0.005 0.005 0.005 0.005 0.005 0.005 0.005 0.005 0.005 0.005 0.005 0.005 0.06

4.2. Fluxes and Amounts of Phosphorus

Which are the large and the small TP-fluxes? And where is the phosphorus stored? Table
8 gives a compilation of all monthly TP-fluxes and a ranking of the annual fluxes. One can
note that the two largest fluxes are biouptake and retention (=outflow) of phosphorus to and
from biota. These fluxes are significantly larger than the fluxes related to in and outflow of
TP between the Baltic Proper and the Himmerfjärden Bay. The fluxes that may be reduced by
remedial measures are bolded in table 8 - the SW-inflow from the Baltic Proper (FTPSWBPHI =
1120 t/yr), inflow to the DW-layer from the Baltic Proper (FTPDWBPHI = 170 t/yr, tributary
inflow (FTPtrib = 26 t/yr) and TP from the purification plant (FTPplant = 19 t/yr). From this, it is
evident that smaller reductions of the TP-emissions (say a factor of 2-4) from the plant will
have small effects on the conditions in the bay. The phosphorus fluxes are dominated by the
exchange processes between the coast and the sea.
The diffusive flux from the accumulation areas sediment (below the theoretical wave
base at 19 m) is very small (<1 t/yr). The modeled TP-concentration in these sediments (0-10
cm) is 0.61 mg/g dw. This model provides values based on the total TP-inventory in the entire
208 Lars Håkanson and Maria I. Stenström-Khalili

area below the theoretical wave base down to 10 cm of sediments. The biologically passive
sediments below 10 cm are expected to have a TP-concentration of about 0.45 in the Baltic
Proper (Jonsson et al., 1990) and this value is also used in this modeling for the
Himmerfjärden Bay. This means that only a small fraction (related to the difference between
0.61 and 0.45) of the phosphorus in the accumulation area sediments could be available for
diffusive transport from these sediments. But the diffusion also depends on the redox-
conditions in the sediments, which depend on the sedimentation of organic matter. The
average values for total sedimentation calculated by the model vary between 0.1 and 0.3
mm/yr or between 10 and 20 µg/cm2·d on the accumulation areas. The modeled water content
(W) of the accumulation area sediments (0-10 cm) is 75% ww, the modeled organic content
(loss on ignition, IG) is 6.3 %dw and the bulk density (d) 1.17 g/cm3. Table 4 gave modeled
values for the SW and DW-water inflow from the Baltic Proper (QSWBPGE = 4050·106
m3/month and QDWBPGR = 450·106 m3/month); modeled monthly tributary inflow (Qtrib);
theoretical water retention times in the SW and DW-layers (TSW = 0.62 months and TDW =
0.41 months, since the DW-volume is small), as calculated from the mass-balance for salt;
fall velocities for particulate phosphorus and suspended particulate matter in the SW and
DW-layers (vSW 2.4 m/month and vDW 2.3 m/month); the particulate TP-fractions in the SW
and DW-layers (PFSW 0.20 to 0.87 and PFDW 0.01 to 0.53; see table 6).
It should also be stressed that land uplift (FLU) is a rather important individual input of TP
to the bay (124 t/yr).
It is interesting to note the difference between fluxes and amounts (compare the results in
table 8 with the data in table 9). The largest TP-fluxes are to and from biota, but the total TP-
inventory in biota is only 16.8 t TP or 6% of the total inventory. By far most TP is found in
the accumulation area sediments (191 t or 66% of the total amount).

Table 9. Amounts of TP (t) in the different compartments; accumulation areas in the

DW-compartment (A-areas), in biota with short turnover times (Biota), in the DW-
layer, in areas of fine sediment erosion and transport (ET) and in the SW-layer.
MV = mean value; M50 = median; SD = standard deviation

Month A-areas Biota DW ET-areas SW

1 192 1.8 8.1 7.5 85.9
2 192 3.5 7.7 6.5 80.3
3 192 13.3 6.8 6.6 60.2
4 191 27.3 5.9 9.0 34.0
5 191 20.2 5.9 23.1 29.8
6 190 19.0 6.4 36.6 26.3
7 189 18.7 6.7 49.7 26.2
8 189 18.9 7.3 61.1 29.2
9 190 33.3 10.1 42.4 39.3
10 192 27.9 8.1 14.3 55.3
11 192 14.5 7.5 6.9 67.2
12 192 2.7 8.1 7.7 84.5 Sum
MV 191 16.8 7.4 22.6 51.5 289
% 66 6 3 8 18 100
M50 191 18.8 7.4 11.7 47.3
SD 1.2 3.6 7.8 6.7 82.3
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 209

5. PREDICTING THE DYNAMIC RESPONSE OF THE SYSTEM

TO CHANGES IN NUTRIENT LOADING

The simulations to estimate a realistic response to changes in nutrient loading will be

presented in four steps. The first step concerns a two-fold increase in the direct emissions
from the plant to mimic the experiment of 1983. The next example concerns a 10-fold
increase in these direct emissions of TP from the plan. The third case concerns a 10%
increase in the TP and SPM-concentrations in the sea outside of Himmerfjärden Bay. The
fourth test concerns a 10% reduction in TN-concentrations in the SW-layer in the bay. These
four cases will be compared to the default values representing the conditions today (1997-
2007). We will also show the dynamic response of the system to sudden changes in the
nutrient loading. The results are complied in table 10:

Table 10. Results related to how changes in phosphorus loading to Himmerfjärden Bay
would likely influence TP-concentrations in SW, TP in DW, Secchi depth, chlorophyll,
cyanobacteria and oxygen concentrations if the default TP input from the plant is
increased by a factor of 2, by a factor of 10, if the TP-inflow from the Baltic Proper is
increased by 10% or if the TN-concentration in the bay is decreased by 10%

TPSW (µg/l) Chlorophyll (µg/l)

Month Default 2·plant 10·plant 1.1·TPsea 0.9·TN Month Default 2·plant 10·plant 1.1·TPsea 0.9·TN
1 33.2 33.6 36.5 36.3 33.2 1 2.0 2.0 2.2 2.2 2.0
2 31.7 32.1 35.0 34.7 31.7 2 3.7 3.8 4.1 4.1 3.7
3 27.8 28.2 31.1 30.4 27.8 3 9.4 9.5 10.5 10.2 9.4
4 23.2 23.6 26.5 25.4 23.2 4 2.6 2.6 3.0 2.8 2.6
5 18.9 19.3 22.0 20.7 18.9 5 2.7 2.7 3.1 3.0 2.7
6 17.2 17.5 20.3 18.8 17.2 6 1.8 1.8 2.1 2.0 1.8
7 17.0 17.3 20.1 18.6 17.0 7 1.5 1.5 1.8 1.6 1.5
8 18.2 18.5 21.3 20.0 18.2 8 2.0 2.0 2.3 2.2 2.0
9 27.4 27.8 31.0 29.8 27.4 9 6.4 6.5 7.3 7.0 6.4
10 31.5 31.9 35.1 34.2 31.5 10 6.8 6.9 7.6 7.4 6.8
11 30.9 31.3 34.4 33.7 30.9 11 6.1 6.2 6.8 6.7 6.1
12 32.9 33.3 36.3 36.0 32.9 12 2.3 2.4 2.6 2.6 2.3
MV 25.8 26.2 29.1 28.2 25.8 MV 3.9 4.0 4.4 4.3 3.9
Diff. 0.4 3.3 2.4 0.0 Diff. 0.1 0.5 0.4 0.0
M50 27.6 28.0 31.0 30.1 27.6 M50 2.6 2.7 3.1 2.9 2.6
SD 6.5 6.6 6.7 7.1 6.5 SD 2.6 2.6 2.9 2.8 2.6
TPDW (µg/l) Cyanobacteria (µg/l)
1 34.3 34.6 36.7 36.7 34.3 1 0.2 0.2 0.2 0.2 0.2
2 32.9 33.2 35.6 35.2 32.9 2 0.5 0.5 0.7 0.7 0.6
3 28.9 29.2 31.4 31.0 28.9 3 7.0 7.4 10.4 9.6 8.1
4 25.3 25.6 27.8 27.1 25.3 4 76 81 130 109 90
5 25.2 25.5 27.8 27.0 25.2 5 118 125 208 153 119
6 27.2 27.5 29.9 29.2 27.2 6 138 147 227 183 138
7 28.6 28.9 31.2 30.6 28.6 7 151 160 249 201 151
8 31.1 31.4 33.8 33.2 31.1 8 162 172 255 213 162
9 43.0 43.3 45.9 45.3 43.0 9 356 375 535 473 400
10 34.6 34.9 37.6 36.7 34.6 10 191 198 264 245 209
11 31.9 32.2 34.4 34.1 31.9 11 32 34 45 43 36
210 Lars Håkanson and Maria I. Stenström-Khalili

Table 10. (Continued)

TPDW (µg/l) Cyanobacteria (µg/l)
Month Default 2·plant 10·plant 1.1·TPsea 0.9·TN Month Default 2·plant 10·plant 1.1·TPsea 0.9·TN
12 34.7 34.9 37.1 37.1 34.7 12 0.9 0.9 1.2 1.2 1.0
MV 31.5 31.8 34.1 33.6 31.5 MV 103 108 160 136 110
Diff. 0.3 2.6 2.1 0.0 Diff. 5.4 57.5 32.9 6.7
M50 31.5 31.8 34.1 33.6 31.5 M50 97 103 169 131 105
SD 5.0 5.0 5.1 5.1 5.0 SD 107 112 162 141 117
Secchi (m) Oxygen concentration (mg/l)
1 9.1 9.1 9.1 8.3 9.1 1 0 0 0 0 0
2 9.1 9.1 9.1 8.3 9.1 2 0 0 0 0 0
3 6.9 6.9 6.8 6.4 6.9 3 0 0 0 0 0
4 5.6 5.5 5.4 5.2 5.6 4 0 0 0 0 0
5 6.7 6.7 6.5 6.3 6.7 5 7.0 7.0 7.0 6.9 7.0
6 6.3 6.3 6.1 5.8 6.3 6 6.5 6.5 6.5 6.4 6.5
7 6.3 6.3 6.1 5.8 6.3 7 6.2 6.2 6.1 6.0 6.2
8 6.6 6.6 6.4 6.1 6.6 8 6.5 6.5 6.4 6.3 6.5
9 5.9 5.8 5.6 5.5 5.9 9 7.5 7.5 7.4 7.3 7.5
10 6.0 6.0 5.8 5.7 6.0 10 0 0 0 0 0
11 6.4 6.3 6.2 5.9 6.4 11 0 0 0 0 0
12 8.5 8.5 8.4 7.7 8.5 12 0 0 0 0 0
MV 6.9 6.9 6.8 6.4 6.9 MV 6.8 6.7 6.7 6.6 6.8
Diff. 0.0 -0.1 -0.5 0.0 Diff. -0.06 -0.13 -0.23 -0.05
M50 6.5 6.5 6.3 6.0 6.5 M50 6.5 6.5 6.5 6.4 6.5
SD 1.2 1.3 1.3 1.1 1.2 SD 0.50 0.50 0.51 0.53 0.50

The predicted values for TP-concentrations in the SW-layer, TP-concentrations in the

DW-layer, Secchi depths, chlorophyll-a concentrations, concentrations of cyanobacteria and
the oxygen concentrations in the deep-water layer at steady-state are given for the four cases
and the results are compared to the default conditions. Case 1 (a 2-fold increase of TP-
emissions from the plant) would influence the system very little, e.g., the mean annual TP-
concentration would increase from 25.8 µg/l to 26.2 µg/l and the Secchi depth would not
change at all.
Case 2 (a 10-fold increase in TP-emission from the plant) would, influence the system
markedly. The TP-concentrations in the SW-later would increase by 3.3 µg/l, the average
chlorophyll concentration would increase by 4.4 µg/l, the maximum concentration of
cyanobacteria would increase from 360 to 540 µg/l.
Case 3 (a 10% increase in TP and SPM-inflow from the sea) would also create substantial
changes corresponding to the changes in case 2.
Case 4 (a 10% reduction in TN-concentrations in the bay) would only change the
predicted concentration of cyanobacteria, which would increase from a maximum value of
360 to a maximum monthly value of 400 µg/l. Note that, as explained, we have not modeled
the TN-concentrations dynamically.
The dynamic response of the system related to sudden 2-fold and 10-fold increases in the
TP-emissions from the plant month 25 are shown in Figure 5. One can see from Figure 5, that
the system will reach a new steady-state within a year. The main reason for this quick
adjustment is related to the relatively fast water turnover of the system. The theoretical
surface-water retention time is about 19 days, i.e., about 19 total water exchanges per year
with the outside sea.
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 211

40 25
A.
10

TP-conc. in SW (µg/l)
1- 2

25

10
1 25 49 73 97
Months
14
B.
Chlorophyll (µg/l)

10
7
1- 2

0
1 25 49 73 97
Months
600
C. 10
Cyanobacteria (µg/l)

1- 2

300

0
1 25 49 73 97
Months

Figure 5. Illustration of the dynamic response of the system (Himmerfjärden Bay) to sudden 2-fold and
10-fold increases in phosphorus loading from the treatment plant in the bay month 25 (January) for A.
TP-concentrations in the SW-layer, B. chlorophyll-a concentrations and C. concentrations of
cyanobacteria

We also believe that these results largely explain important aspects of previous results
related to the experiments carried out during the last 25 years (see the background given in
section 2.1) and that, since these results are based on a general process-based modeling
approach, which may be applied to most coastal areas, one would also hope that this type of
analysis could be more widely used.
The results given in the tables for the phosphorus fluxes and in Figure 5 indicate that for
this, and many other coastal bays, it seems very important to lower the nutrient concentrations
in the outside sea. This will be shown in the next scenario. The background for this scenario
is as follows: Today HELCOM has adopted a new strategy (HELCOM, 2007) to lower the
eutrophication in the Baltic Sea by suggesting that 133,000 tons of nitrogen and 15,000 tons
of phosphorus should be reduced from the present annual nutrient loading to the system. One
can safely assume that it is practically impossible to remediate all human emissions of TP to
the Baltic Sea. The 15,000 t/yr suggested by HELCOM (2007) represent a reduction of 50%
of the 30,000 t/yr of TP transported via rivers/countries to the Baltic Sea. From Sweden and
other countries or regions, which have already carried out costly measures to reduce nutrient
discharges to the Baltic Sea, one can assume that only a smaller part of the remaining
212 Lars Håkanson and Maria I. Stenström-Khalili

anthropogenic nutrient fluxes can be reduced, as suggested by HELCOM (e.g., 290 t/yr from
Sweden). In the following scenario, TP will be cut off a given month, month 25 (i.e., in
January). How would the Baltic Sea system react to such a hypothetical sudden change? This
has been discussed in great detail by Håkanson and Bryhn (2008b) and in this scenario we
will use results from those simulations and apply the results for the conditions in the
Himmerfjärden Bay. Note that HELCOM (2007) did not suggest that one should reduce the
nutrient loading suddenly, as this scenario simulates, only gradually. In this scenario, we will
also give predicted monthly data on Secchi depths, chlorophyll, cyanobacteria and
phosphorus concentrations.
Håkanson and Bryhn (2008b) challenged HELCOM‘s strategy and motivated and
presented a scenario (called the ―optimal‖ scenario) with a total reduction of 9775 t/yr of
phosphorus (and no reductions in nitrogen emissions) and of these reductions 6625 t/yr (48%
of anthropogenic emissions) are removed from the countries/rivers adding nutrients to the
Baltic Proper, 2725 t/yr from the Gulf of Finland (corresponding to 60% of the anthropogenic
input) and 425 t/yr of TP to the Gulf of Riga (or 46% of the anthropogenic input to this
basin). This would give a Secchi depth of 7 m in the Gulf of Finland on an average annual
basis, a Secchi depth of almost 10 m (9.7 m) in the Bothnian Sea, of about 8 m in the
Bothnian Bay, 5.6 m in the Gulf of Riga and almost 8 m (7.9 m) in the Baltic Proper. These
conditions would be close to the situation in the Baltic Sea as it was before the main
eutrophication started in 1920. After 1980 trend analyses based on comprehensive data show
that the Baltic Sea system is slowly recovering (Håkanson and Bryhn, 2008b).

40
A. Surface water (0-44 m), entire Baltic Proper
TP-concentration (µg/l)

9775 t TP removed "optimally"

20

0
1 61 121 181 241
Months
100
B. Middle water (44-75 m), entire Baltic Proper
TP-concentration (µg/l)

9775 t TP removed "optimally"

50

0
1 61 121 181 241
Months

Figure 6. Simulation results for the TP-concentrations in the surface and middle-water layers in the
Baltic Proper to illustrate how the system of connected sub-basins forming the Baltic Sea would likely
react to reductions in phosphorus loading. The ―optimal‖ remedial strategy means that 6625 t TP to the
Baltic Proper, 2725 t TP to the Gulf of Finland and 425 t TP to the Gulf of Riga, would be reduced
month 25. Data from Håkanson and Bryhn (2008b)
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 213

Figure 7. Illustration of the dynamic response of the system (Himmerfjärden Bay) to sudden total
reductions (month 25) of all phosphorus emissions from the local treatment plant (curves 2) and to the
―optimal‖ remedial scenario for the Baltic Sea (from Håkanson and Bryhn, 2008) with a reduction of
6625 t phosphorus to the Baltic Proper, 2725 t phosphorus to the Gulf of Finland and 425 t phosphorus
to the Gulf of Riga (curves 3) for A. TP-concentrations in the SW-layer, B. chlorophyll-a
concentrations, C. concentrations of cyanobacteria and D: Secchi depths

Figure 6 gives results where the consequences of nutrient reductions have been simulated
using the CoastMab-model for the entire Baltic Sea (from Håkanson, and Bryhn, 2008b).
Figure 6 gives the results for the surface water (0-44 m) and middle-water layers (44 to 75 m)
in the entire Baltic Proper. In the following simulations, we have used the data given in
Figure 6, but since these values are close to but not identical with the data from the reference
site just outside the Himmerfjärden Bay, we have adjusted these vector files to the mean
monthly values from the reference site outside the bay. This means that, e.g., the average
annual surface-water concentration for TP for the Baltic Proper is a factor of 1.083 higher
than the data given in Figure 6.
This ―optimal‖ scenario would imply that the primary phytoplankton production would
go down by, on average, 35-40% in the Baltic Proper. Furthermore, the risks of harmful algal
blooms (of cyanobacteria) would be significantly reduced, by a factor of 3 to 5 in the Baltic
Proper. It is also interesting to note the dynamic response of the system. In these scenarios
with the hypothetical sudden reduction a given month (month 25), there are two response
phases related to TP-concentrations in water, first an initial quick response of about 6 years
(72 months) and then a much slower response and that after about 10 years, the system has
almost reached a new steady state. To reach a new steady-state takes longer in the sediments.
To see how these changes in the Baltic Proper would influence the Himmerfjärden Bay
compared to reductions in direct TP-loading to the bay, we have set all TP-emissions from the
treatment plant to zero month 25.
The results are given in Figure 7 for the TP-concentrations (A), the chlorophyll-a
concentrations (B), the concentrations of cyanobacteria (C) and the Secchi depths (D). One
can note very small improvements indeed if the direct TP-emissions from the plant are
removed (curve 2 as compared to curve 1, which gives the default condition), but significant
214 Lars Håkanson and Maria I. Stenström-Khalili

changes when 9775 t of TP are removed according to the ―optimal‖ scenario: The average
annual TP-concentration would go down from almost 26 µg/l to 17.4 µg/l, the concentrations
of chlorophyll and cyanobacrteria would follow the reduction in TP and the Secchi depth
would likely increase from about 7 to about 7.5 m.

6. CONCLUDING REMARKS
This work has presented a general method to calculate how a given coastal area would
likely respond to changes in nutrient loading. This approach makes it possible to carry out
structured analyses of the costs and environmental benefits of remedial actions designed to
reduce nutrient input to coastal areas and to put such reductions or changes into a process-
based holistic context where all important transport processes to, within and from the given
coastal area are accounted for on a monthly basis to achieve seasonal variations, which is
essential for most biological variables and key bioindicators of coastal eutrophication. The
dynamic modeling also provides quantitative values of the time-dependent response of the
system. The method discussed here may be applied to most coastal systems and the data
necessary for this analysis have also been discussed.
These results demonstrate that the conditions in the case-study area, the Himmerfjärden
Bay, are dominated by the water exchange between the bay and the outside sea (the Baltic
Proper). The theoretical surface-water retention time is 19 as days, as determined using the
mass-balance model for salt, which is based on comprehensive and reliable empirical data.
This means that although this bay is quite enclosed, with an exposure of 0.0194, it is still
dominated by the water exchange towards the sea. Local emissions of nutrients to the
Himmerfjärden Bay are small compared to the nutrient fluxes from the sea. If the conditions
in this, and many similar bays, are to be improved, it is very important to lower the nutrient
concentrations in the outside sea. To do that in the best possible manner, one must apply the
same process-based mass-balance principles for the larger system as discussed in this work
for a coastal bay. This means that the major phosphorus fluxes to the sea, in this case the
Baltic Proper, should be reduced in the most cost-efficient manner. That remedial strategy has
not penetrated fully into management decisions neither for the Himmerfjärden Bay nor for the
Baltic Proper or the Baltic Sea.

ACKNOWLEDGMENTS
This work has been carried out within the framework of the Thresholds-project, an
integrated EU project coordinated by Prof. Carlos M. Duarte, CSIC-Univ. Illes Balears,
Spain, and we would like to acknowledge the financial support from the EU.
 How Important Are Local Nutrient Emissions to Eutrophication in Coastal Areas… 215

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 219-247 © 2011 Nova Science Publishers, Inc.

Chapter 7

ENVIRONMENTAL CONSEQUENCES OF
INNOVATIVE DREDGING IN COASTAL
LAGOON FOR BEACH RESTORATION

Emmanuel Lamptey*
Department of Oceanography and Fisheries, University of Ghana, Legon, Ghana

ABSTRACT
Evidence suggests that hydraulic dredging is accompanied by considerable adverse
environmental impacts on the receiving ecosystem especially on the benthos and water
quality. Recently, innovative dredging is designed to minimise environmental impacts
and enhance the ecological settings. Evaluations of environmental consequences of such
innovative dredging are essential to quantify the ecological benefits and the associated
impacts to ensure good environmental management. Congruently, innovative dredging
(‗design with nature‘ principle) in a large tropical coastal lagoon in Ghana (Keta lagoon),
West Africa, was assessed Before, During and After dredging operations on spatio-
temporal scales to ascertain the environmental impacts on the macrobenthic fauna,
shorebirds and water quality. A total of 9091 million cubic meter of sediment was
removed from the 8m stretch of the lagoon for beach nourishment, land reclamation and
creation of habitat islands. The macrobenthic fauna was sampled once in 2000 (Before),
2001 (During) and 2002 (After) along seven stations (A-0 to G-0 of 1-km interval) in the
dredged channel. Water quality was assessed at the subsurface and bottom layers
quarterly from June, 2001 to September, 2002. The shorebirds community abundance
were quantified monthly from August 2000 to 2002, but only parallel data from August-
December (peak periods of shorebirds abundance) of each year (2000-2002) was used for
statistical analyses.
The results demonstrate that dredging had initial adverse effects on numerical
abundance of macrobenthic fauna but with evidence of recovery a year after the dredging
(2002). Species recorded in 2001(During Dredging) and 2002 (After Dredging) were very
similar in terms of composition particularly in the wet periods, suggesting the influence
of seasonal environmental factors. The abundance of the species showed significant

*
Corresponding author: elamptey@ug.edu.gh, Tel: +233 24 483 1455, Fax: +233 21 520298
220 Emmanuel Lamptey

spatio-temporal variations (p<0.05). The macrobenthic fauna was dominated by

opportunistic species of the family Capitellidae. Although, Nepthys lyrochaeta revealed
higher frequency of occurrence (52%), there was significant (p<0.05) decrease in
abundance after dredging (2002). Conversely, Notomastus cf. latericeus depicted
significant (p<0.05) increase (recovery) after dredging (2002).
There was no apparent impact on coastal avifauna although numerical abundance of
wader group decreased from 78% in 2000; 69% in 2001 to 51% in 2002. Conversely,
terns showed increased abundance from 17% in 2000, 21% in 2001 and 47% in 2002
indicating positive impact. The shorebirds placed in the ‗others‘ category experienced
peak and trough between the period (6% in 2000; 10% in 2001, and 2% in 2002). In
general mean numerical abundance of the shorebirds increased from 8.8% in 2000
(Before) to 81.5% in 2002 (After) of the periods.
Temporal and spatial variability occurred in the physicochemical parameters
measured (e.g., salinity, total dissolved solids, total suspended solids and sulfate).
However, elevated turbidity occurred in localised areas along the fetch during the
dredging operation. The results of the analysis presented are pertinent to several
questions, such as what are the expected ecological benefits of innovative dredging and
adverse impacts on the receiving ecosystem.

Keywords: Innovative Dredging, Environmental Impacts, Ecological Benefits, Coastal

Lagoon, Macrobenthic Fauna, Coastal Avifauna, Water Quality

1.0. INTRODUCTION
Coastal lagoons are fragile ecosystems but accounts for 13-15% of the world‘s littoral
zone [Kjerfve, 1994, Marcovecchio et al. 2005]. They are highly productive than several
riverine and estuarine ecosystems in terms of fisheries yield [Kapetsky, 1984], attributable to
high primary production as a sequel of nutrients inflow from land drainages [Nixon, 1982].
Coastal lagoons constitute an essential environmental reservoir for fluvial sediments due to
their capacity to retain them and therefore accompanied elemental pollutants.
In recent times it has been a common practice to redistribute large amount of coastal
sediments for beach nourishment projects to combat shoreline retreat. The problem of
beach/coastline recession/erosion are as a result escalating impacts of emerging global
geophysical changes, such as rising sea levels, and coastal development [Rakocinski, 1996].
Engineered solutions of massive dredge-and-fill methods have increasingly been adopted
worldwide. But the activities accompanying dredge-and-fill projects such as the dredging
itself, transportation and disposal of dredged materials result in adverse environment impacts
to the ecology and economy of the receiving ecosystem. There is a huge body of literature
that have documented adverse environmental impacts of dredging on the benthos, and water
quality characteristics [ICES 1992, 2000; Kenny, 1995; Newell et al., 1998; Bemvenuti et al.,
2005] with relatively few on aquatic shorebirds (Grippo et al., 2007). Other reports
nonetheless have indicated beneficial uses of the dredged materials for beach nourishment,
land reclamation, berm creation, replacement fill, capping and habitat creation for wildlife
utilization leading to increased biodiversity and economic improvement [Krause and
McDonnel, 2000]. However, evidence of benefits of restoration to wildlife is still somewhat
ambiguous [Simenstad et al., 2005]. It is uncertain if restoration projects increased habitat use
by wildlife or not. Therefore monitoring and assessment of environmental consequences of
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 221

dredge-and-fill projects is a fundamental step towards understanding the associated impacts in

particular biological resource responses.
Relatively very few studies have addressed the environmental consequences (adverse
impacts & beneficial uses) of dredging. The extent of dredging impacts on the environment
may depend on a number of factors including location, characteristics of the bottom sediment
and surface water, the methods of dredging and timing, sensitivity of the ecosystem, and
ecological objective. The difficulty in predicting the type of response from organisms in
ecosystem subjected to dredging requires that studies and analyses of such effects be
conducted on a case-by-case basis [Harvey et al., 1998]. As such, environmental studies
investigating impacts of dredging (physical disturbance) on the biological resource and water
quality are essential requirements for biodiversity resource management. When an impact
causes complete loss of biological community and deterioration of water quality, studies of
environmental impacts are useful in assessing recovery/amelioration and also an empowering
tool for sustainable development.
A variety of study designs existed to detect and assess effects of impacts of general
anthropogenic activities in aquatic systems. Green‘s [1979] BACI (Before-After-Control
Impacts) design have been extensively used in such impact studies where samples are taken
before and after a planned impact. It is believed that such design may confound the effects of
the impacts with other types of unique natural fluctuations that occur at one site but not at the
other [Osenberg and Schmitt, 1996; Hurlbert, 1984; Stewart-Oaten et al., 1986]. This is
because anthropogenic sources of stress, often interact with natural processes [Gaston and
Edds, 1994; Gaston, 1985; Parker et al., 1980]. A recent design suggests sampling before and
after the impacts, at several control sites temporally [Underwood, 1992, 1994].

1.1. Geomorphology and Sedimentation of Coastal Lagoon

A coastal lagoon is a shallow water body separated from the ocean by a barrier,
connected at least intermittently to the ocean by one or more restricted inlets, and usually
oriented parallel to the shore [Kjerfve, 1994]. All coastal lagoons are recent and transitional
geological happenings. The fundamental processes that contributed to their formation took
place in the Holocene and were due to changes in (eustatic) sea level about 6000 to 7000
years ago [Emery and Stevenson, 1957; Phleger, 1969] together with the rise and fall of the
coastal area [Zenkovitch, 1969]. In the case of an emergent coastline, the shallowness of the
water and the plain may give rise to a submerged beach that contributes to the formation of a
barrier, which isolates interior water and, thus, forms a lagoon. In the case of sinking
coastline the mechanism that operates is a continual and gradual rise in sea level forming a
barrier [Zenkovitch, 1969] or with regard to a slight sloping coast, the coastal water from the
sea may flood a coastal depression, in a process that under certain circumstances may form a
barrier that encloses the depressions and forms a lagoon [Lankford, 1977].
In geomorphologic terms, coastal lagoons usually occur where valley mouths or lowlands
have been submerged by the sea during the later stages of the Late Quaternary marine
transgression, which on tectonically stable coasts brought the sea up to approximately its
present level about 6000 years ago [Bird, 1994]. Once formed, coastal lagoons are modified
by erosion and deposition. Infilling by accumulation of in-washed sediment, organic deposits
222 Emmanuel Lamptey

such as peat or shells, precipitated material, results in shallowing and shrinkage of lagoons
[Bird, 1994]. Contrasting sea-level histories have exerted a fundamental control on coastal
sedimentation [Dominguez, 1984]. Under conditions of sea-level rise, Barrier Island/lagoonal
systems become important environments of sedimentation. Barrier islands form preferentially
under conditions of sea-level rise. According to Bruun‘s rule [Bruun, 1962], if the coastal
profile is accepted as an equilibrium response of the sea floor to the coastal fluid power
expenditure, then the effects of a sea-level rise could be deduced as a landward and upward
translation of the profile. Thus, as sea level rises along a low-relief coastal plain, the beach
and dune are nourished by the longshore drift and grow upwards at the same rate of sea-level
rise following Bruun‘s rule. The swale behind the dune, however, remains at the same altitude
and, as sea level rises, becomes a lagoon [Martin and Dominguez, 1994]. When sea level
falls, the inverse of Bruun‘s rule applies, resulting in a seaward and downward translation of
the coastal profile, and shallow back-barrier lagoons eventually become emergent [Martin and
Dominguez, 1994]. Because lagoons are generally shallow, they are very sensitive to
fluctuations of sea level, small rises and falls translate respectively into widespread
inundation and emergence of coastal lagoons. Thus, coastal lagoons during their geological
history may be affected by multiple episodes of invasion and emergence.
Ecological conditions, particularly water salinity and temperature, are important in the
geomorphological evolution of coastal lagoons. They control the extent to which vegetation
can colonize lagoon shores, impeding erosion, promoting pattern of sedimentation and
generating organic deposits [Bird, 1994]. Coastal lagoons around the world show great
contrasts, but the same processes have operated in similar situations. In general, coastal
lagoons are formed and maintained through sediment transport processes. Sediments are
carried by rivers, waves, currents, wind, and tides (Nichols and Boons, 1994). Lagoons fed by
rivers receive sediments ranging from coarse sand to silt and clay. The coarser material is
deposited as the river enters the lagoon, and may be added to lagoon beaches and spread
around the shore by wave action; the finer sediment is carried out into the lagoon and
deposited on the floor, progressively reducing the depth. Rates of fluvial sediment yield to
lagoons may be accelerated by the reduction of vegetation cover and the onset of soil erosion
in the river catchments [Bird, 1994]. Studies have also indicated that higher energy conditions
are responsible for the composition and distribution of sediments in a lagoon (Hubbard, 1992;
Kalbfleisch and Jone, 1998; Kench, 1998). The development of these sediments is attributed
to short-lived, storm-induced high energy conditions (Beanish and Jone, 2002).

1.2. Value of Coastal Lagoons

Coastal lagoons present many ecological and socio-economic values, albeit the debate as
to whether natural systems usurp an intrinsic value of their own that lies outside human
determination (Rolston, 1994; Williams, 1994). Coastal lagoons support a wide range of
natural services that are highly valued by society including fisheries, storm protection and
tourism. They are important as nursery grounds for a variety of marine fishes and shrimps
[Day and Yanez-Arancibia, 1985; De Wit, 2003]. Significant fisheries of oyster, shrimp and
bony fish exist within many lagoons. Migrating birds make extensive use of lagoons, where
they feed, roost and may spend most, or all of their lives there (Armah, 1993). Lagoons serve
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 223

as sanctuaries in certain areas for endangered species such as crocodiles and hippopotami
[Day and Yanez-Arancibia, 1985]. Many of the coastal lagoons serve as important harbors,
navigation routes and also for recreation. They therefore, constitute important sites for
industries that are connected with tourism. The shores of certain coastal lagoons are preferred
locations for construction of residences owing to its numerous benefits.
Lagoon reefs made of molluscs are extensively used for concrete aggregate in low coastal
areas, which are far from source hard rock. Some lagoons are dumping areas for disposal of
waste from urban and industrial areas. They constitute areas for the production of significant
amount of salt from local techniques of evaporated pans (e.g., Keta lagoon in Ghana). In
some places, their water is used for the cooling of generators of electric power plants, which
return effluent of warmed water to the lagoon. Coastal lagoons are economically important in
their use for aquaculture facilities [Day and Yanez-Arancibia, 1985; De Wit, 2003]. Coastal
lagoons facilitate processes, particularly those resulting in loss or accretion of natural
wetland. They provide numerous ecosystem goods and services.

1.3. Environemntal Impact Studies

The environment is the sum total of all causal factors that show actual interactions, and
comprises the input and output components, with resources and conditions constituting the
input environment. Environmental conditions are all things outside an organism that affect it
but, in contrast to resources, are not consumed by it [Begon et al., 1990]. Impact is defined as
any effect caused by human activity (activity is basic element of a project that has potential to
affect any aspect of the environment, see EIA for developing countries) on the environment
including flora, fauna, sediment, air, water, climate, landscape or other physical structures or
the interactions among these factors [Convention on Environmental Impact Assessment,
1991].
Environmental Impact Assessments (EIAs) is a requirement for any project that may have
the potential to result in significant impacts to the environment. A principal objective of the
EIA (Ghana perspective) is to provide enough relevant information to the Environmental
Protection Agency (EPA) to enable the Agency to set an appropriate level of assessment for a
proposed project. The information collected through the EIA may be presented in one of
several forms, but for larger projects, the most common is an EIS. Environmental impact
studies are composed of two distinct phases (i) impacts analysis phase, which is meant to
identify, predict, quantify and evaluate the effects of expected impacts before a project occurs
and (ii) a monitoring and assessment phase, which is meant to measure and interpret
environmental effects during the project and after it has been completed. Impact hypothesis
draws on the results of earlier studies of environmental characteristics and their variability
[British Geological Survey, 1999]. Impacts whether they are significant or not, can be direct
or indirect.
Direct impacts to biological resources result when biological resources or critical habitats
are altered, destroyed, or removed during the course of project implementation. Indirect
impacts to biological resources may occur when project activities result in environmental
change that directly influence the survival, distribution, or abundance of native species (or
increase the abundance of undesired nonnative species). It is also possible to have beneficial
224 Emmanuel Lamptey

impacts, directly or indirectly. Impacts may also be short- or long term. Short-term impacts
are generally not considered significant, by definition. Impact thresholds are based on factual
evidence of physical disturbance of habitat, and the loss or disturbance of recorded species.
Impact thresholds could have significant impacts on biological resources (i.e., plankton and
benthos) through (i) loss in substantial number of individual of species or loss that could
affect abundance, (ii) a substantial adverse effect on species, natural community, or habitat
which is recognised as biologically significant, (iii) significant degradation of pelagic or
benthic habitats for rare species and/or native species, and (iv) disruption of the trophic
structure of the biological communities.
In assessing the impacts on biological resources, the temporal and spatial variability of
the benthic assemblages along with predicted area and rate of recolonization constitute a good
consideration. Biological communities exhibit complex interacting behaviours among
themselves and with the non-living abiotic environment [Lamptey and Armah 2008]. These
communities play multiple ecological roles within an ecosystem and therefore, are a critical
part in monitoring and evaluation of project impacts. Changes in soft bottom zoobenthic
communities in response to the environmental impact have been successfully implemented
world-wide in pollution assessment studies and monitoring programs [Pearson and
Rosenberg, 1978].

1.4. Environmental Impacts of Dredging

The principal biological impacts of dredging include disturbance and removal of benthos
and alteration of the substrate upon which colonization depends [British Geological Survey,
1999]. The environmental impacts of dredging have been well documented, with general
reviews of the topic provided by ICES [1992, 2001]; Kenny et al., [1998] and Newell et al.,
[1998]. It was clear from such reviews that most studies have been concerned with impacts of
dredging soft sediments or those associated with beach nourishment projects. A direct impact
of dredging would come from loss of invertebrates via mortality and removal of sediment.
Physical removal of substratum and associated plants and animals from the seabed, and burial
due to subsequent deposition of material are the most likely direct effects of dredging and
reclamation projects [Newell et al., 1998]. New habitats may also be created as a result of the
operation, either directly in the dredged area or by introduction of new habitats on the slopes
of a reclaimed area (e.g. hard substratum in the form of breakwaters and revetments).
Dredged material may come into suspension during dredging itself as a result of
disturbance of the substratum, but also during transport to the surface, overflow from barges
or leakage of pipelines, during transport between dredging and disposal sites, and during
disposal of dredged material [Jensen and Mogensen, 2000]. Dredging may change the
physical environment and could directly impact on macrobenthic organisms through (i)
compaction of sediment, (ii) burial of organisms, or (iii) smothering through increased
turbidity and siltation [Goldberg, 1989]. Dredging has effects at two locations, the site of
removal and the site where the material is dumped [Hall, 1994]. The natural processes of
sedimentation in coastal lagoons are significantly altered by dredging activities. The
consequence changes in sediment composition as a result, affect the associated macrobenthic
fauna. Bonsdorf [1983] examined recolonization after dredging at three shallow brackish sites
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 225

in Finland. The study showed that the pool of available colonists is important in determining
the dynamics of disturbed patches. At one site dredging occurred to below the thermocline
and the benthos at this level were exposed to deoxygenation events every year which
defaunated the sediment. Deoxygenation took approximately two months to kill the fauna and
this was followed by a gradual recovery with the peak in species richness occurring after
about 10 months.
In contrast, just above the thermocline a stable community developed over the six years
of the study and this region provided colonists for deeper parts. With the progressive recovery
of the upper region, a more diverse and abundant pool of colonists was available to recolonise
the deeper parts, which led to successively higher peaks in species richness each year. At a
second site at 8-9m depth in a channel, it took 4-5 years for the community to return to a
background level, despite the area containing only about three species. Interestingly, early in
the colonization sequence, three species established which had not occurred in the area before
dredging. Species richness declined after five years and these three species were not found in
the final community which itself contained only three species.
Maurer et al., [1986] reviewed studies of burial effects and concluded that the pattern of
susceptibilities can be reversed when sediments containing silt/clay are compared with those
comprising sand. This was based on earlier experimental studies, which indicated that
atypical sediments for the area caused the highest mortalities in estuarine bivalve species
following burial in natural and exotic sediments [Maurer et al., 1986]. Maurer et al., [1986]
cited Kranz [1972] who studied the burrowing of 30 species of bivalves showed that the life
habits of the taxa affected the susceptibility of the fauna to mortality. Mucous tube feeders
and labial palp deposit feeders were most susceptible, followed by epifaunal suspension
feeders, boring species and deep burrowing siphonate suspension feeders, none of which
could cope with more than 1 cm of sediment overburden. Infaunal non-siphonate suspension
feeders were able to escape 5 cm of their native sediment, but normally less than 10 cm. One
potentially complicating factor, when considering the effects of dumping dredge spoil, is that
many types of sediment will be contaminated [Hall, 1994]. Indeed, much of the motivation
for studies on dumping dredge spoil effects stems from concern over chemical pollutants
rather than dumping per se.
Flemer et al., [1997] concluded that there was no apparent consistent gross effects of
dredged material disposal on macrobenthic community structure at coastal Louisiana and
suggested that some long-term unidentified factor (e.g. sediment toxicity) maintained
differences in macrobenthic community structure in the three different study areas. A number
of factors influence the effects of dredging on local populations including the types of
organisms which remain in the vicinity [Thrust et al., 1992], the life histories and mechanisms
of dispersal in different fauna [Levin, 1984], the patchiness of the environment [Hall et al.,
1994], the spatial and temporal variability of dredging disturbance, the effects of existing or
new residents on the substratum [Rhoads and Boyer 1982, Davoult and Richard, 1990] and
the potential interactions between dredging disturbance and other perturbations [Jewett et al.,
1999].
Dredging activities is also usually associated with profound changes in water quality as a
result of alterations to natural suspended sediment loads and localized sedimentation resulting
in clouding and colouring of the surface water. Impacts associated with increased suspended
particles in the water column include high turbidity levels, reduced light transmittance and
reduction or loss of benthic habitats. The intensity and duration of sediment re-suspension
226 Emmanuel Lamptey

from dredging and disposal operations highly dependent on the type of equipment, operator,
characteristics of sediment, and the hydrodynamic conditions [Collins 1995; Clark and
Wilber, 2000]. Elevated suspended sediments have also been shown to adversely affect the
respiration of fishes, reduce egg buoyancy, disrupt icthyoplankton development and reduce
filtering activities of benthic organisms [Messieh et. al., 1991; Barr, 1993].
Other forms of dredging like aggregate mining can reduce localized current strength,
resulting in lowered dissolved oxygen concentrations. Reduced oxygen levels adversely affect
the ability of fish and invertebrates to utilize specific areas for spawning, feeding and
development [Pacheco, 1984]. The release of material into the water column during dredging
can alter water quality, especially if excavated material is high in organic matter. The effects
of mixing in the water column are likely to increase the demand of oxygen by decomposing
organic matter and the release of nutrients [ICES, 1992]. Furthermore, dredging could
increase or decrease the exchange rate of nutrients between the sediments and water column
and introduce pulses of productivity during nutrient recycling. Dredging activities therefore
affect certain physical and chemical conditions of the water such as degree of oxygenation
and mineralization, temperature, salinity, water flow, depth and water level fluctuations.
The actual impact of dredging operation will be a function of the spatial extent and
degree to which the post-construction environment differs from pre-construction conditions.

1.5. Overview of the Keta Restoration Project

The Keta Lagoon area is an ecologically important wetland in West Africa and has been
recognized as a designated Ramsar site (a wetland of international importance especially as a
habitat for waterbirds). Ghana has ratified both the Ramsar and Bonn (which addresses the
conservation of migratory species of wild animals) Conventions in 1988. Due to the high
population density of people in the Keta Lagoon area, the Ramsar Convention is particularly
applicable because it promotes the conservation and preservation of wetlands through
sustainable and ―wise-use‖, as opposed to outright protection through ―non-use‖.
The Keta lagoon covers an estimated area of 340 km2 with water depths ranging from
0.47 to 0.94 m in the wet season and 0.14 to 0.56 m in the dry season [Lamptey and Armah,
2008]. The lagoon has a maximum coastal length (east–west) and width (north–south) of 25
and 13.5 km, respectively [Lamptey and Armah, 2008]. It is separated from the sea by a
narrow sand bar (Figure 1) and, therefore, receives sea water only through spillover during
periods of high tide. The Keta basin was formed by coastal subsidence during the
Precambrian [Akpati, 1975]. The upper geologic strata (about 24 m) are composed of coarse,
unconsolidated beach sand and gravels both of fluviatile and shallow marine to estuarine
origin [Akpati, 1975]. Most areas in the lagoon are typically muddy in the upper 10 cm. The
sea grass Ruppia maritima used to occur in the northeastern part of the lagoon and portions of
the southern part until disappeared in 2004. The macrophytic flora in the lagoon is dominated
by Typha domingensis and Paspalum vaginatum in the northwestern and southwestern
portions in the freshwater tributaries of the lagoon. The southwestern part is dominated by
Paspalum vaginatum.
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 227

Figure 1. Aerial view of the created habitat island using dredged material (Source: GLDD/ESL/EPA

The lagoon receives fresh water from a large catchment area including (1) runoff from
the Tordzie river, which originates from the Akwapim–Togo ranges; (2) runoff from the Aka
and Belikpa catchments, which enters the lagoon from the north; and (3) inflows from the
Volta estuary through Anyanui creek [Entsua-Mensah and Dankwa, 1997]. The Tordzie river
has a catchment area of 2,200 km2 and a mean annual flow of 11 m3 s−1; Aka and Belikpa
have catchment areas of 280 and 420 km2, respectively; the total drainage area of the Volta
estuary is 37,900 km2 [Finlayson et al., 2000]. Nevertheless, the volume of water (84,446 m3)
transferred to the lagoon during one flood period in January 2001 from the Volta estuary via
Anyanui creek resulted in a tidal excursion of 5.4 km [Sørensen et al., 2003], indicating that
the fresh water that flows from the Volta estuary into the lagoon is not substantial. The
estimated static capacity of Keta lagoon is 360×106 m3 when there is no flow of water into it
[Finlayson et al., 2000]. The area lies within the dry equatorial region of Ghana, which has
two wet seasons, one from May to July (major rainy season) and from September to
November (minor rainy season). The mean annual rainfall is 750 mm [Dickson and Benneh,
1988]. The dry season begins in January and ends in March. Annual mean air temperatures
range between 24°C and 32°C. Evaporation in the area far exceeds annual rainfall. It is only
during the major wet season that monthly rainfall may exceed evapotranspiration and
temporary streams flow [Biney, 1986]. The prevailing wind direction is from the southwest
(the southwest monsoon), which is a feature of the entire coastal belt of the country
[Finlayson et al., 2000]. The mean monthly averages of daily wind speeds range from 5.86 to
8.06 m s−1 [Finlayson et al., 2000].
Restoration project of the Keta beach was driven by episodes of erosion threats dated
back 1920s. The project tarried until in 2000 after a definitive study in 1996 and engineering
solution recommended [ESL/RPI/GLDD, 2004]. Prior to the restoration project, flooding
from the Keta lagoon following torrential rains displacing immediate inhabitants was a
perennial characteristics feature. The restoration project was initiated in 2000 by Great Lakes
Dredge & Dock (GLDD). The project had four principal components: i) sea defense, ii) land
reclamation via beach nourishment; iii) construction of a road along the lagoon; and iv)
construction of a flood relief structure. As a complement to the specific objectives of each
component, an overall objective of the project was to minimize impact to, or even improve
the general environmental conditions and enhance the ecological setting against the
background a designated Ramsar site. Restoration science, and its recent manifestation,
228 Emmanuel Lamptey

sustainability science (Kates et al., 2001], are partly rooted in ecological fidelity; i.e., those
restoration goals characterized by structural replication, functional success, and durability
(self-sustainability) [Higgs, 1997].
To give impetus for the project, dredging of the Keta lagoon to obtain appropriate
sediment materials for road construction, beach nourishment, and infilling the reclaimable
land became a viable option. However, aware of the adverse impacts associated with
dredging, innovative dredging was designed to ensure beneficial uses of the dredged material.

1.6. Objectives

The main aim of the study was assess the dredging impacts on the receiving environment
on spatial and temporal scales. The potential environmental impacts can be positive
(beneficial) or negative, direct or indirect and short-term or long-term. This assessment is
focused primarily on the biological habitats, species and water quality conditions.
The goal was to assess the effect on a soft bottom community resulting from the removal
of approximately 9,091,000 m3 of sediment during the dredging of the channel.

MATERIALS AND METHODS

2.0. Field Sampling

The sampling was designed to provide a sound monitoring plan that assessed the
potential impacts of the dredging on the lagoon ecology especially biological resources and
water quality. The sampling strategy/design followed Underwood‘s (1994) BACI; (before-
after control-impact) approach but included in it aspect during the dredging phase. Following
the design seven impacted sites were located in the dredged channel (1-km interval) labelled
alpha-numerically (A-0 to G-0), and also a control non-impacted site.
Quantitative sampling of macrobenthic fauna was carried out using Orange-peel grab at
each location September 2000 (Before Dredging), September 2001 (During Dredging) and
September, 2002 (After Dredging) of dredging operations. Four replicate samples were taken
at each site. A grab sample constituted a sediment volume of 2.036 x 10-3 m3. The samples
were processed by passing through a 0.5mm sieve, processed and fixed with 10% borax pre-
buffered formaldehyde solution.
Water quality parameters were collected quarterly at the surface and bottom (during and
after dredging period) using a Van Dorn water sampler. In-situ measurements of dissolved
oxygen, temperature, pH, water depth, salinity, transparency were carried out. Additional
water samples were collected for laboratory analyses of nutrients (nitrate, phosphate, silicate,
sulfate), turbidity, suspended solids, and dissolved solids.
Avifauna observations were made using a 60 mm, 15-60x zoom spotting scope mounted
on a tripod (Figure 1) and 7 x 50 binoculars. Observations of the shorebirds were made in the
morning (6:00 AM) and early evening (6:00 PM). Five monitoring stations within the sphere
of the project site were visited in each survey session to quantify shorebirds abundance.
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 229

2.1. Laboratory Sample Processing

Macrobenthic faunal samples were washed thoroughly with fresh water in 450-µm
stainless sieves to get rid of the formaldehyde solution and excess mud. The washed sediment
samples were separately placed in 50 x 40m sorting tray with a white background thinly
spread and the organisms picked into storage vials with the aid of hand lens and preserved in
70% ethanol mixed with glycerol. During sorting the organisms were grouped into broad
taxonomic units such as polychaetes, mollusks, crustaceans etc. These broad taxa were
identified to genus or species levels as possible and counted. Identifications were based on
taxonomic guides and manuals [e.g., Day, 1967a, b; Edmund, 1978] as well as voucher
specimens in the Zoological Museum of the University of Ghana. Voucher specimens are
available for examination.
Sediment samples collected for physical and chemical analyses were taken at each
sample location at 20-cm deep core. The samples were homogenized, air-dried, and used for
granulometric analysis (i.e., sand, silt, and clay fractions) following Bouyoucos‘ [1934]
method and also percent organic carbon and percent sulfur contents using the ELTRA 500 C-
S determinator after pretreatment of the sediment with hydrochloric acid to remove inorganic
carbon.
Water samples collected at the subsurface and bottom were analyzed in the laboratory for
nitrate, phosphate, silicate, sulfate, conductivity, turbidity, suspended solids, and dissolved
solids using the HACH DR/2010 spectrophotometer following the methods in A.P.H.A. et al.
[1998].

2.2. Data Analyses

The data set was analysed using both univariate and multivariate statistics. Spatial and
temporal distributional trends were plotted to indicate the impacts of the project on the
macrobethic fauna, shorebirds and water quality.
To test for differences in community structure between the study shores; one-way
Analysis of Similarity (ANOSIM) was utilized [Clark and Warwick, 1994]. This program
computes r-statistics as a measure of discrimination. First, a global R-value was computed to
indicate the overall effect of similarity between the study shores. Values of R=1 are obtained
when all replicates (sites) within the groups (zones) are more similar. The p-value for the
statistics was obtained by simulating all possible permutations of assigning replicates (sites)
to study zones. In this study, a random sample of 999 permutations was used in each
calculation.
The species that contributed the most and discriminated one study zone from another
were investigated using non-metric similarity percentage procedure (SIMPER) [Clark and
Warwick, 1994]. These results assisted in interpretation of the community changes
responsible for the observed pattern in the ordination [Clarke, 1993]. The group of species
with cumulative contribution above the 50% (dis)similarity threshold were considered
important in controlling the taxa assemblages in the studied area.
230 Emmanuel Lamptey

3.0. RESULTS

3.1. Distribution of Dredged Materials on Restoration Sites

Two hydraulic cutter dredges were used to remove varied quantities of sediments in two
burrow pits and access channel (Figure 2). The average depths of the burrow pits were
approximately 9.6 m and 11.1 m for pits 1 and 2 respectively (Figure 2). The depths for the
access channels ranged from 2-4 m. The burrow pits were approximately 300 m wide while
the access channels were 40 m wide. Table 1 presents the quantity of sedimentary materials
deposited at each construction site. The total sedimentary material deposited on each
constructional site was 2,861 million cubic meter for beach restoration with a daily average
production of approximately 11,800 cubic meters. The total dredged material production to
the avifauna habitat islands was 2,010 million cubic metres with average daily production of
approximately 9,050 cubic meters of sedimentary material. At the site for reclamation, a total
of 4,220 million cubic metres and a daily production of approximately 10,300 m3 were
deposited. The water to solids ratios were 10–16% in medium sand and 12–20% in cohesive
soils [ESL/RPI/GLDD, 2001-2004]. The dredging activities in the lagoon varied throughout
the period according to actual sand requirements, but it was estimated that on average
300,000-350,000 m3 of sediment were dredged monthly.

Figure 2. Schematic diagram of relative locations of burrow pits and access channels and their
approximate lengths and sampling stations of the dredged channel

Table 1. Average and total dredged sediment deposited at the project specific area

Project Average daily Total material No. of days

Component Production (m3) deposited (m3) for deposition
Beach restoration 11,800 2,861,000 242
Land reclamation 10,300 4,220,000 410
Habitat island 9,050 2,010,000 222
Total 31,150 9,091,000 874
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 231

3.2. Impacts of Dredging Operations on Shorebirds‟ Abundance

The total shorebirds abundance increase considerably from 12346 (2000), 13643 (2001)
to 114, 398 (2002). Averagely shorebirds‘ abundance indicated significant (p<0.05) increase
after dredging (Figure 3) suggesting a positive impact of the project. Nonetheless, the
numerical abundance of wader bird group decreased after the dredging operations in 2002
(Figure 4). Conversely, terns showed increased trends from 2000 to 2002, whereas ‗other‘
category fluctuated between the periods (Figure 4).

Figure 3. Mean total abundance of shorebirds before, during and after the dredging periodicity
(composite abundance was from August to December of each year)

Figure 4. Percent abundance of shorebirds groups before, during and after the dredging periodicity
(composite abundance was from August to December of each year)
232 Emmanuel Lamptey

3.3. Dredging Impacts on Macrobenthic Fuanal Community Structure

The macrobenthic community of the dredged channel showed significant reduction in

abundance (using one-way ANOSIM) between 2000 (Before) and during (2001) (r=0.205,
p<0.05), as well as 2000 (Before) and 2000 (After) the dredging (r=0.166, p<0.05)
periodicity. The species that contributed to significant difference in the periods were
Ischyroceros sp., Nereis operta, Notomastus cf. latericeus, Nephtys lyrochaeta, Tellina
nymphalis, Capitella capitata (Table 2). The first four species contributed greater than 50%
for the average dissimilarities of 85.29% and 83.57% realized respectively between 2000 and
2001, also between 2000 and 2002. However, three species namely Nepthys lyrocheata,
Tellina nymphalis and Notomastus cf. latericeus contributed greater than 50% to the average
dissimilarity of 87.71% between 2001 (During) and 2002 (After). The differing abundances
of these species largely influenced the macrobenthic assemblage structure of the dredged
channel.

Table 2. SIMPER analysis results: species contributing to the average Bray–Curtis

dissimilarity between the 2000 (Before), 2001 (During) and 2002 (After) dredging based
on simultaneous analysis of taxa abundance data. δi: contribution of the i-th faunistic
group to the average Bray-Curtis dissimilarity (δ) between the project periods , also
expressed as a cumulative percentage (∑δi%). Diss/SD is the ratio of dissimilarity to
standard deviation and F is the frequency of occurrence of the 7 sites. For brevity, only
species that contributed to ≥ 5.0% and cumulative percentage of ≥70% are listed. The
codes in the parenthesis after the species name indicate: „C‟ crustacean, „P‟ Polychate,
„B‟ Bivalve

Species Ave. Diss Diss./SD (δi) ∑δi%) (F%)

Average dissimilarity between year 2000 and 2001 =85.29
Ischyroceros sp. (C) 14.84 1.36 17.40 17.40 38
Nereis operta (P) 13.96 0.97 16.37 33.77 29
Notomastus cf. latericeus (P) 10.20 1.14 11.96 45.72 43
Nepthys lyrochaeta (P) 10.17 1.12 11.93 57.65 52
Tellina nymphalis (B) 8.15 0.75 9.55 67.20 33
Capitella spp. (P) 6.22 0.59 7.41 74.62 24
Average dissimilarity between year 2000 and 2002 =83.57
Ischyroceros sp. (C) 15.84 1.29 18.95 18.95 38
Nereis operta (P) 14.55 0.94 17.41 36.36 29
Notomastus cf. latericeus(P) 11.16 1.10 13.36 49.72 43
Nepthys lyrochaeta (P) 9.68 1.00 11.58 61.30 52
Capitella spp. (P) 7.21 0.64 8.62 69.93 24
Tellina nymphalis (B) 5.37 0.76 6.42 76.35 33
Average dissimilarity between year 2001 and 2002 =87.71
Nepthys lyrochaeta (P) 23.16 0.73 26.40 26.40 52
Tellina nymphalis (B) 20.51 0.70 23.38 49.79 33
Notomastus cf. latericeus (P) 15.96 0.69 18.20 67.98 43
Capitella spp. (P) 7.33 0.78 8.35 76.34 24
Ischyroceros sp. (C) 6.48 0.46 7.38 83.72 38
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 233

Figure 5. Temporal distribution of macrobenthic faunal abundance before, during and after dreding

Individual macrobenthic faunal species showed spatio-temporal differences (Figures 6

&7) in numerical abundance such that higher numbers occurred at Stations C-0 (Tellina
nymphalis) and G-0 (Nephtys lyrochaeta, Notomastus cf. latericeus and Capitella spp.)
during September 2001. Stations F-0 and G-0 were freshly dredged during this period. A
notable feature was the absence of mactra nitida at any of the stations before dredging but
occurred in appreciable numbers in 2001 (During dredging) (Figure 7). Capitella capitata
was also abundant at station D-0 in 2002 (After).

Figure 6. Spatial abundance of macrobenthic fauna before, during and after dredging. Error bars
indicate 95% confidence interval
234 Emmanuel Lamptey

Figure 7. Temporal distribution of macrobenthic taxa before, during and after dredging periods

The effect of spatial declension in species abundance after dredging was significantly
pronounced at Stations A-0, B-0, E-0, F-0 and G-0 (Figure 6). Conversely, Stations C-0
showed significant increased in taxa abundance after dredging. Station D-0 depicted evidence
of community recovery. Certain stations notably Stations A-0, B-0, E-0 and F-0 recorded no
species after dredging. Probably, the dredged material mainly smothered the species.

3.4. Dredging Impacts on Water Quality

3.4.1. Spatial Pattern Of Water Quality

The water quality parameters showed both temporal and spatial variation during the
periods of the study (Figure 8). Spatio-temporally, parameters such as total dissolved solids,
sulfate and salinity showed a trend. Higher values of these parameters were observed at
Stations E-0 and F-0 during May 2002. The lowest values occurred at stations A-0 and D-0.
Turbidity did not show any trend, however higher turbidity was recorded at Stations D-0
(Sept. 2001), which could possibly be due to the movement of dredged plume from stations
F-0 and G-0 eastward. Levels of turbidity and suspended solids were extremely low at Station
G-0 throughout the study period due possibly to the direction of the fetch carrying the
dredged plume eastward.
The distribution of variables such as dissolved solids, sulphate and salinity seemed to
mimic each other spatially. Stations E-0 and F-0 recorded the highest values for these
parameters. The other stations recorded values within very narrow range to each other.
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 235

Figure 8a. Spatial distribution of water quality variables at the surface of sampling stations
236 Emmanuel Lamptey

Figure 8b. Spatial distribution of water quality variables at the bottom of sampling stations
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 237

3.4.2. Temporal Patterns Of Water Quality Regimes

Temporal distribution of water quality variables in the dredged channel are presented in
figure 9. The surface waters always stayed well oxygenated and generally saturated. The
oxygen concentrations between the surface and bottom waters were significantly different
throughout the period except in September 2001. There was no existence of channel prior to
this period and hence reference could not be made to pre-dredging periods of differences in
surface and bottom oxygen content
The pH measurements showed that the dredged channel water was moderately basic with
slight increases in June. The surface waters were moderately basic than bottom.
Water temperatures during the period ranged from 27 to 31ºC. Temperatures fluctuated
between the periods possibly reflecting the prevailing seasonal climatic conditions.
Understandably, surface temperatures were moderately higher than the bottom except in Jun-
02 where the contrast occurred. Nonetheless, the no significant differences existed between
the surface and bottom waters. Temperature changes due to dredging are not much of
importance. No abnormal thermal regimes were noticed in the dredged channel. Generally,
temperature influences molecular diffusion and metabolic rates.
The salinity generally mimicked the pattern of water temperature, but showed direct
positive relationship with nitrate. The salinity influences many important processes and
functions in aquatic systems. For example, the aggregation and flocculation of suspended
particles increase with increasing salinity, meaning that water clarity increases [Håkanson,
2006] leading to increasing primary production of benthic algae and phytoplankton
[Preisendorfer, 1986]. It is likely salinity spews from the sediment occurred as a result of
dredging operations.
Turbidity is an important parameter which influenced water quality during dredging.
Turbidity was generally low except September 2001 during the peak of the dredging when it
increased sharply in the bottom waters. Ostensibly, the bottom waters experienced higher
turbidity than the surface throughout the period. The prevalence of moderately higher
turbidity at the bottom waters indicates impacts of dredging operations.
Water depth showed increased moderately after January 2002 after the dredging.
However, the temporal pattern did not any significant difference.
Nutrient incursions into the coastal lagoons are routed through land drainages and often
in sinks/sources. All the nutrients (nitrate, phosphate, silicate and sulfate) measured were
generally higher at bottom waters. This indicates the likelihood of bottom sediments releasing
quantitative amounts of nutrients into the water column as sequel of the dredging operations.
The highest concentrations of phosphate and silicate were recorded in September during
dredging operations (Figure 9). Frequent resusupension episodes decreases phosphorus
content in the sediment [Sørensen et al., 2003] resulting in increased concentration in the
water column [Watts 2000]. The importance of sediments as a potential source of phosphorus
has also been reported in shallow coastal areas [Fisher et al., 1982].
Further, the strong positive correlations of salinity and nutrients lend credence to the
efflux of saline nutrient-rich water from the sediment due to the dredging. Sediments
constitute an essential environmental reservoir in coastal systems due to their capacity to
retain and release different compounds from or to the water column.
238 Emmanuel Lamptey

Figure 9. Temporal variations of water quality variables at the surface and bottom of the dredged
channel of Keta lagoon
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 239

0.5 Surface Bottom

0.4
Phosphate (mg/L)
0.3

0.2

0.1

0.0

Figure 9. Temporal variations of water quality variables at the surface and bottom of the dredged
channel of Keta lagoon

4.0. CONCLUSION

4.1. Distribution Pattern of Avifauna Community

The coastal water bodies of Ghana constitute important habitats for both resident and
migratory shorebirds from the East Atlantic and the Mediterranean flyways [Ntiamoa-Baidu
& Hepburn, 1988; van de Kam et al., 2004]. The shorebirds use these coastal areas for food,
resting and breeding. The Keta lagoon complex is one of the five Ramsar sites being managed
[Willoughby et al., 2001; Ryan, 2005], with Songor, Sakumo, Densu and Muni-Pomadze are
the other four.
Management of these Ramsar sites mainly includes implementation of civil works to
minimize the impact of identified problems amongst others. This management objective was
considered in the implementation of the KSDPW. As such, the dredged materials were used
for birds‘ habitats creation. The positive impact of the habitats creations for shorebirds was
evident in the abundance of reported after the project (Figure 3). Notably, the impact was
positive for the terns (Figure 4). Possibly, the dredging materials used to create the birds
islands not only provide habitat refuge for the shorebirds but also exposed benthic
invertebrates serving as reliable source of food.
240 Emmanuel Lamptey

Rapid exposure of wetland substrate [e.g. Velasquez, 1992] could lead to rapid exposure
of fresh patches of unexploited feeding areas which would consequently attract foraging
birds. According to Jan et al. [2003], foraging waterbirds are uncertain about their chances of
success on arrival at a patch and therefore sample their environment to get information on the
presence of food so as to ‗make decisions‘. Since the decision on whether to keep on feeding
or leave a patch depends largely on prey encounter rates. The increased abundance of the
shorebirds after the project suggests that they had found reliable patch with increased
encounter rate as a result of the project.
The waders and ‗others‘ shorebirds categories were negatively impacted by the project as
were substantial reduction in their abundance after the dredging operation in 2002 (Figure 4).
These shorebirds probably moved away from the noise generated as a result of the project
activities and human presence in the vicinity.

4.2. Impact of Dredging on Macrobenthic Fauna

The dredged material (approx. 9091,000 m3), mainly peat smothered the macrobenthic
fauna in area where the sediment were deposited (habitat islands). It however, exposed new
area (burrow pit) for colonization. The rate and period of recovery for the macrofauna would
be indicators for assessing the enormity of the impacts. Disturbance likely leads to a non-
equilibrium state in community structure where communities are continually recovering the
last disturbance [Reice, 1994] as occurred during the dredging phase of the KSDWP.
Disturbance of coastal macrobenthic communities induced through experimental
manipulation suggest that colonization may be relatively rapid, but time to recovery is
variable and depends on the timing of disturbance, nature of the habitat, reproductive
periodicity of macrobenthos, and abiotic and biotic factors [e.g. Probert, 1984; Zajac and
Whitlatch, 1982].
In this study, macrobenthic faunal community showed a good deal of dominance and
diversity 2001 (During Dredging) and 2002 (After Dredging) dredging. In fact, during the
periods of dredging the dominant species encountered in the channel was Tellina nymphalis,
which possibly survived the low oxygen at the bottom of 9m water depth. This is possibly due
to their long siphons, which enable them to filter the water column for food. Gradually,
however this species disappear and could not be recorded in the subsequent samples. Exactly
a year later colonization by similar species, which were recorded during the dredging and few
months after dredging, showed signs of recovery with appreciable numbers recorded. This
probably was due to the more favorable conditions that existed in the channel at the time. It
must be noted that the species recorded during dredging and a year after were very similar in
terms of composition during the wet periods where environmental condition were in the
tolerable ranges of the organisms. The abundance of the species showed both spatial and
temporal variation. In the 2001 (During Dredging) samples, the abundance of Tellina
nymphalis was high at station C-0 and Capitella capitata and other Capitellids were high in
Station G-0 (where highest species richness and diversity was recorded). This was due to the
fact that sampling was done few days after dredging where most of the recorded species were
still surviving. However, in 2002 (After Dredging), the abundant of species occurred in
Stations C-0 (though numbers and diversity varied with the previous year‘s results) and D-0.
 Environmental Consequences of Innovative Dredging in Coastal Lagoon… 241

In this case, dominant species were Notomastus sp. Capitella capitata and Tellina nymphalis
but Station G-0 did not record many species. It could also be realized that the dominant
species in each instance were opportunistic species, able to tolerate stressful environments.
This corroborates findings by Hall, et al., [1994] that a common consequence of high physical
disturbance is a numerical reduction in non-opportunistic taxa.
The only exception being the dredge spoils which created a very high turbid environment.
Nevertheless, the impact of the dredging on the macrobenthic fauna was measurably felt
within the few months as the substrates that served as habitats and on which colonization
depends were continuously removed and palpably the first 8 months saw no colonization
process in place. However, with the emergence of those species that were decimated, a year
after, the channel is expected to fully recover to climax in a year or two. The re-colonization
of the macrobenthic fauna was dependent on local hydrodynamic regimes and sediment
characteristic, which showed spatial and temporal variations.

4.3. Impacts of Dredging on Water Quality

Temporal and spatial variability were observed in the physico-chemical parameters

measured (e.g. salinity, total dissolved solids, total suspended solids and sulfate) in the
channel (Figures. 8 & 9). Turbidity and salinity were the most commonly observed changes in
the water during the dredging operations.
Higher turbidity may have ecological consequences not only adversely affect the
production of phytoplankton as it interferes with primary production by limiting light
penetration [Jonhston Jn. 1981], but affect fish gills its clogging action and can also clog the
membranes of filter feeding organisms [Bray 1979].
Many of the water quality variables fluctuated between the periods possibly reflecting
natural conditions. Ostensibly, estuaries and coastal lagoons are characterized by variability
and low predictability of their environmental conditions. Consequently, their physico-
chemical parameters exhibit large variation (e.g. seasonal), with the highest concentration
generally found following a rainy period. It is therefore sometimes maze decoupling natural
phenomenon from human-induced activities such as dredging.

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Chapter 8

STATE OF KNOWLEDGE OF THE TROPHIC STATE OF

WORLDWIDE LAGOON ECOSYSTEMS:
LEADING FIELDS AND PERSPECTIVES

Monia Renzi*1, Antonietta Specchiulli2, Raffaele D’Adamo2 and

Silvano E. Focardi3
1
Research Centre in Ecology, aquaculture and fishery (Ecolab), Polo Universitario
Grossetano, University of Siena, Orbetello (GR), Italy
2
National Research Council - Institute of Marine Science,
Department of Lesina (FG), Lesina (FG), Italy
3
Department of Environmental Science, University of Siena, Siena, Italy

ABSTRACT
In the latest years, the environmental research has focused on studying the water
quality of marine-coastal ecosystems and on the main consequences of human activities
within these environments, their surroundings and catchments. Among aquatic water
systems, coastal lagoons are particularly vulnerable to water-quality deterioration, due to
their restricted water exchange. In addition, they are used as nursery areas for aquaculture
and fisheries exploitations, which represent the main economic relevance for local
inhabitants. Protection of the ecological status of worldwide lagoons has to be the key
purpose of the International directives, as coastal lagoons are naturally stressed
ecosystems which suffer from frequent environmental disturbances and fluctuations
related to their geomorphologic characteristics, general hydrodynamics, abiotic and
biological parameters. The main keys of ecological research studies in coastal lagoons are
represented by the need to improve the general knowledge on system dynamics focusing
on the leading aspects useful to develop eco-compatible management plans which allow
us to preserve their productivity avoiding losses of biodiversity related to the increase of
bioavailabile nutrients. The increasing number of ecosystems exhibiting frequently a
progressive decline of water quality has led environmental researchers and managers to

* Corresponding author: renzi2@unisi.it, Research Centre in Ecology, aquaculture and fishery (Ecolab) Polo
Universitario Grossetano, University of Siena, via Lungolago dei pescatori s.n.; 58015, Orbetello (GR), Italy.
250 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

identify eutrophication as a major worldwide problem. The development of simple and

not expensive well calibrated indices of eutrophication represents one of the most actual
ecological fields in which researchers are involved. Many European countries have
developed within the Water Framework Directive (CE 2000/60), an environmental
quality classification scheme in order to assess the trophic state and water quality through
the use of specific indices based on environmental factors. Our aim is to evaluate
nowadays the state of knowledge related to eutrophication of worldwide lagoon
ecosystems, highlighting the main fields of interest and major problems. Leading
problems are related to the choise of useful indices, their calibration, their efficiency in
describing dynamics of lagoons characterized by different trophic levels and the selection
of the opportune pristine ecosystem as reference for lagoon classifications related to
water quality.

8.1. INTRODUCTION
Coastal lagoons represent ecosystems of particular ecological, social and economic
interest. Compared to the sea, they are able to sustain higher fish production rates,
representing an important economic relevance for local inhabitants and helping aquaculture
and fisheries exploitation. This efficiency is directly related to the fact that coastal lagoons are
a natural sink for nutrients, supporting primary producers and, subsequently, other species of
the lagoon trophic web. Nevertheless, nutrient enrichments represent the major problem for
these systems. Ecological dynamics of coastal lagoons are regulated on the basis of prey-
predator complex relationships. If the growth of primary producers is excessive and not
balanced by herbivores, nutrient increases determine changes in community structure that
could, also, evolve towards a dramatic reduction of the ecosystem biodiversity and fish
productivity. Lower nutrient levels (low trophism) are associated with lower primary
production rates; on the contrary, higher levels of available nutrients (high trophism) could
determine hyper-proliferations of macro and microphyto communities (Perez-Ruzafa et al.,
2005). Following an increasing concentration of available nutrients in water, aquatic
ecosystems could be classified within four trophic classes: oligotrophic, mesotrophic,
eutrophic and hypertrophic (Nixon, 1995). A trophic level is not a fixed characteristic but
represents the equilibrium reached by a specific aquatic ecosystem as sum of multiple
different factors just at the moment when the observations are occurring. This means that it
could rapidly and reversibly evolve as a response to specific natural or human-mediated
stressors. For the exposed reasons, it is evident that the regulation of lagoon dynamics,
directly or indirectly related to nutrient loads, represents the most important target to develop
sustainable management plans in coastal lagoons. Unfortunately, ecosystem processes are
controlled by complex interactions among natural and human-mediated stressors and fluxes
of materials between land, ocean and atmosphere, making coastal lagoons the most
changeable and vulnerable environments worldwide (Viaroli et al., 2007). Due to their
morphologic, geomorphologic and hydrologic characteristics, which favour nutrient
accumulation and reduce contextually their potential dilution potential and carrying capacity,
lagoons are naturally stressed ecosystems characterized by frequent environmental
disturbances and fluctuations. Furthermore, additive interferences due to human activities
increase complexity of system dynamics, modify ecological equilibrium and reduce, as final
effect, system resistance and resilience. If ecological relationships are not balanced, systems
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 251

could highlight successive cycles characterized by alternative crises and partial community
recoveries with a progressive deterioration of the ecosystem quality. The increasing number
of ecosystems which exhibit a progressive decline of water quality has led environmental
researchers and managers to identify the eutrophication as the major problem for coastal
lagoons worldwide. Briefly, eutrophication could be described as a well-known ecological
phenomenon supported by nutrient enrichments causing a significant increase of primary
productivity, which could determine a notable reduction of the secondary ones (Kjerfve,
1994). In order to allow the conservation and natural productivity of these ecosystems, the
protection of the ecological status of lagoons has to be the key purpose of the International
directives. From 1980 to date, significant progress has been made in the development of
regulations designed for the coastal lagoon protection and management. The interest from the
governments for these systems has led to an exponential enhancement of specific scientific
research studies (Basset, 2010). In the latest years, the main target of ecological studies is
represented by the need to improve the general knowledge on system complex dynamics
focusing on the leading aspects useful to develop eco-compatible management plans which
allow us to preserve their productivity avoiding losses of biodiversity related to the increase
of bioavailable nutrients. Research worldwide has focused on the complex relationships
between human pressure and ecosystem response (eutrophication). The development of
simple, not expensive, and well calibrated indices of eutrophication represents one of the
most actual ecological fields in which research studies are involved. Many European
countries have developed within the Water Framework Directive CE 2000/60 (European
Commission, 2000) an environmental quality classification scheme for the water quality
assessment, through the use of specific indices based on environmental factors. In this chapter
an evaluation of the eutrophication state of lagoon ecosystems worldwide is reported,
highlighting the main fields of interest, major problems, international regulations that aim to
contrast this phenomenon and major scientific research perspectives. Leading problems are
related to the choice of useful indices, their calibration, their efficiency in describing lagoons
dynamics characterized by different trophic levels and the selection of the opportune pristine
ecosystem as reference for water quality classifications of the lagoons.

8.2. COASTAL LAGOON PRODUCTIVITY: AN ECONOMIC VALUE

LINKED TO THE TROPHIC LEVEL
It is well known by the literature that coastal lagoons represent peculiar ecosystems for
primary and secondary productivity (Nixon, 1995). The net primary production estimated for
these ecosystems and calculated over 70 lagoons ranges from 10 to 7000 g of C m-2y-1
(Troussellier and Gattuso, 2007). Relationships between available nutrients and ecosystem
metabolism have been highlighted (Viaroli et al., 2008). In particular, oligo and mesotrophic
systems show values <300 g C m-2y-1, while 300–500 g C m-2y-1 are associated with eutrophic
lagoons. Hypertrophism (>500 g C m-2y-1) could determine a rapid evolution towards the
ecological status of dystrophy. Primary productivity could be characterized by a dominance
of phytoplankton, macroalgae or phanerogams. For macroalgae productivity, data acquired in
1996 by Morand and Briand highlighted that the seaweed annual productivity was notably
high in Italian lagoons (1,000,000 t wet weight, w.w.), while lower values were reported for
252 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

French (100,000–200,000 t w.w.) and Australian areas (100,000–600,000 t w.w.) with

densities ranging from 0.2–400 kgm-2 and mat thicknesses included within 2–100 cm. Species
dominances are linked to the ecological values of the system and population shifts are reliable
to changes of trophism (Knoppers, 1994; Zaldivar et al., 2008a). Unfortunately, prediction
models based on simple relationships among nutrient levels and abundance or distributions of
different primary producers are not applicable to shallow coastal lagoons because of the wide
variability and the overlapping of the boundaries (Nixon et al., 2001). Nevertheless, additions
of nutrients could produce cascade effects on trophic webs with significant variation of
abundances and biomasses also in upper predators (Zaldivar et al., 2008a). Relationships
linking water physico-chemical properties, primary productivity levels, and trophic status of
coastal lagoons are summarized in figure 8.2.1.

Figure 8.2.1 Relationships linking water physico-chemical properties, primary productivity levels, and
trophic status of coastal lagoons.

Numerous factors could affect water trophism in coastal lagoons, but human activities
represent important direct or indirect stressors. For this reason, the evaluation of sustainability
of human activities in these ecosystems becomes a main and not a secondary aspect. The
sustainability of human activities in the biosphere is a widely discussed problem (UNWCED,
1987). Early discussions between ecologists and economists have stressed limits imposed by
the physical environment to the economic development, concluding that humans should
utilize species and ecosystems in such a way to allow them to go on renewing indefinitely
(Anand and Sen, 2000). As result of the anxieties expressed by environmental scientists and
ecologists, policymakers and economists have attempted to formulate the concept of
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 253

sustainable development. The main problem derived from the need to translate ecosystem
properties and their value for the human development into an economic and political
language. For this reason, ecosystem services are considered in terms of benefits for human
populations directly or indirectly derivable from different ecosystem functions (Costanza et
al., 1997). On the basis of this approach, the determination of total economic value of any
ecosystem is performable, calculating single value of market and non-market components
derived from it. Even if the evaluation of the non-market values of ecosystems represents the
major target of the economists, this procedure is affected by severe methodological limits
(Pimm, 1998). Despite prices are simple to define for market objects, the calculation of value
assignable to different world‘s ecosystems could produce severe mistakes. Nevertheless, this
strategy could represent an useful universal language of communication among politicians,
populations and scientists making ecological values comparable, on an economic point of
view, to economic services and manufactured capitals (Costanza et al., 1997). On these bases,
wetlands economic values per hectare was estimated to be 165 US$y-1 (Schuyt and Brander,
2004). Due to the fact that the world surface covered by wetlands is about 320,000 km2
(Troussellier and Gattuso, 2007), their total value is about of 5.3 109 US$y-1. Obtained
estimations by Costanza and colleagues (1997) reported a total value of 20,070 US$ ha -1y-1
(average) for tidal marshes, while Mangroves habitats were evaluated 11,029 US$ ha-1y-1.
The values of different ecological functions could be evaluated considering both the
economic damages derivable from their losses and/or advantages from their preservation. As
example, wetlands produce a climate regulation function due to the carbon sequestration,
evaluable in terms of 265 US$ ha-1y-1, a positive effect on the regulation of disturbance
(mainly due to the flood control and storm protection) of 1,839 US$ ha-1y-1. Considering only
coastal wetlands, advantages derived from nutrient cycling and waste treatment were
estimated to be 4,500 US$ ha-1y-1. The nursery value was calculated to be 170 US$ ha-1y-1,
while the habitat value for the protection of migratory species was considered to be of 439
US$ ha-1y-1. The economic value related to the food production and the collection of raw
material derived from the productivity of these systems, ranged from 1,142-2,752 US$ ha-1y-1
(Costanza et al., 1997).
On these bases, it is clear as the conservation of these ecosystems represents an economic
relevance. It is to notice that if the evaluation of the economic values derived from some
functions of these ecosystems, such as the primary and secondary production is reasonable;
on the contrary evaluations concerning not-marketable benefits are very difficult to perform
and could produce questionable results. In fact, these ecosystems constitute an invaluable
historical and cultural heritage of not simple conversion into economic terms (Viaroli et al.,
2007). As example, it could be quite impossible to evaluate in economic terms the possible
losses which could be derived from the ecological deterioration of the Venice lagoon (Italy)
listed in 1987 by the UNESCO as world heritage site.
254 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

8.3. NATURAL AND HUMAN-CONTROLLED FACTORS THAT AFFECT

TROPHIC LEVEL
Trophic level in coastal lagoons is a result of different synergic factors acting both to
global and local scales and deriving from natural dynamics or human activities. In relation to
natural factors, the main forcing feature on a global scale is represented by the geographical
localization, while geomorphology, tidal effects, and salinity are more related to local
component. Geographical localization is the first factor able to determine some effects on
lagoon trophic level. In fact, it defines the general environmental context forcing the main
physico-chemical and ecological characteristics. For instance, water renewal is the process
characterizing the reduction of nutrient levels inside the lagoon by dilution with the
surrounding sea water. The trophic level of the near sea water represents the minimum base
value for the lagoon ecosystems. Seas characterized by high nutrient levels show a low
dilution efficiency compared to oligotrophic ones. Recent studies have shown that the
Mediterranean sea is characterized by different trophic status. Generally, it is oligotrophic
(Fogg, 1995), but the Adriatic Sea is mesotrophic, because of the Po River inputs (Crispi et
al., 2001), while the Aegean Sea is mostly eutrophic for the discharges from the Black Sea
(Crispi et al., 2001). Climate represents an aspect linked to both global and local dynamics.
Local and occasional climatic events could determine significant effects on lagoon structure.
As example, tropical coastal areas are frequently subjected to hurricanes which could affect
the lagoon structure (Medina-Gómez and Herreira-Silveira, 2003), producing significant
differences among systems. Meteorological factors have also impacts on lagoon morphology
and related physico-chemical characteristics. Rainfall and the runoff could determine
significant changes in rapidly responding variables such as nutrients, phytoplankton and
zooplankton biomass and composition (Rissik et al., 2009). Hydrological balance depends on
different co-occurring global and local-driven phenomena such as evaporation, water inflows,
rains and water losses due to outflows. When evaporation exceedes freshwater supplies
volumes, a hyper saline character is usually highlighted (Moreira-Turcq, 2000). Winds are the
main factor responsible of natural hydrodynamics in coastal lagoons scarcely affected by
tides. Winds enhance water exchanges and fluxes, favouring oxygenation; on the contrary
they could produce sediment resuspention (Medina-Gómez and Herrera-Silveira, 2003). The
resuspension of steady soft sediments raises organic particulate and dissolved organic matter
towards the surface (Hopkinson, 1985) increasing phosphorous levels (Søndergaard et al.,
1992), activating bacterial oxidative mineralization (Fanning et al., 1982) and increasing the
remineralisation rates (Wainright, 1987; Wainright, 1990). Resuspension also activates
nutrient release in interstitial water from sediment particles (Wainright and Hopkinson, 1997).
Geomorphologic features are important aspects in system classifications, able to influence
lagoon dynamics. In fact, they could determine differences in sunlight exposure and water
exchanges (McLusky and Elliot, 2007), helping nutrient accumulation and high primary
productivity rates. On a general basis, coastal lagoons are usually oriented shore-parallel
(Bossard et al., 2000) and the width of the connections with the adjacent sea are less than
20% of the barrier length during high tide (Bird, 1994). Barriers are constituted by sand or
single banks, bars, or coral (McLusky and Elliot, 2007) depending on both local
geomorphology and geographical localization. In fact, temperate coastal lagoons are typically
characterized by sandbars, while tropical and sub-tropical lagoons are mainly characterized
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 255

by the presence of coral reef barriers originated shore parallel or circularly around islands
derived from volcanic activities. Both barriers nature of the barriers and dimensions of the
communicating channels (width, length and depth) affect water exchanges between lagoons
and the surrounding sea. The morphology of the communicating channels is strictly related to
the geomorphology of the region and general marine and climatic features. A recent study
performed on 40 Atlantic-Mediterranean coastal lagoons have shown that the geomorphologic
features (volume, sea influence and shoreline development) explained alone the 22% of the
variance in the canonical analysis and an additional 75% in conjunction with the
hydrographical and trophic characteristics (Perez-Ruzafa et al., 2007). For these reasons,
human management of barriers could determine significant effects on trophic level, diversity
or assessment of biological communities as observed during occasional artificial openings of
sandbars (Kozlowsky-Suzuki and Bozelli, 2004). Geological structure of bottom sediments
could significantly affect nutrient dynamics. Nutrient release from sediments is a process
strictly related to grain-size structure. Chemical composition of sediments could determine
different releasing processes during resuspension. In fact, sediments resuspension may lead to
the oxidation of the iron into its ferric forms (oxides) which adsorb orthophosphates removing
them from the water column (Golterman, 1995; 2001). Also, lagoon soil geology could
determine significant difference in nutrient fluxes; karstic substrates determine the absence of
river or stream inflows, favouring the presence of spring water (Medina-Gómez and Herrera-
Silveira, 2003) and reducing notably the nutrient inputs coming from agriculture and soil
drainage. Evolutionary trends in lagoon systems could be extremely rapid. As example,
changes of the geomorphologic structure occurred in Tindari lagoons (Sicily, Italy) have
produced a net migration of the whole sandbar system in the NW-SE direction and a
significant natural decrease of the lagoon surface (about 54.000 m2 from 1997 to 2009). This
constant evolve of the system has produced, as consequence, significant effects on water
chemism (Ruta et al., 2009), trophic levels and biological communities (Leonardi and
Giacobbe, 2001). This behaviour does not represent an exception, the Illa de Buda area (Ebro
delta) showed the same evolutionary trend with a net reduction of the total surface area of 150
ha from 1957-2000 at a rate of 2 hay-1 (Valdemoro et al., 2007). It is well known that tidal
effects differentiate substantially worldwide. Related to the geographical localization of the
lagoon systems, water volumes exchangeable between lagoon and sea and the potential
dilution effect exercised by the water flux on nutrient levels vary significantly. In fact, the
Mediterranean sea, except the Northern Adriatic area, is characterized by lower tidal effects
compared to the ocean coastal areas. According to the tide influence, lagoons could be
classified in three different groups: lentic non-tidal lagoon (tidal range <50 cm), lentic
microtidal lagoon (tidal range >50 cm) (McLusky and Elliot, 2007) and mesotidal lagoon
(wide tidal in the range of 1-2 m), as highlighted for the Atlantic Ocean (Zaldivar et al.,
2008a). Systems characterized by wide and significant tidal inlets could represent a source of
nutrients and suspended solids for the surrounding coastal area. As example, fluxes of
suspended solids related to the tide of 13-15 t per tidal cycle were recorded in the Tapong
lagoon (WeiChun et al., 2010).
Due to their location, between the land and sea, coastal lagoons are characterized by a
mixing area between saline and fresh water. Based on hydrological balance within the lagoon
(Kjerfve, 1994) and meteorological events, water salinity may vary from fresh water (<3‰)
to hyposaline/brackish (3–30 ‰), to marine (30–35 ‰) or hypersaline (>35 ‰). Changes of
salinity related to changes of the morphological components (Valdemoro et al., 2007),
256 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

phytoplankton (i.e. diatoms, Saunders et al., 2007), zooplankton (Kozdowsky-Suzuki and

Bozelli, 2004) and vegetation assessment (Valdemoro et al., 2007) have been observed. A
study performed on 42 fish species in the Koycegiz Lagoon Estuarine System, located on the
north-western Turkish coast showed that salinity and turbidity were the most important
environmental parameters affecting secondary productivity and determining changes in the
fishes assemblage structure (Akin et al., 2005). Relationships between zooplankton and
abiotic variables (temperature, precipitations, pH, and duration of ice cover) have been
reported by Feike and colleagues (2007). It has been observed that, in temperate systems
salinity changes have caused the dominance of Daphnia spp., while fluctuations occurring at
species level in tropical lagoons have to be better explored (Kozlowsky-Suzuki and Bozelli,
2004). Approximately 60% of the world‘s population is concentrated in settlements within the
coastal zone, i.e. areas that extend 50 km inland from the coastline (Crossland et al., 2005).
However, coastal areas have consistently been neglected, poorly understood and exploited,
and are under increasing pressure from rapid human population growth and over-exploitation
of resources. Humans could affect these ecosystems with great pressures (Aliaume et al.,
2007) even if it is to notice that human management and regulation strategies performed
throughout the history have allowed some systems to be conserved until nowadays (Carrada,
2007). As result of recent human activities, many coastal lagoon in the eastern Australia have
evidently changed. In the Orielton Lagoon (south-east Tasmania, Australia) recent
anthropogenic hydrological modifications have influenced water salinity, affecting the lagoon
ecology (Saunders et al., 2007). Human activities could strongly influence trophic level by
acceleration of natural processes increasing significantly nutrient levels for the primary
producers. Man-made pressure has been dramatically increased over the last several decades
as a consequence of uncontrolled agricultural, industrial and tourist development.
Mediterranean area is a suitable zone for agriculture and tourism. In tropical and sub-tropical
systems, the occurrence of acid sulphate soils determines high drainage rates of soil nutrients
and fertilizers into the reef (Sammut et al., 1996). These land use practices led to an
accelerated soil erosion and a related increasing in fertiliser and pesticide leakage to the
aquatic system (Anon, 2003). Effluents from municipal waste water treatment plants (Renzi et
al., 2009), industrial activities and human settlements, directly or indirectly collected into
coastal lagoons, determine a significant increase of bioavailable nutrients in water (Ibrekk et
al., 1991), enhancing the micro and macrophytes proliferations (Perez-Ruzafa et al., 2005).
On the basis of the consideration exposed, it is evident that many studies on coastal lagoon
have to be necessarily included. During monitoring studies, a critical and preliminary
consideration on factors affecting these ecosystems could allow researchers and politicians to
evaluate the relative weight of single variables and perform well-sized sampling campaigns,
monitoring and management programmes. A summarize of major natural and human-
mediated factors affecting lagoon trophism is represented in figure 8.3.1.
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 257

Figure 8.3.1. Summary of major natural and human-mediated factors affecting lagoon trophism.

8.4. WHEN THE IMBALANCE OCCURS: EUTROPHICATION, MAIN

FEATURES AND ECOLOGICAL EFFECTS
During the last thirty years several coastal environments have shown the occurrence of
eutrophication, particularly enhanced in lagoons and estuaries. The eutrophication represents
a natural human-enhanced phenomenon which could compromise the ecosystem productivity
because of an increase in the rate of supply of organic matter (Nixon, 1995). The ecological
characteristics of all organisms living in coastal lagoon are related to environmental stress due
to the alternating inputs of marine and freshwaters, in addition to the increased nutrient inputs
related to human activities (Sfriso et al., 1992). Dynamics occurring in abiotic matrices (water
and sediment) and biological populations (plankton, benthos, nekton) have been widely
documented by literature (Zaldivar et al., 2008a and all citations within the paper). The main
ecological effect produced by nutrient enrichment is represented by an acceleration in the
growth of micro and macroalgae species, causing a loss of water quality (European
Commission, 1991). Eutrophication involves a reduction of the available light in the water
column, due to the increase of phytoplankton mass, the growth of epiphytes on the seagrass
and reduction of their photosynthetic powers. Under conditions of eutrophication, seagrasses
are less competitive than opportunistic macroalgae. An increase in organic matter and
sulphide concentration in sediments could cause a reduction of seagrass biomasses, allowing
opportunistic macroalgae to replace them (Goodman et al., 1995). This phenomenon is
reversible and a reduction in nutrient concentrations could lead to seagrass recovery (Ben
Charrada, 1995; Lenzi et al., 2003; Plus et al., 2003). Sediment characteristics as pH, Eh
(redox-potential), grain-size, nutrient and trace elements concentrations are key factors for
seagrass establishment and presence in an eutrophic ecosystem (Ben Charrada, 1995; Plus et
al., 2003; Renzi et al., 2007). Many eutrophic coastal lagoons and estuaries produce excessive
macroalgal biomass during warmer months (Morand and Briand, 1996). These conditions
lead to a settlement of organic matter in sediments and an increase in sulphate-reduction. In
these ecosystems more than 50% of organic matter is degraded by sulphate-reduction
(sulphate respiration) bacterial processes (Jørgensen, 1983). High decomposition rates of
organic matter involve toxic gases such as CO2 and H2S. Dissolved sulphides have a toxic
258 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

effect on biota, producing a relevant impact on the system (Heijs et al., 1999). In this
condition, pH values in sediments decrease at levels of greater acidity (for marine
ecosystems) and Eh can reach very low values (about -400 mV), leading to a build-up of both
reduced and reducing components. Low values of Eh and pH induce to ammonium
production (Marty et al., 1990) and nitrite increase by ammonification of organic matter,
causing a toxic effect on biota (Torres-Beristain et al., 2006) and stimulating production of
nitrophilic algal species. This is particularly evident for rooted plants, whose development is
curbed by bacterial and chemical conditions in the sediment, leaves epiphytes development,
phytoplankton shielding out light and floating macroalgae masses that can suffocate seagrass
meadows (Den Hartog, 1994; Raffaelli et al., 1998). High levels of eutrophication could
induce changes from seagrass to seaweed and, if the conditions worsen, to opportunistic
microphytes characterized by an higher turnover (Duarte, 1995). Lenzi and colleagues (2003)
have observed a macroalgal distribution gradient with phosphorophilic macroalgae near the
human nutrient source and nitrophilic macroalgae farer. The anoxia and bacteria associated
with the sulphur cycle could mobilise pollutants stored in sediments such as mercury
(cinnabar) and methylmercury (CH3Hg+) (Wood and Wang, 1983; Kim et al., 2006). These
mechanisms are not yet well known and require further researches. In order to face the effects
produced by the eutrophication in coastal lagoons, human control measures are mainly based
on engineering approaches (creation of underwater canals, use of pumping stations to increase
sea water inflows, use of flow accelerators). Often excesses of macroalgae biomasses are
removed using harvesting boats to avoid the occurrence of decomposition processes. These
approaches require expansive maintenance which frequently can not be sustained. A not
expensive strategy could be represented by human induced sediment disturbance, which could
induce oxidative mineralising activities (Logan and Kirchman, 1991), increase of biodiversity
(Widdicombe and Austen, 2001), development of phanerogam meadows with reduction on
phosphorus limited macroalgae (Lenzi et al., 2003). Nevertheless, the application of this
techniques requires the absence of significant pollution of sediments. In fact, pollutants are
released from sediment to the water column when oxidation of the organic matter occurs and
could be transferred towards the food chain (Kim et al., 2006), producing ecotoxicological
risks for biota.

8.5. AN OVERVIEW ON RECENT DATA RELATED TO THE TROPHISM

OF LAGOONS WORLDWIDE

A review of recent literature reporting trophic levels and specific characteristics of

coastal lagoon worldwide is explained. All data have been acquired from major databases of
literature, but also public reports of international interest have been considered and included.
Despite the great number of coastal lagoon worldwide, not all world‘s area have been well
documented by a recent literature. As example, tropical sedimentary lagoon systems are
poorly studied (Gordon, 2000). Explanation for this occurrence is mainly related to local,
political, economic and social troubles and lack of resources to perform ecological studies.
Often, data are acquired on a local basis to allow management plans, but they are not
efficiently diffuse throughout international databases or scientific publications. Actually,
scientific researches performed in European Countries are the most represented in
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 259

international papers, as the application in the European Community of the Water Framework
Directive has enhanced these researches and a large economic support has been given to
develop suitable monitoring programs.
The geographical localization of recent studied lagoons worldwide is summarized in
Figure 8.5.1 Only papers reporting information concerning trophic levels have been included.

Figure 8.5.1. The geographical localization of recent studied lagoons worldwide.

260 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

Water exchanges with the surrounding sea are naturally regulated in tropical and sub-
tropical lagoons. In fact, the occurrence of a long rainy season determines notably an increase
of lagoon volume which could also produce flooded of communicating channels. During the
dry season the evaporation exceeds freshwater supplies and the trophic level generally
increases in these systems. Desert areas, lying in dry equatorial regions, are characterized by
high evaporation rates and wide depth excursions (Lamptey and Armah, 2008), which could
also produce the complete desiccation of the lagoon during dry seasons and determine a
temporary behaviour. In high evaporative systems the exploitation for the production of salt
has acquired a notable importance (Lamptey and Armah, 2008).
Coastal lagoons located in not developed Countries are particularly subjected to human-
derived pollution. As example, about 3.6 billion people live in Asia exploiting natural
resources along the coasts (Jennerjahn et al., 2009). The agriculture consumes about 81% of
Asia‘s annual water withdrawal overstressing coastal lagoon systems (World Resources
Institute, 2005). It has been highlighted by some studies that tropical Asia represents the area
with maximum nutrient and sediment inputs to the seawater (Elvidge et al., 1997).
Overpopulation could determine a significant nutrient charge also for coastal ecosystems
characterized by rapid water exchanges with the ocean. An example is represented by Tapong
lagoon (Taiwan, Asia), characterized by wide tidal excursions (2.2-6.0 m), with the strongest
tidal current reaching about 75 cms-1 over a spring-ebb tidal cycle (WeiChun et al., 2010).
Nevertheless, the lagoon is subjected to eutrophication phenomena, as its surroundings are
overpopulated and over-exploited by aquaculture and fish farming. Loading rates of nutrients
(N and P) have been reported to be about 1.87 and 0.51 mol m-2y-1, with a residence time of
about 10 days (Hung and Hung, 2003). In this system, aquaculture is mainly addressed to the
oyster cultures. A recent study in Tapong lagoon has shown that, oysters may increase
nutrient levels in the water column via recycling from excretion and remineralisation of feces
and pseudofeces (Lin et al., 2006). The application of not well sized management plans can
determine not desired effects in lagoon systems. During 2002, all of the oyster culture racks
were removed from Tapong lagoon, as it was designated a National Scenic Area, with the aim
to reduce nutrient loads. Removal of oyster culture racks resulted in phytoplankton blooms
and increasing of eutrophication only in the inner region, which was subject to poor flushing
(Huang et al., 2008). Some studies (Lin et al., 2006; WeiChun et al., 2010) have shown that
in many tropical lagoons (e.g. Chiku, Terminos, Tampamachoco, Celestun, Huizache-
Caimanero) the food web is dependent on the accumulation of detritus in sediments, while in
Tapong lagoon the trophic web is mainly supported by herbivores. Researches performed in
the eutrophic Lake Nakaumi (Japan) have highlighted that the first biological response to the
water eutrophication is related to the benthic community, occurring after 20 years from the
first evidence of phenomenon, on a longer temporal-scale if compared to that of the water
(Katsuki et al., 2008). In tropical lagoon systems the major control on nutrients, during dry
season, is exerted by natural processes such as recycling in mangroves (Jennerjahn et al.,
2009). As reported by Jennerjahn and colleagues, the eutrophication in the Segara Anakan
lagoon (Indonesia) ranges from low to moderate because of the rapid exportation of nutrient
towards the Ocean and the strong control exercised by natural processes in nutrient regulation
dynamics. Chilika lagoon (India) represents a Ramsar site of particular interest for its high
biodiversity. The lagoon has shown environmental and anthropogenic impacts over the last
several decades, such as environmental degradation, siltation, changes in salinity gradients,
extensive growth of invasive species, depletion of fishery resources, shifting of the lagoon
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 261

inlet, choking of the lagoon-sea channel. From a previous study, performed for six years from
1999 to 2004, it has been determined that the lagoon was slightly eutrophicated and that the
water quality was largely determined by salinity changes (Jeong et al., 2008). Management
strategies performed to enhance sea-water exchanges in these ecosystems have led no suitable
effect on salinity and turbidity which affect fish catchments and total biodiversity (Mohapatra
et al., 2007).
Effects related to wars, poverty and the lack of a technological development represent the
major problems to face off in many Nations. Countries affected by socio-political problems
and human health diseases show a lack of knowledge on coastal areas. An example is
represented by Africa whose economic and political assessment do not allow to allocate
national resources for studying critical areas and widely characterizing coastal lagoons, but
they are mainly aimed to face social problems related to the absence of food, drinkable water
for local populations and human diseases. The reconciliation among environmental
sustainability, humans needs and economic development represents a challenging problem. In
order to favour scientific knowledge and support these Countries, the European Commission
has developed numerous multidisciplinary projects including the MELMARINA which was
established to monitor and model coastal lagoons in Morocco, Tunisia, and Egypt with the
aim to evaluate environmental changes in the Southern Mediterranean Region linked to sea-
level rise changes (Flower and Thompson, 2009). Recent studies have showed as in this
Mediterranean area water resources are under extreme and growing pressure and water
pollution, land reclamation are the main causes of wetland losses around the Mediterranean
(Flower and Thompson, 2009). In addition, studies related to the MELMARINA project have
deduced that excess nutrients and discharge of waste or agricultural return water together with
land reclamation are probably the most serious current and common problems confronting
sustainability of the North African lagoons (Ramdani et al., 2009). Many data are available
by literature from Burullus, Edku, Manzala, Maryut lagoons located in the Nile Delta, Egypt
(Oczkowski and Nixon, 2008). These systems support alone the 60% of the Egypt‘s fish
production. Egypt‘s fertilizer consumption hasincreased steadily from 3.4 x 105 t in 1965 to
1.3 x 106 t in 2002 (FAO, 2006). Given the dramatic increase in human-derived nutrient loads
on the Nile Delta, a considerable eutrophication in lagoon waters during the last decades has
been observed (Okbah and Hussein, 2006), threatening fish productivity. Despite inorganic
nitrogen changed from 1 µM (1957) to over 1000 µM (1995), primary production in these
systems was dissolved inorganic nitrogen limited (Oczkowski and Nixon, 2008). In relation
to Tunisia, researches performed in Slimane lagoon have highlighted the occurrence of a
constant enrichment in phosphorous compounds due to human activities, with nitrogen as the
limiting factor (Hadj Amor et al., 2008). Bizerte lagoon represents a highly human impacted
ecosystem for the presence of urban, agricultural, industrial activities, fisheries and
aquaculture farms. Nevertheless, on the basis of the chlorophyll a levels, it could be classified
in lower range of eutrophicated systems (Grami et al., 2008). Studies performed on the Ghar
El Mehl lagoon (Northern Tunisia), characterized by an eutrophic behaviour, have shown that
in this system loads of human origin produced 182 ty-1 of total nitrogen and 26 ty-1 of total
phosphorous (Rasmussen et al., 2009). Keta lagoon (Ghana, West Africa) represents the
largest of more than 90 lagoons along the 550 km coastline of Ghana (Lamptey and Armah,
2008). In this system high evaporation rates, induced by solar exposition, cause a natural
increase of nutrients during summer (Hadj Amor et al., 2008) and presence of permanent
hypersaline nutrient enriched waters, which involve osmotic stress for aquatic organisms and
262 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

significant changes of populations along the environmental gradient (Lamptey and Armah,
2008). Salinity changes have a clear control on spatial and temporal variations of zooplankton
communities, while the role of the trophic status could be not clearly highlighted as in Grand-
Lahou Lagoon, Cote d‘Ivoire (N‘doua Etilé et al., 2009). Ebrié Lagoon represents the largest
coastal ecosystems in the Western Africa. In this system nutrient loads are mainly due to the
river inputs and land runoff phenomena. Total annual nitrogen loads in 2000 were estimated
to be 33 kt, of which 45% from urban sources, 42% from runoff and 13% from atmospheric
deposition. In this system domestic loads are responsible of the 95% of the urban nutrient
load (Scheren et al., 2004).
Although the Australian continent is characterized by many transitional ecosystems
(more than 200 lagoons and estuaries considering only the New South Wales), there are few
detailed site-specific studies (Sanderson and Coade, 2010). Consequently, conservation and
restoration programmes have been difficult to implement (Saunders et al., 2007). As reported
by some studies, Tasmania‘s coastal lagoon waters (ranged in size from 0.02-40 km2) are
characterized by a clear nitrogen limitation (Harris, 2001). Many Australian estuaries and
lagoons are shallow and the growth of benthic macrophytes would not be limited by the
availability of photo-synthetically active radiation under natural sediment and nutrient loads
(Sanderson and Coade, 2010). In these systems, which directly exchange water with the open
ocean, eutrophic levels during the year could be influenced by the regulation of water
volumes inside the lagoon. In fact, a study performed on Dee Why Lagoon (northern beaches
of Sydney) has shown that after a prolonged summer dry period, the lagoon filled up over 5
weeks of continuing rainfall until it broke open to the sea, transporting a substantial flux of
nutrients and carbon towards the ocean, which, with the subsequent tidal flushing (>60% of
volume each tidal cycle) until the lagoon closed, would assist in maintaining mesotrophic
conditions within the lagoon (Rissik et al., 2009). The lagoon of the Great Barrier Reef,
located off the Queensland coast of Australia, is an area where tourism represents the major
economic source (Productivity Commission, 2003). Such a system is characterized by a great
surface, over than 1,500 km from Bundaberg (in the south) to the tip of Cape York (in the
north). This extention justifies ecological changes from typicaly tropics to typicaly subtropics,
with related changes in rainfall patterns (Gordon, 2007). In this lagoon systems major threats
are represented by human pressure associated with land use practices (agricultural activities
and urbanization) and harbour activities (Gordon, 2007). Further studies have shown that
urban waters are responsible of nutrient input for the whole reef lagoon area, while other
human activities, such as effluents from urban sewerage treatment plants and aquaculture
facilities, contribute less than 3% to the overall nutrient load (Anon, 2003) and are able to
affect lagoon dynamics only on a local basis. Nevertheless, the quick expansion of the
aquaculture along the Great Barrier Reef coast could represent a potential source in the near
future (Boyd, 2003). In such a system, rivers represent a notable source of nutrients.
Dissolved inorganic nitrogen measured in river plumes are reported to be typically 10–50
times the concentrations exceeding the trigger levels for environmental harm on corals,
seagrasses and algae (Furnas, 2003). Notable effects on inshore coral reefs produced by
eutrofication have been described by Fabricious (2005).
In relation to American coastal lagoons, tropical and sub-tropical regions, such as the
Caribbean Sea and the Gulf of Mexico, are particularly studied. In these areas hurricanes
frequently occurs and pristine ecosystems are characterized by low trophic levels (chlorophyll
a, chla, ranging from 0.71 to 7.00 mgm-3) as reported by recent literature in Celestun,
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 263

Chelem, and Dzilam lagoons (Herreira-Silveira et al., 2002; Medina-Gómez and Herreira-
Silveira, 2003; 2006; Tapia Gonzalez et al., 2008). In these ecosystems, groundwater inputs
could represent an important source of silicates, phosphorous (Puerto Morelos Reef lagoon)
and nitrogen compounds (Nichupte lagoon system) (Carruthers et al., 2005). Nutrient shifts,
causing phytoplankton growth limitation, occur following natural cycles (Herreira-Silveira,
1998). A large part of lagoons are characterized by high pollution levels mainly related to
agricultural and urban activities. As example, Indian River lagoon, Florida, is affected by
human-related sources of nitrogen (832,645 kgy-1) and phosphorous (94,476 kgy-1)
compounds (Sigua and Tweedale, 2003; Philips et al., 2010) and Ciénaga de Tesca lagoon
(Colombia) collects the 60% of waste domestic waters from the Cartagena City. In this last
ecosystem, eutrophication levels are very high with a phytoplankton biomass ranging from
110 to 160 mgm-3 of chla and ammonium concentrations in water from 0.3 to 1.0 mgL-1 of N
(Lonin and Tuchkovenko, 2001). Coastal lagoons in Southern America are generally
characterized by higher salinities, related to high evaporation rates, and significant
fluctuations during the year related to the climate dynamics, with considerable effects on
trophic level and local biota (Moreira-Turcq, 2000; Souza et al., 2003).
The knowledge of coastal lagoons in European countries has been remarkably improved
by the introduction of the Water Framework Directive and, actually, scientific researches on
European lagoons are the most represented in literature. Furthermore, the European
Community has also encouraged and financed long term researches in Mediterranean areas
not only in Europe, but also in the Northern part of Africa, the Middle-Est, and Southern
America. On a general basis, in Mediterranean and Temperate areas, exchanges between
lagoons and sea are mainly regulated by humans, because of minor effect of climatic
phenomena. Most of physical and environmental variability of Atlantic-Mediterranean coastal
lagoons is related to its size, salinity differences compared to the open sea and the trophic
status (Perez-Ruzafa et al., 2007). A large lagoon perimeter with shoreline development helps
nutrient inputs; for this reason the fishing yield increases with increasing of the
perimeter/surface ratios. In these systems the increase of primary productivity involves the
abundance of some species at expense of species richness (Perez-Ruzafa et al., 2007).
Lagoons located in the Baltic Sea (Northern Europe) are characterized by low values of
salinity during the whole year and presence of iced surface during winter (Schumann et al.,
2006). In Kursu Marius (Curonian) lagoon, the eutrophication (83-103 mgm-3 of chl a) is
associated to the blue-green algae bloom (Aleksandrov and Dmitrieva, 2006). Toxic
proliferations are probably due to nitrogen reduction unbalanced than that of phosphorous
(Schernewski et al., 2008). Long term monitoring programs performed on both freshwater
Curonian (Kursu Marius) and brackish Vistula lagoons have highlighted a general increasing
of nutrients in the Baltic Sea waters during the 20th century. In the late 1980s, in Curonian
lagoon, the input of N ranged from 60.8 to 109.6 gm-2y-1, while the P ranged from 3.7 to 8.5
gm-2y-1. The crisis in industry and agriculture in 1990s resulted in a nutrient loading under the
permissible level leading to eutrophication, but an associated reduction of eutrophication was
not observed (Aleksandrov, 2009; 2010). Climate warming and an increase in the number of
―warm‖ years in the 1990s and 2000s have been regarded as possible causes for the
continuing eutrophication of the Curonian Lagoon despite a significant reduction of
anthropogenic impact. In contrast, the trophic state of Vistula lagoon has not attained high
levels, because hydrodynamic activity and brackish waters of this lagoon have prevented a
high primary production. In Mediterranean coastal wetlands, highly affected by agricultural
264 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

activities, external freshwater inputs are considered the main driver of nutrient supplies
(mainly as inorganic nitrogen) causing a fertilization effect (Chapelle et al., 2000; Lucena et
al., 2002; Perez-Ruzafa et al., 2005).
The trophic level of lagoons could significantly influence the structure of the trophic web.
Although the food web length is conserved in high eutrophic lagoon, some researches
performed in French Mediterranean lagoons (Canet and Lapalme) have pinpointed that
several consumers occupied a lower trophic level in eutrophic basins (Canet) than in
mesotrophic ones (Lapalme), because of a more omnivorous feeding regime in Canet (Carlier
et al., 2008). Links between global climate and dystrophic events have been highlighted in the
eutrophic Thau lagoon, France (Harzallah and Chapelle, 2002). The Mar Menor lagoon is a
well studied ecosystem, characterized by a high touristic impact, hypersaline feature but
nutrient levels under the limit of the eutrophication risk. Urban effluents represent a notable
source of nutrients and the presence of coastal marshes effectively involves a reduction of
water eutrophication, as highlighted by Alvarez-Rogel and colleagues (2006), because they
act as a filter to reduce nutrient concentrations before the polluted water flows into the Mar
Menor lagoon. Nevertheless, the canalization of urban effluents, performed as management
strategy, could determine a lower efficiency in nutrient reduction and an increase of
eutrophication. Other studies made on this basin have shown a link between nutrient inputs
and not-point agricultural sources, with maxima values of nitrates observed after heavy rains
in autumn (Velasco et al., 2006). Furthermore, benthic communities play an important role in
regulating the resistance capacity of lagoon ecosystems (Lloret and Martin, 2009). In fact,
Caulerpa prolifera represents an important organism able to increase system resistance
towards eutrophication processes (Lloret et al., 2008). In this ecosystem relationships
between chla levels and fish larvae density suggests the occurrence of a top-down control of
the trophic web (Perez-Ruzafa et al., 2005). A large quantity of scientific papers describes the
trophic level of coastal lagoons in Portugal, and Ria de Aveiro (Figueiredo da Silva et al.,
2002; Lopes et al., 2005; Lopes and Silva, 2006; Rodrigues et al., 2009), Ria Formosa
(Edwards et al., 2005; Nobre et al., 2005; Newton et al., 2003; Newton and Mudge, 2005;
Gamito and Erzini, 2005; Gamito, 2008; Mudge et al., 2008), Obidos (Pereira et al., 2009a, b)
and Algarve (Coelho et al., 2007; Cartaxana et al., 2009) lagoons are the most studied coastal
systems. Ria the Aveiro lagoon is estimated to receive 6,118 ty-1 of total N and 779 ty-1 of
total P from rivers. In this system sewage effluents contribute for the 5% (yearly basis) of the
total charge, with an increase to 65% during summer (Figueiredo da Silva et al., 2002).
Nevertheless, further studies have stressed that eutrophication is not frequent in this area
(Lopes and Silva, 2006). Researches performed on Obidos lagoon have shown that the system
is subjected to time-spatial fluctuations of nutrient levels (Pereira et al., 2009a). It is therefore
necessary to perform observations at different time scales in eutrophic coastal lagoons,
because of great differences observed in daily/night cycles related to the nutrient availability
in water column (Pereira et al., 2009b). Ria Formosa lagoon has shown an enrichment in
phosphorous during the observation year, while nitrogen enrichments have been observed in
autumn during the rainy season (Newton et al., 2003; Newton and Mudge, 2005). In this last
system a significant tidal effect has been highlighted, determining an important additive
factor which produces the land-ocean gradient stressor (Gamito, 2008).
In Italy, ecosystems studied in detail are Venice (Carrer and Optiz, 1999; Bendoricchio
and De Boni, 2005) and Orbetello lagoons (Benedetti-Cecchi et al., 2001; Brando et al.,
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 265

2004; Specchiulli et al., 2008) due to their social, economic and ecological relevance and to
the occurrence of frequent dystrophic crises.

8.6. INTERNATIONAL DIRECTIVES: THE NEED FOR ORGANIZING A

STRATEGIC REGULATION
The progressive decreasing of the surface occupied by wetlands and, in particular, by
estuaries and lagoons, is a phenomenon occurring worldwide, probably related to different
natural and human-mediated factors (Boesch et al., 1994). These systems are not stable and
affected by littoral processes along the shoreline (Valdemoro et al., 2007), currents and
relative sea level rise (McFadden et al., 2007) linked to the vertical accretion (Day et al.,
1997). Recent projections performed by McFadden and colleagues (2007) have stressed that
the increasing of only 38 cm of sea-level will determine in 2080 the loss of 22% of the total
surface actually covered, on a world basis. Human mediated factors, such as the increase of
urban settlements along the coastal area and land use, directly and indirectly affect the
reduction of coastal lagoon surface, producing changes in the natural land cover assessment
(Ruiz-Luna and Berlanga-Robles, 2003). Also, reclaiming processes of land, out of necessary
of agricultural activities, and planned remediation of wetlands, performed worldwide to face
the health disease because of malarial infections, represent a significant human impact. Health
diseases are not a secondary cause with that human communities have been face during the
last century. Moreover, the occurrence of infections caused by the Plasmodium spp.
represents an actual widespread endemic health problem (Leder et al., 2004). These parasites
are transmitted to humans throughout the puncture of about a thirty of different types of
female mosquito species functioning as vectors (Collins and Jeffrey, 2007). From a
standpoint of human health, wetlands represent areas to remediate rather than ecosystems to
protect and to study, although they are systems of particular ecological, for their great variety
of environments and flora and fauna richness, and clear economic interest (Costanza et al.,
1997). It is considerable to notice that human perception of social and economic values
deriving from wetland protection strategies is a function which varies depending on the
geographic and economic situation of the country, because of different market values of
commercial products and local populations needs (Costanza et al., 1997). In the
Mediterranean basin it has been estimated that there still are 28,500 km2 of wetlands and
about two-thirds of wetlands in Spain, France, Italy and Greece have been drained during the
last two generations (Diamantopoulou et al., 2008).
The consciousness of the ecological and economic importance of these ecosystems is a
quite recent and not totally completed process. Policies finalized to protect transitional
ecosystems have been originated from the Ramsar Convention on wetlands hold in Ramsar
(1971), Iran. Although this event has been thought to preserve important habitats for birds
migrating species protection, it focused for the first time the importance of wetlands for
biodiversity conservation, performing a classification system for wetland types (Christian and
Mazzilli, 2007) and stimulating further initiatives. Later, at the United Nation Conference on
Environment and Development (UNCED) occurred in 1992 at Rio the Janeiro, the Agenda 21
document was adopted. It was a document related to the coastal area integrated management
and structured to allow successive agreements and legal instruments. An increasing interest in
266 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

wetlands has been recording since then (Carlsson et al., 2003). This tendency had led to the
development of directives and guide lines for the preservation of these ecosystems
worldwide.
National regulations for managing and protecting coastal water have been developed
worldwide; nevertheless, the management of eutrophication-related problems often needs to
plan programs on a wider scale than political one. Kursiu Marus/Curonian lagoon is
connected to the Baltic sea only throughone channel, whose northern part is under the
jurisdiction of Lithuania and the southern part is under the Russia‘s jurisdiction (Aleksandrov
and Dmitrieva, 2006; Zelmys et al., 2008). This example shows as national legislations could
be inefficient to protect and manage coastal ecosystems.
In European Countries the introduction of the Water Framework Directive represents the
first important step towards the environmental protection of aquatic habitats, integrating the
EU political strategies aimed at management and conservation. It came into force in
December 2000 and was aimed at attaining in all Member States good ecological status
(Annex V) for all surface waters by 2015. Due to its innovative structure, the WFD focuses
on the quantification of the ecological status of aquatic ecosystems rather than on the external
pressures, the response of the biological components rather than on the physical and chemical
context. The WFD in the Article 5 define that Member States have to characterize their River
Basin Districts by the identification of surface water types and anthropogenic pressures. This
innovative structure has changed the study approach of ecosystems, focusing the main
attention on the role of biological indicators of ecosystem quality. In the WFD there are not
explicit requirements related to monitoring criteria and variable selection on
hydromorphological quality elements, even if these represent an important element to define
system behaviour related to eutrophication. European commission has enhanced
multidisciplinary researches projects in not-European countries. As example, the DGXII
project was finalized to the development and management tools for wetland resources in
Latin America (Loiselle et al., 2001).
The National Estuarine Eutrophication Assessment (NEEA) represents in the USA a tool
to evaluate actual eutrophic conditions and the effectiveness of the management actions
performed by locals to reduce water eutrophication (Bricker et al., 2007). The integrated
methodology for the Assessment of Estuarine Trophic Status (ASSETS) has been applied to
138 estuaries, but it may be comparatively applied to rank the eutrophication status of
estuaries and coastal areas and to address management options. It includes quantitative and
semi-quantitative components and uses field data, models and expert knowledge to provide
Pressure-State-Response (PSR) indicators. ASSETS additionally aims to contribute to the EU
Water Framework Directive classification system, regarding a subset of water quality and
ecological parameters in transitional and coastal waters, including in its model three
diagnostic tools: a heuristic index of pressure (Overall Human Influence), a symptoms-based
evaluation of state (Overall Eutrophic Conditions) and an indicator of management response
(Definition of Future Outlook) (Bricker et al., 2003).
 State of Knowledge of the Trophic State of Worldwide Lagoon Ecosystems: … 267

8.7. ACTUAL PERSPECTIVES: IMPROVE THE KNOWLEDGE

THROUGHOUT SCIENTIFIC RESEARCH

A detailed knowledge of coastal lagoons was overlooked by the scientific community

untill the last twenty years, when an increasing interest towards these ecosystems was
highlighted. The first international event, organized in 1981 by the UNESCO/SCOR
Consultative committee on coastal systems, focused on the need of an improvement of the
scientific researches on these environmnets (Lasserre and Postma, 1982). From this event,
researches focused on transitional waters as confirmed by the rapid increase of published
papers on these observed from 1986 to 2007 (Basset, 2010). The need to define reference
conditions is conceptually questionable since pristine conditions of aquatic ecosystems must
incorporate human society. Coastal ecosystems characterized by the presence of international
networks could represent potential sentinel ecosystems for coastal observations on global
changes (Christian and Mazzilli, 2007).
The assessment of the trophic state in aquatic ecosystems generally includes the
determination of nutrient levels (ammonium, nitrites, nitrates, soluble reactive phosphorous),
the quantification of algal development (chlorophyll a), fluctuations of dissolved oxygen, pH,
levels of organic matter (Newton et al., 2003; Dell‘Anno et al., 2002). The concentration
limit approaches (CLA) defines limits of chemicals, such as nutrients, in waters and
represents an interesting jurisdictional tool due to the relatively easiness to define out layers
and critical sites. Nevertheless, it evidences structural limits related to the definition of
significant pollution and biological effects related to this occurrence. Due to the transitional
water quality paradox described for estuaries by Elliot and Quintino (2007), the definition of
pristine conditions related to eutrophication is difficult. For this reason, techniques developed
for freshwater and coastal areas should be carefully evaluated and tested before being applied
in transitional ecosystems as coastal lagoons (Zaldivar et al., 2008a,b). Palaeoecological
approach using diatoms were developed to reconstruct recent changes of physico-chemical
variables in a water column (such as salinity) and discriminate human impacts over the time
(Saunders et al., 2007). This approach has been successfully applied to evaluate changes of
numerous aquatic environmental variables such as salinity (Gell et al., 2002; Tibby et al.,
2007), pH (Tibby et al., 2003) and nutrients (Weckstròm et al., 2004).
Modelling methods represent a complex but promising strategy to evaluate the
eutrophication risk in lagoon ecosystems. Recent models allow us to estimate the coverage of
lagoons with benthic macrophytes and how sensitive this coverage is to the effective total
nitrogen load per unit area of waterway (Sanderson and Coade, 2010). Furthermore, models
could integrate different self-regulating dynamics in coastal ecosystems linking physico-
chemical and morphological features to biological effects and aim for developing well-sized
management strategies (Pinazo et al., 2004). The major goal is represented by the ability to
link, through evaluation models, potential modifications in wetlands, due to the local
functions, and regional socio-economic context. Useful tools could be represented by the
analysis of energetic fluxes through the trophic web (Loiselle et al., 2001). Recently, some
authors have suggested that approaches based on the life cycle impact assessment (LCIA)
modelization could represent a tool to evaluate the environmental impact derived from human
activities on aquatic ecosystems (Hadj Amor et al., 2008).
268 Monia Renzi, Antonietta Specchiulli, Raffaele D‘Adamo et al.

The increase of knowledge on transitional water environements (lagoons, wetlands and

saltmash systems) needs the development of strategies allowing a rapid diffusion of
significant advances. For this reason, worldwide, a groving number of no-profit scientific
associations are instituted with the aim to promote rapid cultural exchanges among
researchers working on these ecosystems. In Europe among the associations that are actually
working to support and encourage co-operation of research groups are avialable on-line the
international organisation ECSA (Estuarine & Coastal Sciences Association) and the Italian
observational network LaguNet.

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transitional waters: an overview. Transitional Waters Monographs, 1: 1-78.
Zaldivar J.M., Strozzi F., Dueri S., Marinov D., Zbilut J.P. 2008b. Recurrence quantification
analysis as a method for the detection of environmental thresholds. Ecological Modeling,
210: 58-70.
In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 279-300 ©2011 Nova Science Publishers, Inc.

Chapter 9

TREATMENT OF CONTAMINATED SEDIMENTS BY

CHEMICAL OXIDATION

Sabrina Saponaro*1, Alessandro Careghini1, Kevin Gardner≠2 and

Scott Greenwood2
1
Politecnico di Milano, Dipartimento di Ingegneria Idraulica, Ambientale,
Rilevamento, Infrastrutture Viarie – Sezione Ambientale, Milano Italy
2
University of New Hampshire, Environmental Research Group,
Durham, NH (USA)

ABSTRACT
A number of different approaches can be used when managing contaminated
sediments depending on site-specific conditions, sediment characteristics, mix of
contaminants in the sediment and local regulations. Ex situ management options can
include landfill disposal or, more generally, the application of remediation treatments for
beneficial reuse, which may improve the economics of management and/or be required to
meet regulatory requirements.
Chemical oxidation involves the use of chemical additives to remediate sediments
contaminated by organic compounds. Due to electron transfers between two (or more)
compounds, pollutants are degraded into less toxic or biologically available chemical
forms. Chemical oxidation also changes the pH and redox conditions of the treated
system, which may also alter the mobility of the target and other compounds and
elements.
Several different oxidizing agents are available that result in different effectiveness
on different pollutants. The most commonly used oxidants are Fenton-like reagents
(hydrogen peroxide catalyzed by bivalent iron ions), ozone, permanganate, and
persulfate. Recent laboratory studies have also shown good results in peroxy-acid

* Politecnico di Milano, Dipartimento di Ingegneria Idraulica, Ambientale, Rilevamento, Infrastrutture Viarie –

Sezione Ambientale, Piazza Leonardo da Vinci 32 – 20133 Milano (Italy), sabrina.saponaro@polimi.it
≠ University of New Hampshire, Environmental Research Group, Gregg Hall – 03824 Durham, NH (USA),
kevin.gardner@unh.edu
280 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

systems (an organic acid mixed with hydrogen peroxide) to degrade compounds such as
Polycyclic Aromatic Hydrocarbons (PAHs).
Oxidation is a non-selective process. Therefore, the oxidizable material within the
sediment (natural organic matter, detritus, etc.), which may be a significant percentage of
the sediment mass, can consume the oxidizing agent. Moreover, many different reactions
can occur (acid/base reactions, sorption/desorption, dissolution, hydrolysis, ion exchange,
oxidation/reduction, precipitation, etc.). Pollutant removal efficiency strictly depends on
the contamination (pollutants, concentrations) and the sediment being treated (physical-
chemical properties and composition). Laboratory tests are always necessary to evaluate
the feasibility of the treatment to select the best oxidizer and the proper treatment
configuration.
This chapter reports on laboratory batch tests conducted on sediments from Porto
Marghera (Italy) and New York/New Jersey Harbor (NY, USA). Porto Marghera
sediments were treated with Fenton-like reagents to remove total petroleum
hydrocarbons, PAHs, and polychlorinated biphenyls. Different oxidizers (Fenton-like
reagents, persulfate, and peroxy-acid) were used for the New York City sediments
polluted by PAHs. For the latter sediments, the leachability of metals in the treated
sediments and filtration resistance were also assessed to understand potential unintended
consequences of treatment on metal availability and sediment dewatering operations.

INTRODUCTION
A large quantity of sediments is dredged all over the industrialized countries, mainly for
the maintenance of commercial functions of lagoons, harbors, and waterways. In the USA
about 200-300 Mm3 of sediments are dredged every year. About 2.3-4 Mm3 of sediments are
dredged for maintenance purposes in the NY/NJ harbor area [Jones et al., 1998; U.S. EPA
2004; U.S. EPA, 2005; Wargo, 2002]. In Europe, the amount is estimated to be 200 Mm3 a
year, with very different situations among the countries: 0.1 Mm3 in Norway, 28 Mm3 in The
Netherlands, 46 Mm3 in Germany, 56 Mm3 in France [Palumbo, 2007]. In Italy, 6 Mm3 a year
were dredged in the period 1988-1997, but no data are available about the current situation
[Palumbo, 2007].
The final destination of the dredged material is one of the key points in the sediment
management system. Only a small percentage of the volumes mentioned above is
contaminated, but the management can be a serious issue especially for areas with severe
disposal limitations [Dubois et al., 2008; Hamer et al., 2005]. Among the options, there are
relocation in water, when the pollutant concentration is low enough, disposal to landfill, or
treatment to accomplish cleanup goals [Reis et al., 2007; Rulkens, 2005]. Local situations can
be critical; for instance, about 70-80% by weight of the NY/NJ dredged materials can not be
disposed of in the ocean due the high concentrations of organic and inorganic pollutants
[Jones et al., 1998; Wargo, 2002]. In the case of disposal or treatment, pre-treatments are
usually applied to reduce the volume/weight of sediments and/or reduce salinity [Hakstege et
al., 2007; Hamer et al., 2005].
Chemical oxidation involves the use of additives to induce electron transfers between two
(or more) species, theoretically resulting in the degradation of organic pollutants to carbon
dioxide and water. Inorganic pollutants can change their chemical form, also due to changes
in the pH and redox conditions of the system [Reis et al., 2007].
 Treatment of Contaminated Sediments by Chemical Oxidation 281

The chemistry in the oxidative systems is very complex because of the many different
kinds of reactions that can occur (oxidations/reductions, acid/base reactions, hydrolysis,
sorption/desorption, ion exchange, precipitation, etc.). The reaction pathway is strongly
affected by the reactants being used. Moreover, very unstable and reactive radical species can
be produced during the primary oxidation pathway, which in turn induce other oxidative
reactions [Ferrarese et al., 2008; N‘Guessan et al., 2004a].
Common oxidants used in this kind of treatments are Fenton-like reagents (hydrogen
peroxide catalyzed by bivalent iron ions), ozone, permanganate, and persulfate [Ferrarese et
al., 2008; Huling et al., 2006]. Recent studies also report the degradation of polycyclic
aromatic hydrocarbons (PAHs) in peroxy-acid systems (organic acid mixed with hydrogen
peroxide) [Alderman et al., 2007; N‘Guessan et al., 2004b]. The strength of oxidants is
usually expressed by the Oxidation Standard Potential (OSP): the higher its value, the
stronger being the oxidant. Table 1 reports the OSP for the most common oxidants and radical
species. To date, no OSP values are available for peroxy-acids.

Table 1. Oxidation Standard Potential (OSP) for the most common oxidants and radical
species [Huling et al., 2006].

Oxidant OSP (V)

Permanganate (sodium/potassium) 1.7
Hydrogen Peroxide 1.8
Persulfate (sodium) 2.0
Ozone 2.1
Sulfate free radicals 2.6
Hydroxyl radical 2.8

FENTON-LIKE REAGENTS
Hydrogen peroxide (H2O2) is a strong oxidizer. However, when used without a catalyzer,
the decomposition of hydrogen peroxide to water and molecular oxygen tends to be faster
than the oxidation reaction on many common pollutants.
In the classic Fenton‘s treatment, hydrogen peroxide at low concentration is mixed with
bivalent iron ions (Fe2+) in an acidic solution (pH between 2 and 4). Iron ions catalyze the
production of hydroxyl radicals (•OH), hydroxyl ions (OH–) and trivalent iron ions (Fe3+),
according to the starting reaction:

H2O2 + Fe2+  •OH + OH– + Fe3+ (1)

Strong acidic conditions are necessary to enhance the electron transfer between Fe2+ and
H2O2 and keep the iron ions dissolved. This seems the major problem when treating soils and
sediments, due to the large quantity of acid necessary to consume the buffer capacity of the
solid matrix. This, in turn, often results in irreversible damages to the mineral structure of the
matrix being treated [Huling et al., 2006; Suthersan et al., 2005].
In order to overcome these points, different treatments have been developed, based on
Fenton-like reactants (or modified Fenton‘s reactants). One or more of the following options
282 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

are applied: a) hydrogen peroxide is used at high concentrations; b) chelating agents are used
to keep iron dissolved under neutral pH conditions; c) oxides/oxyhydroxides/iron (II or III)
minerals in the solid matrix are used as the catalyzer [Ferrarese et al., 2008; Suthersan et al.,
2005].
When high H2O2 concentrations are used, many other reactions develop besides reaction
(1). These result in the production of additional reactive species, such as hydroperoxide
radical (•HO2), superoxide anion (•O2–), and hydroperoxide anion (HO2–). These radical
forms are very reactive and can degrade most recalcitrant compounds sorbed on the solid
particles. However, excessive oxidant concentrations tend to enhance hydrogen peroxide self-
consumption [Ferrarese et al., 2008; Huling et al., 2006].
Fenton‘s treatments on soils and sediments have proved effective in treating total
petroleum hydrocarbons (TPHs), monoaromatic solvents, methyl tert-butyl ether, tert-butyl
alcohol, PAHs, phenols, chlorophenols, chlorinated ethenes, chlorobenzene, and explosives.
Poor abatements have been obtained on carbon tetrachloride, chloroform, methylene chloride,
and dichloroethanes. Site-specific effectiveness has been reported for trichloroethane,
polychlorinated biphenyls (PCBs), and pesticides [Huling et al., 2006; ITRC, 2005].
Due to their high reactivity and non-specificity, hydroxyl radicals are consumed in
reactions not involving the target pollutants. Therefore, the H2O2 dosage should take into
consideration the amount of radicals reacting with natural organic matter, carbonates, and
bicarbonates [Di Palma, 2005; Flotron et al., 2005; Suthersan et al., 2005].
Fenton‘s reactions are strongly exothermic. The heat developed during the treatment can
enhance pollutant dissolution and volatilization, with potential release in the environment
[Ferrarese et al., 2008; Huling et al., 2006].

OZONE
Ozone is a strong oxidant widely used for both ex situ and in situ applications. It can
oxidize contaminants directly or by the induced hydroxyl radicals, being the prevailing
mechanism dependent on the matrix being treated, and the environmental conditions
(temperature, pH). Radical attack is favored under alkaline conditions [Di Palma, 2005;
Haapea et al., 2006]. Addition of hydrogen peroxide promotes the generation of hydroxyl
radicals [Huling et al., 2006].
Non-halogen substituted olefins, phenols, PAHs, non-protonated amino-compounds, and
thio-compounds can be easily oxidized by ozone directly. Hydroxyl radicals are necessary to
degrade aliphatic hydrocarbons, trichloroethene, tetrachloroethene, benzene, chlorobenzene,
and PCBs. Ozone can rapidly react with both electron-rich olefins and aromatic compounds.
With olefins, the reaction rate decreases as the number of chloride substitutions increases.
With aromatic compounds, the reaction rate increases as the number of functional groups
increases [Cassidiy et al., 2002; O‘Mahony et al., 2006].
Ozone has a short retention time in the environment, as it reacts with a wide range of
naturally-occurring substances [Huling et al., 2006; Rivas, 2006].
 Treatment of Contaminated Sediments by Chemical Oxidation 283

PERMANGANATE
Permanganate salts (usually potassium or sodium permanganate) in an aqueous system
generate permanganate ions MnO4–. Equation (2) shows the reaction occurring at pH values
between 3.5 and 12:

MnO4– + 2 H2O + 3e–  MnO2 (s) + 4 OH– (2)

MnO4– ions do not generate radical species and oxidize pollutants by direct electron
transfer. Compared to Fenton‘s systems, permanganate has slower reaction rates and persists
in the environment longer, which can be an advantage for in situ applications [Huling et al.,
2006].
Despite the relatively low OSP value, permanganate has proved effective on a wide range
of organic compounds, including molecules with carbon-carbon bounds, aldehyde groups or
hydroxyl groups. It is recommended for in-situ and ex-situ applications for many petroleum
hydrocarbons. Some pollutants, such as 1,1,1-trichloroethane, 1,1-dichloroethane, carbon
tetrachloride, chloroform, methylene chloride, chlorobenzene, benzene, some pesticides, and
PCBs, seem to be recalcitrant to degradation with permanganate [Dash et al., 2009; Huling et
al., 2006, Ferrarese et al., 2008].
A wide range of natural compounds (above all, natural organic matter and reduced
chemical species) can react with MnO4–, resulting in a high oxidant demand. Metal oxidation
can increase their leachability, and this is the case of chromium and nickel [Al et al., 2006;
Huling et al., 2006].
The reaction product MnO2 is poorly soluble in the pH range 3.5-12. Its deposition on the
solid matrix can negatively affect pollutant removal efficiency due to mass transfer
limitations. However, MnO2(s) behaves as a sorbent for many heavy metals (Cd, Co, Cr, Cu,
Ni, Pb, Zn), especially at high pH values. Moreover, it has the role of primary electron
acceptor in the oxidation of As(III) to the less soluble As(V) [Huling et al., 2006].

PERSULFATE
Persulfate salts dissociate in aqueous solution to create persulfate anion S2O8–, which is a
strong oxidant. Persulfate anion, in turn, can produce the sulphate radical •SO4–, more
powerful than S2O8– itself and the hydroxyl radical. The production of •SO4– can be achieved
by "activating" the system as follows: i) heating to temperatures of about 35-40 °C; ii) adding
transition metal ions (such as bivalent iron ions); iii) by UV irradiation; iv) rising the pH
value above 10; v) by H2O2 [Ferrarese et al., 2008; Huling et al., 2006; Liang et al., 2008].
Equation (3) shows the chemical activation reaction based on Fe2+:

S2O8– + Fe2+  Fe3+ + •SO4– + SO42– (3)

Persulfate is effective on a wide range of organic contaminants, including mono- and

poly-aromatic compounds [Cuypers et al., 2000].
284 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

Beside reactions with the target contaminants, sulphate radicals react with a wide range
of species in the sediment. An excessive use of activating Fe2+ results in unwanted
consumption of the oxidant as well. Usually, the amount of persulfate dosed in the treatments
widely exceeds the stoichiometric requirements [Huling et al., 2006; Liang et al., 2008].

PEROXY-ACIDS
A peroxy-acid system is based on using hydrogen peroxide and an organic acid to
produce a peroxy-acid compound. This can react directly with the organic pollutants, or
produce hydroxyl cations that in turn react with the pollutants [N‘Gussan et al., 2004b]. In
N‘Gusussan et al. [2004a], the acetic acid was used to induce a cyclical catalytic process, as
shown in Figure 1.

Figure 1. Peroxy-acid cyclical catalytic process obtained with acetic acid [modified from N‘Guessan et
al., 2004a].

Peroxy-acids are relatively selective oxidizing agents. They act on aromatic rings, double
and triple bonds, whereas they do not react in unwanted competing reactions with molecules
such as sugars [N‘Guessan et al., 2004b]. On the other hand, the additions of large amounts of
acetic acid to sediments have significant environmental implications, in particular due to the
drastic decrease of the system pH [N‘Guessan et al., 2004a].
Peroxy-acid oxidation is a well-known technology in pulping industry. Its use for the
remediation of contaminated soils and sediments is a recent application [Ciotti et al., 2008;
Levitt et al., 2003]. In literature, some works are reported on the use of peroxy-acid systems
for the degradation of PAHs, but information is not available yet about the effectiveness on
other organic pollutants. In N‘Guessan et al. [2004b], α-methylnaphthalene and
benzo[a]pyrene on artificially contaminated sediments were degraded at laboratory scale with
acetic acid or propionic acid in peroxy-acid systems. Although the reaction rates with the
 Treatment of Contaminated Sediments by Chemical Oxidation 285

propionic acid were faster than with the acetic acid, the latter provided a higher removal
efficiency of the target pollutants. Alderman et al. [2007] used a PAH-contaminated soil from
a U.S. Superfund site to evaluate the effectiveness of peroxy-acid oxidation at lab scale. No
significant difference was found in the removal rate of low and high molecular weight PAHs.
Ciotti et al. [2008] carried out laboratory tests using different acetic acid to hydrogen
peroxide mole ratios on two sediments spiked with anthracene and pyrene. The highest
removal efficiency (>95% in 24 hours) was reached with an acetic acid to H2O2 mole ratio of
3.

CASE STUDIES
The oxidizers mentioned above show different effectiveness in treating sediments,
according to the pollutants, the sediment and the environmental conditions involved.
Experimental tests are recommended to assess site-specific feasibility of chemical oxidation
and to select the most appropriate treatment conditions [Huling et al., 2006; Rivas, 2006].
Two case studies are discussed in this chapter, for which chemical oxidation was tested at
lab scale on polluted sediments from Porto Marghera (Venice, Italy) and New York/New
Jersey Harbor (NY, USA). In the first case, Fenton-like reagents were used to treat total
petroleum hydrocarbons (TPHs), PAHs, and PCBs. In the second case, different oxidizers
(Fenton-like reagents, chemically activated persulfate, and peroxy-acid) were tested on
sediments with high PAH concentrations, also assessing under selected conditions changes in
metal leachability and Specific Resistance to Filtration (SRF) of the treated sediments.

MATERIALS AND METHODS

Sediments

Porto Marghera Sediments

Located next to Venice lagoon, Porto Marghera is one of the most important
industrial/commercial harbors in Italy. From the 1950s to 1980s, many chemical and
petrochemical industries have settled at the site, but after this period, the recognition of
human health hazards due to pollution brought to the progressive reduction of industrial
activities. In 1993, a protocol was signed by the local authorities and the Italian
Environmental Ministry, establishing specific limit values for the sediments dredged in the
lagoon. According to this protocol, the final destination of the dredged sediments must take
into account pollutant concentrations. In 1998, Porto Marghera was recognized as a National
Priority Site (NPS) by the Italian Law n° 426. An official agreement was signed between
different public institutions and private companies to remediate the site [Carlon et al., 2005].
The sediments used for this study were dredged in the Northern canal. To ensure the
stability of their physical-chemical properties over the duration of the research program (2
years), after dredging the material has been air-dried for 72 hours, sieved to less than 4 mm to
remove wood and shells, homogenized, and stored under controlled conditions.
286 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

The sediment was composed of sand (39  2 % w./w.) and particles <63 μm (61  3 %
w./w.); particles <45 μm accounted for more than 50% on weight basis. The residual moisture
was 2.8 %  0.3 w./d.w. The organic carbon content was 2.0  0.2 w./d.w. pH was 8.6  0.3.
As far as the elemental composition is concerned, the sediment contained about 15% Si, 12%
Ca, 4.5% Al, 3.5% Mg and Fe, about 2% Na and K, and 1% Cl. Pollutant concentrations are
reported in Table 2, and compared to the concentration limits in the Venice protocol. Light
PAHs (2- to 3- aromatic ring PAHs) and heavy PAHs (4- to 6- aromatic ring PAHs) were
approximately 8.0% and 92% (on weight basis) of total PAHs. Table 3 reports the
concentrations of selected PCB congeners.

Table 2. Pollutants measured in Porto Marghera sediments and classification based on

Venice protocol. “Light PAHs” refers to the 2- and 3- aromatic ring PAHs, “heavy
PAHs” refers to 4- to 6- aromatic ring PAHs.

Venice protocol limits

Pollutant Unit Measured value Classification
A B C
As mg/kg d.w. 23 ± 2 15 25 50 B
Cd mg/kg d.w. 6.0 ± 0.6 1 5 20 C
Cr (total) mg/kg d.w. 661 ± 186 20 100 500 Above C
Cu mg/kg d.w. 101 ± 31 40 50 400 C
Pb mg/kg d.w. 144 ± 13 45 100 500 C
Zn mg/kg d.w. 826 ± 28 200 400 3000 C
TPHs mg/kg d.w. 213 ± 38 30 500 4000 B
PAHs (total) mg/kg d.w. 90 ± 5 1 10 20 Above C
Light PAHs mg/kg d.w. 7.0 ± 1.5 - - - -
Heavy PAHs mg/kg d.w. 83 ± 5 - - - -
PCBs (total) μg/kg d.w. 202 ± 98 10 200 2000 C

Table3. PCB congeners measured in Porto Marghera sediments.

Congener IUPAC Name Value (μg/kg d.w.)

BZ-8 2,4‘-dichlorobiphenyl 10.1 ± 3.9
BZ-18 2,2‘,5-trichlorobiphenyl 11.3 ± 4.8
BZ-28 2,4,4‘-trichlorobiphenyl 2.8 ± 1.0
BZ-52 2,2‘,5,5‘-tetrachlorobiphenyl 3.7 ± 1.4
BZ-101 2,2‘,4,5,5‘ -pentachlorobiphenyl 6.8 ± 2.6
BZ-81 3,4,4‘,5-tetrachlorobiphenyl 11.6 ± 1.4
BZ-77 3,3‘,4,4‘-tetrachlorobiphenyl 9.4 ± 5.9
BZ-123 2,3‘,4,4‘,5‘ -pentachlorobiphenyl 13.2 ± 3.3
BZ-118 2,3‘,4,4‘,5 -pentachlorobiphenyl 7.0 ± 2.4
BZ-114 2,3,4,4‘,5 -pentachlorobiphenyl 9.0 ± 3.5
BZ-105 2,3,3‘,4,4‘-pentachlorobiphenyl 1.8 ± 0.2
BZ-138 2,2‘,3,,4,4‘,5‘-hexachlorobiphenyl 9.9 ± 4.4
BZ-126 3,3‘,4,4‘,5-pentachlorobiphenyl 9.4 ± 2.8
BZ-167 2,3‘,4,4‘,5,5‘-hexachlorobiphenyl 2.4 ± 0.3
BZ-156 2,3,3‘,4,4‘,5-hexachlorobiphenyl 1.7 ± 0.2
BZ-157 2,3,3‘,4,4‘,5‘-hexachlorobiphenyl 1.7 ± 0.3
BZ-180 2,2‘,3,4,4‘,5,5‘-heptachlorobiphenyl 8.7 ± 4.3
BZ-169 3,3‘,4,4‘,5,5‘-hexachlorobiphenyl 2.3 ± 1.5
BZ-198 2,2‘,3,3‘,4,5,5‘,6-octachlorobiphenyl 1.6 ± 0.0
BZ-189 2,3,3‘,4,4‘,5,5‘-heptachlorobiphenyl 1.6 ± 0.0
BZ-206 2,2‘,3,3‘,4,4‘,5,5‘,6-nonachlorobiphenyl 2.3 ± 0.7
BZ-209 Decachlorobiphenyl 9.4 ± 2.7
 Treatment of Contaminated Sediments by Chemical Oxidation 287

Gowanus Canal Sediments

Located in Kings County (Brooklyn), New York City (NY, USA), Gowanus canal is an
industrial waterway constructed in the mid-19th century. Its banks became the site of intensive
industrial activities (such as refining, coal gasification, soap making and tanning). Today
many of these industrial activities have ceased, but sediments remain contaminated by
inorganic and organic pollutants. In particular, PAHs are a critical group of contaminants. The
canal area remains densely populated and community pressure is providing an impetus for
remediation and redevelopment [U.S. ACE, 2004].
The sediments were dredged, mixed and characterized. The pre-treatment described for
Porto Marghera sediments was not applied in this case, as the duration of the study was
shorter (6 months).
The sediment was composed of sand (79  4 % w./w.), a small amount of silt (17.0  0.9
% w./w.), and a negligible amount of clay (2.5  0.1 % w./w.). The moisture content was 55 
2 % w./w. The organic carbon content was 6.1  0.4 % w./w. Iron content was 2.2  0.8 %
w./w. pH was 7.9  0.2. The SRF value was 3.1 ( 0.4) · 1012 m/kg; according to the
literature, this value suggests a medium to high filterability of the sludge [Guangwei et al.,
2009]. Table 4 reports pollutant concentrations measured in the sediment and two classes of
values reported in the National Oceanic and Atmospheric Administration Screening Quick
Reference Tables (NOAA SQuiRTs) for marine sediments [Buchman, 2008]. Sediments were
heavily polluted by PAHs; light PAHs and heavy PAHs were 39% and 61% (on weight basis)
of total PAHs respectively. Cd, Cu, Pb, and Zn concentrations were high based on the
screening values in the NOAA tables.

Table 4. Concentration measured in Gowanus canal sediments. Probable Effect Level

(PEL) and Effect Range Median (ERM) values reported in NOAA SQuiRT (National
Oceanic and Atmospheric Administration Screening Quick Reference Tables) are also
shown. “Light PAHs” refers to the 2- and 3- aromatic ring PAHs, “heavy PAHs” refers
to 4- to 6- aromatic ring PAHs.

Pollutant Value NOAA SQuiRT – Marine Sediments

(mg/kg d.w.) (mg/kg d.w.)
PEL ERM
As 8.8 ± 1.3 41.6 70
Cd 8.4 ± 1.4 4.2 9.6
Cr (total) 91 ± 14 160.0 370
Cu 218 ± 25 108.0 270
Pb 346 ± 35 112.0 218
Zn 473 ± 55 271 410
PAHs (total) 1340 ± 265 16.7 44.8
Light PAHs 525 ± 120 1.4 3.2
Heavy PAHs 815 ± 140 6.7 9.6
288 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

Oxidation Tests

Porto Marghera Sediments

For Porto Marghera sediments, Fenton-like reagents were selected for the oxidation
treatment. Each test was carried out in batch, using 5 g d.w. of sediment and a Liquid to Solid
ratio (L/S) of 10: v./w. Different suspending solutions were prepared by mixing:

 deionized water or tap water;

 a commercial solution of hydrogen peroxide;
 ferrous sulphate (FeSO4) as the Fe2+ supplier;
 acidifying agents and buffer solutions: hydrochloric acid (37 % by volume) and
acetic acid (1 M), or phosphoric acid (0.4 % by volume), or acetic acid (1 M).

Table 5 summarizes the experimental conditions; each condition was tested at least in
duplicate. Tests duration varied from 2 to 24 hours. The test designated K* (see Table 5) was
carried out in two steps with different duration (6 h and 18 h respectively): hydrogen peroxide
and phosphoric acid were added in the first one, whereas FeSO4 was added in the second one.
Tests were done in 200 ml glass vessels, sealed with a PTFE-covered gasket. During the
test duration, mixing was ensured by a horizontal-axis shaking table (Tecnovetro, I) operating
at 200 oscillations per minute. At the end, samples were centrifuged at 2000 rpm to separate
solids from the liquid phase. The liquid phase was filtered (0.45 μm) and used to measure
residual hydrogen peroxide, dissolved Fe2+ and Fe3+, and pH. Measurements of organic
pollutants in the liquid phase were occasionally carried out, resulting in a negligible
contribution to the pollutant mass balance. Based on the residual hydrogen peroxide measured
in the liquid phase, sodium sulphite was added stoichiometrically to stop the oxidation
reactions in the solid phase. Then the solid phase was analyzed to quantify TPHs, PAHs and
PCBs.

Table 5. Oxidation tests carried out on Porto Marghera sediments (5 g d.w. sediment,
L/S = 10:1 v./w.)

H2O2 Fe2+ added

(1) Duration HCl + CH3COOH H3PO4 CH3COOH
Test (mmol H2O2/ (mmol Fe2+/
(h) (ml) (ml) (ml)
g d.w. sed.) mmol H2O2)
A and A* 2 16.2 2.4 + 2
B 24 16.2
C 24 16.2 1:990
D 24 16.2 1:123
E 24 32.4
F and F* 24 32.4 1:966
G* 6 and 24 16.2 20
H* 6 and 24 16.2 10
I* 6 and 24 16.2 0.3 + 20
K* 6 / 18 16.2 / 2.74 - / 1:96 20 / -
(1) * indicates that the test was performed with tap water instead of deionized water.
 Treatment of Contaminated Sediments by Chemical Oxidation 289

Gowanus Canal Sediments

Three different kinds of oxidizer were selected for Gowanus canal sediments: Fenton-like
reagents (FEN tests), persulfate (SUL tests), and peroxy-acid (ACI tests). Tests were carried
out in batch, using 5 g d.w. sediment and the L/S reported in Table 6. Different suspending
solutions were prepared by mixing:

 deionized water;
 a commercial solution of hydrogen peroxide for Fenton-like and peroxy-acid tests;
 Na2S2O8 as the oxidant in persulfate tests;
 FeSO4 as the Fe2+ supplier for Fenton-like and persulfate tests;
 acetic acid for peroxy-acid tests,

dosed according to Table 6. The duration of each test was 24 h. Each configuration was
carried out at least in duplicate.

Tests were done in 200 ml glass flasks without cap. Mixing was ensured by a shaking
platform (Innova, NJ-USA) operating at 180 rpm. At the end, samples were centrifuged at
2000 rpm to separate solids from the liquid phase. The liquid phase was filtered (0.45 μm)
before acid digestion for metal analyses. In order to measure the PAH concentration on the
sediment after treatment, the solid material on the filter was joined to the centrifuged solid
phase and quenched with sodium sulphite; the quantity of sodium sulphite was calculated
stoichiometrically on the amount of oxidizer added in the test. Some solid samples, which
were not quenched, were used for SRF measurements, according to the Buchner Funnel test
described in U.S. EPA [1987].

Table 6. Oxidation tests on Gowanus canal sediments.

Test L/S (ml/g d.w. sed) Oxidizer (mmol oxid./ g d.w. sed.) Fe2+ added (mmol Fe2+/ mmol oxid.)
FEN-1 1.7 6.7 -
FEN-2 1.9 6.7 1:50
FEN-3 1.7 3.3 -
FEN-4 1.9 3.3 1:50
FEN-5 5.0 3.3 -
FEN-6 5.0 3.3 1:50
SUL-1 5.0 6.7 1:25
SUL-2 5.0 3.3 1:25
ACI-1 3.7 15.7 H2O2 + 15.7 CH3COOH -
ACI-2 3.7 10.5 H2O2 + 15.7 CH3COOH -
ACI-3 5.0 10.5 H2O2 + 15.7 CH3COOH -

Chemicals and Analytical Methods

All chemicals were reagent-grade commercial products.

Particle size distribution of sediments was measured according to ASTM D422 – 63
[ASTM, 2008]. Sediment pH was measured according to ISO 10390 [ISO, 2005]. The
290 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

Buchner Funnel test described in U.S. EPA [1987] was carried out operating at 64 kPa for 40
min. Organic carbon content was assessed through loss on ignition at 550°C [EN, 2007].
The following chemical methods were used for Porto Marghera sediments: i) EPA 3541
for the extraction of organics [U.S. EPA, 2007]; ii) EPA 3630C for clean-up [U.S. EPA,
2007]; iii) EN 14039 by GC/MS (CV: 20%) for TPHs [EN, 2004]; iv) EPA 8260 B by
GC/MS (CV: 20%) for PAHs [U.S. EPA, 2007]; v) EN 12766-1 by GC/ECD for PCBs [EN,
2000]. Inorganics were measured by X-ray spectrophotometry (internal method). Hydrogen
peroxide concentration was measured by spectrophotometry using the Lange LCW 058 kit.
The concentration of dissolved iron was spectrophotometrically measured according to ISO
6332 [ISO, 1988].
The following chemical methods were used on Gowanus canal sediments: i) EPA 3545A
for the extraction of PAHs [U.S. EPA, 2007]; ii) EPA 3630C for clean-up [U.S. EPA, 2007];
iii) EPA 8260 B by GC/MS (CV: 20%) for PAHs [U.S. EPA, 2007]. Inorganics were
measured by microwave oven acid digestion (EPA 3051 A [U.S. EPA, 2007] and ICP
analyses by EPA 6010C [U.S. EPA, 2007].

RESULTS AND DISCUSSION

Porto Marghera Sediments
Table 7 reports the measured concentrations of H2O2, Fe(II) and Fe(III) in the aqueous
phase normalized to the slurry weight and the pH values at the beginning and at the end of the
tests. In G*, H*, I* and K*, results obtained after 6 hours of treatment are also reported in
parentheses. Hydrogen peroxide was completely consumed in most 24 hour-tests; residual
concentrations of H2O2 were measured only where phosphoric acid was added (G* and K*)
due to its stabilizing effect on hydrogen peroxide [Charlot, 1977]. A limited consumption of
hydrogen peroxide was achieved after 2 or 6 hours of treatment.

Table 7. H2O2, Fe(II) and Fe(III) in the aqueous phase and pH values. For K*, results in
parentheses refer to 6 hours of treatment.

H2O2 Fe(II) Fe(III)

pH
Test (% w. H2O2/ w. slurry) (% w. Fe2+/ w. slurry) (% w. Fe3+/ w. slurry)
start end start end start end start end
A 5 3.7 3.9E-4 7.7E-4 3.6E-4 2.2E-4 3.6 3.7
A* 5 2.5 4.6E-4 3.5E-4 3.9E-4 1.4E-4 3.6 3.5
B 5 <0.09 1.8E-5 7.3E-6 7.5E-6 2.5E-6 7.1 7.7
C 5 <0.09 1.2E-3 4.6E-6 4.0E-5 4.9E-6 7.0 8.0
D 5 <0.09 6.7E-3 2.2E-5 5.8E-4 1.0E-6 6.8 7.8
E 10 <0.09 1.1E-5 5.1E-6 2.0E-5 3.6E-6 7.1 7.9
F 10 <0.09 4.7E-3 7.6E-6 2.2E-5 7.9E-6 6.5 8.0
F* 10 0.5 1.1E-7 5.3E-6 2.2E-5 2.5E-6 6.5 7.6
G* 5 (3.9) 1.2E-7 (2.6E-7) 1.6E-7 (3.1E-8) 5.0 (4.9)
2.5 3.1E-7 4.7E-8 4.6
H* 5 (1.5) 2.0E-6 (2.5E-7) 3.1E-8 (<1.0E-9) 5.0 (5.8)
<0.09 1.1E-7 4.7E-8 7.7
I* 5 (0.8) 1.1E-6 (5.0E-7) 4.7E-8 (<1.0E-9) 5.0 (5.9)
<0.09 1.8E-7 6.2E-8 7.2
K* 5 (3.9) 1.2E-7 (2.6E-7) 1.6E-7 (3.1E-8) 5.0 (4.9)
2.1 2.2E-7 <1.0E-9 4.7
 Treatment of Contaminated Sediments by Chemical Oxidation 291

Fe(II) dissolved concentration at the beginning of the treatments without acidification

(tests B to F* in Table 7) was high where FeSO4 and deionized water had been added (C, D,
and F). Comparison between F (deionized water) and F* (tap water) suggests that tap water
negatively affected FeSO4 dissolution. This could be related to the presence of major species
in tap water (22 mg NO3−/l, 65 mg SO42−/l, 284 mg CaCO3/l) interfering with the dissolution
kinetics and chemical equilibria in the slurry system [Greenberg et al. 1992]. In C, D and F,
Fe(II) dissolved concentration at the end of tests was about three orders of magnitude lower
than the starting value and similar to the ending value in F*.
The pH values were quite stable during the treatments, but in H* and I* the pH increased
more than 2 units at the end of the treatment, with stable values within the first six hours.
Figure 2 shows the TPH concentration measured in the sediment after the oxidation
treatments. The removal efficiency was high (>80%) for all the configurations tested. The
highest abatement (95%) was achieved in G*. Treatments A*, G*, H* and I* were effective
in downgrading the classification of the sediment (from class B to class A) for TPHs.
Total PAH concentrations are shown in Figure 3. The highest abatement (50%) was
achieved in A*. A 40% removal efficiency was reached in H*, whereas no significant
removals were observed in the other tests. No treatments were able to downgrade the
classification of the sediment for total PAHs. Figure 4 shows results for light and heavy
PAHs. Abatements between 34 and 45% were obtained A*, F, K* and I* for light PAHs. For
heavy PAHs, the highest removal efficiencies were achieved in A* (50%) and H* (35%).
According to these results, treatment A* exhibited the highest effectiveness for PAHs.
Total PCBs in the sediment after the oxidation treatments are shown in Figure 5. No
significant differences between SED and the treated samples was observed due to the high
standard deviation in results. However, in terms of average value, tests A*, F* and G*
resulted in the lowest residual concentration. The highest removal efficiencies (>99%) were
achieved in A* for BZ-77, BZ-123, BZ-105, BZ-126, BZ-198, BZ-189, BZ-206, and BZ-209,
and in A for BZ-198, BZ-189, BZ-206, and BZ-209. BZ-8 congener concentration increased
in all the configurations tested; moreover, PCB chromatograms of the treated samples
indicated the presence of unidentified non-PCB chlorinated by-products. These results might
be related to free-radical chlorination of alkanes or alkyl-substituted aromatics, as reported in
Manion [2000] and Poerschmann et al. [2009]. Actually, the lagoon sediment contains free
chlorine atoms and alkanes, and the presence of non-investigated compounds such as phenols,
chlorophenols or biphenyl cannot be excluded.
In general, tests with tap water resulted in higher removal efficiencies than with
deionized water. This might be related to a slower kinetics of iron dissolution, in turn
reducing hydroxyl radical scavenging [Watts et al. 1996]. Fe(II) additions did not
significantly modify the pollutant removal efficiencies. Time was not a key factor, as no
significant difference in the residual pollutant concentration was measured after 6 and 24
hours of treatment in G*, H* and I*. The best results were obtained in A*, in spite of the short
contact time (2 h). This test was characterized by strong acidic conditions, which could have
heavily modified the solid matrix. The production of unidentified by-products seems to be a
critical point in the oxidation treatments, due to their potential toxicity and/or bioavailability.
292 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

250

200

mg/kg d.w.
150

100

50

0
A* A B C D E F* F G* H* I* K* SED

Figure 2. TPH concentration after oxidation treatments compared to the untreated sample (SED). The
horizontal line represents the limit for "class A" sediments according to the Venice protocol. Results for
G*, H*, and I* are reported as the mean value after 6 and 24 h, as no significant differences were
observed in the values.

140

120

100
mg/kg d.w.

80

60

40

20

0
A* A B C D E F* F G* H* I* K* SED

Figure 3. Total PAH concentration after oxidation treatments compared to the untreated sample (SED).
The horizontal line represents the limit for "class C" sediments according to the Venice protocol.
Results for G*, H*, and I* are reported as the mean value after 6 and 24 h, as no significant differences
were observed in the values.

Light PAHs Heavy PAHs

120

100

80
mg/kg d.w.

60

40

20

0
A* A B C D E F* F G* H* I* K* SED

Figure 4. Light PAH (2- to 3- aromatic rings) and heavy PAH (4- to 6- aromatic rings) concentrations
after oxidation treatments compared to the untreated sample (SED). Results for G*, H*, and I* are
reported as the mean value after 6 and 24 h, as no significant differences were observed in the values.
 Treatment of Contaminated Sediments by Chemical Oxidation 293

Figure 5. Total PCB concentrations after oxidation treatments compared to the untreated sample (SED).
The horizontal line represents the limit for "class B" sediments according to the Venice protocol.
Results for G*, H*, and I* are reported as the mean value after 6 and 24 h, as no significant differences
were observed in the values.

Gowanus Canal Sediments

Figure 6 shows the concentration of total PAHs measured after oxidation compared to the
untreated sediment (SED). A significant removal was achieved in all tests. In terms of
average abatement, the highest value (54%) was achieved in ACI-1, where the highest
amount of oxidizer was used. This trend was observed also in FEN tests (FEN-1 vs. FEN-3
and FEN-5; FEN-2 vs. FEN-4 and FEN-6), but not in SUL tests. In Fenton-like treatments,
the addition of Fe(II) improved the average abatement of total PAHs (FEN-1 vs. FEN-2,
FEN-3 vs. FEN-4, FEN-5 vs. FEN-6). The liquid to solid ratio did not affect the total PAH
removal in any of the systems in which this factor was investigated (FEN-3 vs. FEN-5, FEN-
4 vs. FEN-6; ACI-2 vs. ACI-3).

1600
1400
1200
mg/kg d.w.

1000
800
600
400
200
0
FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED

Figure 6. Concentration of total PAHs at the end of the oxidation tests and in the sediment.

The concentration of light and heavy PAHs is shown in Figure 7. In general, the lowest
residual concentrations of light PAHs were observed for the treatments in which the highest
amount of oxidizer was used (FEN-1, FEN-2, and ACI-1). No significant difference could be
294 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

pointed out in the residual concentration of light PAHs for the different liquid to solid ratios
applied (FEN-3 vs. FEN-5, FEN-4 vs. FEN-6; ACI-2 vs. ACI-3). On the contrary, the
residual concentration of heavy PAHs was not significantly affected by the oxidant dosage
(FEN-1 vs. FEN-3 and FEN-5; FEN-2 vs. FEN-4 and FEN-6; SUL-1 vs. SUL-2; ACI-1 vs.
ACI-2 and ACI-3). Peroxy-acid was the most effective oxidant on heavy PAHs. As reported
in Valderrama et al. [2009], light PAHs were better removed than heavy PAHs in all Fenton-
like reagent tests and persulfate.
Chemical oxidation effectiveness strongly depends on the matrix and the experimental
set-up; difference in results between this study and the literature can be ascribed to these
factors. The experimental removal efficiencies for Fenton-like reagents and persulfate for
Gowanus canal sediment were lower than in Ferrarese et al. [2008], in which the best
remediation performance was reported for an oxidant dosage of about 100 mmols for 30 g of
sediment. However, the organic carbon in the sediment of Ferrarese et al. [2008] was 190
mg/kg d.w., more than two orders of magnitude lower than in Porto Marghera and Gowanus
canal sediments. The abatement in peroxy-acid tests in the present study was close to that
reported in Alderman et al. [2007] for the experiment on Bedford LT soil with ratios of
hydrogen peroxide to acetic acid and water similar to those used in the present study. The
high organic content in the Bedford LT soil (up to three times higher than in the sediment
used in the present study) is supposed not to have negatively affected the treatment due to the
peroxy-acid selectivity. Anyhow, the measured removal efficiencies for PAHs in this study
were consistent with those reported for matrices that were not artificially spiked with
contaminant in the laboratory [Brown et al., 2009; Jonsson et al., 2007; Vanderrama et al.,
2009].

Light PAHs Heavy PAHs

1050
900
750
mg/kg d.w.

600
450
300
150
0
FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED

Figure 7. Light (2- to 3- aromatic rings) and heavy (4- to 6- aromatic rings) PAHs after oxidation
compared to the untreated sediment.

Figure 8 and 9 show metals dissolved in the liquid phase and the pH values after filtration
for some selected tests. Negligible quantities of metals were recovered in the liquid phase for
Fenton-like tests, except for cadmium in FEN-4 and FEN-6. On the contrary, sediments
treated with persulfate and peroxy-acid showed a high amount of metals in the liquid phase,
suggesting increase in their leachability. Changes in metal speciation could occur due to pH
and redox variations compared to the untreated sediment and from addition or organic
compounds that complex metals; in fact, ACI and SUL tests had the lowest pH values at the
 Treatment of Contaminated Sediments by Chemical Oxidation 295

end of treatment. Oxidation of sulphide-metal species may also contribute to mobilize

inorganic pollutants [Di Palma, 2005; Sparrevik et al., 2009]. Moreover, organic-based
structures in the sediment might degrade when these two oxidants are used, resulting in metal
release and dissolved complexing agent formation. These results underline the need of proper
control (and treatment before discharge) of the liquid phase at full-scale application. They
also underline the potential risk associated with different metal species in the treated
sediments, for either leachability or toxicity [Martin et al., 1998].

100
As 100
Cd

% (w./w.) in liquid phase

% (w./w.) in liquid phase

90 90
80 80
70 70
60 60
50 50
40 40
30 30
20 20
10 10
0 0
FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED

100
Cr (tot) 100
Cu
% (w./w.) in liquid phase

% (w./w.) in liquid phase

90 90
80 80
70 70
60 60
50 50
40 40
30 30
20 20
10 10
0 0
FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED

100
Pb 100
Zn
% (w./w.) in liquid phase

% (w./w.) in liquid phase

90 90
80 80
70 70
60 60
50 50
40 40
30 30
20 20
10 10
0 0
FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED FEN-1 FEN-2 FEN-3 FEN-4 FEN-5 FEN-6 SUL-1 SUL-2 ACI-1 ACI-2 ACI-3 SED

Figure 8. Metals in the liquid phase. Percentage is referred to the amount of metal in the untreated
sediment.

7
6

5
pH

3
2

0
FEN-1 FEN-2 FEN-3 FEN-4 SUL-1 SUL-2 ACI-1 ACI-2 SED

Figure 9. pH values measured in the liquid phase after filtration.

296 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

Figure 10 shows the SRF values measured in selected tests and Figure 11 shows the
residual moisture in the oxidized sediment after the filtration test. Results indicate that the
different oxidation treatments did not significantly change the SRF value compared to the
filtered untreated sediment. Significant decreases of residual moisture were measured in FEN-
3, SUL-1 and ACI-1 tests compared to the filtered untreated sediment, but these changes
seem too low for practical interest.

1.00E+13
SRF (m/kg)

1.00E+12

1.00E+11

1.00E+10
FEN-1 FEN-2 FEN-3 FEN-4 SUL-1 SUL-2 ACI-1 ACI-2 SED

Figure 10. SRF values by filtration tests.

40
Moisure content (% w./w.)

35
30
25
20
15
10
5
0
FEN-1 FEN-2 FEN-3 FEN-4 SUL-1 SUL-2 ACI-1 ACI-2 SED

Figure 11. Residual moisture after filtration tests.

Comparison Between the Two Sediments

Comparison between results obtained with the two sediments investigated is hard, due to
the differences in terms of sediment physical-chemical properties, contamination, and
pollutant concentrations, as well as not completely homogeneous test conditions. Tests B and
D on Porto Marghera sediments, and FEN-1 and FEN-2 on Gowanus canal sediments are the
most similar in treatment conditions. Comparison is reported in Table 8.
 Treatment of Contaminated Sediments by Chemical Oxidation 297

Table 8. PAH results for tests B and D on Porto Marghera sediments and tests FEN-1
and FEN-2 on Gowanus canal sediments.

Total PAHs Total PAH Light PAHs Light PAH Heavy PAHs Heavy PAH
Tests (mg/kg d.w.) removal (mg/kg d.w.) removal (mg/kg d.w.) removal
(%) (%) (%)
Start End Start End Start End
B 90 67 26 7 6.3 10 83 61 27
D 90 97 0 7 9.6 0 83 88 0
FEN-1 1340 898 33 523 212 59 816 687 16
FEN-2 1340 718 46 523 119 77 816 599 27

Based on total PAH removal efficiency, oxidation was more effective on Gowanus canal
sediment, despite of the lower amount of oxidizer added (6.7 mmol H2O2/g d.w. Gowanus
canal sediment, compared to 16.2 mmol H2O2/g d.w. Porto Marghera sediment). The presence
of many different oxidizable chemical species in Porto Marghera sediments has probably
limited the efficiency towards PAHs. The removal trend of light PAHs agrees with that of
total PAHs. For heavy PAHs, the removal efficiency was higher in test B than in FEN-1, and
as equal as in FEN-2. Iron addition improved PAH removal in Gowanus canal tests, but had
no effect for Porto Marghera sediments; the lower iron content in the Gowanus canal
sediment or different iron species in the sediments could explain this behavior. In addition,
the Gowanus canal sediments had significantly higher total PAH concentrations; availability
of PAH in easily exchangeable form may be a prerequisite to effective oxidation and excess
PAH (i.e. not tightly bound in the sediment matrix) may yield higher degradation in general.

CONCLUSION
Chemical oxidation tests resulted in some positive results, but also highlighted some
complexities that need further investigation.
With Porto Marghera sediments, high removal efficiencies for TPHs were observed in the
oxidation experiments (Fenton-like reagents). The majority of the conditions tested
downgraded sediment classification for this parameter. On the contrary, changes in the
classification were not obtained for PAHs and PCBs. Concerning the investigated process
parameters, tap water and strong acidic conditions resulted in the highest pollutant abatement.
The addition of Fe2+ did not seem a key factor in gaining better abatements. Unidentified by-
products were found in the oxidized sediments. Tests conducted on Gowanus canal sediments
resulted in significant decreases of total PAHs in all the configurations tested. The maximum
removal efficiency (54%) was achieved in the peroxy-acid system. The oxidation reactions
with persulfate and peroxy-acid resulted in high metal leachability.
Based on total PAH removal efficiency, oxidation was more effective on the Gowanus
canal sediment, despite the lower amount of oxidizer added. The presence of more types of
oxidazable chemical species in Porto Marghera sediments may have limited the efficiency on
PAHs, and the significantly higher total PAH burden in the Gowanus canal sediments may
have increased the contaminant availability for oxidation. Iron addition improved PAH
removal in Gowanus canal tests, but had no effect on Porto Marghera sediments; the lower
298 Sabrina Saponaro, Alessandro Careghini, Kevin Gardner et al.

content of iron in the Gowanus canal sediment or different iron species in the sediments could
explain this behavior.
For ex-situ application, the treatment of water used in the process seems to be mandatory
before discharge. Moreover, mineralization of the target organic compounds does not seem
certain. Many by-products could be produced, with doubts about toxicity and environmental
behavior. Ecotoxicological tests should be performed on the treated material prior to its full-
scale use. The use of a bioslurry post-treatment could be a possible step to remove the
intermediates or reduce toxicity [Palmroth et al., 2006]. Moreover, the sequential treatment
(chemical oxidation + biodegradation) could improve the overall removal of organic
pollutants [Kulik et al., 2006; Vanderrama et al., 2009].
No effect of chemical oxidation was observed on specific resistance to filtration in all
tests. Small changes occurred on residual moisture in the sediment after filtration for three
tests, but the extent of changes were not of practical interest.

ACKNOWLEDGMENTS
This work was supported by the Italian Ministry of Education, University and Research
(PRIN 2005 Project) and the Cooperative Institute for Coastal and Estuarine Environmental
Technology.

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Editor: Adam G. Friedman, pp. 301-332 © 2011 Nova Science Publishers, Inc.

Chapter 10

RECONSTRUCTION OF THE EUTROPHICATION

IN THE GULF OF FINLAND USING A DYNAMIC
PROCESS-BASED MASS-BALANCE MODEL

Lars Håkanson*
Dept. of Earth Sciences, Uppsala University, Uppsala, Sweden

ABSTRACT
The Gulf of Finland is a large bay in the Baltic Sea where major changes have taken
place during the last 100 years. The Secchi depth has, for example, decreased from more
than 7 m to about 5 m. The basic aim of this work has been to try to reconstruct the
development that has taken place in this bay during the last 100 years. Since the
conditions in the Gulf of Finland depend very much on both the river input of nutrients
directly to the bay and the exchange of nutrients and water between the bay and the Baltic
Proper, this work has focused on such interactions. The work describes how a general
process-based mass-balance model (CoastMab) has been applied for the Baltic Proper
and the Gulf of Finland. The model has previously been extensively tested and validated
for phosphorus, suspended particulate matter, radionuclides and metals in several lakes
and coastal areas. The transport processes quantified in this model are general and apply
for all substances in all aquatic systems, but there are also substance-specific parts
(mainly related to the particulate fraction and the criteria for diffusion). This is not a
model where the user should make any tuning or change model constants. The idea is to
have a model based on general and mechanistically correct algorithms describing the
monthly transport processes (sedimentation, resuspension, diffusion, missing, etc.) at the
ecosystem scale and to calculate the role of the different transport processes and how a
given system would react to changes in inflow related to natural changes and
anthropogenic reductions of water pollutants. The results presented in this work indicate
that it is possible to remediate the Gulf of Finland and the Baltic Proper to the conditions
that characterized the system 100 years ago. About 7000 tons of phosphorus (including
1800 tons from the tributaries to the Gulf of Finland) must then be removed on an annual
basis from the present annual tributary load of about 30000 tons to the Baltic Proper. The

*
Corresponding author: E-mail: Lars.Hakanson@geo.uu.se, Fax: +46-18-471-2737, Phone: +46-18-471-3897.
302 Lars Håkanson

trophic conditions in the Baltic Proper have varied relatively little during the last 25-30
years. The most marked changes in Secchi depth in the Gulf of Finland took place
between 1920 and 1980.

Keywords: coastal waters; nutrients; eutrophication; Baltic Sea; Gulf of Finland; mass-
balance modeling; Secchi depth; chlorophyll, cyanobacteria.

1. INTRODUCTION AND AIM

The conditions in the Baltic Sea, and specifically in the Baltic Proper and the Gulf of
Finland, have been discussed in many papers and books (see recent compilations by Pitkänen
and Tallberg, 2007; and also Ambio, 2001, 2007; Schernewski and Schiewer, 2002;
Schernewski and Neumann, 2005; Wulff et al., 2001). The aim of this work is to focus on the
conditions in the Gulf of Finland, since this is one of most heavily eutrophicated, major sub-
basins in the Baltic Sea (see Figure 1 and the HELCOM website), and to try to reconstruct the
development that has taken place in this bay between the years 1900 and 2000. The
eutrophication in the Gulf of Finland has been discussed in many papers and reports (see, e.g.,
Kiirikki et al., 2001; SYKE, 2003, 2006; HELCOM, 2006). Since the Gulf of Finland is open
to the Baltic Proper, the conditions in the Baltic Proper will influence the conditions in the
Gulf of Finland beside the direct discharges to the Gulf (see, e.g., Savchuk and Wulff, 1999).

Figure 1. Average annual Secchi depths in the Baltic Sea and parts of the North Sea in the upper 10 m
water column based on HELCOM data for the period from 1990 to 2005 (from Lindgren and Håkanson,
2007)

The main objective of this work can be illustrated by the data on Secchi depth given in
Figure 2 (see also Aarup, 2002). These data come from the HELCOM database and concern
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 303

how the water clarity (the Secchi depth) has changed in the period from 1900 to 1991. An
initial trend analysis, a linear regression between measured Secchi depths and time (month 1
is January of 1900), indicates the negative development: The Secchi depth has decreased from
about 7-8 m 100 years ago to about 5 m today. One can also note the large scatter in the data
from the individual sampling sites. The aim of this work is to try to explain the development
shown in Figure 2 by using:

1. a process-based dynamic mass-balance model for salt (CoastMab for salt; see
Håkanson et al., 2007) to get realistic and reliable data on the water fluxes to, within
and from the Gulf of Finland;
2. a process-based dynamic mass-balance model for phosphorus (CoastMab for
phosphorus; see Håkanson and Eklund, 2007a; Håkanson and Bryhn, 2007a) to
quantify how the system would react to changes in nutrient loading;
3. linked to the mass-balance model for phosphorus, there are empirically-based sub-
models for Secchi depth, chlorophyll-a concentration, concentration of
cyanobacteria, sedimentation, total nitrogen and suspended particulate matter (which
will be discussed later); and
4. linked to these models, there is also a more comprehensive dynamic foodweb model
for 10 functional groups (CoastWeb, see Håkanson and Gyllenhammar, 2005;
Håkanson and Bryhn, 2007b; Håkanson and Lindgren, 2007), which is used in this
work to calculate biouptake and retention of phosphorus in biota.

The CoastMab-model has previously been extensively tested and validated for
phosphorus from over 20 different coastal areas and more than 40 lakes, for suspended
particulate matter in over 20 coastal areas and more than 10 lakes and for toxic substances
(radionuclides and metals) in several lakes and coastal areas.

Figure 2. HELCOM data on the Secchi depth in the Gulf of Finland 1990 to 1991 and a trend analysis;
regression line, coefficient of determination (r2), number of data (n) and statistical certainty (p)
304 Lars Håkanson

The basic idea is to demonstrate (A) how this modeling works and how well modeled
phosphorus concentrations, Secchi depths and chlorophyll values agree to empirical data, (B)
how reductions in nutrient loading to the Gulf of Finland and to the Baltic Proper would
influence the conditions for these target variables in the Gulf of Finland, and (C) how a
reconstruction of the development could be made so the that the changes in the Gulf of
Finland shown by the data in Figure 2 may be explained and understood. This would also
imply that important information to reverse the development in the Gulf of Finland and the
Baltic Proper could be gained.
To reduce nutrient inputs from urban areas, industries, catchments or diffuse sources
involves complex and often expensive remedial measures (see, e.g., Nixon, 1990; Moldan and
Billharz, 1997; Livingston, 2001; Bortone, 2005). A central question is then how a given
system would respond to the suggested measures? How long would it take to reach a new
steady state? What are the characteristic new nutrient concentrations in the water? How
would key bioindicators for eutrophication, such as chlorophyll-a concentration,
concentration of cyanobacteria or Secchi depth change? In short, what is the environmental
benefit related to the remedial costs? To address such questions, two important issues must be
dealt with:

1. A validated process-based dynamic model, which has proven to predict the target
variables well, must be at hand to provide realistic values for the dynamic (time-
dependent) response of a reduced nutrient loading since this can not generally be
done by static empirical regression models? One aim of this work is to use such a
dynamic model, the CoastMab-model. This model has been presented and critically
tested with good results for many aquatic systems (see Håkanson and Eklund, 2007a)
and it will be used in this work for the Gulf of Finland and also for the Baltic Proper,
since the condition in the Baltic Proper influence the Gulf of Finland very much.
2. The dynamic model must quantify all important fluxes to, within and from the
system and include information on the natural load and the anthropogenic load and,
preferably also, information on how much of the anthropogenic load from different
sources that can, realistically, be reduced. An important reason for selecting the Gulf
of Finland as a case-study is that for this bay the author can access the necessary
data:
First, data on the salinity inside and outside the bay, and the tributary water fluxes to the
bay, must be available so that a reliable mass-balance for salt can be established, so
that the water exchange with the outside sea (the Baltic Proper) can be quantified
realistically and also the theoretical water retention time in the bay, which influence
important internal processes, such as stratification, mixing and diffusion. The
CoastMab-model also includes a mass-balance model for salt structured in the same
way as the model for phosphorus except that the mass-balance model for phosphorus
also calculates sedimentation, resuspension, burial and biouptake of dissolved
phosphorus. By definition, total phosphorus (TP) in the water generally includes
living and dead plankton, but not larger animals such as zoobenthos and fish. A new
aspect of this version of the CoastMab-model (as compared to the basic version from
Håkanson and Eklund, 2007a) is that this model calculates phosphorus uptake and
retention in biota with short turnover times (phytoplankton, bacterioplankton,
herbivorous zooplankton and benthic algae) and long turnover times (predatory
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 305

zooplankton, prey and predatory fish, macrophytes, zoobenthos and jellyfish) using
the CoastWeb-model.
Second, data on the TP-concentration in the water outside the bay must be at hand so that
the inflow from the Baltic Proper can be calculated. Data on the TP-transport from
different sources on land are also needed and such data are available for the Gulf of
Finland from the HELCOM data base. HELCOM also gives information on the
natural background losses, the diffuse losses and the point sources discharges of TP
to the Gulf of Finland and from this one can use the CoastMab-model to estimate
how various reductions in the anthropogenic load would influence the system. This is
essential information for the reconstruction requested in this work. Even though the
focus is on the changes in Secchi depth, this work will also discuss changes in other
bioindicators of eutrophication, mainly the chlorophyll-a concentration, as a standard
measure of phytoplankton biomass, and the concentration of cyanobacteria, as a
measure of the mass of ―harmful‖ algae.

2. DATA FROM THE GULF OF FINLAND AND INFORMATION

ON THE MODEL STRUCTURE

2.1. Data and Methods

Figure 1 shows that the Gulf of Finland today generally has a relatively low Secchi depth
compared to other basins in the Baltic Sea. Table 1 gives background data from the Gulf of
Finland and the Baltic Proper and shows that the limiting section area towards the Baltic
Proper is 3.74 km2. This means that the Gulf of Finland is quite open to the Baltic Proper.
Table 1 also gives information on, e.g., total area, volume, mean depth, maximum depth, the
depth of the theoretical wave base. Table 2 gives data on the volume of the surface-water
layer and the middle-water layer separated by the theoretical wave base and the deep-water
layer separated from the middle-water layer by the depth of the average halocline. The annual
fresh-water flux to Gulf of Finland used in this work is the average annual value from
Savchuk (2000; 3552 m3/s), Myrberg (1998; 3615 m3/s) and Stålnacke et al. (1999; 3875;
m3/s). The monthly data on water discharge used in the modeling have been calculated from
the average annual value using the dimensionless moderator for this purpose (from
Abrahamsson and Håkanson, 1998). This moderator is based on data on the size of the
catchment area, mean annual precipitation and latitude (see table 1). Since the author does not
have access to reliable monthly data on water discharge for the study period (1990 to 1998), it
should be stressed that this modeling concerns average, characteristic conditions on a monthly
base for this period of time and not the actual sequence of months. The results from 1990-
1998 concerning the processes and fluxes will then be put into a wider time frame (1990 to
2000).
306 Lars Håkanson

Table 1. Basic data for two main sub-basins in the Baltic Sea, the Gulf
of Finland and the Baltic Proper (from Håkanson and Lindgren, 2007)

Gulf of Finland (GF) Baltic Proper (BP)

Area (km2) 29600 211100
Max. depth (m) 105 459
Volume (km3) 1073.2 13054.6
Mean depth (m) 36.3 61.8
Wave base (m) 41 43.8
Section area (km2) 3.74 -
Halocline depth (m) 75 75
ET-areas (%) 63 47
Water discharge (km3/yr) 29.0 250
Catchment area (km2) 421000 568973
Latitude (°N) 60 58
Precipitation (mm/yr) 593 750

Table 2. Data on volumes and areas (below the given depths) based on new
hypsographic curves (from Håkanson and Lindgren, 2007)

Basin Level Volume Area below the given level

(km3) (km2)
Gulf of Finland SW 851.2 29600
MW 202.0 10900
DW 20.0 2400
Baltic Proper SW 7315 211100
MW 3050 123500
DW 2690 73000

Also note that the values presented in this work relate to the definitions of the surface-
water, the middle-water and the deep-water layers, the given time period (1990 to 1998) and
the given hypsographic curves (from Håkanson and Lindgren, 2007). This means that
although these data correspond quite well with other values (see, e.g., Voipio, 1981;
Mikulski, 1985; Monitor, 1988), they are not directly comparable.
The theoretical wave base is defined from the ETA-diagram (erosion-transport-
accumulation; from Håkanson, 1977), which gives the relationship between the effective
fetch, as an indicator of the free water surface over which the winds can influence the wave
characteristics (speed, height, length and orbital velocity). The theoretical wave base
separates the transportation areas (T), with discontinuous sedimentation of fine materials,
from the accumulation areas (A), with continuous sedimentation of fine suspended particles.
The theoretical wave base (Dwb in m) is at a water depth of 41 m in the Gulf of Finland. This
is calculated from eq. 1 (A = area in km2):

Dwb= (45.7·√A)/(√A+21.4) (1)

 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 307

This approach gives one value for the theoretical wave base related to the area of the
system. So, the Gulf of Finland has been divided into three depth intervals:

1. The surface-water layer (SW), i.e., the water above the theoretical wave base at 41
m.
2. The middle-water layer (MW) between the theoretical wave base and the average
depth of the halocline at 75 m.
3. The deep-water layer (DW) is defined as the volume of water beneath the average
depth of the halocline at 75 m.

It should be noted that the theoretical wave base describes average conditions. The actual
wave base varies around 41 m. During storm events, the wave base will be at greater water
depths (see Jönsson, 2005) and during calm periods at shallower depths. Håkanson and
Lindgren (2007) have presented new hypsographic curves for the Gulf of Finland calculated
using GIS (Geographical Information System) and bathymetric data provided by Seifert et al.
(2001). Those values have been used in these calculations. One can note from table 2 that the
area below the theoretical wave base (Dwb) at 41 m is 10900 km2 and that the volumes of the
SW, MW and DW-layers are 851.2, 202.0 and 20.0 km3 and the entire volume is 1073.2 km3.
The Gulf of Finland is also relatively shallow and 63% of its bottom area is dominated by
resuspension processes of fine materials (these are the erosion and transportation areas, ET; as
calculated by the CoastMab-model; see table 1).
Figure 3 illustrates the number of sampling sites for the Secchi depth data from the
HELCOM data base used in this work. Empirical data on salinities, Secchi depth, chlorophyll
and nutrient concentrations will be given later and compared to modeled values. There are no
corresponding empirical data on cyanobacteria available to the author from the Gulf of
Finland. The empirical temperature data from the HELCOM data base (from 1990 to 1998)
have been used to model stratification and mixing. The standard deviations (SD) for the
monthly mean empirical values are very important in the sense that the variables with the
high inherent SD-values cannot be expected to be predicted as well as variables with
comparatively low SD-values (such as salinity).

Figure 3. Sampling sites for Secchi depth in the Gulf of Finland (from HELCOM)
308 Lars Håkanson

Table 3. Calculated monthly values for the theoretical SW, MW and DW water
retention times (TSW, TMW and TDW), the water fluxes (Q) from the Baltic Proper (BP) to
the Gulf of Finland (GF) in the three layers (SW, MW and DW), the mixing transport
(abbreviated with an x) between the MW and SW and the DW and MW layers and the
water velocity in the section area (uAt) from the mass-balance model for salt. These
values are used in the mass-balance model for phosphorus

Mont TSW TMW TDW QSWBPGF QMWBPGF QDWBPGF QMWSWx QDWMWx uAt
h
months months months km3/month km3/month km3/month km3/month km3/month cm/s
1 8.6 7.6 2.5 69.6 7.1 7.1 19.5 0.8 2.0
2 8.6 7.8 2.6 68.4 7.0 7.0 18.8 0.7 2.0
3 8.7 7.8 2.5 69.5 7.1 7.1 18.8 0.8 2.0
4 8.6 7.5 2.5 69.8 7.1 7.1 19.8 0.8 2.0
5 8.1 6.6 2.7 63.5 6.5 6.5 23.9 1.0 2.0
6 8.1 6.8 2.8 60.6 6.2 6.2 23.7 1.0 2.0
7 8.0 6.1 2.5 67.7 6.9 6.9 26.2 1.1 2.0
8 7.8 5.5 2.4 69.5 7.1 7.1 29.7 1.2 2.0
9 10.3 19.0 2.7 70.6 7.2 7.2 3.4 0.1 2.0
10 10.4 20.4 2.7 70.6 7.2 7.2 2.6 0.1 2.0
11 8.5 7.1 2.4 71.7 7.3 7.3 21.0 0.9 2.0
12 8.2 6.3 2.4 70.5 7.2 7.2 24.6 1.0 2.0

2.2. The Dynamic Coastmab-Model

The model consists of seven compartments: surface water (SW), middle water (MW),
deep water (DW), erosion/transportation areas for fine sediments (ET-areas), accumulation
areas for fine sediments below the theoretical wave base (A-areas), biota with short turnover
times (BS) and biota with long turnover times (BL). There are algorithms for all major
internal TP-fluxes (outflow, TP from land uplift, sedimentation, resuspension, diffusion,
mixing, biouptake and retention in biota and burial; see Håkanson and Eklund, 2007a, for a
more detailed model description).
To calculate the inflow of TP to the Gulf of Finland (GF) from the Baltic Proper (BP),
modeled data on the TP-concentrations in the surface, middle and deep-water layers in the
Baltic Proper from Håkanson and Bryhn (2007a) have been used. The water fluxes between
the Gulf of Riga and the Baltic Proper are calculated from the mass-balance for salt. So, the
inflows to the three layers (SW, MW and DW) from the Baltic Proper are given by the water
discharges in table 3 (QSWBPGR, QDWBPGR and QDWBPGR) and the modeled TP-concentrations.
The transport of TP from the catchment area to the Gulf of Finland uses data from HELCOM:
1191 t TP/yr from natural background losses, 2112 t TP/yr from diffuse losses and 2431 t
TP/yr from point source discharges. These annual TP-fluxes have been transformed into
monthly values by division with 12 and by applying a seasonal moderator for water discharge
(characteristic mean monthly Q-values divided by the annual mean water discharge).
From extensive measurements in many coastal areas (see Håkanson et al., 1986), one can
conclude that typical water velocities in limiting section areas range between 0.5 and 20 cm/s
for coastal areas in the Baltic Sea. Lower velocities that 0.5 cm/s would be rather unrealistic
on a monthly or annual basis. Typical velocities in the coastal jet zone in the Baltic Sea are in
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 309

the range 15-25 cm/s (see FRP, 1978). The water velocity in the section area has been
calculated for the total outflow (km3/yr) divided by half the section area since there is also
inflow of water to maintain a given water level ((km3/yr)·(1/(0.5·km2). Savchuk (2006) gave a
total water outflow from the Gulf of Finland of 554 km3/yr, which is a factor of 2 lower than
the value obtained in this work (990 km3/yr) and 554 seems a less likely value since it would
imply that the average water velocity in the section area would be lower than 1 cm/s. These
calculations give an average velocity in the section area of 1.9 cm/s.
Some key questions for this work are: How will the system react if the diffuse losses and
the point source discharges of TP to the Gulf are reduced? How would the system respond if
similar reductions to the entire Baltic Proper are also done? To calculate the changes in the
concentrations of TP in the SW, MW and DW-layers, the CoastMab-model has also been
applied to the entire Baltic Proper (see Håkanson and Bryhn, 2007a).
The theoretical water retention times in the three layers (see table 3) from the basic mass-
balance for salt are used together with the temperature dependent mixing rate in the mass-
balance model as indicators of how the turbulent mixing influences the settling velocity for
particulate phosphorus – the faster the water renewal, the more turbulence, the slower the
settling velocity. The small TP-input from precipitation onto the water surface of the Gulf of
Finland has been estimated from the characteristic annual precipitation of 593 mm and a TP-
concentration in the rain of 5 µg/l (see Håkanson and Eklund, 2007a).
The internal processes are: sedimentation of particulate phosphorus from surface water to
middle water and deep water (FSWMW and FSWDW), sedimentation from the SW-layer to areas
of erosion and transportation (FSWET), sedimentation from the MW and DW-layers to the
respective accumulation areas (FMWAMW and FDWADW), resuspension (advection) from ET-
areas (including TP from land uplift, FLU) either back to the surface water (FETSW) or to the
middle water (FETMW), diffusion of dissolved phosphorus from accumulation area sediments
in the MW and DW-layers to water in the MW and DW-layers (FAMWMW and FADWDW),
diffusion from MW and DW-water layers to the SW and MW-layers, respectively (FMWSWd
and FDWMWd), upward and downward mixing between the water layers (FSWMWx, FMWSWx,
FDWMWx and FMWDWx) and biouptake and elimination of phosphorus from biota with short and
long turnover times (FbioupBS and FretbioBS and FbioupBL and FretbioBL). When there is a
partitioning of a flux from one compartment to two compartments, this is handled by a
distribution coefficient (DC).

1. The DCs regulating the amount of phosphorus in particulate and dissolved fractions
in the SW, MW and DW-layers. These DCs are called particulate fractions (PF). By
definition, only the particulate fraction of a substance is subject to gravitational
sedimentation and only the dissolved fraction (DF = 1 – PF) may be taken up by
biota.
2. The DC regulating sedimentation of particulate phosphorus either to areas of fine
sediment erosion and transport (FSWET) or to the areas beneath the theoretical wave
base (FSWMW). The ET-value is 0.63 (i.e., 63% of the total area should function as
areas of fine sediment erosion and transport).
3. The DC describing the resuspension flux from ET-areas back either to the surface
water (FETSW) or to the MW-compartment (FETMW), as regulated by the form factor
(Vd, where DC=Vd/3, Vd = 3·Dm/Dmax, Dm = the mean depth, Dmax = the maximum
depth).
310 Lars Håkanson

4. The DC describing how much of the TP in the water that has been resuspended
(DCres) and how much that has never been deposited and resuspended (1-DCres) in
the layers. The resuspended fraction settles out faster than the materials that have not
been deposited.

Land uplift (FLU) is a special case. Land uplift is a main contributor of TP to the Baltic
Proper (Håkanson and Bryhn, 2007a). From the map illustrating the spatial variation in land
uplift (see Voipio, 1981), one can estimate that the mean land uplift in the Gulf of Finland is
about 1.2 mm/yr and this value has been used in these calculations. Land uplift has been
discussed in many contexts (Voipio, 1981; Jonsson et al., 1990; Jonsson, 1992) and the
algorithm to quantify how land uplift influences the concentration of TP has been given by
Håkanson and Bryhn (2007a). The total area above the theoretical wave base in the Gulf of
Finland is about 18700 km2 and the sediments in this area will be exposed to increased
erosion by wind/wave action due to land uplift. The sediments in the shallower parts, which
may have been deposited more than 1000 years ago, will be more consolidated than the recent
materials close to the theoretical wave base. The calculation of the TP-flux from land uplift
uses (1) modeled data on the TP-concentration in the accumulation area sediments from the
MW-zone, (2) a water content of the sediments exposed to increased erosion set to be 15%
lower than the modeled water content of the recent sediments and (3) the total volume of
sediments above the theoretical wave base lifted each year.

2.3. Regressions between Modeled TP-Values versus Total-N and

Bioindicators

The Secchi depth (Sec in m) is a target bioindicator in this study and it is calculated from
a model illustrated in Figure 4 relating Secchi depth to the concentration of suspended
particulate matter in the SW-layer (SPMSW in mg/l) and the salinity of the SW-layer (SalSW)
according to eq. 2 (from Håkanson, 2006).

SPMSW = 10^(-0.3-2·(log(Sec)-(10^(0.15·log

(1+SalSW)+0.3)-1))/((10^(0.15·log(1+ SalSW)+0.3)-1)+0.5)) (2)

One can note from Figure 4 that for the Gulf of Finland with a SW-salinity of about 6
psu, one should expect a fairly rapid (non-linear) improvement in Secchi depths if the SPM-
concentration is lowered from 4 to 3 mg/l. SPMSW, in turn, is calculated from dynamically
modeled TP-concentrations in the SW-layer using the following regression (from Håkanson
and Bryhn, 2007b):

SPM = 0.0235·TP1.56 (3)

(r2 = 0.895; n = 51)

 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 311

Figure 4. The relationship between Secchi depth, concentration of suspended particulate matter (SPM)
and the surface-water salinity (from Håkanson, 2006)

Eq. 3 will translate modeled TP (in µg/l) into SPM-values (in mg/l) and together with
modeled data on the salinity, translate those values into Secchi depths using eq. 2. The Secchi
depth is important for predictions not just of water clarity and the depth of the photic zone but
also of, e.g., macrophyte cover and biomass of benthic algae using the CoastWeb-model. It
should be noted that eq. 3 is based on data from systems with salinities ≤ 15‰. This means
that it may provide more limited predictive power for coastal systems with salinities ≥ 15‰.
In this work, mean concentrations of chlorophyll-a (Chl in µg/l) for the growing season
are first predicted from modeled TP-concentrations and from modeled SW-salinities using an
approach presented by Håkanson and Eklund (2007b). In this work, the modeling is done on a
monthly basis and in the CoastMab-model there is information on the dissolved fraction of
phosphorus. This mean that the basic approach for the mean conditions during the growing
season (ChlGS in µg/l) has been modified to predict the requested mean monthly chlorophyll
values (Chl). These calculations use simple dimensionless moderators to account for
seasonal/monthly changes in the light conditions (DayL; mean monthly number of hours with
daylight in the Gulf of Finland; from standard tables) and in the amount of
bioavailable/dissolved phosphorus (DFSW). This means the chlorophyll-a concentration are
predicted from:

Chl = (DayL/12.3)·(DFSW/0.44)·ChlGS (4)

Where the basic model between the TP-concentration in the SW-layer (TPSW in µg/l,
modeled), the salinity in the SW-layer (SalSW, modeled) and ChlGS is shown in Figure 5.
(DayL/12.3) is a dimensionless moderator based on the ratio between the monthly DayL-
values divided by the mean annual number of hours with daylight (12.3) in the Gulf of
Finland. The modeled monthly values of the dissolved fraction in the SW-layer (DFSW) have
been transformed into a dimensionless moderator by division with the average DF-value of
0.44 for phosphorus in surface water conditions (see Håkanson, 2006). This means that the
312 Lars Håkanson

predicted chlorophyll-values are low if the DF is low, the number of hours with daylight low
and the modeled TP-values low. The small variations in salinity (see table 4) will not
influence the predicted Chl-values very much, but such variations are also accounted for.

Table 4. A comparison between measured (empirical; data from HELCOM for 1990 to
1998) data and modeled values on the salinity in the SW, MW and DW-layers in the
Gulf of Finland. Note that there are no reliable mean monthly data accessible from the
MW and DW-layers and the data given for these layers (7.0 and 10.0) should be
regarded as the “best possible” estimates based on few and scattered data from the Gulf
of Finland and from the area of the Baltic Proper outside the Gulf of Finland

Month SalSW SalSW SalMW SalMW SalDW SalDW

psu psu psu psu psu psu
mod emp mod emp mod emp
1 6.20 5.87 6.91 7.00 10.10 10.00
2 6.20 6.15 6.91 7.00 10.09 10.00
3 6.20 6.37 6.91 7.00 10.09 10.00
4 6.21 6.32 6.92 7.00 10.08 10.00
5 6.19 6.30 6.91 7.00 10.06 10.00
6 6.14 6.24 6.88 7.00 10.01 10.00
7 6.10 6.40 6.86 7.00 9.98 10.00
8 6.12 6.14 6.84 7.00 9.95 10.00
9 6.13 6.38 6.84 7.00 9.99 10.00
10 6.14 6.53 6.89 7.00 10.11 10.00
11 6.16 6.15 6.91 7.00 10.14 10.00
12 6.19 5.80 6.91 7.00 10.10 10.00
Mean 6.17 6.22 6.89 7.00 10.06 10.00
Median 6.18 6.27 6.91 7.00 10.09 10.00
SD for emp 0.22 0.00 0.00
Diff.
1 0.33 -0.09 0.10
2 0.05 -0.09 0.09
3 -0.17 -0.09 0.09
4 -0.11 -0.08 0.08
5 -0.11 -0.09 0.06
6 -0.10 -0.12 0.01
7 -0.30 -0.14 -0.02
8 -0.02 -0.16 -0.05
9 -0.25 -0.16 -0.01
10 -0.39 -0.11 0.11
11 0.01 -0.09 0.14
12 0.39 -0.09 0.10
Mean diff. -0.06 -0.11 0.06
SD for diff. 0.23 0.03 0.06
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 313

Figure 5. Illustration of the model for how salinity influences the Chl/TP-ratio (the Ysal-moderator) and
the equations (from Håkanson and Eklund, 2007b)

Figure 6. Outline of the model to predict median summer values of cyanobacteria from total
phosphorus, total nitrogen, salinity and surface-water temperatures. From Håkanson et al. (2007b)

The empirically-based model to predict the total concentration of cyanobacteria

(Håkanson et al., 2007b) is given in Figure 6. The following simulations will use dynamically
314 Lars Håkanson

modeled monthly TP-concentrations in the SW-layer, empirical mean monthly SW-

temperatures, dynamically modeled SW-salinities and modeled monthly TN-concentrations in
the SW-layer (see eq. 5) to predict monthly values of cyanobacteria in the SW-layer. Note
that there are no empirical data available to the author to test the predicted values for
cyanobacteria, but these values are basically predicted from an empirical approach which
yielded an r2-value of 0.78 (coefficient of determination), which is close to the maximum
possible predictive power for cyanobacteria because of the inherently very high coefficient of
variation (CV) for cyanobacteria (see Håkanson et al., 2007b). Nitrogen fixation by
cyanobacteria counteracts long-term nitrogen deficits, and the N-fixation rate depends on the
TP-concentration, water temperature and the TN/TP-ratio (see Figure 6).
The mechanisms showing that phosphorus is generally the long-term controlling nutrient
for the primary production were first demonstrated in whole-lake experiments by Schindler
(1977, 1978). The same mechanisms have also been used to explain primary production and
nutrient concentrations in the Baltic Proper, e.g., in modeling work by Savchuk and Wulff
(1999), and have been tested globally by Tyrrell (1999) (see also Hecky and Kilham, 1988;
Howarth, 1988; Guildford and Hecky. 2000). However, these results demonstrating the role
of phosphorus as a long-term limiting nutrient have not yet been rooted in management
policies for the Baltic Sea. Reductions of nitrogen favor the production of cyanobacteria.
It is well established (Redfield, 1958; Redfield et al., 1963) that plankton cells have a
typical atomic composition of C106N16P, which means that 16 times as many atoms (and 7.2
times as many grams) are needed of N than of P to produce phytoplankton. This means that
one generally finds a marked co-variation between phosphorus and nitrogen concentrations in
aquatic systems (see Wallin et al., 1992) and in this work total nitrogen (TN) concentrations
have been predicted from dynamically modeled monthly TP-concentrations using a regression
from Håkanson and Eklund, 2007b):

log(TN) = 0.70·log(TP) + 1.61 (5)

(r2 = 0.88; n = 58 coastal systems)

The following section will demonstrate how this modeling predicts first the salinities in
the three layers, then the TP-concentrations, Secchi depths, cyanobacteria and nitrogen and
also other variables of interest, such as TP-concentrations in sediments (0-10 cm) below the
theoretical wave base (the accumulation-area sediments) in the MW and DW-zones,
sedimentation in the three layers, settling velocities for particulate phosphorus (and suspended
particulate matter) and the dissolved fractions of phosphorus in the three layers (and hence
also the particulate fractions, PF = 1-DF). Whenever possible, the modeled values will be
compared to empirical data and to the uncertainty bands related to the empirical data and all
calculated TP-fluxes in the Gulf of Finland and all calculated TP-amounts (= where would
one find the TP?)
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 315

3. RESULTS

3.1. Modeled Values versus Empirical Data

Table 4 gives modeled values for the salinity compared to the mean empirical monthly
data for the period 1990 to 1998 and also to the standard deviations (SD) for the mean
empirical values. If the model yields values close to the empirical mean values and in-
between the uncertainty bands given by ± one standard deviation, the predictions should be
regarded as good. For all these comparisons between modeled and empirical data, it should be
noted that:

The monthly inflows of water and phosphorus have not been calculated using data for
this period of time (1990-1998) but using a general model for water discharge (see
Abrahamsson and Håkanson, 1998). This will explains some of the differences
between the modeled and the measures monthly values for salinity, TP and other
variables.
The monthly calculations of the inflow of water, salt and phosphorus from the Baltic
Proper use mean values for the SW and MW-compartments not in the inflowing
water from the area just outside the Gulf of Finland, which would have been more
appropriate, but for the entire Baltic Proper. For the inflow to the DW-compartment,
a value of 70.9 µg TP/l (from Karlsson, 2007) has been used. The reason why the
more appropriate data have not been used is simply that it has been difficult to find
such data. This likely also further explains some of the differences between the
modeled and the measured monthly values.

With these reservations, one can note from table 4 that the predicted monthly salinities in
the SW-layer are generally close to the empirical data and within the defined uncertainty
bands of the empirical data (± 1SD = 0.22). The average error (the mean difference for the 12
months) is 0.02 psu. It should be noted that the available data from the MW and DW-layers
are few and the values 7 and 10 for the two layers are uncertain. The CoastMab-model gives a
value of 6.75 psu for the mean salinity in the MW-layer and of 10.02 psu in the DW-layer.
The water fluxes between the Gulf of Finland and the Baltic Proper calculated from the mass-
balance model for salt and the corresponding fluxes for mixing and for molecular diffusion
are used without any changes also in the mass-balance calculations for phosphorus, except, of
course, that phosphorus has a particulate fraction. The main message here is that there should
be no ―tuning‖ of the mass-balance calculations and the same algorithms and values have
been used for mixing, diffusion and water fluxes for salt and phosphorus. There are
substance-specific parts in the CoastMab-model and they mainly concern the algorithms for
the particulate fraction and for diffusion.
The results for phosphorus are given in table 5.

(A) The TP-concentrations in the SW-layer are generally close to the empirical data and
(mean difference 0.5 and median difference 0.2 µg/l) well within the uncertainty
bands of the empirical data (±1SD).
316 Lars Håkanson

(B) Also the average TP-concentrations in the MW-layer are close to the empirical
average value (the mean difference between the mean values is 2.9 µg/l), which is a
small difference compared to the relatively high standard deviation for the empirical
data (18.6 µg/l).
(B) The average TP-concentrations in the DW-layer differ more (mean difference 25.4)
but also this is close to the inherent uncertainty in the empirical data (SD = 22.0
µg/l).
(C and D) The target variables, the two bioindicators Secchi depth and chlorophyll-a
concentration in the SW-layer, are close to the empirical values (the mean error for
Secchi depth is 0.2 m and for chlorophyll 2.3 µg/l) and within the uncertainty bands
defined by one standard deviation of the empirical mean value. The modeled
chlorophyll concentrations also give the ―twin-peak pattern‖ as indicated by the
empirical data. It should be stressed that the chlorophyll concentrations are predicted
from a regression including dynamically modeled TP-concentrations in the surface
water and a dimensionless moderator for the light conditions (eq. 4) and the
calculated dissolved fraction of phosphorus. These calculations also include
considerations to the biouptake of dissolved phosphorus in all types of biota
(functional groups) included in the CoastWeb-model. However, the temporal patterns
are calculated in the standardized pattern to reveal the most typical, characteristic
condition in the Gulf of Finland, and the given presuppositions including the
relatively high uncertainties in the empirical data, one cannot hope to obtain very
much better predictions than these.
(F) The TN-concentrations are predicted from a simple regression using dynamically
modeled TP-concentrations in the SW-compartment. There is a relatively good
correspondence between modeled and measured TN-concentrations (the mean error
is 1.3 µg/l).

The TN/TP-ratios based on modeled values, modeled salinities in the SW-layer and
empirical temperature data for the SW-layer will be used to calculate the concentration of
cyanobacteria (see later).
From this, one can conclude that the model predicts the target variables quite well given
the factual limitations in the seasonal patterns in the driving variables for tributary water
discharge (since this pattern in the modeling is not based on measured data for the modeled
period) and in the seasonal pattern for the TP-concentrations outside the Gulf of Finland
(since these data for the SW and MW-layers emanate not from the area outside of the Gulf
but from the entire Baltic Proper and since the empirical value for the TP-concentration in the
Baltic Proper outside the Gulf of Finland is uncertain). Note that there has been no tuning of
the model to achieve these predictions and that the basic model has been shown to describe
the transport processes for phosphorus very well for many other coastal areas (see Håkanson
and Eklund, 2007a). This should lend some credibility to the following simulations.
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 317

Table 5. A comparison between empirical data (data from HELCOM from

1990 to 1998) and modeled values on TP-concentrations, Secchi depths,
chlorophyll-a concentrations and total-N concentrations (TN) in the
three layers (SW, MW and DW) in the Gulf of Finland. The lower part
of the table gives the differences between modeled and measured values

Month TPSW TPSW TPMW TPMW TPDW TPDW Sec Sec Chl Chl TN TN
µg/l µg/l µg/l µg/l µg/l µg/l m m µg/l µg/l µg/l µg/l
mod emp mod emp mod emp mod emp mod emp mod emp
1 23.0 34.1 37.0 37.7 90.4 71.7 6.1 6.3 3.1 0.5 366 439
2 24.0 32.2 35.0 35.1 90.5 43.2 5.6 5.1 5.9 1.3 376 422
3 24.8 30.1 32.7 33.9 89.3 31.3 5.4 5.1 7.9 2.2 386 410
4 25.3 30.1 32.0 35.6 86.9 57.2 5.3 5.4 8.3 10.5 391 394
5 25.6 22.5 32.8 32.3 85.1 47.8 4.7 5.6 7.5 7.3 394 394
6 26.5 24.0 35.0 40.9 84.7 69.2 4.2 5.5 7.2 2.4 403 458
7 26.8 16.2 36.5 39.1 85.4 69.5 4.6 5.0 6.8 3.5 407 352
8 27.0 17.5 38.0 38.2 85.0 50.6 4.6 5.8 5.9 3.0 409 329
9 25.6 16.6 38.1 39.6 87.6 68.0 5.2 5.3 7.5 5.8 394 291
10 22.7 16.9 36.2 51.5 85.3 126.1 6.4 4.8 5.1 3.6 362 294
11 21.2 24.2 38.0 40.7 79.2 47.8 7.3 3.3 1.5 0.4 345 375
12 22.1 24.2 39.0 40.7 86.2 47.8 6.7 6.3 2.3 0.5 356 447
Mean 24.5 24.1 35.8 38.8 86.3 60.9 5.5 5.3 5.7 3.4 382 384
Median 25.1 24.1 36.3 38.7 85.8 53.9 5.3 5.3 6.3 2.7 388 394
SD for emp. ±8.9 ±18.6 ±22.0 ±1.6 ±2.6 ±41
Diff.
1 -11.1 -0.7 18.7 -0.2 2.6 -73.0
2 -8.3 -0.1 47.3 0.5 4.6 -45.7
3 -5.3 -1.2 58.0 0.3 5.7 -24.0
4 -4.8 -3.7 29.7 -0.1 -2.2 -3.4
5 3.1 0.5 37.3 -0.9 0.3 0.2
6 2.5 -5.9 15.5 -1.3 4.8 -54.5
7 10.6 -2.7 15.9 -0.4 3.3 54.8
8 9.5 -0.2 34.4 -1.2 2.9 80.4
9 9.0 -1.5 19.6 -0.1 1.7 102.8
10 5.8 -15.3 -40.8 1.6 1.5 68.1
11 -3.0 -2.7 31.4 4.0 1.1 -29.8
12 -2.1 -1.7 38.4 0.4 1.8 -91.5
Mean diff. 0.5 -2.9 25.4 0.2 2.3 -1.3
Median diff. 0.2 -1.6 30.5 -0.1 2.2 13.7
SD for 7.3 4.3 24.6 1.4 2.2 63.9
diff.

3.2. Fluxes and Amounts of Phosphorus

Which are the large and the small TP-fluxes? And where is the phosphorus stored? Table
6 gives a compilation of the monthly TP-fluxes and a ranking based on the annual fluxes. One
can note that the two largest fluxes are biouptake and retention (=outflow) of phosphorus to
and from biota with short turnover times (BS). These fluxes (about 500000 t/yr) are 25 times
larger than the fluxes related to the following fluxes because the organisms in this group have
very short turnover times (about 3-6 days). The following fluxes are: sedimentation from the
MW-layer to accumulation areas within the MW-zone (FTPMWAMW = 28000 t/yr),
318 Lars Håkanson

resuspension from ET-sediments to the SW-layer (27500 t/yr), outflow of TP from the Gulf
of Finland (GF) to the Baltic Proper (BP) in the SW-compartment (21000 t/yr). The fluxes
that may be reduced by remedial measures are bolded in table 6: the SW-inflow from the
Baltic Proper (FSWBPGF = 14000 t/yr), total tributary inflow (Ftrib = 5735 t/yr) and inflow to the
DW and MW-layers from the Baltic Proper (FDWBPGR = 8880 and FMWBPGR = 4100 t/yr,
respectively). The diffusive flux from the accumulation areas sediment (below the halocline
at 75 m) is rather small (10 t/yr). The modeled TP-concentration in the accumulation area
sediments (0-10 cm) in the MW-layer is 2.4 mg/g dw and in the DW-layer 0.63 mg/g dw (see
table 7), which agrees with measured values for the Baltic Proper (see Carman et al., 1996).
This model provides values based on the total TP-inventory in the entire area below the
theoretical wave base and below the average halocline down to 10 cm of sediments. The
biologically passive sediments below 10 cm are expected to have a TP-concentration of about
0.45 in the Baltic Proper (Jonsson et al., 1990) and this value is also used in this modeling for
the Gulf of Finland. This means that only a minor part (reflecting the difference between the
calculated value of 0.63 and 0.45) of the phosphorus in the accumulation area sediments in
the DW-zone could be available for diffusive transport from these sediments. The diffusion
rate depends on the redox-conditions in the sediments, which depend on the calculated
sedimentation of matter. The average values for total sedimentation calculated by the model is
about between 0.7 and 1.5 mm/yr in the MW-layer and less than 1 mm/yr in the DW-layer or
between 4 and 131 µg/cm2·d on the accumulation areas. The predicted water content (W) of
the accumulation area sediments (0-10 cm) is 75% ww, the organic content (loss on ignition,
IG) 6.3 %dw and the bulk density (d) 1.17 g/cm3. Table 7 also gives modeled values for the
dissolved fraction in the three layers and these values vary between 0.8 and 0.99 in the DW-
zone, between 0.64 and 0.98 in the MW-layer and between 0.22 and 0.64 in the SW-layer.
It should also be stressed that land uplift (FLU) is a very important individual input of TP
to the system (18000 t/yr).
It is interesting to note the difference between fluxes and amounts (compare the results in
table 6 with the data in table 8). The largest TP-fluxes are to and from biota with short
turnover times, but the total TP-inventory in biota with short turnover times is only between 1
and 5 kt (on a monthly basis). By far most TP is found in the accumulation area sediments in
the MW-zone (about 590 kt), and a significant part of this is potentially available for
diffusion.

3.3. Changes in the Gulf of Finland during the Last 100 Years

Figure 1 shows measured Secchi depths from the Gulf of Finland during the last 100
years and table 9 gives selected results from statistical analyses of the data. One can note that:

1. The changes in Secchi depth are small and/or not statistically significant for the
periods between 1900 to 1945 and 1980 to 19991.
2. The most pronounced changes in terms of significance and slope of regression line
appears for the data from 1920 to 1980.
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 319

Table 6. A ranking of the annual fluxes (t/yr), as calculated using the CoastMab-model
from the monthly fluxes (t/month) of TP to, in and from the Gulf of Finland.
The key fluxes for remedial measures are bolded. F = flux, SW = surface water,
MW = middle water, DW = deep water, GF = Gulf of Finland, BP = Baltic
Proper, trib = tributary, d = diffusive flux, x = mixing flux, LU = land uplift, ET =
erosion and transport areas, A = accumulation areas, BS = biota with short turnover
times, BL = biota with long turnover times, bur = burial

Month 1 2 3 4 5 6 7 8 9 10 11 12 Annual
FTPbioupBS 33010 42102 56886 57493 49979 38693 37909 37807 38434 54519 40518 17391 504740
FTPbioretBS 31491 41569 54658 56791 49823 39015 37506 37506 38036 52083 41010 16860 496349
FTPMWAMW 2798 2620 2641 2461 2281 2174 2371 2240 2189 3040 1350 1832 27998
FTPETSW 2549 2464 2335 2300 2351 2840 2793 3060 3209 376 351 2941 27568
FTPSWGFBP 1569 1642 1718 1773 1800 1872 1958 1923 1926 1813 1606 1494 21094
FTPSWET 1694 1487 1031 1116 1412 1795 1982 2106 2120 1676 1751 2302 20472
FTPLU 1535 1535 1535 1536 1536 1537 1537 1538 1538 1538 1536 1535 18438
FTPburAMW 1420 1398 1379 1369 1365 1343 1326 1341 1343 1364 1410 1448 16507
FTPETMW 1344 1300 1232 1213 1240 1498 1473 1614 1693 198 185 1551 14540
FTPSWBPGF 1036 1153 1238 1352 1449 1381 1303 1292 1126 959 818 880 13987
FTPSWMW 988 867 601 650 823 1046 1155 1228 1236 977 1021 1342 11933
FTPMWSWx 965 920 857 831 870 1083 1134 1297 1522 172 125 1018 10792
FTPAMWMWd 1021 1253 1187 1040 878 754 717 762 732 976 942 488 10748
FTPDWGFBP 917 949 933 936 915 815 774 872 892 932 909 856 10700
FTPDWBPGF 752 743 730 742 745 678 647 723 742 753 754 765 8775
FTPMWDW 790 740 746 695 644 614 670 632 618 858 381 517 7905
FTPSWMWx 473 477 463 493 551 710 736 820 933 93 64 522 6336
FTPtrib 361 414 486 417 400 774 948 526 416 355 349 288 5735
FTPMWSWd 666 497 354 217 196 260 362 450 517 628 677 751 5574
FTPbioupBL 234 331 460 511 472 379 358 354 356 445 316 116 4331
FTPbioretBL 295 309 330 365 388 388 381 373 365 357 352 310 4212
FTPDWMWd 313 374 381 379 359 339 337 322 307 431 373 213 4128
FTPMWBPGF 358 345 334 335 339 314 302 338 356 368 366 367 4123
FTPburADW 107 105 104 103 103 101 100 101 101 103 106 109 1245
FTPDWADW 113 113 120 121 117 117 110 118 120 6 5 120 1180
FTPprec 7.3 7.3 7.3 7.3 7.3 7.3 7.3 7.3 7.3 7.3 7.3 7.3 88
FTPADWDWd 0.9 0.9 1.0 1.0 0.9 1.0 0.9 1.0 1.0 0.2 0.2 1.0 10

Table 10 gives a statistical compilation of data (mean values, medians, standard

deviations, coefficients of variation and number of data) for three interesting periods, 1900-
1920, 1920-1980 and 1980-1991. One should note the high CV-values (about 0.35) and that
the mean Secchi depths have decreased from 7.1 to 4.8 m. This is a significant change
influencing the entire ecosystem since it influences the depth of the photic zone and the
benthic production, which is highly dependent of water clarity. If there are major changes in
primary phytoplankton and benthic algae production, one should also expect major changes in
secondary production (of zooplankton, zoobenthos and fish). To discuss such changes is
outside the scope of this paper, but such changes will be addressed in a coming paper using
the CoastWeb-model. The question here is if it is possible to reconstruct the changes in
Secchi depth shown in Figure 1 and tables 9 and 10.
320 Lars Håkanson

Table 7. Compilation of monthly data for modeled TP-concentrations

in A-sediments (in mg/g dw) from the AW and DW-layers, water
content (%ww) and loss on ignition (IG) of A-sediments (%dw), sedimentation
(Sed) in the the MW and DW-layers (cm/yr and µg/cm2·yr), settling velocities
(v) in the three layers (m/month) and dissolved fractions (DF) in the three layers (dim. less).

Month CTPAMW CTPADW W IG SedAMW SedADW SedDW SedMW vSW vMW vDW DFDW DFMW DFSW
1 2.4 0.63 75 6.3 0.14 0.10 113 79 0.61 0.78 2.00 0.83 0.7 0.49
2 2.4 0.63 75 6.3 0.14 0.10 114 83 0.62 0.77 2.03 0.83 0.68 0.64
3 2.4 0.63 75 6.3 0.13 0. 10 106 84 0.62 0.76 2.04 0.82 0.68 0.63
4 2.4 0.63 75 6.3 0.12 0. 10 98 81 0.63 0.75 2.04 0.82 0.68 0.54
5 2.4 0.63 75 6.3 0.13 0. 10 94 82 0.63 0.74 2.02 0.82 0.66 0.40
6 2.4 0.63 75 6.3 0.12 0. 10 102 76 0.63 0.74 2.00 0.83 0.67 0.34
7 2.4 0.63 75 6.3 0.12 0. 10 97 82 0.63 0.74 1.99 0.81 0.67 0.33
8 2.4 0.63 75 6.3 0.16 0. 10 95 83 0.63 0.75 1.99 0.81 0.66 0.33
9 2.4 0.63 75 6.3 0.07 0.01 131 4 0.62 0.75 2.00 0.99 0.98 0.53
10 2.4 0.63 75 6.3 0.24 0.00 58 4 0.60 0.76 2.04 0.99 0.98 0.52
11 2.4 0.63 75 6.3 0.10 0. 10 79 84 0.59 0.77 2.01 0.79 0.64 0.22
12 2.4 0.63 75 6.3 0.15 0. 10 121 78 0.60 0.77 1.98 0.82 0.68 0.41

Table 8. Amounts of TP (1000·t) in the different compartments, i.e.,

accumulation areas in the DW-compartment (ADW), accumulation
areas in the MW-compartment (AMW), the DW-layer, areas of fine
sediment erosion and transport (ET), the MW-layer, the SW-layer, in biota
with long turnover times (BL) and in biota with short turnover times (BS).

Month MTPADW MTPAMW MTPDW MTPET MTPMW MTPSW MTPBL MTPBS

1 44.3 588 1.7 25.9 7.9 16.3 1.2 2.5
2 44.3 588 1.8 25.4 7.5 16.4 1.2 3.2
3 44.3 588 1.8 24.9 7.1 16.1 1.3 4.3
4 44.4 588 1.8 24.3 6.6 16.6 1.5 4.6
5 44.4 588 1.7 23.9 6.5 17.3 1.6 4.2
6 44.4 588 1.7 23.6 6.6 18.3 1.6 3.4
7 44.4 589 1.7 22.7 7.1 19.4 1.6 3.1
8 44.4 589 1.7 22.2 7.4 19.7 1.6 3.1
9 44.4 589 1.7 21.5 7.7 19.8 1.5 3.1
10 44.4 589 1.8 22.4 7.7 17.6 1.5 4.1
11 44.3 588 1.7 25.4 7.3 15.9 1.5 3.4
12 44.3 588 1.6 26.8 7.7 16.6 1.4 1.4

Table 9. Changes in Secchi depths in the Gulf of Finland

during different periods of time

1900-1991
Sec = -0.0025·month + 7.84; r2 = 0.141; n = 738; p < 0.0001
1900-1945
Sec = +0.0005·month + 7.10; r2 = 0.0008; n = 352; p = 0.61; not significant
1945-1991
Sec = -0.0024·month + 7.67; r2 = 0.010; n = 386; p = 0.048
1980-1991
Sec = -0.0068·month + 11.69; r2 = 0.019; n = 60; p = 0.29; not significant
1920-1980
Sec = -0.0031·month + 8.38; r2 = 0.141; n = 555; p < 0.0001
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 321

Table 10. Statistics of Secchi depth measurements from

different periods from the Gulf of Finland

1900-1920 1920-1980 1980-1991

Mean (MV) 7.1 6.3 4.8
Median (M50) 7.0 6.1 4.5
Standard deviation (SD) 2.45 2.2 1.6
Coefficient of variation (CV) 0.35 0.35 0.33
Number of data (n) 123 556 60

Figure 7. Trend analysis of chlorophyll-a changes in the Baltic Proper from 1974 to 2005 for surface-
water samples (based on HELCOM data)

The changes in the Baltic Proper between the years 1974 to 2006 for the chlorophyll-a
concentrations in the SW-layer provide a complementary picture and are shown in Figure 7.
In this period, there is a weak and continuous decline in the chlorophyll values, which
demonstrates that the eutrophication is not getting worse in the Baltic Proper, but rather the
opposite. It is also interesting to note that the individual data in the surface water of the Baltic
Proper cover all trophic classes from oligotrophic to hypertrophic. The median chlorophyll-a
value in the surface-water is at the class limit between mesotrophic and oligotrophic, i.e., at 2
µg Chl/l.
Figure 8 gives chlorophyll data from the Gulf of Finland relative to water depth. All these
data emanate from the SW-layer, as this is defined in this work from the theoretical wave
base. One can see from Figure 8 that there is only a weak correlation between the measured
chlorophyll values and the water depth. This indicates that the SW-zone is relatively well
mixed. That conclusion is supported by the data in Figure 9 showing measured TP-
concentrations in the entire water column. Some important depth intervals are also shown in
this Figure The mean depth of the Gulf of Finland is 36 m, the theoretical wave base is at 41
m and the average depth of the halocline at 75 m. One can see from Figure 9 and from table
11, which gives a statistical compilation of monthly TP-data, that there are important
differences between the three zones discussed in this work (see table 5 for data).
322 Lars Håkanson

Figure 8. Chlorophyll data from the Gulf of Finland (1990-98) collected at different water depths
(based on HELCOM data)

Figure 9. Total phosphorus concentrations in the Gulf of Finland (1990-98) collected at different water
depths (based on HELCOM data)

For the reconstruction of the development in the Gulf of Finland, one can conclude that
(1) there were likely no or only small changes in the nutrient loading and eutrophication in the
Gulf of Finland from 1900 to about 1920, (2) the most significant changes occurred between
1920 and 1980 and (3) after that the system has not changed very much (and there may even
be a slight improvement, at least in the Baltic Proper which would also reflect on the
conditions in the Gulf of Finland).
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 323

Table 11. Statistical compilation (means values, standard deviations and number of
data) of empirical monthly data on TP-concentrations in the three layers (SW, MW and
DW) from the Gulf of Finland (data from HELCOM from 1990 to 1998)

Month SW MW DW
1 MV 34.1 37.7 71.7
SD 11.4 18.2 21.8
n 138 53 7
2 MV 32.2 35.1 43.2
SD 6.7 12.4 20.0
n 286 91 10
3 MV 30.1 33.9 31.3
SD 5.7 10.1 0.0
n 117 45 1
4 MV 30.1 35.6 57.2
SD 7.1 15.5 22.1
n 204 77 12
5 MV 22.5 32.3 47.8
SD 8.5 16.6 16.9
n 149 63 11
6 MV 24.0 40.9 69.2
SD 15.0 18.5 21.2
n 51 22 4
7 MV 16.2 39.1 69.5
SD 7.2 18.3 19.7
n 377 81 12
8 MV 17.5 38.2 50.6
SD 7.8 21.7 25.1
n 846 168 32
9 MV 16.6 39.6 68.0
SD 8.0 23.7 14.6
n 79 37 6
10 MV 16.9 51.5 126.1
SD 9.4 38.3 50.1
n 59 26 4
11 MV 24.2 40.7 47.8
SD 7.6 11.4 8.9
n 282 92 14
12 MV 33.3 54.1 58.6
SD 17.4 24.5 37.5
n 65 30 3

3.4. Reconstruction the Conditions in the Gulf of Finland

The simulations to estimate the changes that have taken place during the last 100 years in
the Gulf of Finland will be presented in two steps. The first step concerns substantial but
realistic reductions of the direct anthropogenic emissions of TP to the Gulf of Finland from
diffuse sources and point sources. The values given by HELCOM (2000) are 2112 t/yr and
2431 t/yr, respectively, and the natural loading is 1191 t/yr. It is not realistic to assume that all
the anthropogenic emissions can be removed, and at the first step, it will be assumed that 40%
of these emissions are eliminated (i.e., 1817 t phosphorus so that the annual loading would be
324 Lars Håkanson

reduced from 5734 to 3917 t TP). In reality, this would require major investments. It would
also take a long time to implement such actions. In the following, it will be assumed these
emissions are suddenly removed (month 31, i.e., in July). The aim is also to demonstrate the
dynamic response of the system to such a sudden change in nutrient loading. At the next step,
it will be assumed that also the conditions in the Baltic Proper will be altered. An overall
budget for nitrogen and phosphorus fluxes to the Baltic Proper (including the Gulf of Riga
and the Gulf of Finland) is given in table 12. On average, the total tributary load of
phosphorus to the Baltic Proper is about 30000 t/yr. Values of the proportion between natural
load, load from diffuse sources and from point source emission for the nutrient to the entire
Baltic Proper are given by HELCOM (2006) and here it will be assumed that in total 7200 t
TP/yr of the total transport of 30000 t TP/yr will be removed. There have been several tests
and the following results mainly concern this particular reduction.

Table 12. Transport of nitrogen and phosphorus to and from the Baltic
Proper (tons/yr). The data from SNV (1993) concern mean values for
the period between 1982 and 1989; the data from HELCOM (2000)
concerns year 2000 (from Håkanson and Lindgren, 2007)

Total-N Total-P
SNV HELCOM HL07 SNV HELCOM HL07
A. From countries
Sweden 44 300 46 636 1780 1219
Baltic states 72 600 145 697 1890 5408
Finland 35 981 1874
Russia 90 229 5863
Poland 109 900 191 521 19 100 12 698
Germany 20 000 20 602 2750 512
Denmark 51 000 27 664 7860 1193
Sum inflow from countries: 297 800 558 046 33 380 28 767
≈ 500 000 ≈ 30 000
B. From processes and water inflow from adjacent basins
Precipitation 289 900 192 400 3420
Nitrogen fixation 130 000
Land uplift 480 000 160 000
Inflow from Kattegat 120 000 14 000
Inflow from Bothnian Sea 340 000 14 000
Sum from processes: 1 261 000 – 1 359 000 191 420
≈ 1 300 000 ≈ 190 000
Total inflow: ≈ 1 800 000 220 000
C. Water outflows to adjacent basins
To the Bothnian Sea 340 000 24 000
To Kattegat 260 000 18 000
Total outflow: ≈ 600 000 40 000
D. Rest terms
Burial in sediments (3·180 000)* = 540 (220 000
000 – 40 000)
= 180 000
Denitrification (1 800 000 - 600 000 –
540 000) = 660 000
* the nitrogen concentration is 3 times higher than the phosphorus concentration in these sediments
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 325

Steady-state results are first shown in table 13. This table gives the predicted values today
for the Secchi depth (mean value = 5.5 m), the monthly maximum concentration of
chlorophyll-a (8.3 µg/l; since the maximum value is of great interest in contexts of algal
blooms), the monthly maximum concentration of cyanobacteria in the SW-layer (86 µg/l), the
mean predicted TP-concentrations in the SW, MW and DW-layers (24.5, 36 and 86 µg/l,
respectively). The second column gives the corresponding steady-state values if 1871 t TP
from the direct tributary inflow to the Gulf of Finland are reduced. Then, the Secchi depth
would be 6.7 m, which is lower than the value 100 years ago (7.1 m, see table 10). So, it is
not enough to reduce anthropogenuous TP-inflow via the rivers to the Gulf of Finland by
40%. If 7200 t TP are removed from the present TP-inflow via rivers to the Baltic Proper
(including 1817 t to the Gulf of Finland), then the requested mean annual Secchi depth of 7.1
m in the Gulf of Finland will be reached and there are also major changes in the chlorophyll-a
concentration and the maximum concentration of cyanobacteria.
Figure 10 shows the dynamic response of the system. In these simulations, 7200 t of TP
to the Baltic Proper (including 1871 t to the Gulf of Finland) have been removed month 31
and the response of the Gulf of Finland is shown for (A) the Secchi depth, (B) chlorophyll
concentrations, (C) cyanobacteria, (E) TP in surface water, (E) TP in surface water in the
Baltic Proper and (F) predicted SPM-concentrations in the SW, MW and DW-layers in the
Gulf of Finland. Whenever possible, this figure are compares the modeled values during the
initial 31 months, corresponding to the conditions prevailing today, to the uncertainty bands
in the empirical data. From Figure 10A, one can see that during the initial period there is a
very good correspondence between the modeled values and the empirical data given by the
uncertainty band related to ± 1 standard deviation of the measured mean Secchi depth. There
is also a good correspondence between measured and modeled values for chlorophyll (Figure
10B) and for TP in the SW-layer in the Gulf of Finland (Figure 10D).
It is interesting to note that under these hypothetical presuppositions (that 7200 t TP
would suddenly be removed month 31), there is an initial phase with a relatively fast recovery
of about 7 years and then a phase with a slow recovery related to the fact that the steady-state
adjustment to changes is very slow for the sediments in the MW and DW-zones (the
accumulation area sediments).

Table 13. How would mean annual Secchi depths, maximum monthly chlorophyll-a
concentrations, maximum concentrations of cyanobacteria and mean annual TP-
concentrations in the three layers (SW, MW and DW) change from today if, first, 1817
tons of TP to the Gulf of Finland and, secondly a total of 7200 tons of TP from river
inflow to the Baltic Proper (including 1817 tons to the Gulf of Finland) were reduced?
The table gives steady-state values

Today 1817 t TP reduced 7200 t TP reduced

from trib. to GF to BP
Mean Secchi (m) 5.5 6.7 7.2
Max. chlorophyll-a (µg/l) 8.3 7.7 7.5
Max. cyanobacteria (µg/l) 86 63 55
Mean TPSW (µg/l) 24.5 21.9 18.7
Mean TPMW (µg/l) 36 32 30
Mean TPDW (µg/l) 86 80 79
326 Lars Håkanson

Figure 10. The dynamic response of the Gulf of Finland if 7200 tons of phosphorus (including 1817
tons from tributaries to the Gulf of Finland) were hypothetically reduced month 31 for (A) Secchi
depth, (B) chlorophyll, (C) cyanobacteria, (D) TP-concentrations in the SW-layer, (E) TP-
concentrations in the SW-layer in the Baltic Proper and (F) concentrations of suspended particulate
matter (SPM) in the SW, MW and DW-layers in the Gulf of Finland. This figure also gives uncertainty
bands for the empirical data (± 1 standard deviation) valid for the initial period (the first 31 months) for
Secchi depth, chlorophyll and TP in the SW-layer in the Gulf of Finland

Reconstruction of Secchi depths in the Gulf of Finland

14
Empirical data (o)
12 Modeled values (x)

10
Secchi M)

0
0 200 400 600 800 1000 1200
Month
1900 1917 1933 1950 1967 1983 2000

Figure 11. Reconstruction of Secchi depths in the Gulf of Finland when 7200 tons of phosphorus
(including 1817 tons from tributaries to the Gulf of Finland) have been reduced between the years from
1920 to 1980 compared to measured data (from HELCOM)
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 327

The reconstruction results are given in Figure 11. The measured data on Secchi depth
(from Figure 1) have been compared to the modeled values, first when there were no changes
in the TP-inflow to the Baltic Proper and the Gulf of Finland in the years 1900 to 1920 (3917
t via tributaries to the Gulf of Finland; 22800 via tributaries to the Baltic Proper including the
tributaries to the Gulf of Finland). Then, in the period 1920 to 1980 7200 t (including 1817 t
from the tributaries to the Gulf of Finland) have successively been reduced (7200/60·12 = 10 t
per month). Finally, the discharges of today have been used in the period from 1980. From
Figure 11, one can see that this will reflect the measured Secchi depths in the Gulf of Finland
quite well. There are several individual Secchi depth measurements higher and lower than the
predicted mean monthly values, but the general correspondence between the measure and the
modeled Secchi depths is good.
This also means that one can run this scenario in the other direction and conclude that if
the present tributary TP-load could be reduced by 7200 t, the Baltic Proper and the Gulf of
Finland would return to the conditions as they were 100 years ago. If the reductions are done
as in Figure 11, it would take 60-70 years to get a new steady-state condition. If the
reductions are implemented slower, it takes longer, and vice versa.

3.5. Sensitivity Tests

In the following sensitivity tests, one variable has been changed (reduced by 50% as
compared to the default situation) and all else in the model kept at the initial default
conditions. The results will be presented for two target variables, the dynamically modeled
TP-concentrations in the SW-layer and the Secchi depths. The first column in table 14 gives
the default conditions (today), the second column the results when the TP-flow from land
uplift has been reduced by 50%. Then, one can note that the modeled TP-concentration would
be 19.8 µg/l, which is significantly lower than the reference value (24.5 µg/l) and also the
empirical mean annual value (24.1 µg/l, see table 5). The Secchi depth would be 7.9 m, which
is markedly higher than the empirical mean value (7.1 m) a hundred years ago.
In the next sensitivity test, the two diffusive TP-fluxes from the sediments (from
accumulation area sediments in the MW and DW-layers) have been reduced by 50%. Since
these diffusive fluxes are relatively small, the changes are not great: annual mean TP has been
reduced from 24.5 to 23.4 µg/l, and the Secchi depth increased from 5.5 to 6 m. Also the
diffuse TP-fluxes in the water have been reduced by 50%, and the results are close to the
results for the diffusive sediment fluxes: mean annual TP has decreased to 23.2 µg/l and the
Secchi depth increased to 6.1 m.
Since it is fairly complicated to calculate the production and biomasses of functional
groups or species of organisms and since most mass-balance models for nutrients would not
do this, it is also interesting to see what would happen of 50% of the biouptake to organisms
with short turnover times would be changed. The results show that this would neither alter the
predicted TP-concentrations very must (from 24.5 to 24.9 µg/l) nor the predicted Secchi
depths (5.5 to 5.4 m). This is also the result if 50% of the biouptake to organisms with long
turnover times are being reduced.
328 Lars Håkanson

Table 14. Steady state results from 8 sensitivity analyses where the influence from (1)
land uplift, (2) diffusion from sediments, (3) diffusion in water, (4) biouptake and
retention in biota with short turnover times and (5) in biota with long turnover times,
(6) the particulate fraction of phosphorus in the deep-water zone, in (7) the middle-
water zone and (8) the surface-water zone were reduced by 50%. This has been
calculated for (A) TP-concentrations (µg/l) and (B) Secchi depths (m)

A. TP-concentrations in the surface-water layer

Month Today Landup. Diff sed Diff wat BioS BioL PFDW PFMW PFSW
1 23.0 18.5 21.8 21.3 23.3 23.3 22.5 23.0 24.3
2 23.9 19.0 22.7 22.4 24.2 24.2 23.4 23.9 24.9
3 24.8 19.6 23.7 23.5 25.2 25.2 24.3 24.8 25.6
4 25.2 20.0 24.1 24.1 25.7 25.7 24.7 25.2 26.1
5 25.6 20.4 24.5 24.5 26.0 26.1 25.1 25.6 26.6
6 26.4 21.1 25.3 25.3 26.8 26.9 25.9 26.4 27.6
7 26.7 21.5 25.7 25.5 27.0 27.2 26.2 26.7 27.9
8 27.0 21.5 25.9 25.7 27.2 27.4 26.4 27.0 28.1
9 25.5 20.7 24.4 24.1 25.8 26.0 25.1 25.5 26.8
10 22.6 19.2 21.4 20.8 23.2 23.3 22.3 22.6 24.0
11 21.1 18.0 19.8 19.2 21.6 21.7 20.8 21.1 22.8
12 22.0 18.1 20.9 20.2 22.3 22.4 21.6 22.1 23.6
MV 24.5 19.8 23.4 23.1 24.9 24.9 24.0 24.5 25.7
B. Secchi depth
1 6.1 8.9 6.7 .0 6.0 6.0 6.4 6.1 5.6
2 5.6 8.3 6.2 6.3 5.5 5.5 5.9 5.6 5.3
3 5.4 8.1 5.8 5.9 5.2 5.3 5.6 5.4 5.1
4 5.3 7.9 5.7 5.7 5.1 5.1 5.5 5.3 5.0
5 4.7 6.9 5.0 5.0 4.5 4.5 4.8 4.7 4.4
6 4.2 6.1 4.5 4.5 4.1 4.1 4.4 4.2 3.9
7 4.6 6.7 4.9 5.0 4.5 4.5 4.8 4.6 4.3
8 4.7 6.8 5.0 5.1 4.6 4.5 4.8 4.7 4.3
9 5.2 7.4 5.6 5.7 5.1 5.0 5.4 5.2 4.8
10 6.4 8.5 7.0 7.4 6.1 6.1 6.5 6.4 5.8
11 7.3 9.6 8.1 8.6 7.0 7.0 7.5 7.3 6.4
12 6.6 9.2 7.2 7.6 6.5 6.4 6.8 6.6 5.9
MV 5.5 7.9 6.0 6.1 5.4 5.3 5.7 5.5 5.1

There are also uncertainties regarding the distribution of phosphorus in dissolved and
particulate forms. Only the dissolved forms can be taken of by biota and only the particulate
forms can settle out due to gravity. If one would first decrease the particulate fraction for
phosphorus in the DW-zone, this could be a reflection of lower oxygen concentrations in the
DW-layer and it would increase the dissolved fraction in the DW-layer, reduce sedimentation
in the DW-layer, increase diffusion to the MW-layer but not influence the TP-concentration
in the SW-layer much since this change would mainly influence relatively small TP-fluxes in
the Gulf of FInland. If the particulate fraction in the MW-layer is reduced by 50%, it would
influence the predicted TP-concentrations in the SW-layer even less and hence also the
 Reconstruction of the Eutrophication in the Gulf of Finland Using a Dynamic… 329

Secchi depth. If, however, the particulate fraction in the SW-layer itself is reduced by 50%,
this would lower the sedimentation more and also increase the predicted TP-concentration
(from 24.5 to 25.7 µg/l) and also decrease the Secchi depth (from 5.5 to 5.1 m).

4. CONCLUDING REMARKS
These results indicate that it is possible to remediate the Gulf of Finland to the conditions
that characterized the system 100 years ago. About 7000 tons of phosphorus must be removed
on an annual basis. This should be done in the most cost-efficient manner so that the largest
fluxes of phosphorus are removed per euro or dollar.
The trophic conditions in the Baltic Proper have varied very little during the last 30 years.
The most marked changes in Secchi depth in the Gulf of Finland took place between 1920
and 1980. Process-based mass-balance models are - categorically - the only tool to quantify
fluxes, concentrations and amounts and to make predictions of how the concentrations would
change in response to reductions in loading.
Evidently, this modeling could and should be expanded and it would be very interesting
to link all major sub-basins of the Baltic Sea into one system of communicating basins. It
would also be interesting to expand such modeling to include also key functional groups (e.g.,
the CoastWeb-model, see Håkanson and Gyllenhammar, 2005). This would imply that it may
be possible to predict how future climate changes would likely influence the structure and
function of the Baltic Sea ecosystem more realistically and holistically. However, those
expansions are certainly outside the scope of this work.

ACKNOWLEDGMENTS
This work has been carried out within the framework of the Thresholds-project, an
integrated EU project coordinated by Prof. Carlos M. Duarte, CSIC-Univ. Illes Balears,
Spain, and I would like to acknowledge the financial support from the EU and to Dan
Lindgren for valuable help and comments concerning the GIS-data, and to Andreas Bryhn for
valuable discussions.

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 333-350 © 2011 Nova Science Publishers, Inc.

Chapter 11

ENVIRONMENTAL MANAGEMENT
AND SUSTAINABLE USE OF
COASTAL LAGOONS ECOSYSTEMS

Rutger de Wit, Behzad Mostajir,

Marc Troussellier and Thang Do Chi
Unité Mixte De Recherche ―Ecosystèmes Lagunaires‖, Université Montpellier 2, Centre
National de la Recherche Scientifique (CNRS), IRD & Ifremer, Montpellier, France

1. INTRODUCTION
This chapter illustrates some of the major issues for the management and use of coastal
lagoons using two examples from the South of France. These are the mesotidal Bassin
d‘Arcachon on the Atlantic coast and the microtidal Etang de Thau on the Mediterranean (see
Figure 1). Oyster-farming is a major use in both lagoons. Coastal lagoons are part of a coastal
landscape and are therefore typical transition zones between the continent and the sea,
characterised by gradients and ecotones. Thus, it is most important to consider the coastal
lagoon ecosystems in the context of the coastal zone and consider their links both with the
ocean as well as with the hinterland. The latter requests a thorough knowledge of the
watershed of the lagoon. Coastal areas, which are commonly defined as the interface or the
transition area between land and sea, are diverse in function, form and dynamics. In general,
these systems are not well defined by strict spatial boundaries and include low lands,
intertidal zones, salt marshes, wetlands, lagoons and their watersheds. From the development
and management point of view, the coastal areas are characterised by the economical
activities that they support and by the impact of these activities on the environment.
Accordingly, the coastal areas are characterised by i) the production of living resources, ii)
highly diverse human uses including urban development, exploitation of sediments, shipping
and harbours, commercial and sport fishing, aquaculture, tourism, and as a receptacle of
industrial and agricultural waste, iii) their role in providing protection against flooding and by
iv) their biodiversity and role in the functioning of the ecosystems at different spatial levels.
334 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

Figure 1. Localisation in France of the Bassin d‘Arcachon (Atlantic coast) and the Etang de Thau
(Mediterranean coast). Below both lagoons are depicted on the same scale (cf bar indicating 10 km

However, biodiversity and ecosystem functioning may be impaired or negatively affected by

economic use of lagoons. Coastal lagoons represent an important natural heritage and are
noticeably important habitats for waterfowl, marine wildlife, algae and halophytic plant
species. The objective of sustainable use of coastal ecosystems, therefore, is to conserve the
natural heritage and guarantee the living resources for future generations and develop
management schemes that allow an acceptable degree of human exploitation that does not
impair the functioning of the ecosystem in the long term.
Population densities are usually very high in coastal areas, which results in a
concentration of economic activities. Thus, the consequences on the natural environment and
on the living resources may be particularly strong, which points out to some extent the
incompatibility between the development process and the ecosystems conservation
requirements. Coastal lagoons were early sites for human settlement and are becoming
increasingly important areas for human economic, social and cultural development. Some
lagoons have disappeared as the consequence of land-reclamation programmes, particularly in
densely populated countries as Japan and in the Netherlands. Tourism started in the 19th
century in some lagoons, with the Bassin d‘Arcachon as a historical example in France. Many
other lagoons, as e.g. in the Languedoc-Roussillon region, were long-time considered as
unattractive as seaside resorts and have been developed for tourism only during the second
half of the 20th century. Tourism has grown into a real industry in Southern Europe, implying
that population densities during holiday periods may exceed local population by several
factors. The urbanisation of these attractive areas has been further reinforced by suburban
developments. Thus, the surroundings of the Etang de Thau and the Bassin d‘Arcachon
increasingly serve as suburban areas for the cities of Montpellier and Bordeaux, respectively.
This has resulted in increasing pressures on these coastal ecosystems and spatial planning and
proactive environmental management are requested for sustainable use. Management schemes
depend on identifying the spatial area that needs to be managed in a coherent way. This is
difficult in the coastal zone, because of the openness of the coastal ecosystems that depend on
 Environmental Management and Sustainable Use of Coastal… 335

their continental watersheds and interact with the coastal sea and because of the traditional
administrative boundaries which often do not follow the natural boundaries. Hence, we first
describe the scientific definition of coastal lagoons. Second we describe some definitions of
operational units which have been proposed from the point of view of the managers and we
pay particular attention to the definitions used in the European Water Framework Directive.

Definitions of Coastal Lagoons, Transitional Waters and Coastal Waters

In 1980, Barnes published a classical book titled ―Coastal Lagoons; the natural history of
a neglected habitat‖. He indicated that in English language (Oxford English Dictionary) the
word ―lagoon‖ allows two meanings, i.e. ―an area of salt or brackish water separated from the
adjacent sea by a low-lying sand or shingle barrier‖, and ―a stretch of water enclosed in a
coral atoll‖. For the latter, French language uses a specific word, i.e. ―lagon‖ as opposed to
―lagune côtière‖ that corresponds to the first definition, i.e. a coastal lagoon. Hence, coastal
lagoon is a typical geomorphological term. We recommend the use of the definition proposed
by Kjerfve (1994, adapted from earlier definitions by Pritchard and Phleger); accordingly,
coastal lagoons are shallow water bodies separated from the ocean by a barrier, connected at
least intermittently to the ocean by one or more restricted inlets, and usually oriented shore-
parallel. Nevertheless, you may find some scientific publications where some coastal lagoons
are actually described as bar-built estuaries (for a discussion see Kjerfve, 1994).
In the socio-historical context of South-western Europe, lagoons are well recognised and
distinguished from estuaries as is shown by the vernacular languages that contain specific
words for the coastal lagoons, their barriers and inlets. Thus, coastal lagoons are named
―laguna‖ in Spanish and Italian, ―lagoa‖ in Portuguese and ―lagune côtière‖ in French.
However, in the Languedoc-Roussillon region in Mediterranean France the coastal lagoons
are called ―Etangs‖, i.e. the Etang de Thau.
For coastal zone management, coastal areas are delimited based on a compromise
between political, administrative, ecological and pragmatic considerations. A general
definition of the coastal zone would include the coastline and the coastal ocean extending for
legal reasons up to the 12 nautical miles (national jurisdiction) or up to the 200 nautical miles
(EEZ: economic exclusive zone) and on the continent to the boundaries of the watershed.
However, such an area is far too wide and too diverse for most management purposes and it is
often better to delimit specific coastal ecosystems as subsystems where the highest levels of
interactions and conflicts are observed. A narrow coastal zone is often sufficient if the
intertidal zone and the coast line have to be managed. However, the watershed of the coastal
ecosystem needs to be considered for the control of water quality, because the coastal
ecosystems are the receptacle for contaminants and nutrients that may cause eutrophication.
The Large Marine Ecosystem concept (LME) (Sherman et al., 1990) should be considered in
case of interactions between the coastal zone and the high sea, as e.g., for migratory species.
The latter support sequential fisheries based on the exploitation of juveniles in lagoons and
estuaries and of the adults off shore.
336 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

BOX 1. TERMINOLOGY INTRODUCED BY THE EUROPEAN

WATER FRAMEWORK DIRECTIVE
The European Water Framework Directive (2000/60/EC of 23 October 2000),
abbreviated as WFD, establishes a new framework for European Community action in the
field of water policy (http://europa.eu.int/comm/environment).
The WFD has introduced new terminology for aquatic systems, according this
terminology coastal lagoons are either classified as Transitional Waters or as Coastal
Waters. According WFD, Transitional Waters are defined as ―Bodies of surface water in
the vicinity of river mouths which are partly saline in character as a result of their
proximity to coastal waters, but, which are substantially influenced by freshwater flows‖.
Therefore, many of the coastal lagoons could be characterised without problems as
Transitional Waters, since most of them receive freshwater inputs. Nonetheless, national
working groups have interpreted the ―substantially influenced by freshwater flows‖ rather
strictly and decided that many lagoons on the Atlantic coast that are even more
substantially influenced by seawater tidal flushing should be considered as ―coastal
waters‖ (http://www.ecowin.org/TICOR/, Bettencourt et al., 2003. The WFD uses a very
complicated bureaucratic definition for Coastal Waters, i.e., ―surface water on the
landward side of a line, every point of which is at a distance of one nautical mile on the
seaward side from the nearest point of the baseline from which the breadth of territorial
waters is measured, extending where appropriate up to the outer limit of transitional
waters‖. To say it in other words, this means that one should first use the coastline as it
has been used for defining the breadth of the territorial waters, and secondly draw an
imaginary line in the coastal sea at one nautical mile distance from this coastline. All
marine saline waters between the coastline and this imaginary line at one nautical mile
distance are unambiguously recognised as coastal waters. However, a problem of
interpretation arises for some bays and lagoons where saline waters may extent inland
from the defined coastline. The Portuguese and French national working groups have thus
classified some of their Atlantic lagoons as coastal waters, while the Italian approach is to
consider these waters on the inland side of the coastline by definition not as coastal
waters. The one nautical mile limitation means that on average about 20 % of the
European coastal ocean with a depth less than 200 m is taken into account as Coastal
Waters in the frame of the WFD Borja (2005).
The term of Transitional Waters has been adopted as an interesting and useful
typology by the scientific community and recently two new scientific journals have been
founded that are dedicated to studies on these ecosystems, which are called Transitional
Waters Bulletin (TWB) and transitional Waters Monographs (TWM), respectively. These
journals have defined the Transitional Waters simply as river mouth ecosystems, lagoons,
coastal lakes and brackish wetlands. No reference was made to the definition in the WFD,
because it was considered that when this definition is taken alone it is actually quite
confusing and becomes clear only when compared with the definition of coastal waters.
 Environmental Management and Sustainable Use of Coastal… 337

Glossary of Terms Provided by the European Environment Agency

We found the multilingual Glossary of terms (http://glossary.eea.eu.int/EEAGlossary)

provided by the European Environment Agency a very helpful on-line tool for looking
after the definitions of the different environmental terms used in the context of European
Environmental Policies and Legislations. The European Environment Agency (EEA) is
located in Copenhague (Denmark) and currently has 31 member countries, which include
all the 27 member states of the European Union as well as Turkey, Iceland, Norway and
Liechtenstein. Its main task is task is to provide decision-makers with the information
needed for making sound and effective policies to protect the environment and support
sustainable development. The Agency also ensures this information is available to the
general public through its publications and website (http://www.eea.eu.int/ ).

The European Water Framework Directive has introduced a specific typology (see Box
1). Accordingly, the transitional waters include both the majority of the lagoons as well as
the estuaries and river deltas. The coastal waters have been limited on the seaside by a
baseline that is located at one nautical mile distance from the coastline. Within the frame of
implementation of the WFD, the coastal lagoons on the Mediterranean shore in Languedoc-
Roussillon, including the Etang de Thau, are all considered transitional waters, while the
mesotidal lagoons on the Atlantic as Ria Formosa (Faro, Portugal) and the Bassin d‘Arcachon
(S.W. France) are being considered as coastal waters (see Box. 1).

2. ECOLOGICAL AND ECONOMICAL IMPORTANCE OF

THE COASTAL LAGOONS; ENVIRONMENTAL
ISSUES AND CONFLICTS
Coastal lagoons were originally clear water systems, characterised by the presence of
extensive seagrass meadows. Seagrasses are rooted phanerogamms and flowering plants
(Magnioliophyta) that belong to the Zosteraceae, Potamogetonaceae and Ruppiaceae families.
In the mesotidal Bassin d‘Arcachon (Atlantic coast of France) 30,000 to 45,000 brent geese
(Brenta bernicla bernicla) overwinter, which represent 10 to 20 % of the world population of
this species. These species use the seagrass Zostera noltii as their food source.
Primary production rates of seagrass communities range from 0.2 to 1.5 kg C m-2 yr-1,
which are higher than most coastal phytoplankton but lower than most salt marshes (Valiela,
1995). Nonetheless, over the last decades, many of these coastal lagoons in Western Europe
have suffered dramatic losses of their seagrass populations. The loss of the seagrass
communities has been related to increasing eutrophication (De Wit et al., 2001 and references
cited therein). The replacement of the seagrass communities by floating algae or dense
phytoplankton blooms has often occurred suddenly and the change can be characterised as a
drastic shift. This shows that while seagrass communities have some inbuilt resistance
towards change at low forcing levels when these are exceeded, dramatic non-linear changes
occur. The ROBUST project, a EU research programme that run from 1996-2000 (De Wit et
338 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

al., 2001) has focused on the study of mechanisms that provide these inherent resistances,
which have been invoked as buffering capacities (Box 3).
Coastal lagoons and estuaries are ecosystems that play a major role in the life cycles of
economically important finfish and shellfish species by providing feeding, spawning grounds,
breeding, and nursery habitat. For example, over 90 percent of all fish caught in the Gulf of
Mexico are reported to be estuarine dependant to some degree. Many of these ecosystems
have been exploited for aquaculture e.g. oyster farming is the main aquaculture both in the
non-tidal Etang de Thau (Mediterranean coast of France) and in the Bassin d‘Arcachon
(Box 2).
Oysters are filter-feeding organisms that consume phytoplankton, bacteria and detritus
from the water column. Therefore, the aquaculture in the lagoon is particularly sensitive to
environmental quality as a degradation of the habitat and inappropriate food will result in low
quality products. Hence, by accumulating micro-organisms, viruses, heavy metals and
persistent organic pollutants from the water column shell fish farming may present a risk
factor for human health.
A major source of degradation of estuaries and lagoons is their continued use as pollutant
discharge areas. Besides the outright fish kills and other dramatic effects, pollution causes
pervasive and continuous degradation, shown by the gradual disappearance of fish, shellfish,
and waterfowl and of plant and algal species, as well as by a general decline in the natural
carrying capacity of the system. The most likely sources of pollution are agricultural and
industrial chemical and organic wastes. Such contaminants tend to accumulate in coastal
lagoons due to long residence times and restricted water exchange. Above certain threshold
concentrations these create a hostile environment that drives away fish, prevents shellfish
from reproducing or undermines the food chain (Clark, 1992). Tributyltin (TBT) is a specific
tin (Sn)-containing persistent organic pollutant that has been used as an anti-fouling paint in
shipping. As early as 1975, repeated severe disturbances were observed in the Crassostrea
gigas oyster farms of the Bassin d‘Arcachon, which were attributed to TBT. As a
precautionary principle, the use of TBT for ships of less than 15 m has been banned in France
since 1982. Since then it has been shown that TBT is extremely toxic for marine animals in
general and for gastropods and bivalves in particular (Alzieu, 2000). Alteration in the
functioning of coastal lagoons as e.g. the algal blooms in the Mediterranea, in the Carribean,
in the North Sea, Western Pacific and other areas are often linked to the pollution and
eutrofication and its consequences are of sanitary concern as well as for the food safety. In the
Thau lagoon (Southern France) bacterial contaminants are the major environmental and
sanitary issue (see below) as this area is supporting the main shellfish farming production of
the French Mediterranea.
The proliferation of human and animal pathogens in coastal lagoons needs to be
prevented, particularly for sanitary reasons in those environments where fish and shellfish are
farmed and/or harvested. Within the EU shellfish farming and shellfish harvesting areas are
classified depending on the degree of faecal pollution, which is based on the monitoring of
the gut-bacterium Escherichia coli. The highest quality, i.e. sanitary class A requires that
 Environmental Management and Sustainable Use of Coastal… 339

BOX 2. LIFE-CYCLE OF THE JAPANESE OYSTERS

CRASSOSTREA GIGAS, WHICH ARE FARMED IN THE
BASSIN D‟ARCACHON AND THE ETANG DE THAU

Figure 2. Life cycle of Japanese oysters Crassostrea gigas (Thunberg, 1793)

Both in the Bassin d‘Arcachon and in the Etang de Thau, nowadays Japanese oysters
Crassostrea gigas (Thunberg, 1793) are the main oyster species used for oyster farming.
In the Etang de Thau, most often oysters of small size are imported from other regions in
France. These small oysters are cemented to a rope and immerged into the microtidal
lagoon in places where water depths is about 5 to 8 m. These small oysters are grown to
adult sizes (6 – 12 cm) in about 1.5 year and show high growth rates because of high
water temperatures and quite eutrophic conditions in the Etang de Thau. In the mesotidal
Bassin d‘Arcachon, traditionally since the mid 19th century oysters have been cultured
directly on the intertidal mudflats. To facilitate the harvesting, nowadays, the oysters are
often grown in bags of black plastic mesh that are placed as trays on metallic supports
some 10-20 cm above the surface of the tidal flat. The conditions in the Bassin
d‘Arcachon are particularly favourable for the reproduction of the oysters. The oyster
farmers exploit these favourable conditions and many of them have specialised on
capturing the larvae from the water column by facilitating the settlement on artificial
structures and growing them subsequently in about 8 months into juvenile oysters (3-4
cm), a size suitable for exportation to the other oyster farming regions in France. This
technique called ―captage‖ in French was developed in the 1860‘s by the naturalist Costes
and the mason Michelet who designed the collectors comprising tiles coated with a
340 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

mixture of chalk and sand. These collectors are placed along the intertidal channels and
have proven particularly good in facilitating the settlement of the larvae. To understand
and manage this process, knowledge of the life-cycle of the oysters is essential. The
Japanese oysters are hermaphrodites showing irregular sexuality. This means that the
sexually mature individuals are either male or female, but can change gender in between
reproductive seasons. There is a certain tendency to protandry, which means that younger
individuals are males and become females later in their lives. Sexual differentiation takes
place in autumn. They have simple reproductive systems consisting of gonads where the
gamets are formed. Gametogenesis becomes very active in March and April and sexual
maturity reaches its optimum between May and July. The outer part of the gonads become
creamy-white and very rich in lipids, in vernacular language the local people say that
oysters have become ―laiteuses‖ i.e. creamy-milky. Spawning, i.e. the release of the
gametes into the water column is induced by temperature (requiring temperatures > 22.5
°C) and other physical-chemical factors, and takes place in the Bassin d‘Arcachon from
early June to mid September. A fertilised oocyte develops within 24 h through different
developmental stages into a D-hinged larvae of 50-100 µm size, provided that the water
temperature is between 22 and 24 °C. It owns its name to its typical shape resembling the
letter D. The concentration of larvae in the water column during the summer periods
ranges from 100 – 500,000 ind. m-3. The larvae mainly feed on bacteria, small uni-cellular
phytoplankton, so-called pico-phytoplancton < 3 µm and nano-phytoplancton < 20 µm
and enter in competition with other zooplancton. In 15-18 days the larvae grow in size to
about 250 µM and develop an appendix (pediveliger larvae). This is the last stage of the
pelagic phase of the life cycle. The pediveliger larvae is cable to settle on hard surfaces
and the appendix is involved in motility and finally in cementing the oyster on the surface.
Thereafter, the oyster larvae metamorphose and start making their shells. In Arcachon this
phenomenon is facilitated by introducing the characteristic collectors developed in the mid
19th century. The juveniles growing on the tiles are called ―naissain‖ in vernacular
language. These need to be thinned regularly to avoid intraspecific competition and are
thus grown for a 8 month period to a size of about 3-4 cm. These juveniles are used for
growth on the intertidal flats in the lagoon or exported to other regions (transportation in
refrigerated trucks). It has been estimated that 60 to 70 % of the oyster production in
France is raised from the juveniles grown in the Bassin d‘Arcachon. Therefore, a high
success of capturing larvae on the collectors is most important for the local aquaculture
economy as well as for the well-being of entire oyster farming branch in France. Success
rate is variable in between years. After a particularly bad year was 1998, when the number
of metamorphosed larvae settled on the collectors was below 50 per tile, while in normal
years it ranges from several hundreds to 20,000. This raised a lot of concern in this
economic branch and IFREMER, the French Institute for the study and exploitation of the
Sea, was asked to perform a specific study to find out whether the low success rate was
due to natural variability or caused by structurally changed environmental factors and a
final report was delivered in 2004 (Auby and Maurer, 2004). Auby, Maurer and their
coworkers checked several hypothetical possibilities and developed a study comprising
both the factors determining the health status of adult oysters as well as the aquatic
ecology of the system to understand the survival rate of veliger larvae. Although, it could
not be fully excluded that there was some negative effect of organic pollutants from
agriculture and maritime activities (i.e. anti-fouling paints as TBT and Cu-containing
 Environmental Management and Sustainable Use of Coastal… 341

organics) it was concluded that most of the variation of reproductive success of oysters
was explained by food availability in spring (the intensity of the spring phytoplankton
blooms expressed as chlorophyll concentrations) and of the temperature during the
summer period of spawning and veliger larvae development (Auby and Maurer, 2004).
The juvenile and adult oysters are filter feeders, which potentially consume a variety of
species of phytoplankton, bacteria, detritus and viruses from the surrounding water. The
adult oysters may filter up to 10 L of water per hour and they perform best when their diet
comprises diatoms and chrysophytes.

100% of shell samples contain less than 230 Echerichia coli per 100 g of shellfish flesh.
Sanitary class B requires that 90% of shell samples contain less than 4600 E. coli per 100 g
of shellfish flesh and the remaining 10% less than 46,000 E. coli per 100 g of shellfish flesh..
Class A can be sold directly for consumption. For class B, self-purification (depuration) in
tanks of clean seawater is requested. Because of recurrent problems with water quality in the
Etang de Thau due to fecal polution, this lagoon has been classified as B-quality for oyster
farming activities. In addition, phytoplankton communities need to be monitored to check for
possible occurrence of toxic algae. Although it remains sometimes enigmatic what are the
factors that trigger the occurrence of the so-called harmful algal blooms; it is without doubt
that human pressure has increased the importance of this phenomenon.
A major objective of the European Water Framework Directive (WFD – see Box 1) is to
achieve good ecological status for all the European waters in 2015. Hence, the WFD can be a
very good policy aim to achieve the good water quality requested for sustaining the use of
coastal lagoons in the long term. However, WFD is much more ambituous in scope than the
abovementioned policies aiming at protecting the human populations against consumption of
unhealthy fisheries and aquaculture products. Therefore, WFD request a more elaborate
assesment scheme for describing the ecological status (see chapter 2) than provided by the
sanitary classes mentioned before. Monitoring based on use of ecological indicators is
therefore an essential methodology. So far (2006), the EU countries have not yet fully
approved the indicators that should be used for assessing the ecological status of transitional
and coastal waters. Therefore, some basic scientific research is still needed to understand the
meaning of the different indicators and finally the application and interpretation needs to be
homogenised among the member states by an intercallibration excercise. Nonetheless, the
monitoring programme of coastal lagoons in the Languedoc-Roussillon region is a very good
example of how policies in the regions and counties of the E.U. are currently providing the
tools for the implementation of the WFD. For the Bassin d‘Arcachon the implementation of
criteria for WFD are still preliminary (see Box 1). At the local level it is realised that all
measurements aimed at improving the water quality in the Etang de Thau will also allow to
decrease the faecal pollution and finally allow to class this environment as A for shellfish
farming. Such a classification has an immediate impact on the commercial value of the
oysters and therefore, policies to improve water quality receive strong support from the
shellfish farming branch and a ―réconquête‖ of class A classification is now a strong political
objective in the Région Languedoc-Rousillon. The Bassin d‘Arcachon lagoon is favourable
for the reproduction of oysters and the oyster farming branch has taken advantage of this
phenomenon to specialise in breeding the juveniles for other oyster-farming regions (see Box
2). For example, 1998 was a particularly bad year for the reproduction of the oysters. This
342 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

raised a lot of public concern and environmental degradation was invoked as a possible
explanation (see Box 2). Thus, water quality management is paramount in the context of
environmental management for sustainable use. However, this needs to be completed with
sustained action to ensure the conservation of different habitats or to allow for the
development of ecological potential. This combined approach is the objective of WFD and in
this chapter we will focus on the different aspects.
Primary producer communities have been particularly proposed for elaborating
ecological evaluation index (Orfanidis et al., 2003). This is based on the observation that
ecosystem shifts can be evaluated from primary producer communities (see above cf. Figure
2, De Wit et al., 2001 and references cited therein). Accordingly, all seagrasses and a
selection of seaweeds were considered as indicators for the pristine ecological status, while
opportunistic algae mainly those including with sheet-like (e.g. Ulva and Monostroma spp.)
and filamentous thalli, were considered as indicative of a degraded environmental status. The
monitoring programme of coastal lagoons in the Languedoc-Roussillon region (S. France),
which is coordinated by Ifremer, Sète and includes the Etang de Thau, uses a combination of
different characteristics to classify the ecological status of the lagoons (website:
http://rsl.cepralmar.com/intro_01.html in French). In addition to primary producers
(macrophytes and phytoplankton), this programme takes into account the biogeochemistry of
the sediments, physicochemical features of the water column and macrofaunal assemblages.
Accordingly, most of the Etang de Thau including those where are located the oysterparks has
been classified as moderate and a small part in the center as good.

3. WATER FLOWS IN COASTAL LAGOONS

AND MANAGEMENT OF THE WATERSHED

The marine connection between the coastal lagoon is maintained by inlets or tidal
channels, which are called grau on the Mediterranean coast and les passes for the Bassin
d‘Arcachon. The Etang de Thau is connected to the sea by the canal of Sète (90% of
exchanges) and by the Grau de Pisse Saumes (10% of exchanges), located in the northern and
southern parts, respectively (see Figure 1). Tidal movements of the coastal sea will propagate
through the tidal channels into the lagoon. Tidal amplitude has been used to characterize
coastal lagoons viz. macrotidal lagoons have a tidal range between 4 and 6 m, while
mesotidal and microtidal lagoons have amplitudes ranging between 2-4 and 0-2 m,
respectively. The Bassin d‘Arcachon is a mesotidal lagoon (mean tidal range 3 m) and the
Etang de Thau is microtidal, but considered as ―non-tidal‖ in the frame of the WFD, because
the tidal difference is less than 0.25 m. In the Mediterranean, microtidal lagoons, with a tidal
range close to 1 m, are only found in the North Adriatic. Flushing is the process by which a
certain volume of water leaves the lagoon and is replaced by water from another source. Tidal
flushing is the predominant flushing mechanism in the Bassin d‘Arcachon. However, flushing
can also be induced by other mechanisms as for example it can be driven by wind or the
consequence of freshwater inputs from the catchment. Understanding of flushing phenomena
together with the knowledge of what is delivered to the lagoon from the watershed is most
essential for water quality management in coastal lagoons. A first practical approach is
provided by the Land Ocean Interaction in Coastal Zone (LOICZ) procedure. However,
 Environmental Management and Sustainable Use of Coastal… 343

coastal lagoons do not behave as continuously stirred homogeneous reactors and the extent of
freshwater inputs and flushing phenomena are very variable in space and in time. Therefore, a
more detailed knowledge of water movements and dilution of water masses requires detailed
hydrodynamic modelling. Detailed 3-D hydrodynamic models do exist for the Etang de Thau
(MARS 3D) and have recently been developed for the Bassin d‘Arcachon.
Due to these heterogeneities, the distribution of nutrient loading from the watershed into
the Bassin d‘Arcachon is very different due to hydrodynamics and accordingly three
hydrological sectors have been distinguished. The W sector and the center of the lagoon are
most strongly influenced by tidal flushing. The SE sector of the lagoon directly receives the
highest nutrient loadings and is characterised by relatively long residence times (up to 3
weeks) and therefore most prone to eutrophication phenomena. Indeed this sector was
characterised by dense blooming of the macroalga Monostroma obscurum in 1992 and 1993.
This macroalgae is notoriously nitrophilous (nitrogen loving), which reflects that since the
end of the 1970‘s the N/P ratio has strongly deviated from the Redfield ratio in favour of N.
Nowadays, total nitrogen inputs into the lagoon fluctuate among years corresponding to
average loadings of 60 to 120 kg N ha-1 year-1. The 3000 km2 watershed of the Bassin
d’Arcachon is dominated by sand soils of pleistocene origin which are typical for the Les
Landes system. The average slope is as low as 0.25 % and land-use is dominated by forestry
(84 % of the surface), mainly pine trees. While intensive agriculture occupies only 11 % of
the surface in the watershed, this activity contributes more than 65 % of the nitrogen input
into the lagoon. In total ninety percent of the nitrogen input into the lagoon comes from
runoff, while 9 % corresponds to atmospheric deposition and about 1 % enters through
ground water flow. Agricultural inputs are dominated by nitrate (90 % of total nitrogen),
while forestry releases mainly organic nitrogen (70 % of total nitrogen). Nitrogen abatement
is very low in the surface fresh water systems, because of short residence times, and low
aquatic primary production due to acidity and humic substances of the water. In contrast, the
freatic environment has the capacity to denitrify provided that organic matter input is
sufficient. Hence, nitrogen abatement has been observed in waterlogged sand soils in buffer
zones surrounding some of the agricultural areas (De Wit et al., 2005). In conclusion, this
watershed is extremely sensitive to land use changes. Therefore, local policies have arrested
the increase of agricultural area for the time-being, since it can be expected that an increase in
agricultural surface will proportionally increase the N-loading to the lagoon thus increasing
risk of eutrophication.
One hundred percent of the urban wastewater from the entire urban zone encircling the
Bassin d‘Arcachon is nowadays collected in a collectively operated wastewater collection
system and directly diverted to the open ocean after treatment. Thus, household and industrial
wastewater from this zone stopped contributing to contamination and nutrient loading of the
lagoon since the early 1980‘s. In the remaining rural area (6,000 inhabitants) wastewater is
treated in different autonomous wastewater treatment plants, which constitute point sources of
N and P and faecal bacteria in the watershed. The wastewater treatment resulted in a strong
reduction both of the phosphorus loadings and of the faecal contamination. Until 2002, there
were no problems with faecal contaminations in the Bassin d‘Arcachon, but in 2003 higher
levels were detected and the Bassin d‘Arcachon was even provisionally placed in category B
for shellfish farming. In contrast to P, N delivery was not significantly reduced after the
introduction of urban wastewater collection and treatment around the lagoon, because it
mostly comes from agricultural diffuse sources. This resulted in an increase of the N/P ratio
344 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

since the end of the 1970‘s largely above the Redfield ratio. Such phenomena favour the
proliferation of nitrophilous (nitrogen loving) algae and could induce a shift towards
phosphorus limitation of primary production. However, sediments may present a significant
source of P and therefore exchanges of nutrients along the sediment water interface need to be
studied in concert with the direct nutrient loading from the tributaries to characterise the
limiting nutrients for primary productivity (see Box 3).
The watershed of the Etang de Thau is about 280 km2. It is drained by numerous small
streams which flows are intermittent due to the Mediterranean climate. The geology of this
watershed is very contrasted: the northeast is mainly formed by karstic limestone while clay
marls dominate the southwest. Land use in the watershed is mainly agriculture (vineyards).
There are also industrial activities (agro-food and fertilizer industries) and increasing
urbanisation. Approximately 80,000 people live around the lagoon, half of them in the town
of Sète. However the population doubles during the summer. A strong demographic increase
is still expected for the coming years, because this area develops as a suburban area for
Montpellier. The urban wastewater is treated in different autonomous wastewater treatment
plants, which constitute point sources of N and P and faecal bacteria in the watershed. Within
the frame of the E.U. project DITTY a Decision Support System has been developed
(http://www.dittyproject.org/etangDeThauPresentation.asp) to determine how investments
can be optimized to get the highest increase in environmental quality. These are based on
confronting the loss of income due to insufficient quality of oysters with the costs of
improving the waste water treatment plants and finding their optimal locations.

4. IMPORTANCE OF INTERNAL PROCESSES IN THE

LAGOON FOR MAINTAINING WATER QUALITY
AND FOR PROVIDING HABITATS

Figure 3 compares the link between primary producer communities in coastal lagoons
with their impact on biogeochemical cycling and water quality. Rooted phanerogamms are
perennials with slow growth rates. The growth rates peak during spring and early summer and
the plants form continuously new leaves during that period. Some of the older leaves are
shed, but before these are shed from the plants such leaves are impoverished in elements like
N and P by translocation processes. Therefore, degradation of such leaves in the environment
are slow. Standing biomass varies between 100 and to 200-400 g DW m-2 in winter and
summer, respectively, with Ruppia attaining higher biomass densities than Zostera noltii (De
Wit et al., 2001). Moreover, about half of the biomass of the plants occurs belowground as
rhizomes and roots. The rhizosphere of these plants is an area of intense microbial activities
showing important plant-microbe interactions. In the Bassin d‘Arcachon, nitrogen fixing
bacteria are present in the rhizosphere, which seems to indicate an plant-microbe association
particularly well adapted to N- deficient environments (De Wit et al, 2001 and references
cited therein). Oxygen is released from these roots, which contributes to oxidation of the
sediment. The moribund parts of the root system are an additional input of organic matter to
the sediments, which occurs at depth. Due to the autotrophy of the plants, oxygen release
 Environmental Management and Sustainable Use of Coastal… 345

Rooted Floating macroalgae Planktonic microalgae

Phanerogamms and cyanobacteria
oxic
high water column
transparencies well mixed

fluctuating O2
decomposing
anoxic thalli

PO4 3- sequestered HS-, NH4+, organic N, PO4 3-

in the sediment HS-, NH4+, organic N, PO4 3-
sediment oxygenation
from roots

perennial life cycle seasonal life cycle short generation times

low growth rates high growth rates high growth rates

high biodiversity low biodiversity low biodiversity

shelter habitats for meiofauna
high pulsed input of OM high pulsed input of OM
deep regular input OM at the sediment surface at the sediment surface
sulfate reduction - trapping sulfate reduction sulfate reduction
of sulfide with iron

Figure 3. Different communities of primary producers in coastal lagoons and their differential impacts
on biogeochemical cycling and on water quality

from their root systems, the fact that half of the dead plant debris into the sediment is at depth
and because of the nature of the plant debris, the surface sediments remain well oxidised. As a
result, PO43-, HS- and NH4+ do not diffuse out of the sediment (see Box. 3). The highly
structured plant canopies therefore have a strong positive impact on ecosystem functioning
and can be considered as ecosystem engineers. They also create shelter habitats for meiofauna
and small gastropods and thus contribute to maintaining high biodiversity.
Floating macroalgae with sheet-like (e.g. Ulva and Monostroma spp.) and filamentous
thalli (e.g. Enteromorpha clathrata) are capable of high specific growth rates and often show
a clear seasonal dynamics. Thus for Ulva and Monostroma spp., growth rates are high during
the end of the winter and in spring and as a result standing biomass may built up to values of
1,000 g DW m-2 or higher. In contrast to the phanerogamms, all their biomass is suspended in
the water column or deposited at the sediment surface at low tides in intertidal areas. Within
such dense beds extreme variations of oxygen occur during day and night time. Selfshading
may become important and algae that are at the bottom may start to die off resulting in
hypoxic or anoxic conditions in the lower part of the bed. This process finally provokes the
death of the macroalgae and massive consumption of oxygen leading to a dystrophic crisis
(see Box 3). The dead material settles on the top of the sediment surface. Therefore, microbial
degradation processes are particularly intense in the surficial layers. This may result in
diffusive transfer of PO43-, Mn2+, HS- and NH4+ from the sediment into the water column (see
Box 3) with both toxic effects on biota (Mn2+, HS- and NH4+ ) as well as enhanced
remobilisation of N and P (PO43-, and NH4+, respectively) for growth of primary producers.
That latter phenomenon is an example of positive feedback which reinforces the maintenance
of the macroalgal state of the ecosystem and makes a move (back) to the phanerogamm
dominated state less likely. In addition, macroalgal dominated systems generally seem to have
a lower biodiversity than the rooted phanerogamm dominated system, although this is not
always the case.
346 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

BOX 3. ROLE OF SEDIMENT PROCESSES

AND RISKS OF DYSTROPHIC CRISES

The sediments are an important biogeochemical compartment in coastal lagoons.

Densities of microbes within sediments exceed the densities of pelagic (water column)
microbes by orders of magnitude (i.e., typically 104). The organic matter inputs into
lagoons and organic matter production in coastal lagoons is reminerilised mainly within
the sediment compartment. This creates a high oxygen demand for the sediment, which
drives a flux of oxygen from the water column to the sediment. Muddy sediments are
almost impermeable, meaning that interstitial water does not move. Hence, soluble
compounds, like dissolved oxygen, are transported by molecular diffusion only, which is a
slow process. In contrast, sandy sediments are permeable and the interstitial water can
move through the pores when it is forced by hydrodynamic pumping. This creates a
convective movement in the sediment. In these systems the dissolved compounds are
transported both by molecular difusion and by the convective currents, the latter may
enhance the transport rates by orders of magnitude. At a certain depth in the sediment, the
delivery of oxygen is insufficient to supply the oxygen for mineralization processes and
the sediment becomes anoxic. In the muddy sediments of the Etang de Thau and the
Bassin d‘Arcachon, oxygen penetration depths, which have been measured with oxygen
micro-electrodes, typically ranges from 1 mm to 4 mm depth. A suite of compounds
including NO3-, Fe3+, MnO2, SO42- and CO2 can be used as electron acceptors for bacterial
mineralization as an alternative for oxygen, which are reduced to N2 or NH4+, Fe2+, Mn2+,
HS- and CH4, respectively. Because sulfate concentrations are very high in marine systems
(i.e. 28 mM at 37 salinity), the process of sulfate reduction (see Figure 4) is quantitatively
very important and may represent 50 % or more of the total organic carbon
remineralisation. The reduced compounds NH4+, Mn2+, and HS- are noxious for most of
the water colum biota and their efflux into the water column is therefore undesirable. A
high efflux of HS- and H2S into the water column will create a so-called dystrophic crisis
that is characterised by fish and mollusc mortality. Fortunately, under balanced conditions,
these reduced compounds are oxidised in the superficial layers of the sediments. Such
balanced conditions are typical for the phanerogamm beds due to a combination of factors
(see Figure 3). First of all, growth of phanerogamms is slow and more spread out in time
than the seasonal growth of the nitrophilous macroalgae; as a result detritus inputs
(organic matter) occurs at a lower rate than during the collaps of an macroalgal bloom.
Secondly, phanerogamms often have about 50 % of their biomass below ground as roots
and rizomes and dead parts of these organs contribute to organic matter input deeper into
the sediment thus not impacting the superficial layer. Thirdly, many phanerogamms may
excrete oxygen from their roots systems and thus contribute to increase the transport of
oxygen into the sediment.
It is also most important to consider how the sulfide (HS- and H2S) interact with the
rest of the sediment microbiology and geochemistry. HS- and H2S can be oxidised as
mentioned before in the superficial layers by sulfur-oxidising bacteria that consume
oxygen; however, in addition specialised sulfur-oxidising bacteria can oxidise these
compounds in a chemical reaction with nitrate as the electron acceptor and others in a
 Environmental Management and Sustainable Use of Coastal… 347

Fe 3+ Binds phosphates
Iron III
+ O2 or
sulfur
+ NO3-
oxidation
+ O2 or Fe 2+
+ NO3- S + O2 or
Iron II
sulfur + NO3-

SO42- photons : h. H S <-> HS-+H+ FeS

2
sulfate free sulfides iron sulfide

FeS2
Sulfate reduction
pyrite
Figure 4. Interactions between sulfur cycling and iron chemistry in the sediment. From De Wit et
al., 2001, reproduced with permission of Elsevier

photosynthetic reaction using light. HS- and H2S can also be sequestered in the sediment
by reaction with iron forming ironsulfide (FeS) and pyrite (FeS2). However, iron is also
important for sequestering phosphates by a reaction that occurs in the aerobic part (see
Figure 4). Hence, through redox conversion, sulfide and phosphate may compete for
binding with iron and as a result under highly reducing conditions with a high amount of
HS- and H2S in the sediment, the phosphate can be liberated from the iron complexes and
flux as ortho-phosphate into the water column. Such a phenomenon will enhance the
eutrophication of the water column, that might induce a shift in the primary producer
communities (see Figure 3). Hence, excessive reduction of sediments followed by a
dystrophic crisis may induce dangerous postive feedback loops that stabilise the system in
a undesired state characterised by a high level of eutrophication, loss of phanerogamm
species and frequently occurring dystrophic crises. In this respect, systems that are poor in
iron are more sensitive towards this phenomenon campared to iron rich systems. In
general for understanding the water quality it is necessary to gain some insight into the
functioning of the sediments.

Another possible state of the ecosystem is a turbid water column dominated by

phytoplankton species. In hypertrophic freshwater systems and in some brackish lagoons on
the Baltic coast filamentous cyanobacteria are forming dense blooms in the water column and
present a nuisance. This represents a particular risk factor for ecosystem health since many of
these planktonic cyanobacterial species produce toxins. Fortunately, these species do not
resist salt concentrations above 10. In some hypertrophic lagoons, small Chlorophycean
phytoplankton may develop very high biomass densities as e.g. in the Etang de Maugio
located to the East of the Etang de Thau. The high turbidity of the water column is strongly
detrimental to the phanerogamms. Oxygen concentrations may change significantly between
348 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

day and night time. The dying algae are an important input of organic matter to the ecosystem
and their degradation may take place in the water column or in the very surficial layers of the
sediment.
The abovementioned shows that an antagonistic relationship may exist between
phytoplankton and rooted phanerogamms and that the community dominated by the rooted
phanerogamms represents a more-appreciated ecosystem state. However, one should realise
that the oyster farming activity drives on the use of natural phytoplankton as a food source for
the oysters. Hence, while it is absolutely necessary to prevent the phytoplankton dominated
state of the ecosystem, a certain level of productivity of the lagoonal phytoplankton needs to
be guaranteed to sustain the productivity and reproduction of the oysters (see Box 2). It is not
unlikely that under fully pristine conditions, i.e. the reference state for the WFD,
phytoplankton productivity was insufficient for sustaining the oysterfarming yields obtained
nowadays in both lagoons. Therefore, coastal zone management needs to find a balance
between favouring sufficient phytoplankton growth for sustaining the productivity of the
oyster farming and the conservation and restoration measures aimed to restore good
ecological state for the ecosystem close to the reference state. Unfortunately, little research
has been performed on the direct interactions between seagrasses and phytoplankton. This
contrasts with the study of the interactions between seagrasses and macroalgae where a large
body of information is available nowadays (Valiela et al., 1997).
Sediments represent a particularly important ecosystem compartment in coastal lagoons.
These represent the habitat for the benthic community, are chemically enriched and capable to
store both the elements which are essential for primary productivity as well as the noxious
compounds. Sediments are real biogeochemical reactors responsible for the mayor part of the
remineralisation of organic matter. In addition, several of the material cycles interact within
sediments. Therefore, the sediment processes are dealt with in a special Box (i.e. Box 3)

5. EFFECTS OF THE CLIMATE CHANGE

ON THE COASTAL LAGOONS

The coastal lagoons as well as the other aquatic ecosystems are submitted to the global
change however, regarding their geographic position between land and sea and their
confinement and shallowness water, the coastal lagoons could be more sensitive than the
adjacent sea. The changes of several variables issues of global change such as temperature,
wind direction and precipitation regime, ultraviolet-B radiation, sea level, CO2 concentration
can drastically modify the functioning of the coastal lagoons. For example, increasing CO2
concentration results in proton addition to the water (dissociation of the weak acid H2CO3)
and may therefore induce a decrease of pH with a negative impact on biocalcification.
Sealevel rise in coastal areas will have a dramatic negative effect on intertidal areas and
particularly the morphometry of the coastal lagoons will be strongly affected. Colectively,
these changes influence primary production rates, bacterial growth rates, biogeochemical
cycles, structure of food web and finally the exploitable resources of the lagoons.
Water temperature increase is probably one of the most important variable that can be
affected the functioning of the coastal lagoons. The lagoon species are adapted to a high
variation of water temperature especially in the Mediterranean climate, however if the water
 Environmental Management and Sustainable Use of Coastal… 349

temperature increases more than the optimal level of tolerance by these species, the food web
structure will be modified. Any changes of food web structure can significantly modify the
exploitable resources of the coastal lagoons. Economic activities as e.g. oysterfarming depend
directly on the ressources of the lagoon. In general, all socioeconomic activities are directly or
indirectly related to these resources and to the biological components of lagoons. It should be
noted that the increase of water temperature during a short period (several years) can be
beneficial for the exploitable resources in the lagoons; however, the prevision (quantification)
of combined effects of several variable changes is very difficult consisting a challenge for
researchers working on.
These potential changes and complexity of the ecosystem responses should be considered
in the management of the coastal lagoons. This can be addressed with reference to an
integrated coastal zone management (ICZM) approach (Clark, 1992).

6. CONCLUSION AND PERSPECTIVE

Water quality management is paramount for sustainable use of coastal lagoons and
particularly crucial for aquaculture activities as oyster farming. The water quality
management should, however, not be limited to sectorial policies, but rather be elaborated as
an integrated approach considering the entire ecosystem. This is most important because
causes and effects are coupled at different spatial and temporal scales, as e.g. demonstrated by
the coupling between land use in the watershed and nutrient loadings into the lagoon. In
addition, internal processes in the lagoon ecosystem have a large impact on water quality. In
this respect, measures to protect seagrass meadows are particularly important for ecosystem
health. The European Water Framework Directive appears as a very good framework to
achieve these goals, particularly because it requires an integrated approach and focuses on
ecosystem functioning for water quality management. However, these developments should
also be considered with respect to climate change and sealevel rise.
Ecological and socioeconomic spatial consideration should be taken into account to
define the boundaries of the coastal lagoons ecosystems. However, historically, the
administative and political boundaries (municipalities, counties, regions and countries) do
often not concur with the natural boundaries needed to manage lagoons in an efficient way
and complicated interadministrative collaborations are often requested. Due to the diversity of
the ―exploitation patterns‖ of the coastal lagoons, the boundaries of the management unit (or
for the conservation of Transitional and Coastal waters in the frame of WFD) should be
ideally that of the area wher the conflicts and interactions levels are the highest. For example,
on one hand, the management area of a lagoon includes also the related watershed. On the
other hand, if the coastal lagoon shows evidence of interaction with resources from the oceans
and/or the EEZ (Exclusive Economical Zone) (e.g. migratory species such as snapers or sea-
bream, the LME concept (large marine ecosystem) (Sherman et.al., 1990) should be applied.
350 Rutger de Wit, Behzad Mostajir, Marc Troussellier et al.

REFERENCES
Alzieu, C. (2000). Impact of Tributyltin on marine invertebrates. Ecotoxicology, 9, 71-76.
Auby, I. & Maurer, D. (2004). Etude de la reproduction de l'huître creuse dans le Bassin
d'Arcachon- Rapport final. R.INT.DEL/AR 04.03, 201, + Annexes.
Barnes, R. S. K. (1980). Coastal lagoons; the natural history of a neglected habitat. 106.
Cambridge University Press, Cambridge.
Bettencourt, A., Bricker, S. B., Ferreira, J. G., Franco, A., Marques, J. C., Melo, J. J., Nobre,
A., Ramos, L., Reis, C. S., Salas, F., Silva, M. C., Simas, T. & Wolff, W. (2003).
Typology and reference conditions for Portuguese transitional and coastal waters,
Development of Guidelines for the Application of the European Union Water Framework
Directive, INAG/IMAR (2003) 98 pp.<http://www.ecowin.org/TICOR/>.
Borja, A. (2005). The European water framework directive: a challenge for nearshore, coastal
and continental shelf research, Continental Shelf Research, 25, 1768-1783.
Clark, J. R. (1992). Integrated management of coastal zones. FAO Fish. Tech. Report, 327,
167.
De Wit, R. Stal, L. J., Lomstein, B. Aa., Herbert, R. A., Van Gemerden, H., Viaroli, P.,
Cecherelli, V. U., Rodríguez-Valera, F., Bartoli, B., Giordani, G., Azzoni, R., Schaub, B.,
Welsh, D. T., Donelly, A., Cifuentes, A., Antón, J., Finster, K., Nielsen, L. B., Underlien
Pedersen, A. G., Turi Neubeurer, A., Colangelo, M. A. & Heijs, S. K. (2001). "ROBUST:
The ROle of BUffering capacities in STabilising coastal lagoon ecosystems. Continental
Shelf Research, 21, 2021-2041.
De Wit, R., Leibreich, J., Vernier, F., Delmas, F., Beuffe, Ph. Maison, H., Chossat, J. C.,
Laplace-Treyture, C., Laplana, R., Clavé, V., Torre, M., Auby, I., Trut, G., Maurer, D. &
Capdeville, P. (2005). Relationship between land-use in the agro-forestry system of les
Landes, nitrogen loading to and risk of macro-algal blooming in the Bassin d'Arcachon
coastal lagoon (SW France). Estuarine, Coastal and Shelf Science, 62, 453-465.
Kjerfve, B. (1994). Coastal Lagoons, chapter 1. In: B. Kjerfve, (ed.) Coastal lagoon
processes. 1-8. Elsevier Oceanography Series, Amsterdam.
Orfanidis, S., Panayotidisb, P. & Stamatisa, N. (2003). An insight to the ecological evaluation
index (EEI). Ecological Indicators, 3, 27-33.
Sherman, K., Alexander, L. M. & Gold, B. D. (1990). Large marine ecosystem : Patterns,
processes and yields. American Association for the Advancement of Science, 242.
Valiela, I. (1995). Marine ecological processes. Springer-Verlag, Berlin (ISBN: 3540943218)
Valiela, I., McClelland, J., Hauxwell, J., Behr, P. J., Hersh, D. & Foreman, K. (1997a).
Macroalgal blooms in shallow estuaries: Control and ecophysiological and ecosystem
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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editors: Adam G. Friedman, pp. 351-370 ©2011 Nova Science Publishers, Inc.

Chapter 12

INVOLVEMENT OF LOCAL USERS IS THE

OVERLOOKED BACKGROUND INFORMATION FOR
IMPROVING IMPLEMENTATION OF
CONSERVATION SOLUTIONS IN COASTAL LAGOON
MANAGEMENT: THE CASE OF THE ICHKEUL
NATIONAL PARK (TUNISIA)

Caterina Casagranda*
Marine Biologist
Formerly of the UMR 6540 CNRS Dimar "Diversité, Evolution et Ecologie fonctionnelle
marine", Centre d‘Océanologie de Marseille.

ABSTRACT
The Garaet El Ichkeul in Northern Tunisia has long been recognized as one of the
four major wetland areas in the Western Mediterranean basin (MAB Reserve in 1977,
World Heritage and Ramsar site in 1980). The Ichkeul lagoon and its marshes perform
essential ecological functions which are the basis of multiple services that contribute to
the wellbeing and economy of the local community. The villagers living within the core
area and the buffer zone have used to make a living off the land that did not seem to pose
any threat to the functions and services of these ecosystems. However, the construction of
dams on the rivers which provide water for the lake and marshes, as planned by the
Tunisian Ministry of Agriculture for the purposes of agricultural, urban and industrial
development, has had an impact on the ecological character of the site.
The Tunisian authorities, aware of the impact of these dams on the natural
environment at Ichkeul, founded a National Park. Unfortunately, the Park regulations
were introduced without taking properly into account the reality of the socio-economic
conditions of local residents. The lack of rehabilitation measures forced the villagers to

* 6a, rue Crudère, F-13006 Marseille (France), e-mail: caterina.casagranda@wanadoo.fr

352 Caterina Casagranda

exploit the resources in a non-selective way, which in turn further aggravated the existing
pressure on the Park and the precarious social conditions in which the families survive.
An international multidisciplinary study of all biotic and non-biotic aspects of the
National Park drew up an integrated management plan which was designed to take into
account the socio-economic development of the region. Since then, a number of
conservation measures have been adopted by the Tunisian authorities. They mainly take
into account the flora and fauna but without consultation of the people affected by these
measures – a fact that possibly explains the limited implementation of the management
plan proposed by the multidisciplinary study.
The question is of more than local interest, since similar problems arise throughout
the Mediterranean and elsewhere, i.e. conservation measures have been introduced but
the legislation is not respected in practice. When stakeholders are not involved initially or
are brought into the process at a later date, without the opportunity to provide input, they
are seldom supportive of the policy outcome. This is due in large part to the continued
reluctance of natural scientists and developers to learn from local community practices,
as opposed to management systems established on the basis of scientific facts. However,
recent studies on traditional ways of living off the land claim that the local communities
have developed elaborate processes for sustainably exploiting their resources. Such
practices can provide an important information base for integrated resource management.
The goal is: (1) to promote recognition of the traditional resource practices and the
accumulated wisdom as important features within ecological research, and (2) to
stimulate debate about whether their input will have significance for improving
environmental management policy.

1. INTRODUCTION
Historically, agriculture and urbanization have been the chief destroyers of ―useless‖
swamps and lagoons since these ―dirty‖ and ―smelly‖ places full of ―snakes‖ (i.e. eel) and
mosquitoes are impossible to plow or build upon. So why not get rid of them ? The
Mediterranean countries are characterized by their high attractiveness for tourism and many
governmental programs have encouraged the transformation of coastal lagoons and wetlands
into exploitable land or waters. As a consequence, many Mediterranean shores have suffered
from draining, dredging, dike building, mining for sand and gravel, ditching, road building
for the extension and development of seaside resorts (marinas, artificial beaches) (Meinesz et
al. 1991) because they had been seen as having little value. Human communities, which rely
directly on lagoonal resources for subsistence, do not necessarily share this view and often
have a detailed understanding of the goods and services such areas may provide. Since the
mid-twentieth century, scientific research on the functioning of lagoons has led to a change of
attitude. These literally ―wet lands‖ are transitional zones between terrestrial and aquatic
systems. They perform far-reaching functions within the ecosystem itself and as pathways
between land, freshwater habitats and sea (Levin et al. 2001). These essential ecological
functions provide services which contribute to human wellbeing and the economy. Scientific
acknowledgement of their value has led to an intensification of impact assessments in the
Mediterranean and elsewhere, but broader application of mitigation and restoration plans
remains difficult.
At Ichkeul (Tunisia) (Fig. 1), the most spectacular illustration of its natural functions and
services are the 150 000 - 250 000 wintering Palaearctic waterfowl present there at one time
 Involvement of Local Users is the Overlooked Background Information … 353

(Tamisier et al. 1987). The high identified value of Ichkeul is reflected in its exclusive listing
in three international conventions: (1) Biosphere Reserve in 1977 (UNESCO 2010); (2)
World Heritage Convention in 1980 (UNESCO World Heritage Centre 2010) and (3) Ramsar
Convention in 1980 (Ramsar Convention & Wetlands International 2010). The documents
presented at the time of Ichkeul‘s inclusion in these international conventions noted that the
construction of 6 dams on the wadis (i.e. temporary rivers) which provide freshwater for the
lake and marshes, as planned in the ―Master Plan for the Waters of Northern Tunisia‖, was
likely to have an impact on the ecological character of the site. The Ichkeul National Park was
formally founded in 1980 by presidential decree and an international multidisciplinary
research programme entitled ―Etude pour la Sauvegarde du Parc National d‘Ichkeul‖
(BCEOM et al. 1994, 1995) drew up an integrated management plan. A number of measures
have been adopted by the Tunisian authorities which are essentially a response to the primary
concern of the MAB-Programme, i.e. the objective of conservation of the flora and fauna.
However, the wider implementation of the management plan still remains difficult (Baccar et
al. 2000).

Figure 1. The Ichkeul National Park (Tunisia) and its catchment.

354 Caterina Casagranda

About 350 people live within the core area of the reserve who made a living off the land
in a way that did not seem to pose any threat to the integrity of the ecosystem (Muller 1976,
Hollis 1977, Hollis 1986, BCEOM et al. 1994). Nevertheless, the local population affected by
the conservation measures has not been involved in the process of identifying problem areas -
a fact that possibly explains the limited implementation of the management plan proposed by
the Safeguard study. The National Park regulations have been imposed on local communities
from above and the lack of rehabilitation measures forced the villagers to exploit the
resources in a non-selective way, which in turn further aggravated the existing pressure on the
Park and the precarious social conditions in which the families survive (BCEOM et al. 1994).
The question that arises is: Is traditional resource use the overlooked management tool for
improving coastal lagoon conservation ? The Park is still perceived by the local residents and
stakeholders as a burdensome collection of prohibitions. Rural communities and their
knowledge of the resource, which receive little attention in management planning, will be the
focus of this presentation. The question is of more than local interest, since similar problems
arise throughout the Mediterranean and elsewhere, i.e. conservation measures have been
introduced but the legislation is not respected in practice.
In this presentation, I describe the natural functions and services of the Ichkeul
ecosystem, with particular reference to local resident communities, and their social and
practical usefulness. I then examine the economic, ideological and institutional factors that
combine to perpetuate the marginalisation and neglect of local knowledge, and discuss some
of the requirements for applying local knowledge in modern management. The paper brings
together a fair amount of hitherto dispersed and unpublished information which is not easily
available to international readers.

2. GEOGRAPHICAL CONTEXT
The designation ―Biosphere Reserves‖ refers to a mosaic of habitats. The Ichkeul
National Park is made up of three major landscape units that include a particularly diverse
variety of habitats:

[1] A permanent shallow brackish water lake in northern Tunisia, with an area of 90
km² , connected to the marine lagoon of Bizerte by a small winding channel,
improperly referred to as Tinja wadi (i.e. temporary river) Fig. (1).
[2] Temporarily flooded marshes of an area of about 36 km². The region has a
typically Mediterranean semi-arid climate which leads to a temporary drying out
of the marshes during the summer (Fig. 2).
[3] The isolated and wooded djebel (mountain in Arabic) rising on the southern
shore of the permanent lake.
 Involvement of Local Users is the Overlooked Background Information … 355

Potamogeton pectinatus meadow Scirpus maritimus rush

Ruppia cirrhosa meadow Bare bottom
Phragmites australis reed National Park limit

Figure 2. Schematic annual alternation of surface and water level at Ichkeul lagoon (Tunisia) under pre-
dammed conditions. Maximum water depth in winter: 2-3 m with all marshes inundated, in summer 1m
with all marshes dried up.
356 Caterina Casagranda

3. ECOSYSTEM FUNCTIONS
Ecosystem functions refer variously to the habitat, biological or system properties or
processes of ecosystems. Coastal lagoons and wetlands are critical transition zones (CTZ) that
link terrestrial and aquatic systems (Levin et al. 2001). They perform essential ecological
functions, including decomposition, nutrient cycling and production, regulation of fluxes of
nutrients, water, particles, and organisms to and from land, freshwater habitats and sea.
Ecological functions at each wetland depend on its location, size, and relationship to adjacent
land and water areas. By analogy to Levin et al. (2001), functions at Ichkeul are performed as
follows:

3.1. Within the Ecosystem Itself

Primary and secondary production.- Coastal wetlands and lagoons are among the most
productive natural systems in the world. Global contributions are proportionally much greater
than might be expected from their small coverage area (Costanza et al. 1997).
At Ichkeul, phytoplankton density was found to be remarkably low, with < 1.5·106 cells/l
(BCEOM et al. 1995). Macroalgae were locally and temporally limited to the north-eastern
border in autumn (BCEOM et al. 1995). Both groups were considered negligible as primary
producers. The primary producer that fuels secondary and higher order production at Ichkeul
are seagrasses (Casagranda & Boudouresque 2007). The western and southern areas, supplied
with freshwater from the wadis, are covered by extensive monospecific beds of Potamogeton
pectinatus L., 3050 and 690 ha respectively (Casagranda & Boudouresque 2007). The eastern
area close to the Tinja channel and supplied with seawater is covered by a meadow of Ruppia
cirrhosa (Petagna) Grande (300 ha). The central area (4960 ha) is completely free of
vegetation (Casagranda & Boudouresque 2007). The mean primary production was very high
(Table 1), at 203 g dry mass (DM)/m² (Casagranda & Boudouresque 2007). The total primary
production extrapolated over the whole lagoon surface (9 000 ha) would amount to 18 233
tDM.
The keystone process that channels the energy fixed in the biomass through the
ecosystem is the primary consumption, i.e. it determines how much of this energy enters the
herbivore and/or the detritivore pathway. By analogy to Asmus (1987), the macroinvertebrate
consumers can be divided into 2 functional compartments at Ichkeul:

[1] a ―turnover compartment‖ that consists of shredders and epibenthic deposit

feeders. The species are characterized by relatively low production, high P/B
ratio (Table 1) and are subject to strong predation. The production is mainly
transferred to higher trophic levels. This compartment governs the
decomposition and nutrient transfer in the community.
[2] A ―storage compartment‖ that consists in the case of Ichkeul of endobenthic
deposit feeders. These species are characterized by high production, low P/B
ratio (Table 1) and are subject to only little predation. The production is mainly
sequestrated within the ecosystem leading to further biomass increase. This
compartment governs the nutrient and oxygen conditions for the community.
 Involvement of Local Users is the Overlooked Background Information … 357

Table 1. Mean primary producer and macroinvertebrate consumer biomasses of the

Ichkeul aquatic ecosystem. DM = dry mass, AFDM = ash-free dry mass.

Functional Mean Mean Turnover Lagoonwide Data

group biomass production P/B production source
Casagranda & Boudouresque
Seagrass 125 gDM/m² 203 gDM/m² 2 18 233 tDM
2007
Shredders <1 gAFDM/m² 1 gAFDM/m² 2 96 tAFDM Casagranda et al. 2006
Epibenthic deposit 1 067
4 gAFDM/m² 12 gAFDM/m² 3 Casagranda et al. 2005
feeders tAFDM
Endobenthic deposit Casagranda & Boudouresque
20 gAFDM/m² 8 gAFDM/m² <1 741 tAFDM
feeders 2005

Decomposition and nutrient recycling.- Seagrass beds produce large amounts of dead
plant material (litter). In autumn, thick layers of dead vegetation pile up all along the southern
shores after collapsing and becoming detached. The mean litter biomass buried in the
sediments ranges between 92 and 138 g DM/m² (Casagranda & Boudouresque 2007). The
organic matter is rapidly incorporated into a complex decomposer food web. A significant
proportion (10-25 %) of the plant material leaches out of plants as dissolved organic matter
during the first few weeks after death (Fenchel 1977). The senescent plant parts are rapidly
colonized by microscopicalgae, aquatic microbes and microfauna (Fenchel 1977). Shredder
species which graze on the leaf surface ―fouling‖ (Graça et al. 2000), facilitate the mechanical
breakdown by scraping and shredding (Newell & Bärlocher 1993) and enhance the nutrient
transfer to higher trophic levels (Lillebo et al. 1999). Litter bag experiments by Verhoeven
(1980) showed how important shredding and grazing invertebrates were for macrophyte
decomposition. He found that half of the material had decomposed within two months and
that after a year practically no plant material was left. High rates of decomposition are critical
to the sustained functioning of coastal lagoons. No accumulation of organic matter, algal
blooms or summer anoxia characteristic for eutrophic lagoons have ever been reported from
Ichkeul (Chaumont 1956, Zaouali 19974, Dridi 1977, Hollis 1986, Tamisier et al. 1987, Ben
Rejeb-Jenhani 1989, BCEOM et al. 1994, 1995, Casagranda 2005 and many other
unpublished reports).

3.2. Pathway Functions that Connect and Transfer Water, Material, and
Organisms between Land and Sea

Mixing of water and salt.- Garaet El Ichkeul was a freshwater lake (―garaet‖ means
freshwater basin in Arabic) before the deepening and widening in 1881 of the canal linking
Bizerte lagoon to the sea (Fig. 1). It has been characterized since then by the alternation of
fresh water in winter and brackish water in summer. Until the early 1990s, it was filled up in
winter with freshwater from direct precipitation and from the drainage basin by 7 wadis (i.e.
temporary rivers) that overflowed into the Bizerte Lagoon. In summer, high evaporation
lowered the water level and allowed saline water to enter the lake. Its surface varied
considerably between summer and winter: from 80 to 90 km² in summer to 110 to 130 km² in
winter with all marshes inundated. The freshwater output through the Tinja channel was 47 to
955·106 m3/a, the mean saltwater input was about 60·106 m3/a (Chaumont 1956, Hollis 1977,
358 Caterina Casagranda

Lemoalle 1983a, BCEOM et al. 1995). The salinity displayed considerable seasonal changes
from 3 in the innermost parts in spring to over 38 at the mouth of the Tinja channel in autumn
(Lemoalle 1983b, Ben Rejeb-Jenhani 1989, BCEOM et al. 1995).
Three dams have been constructed on the wadis providing Ichkeul with freshwater
(Joumine in 1983, Ghezala in 1984 and Sejnene in 1994) while three more are planned on
Douimiss, Melah and Tine (Fig. 1) in the ―Master Plan for the Waters of Northern Tunisia‖.
The filling period of the Sejnene dam 1994 to 1998 fell unfortunately within a ten-year period
of low rainfall. In addition to the reduced inflow from the catchment, there was also an
increased backflow of saline water from the Bizerte Lagoon. As a result, the salinity of the
lake in summer sharply increased sometimes reaching values over 60, hence twice the salinity
of sea water (Dridi pers. com., ANPE 2010). The increased salinity caused the extirpation of
P. pectinatus and a serious loss of biological diversity, especially of migrant waterfowl and
fish (Shili pers. com., Shili et al. 2007). Reedfringe and freshwater macrophytes disappeared
and rush beds were replaced by halophytic plants with a significant reduction of breeding
birds that no longer had any nesting cover in the vegetation (Shili et al. 2007).
By a stroke of good luck, the winters of both 2002/03 and 2003/04 were exceptionally
wet for Tunisia, filling the dams to the extent that they overflowed into Ichkeul. These
releases were in addition to inflow from the undammed rivers and direct precipitation. As a
result, practically all the salt that had accumulated in the lake over the previous decade was
leached out via the Tinja channel. The low salinity levels have allowed Potamogeton
pectinatus to reappear in the lake, while rush stands have begun to grow again in the marshes
(Shili et al. 2007).
Nutrient transfer and transformation.- According to the eutrophication study of the
OECD (Organisation for Economic Cooperation and Development) (Vollenweider & Kerekes
1982), Ichkeul can be considered as ultraoligotrophic in mean total nitrogen terms (Ntot , 21
μmoles/l) and hypertrophic in mean total phosphorous terms (Ptot , 4 μmoles/l) (BCEOM et al.
1995). BCEOM et al. (1995) reported low inputs from the western catchment and the Tinja
channel, but high inputs from the southern catchment and internal supply. High organic N
(Norg) values in the water column during autumn (156 mol/l) indicate inputs from seagrass
meadow senescence.
The water column of the southern basin is subject to high pollution-induced turbidity
from municipal sewage from the town of Mateur through the Joumine wadi (Secchi depth less
than 10 cm), essentially soluble reactive phosphorous (P-PO4, 102 mol/l) and ammonium
(N-NH4, 1131 mol/l), i.e. the assimilable N and P fractions by plants. However, P-PO4 and
N-NH4 levels in the water column of the lake were low (0.2 mol/l and 5.8 mol/l
respectively) (BCEOM et al. 1995). Low P-PO4 and N-NH4 levels in the water column
indicate macrophyte uptake; however, most P-PO4 and N-NH4 is supposed to be concentrated
in the sediments. At Ichkeul, rapid elimination of P-PO4 from the water column by sediments
has been demonstrated. Ben Rejeb-Jenhani (1989) showed that the Ichkeul sediments have
high P-PO4 adsorption capacity. As the dissolved oxygen is in the range of 83-117 % of
saturation, the BOD5 low (1.5-2.8 mg/l) and the redox potential high (370-400 mV) (BCEOM
et al. 1995), P-PO4 storage in the sediments and N fixation rather than denitrification would
be more likely. Under aerobic conditions and lack of assimilable N and P in the water
column, sediments are the major nutrient source for seagrasses. Moreover, BCEOM et al.
(1995) reported high outputs of organic N and N-NH4 through the Tinja channel, a factor that
 Involvement of Local Users is the Overlooked Background Information … 359

further aggravates the impoverishment of the lake water in nitrogen. Under pre-dam
conditions, it can be postulated that seagrasses controlled P availability and suppressed light-
limiting phytoplankton blooms.
Particle flows and pollutant transport.- According to Chaumont (1956), around 1 000
000 t of sediment can be transported into Ichkeul via wadi inflow and runoff from land, of
which around 100 000 t would be evacuated via the Tinja channel (Lemoalle, in Ben Rejeb-
Jenhani, 1989). In Roman times, the extension of the permanent lake was likely to be much
greater than nowadays and the Djebel must have been an island (Chaumont 1956). Hollis
(1986) reported a sedimentation rate of about 6 mm/a. Seagrass beds slow water flow, and
enhance the deposition of fine particles and the trapping and transformation of pollutants
(Fonseca 1996). The decline of the seagrass meadows in the 1990s and the construction and
operation of the Tinja sluice in the summers to maintain fresh water in the lake may have had
an impact on sedimentation patterns in the lake. Sediments, which would formerly have been
carried away through the Tinja channel, may have been held back in Ichkeul by the sluice. It
may be therefore that the depth of the lake is decreasing more rapidly, which might induce
changes in the distribution and species composition of vascular plants and animals, water
regime or flooding (Shili et al. 2007). The closing of the Tinja sluice is far from being a cheap
solution in water quota terms since its operating is triggered by the water salinity and the
levels measured.
Organism movements.- Animals moving within or through CTZs are vectors that
transport nutrients and organic matter across terrestrial, freshwater, and marine interfaces
(Levin et al. 2001). The most spectacular illustration of this pathway function are the 150 000
- 250 000 wintering Palaearctic waterbirds present at one time which use the lake and
marshes at Ichkeul. The high records of migratory birds, in particular ducks, coot, geese,
storks and flamingos, indicate that Ichkeul is the most important wintering station in North
Africa, i.e. 5 to 7 times more than any other site in the Western Mediterranean offering
similar wintering conditions, such as the Camargue (France), the El Kala (Algeria) or the
Coto Doñana (Spain) (Tamisier et al. 1987, Tamisier 1992, BirdLife International 2010).
They use it in conjunction with other wintering or staging areas in the Mediterranean (Ramsar
criteria 1, 3, 5 and 6). Extensive stands of rushes (Bolboschoenus maritimus (L.) Palla and
Schoenoplectus lacustris (L.) Palla) in the surrounding marshes provide the major food source
for a large population of greylag geese (Anser anser (L.)) (3 000).
The annual trophic impact derived from migratory fish comes almost entirely from 3
euryhaline migrant species, the European eel Anguilla anguilla (L.) (―Anguille‖) and the
mullet Liza ramada (Risso) (―Bitoum‖ in Tunisian) and Mugil cephalus L. (―Bouri‖). Other
species such as Dicentrarchus labrax (L.), Belone belone (L.), Solea vulgaris (L.), Sparus
aurata L. and Alosa fallax (Lacepède) account for this impact to a far lesser extent (BCEOM
et al. 1995).
Mullet fry and eel elver enter Ichkeul from the Tinja channel in spring, mainly in
February and March, and feed and grow for a variable number of years, ranging from 3 to 5
years for the mullet and around 4 years for the eel (Casagranda & Boudouresque 2010) until
sexual maturation, whereupon the fish leave the lake for spawning.
In the macrophyte meadows there occur small sized eurybiont fish of short life and early
sexual maturation such as Atherina boyeri Risso, Pomatoschistus microps (Krøyer), Aphanius
fasciatus (Valenciennes), Syngnathus acus L. and Gambusia affinis (Baird & Girard), which
do not migrate but spend their entire life cycle in Ichkeul. The species constitute the main
360 Caterina Casagranda

prey of eel and seabass, and thus hold a significant position in the flow of organic material
into and out of the ecosystem.

4. ECOSYSTEM SERVICES
According to Costanza et al. (1997), coastal lagoons and wetlands cover less than one
percent of the earth's surface, but are the source of one-6th of the world's productivity in
monetary terms. Ecosystem goods (such as food) and services (such as waste assimilation)
represent the benefits that human populations derive, directly or indirectly, from ecosystem
functions. It is important to emphasize the interdependent nature of many ecosystem
functions. In addition, ecosystem functions and services do not necessarily show a one-to-one
correspondence. A single ecosystem service can be the product of two or more ecosystem
functions whereas a single ecosystem function can contribute to two or more ecosystem
services. Ichkeul has - in addition to its birds - numerous goods and values, marketed and
non-marketed ones, that are given too little weight in policy decisions. The problem with non-
marketed ecosystem services is that the costs of degrading these resources are hidden. In the
following section, I attempt to make the range of potential values of services more apparent.
The goal is to help ensure that the absence of market value does not mean that the valuable
services these resources provide are taken for granted since many ecosystem services are
literally irreplaceable.
Hydrological values.- The wetland is the last remaining site of a chain of freshwater lakes
which once extended across North Africa (World Heritage‘s criterion iv). Lake Ichkeul acts
as a waste water purifier, erosion control and sediment retention system, water storage basin,
including mitigating the impact of floods and drought, and supply of groundwater reserves.
The winter inflows flood the surrounding marshes, sediment and pollutants are trapped; soil
particles bind with pollutants. The water slowly soaks into the ground. Bacteria in the water
and soil neutralize wastes. This natural cleansing capacity performs entirely free of charge
what engineers perform in exchange for thousands of dollars. The dense seagrass beds absorb
nutrients and form the base of the food web. The slowed-down, cleansed water flows out
through the Tinja channel but much of it percolates into the ground and recharges the
groundwater that provides most of the drinking water.
Economic resource.- The Ichkeul fishery, which is based on fish traps at the mouth of the
Tinja channel linking Ichkeul to the Bizerte lagoon, is of some national importance. Mullet
(M. cephalus, L. ramada) and eel (A. anguilla), making up 97 % of the catches, are easily
captured on their leaving the lagoon for spawning via the Tinja channel (BCEOM et al.
1994). While the mullet are sold at the local market, the eel are not consumed in Tunisia
(―snakes‖); the fishing rights are sold every winter to an Italian company. During winter
1993/94, the income from the eel alone was 763 000 TD ($ 586 000), and from the mullet
another 381 000 TD ($ 293 000) (BCEOM et al. 1995).
Biological reservoir.- The present aquatic and terrestrial flora and fauna of the area is
recognized as being particularly diverse largely due to the wide variety of habitats. 500 plant
species have been counted in the park. The main vertebrate and invertebrate fauna is typical
of brackish water areas although on the edge of the salt marsh there are freshwater species.
More than 185 bird species have been recorded (Tamsier et al. 1987). Waterbirds using Lake
 Involvement of Local Users is the Overlooked Background Information … 361

Ichkeul include grebe, cormorant, heron, ibis and spoonbills, stork, geese and duck, rail and
coot, shorebirds, gulls and terns, and two raptors that are functionally linked to wetlands (the
Western Marsh-Harrier Circus aeruginosus (L.) and the Osprey Pandion haliaetus (L.))
(Hollis 1986, Tamisier et al. 1987, Tamisier 1992). Total numbers were much higher in
winter than during the breeding season and made up principally by three phytophageous
waterfowl species, the Eurasian wigeon Anas penelope L., the common pochard Aythya ferina
(L.) and the common coot Fulica atra L. In addition to these long-distance migrants,
threatened and endangered species such as Marbled Teal (Marmaronetta angustirostris
(Ménétriés)) rely directly on Ichkeul for their survival. The Purple Gallinule (Porphyrio
porphyrio (L.)) breed at Ichkeul and up to 600 of the threatened White-headed Duck (Oxyura
leucocephala (Scopoli)) (4 % of the known world population) have been recorded (Hollis
1977). Many species of raptor breed on the Djebel.
The herpetofauna Rana ribibunda Pallas and Clemmys leprosa Schweigger can be found
in the marshes and lake (Morgan 1982). One of the most notable of the mammals recorded at
Ichkeul is the otter Lutra lutra L. (Hollis 1977).
The site has internationally important mammal fossil deposits including late Tertiary and
early Quaternary outcrops (Arambourg & Arnould 1949). The Djebel is composed of Triassic
and Jurassic formations (Hollis 1986), mainly as metamorphosed limestone with pseudo-
dolomitic marble correspondence including features of botanical interest and remaining a
geological enigma since it bears little relation to other surrounding geological features.
Cultural heritage.- Since antiquity, the lake, marshes and mountain have been settled and
influenced by man, providing food (game, fish), and raw materials (reeds, peat). It is at the
root of very strong cultural and social traditions. Native people at the djebel have traditionally
raised cattle, sheep and goats, fished in the lake and worked in the quarries on the
mountainside, exploited since Roman times. The hot springs at the foot of the Djebel attract
many Tunisian visitors during spring. In Punic times, the site was a reserve for state hunting
and the wild Asiatic water buffalo (Bubalus bubalis Kerr) is claimed to descend from herds
kept as game animals (Müller 1970).
Living laboratory.- An impressive number and diversity of studies have been carried out
on Ichkeul: Heldt (1948), Chaumont (1956), Massin (1967), Jaeger (1971), Zaouali (1974),
Dridi (1977), Ouakad (1982), Vidy (1983), Ben Rejeb-Jenhani (1989), Casagranda (2005) are
only a few among many others. Some of the earliest scientific studies resulted from the
palaeontological excavations in 1947-49 (Arambourg & Arnould 1949). A programme of
waterfowl observational research has been under way since 1963 in collaboration with
University College London (UCL) (UK), The International Waterfowl Research Bureau
(IWRB) (UK) and the Tour du Valat Biological Station, Camargue (France).
During the 1980s, a number of international research projects were carried out at Ichkeul
in order to investigate the impact of the two dams and predict the likely impact of all six dams
(Hollis 1986). The aim of these projects was to complement existing ornithological data with
hydrological and macrophyte data. In 1993, the Safeguard Study, more thorough than the
previous ones, of all biotic and non-biotic aspects of the National Park was launched to
summarize the existing data, to model the functioning of the whole ecosystem and to devise
an integrated management plan (BCEOM et al. 1995). An on-site technical team, based in the
reception centre on the mountain, has since 1997 been monitoring a number of different
parameters, both abiotic and biotic.
362 Caterina Casagranda

Recreation.- The tourist potential of the National Park is high as the isolated and wooded
djebel rising from the lake gives the site a singular natural beauty. It is very rare to find a
rocky mountain rising from the middle of a wetland (World Heritage criterion iii). According
to Lavauden (1937), ―Ichkeul‖ is probably derived from the Italian word for rock, ―il
scoglio‖. Moreover, the presence of some 200 000 waterfowl during the winter is very
spectacular even for visitors unfamiliar with bird watching. The number of annual visitors is
estimated at 60 000, 90% of them Tunisians. An ecomuseum and a reception centre have been
constructed with assistance from the British Museum of Natural History and the WWF to
inform visitors about the values that explain its inclusion in three International Conventions.
According to Costanza et al. (1997), non-extractive values of ecosystem resources, which
range from the tangible (e.g., water buffalo as a lure for tourists) to the more abstract (e.g., the
value of simply knowing that migrating birds exist, even if one does not ever expect to go
bird-watching), can exceed the value of extractive uses like fishing.

5. IMPROVING REGIONAL EFFORTS IN LAGOON PROTECTION

5.1. Conflicts of Interest

Human use of ecosystem services may or may not leave the original capital stock intact.
At present, Ichkeul National Park is the focus of a number of different interests which come
into conflict: water supply, conservation, agriculture, local residents and stakeholders.
At site level.- The villagers living within the core area and the buffer zone of the Ichkeul
National Park used to make a living off the land that did not seem to pose any threat to the
ecosystem‘s functions and services (Muller 1976, Hollis 1977, Hollis 1986, BCEOM et al.
1994). The people traditionally used the marshes for grazing, fished in the lake and worked in
the marble quarries on the south-eastern slopes of the Djebel, which have been exploited
since Roman times. After the creation of the National Park in 1980, the regulations have
unfortunately been imposed on the local residents from above without giving them the
opportunity to find alternative ways of earning their livelihood or raising awareness of the
need for conservation of the natural resource. The lack of alternative socio-economic
proposals for the villagers directly affected by the Park regulations has led to the over-
exploitation of grazing on the Djebel and the marshes, and greater dependence on - prohibited
- fishing and duck hunting within the reserve (Hollis 1986, BCEOM et al. 1994). The number
of sheep and cattle on the Joumine marsh has increased very substantially since the 1980‘s
and this area now is seriously threatened, although grazing of domestic stock did not appear
to pose any threat to the ecological functions and services until then. Livestock not only
consume the vegetation, they also tend to remain in the same area for an extended period of
time. Their movements to and from riversides can create gullies and otherwise undermine the
banks. While fishing seems to be limited in intensity and relatively few birds are killed,
significant disturbance to the feeding waterfowl and destruction of surrounding vegetation
occurs through repeated use of trails. The park director has watched that all households have
at least one person in full time employment. Although the park wardens consider themselves
fortunate to have a steady paying job, the low pay and the lack of equipment, status and social
 Involvement of Local Users is the Overlooked Background Information … 363

benefits has been frustrating (Yousef M. pers. com.). After writing appeals to the Ministry of
Agriculture, their status has improved as the guards are no longer considered as ―day
workers‖ and are eligible for social security benefits.
Ironically, the activity of the quarries on the southern slopes of the Djebel, although well
within the Park, did not seem to come into conflict with the Park status until the 1990s. Their
extension and the intensification of quarrying seriously threatened the relatively luxuriant
flora and fauna of the Djebel. Moreover, the dust and dumping caused pollution of the maquis
and the marshes, and the fleet of heavy lorries had an adverse impact on the landscape and
wilderness appeal of the Park for tourists. The political decision to close the marble quarries
was only put into practice in 1994, some 14 years after the Park was founded. The call for
restoration has been met by spraying of the surfaces of outcrops with green paint (Casagranda
et al. pers. obs.).
At government level.- In a country such as Tunisia, situated on the northern edge of the
Sahara desert, water is a natural resource of prime importance for economic and social
development. The need to obtain control over surface water resources and to move water
around the country to wherever it is needed has been a national development priority since
independence in 1956 (BCEOM et al. 1994). Another reason for developing the water control
system was to reduce the impact of flash flooding. In September 1969, torrential rain in
central Tunisia caused flash flooding in the plains downstream leading to loss of human lives
and catastrophic damage to transport systems and other infrastructure. The massive downpour
in Algiers (Algeria) in 2001 served as a reminder of this ever-present risk.
The General Directorate for Hydraulic Studies and Works of the Tunisian Ministry of
Agriculture developed ambitious plans, finalized in 1975, to build a series of interlinked dams
on rivers in the well-watered north, six of them dams on rivers flowing into Ichkeul. These
dams are the key element of the so-called ―Master Plan for the Waters of Northern Tunisia‖,
i.e. a national water network which will provide water for agriculture, urban development and
industry. Two of these 6 dams are of considerable size, the Sejnene dam and the Joumine
dam, and the other four rather smaller (Fig. 1).
During the 10-year period of natural and anthropogenic shortage of freshwater input to
Ichkeul, the only possible solutions would have been water releases from the Sejnene and
Joumine dams (Fig. 1). However, it would have been difficult to release water when farmers
themselves are short of water, i.e. for ducks. - The Tunisian authorities decided to suspend the
construction of the remaining dams on the other wadis Douimiss, Melah and Tine until the
Sidi El Barrak dam, situated in a neighbouring catchment, became operational (Shili pers.
com., ANPE 2010). It has further been decided to grant Ichkeul an annual water quota and to
ensure this supply from the Sidi El Barrak dam as soon as it is linked to the Sejnene dam and
from the three remaining dams once they have been built. However, no clear indication has
been made regarding the amount of water to be supplied (Shili pers. com., ANPE 2010). As a
practical measure, a sluice was built on the Tinja channel which would make it possible to
maintain fresh water in the lake or to prevent the flow of saline water into the lake in summer
(BCEOM et al. 1995).
Another concern for the long term conservation of Ichkeul is the saga of the drainage
canal on the Joumine marsh in the southern catchment (Fig. 2). The Ministry of Agriculture‘s
General Directorate of Rural Engineering developed an agricultural improvement scheme in
the Plain of Mateur adjacent to the Park that would involve irrigation of the higher fields of
the Plain and the drainage of the low lying lands adjacent to the marshes of the National Park
364 Caterina Casagranda

(Fig. 1). In addition, the plan involved the substantial use of agrochemicals that would be
carried towards the lake. The Joumine drainage canal (Fig. 1) was formerly a winding wadi
through the Mateur Plain, which was diverted and canalised for the last 200 m before the
marsh fringes in the early 1950‘s. The canal fed into the Joumine marsh and spread its water
over most of the marsh. This was subsequently incorporated into the National Park in 1980
(Tamisier pers. com., Hollis 1977). In the autumn of 1981, i.e. one year after the foundation
of the Park, the existing canal was extended for 2 km to the very edge of the lake. This was
done without consultation with the Park authorities (Tamisier pers. com., Hollis 1986). The
reduced water level led to the drying out of the marshes while the lack of freshwater flooding
restricted vegetation to salt tolerant plants. Before the digging of the drainage canal, the
grazing of the cattle did not appear to be a threat to the ecological ―health‖ of the marsh since
the previously existing reed beds made it inaccessible to domestic livestock (Tamisier pers.
com.).
The filling of this drainage canal has been agreed to by all parties in the Ichkeul
Coordinating Committee since 1984 (Hollis 1986) but no action has been taken by the
General Directorate of Rural Engineering because the filling of the canal may interfere with
the drainage for the Plain of Mateur. The interest of General Directorate of Rural Engineering
as a land drainage organisation is to keep the lake level as low as possible throughout the
winter months. A step towards closer collaboration between different arms of decision has
been taken with the merging of the Ministries of Agriculture and Environment into a single
Ministry of Agriculture, Environment and Water Resources.
At international level.- The Safeguard Study (BCEOM et al. 1995) identified a number of
measures and drew up an integrated management plan for the Park, taking account of its
regional economic context. Studies of this kind, i.e. where both biotic and abiotic data are
assessed simultaneously in a single survey, are very rare in scientific literature. The study
clearly demonstrated that water releases from the dams would be required if the main
elements of the ecosystem were to be conserved and drew particular attention to the filling of
the drainage canal at Joumine to ensure the effectiveness of the water releases.
Despite a certain number of policy decisions taken by the Tunisian authorities (e.g., the
decision to grant Ichkeul an annual water quota, supplied from the Sidi El Barrak dam) and
some practical measures introduced by the ANPE (National Agency for the Protection of the
Environment) (e.g., operating of the Tinja sluice, a monitoring programme), wider
implementation of the management plan drawn up by the Safeguard Study remained difficult.
A World Heritage/Ramsar mission in 2000 (Baccar et al. 2000) took note of the efforts
made on site and at government level, and again stressed the need for the updating and
implementation of the management plan with the involvement of all concerned interest
groups and the restoration of the Joumine marsh. During summer 2008, the lower part of the
drainage canal at Joumine has been filled and autumn rainfall flooded the marsh through
additional small side channels (ANPE 2010) thus restoring the conditions that existed when
the National Park was created 28 years ago.
 Involvement of Local Users is the Overlooked Background Information … 365

5.2. Underlying Causes of the Conflict

Effective implementation of a management strategy requires the involvement of the main

stakeholders, who must be made aware of the need for the conservation of the natural
resource as a guarantee for their current and continued future wellbeing. The Ramsar
Convention has provided guidelines for encouraging and strengthening the participation of
the human users affected by the policy outcome. When stakeholders are not involved or are
brought into the policy formulation and planning process at a later date, without the
opportunity to provide input, they are seldom supportive of the policy outcome. Compliance
with policy, together with requisite monitoring and enforcement, greatly suffers in
consequence, and the policy can even fail outright.
The designation ‗Biosphere Reserves‘ under the UNESCO MAB-Programme requires a
balance between conservation of biological diversity, sustainable human exploitation and
scientific research. The measures adopted by the Tunisian authorities took account of the
primary concern of the MAB-Programme, i.e. the objective of conservation of the flora and
fauna of the Park. However, they failed to meet the objective defined as ―sustainable
development‖ in Agenda 21 of the UN Earth Summit held in Rio de Janeiro in 1992, i.e.
―incorporating care of the environment, living off the land without depleting its capital, with
greater social equity, including respect for rural communities and their accumulated wisdom‖.
It is clearly stated that government agencies, charged with coastal zone protection (e.g., the
ANPE in Tunisia), must integrate traditional ecological knowledge and socio-cultural values
with management agendas. Traditional ecological knowledge is now more specifically
defined as Traditional Ecological Knowledge and Wisdom (TEKW), a concept that combines
the worldview of a people with their use of resources over time (Ford & Martinez 2000). In
addition, Nazarea (1998) reminds us that this knowledge, as well as the preservation of
threatened taxa, is critical for the preservation of biodiversity. Because biotic diversity in
coastal lagoons is inherently low, whereas their functional significance is great, shifts in
diversity are likely to be particularly important. Ecological modelling of the Ichkeul
ecosystem (Casagranda in prep.) provides evidence that single species changes from
anthropogenic influences (e.g., eutrophication, non-nutrient pollutants, habitat alteration,
climate change) have overt, sweeping effects on ecosystem structure, with negative
consequences for functions and services. Beyond the ethical duty to respect rural
communities and their accumulated wisdom, I hypothesize that traditional resource use is
from the ecological point of view important for lagoon management because its sustainable
approach maintains positive interactions among species, promoting stability and resistance to
disturbance. The complexity of interactions between man and species, together with feedback
for ecosystem functions, suggests that social science-based approaches will be required to
gather biological data and to elucidate the role of man in sustaining lagoon functions and
services.
Humans are also components of ecosystem functions, and it is similarly necessary to
identify the individuals, groups of individuals, and institutions that are most critical in this
regard. In this sense, the local users and residents are critical stakeholders in the process of
establishing management plans, which can support its implementation and respect in practice.
366 Caterina Casagranda

5.3. Lessons from Ethno-Science and Fishery Management

The extent of marginalisation and neglect of local knowledge among scientists during the
Safeguard Study and afterwards came as a surprise and is worth pointing out. The personal
experience that alternative resource practices are often denigrated as backward, inefficient
and founded on myth and ignorance is in keeping with Poizat & Baran (1997) who observed
that scientists and environmental managers have generally disregarded the possibilities of
learning from the local communities. It is, however, evident that identifying conservation
priorities based on the best available science alone will not solve conservation problems. - I
agree with Huntington (2000) that this is due to continued inertia in recognising that such
practices can provide an important information base for integrated resource management,
especially in the southern countries, where biological data are usually scarce to non-existent
(Johannes 1981, Dieges 1999, Valbo-Jorgensen & Poulsen 2001). Human communities which
rely directly on their natural resources for subsistence have often developed elaborate
processes for protecting and managing their resources (Gadgil et al. 1993, Berkes 1999).
Furthermore, traditional knowledge benefits from its low cost, both in time and material, and
from the integrative nature of the source which potentially allows the acquisition of
information at several temporal and spatial scales (Mackinson 2001, Valbo-Jorgensen &
Poulsen 2001). To be useful for resource management, however, it must be systematically
collected and scientifically verified. The main difficulty for natural scientists is accessing
traditional ecological knowledge, which is rarely written down and which makes social
science-based approaches necessary (Berkes & Folke 1998). But, the alternative approach for
using the local resource practice as a source of information on lagoon ecology is by
recognizing that villager‘s daily observation of their own ecological system, together with
traditional knowledge learned from elders, could be beneficial to ecological studies and can
also be used as a preliminary stage of an ecological investigation (Valbo-Jorgensen &
Poulsen 2001).

5.4. A New Old Approach

Recent studies on traditional knowledge (Aswani & Hamilton 2004, Wiber et al. 2004,
Silvano & Begossi 2005, Aliaume et al. 2007) confirm that these ―diachronic‖ observations
can complement the ―synchronic‖ observations on which scientifically achieved management
practices are based. This knowledge has accumulated through a long series of observations
transmitted from generation to generation in a constantly evolving adaptation to risk, based on
empirical and practical experience. In addition, it provides a way of checking whether
scientific recommendations are implementable and provides a shortcut to pinpoint essential
scientific research needs (Mackinson 2001).
Although I acknowledge that there are many conceptual and empirical problems inherent
in improving management planning, I think this exercise is essential in order: (1) to establish
at least a first approximation of the relative magnitude of global lagoon functions and services
in the case of Ichkeul; (2) to make the range of potential values of traditional lagoon
knowledge more apparent; (3) to highlight the role that traditional knowledge can and should
 Involvement of Local Users is the Overlooked Background Information … 367

play in regional efforts for conservation; (4) to point out the need to overcome practical and
methodological barriers; and (5) to stimulate additional research and debate.

ACKNOWLEDGMENTS
The author is grateful to Frank Columbus, Nova Science Publishers, for the invitation to
contribute to this book. In preparing this chapter, the author thanks the participants in the
Safeguard Study for discussions of their views on Ichkeul and for providing access to many
of the unpublished works and reports which are not easily available to international readers.
Thanks are due to the Centre d‘Océanologie de Marseille for work facilities. The work would
not have been possible without the support of Prof. Charles François Boudouresque. The
author is of course solely responsible for the views expressed in this presentation. Finally,
thanks are due to Michael Paul for improving the English text.
For Mabrouka and her sons, and all the children of their generation who will have to deal
with all that my generation has bequeathed to the 21st century.

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Editor: Adam G. Friedman, pp. 371-396 © 2011 Nova Science Publishers, Inc.

Chapter 13

BIRTH, EVOLUTION AND DEATH OF A LAGOON:

LATE PLEISTOCENE TO HOLOCENE
PALAEOENVIRONMENTAL RECONSTRUCTION
OF THE DOÑANA NATIONAL PARK (SW SPAIN)

F. Ruiz1, *, M. Pozo2, M. I. Carretero3, M. Abad1,

M. L. González-Regalado1, J. M. Muñoz4, J. Rodríguez-Vidal1,
L. M. Cáceres1, J. G. Pendón5, M. I. Prudêncio6 and M. I. Dias6
1
Departamento de Geodinámica y Paleontología, Universidad de Huelva,
Avda.Tres de Marzo, s/n, 21071-Huelva, Spain
2
Departamento de Geología y Geoquímica, Universidad Autónoma de Madrid,
28049-Madrid, Spain
3
Departamento de Cristalografía, Mineralogía y Química Agrícola,
Universidad de Sevilla, Apdo. 553, Sevilla, Spain
4
Departamento de Estadística e Investigación Operativa,
Universidad de Sevilla. 41071- Sevilla, Spain
5
Departamento de Geología, Universidad de Huelva, Avda.
Tres de Marzo, s/n, 21071-Huelva, Spain
6
Instituto Tecnologico e Nuclear. EN-10, 2686-953-Sacavém, Portugal

ABSTRACT
A multidisciplinary study of sediment cores from Doñana National Park (SW Spain),
a broad region of wetlands in SW Spain, provides the base for the reconstruction of the
main palaeoenvironmental changes that occurred in the Guadalquivir estuary since OIS 3.
The facies analysis differentiates six main facies, deposited in freshwater pond and marsh
(FA-1: laminated silt), brackish marsh or the periphery of a brackish lagoon (FA-2:
greyish silt), a shallow lagoon (FA-3: green silt and clay), the marine connection of this

*
Corresponding author: Email: ruizmu@uhu.es
372 F. Ruiz, M. Pozo, M. I. Carretero et al.

lagoon (FA-4: yellow silt) or sandy spit (FA-6: yellow sand), whereas FA-5 includes
bioclastic silt and sand with a tsunamigenic origin.
The vertical arrangement of these facies, their dates and a detailed comparison with
previous works permit to delimitate ten phases in the Late Pleistocene to Holocene
evolution of this lowland. In the oldest phase (OIS 3), this area was occupied by
freshwater marshes. Phase 2 (OIS 2) was characterized by the alternation of freshwater
and brackish marshes, partly enclosed by aeolian units. During the third phase (Early
Holocene), the brackish marshes constituted the northern limit of a broad lagoon that
extended along the present-day inner shelf. The sea-level highstand of the Present
Interglacial (Flandrian transgression, phase 4: ~6.5 cal BP) caused the inundation of this
area, occupied by an open lagoon. Between 6.5 and 4.6 cal ka (phase 5), incipient
brackish marshes emerged along the margins of this lagoon and a first tsunamigenic
event (5100-4800 cal BP) eroded partially the Doñana spit. The following phase (4.6-3.7
cal ka) was relatively quiet, with predominance of infilling processes. This calm scenario
was interrupted by a new period of instability (phase 7: 3.7-3 cal ka), with two new high-
energy events. The progressive infilling is the main feature of phase 8 (3-2.2 cal ka), with
the emersion of new brackish marshes and a decreasing depth in the adjacent lagoon. The
first historical tsunamis (phase 9: 2.2-1.9 cal ka) induced the creation of washover fans
and bioclastic ridges overlying the previous marshes. Since 1.9 cal ka (phase 10), the
growing of the Doñana spit and the fluvial-tidal sediment inputs caused an important
filling of the Guadalquivir estuary (Doñana National Park), only interrupted by new
tsunami records (~1.8-1.5 cal ka).

1. INTRODUCTION
The Pleistocene-Holocene geological record of littoral areas has received an increasing
attention in the last decades. The multidisciplinary analysis of cores collected in lagoons,
estuaries, salt marshes or deltas has revealed a broad information about the
palaeoenvironmental evolution of these environments, global or regional sea-level changes,
palaeoclimatology or the effects of anthropogenic actions during this period (Borrego et al.,
2004; Vilanova et al., 2006; Selby and Smith, 2007). In this scenario, the mineralogical
composition is an important tool to infer the origin of sediments, the variations of some
physical-chemical water parameters or even palaeoclimatic oscillations (Chamley, 1989;
Carretero et al., 2002; Mackie et al., 2007).
This record includes distinctive sedimentary layers that have been attributed to storms,
cyclones, hurricanes or tsunamis. These high-energy events cause the deposition of
sedimentary layers with characteristic textural and mineralogical features (Clague et al., 2000;
Singarasubramanian et al., 2006; Babu et al., 2007). In most cases, these investigations are
concentrated on a single event (Dawson and Smith, 2000; Wagner et al., 2007), although even
six tsunamis have been recognized in a single section (e.g., Cisternas et al., 2005).
The southwestern Spanish coast is a low-probability tsunamigenic area (Galbis, 1932,
Campos, 1991; Reicherter, 2001), with sixteen documented tsunamis between 218 BC and
1900 AC. Nevertheless, its geological record is poorly known at present (e.g., Luque et al.,
2001; 2002; Ruiz et al., 2004; 2005a; Scheffers and Kelletat, 2005).
The aim of this chapter is to delimitate the main sedimentary facies deposited in the
Doñana National Park (SW Spain) during the Late Pleistocene-Late Holocene period, with
special attention to their textural, mineralogical and palaeontological features. Its vertical and
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 373

lateral dispositions, together with radiometric datings, will permit to reconstruct the
palaeoenvironmental evolution of this area in relation with climatic changes and sea level
oscillations.

2. STUDY AREA
The Doñana National Park (SW Spain) is located on the western bank of the
Guadalquivir estuary, with an extension of 50,720 ha (Figure 1). This area constitutes one of
the largest wetlands in Europe, composed mainly of salt and freshwater marshes that include
temporary ponds and have a modest topographic gradient (0-1 m). These marshes are drained
by two main tributaries (Guadiamar River and Madre de las Marismas Creek) and numerous
ebb-tide channels, with recent and former banks occupied by clayey levees and both
bioclastic and beach-morphology ridges (Figure 1: Veta la Arena, Las Nuevas). In addition,
they are locally covered by sandy ridges located very close to the Doñana spit and disposed in
a NE-SW direction (Figure 1: Carrizosa, Vetalengua).
These inner zones are partly protected by two sandy spits (Doñana and Algaida; 0-30 m
height). They include active dune systems disposed in narrow (< 100 m) and elongated (1–2
km) alignments.
The main hydrodynamic processes are controlled by the fluvial regime, tidal inputs, the
southwestern dominant wave action and the southeastern drift currents. The Guadalquivir
River has a very irregular regime, with an annual mean of 185 m3s-1 and a maximum up to
1000 m3h-1 (Vanney, 1970; Menanteau, 1979). The tidal regime is mesotidal and semidiurnal,
with an average tidal range of approximately 3.6 m (Borrego et al., 1993).

3. MATERIALS AND METHODS

3.1. Textural, Mineralogical and Paleontological Analyses

Two long cores (Figure 1: PLN -93 m-; CM –31 m-) were collected by the Geological
Survey of Spain in the southern part of the Doñana National Park. Additional samples were
obtained from seven short cores included by Ruiz et al. (2004; 2005a) in previous works. The
main facies were established from lithological descriptions complemented with the grain-size
analysis of seventy representative samples, owing the predominance of detrital facies (Figures
2-3-4). Grain-size distribution was determined by wet sieving for the coarser fractions (>100
&#956;m). Fractions lesser than 100 &#956;m were analyzed by photosedimentation
(MicromeriticsR SediGraph 5100 ET). Na-hexametaphosphate has been used as a dispersing
agent.
The mineralogical analysis of samples was carried out by means of X-ray diffraction
(XRD) using a Siemens D-5000 equipment with a scanning speed of 102θ/min and Cu-kα
radiation. XRD studies were performed both on randomly oriented samples (total fraction)
and clay fraction samples (< 2 µm), the last prepared from cation-saturated, ultrasonic treated
suspensions oriented on glass slides. The identification of the clay fraction minerals was
carried out on oriented Mg2+-saturated samples with ethylene glycol salvation, and also after
374 F. Ruiz, M. Pozo, M. I. Carretero et al.

heating at 5500C following K+ saturation. When required, carbonates were eliminated using
0.6 N acetic acid.
Quantitative estimation of the mineral content was carried out using the intensity factors
calculated by Schultz (1964) and Barahona (1974). Results from 65 bulk samples and 41
oriented clay samples are shown in Tables 1 and 2, respectively.

Figure 1. Geographical setting and geomorphology of the Doñana National Park, with location of the
cores
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 375

Figure 2. Long Cores. Distribution of facies and mineralogical samples

Figure 3. Short cores. Distribution of facies and mineralogical samples

376 F. Ruiz, M. Polzo, M. I. Carretero et al.

In addition, the >63 µm fraction was revised under stereoscopic microscope, in order to
effectuate a general revision of the palaeontological record. This revision includes the
taxonomical determination and the estimation of both densities and diversities of bivalves,
gastropods, ostracods and foraminiferids. In addition, the presence and relative abundance of
other groups (scaphopods, barnacles, bryozoans, crabs) have been also detailed.

3.2. Mathematical Procedures

A multivariate analysis was applied to determine the mineralogical sample groups based
on the percentages computed of the main minerals (quartz, calcite, phyllosilicates, feldspars
and dolomite). An initial clustering procedure is applied using a hierarchical agglomerative
technique with the application of the Euclidean distance and the Ward linkage. Results are
contrasted by discriminant analysis, by determining both the dimensions and variables on
which the groups differ. In addition, a stepwise selection procedure was computed and the
contribution of each of the predictor variables to the overall discrimination was determined.
The error rate estimation was obtained by a final cross-validation method. These statistical
techniques were carried out using several subprograms of the Statistical Package for the
Social Sciences (SPSS™). Further details of these techniques may be consulted in Dillon and
Goldstein (1984).

3.3. Radiocarbon Chronology

Two new dates were produced at the Beta Analytic Laboratory (Miami, USA) by
radiocarbon analysis of mollusc shell (Figure 6. core CM), whereas the remaining twelve
dates were obtained from Ruiz et al. (2004; 2005 a, b) and Pozo et al. (2010). All data were
calibrated using CALIB version 5.0.2 (Stuiver and Reimer, 1993) and the Stuiver et al. (1998)
calibration dataset. The final results correspond to calibrated ages (ca.) using 2σ intervals,
with the reservoir corrections suggested by Soares and Dias (2006 a, b) and Soares (2008) for
this area. For the time interval 4500-4000 yr BP, more future results are necessary to
determine a mean value to be used with the marine calibration curve (Soares, personal
communication). Ages discussed below are expressed as the highest probable age of the 2σ
calibrated range (e.g., Van der Kaars et al., 2001).
In addition, the calibrated age of the maximum of the Flandrian transgression has been
used (Zazo et al., 1994; Figure 6: **) and the sedimentation rates (1.5-2.5 mm/yr) deduced
from Spanish Holocene estuarine sequences (Lario et al., 2002; Zazo et al., 2008) for the
interval 10,000-7000 yr BP have been applied to core PLN (see Figure 6: ***)

3.4. Palaeogeographical Reconstruction

The palaeogeographical evolution of this area has been possible with: a) the inclusion of
numerous data obtained by Lario (1996), Zazo et al. (1999) and Yll et al. (2003) in other
cores of the Doñana National Park; b) the analysis of several boreholes drilled near the
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 377

Guadiamar River mouth by Salvany et al. (2001); c) the palaeogeographical interpretation of

numerous seismic profiles effectuated in the Cádiz Gulf (Lobo et al., 2001; 2002); and d)
previous analyses of short cores (Figure 3) by Ruiz et al. (2004; 2005a).

4. RESULTS AND DISCUSSION

4.1. Facies and Palaeoenvironmental Interpretation

Six main facies have been differentiated:

Facies FA-1. Laminated silt.This facies occupies the lowest 30 m of core PLN and the
upper 32 cm of core GR. It consists mainly of clayey silt (Figure 2: Facies FA-1-a), with up
to 65 % of sediments included in the 40 µm-4 µm grain size interval. These sediments show a
fine parallel lamination, with alternation of greyish to greenish (colour 6/1; Munsell scale)
and blackish (colour 4/1) layers. Some layers of sandy-clayey silt (Facies FA-1-b: sand ~10-
15 %) are also interbedded within this general pattern. Phyllosilicates (42-73 %) are clearly
dominant over calcite (11-21%), quartz (8-13 %) and feldspars (2-27 %) in the clayey-silty
layers, whereas quartz increases remarkably (20-40%) in the sandier laminae. The clay
mineral contents are very variable (smectites: 25-56 %; illite: 25-56 %; kaolinite: 4-27 %).
The microscopical analysis reveals the presence of numerous reddish, oxidized fragments
of roots and phanerogams, scarce gyrogonites of characeans (Chara sp., Nitella sp.) and
isolated fragments of undifferentiated bivalves. A freshwater ostracod assemblage
(Cyprinotus salinus, Cyprideis torosa, Ilyocypris gibba, Cyprideis torosa, Herpetocypris
chevreuxi, Cypris bispinosa) is very abundant in core GR, whereas only scarce specimens of
the two first species have been found in core PLN.

Interpretation. The main features of Facies FA-1-a have been observed in temporary
ponds and the surrounding freshwater marshes of the Doñana National Park, with similar
ostracod and characean assemblages (Ruiz et al., 1996; Santos et al., 2006). These ponds are
very shallow (< 1 m in most cases) and contain alkaline, fresh to oligohaline waters (Serrano
and Toja, 1995). Fine laminations will indicate a calm environment with a cyclic
sedimentation suggested by the alternating color shades, probably due to alternating dry or
wet periods, pulses from small tributaries or the vegetation distribution (Whittecar et al.,
2001; Harter and Mitsch, 2003). The almost absence of microfauna in the oldest sediments
may be due to the dissolution of the thin carapaces of the freshwater species (e.g., ostracods),
a process very usual in similar (paleo-)environments during the oxidation of organic matter
(Hoge, 1994; Smith, 1997). The higher grain size of Facies FA-1-b and the absence of faunal
remains are attributed to increasing fluvial inputs.

Facies FA-2. Greyish silt. This facies is widely represented in almost all cores and is
constituted by silt and clay (silt: 55-70 %; clay: 26-43 %) with greyish to greenish colours
(colour 5Y 4/2). Up to 70 % of sediment is comprised between 15 and 2 µm (Figure 4), with
high percentages of fine and very fine silt. They are massive or show a very tenuous
lamination. Phyllosilicates are the main mineral components (24-73 %; mean 48 %), although
378 F. Ruiz, M. Pozo, M. I. Carretero et al.

both quartz (8-34 %; mean 14 %) and calcite (8-35 %; mean 23.3 %) increase in relation to
FA-1. Smectites (> 44 % in most cases) are dominant over illite (mean: 37.2%) and kaolinite
(11.7 %).

Figure 4. Photosedimentation grain-size analyses of the six facies differentiated, expressed as mean
percentages of each grain size interval in each facies. See differences between subfacies in the text

The palaeontological record includes low densities of a high brackish ostracod

assemblage (mainly C. torosa, Loxoconcha elliptica, Leptocythere castanea), salt marsh
foraminifers (Ammonia tepida, Jadammina macrescens, Haynesina germanica, Trochammina
inflata), scarce pulmonate gastropods and undifferentiated fragments of stems and roots.
Reworked specimens of planktonic foraminifers, spines of echinoderms, bryozoans and
marine or brackish bivalves (Cardium edule, Venerupis decussatus) are frequent.
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 379

Table 1. Bulk mineralogy of selected samples

SAMPLES Quartz Calcite Phyllosilicates Feldspars Dolomite Others

CM-9 10 22 62 3 3 0
CM-8 27 24 40 3 3 3
CM-6 44 20 15 19 2 0
CM-5 71 4 3 21 1 0
CM-3 13 23 56 2 6 0
PLN-28 13 28 42 7 7 3
PLN-27 14 31 33 8 11 3
PLN-26 10 19 54 3 9 5
PLN-25 16 26 45 4 2 7
PLN-24 14 28 43 4 8 3
PLN-23 10 22 34 24 9 1
PLN-22 12 12 35 13 24 4
PLN-21 16 21 51 7 5 0
PLN-20 14 28 44 5 6 3
PLN-19 20 20 55 2 3 0
PLN-18 14 31 32 5 17 1
PLN-17 13 24 41 15 5 2
PLN-16 18 24 33 8 14 3
PLN-15 20 32 35 6 7 0
PLN-14 12 33 45 4 6 0
PLN-13 8 23 61 3 5 0
PLN-12 7 31 49 5 6 2
PLN-11 14 34 32 8 12 0
PLN-10 17 28 31 14 8 2
PLN-9 14 21 24 8 32 1
PLN-8 9 27 44 8 12 0
PLN-7 34 8 24 23 11 0
PLN-6 8 18 67 5 2 0
PLN-5 14 16 47 5 18 0
PLN-4 11 11 48 27 3 0
PLN-3 39 15 28 13 5 0
PLN-2 12 21 52 11 4 0
PLN-1 13 32 42 4 9 0
AR2 62 2 30 5 1 0
AR1 13 15 43 2 2 25 (Gypsum)
BR3 4 40 56 0 0 0
BR2 16 21 54 3 4 2
BR1 11 20 62 0 2 5
CR5 75 21 3 1 0 0
CR4 23 24 46 3 4 0
CR3 17 34 43 1 4 1
380 F. Ruiz, M. Pozo, M. I. Carretero et al.

Table 1. (Continued)
SAMPLES Quartz Calcite Phyllosilicates Feldspars Dolomite Others
CR2 20 23 53 2 2 0
CR1 41 35 20 2 2 0
DR3 88 1 6 5 0 0
DR2 75 2 11 10 1 1
DR1 12 16 67 1 4 0
FR6 42 25 13 8 12 0
FR5 45 21 10 8 16 0
FR4 37 30 12 13 8 0
FR3 14 35 44 4 3 0
FR2 36 22 31 4 7 0
FR1 18 20 53 4 5 0
GR3 8 14 73 3 2 0
GR2 11 20 61 3 5 0
GR1 13 21 58 3 4 1
HR10 18 21 53 3 3 2
HR9 10 19 60 5 3 3
HR8 9 21 61 2 3 4
HR7 9 20 65 2 2 2
HR6 11 21 61 2 3 2
HR5 10 24 58 4 2 2
HR4 12 25 55 4 2 2
HR3 13 32 47 1 3 4
HR2 16 27 49 2 3 3
HR1 16 19 51 9 3 2

Interpretation. This facies has intermediate characteristics between FA-1 and FA-3. The
microfossil assemblages are characteristic of brackish marsh or the surrounding margins of a
brackish lagoon. Tidal flows introduced marine faunas toward the more protected areas of this
lagoon. Both mineralogical and palaeontological records are very similar to those observed in
the inner areas of perimediterranean lagoons (Carbonel and Pujos, 1982; Montenegro and
Pugliese, 1996; Ruiz et al., 2006b).

Facies FA-3. Green silt and clay. It consists of greenish clayey silt or silty clay (colour
10YR 5/3), with up to 70 % of sediment (dry weight) comprised between 30 µm and 1 µm
and very low sand contents (< 4 %). This facies exhibits a fine parallel lamination, with
coarse laminae (5-10 cm thick) well defined and scarce evidence of bioturbation.
The bulk mineralogy is dominated by phyllosilicates (32-62 %), reaching usually up to 41
%. Calcite (19-32 %; mean 24 %) and quartz (10-23 %; mean 15.5 %) have more
homogeneous distributions than FA-2, although similar mean values. The highest contents of
feldspars (1-15 %) and dolomite (2-17 %) were found in core PLN (20-25 m depth).
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 381

Table 2. Clay mineralogy of selected samples

SAMPLES Smectites Illite Kaolinite

CM-9 45 38 17
CM-3 46 42 12
PLN-26 30 51 19
PLN-25 26 53 21
PLN-21 32 48 20
PLN-17 31 49 20
PLN-14 38 39 23
PLN-12 58 31 11
PLN-11 44 41 15
PLN-6 31 46 23
PLN-4 56 25 19
PLN-2 25 56 19
PLN-1 47 42 11
AR2 67 31 2
AR1 54 40 6
BR3 41 52 7
BR1 67 29 4
CR5 35 59 6
CR4 50 37 13
CR3 46 50 4
CR2 56 35 9
CR1 52 39 9
DR3 61 37 2
DR2 29 59 12
DR1 56 34 10
FR6 26 60 5
FR4 35 54 11
FR1 49 39 12
GR3 41 51 8
GR2 28 68 4
GR1 53 40 7
HR10 47 43 10
HR9 42 50 8
HR8 34 57 9
HR7 43 49 8
HR6 57 33 10
HR5 60 33 7
HR4 55 36 9
HR3 57 37 6
HR2 51 41 8
HR1 58 36 6

Clay minerals show an interesting contrast between core PLN and the remaining ones. In
the upper part of this core, illite is clearly dominant (48-53 %) over smectites (26-32 %),
whereas these latter are more abundant (51-67 %) in the inner cores or near the protected,
landward side of the Doñana spit.
382 F. Ruiz, M. Pozo, M. I. Carretero et al.

Macrofauna is composed of brackish (mainly Cardium edule) and marine (Venerupis

decussatus, Chamelea gallina) bivalves, together with less frequent specimens of marine
gastropods (Rissoa, Hinia). Ostracods (2-200 individuals/gram; C. torosa, L. elliptica, L.
castanea) and foraminifers (10-1,000 individuals/gram; A. tepida, H. germanica) are frequent
to very abundant in these sediments. The reworked marine faunas of ostracodes, planktonic
foraminifers, spines of echinoderms, fragments of bryozoans or central diatoms may be
locally abundant, composing 20-40 % of the paleontological record.

Interpretation. The most representative species of both ostracodes and foraminifers are
well represented in the deeper, subtidal areas of brackish lagoons (salinity up to 15-20 0/00),
located near a river mouth. In these coastal areas, the tidal renewal is conditioned by the
dimensions of outlets that cross the external, elongated sandy spits (Marocco et al., 1996;
Samir, 2000; Ruiz et al., 2006a). This marine influence is contrasted by the presence of
reworked faunas derived from the adjacent infralittoral zone (Pérez Quintero, 1989; Ruiz et
al., 1997). The different clay mineralogy may be explained by the more open location of core
PLN within this lagoon, with inputs of illite-rich, silty-clayey sediments from the shelf. In
these shallow marine areas of southwestern Spain, illite is dominant over smectites
(Gutiérrez-Mas et al., 1997).

Facies FA-4. Yellow silt. It is constituted by off-white to pale yellow, sandy-clayey silt
(colour 8/2 to 8/3), poorly sorted, with very low to moderate percentages of sand (4-20 %).
They present a very tenuous low-angle cross stratification, parallel lamination or absence of
patent sedimentary structures.
These fine-grained sediments are characterized by moderate to high percentages of quartz
(20-44 %) and low to moderate phyllosilicate contents (15-35 %), In addition, calcite exceeds
20 % and feldspars can be significant (~ 20 %) in the upper part of core CM. Smectites and
illite show similar proportions (40-50 %).
Macrofauna is abundant, with numerous valves and fragments of marine molluscs,
including bivalves (C. gallina, V. decussatus, Acanthocardia tuberculata), gastropods (Rissoa
spp., Hinia reticulata, Lemintina arenaria) and scaphopods (Dentalium vulgare, D.
sexangulum). Benthic marine foraminifers (50-300 individuals/gram; Ammonia beccarii,
Quiqueloculina spp., Elphidium crispum) and ostracodes (Palmoconcha turbida,
Pontocythere elongata, Urocythereis oblonga) are dominant over brackish species. Fragments
of bryozoans, plates of barnacles, claws of crabs, or planktonic foraminifers (Orbulina,
Globigerina, Globigerinoides) are also abundant.

Interpretation. The most abundant assemblages of molluscs, ostracodes and foraminifers

of this facies characterize the shallow areas (< 40 m depth) of the southwestern Spanish shelf
(Pérez Quintero, 1989; Ruiz et al., 1997; González-Regalado et al., 2000). These assemblages
and some brackish specimens (C. torosa, L. castanea) are usually found in the marine zones
of perimediterranean lagoons, very close to the natural or artificial inlets and subjected to
moderate to high hydrodynamic gradients (Ruiz et al., 2000; 2006, a; b).

Facies FA-5. Bioclastic silt and sand. This facies is the main constituent of several
bioclastic ridges located in the margins of recent or former tidal channels (Figure 1: Veta la
Arena, Las Nuevas). These sedimentary beds are characterized by a large lateral extension (3-
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 383

6 km) and a narrow width (20–30 m). Thickness (5-70 cm in most cases) decreases landward,
being disposed usually over FA-2 or FA-3. They display an erosive base, with vegetation
remains and intraclasts of the underlying sediments in the lower centimetres. In the upper
part, bioclasts were disposed in thick laminae (3-5 cm) or present a disorganized disposition,
being fragmented in most cases.
Texture permits to delimitate two subfacies, with a bimodal grain size distribution and a
poor sorting in both cases:

Subfacies FA-5-a. Bioclasts are included in a greenish, clayey-silty matrix (colour 5Y

8/3), with moderate sand contents (10-25 %). Phyllosilicates (43-65 %) are clearly dominant
over calcite (19-40 %) and quartz (4-18 %). Illite is the main clay mineral (43-68%), with
percentages slightly higher than smectites (28-47 %). This subfacies is dominant in Veta la
Arena and the northeastern part of Las Nuevas.

Subfacies FA-5-b. It is represented in the cores located near the Doñana spit. This
subfacies will be transitional to FA-6, with bioclasts included in a greenish to greyish silty-
sandy matriz (colour 5Y 8/6). The mineralogical composition is very variable, ranking from
quartz-rich samples (quartz up to 70 %) to others dominated by phyllosilicates (30-40 %) and
calcite (12-31 %). Dolomite can be occasionally important (10-24 %). Illite ranges between
50% and 60% in all samples. This subfacies is well represented in Vetalengua and the
southwestern part of Las Nuevas. In this last ridge, grain size seems diminish landward and
easternward. In general, these ridges fines upward, passing from basal fine sands to very fine
sands with important silty percentages near the top.
Molluscs represent an important proportion (10-40 % dry weight) of the sediment. Shell
debris and disarticulated bivalve shells of estuarine (mainly Cardium edule) and marine
(mainly Acanthocardia tuberculata, Donax vittatus and Spisula solida) are abundant.
Gastropods are represented by freshwater (Gyraulus laevis, Melanopsis) and marine (Rissoa,
Lemintina, Hinia) specimens. Fragments of barnacles, scaphopods and bryozoans are also
frequent.
Microfauna is better represented in subfacies FA-5-a, with 50-500 individuals/gram of
brackish ostracodes (C. torosa, L. elliptica) and foraminifers (A. tepida, H. germanica),
together with marine specimens of both groups (Basslerites berchoni, Carinocythereis whitei,
Urocythereis britannica, Ammonia beccarii, Elphidum crispum). Some marine miliolids are
also abundant (Triloculina, Quinqueloculina), with a frequent loss or rupture of the last
chambers. Brackish ostracodes present a high-energy population structure, with numerous
individuals (>70 % in most of samples) belonging to adults or A-1 to A-3 moults. Only scarce
specimens of brackish species were observed in the sandier samples of subfacies FA-5-b.

Interpretation. These ridges show numerous features that have been described in
tsunamigenic deposits (Bryant et al., 1992; Bryant, 2001; Costa et al., 2004; Dawson and
Steward, 2007): a) an erosional base; b) presence of intraclasts plant remains near the base; c)
finer sediments toward the top; d) finer sediments landward; e) presence of higher sand
percentages (near the Doñana spit) in relation to the underlying sediments; f) changes in the
clay mineral composition, with a general dominance of illite, probably derived from the
adjacent shelf where this clay mineral is dominant (Gutierréz-Más et al., 1997); g) strong
changes of fauna in relation to the underlying layers; h) presence of numerous marine species
384 F. Ruiz, M. Pozo, M. I. Carretero et al.

of both macrofauna and microfauna with evidence of reworking; or i) high-energy population

structures on ostracodes. Consequently, a tsunamigenic origin has been attributed to these
beds.

Facies FA-6. Yellow sand. This facies is represented in the uppermost part of the sandy
ridges (Carrizosa, Vetalengua) and the dune system of the Doñana spit (core CM). These
layers consists of well sorted, fine to very fine sand with intense yellow shades (colour 10Y
8/6). Up to 60 % of sediment presents a grain size comprised between 500 µm and 80 µm. In
the upper levels of core CM, this facies exhibits cross stratification, whereas sand is massive
in cores AR and DR. Quartz (62-88 %) is dominant over phyllosilicates (3-30 %) and
feldspars (5-21 %). Smectites (54-56 %) are the main clay minerals, with minor proportions
of illite (34-40 %) and kaolinite (6-10 %).
Both macrofauna and microfauna are virtually absent, with exception of some isolated
and fragmented remains of the bivalve Corbula gibba.

Interpretation. These sediments constitute the dune systems of the Doñana spit. The
mineralogical records obtained coincide with those indicated by Flor (1990) and the Spanish
Environmental Ministry (2005) in these aeolian beds.
The sandy ridges of Carrizosa and Vetalengua show the same textural, mineralogical and
faunal features. They occupy the margins of former meanders within the old lagoon system
and are disposed at high angles in relation to the Doñana spit. The contact with this sandy bed
coincides with the presence of an erosive surface within the dune systems of the spit
(Rodríguez Ramírez et al., 1995) and a remarkable slimming of its width.
The presence of these sand layers over FA-2 or FA-3 may be indicative of old tsunamis,
with a partial rupture or erosion of the spit and the deposit of washover fans in its inner side.
In a second episode, these washover fans would be reworked by the tidal fluxes and deposited
in the margins of old tidal channels, constituting the sandy ridges of Carrizosa and
Vetalengua. Simultaneously or in a later stage, a part of these washover fans would be
dismantled and their almost azoic sands were introduced toward the inner areas of the lagoon,
being deposited (as FA-5-b) over fluvial levees or marshes. The vertical facies disposition of
core DR, with basal bioclastic layers below sandy beds, is very similar to that indicated in
some washover fans of the southwestern Spanish coast and southeastern Asia, derived from
recent and past tsunamis (Luque, 2002; Hori et al., 2007).

4.2. Statistical Analysis

4.2.1. Cluster groups

Cluster analysis permits to separate two main groups (Figure 5, A). Group 1 (52 samples)
is characterized by high percentages of phyllosilicates (mean 49.1 %) and calcite (> 23 % in
most cases). A more detailed analysis defines three subgroups, with very high phyllosilicate
contents (Subgroup 1.1), high to very high percentages of both feldspars and dolomite
(Subgroup 1.2) and the highest mean percentages of calcite of all groups or subgroups
(Subgroup 1.3). The clay mineral pattern of the two first subgroups is unclear, with variable
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 385

percentages of smectites (25-67 %) and illite (25-68 %). Smectites are generally dominant
over illite or both present similar contents in the third subgroup.
Samples (13) of Group 2 consist mainly of quartz (mean 53 %), with phyllosilicates and
calcite as secondary constituents. The quartz contents differentiate clearly two subgroups
(Subgroup 2.1: mean ~ 40 %; Subgroup 2.2: mean ~ 74 %). Illite is dominant in subgroup 2.1,
whereas subgroup 2.2 can be divided between azoic (Figure 5: 2.2.A: smectites: 61-67 %;
illite: 31-37%) and bioclastic (2.2.B: smectites: 29-35%; illite ~ 59 %) layers.

4.2.2. Cross-validation
In this final step, all samples are included in the same initial cluster, indicating a true
separation between the two groups differentiated. In addition, 59 samples (up to 90 %) were
included in the same subgroup, whereas the remaining six were relocated in a different
subgroup within Group 1 and no changes were observed in Group 2.

4.2.3. Mineralogical Groups Vs Sedimentary Facies

A comparison between these two variables permits to observe some remarkable
coincidences (Figure 5, B). The `inner´ facies of this coastal palaeoenvironment (FA-1a:
freshwater marsh and pond; FA-2: lagoon margin and brackish marsh; FA-3: subtidal lagoon;
FA-5a: tsunamigenic, inner layers) are included in Group 1, whereas those related with
`external´ inputs (FA-1-b: fluvial; FA-4: marine; FA-5-b: tsunamigenic, externe aeolian
layers; and FA-6: aeolian) are more closely related with Group 2. The presence of some
samples belonging to FA-5-b within Group 1 would be explained by the palaeotopograhy of
the lagoon bottom, probably deeper in the central zone (upper part of core PLN).

4.3. Radiocarbon Datings

The total dataset has seventeen datings, with calibrated ages ranking from ~44 ka to 1.4
ka (Figure 6). Additional data have been inferred in core PLN from: a) the lateral correlation
with the adjacent, bioclastic ridge of Las Nuevas (Figure 6: *); b) the maximum of the
Holocene transgression in this area (Figure 6: **) inferred by Zazo et al. (1994) and Lario et
al. (1995); and c) the general sedimentation ratios (1.5-2.5 mm/yr) deduced between 7000 and
10,000 cal BP interval (Figure 6: ***) in different estuaries of the southern Spanish coast
(Lario et al., 2002; Zazo et al., 2008).

5. LATE PLEISTOCENE-LATE HOLOCENE EVOLUTION

OF THE DOÑANA NATIONAL PARK

The comparison of these data with others obtained by different investigation teams in the
Doñana National Park and the adjacent areas permits to drawn a tentative palaeogeographical
evolution of this zone. Ten phases may be delimitated:
386 F. Ruiz, M. Pozo, M. I. Carretero et al.

Figure 5. A: Cluster analysis of the mineralogical data, B: Comparison between the mineralogical
groups and the sedimentary facies
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 387

Figure 6. Correlation of the cores, with inclusion of the vertical disposition of facies, the
mineralogical groups and datings.

Phase 1 (OIS 3)

Freshwater marsh (Facies FA-1) characterized the easternmost, inner areas of the Doñana
National Park during OIS 3 (Figure 7, a-b), with an increasing hydric availability and a
moister climate in relation to OIS 4 (Yll et al., 2003; Zazo et al., 2005). This general scenario
is only interrupted by a marine input (> 45 ka) that inundated the inner areas and caused the
deposition of Facies FA-4 in core PLN. This event may be related to short-lived warmer
episodes of interstadial character (Behre, 1989), ice retreat phases (Duplessy et al., 1988), the
final phase of a warm period in southern Europe (Van Andel, 2003), a sea level rise
(Yokoyama et al., 2001) or a high-energy event. In the western sector, different aeolian units
(~ FA-6) were deposited in the El Abalario area (Zazo et al., 2005).
Sea level oscillated between -80 m and -100 m during this period (Siddall et al., 2003).
Consequently, the larger part of the adjacent shelf was exposed, with coastal deposits located
in the central area of the Cádiz Gulf (Lobo et al., 2002).

5.2. Phase 2 (OIS 2)

During the Last Glacial Maximum (Figure 7, c), the eastern part of the Doñana National
Park was occupied by alternating freshwater and brackish marshes (FA-1a and FA-2). These
inner areas are partly enclosed by aeolian units (Zazo et al., 2005).
388 F. Ruiz, M. Pozo, M. I. Carretero et al.

This phase coincides with the lowest sea level (~ -125 m to -130 m) of the last 100,000
years (Yokoyama et al., 2000). Consequently, the palaeocoastline was located at ~ 40 km to
the southwestern of its present-day position (Lobo et al., 2001).

Phase 3 (Early Holocene)

Sea level reached -50 + 5 m at 10 ka in the Cádiz Gulf (Hernández-Molina et al., 1994;
Lario, 1996), coinciding with a climatic amelioration between 10 ka and 5.4 ka in this area
(Santos et al., 2003).
In the inner shelf (Figure 7, d), the interpretation of high-resolution seismic profiles has
permitted to recognize the presence of an elongate sandy barrier that protected an adjacent
broad lagoon. Tidal channels of this lagoon had a NW-SE direction and were partially
covered by overwash deposits (Lobo et al., 2001). The northeastern part of this lagoon was
delimitated by aeolian systems (Zazo et al., 2005) and marshes (core PLN; Zazo et al., 1999).

Figure 7. Palaeoenvironmental evolution of the Doñana National Park during the last 65 ka. Left
column: Late Pleistocene to Early Holocene sea level changes (modified from Siddall et al, 2003). a-
d: southwestern corner modified from Lobo et al. (2001; 2002). Additional data obtained from Goy
et al., (1996), Zazo et al. (1999, 2005), Salvany et al. (2001), and Zazo et al. (2008)
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 389

Phase 4 (maximum of the Flandrian transgression -6.5 cal ka BP-)

In the Cádiz Gulf, river mouths were inundated around 6.5 cal ka (Zazo et al., 1994;
Borrego et al., 1999; Dabrio et al., 2000). The Doñana National Park was occupied by an
open lagoon (Figure 7, e), partially protected in its westernmost part by aeolian units (Zazo et
al., 2008). The bottom sediments were constituted by silty sand with abundant remains of
marine faunas (core PLN).
After this maximum, the Doñana spit began to grow (Goy et al., 1996), with a
progressive limitation of the tidal fluxes. In addition, the Guadiamar River caused the
deposition of alluvial terraces at ~6300 yr BP in the northern part of the park (level T2;
Salvany et al., 2001).

Phase 5 (6.5-4.6 cal ka BP)

The first part of this phase is characterized by the growth of the Doñana spit, with the
progressive emersion of the inner side of this incipient barrier (core AR). The bottom
sediments of the adjacent, quiet lagoon were composed of clayey silt (FA-3) with variable
bioclastic contents (Figure 7, f).
Between 5100 and 4800 cal BP (Figure 7, g), a tsunami caused the erosion of this spit
and the deposition of aeolian sand (FA-6) over the new salt marsh.

Phase 6 (4.6-3.7 cal ka BP)

The central part of the Doñana National Park was still occupied by an open lagoon (cores
CR and PLN), whereas the Doñana spit grew toward the southeast. This phase is dominated
by the lagoon infilling, with the deposition of phyllosilicate-rich sediments (FA-3) in the
lagoon bottom (Figure 7, h).

Phase 7 (3.7-3 cal ka)

This area was subjected to arid conditions during this period (Zazo et al., 2008). One or
two tsunami-like events (or very strong storms) caused the erosion of the Doñana spit (Figure
7, i) and the deposition of bioclastic, sandy-clayey silt over the lagoon bottom (core CR). In a
latter period, new high-energy events induced the emersion of the very shallow, southwestern
areas of the lagoon, with the deposits of FA-5 over intertidal sediments (core BR, CR and
PLN).

Phase 8 (3-2.2 cal ka)

During this phase (Figure 7, j), the southwestern part of the Doñana National area
remained emerged (cores AR-BR-CR), whereas the central and southern ones were occupied
390 F. Ruiz, M. Pozo, M. I. Carretero et al.

by a very shallow lagoon (core PLN). The continuous growing of the Doñana spit and the
progressive infilling induced the creation of new brackish marshes (cores DR-HR; core ML-
97, Zazo et al., 1999) or the transition from marine conditions to more restricted scenarios
(core CM).

Phase 9 (2.2-1.9 cal ka)

Several tsunamis eroded the Doñana spit in the following phase (Figure 7, k), with the
creation of small washover fans constituted by aeolian sediments (core DR and CM) and the
accumulation of bioclastic ridges over the lagoon borders (core HR). In addition, the subtidal
palaeoenvironments of the central part are covered by bioclastic, silty-sandy sediments (core
GR).
Additional sedimentary evidence of these events include erosive surface in the Doñana
spit (Rodríguez Ramírez et al., 1995), washover fans near the Gibraltar Strait (Luque et al.,
2002), limestone boulders located at +4 to +15 m asl near Lisbon (Scheffers and Kelletat,
2005) or a turbiditic layer in the SW Portuguese Margin (Vizcaino et al., 2006a). These
tsunamis may be assimilated to the historical tsunamis that devastated the southwestern
Iberian coasts between 218-209 BC and 60 BC (Campos, 1991).

Phase 10 (1.9 cal ka-Present)

The first period of this phase (Figure 7, l: 1900-1600 cal BP) is characterized by an
increasing infilling of the lagoon (cores FR, GR and CM), with a progressive transition
toward intertidal-supratidal conditions. This tendency was interrupted by a new introduction
of marine sediments and, to a lesser extent, aeolian sediments in the southern part of the park
(core FR and, probably, CM), owing to new high-energy events. Ages of these phenomena
coincide with those of a historical tsunami (382 BC; Campos, 1991).
The posterior palaeoenvironmental evolution of the Doñana National Park is marked by
the creation of new wetlands with temporary ponds (core GR) and the growing of the Doñana
and La Algaida spits, with aeolian sands covering intertidal sediments (core CM).
At present, no evidence of the 1755 Lisbon earthquake-induced tsunamis have been
found in this area, although some erosive surfaces located in the southeastermost part of the
Doñana spit might be originated by this event. These tsunamis settled washover fans near the
Gibraltar Strait, imbricated boulders around Lisbon or abyssal tempestites in the SW
Portuguese margin (Luque et al., 2001; Scheffers and Kelletat, 2005; Whelan and Kelletat,
2005; Vizcaino et al., 2006b)

6. CONCLUSIONS
A Late Pleistocene to Holocene evolution of the Doñana National Park has been
proposed, based on the multidisciplinary analysis (texture, colour, geomorphology,
paleontology, mineralogy, dating) of sediments present in two drill cores and seven short
 Birth, Evolution and Death of a Lagoon: Late Pleistocene to Holocene… 391

cores. This study permits to delimitate the geological features of five sedimentary facies
deposited in distinctive palaeoenvironments (freshwater and brackish marshes, open lagoon,
external lagoon and sandy spit) and a sixth, heterogeneous facies with a tsunamigenic origin.
Ten phases have been distinguished since OIS 3, with a general scenario of progressive
lagoon infilling conditioned temporary by sea level changes and high-energy events. These
events caused the deposition of washover fans and bioclastic ridges over previous marshes or
the lagoon bottom. This geological scenario was compared with climatic oscillations and sea
level changes.

ACKNOWLEDGMENTS
This work was funded by two Spanish DGYCIT Projects (CTM2006-06722 and
CGL2006-01412) and three Research Groups of the Andalousia Board (RNM-349, RNM-238
and RNM-293). It is a contribution to IGCP-495 and 526.

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 397-415 © 2011 Nova Science Publishers, Inc.

Chapter 14

THE ALVARADO LAGOON – ENVIRONMENT,

IMPACT, AND CONSERVATION

Jane L. Guentzel1*, Enrique Portilla-Ochoa2,

Alejandro Ortega-Argueta2,3, Blanca E. Cortina-Julio2
and Edward O. Keith 4**
1
Department of Marine Science, Coastal Carolina University, Conway, SC, USA
2
Investigaciones Biologicas, Universidad Veracruzana, Xalapa, Ver., Mexico
3
Ambiente y Sustentabilidad, Instituto de Ecología, Xalapa, Ver., Mexico
4
Oceanographic Center, Nova Southeastern University, Ft. Lauderdale, FL , USA

ABSTRACT
The Alvarado Lagoon System (ALS) in south-central Veracruz State, Mexico, is a
mangrove dominated coastal wetland formed by the confluence of the Acula, Blanco,
Limon and Papaloapan rivers. The ALS has a maximum width of 4.5 km, a mean surface
area of 62 km2, and is connected to the Camaronera Lagoon by a narrow channel and to
the Gulf of Mexico (GOM) via a 0.4 km wide sea channel. Water samples were collected
during the wet (September 2005) and dry (March 2003 and 2005) seasons. Salinity
ranged from 1-25.5 psu and pH was slightly alkaline (7.6-8.6). Levels of total organic
carbon (TOC), total mercury (Hg), and total suspended solids (TSS) ranged from 3.9-20.9
mg C/L, 0.92-26.1 ng Hg/L, and 1-39.2 mg TSS/L, respectively. The strong correlation
(R2=0.71; P=0.001) between total mercury and TSS in the water column suggests that
particulate matter is a carrier phase for mercury within the Alvarado and Camaronera
Lagoons.
The ALS is one of the most productive estuarine-lagoon systems in the Mexican
GOM. Model studies suggest that primary production by sea grasses provides more
energy input to the ecosystem than detritus, which is contrary to most other Mexican
GOM lagoons and estuaries. In 2004 the ALS was nominated Ramsar site no. 1355
because of its important biodiversity, ecological attributes, and high resource production.

*
Corresponding authors: Email: jguentze@coastal.edu
**
edwardok@nova.edu
398 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

Over 100 fish species have been collected from the ALS, representing four ecological
guilds: marine stenohaline, marine euryhaline, estuarine, and freshwater fishes. These
assemblages have not experienced significant changes over the past 40 years, but there
has been a recent decline in diversity. Antillean manatees (Trichechus manatus manatus)
historically have occurred in the ALS but were reduced in the 1970s and 1980s by
hunting and are now considered endangered. The rescue of 6 orphan calves between 1998
and 2000 suggests that manatees are reinhabiting the ALS as a result of conservation
measures. Manatees are most commonly sighted in the Alvarado Lagoon, Acula River
and adjacent lagoons, and are rarely sighted in the Limon River and adjacent lagoons. To
protect the manatees and their habitat an educational program was developed in 1998 and
an assessment of their current status and critical habitat in the ALS was conducted. Our
manatee conservation efforts were recognized in 2001 when September 7th was officially
declared the ―National Day of the Manatee‖ in Mexico. Almost 350 species of birds
occur in the ALS, including the Mexican Duck (Anas diazi), which is undergoing a slow
but marked decline due to habitat destruction and overhunting. The largest threats to the
ALS include unsustainable sugar cane cultivation, cattle-ranching, coastal urban
development, oil and gas exploration and exploitation, water pollution by urban waste
and agricultural runoff, and increases in port and tourism industries. Despite the
establishment of government policy and measures to protect the coastal wetlands of ALS,
the identified threats continue to menace the important biodiversity and human well-
being of the region.

INTRODUCTION
The Alvarado Lagoon System (ALS) in south-central Veracruz state (Figure 1), Mexico,
is a large mangrove dominated coastal wetland located 70 km southeast of the Port of
Veracruz. It has a total area of 2800 km2 of which 258 km2 are covered by water. The
Alvarado Lagoon (AL) is a shallow system (average depth 1.5 m) connected to the
Camaronera Lagoon by a narrow channel and to the Gulf of Mexico (GOM) via a 0.4 km
wide sea channel [Moran-Silva et al., 2005, Cruz-Escalona et al., 2007]. The AL has a
maximum width of 4.5 km and a mean surface area of 62 km2. The ALS is mainly formed by
the Alvarado, Buen Pais, Camaronera and Tlalixcoyan lagoons, but it is also associated with a
great number of smaller aquatic bodies, flood zones, and parts of the Acula, Blanco, Limon
and Papaloapan rivers. The Papaloapan River extends through the states of Oaxaca, Puebla
and Veracruz and traverses a distance of 445 km, passing through the city of Tlacotalpan and
finally emptying into the AL. The Papaloapan drainage basin covers an area of approximately
39,200 km2.
The ALS is one of the most productive estuarine-lagoon systems in the Mexican GOM
[Cruz-Escalona et al. 2007]. It is characterized by a large diversity of interactions with its
adjacent systems, particularly an extensive marsh, which contributes greatly to its biological
productivity. Seasonal changes are well pronounced and are mainly influenced by the
precipitation-drought regime conditions associated with its ecosystem. The ALS has three
separate zones based on physicochemical characteristics; Camaronera Lagoon, Buen Pais
Lagoon and the urban zone of Alvarado Lagoon, and the river zone of Alvarado Lagoon
[Moran-Silva et al., 2005].
Model studies suggest that primary production by sea grasses provides more energy input
to the ecosystem than detritus, which is the opposite of most other Mexican GOM lagoons
 The Alvarado Lagoon – Environment, Impact, and Conservation 399

and estuaries. This may be a consequence of relatively rapid flushing (50 x 109 m3 of water
each year), a short water exchange time (0.5 days), mangrove deforestation, and overfishing
[Cruz-Escalona et al., 2007]. The increase of anthropogenic activities in the surrounding
terrestrial areas coupled with limited waste management planning have contributed to both
local and regional deterioration of the hydrological characteristics of the ALS [Cruz-Escalona
et al., 2007].

Figure 1. Satellite photograph of the Alvarado Lagoon System showing the major lagoons and rivers of
the area. Image courtesy of the Consejo de Desarrollo del Papaloapan (CODEPAP, 2003), Xalapa, Ver.,
Mexico

ENVIRONMENT AND IMPACT

Mercury and Other Water Quality Parameters

We collected sediment, fish, and unfiltered water samples from the Alvarado Lagoon,
Lagoon Camaronera, and the Gulf of Mexico during the wet (September 2005) and dry
(March 2003 and 2005) seasons (Table 1). Water column pH values were slightly alkaline
(7.6-8.6) and the salinity ranged from 1-25.5 psu. Precipitation amounts for the dry season
months of March 2003 and March 2005 were 0.23 cm, and 2.79 cm, respectively, and the wet
season month of September 2005 was 272 cm. Salinity in the ALS was inversely correlated
with rainfall, with highest levels occurring in the dry season samples (March 2003 and 2005)
and lowest levels occurring in the wet season samples (September 2005) (Table 2). Our
salinity values are similar to the salinity ranges (1-14 psu) reported for the lagoon during the
2000-2001 wet, dry, and storm seasons [Moran-Silva et al., 2005]. Levels of nitrate (NO3-N
mg/L) during the 2000-2001 season ranged from 0.03-0.14 mg N/L [Moran-Silva et al.,
2005]. Our values for nitrate (NO3-N mg/L) during the 2003 dry season ranged from 0.73-2.3
400 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

mg NO3-N/L. These values are slightly higher than the 2000-2001 values and may be
indicative of increasing anthropogenic stressors within the lagoon system. Estuaries are
considered at medium risk for eutrophication when nitrate values range from 0.1-1 mg N/L
and high euthrophic risk when the values are greater than 1 mg N/L [Bricker et al., 1999]. It
has been noted that nutrient levels within the lagoon can vary seasonally and spatially as a
result of river discharge, rainfall, resuspension of sediments, and biological activity [Moran-
Silva, et al. 2005]. Concentrations of total inorganic carbon (TIC) ranged from 14.4-22.1 mg
C/L and did not vary seasonally. Levels of total organic carbon (TOC) ranged from 3.9-20.9
mg C/L, with the highest concentrations observed during the rainy season (Table 2).
Total mercury and total suspended solids (TSS) ranged from 0.92-26.1 ng Hg/L and 1-
39.2 mg TSS/L, respectively (Table 2). The strong correlation (R2=0.71; P=0.001) between
total mercury and TSS in the water column suggests that particulate matter is a carrier phase
for mercury within the Alvarado and Camaronera lagoons. A more comprehensive study of
the Alvarado Lagoon, and the Limon, Acula, Blanco, and Papaloapan rivers conducted during
the March 2003 and 2005 dry seasons and the September 2005 wet season found that mercury
concentrations were significantly correlated with total suspended solids in the water column
(R2=0.82; P<0.001) [Guentzel et al., 2007]. The mercury concentrations in the Alvarado
Lagoon, and the Blanco, Acula, and Limon rivers during the March 2003 and 2005 dry
seasons (0.9-4.9 ng Hg/L) were similar to the September 2005 wet season (1.9-4.9 ng Hg/L),
with higher Hg levels associated with higher levels of TSS. Water samples collected from the
Papaloapan River were higher in Hg (10.9-12.7 ng (Hg/L) and TSS (89.1-154.7 mg TSS/L)
during the September 2005 wet season than the March 2003 and 2005 dry seasons (0.9-2.7 ng
Hg/L; 4.8-39.7 mg TSS/L). The sites from the Papaloapan River were sampled within 12
hours of a nighttime rainfall (15cm) event during the September 2005 wet season. The
elevated Hg concentrations from this site during the wet season are likely a result of increased
particulate matter transport within the river during high flow conditions and or input of
dissolved and particulate Hg from precipitation [Guentzel et al., 2007]. A Mercury Deposition
Network (MDN) monitoring site (HD01) within this region reported a rainfall Hg
concentration of 11.4 ng Hg/L during the time period that the samples were collected from the
Papaloapan River [Mercury Deposition Network]. The water column values that we observed
for total Hg (0.92-26.1 ng/L) are below the US EPA ambient surface water quality criteria for
freshwater (0.77-1.4 µg/L) and saltwater (0.94-1.8 µg/L) (US EPA, 2006) and the Mexican
marine aquatic life criteria of 0.02 µg/L [Jimenez et al., 1999].

Table 1. Station identifications and locations for

mercury and other water quality parameters

Latitude Longitude
Station Identification (N) (W)
Alvarado Lagoon I 18 46.132 095 47.333
T 18 45.955 095 48.607
BB 18 44.995 095 44.966
Lagoon Camaronera DD 18 51.178 095 54.654
EE 18 51.589 095 55.187
FF 18 51.716 095 54.412
Gulf of Mexico AA 18 48.422 095 44.420
 Table 2. Water quality parameters measured during the March 2003 and 2005
dry season and the September 2005 wet season

, Month Station Salinity Nitrate pH Total Total Total Total

(psu) NO3-N Inorganic Organic Suspended Mercury
(mg/L) Carbon Carbon Solids (ng/L)
(mg C/L) (mg C/L) (mg/L)
Alvarado Lagoon March 2003 I 9.9 2.3±0.9 8.1 14.9±4.2 5.4±2.1a 9.1±4.5a 0.92±0.05a
March 2003 T 9.8 1.35 8.0 14.4 4.7a 1a 1.78a
March 2003 BB 6.7 1.51 7.9 14.7 3.9a 14.1a 2.67a
March 2005 T 12.9 - 8.1 22.1±0.16 9.5±0.98a 9.1±5.6a 0.92±0.03a
September 2005 T 1 - 7.6 16.7 20.9a 25a 3.8a
Lagoon Camaronera March 2003 DD 14.5 0.86 8.2 17.2 7.3 39.2 26.1
EE 14 1.08 8.2 17.6 7.8 18.6 5.2
FF 13.8 0.75 8.3 17.9 7.6 20.5 10.3
Gulf of Mexico March 2003 AA 25.5 0.73±0.8 8.6 16.4±0.47 6.5±0.04a 1.13a 1.27±0.01a
The values for March 2003 stations I and AA, and March 2005 station T represent the mean and standard deviation of 2 replicate field samples. ―a‖ denotes that
the total organic carbon, total suspended solids and total mercury data for the Alvarado Lagoon and Gulf of Mexico are taken from Guentzel et al., 2007. ―-
― denotes that there is no data for this parameter.
 Table 3. Mercury concentrations in fish, crab, shrimp, and squid and log bioconcentration
(BCF) factors from the Alvarado Lagoon system

n Total Hg (ug Hg/g-wet) Log BCF

March March September March March September
2003 2005 2005 2003 2005 2005
Brown Shrimp (Peneus aztecus)* 20, 20, 20 0.008±0.001 0.065±0.01 0.008±0.001 3.6 4.6 3.6
Bay Squid (Lolliguncula brevis)* 3 0.024±0.002 4.2
Blue Crab (Callinectes rathbunae)* 3 0.026±0.002 4.2
White Mullet (Mugil curema)* 2 0.057±0.026 5.6
Sheepshead (Archosargus 1 0.082 4.7
probatocephalus)*
Big Mouth Sleeper (Gobimorus dormitor)* 2 0.106±0.02 4.8
Fat Snook (Centropomus parallelus)* 2 0.152±0.034 4.9
Spine Snook (Centropomus ensiferus)* 1 0.184 5.1
Striped Moharra (Eugerres plumeri)* 1, 2 0.35 0.301±0.117 5.3 5.3
Catfish (Bagre marina)* 1 0.291 5.3
*The data for mercury concentration is taken from Guentzel et al., 2007. The log BCF is calculated as Log 10([Hg in tissue]/[Hg in water]). The average water
concentration of Hg was 1.6 ng/L. n=the number of samples.
 The Alvarado Lagoon – Environment, Impact, and Conservation 403

We collected sediment from the lagoons and nearby rivers within the ALS. Total mercury
at station T in the AL ranged from 13-22 ng Hg/g-wet and the %C and %N ranged from 0.23-
0.77% and 0.31-0.37%, respectively. Total Hg from sediments in the adjacent rivers (Acula,
Limon, Blanco, and Papaloapan) ranged from 10-78 ng Hg/g wet and the %C and %N ranged
from 05-8.9% and 0.31-0.9%, respectively. There was a moderate correlation (R2=0.435,
p=0.020) between the total Hg and % carbon in the sediments from the ALS [Guentzel et al.,
2007]. The total Hg values for the sediment we collected are below the threshold effects level
of 130 ng Hg/g dry for marine sediments [Buchman 1999] and are within the US EPA
background sediment criteria of 0-300 ng Hg/g dry (US EPA 1997). Aquatic biota that
represent ~87% of the annual catch from the ALS [Cruz-Escalona et al., 2007] were collected
and analyzed for total Hg (Table 3). The total Hg concentration in the invertebrate species
(shrimp, squid, crab) ranged from 0.008-0.026 μg Hg/g wet and the vertebrate species ranged
from 0.082-0.35 μg Hg/g wet. The levels of Hg in the piscivorous and omnivorous fish
(catfish, moharra) are at or slightly above the recommended consumption level of 0.3 μg Hg/g
wet [NAS, 2000].
The log bioconcentration factors for total Hg in the organisms we collected ranged from
3.9-5.3, with no observable seasonal difference (Table 3). Activities such as biomass burning
for land clearing, mangrove deforestation, and urbanization are known stressors to the ALS.
These activities are also associated with increased mercury mobilization in aquatic and
terrestrial environments, which can result in an increase in the bioaccumulation of mercury in
biota from these systems [Friedli et al., 2003; Porvari et al., 2003; Munthe et al., 2007]. There
are a large number of indigenous riverbank communities within the ALS that rely on fishing
for comestible and economic subsistence. Reported total Hg levels in hair samples from
individuals that reside and consume fish from within the ALS ranged from 0.10-3.36 µg Hg/g
(n=47) [Guentzel et al., 2007]. Of these values, 58% are above the recommended
consumption limit of 0.1 µg Hg/kg body/day which corresponds to a hair level of 1.0 µg Hg/g
[NAS, 2000]. Anthropogenic activities that mobilize Hg could result in an increase in the
mercury content of the fish and seafood from the ALS which may ultimately lead to increased
body burdens of mercury in the indigenous peoples that reside in this region.

Vegetation

The ALS features representative and diverse ecosystems of Mexico´s Gulf coastal plain,
such as coastal dunes, reed beds of Cyperus spp., cattail Typha spp., palm forests of Sabal
mexicana, Scheelea liebmannii, and Acrocomia mexicana, oak forest of Quercus oleoides;
apompales (Pachira aquatica), and a large mangrove forest dominated by Avicenia
germinans, Laguncularia racemosa, and Rhizophora mangle [Vazques-Torres, 1998]. There
are 15 distinguishable landscape units (LU) in the area [Portilla-Ochoa et al., 1998 and Silva-
López and Portilla-Ochoa 1998]. The LU were first differentiated as areas disturbed by
agricultural activities, areas disturbed by cattle ranching, and areas where human intervention
is not yet considerable, such that natural vegetation remains the dominant landscape element.
Each LU was described in terms of land use, seasonal flooding, vegetation cover (i.e. primary
and secondary), predominant exploitation systems, the physical medium (i.e. substrate origin
and soil type), hydrologic characteristics, and other data (e.g. human settlements, main roads,
404 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

and observations on deforestation, urban and rural infrastructure, and industrial development)
[Silva-López and Portilla-Ochoa 1998 ].

Fish

There are 107 fish species that have been collected in the ALS which represent four
ecological guilds: marine stenohaline, marine euryhaline, estuarine, and freshwater fishes.
Fish assemblages of the Alvarado Lagoon Estuary have not experienced significant changes
over 40 years, but there may have been a decline in fish biodiversity during that period
[Chávez-López et al., 2005a]. A comprehensive study of Mayan cichlids conducted in the
ALS, by Chavez-Lopez et al., 2005b, reports that there are three genera and seven species of
cichlids (Cichlidae) with the Mayan cichlid (Cichlasoma urophthalmus) being the species
with the highest abundance. The Mayan cichlid is distributed throughout southeastern Mexico
where it inhabits rivers and coastal lagoons. In the ALS it is distributed towards the north in
Camaronera Lagoon. The Mayan cichlid inhabits oligohaline to mesohaline sites that are well
oxygenated and contain submerged vegetation and deep transparent water. The major
abundance and biomass of this species was obtained during December to February. The diet
of Mayan cichlids is primarily herbivorous and consists mainly of plant detrital material and
algae. There are two size classes that occur during the dry and rainy seasons which
correspond to young of the year and reproductive fish. There is only one modal size class of
fish between 60–100 mm during the stormy season. Although individuals with developed
gonads are found throughout the year, the most reproductive adults are found between April
and December. The highest gonadosomatic index (GSI) values occurred during the May
through July time period of peak reproductive activity [Chávez-López et al., 2005b]. Other
families with numerous species reported within the ALS include the Eleotridae and the
Gobiidae, and the species with the highest abundance and biomass were Gambusia affinis,
Petenia splendida, Cathoropus melanopus, Diapterus auratus, and Bathygobius soporator
[Shareet et al., 2009].
A study by Pelaez-Rodriguez et al., (2005) examined the diet of demersal piscivorous
fishes captured as bycatch by the commercial shrimping fleet just ouside of the ALS . Nine
collections distributed throughout the stormy, wet, and dry seasons from November 1993 to
January 1995 yielded a total of 646 fishes which represented 10 families and 14 species.
44.9% of these collections had empty digestive tracts and were excluded from the study. The
most abundant species of dermersal predators found were Trichiurus lepturus and Synodus
foetens. Differences in food consumption of the seven most abundant predators were
observed among the 3 seasons. The greatest variety of prey (20 species) occurred during the
stormy season and the lowest variety (nine species) occurred during the dry season. Prey type
and location of prey within the water column helped to determine the classification of five
distinct trophic guilds based on an overall index of relative importance of prey. The
occurrence of these different trophic guilds may contribute to decreased competition for food
resources on the continental shelf off of Alvarado lagoon [Peláez-Rodríguez et al., 2005].
 The Alvarado Lagoon – Environment, Impact, and Conservation 405

River Otters

A study of the neotropical river otter (Lontra longicaudis annectens) and its habitat based
on personal observations and the information provided by fishermen of the ALS, yielded
three observations of adult otters hunting and eating in lagoons and rivers, together with
records of otter tracks and feces. In addition, an adult otter skin was found in a fisherman‘s
house in November 2002, where residents of the ALS said the otter was killed that year. All
of these records were collected in three of the most conserved LU of the system, which
include an area of 607 km2, encompassing more than 22.7 % of the total area of the ALS
[Silva-López, 2009]. These observations and records, along with comments made by other
Alvarado fishermen, suggest the neotropical river otter occupies the ALS year-round, and
emphasizes the need to conduct more detailed surveys and studies to determine the present
status and ecology of the ―perro de agua‖ (as it is locally known) and its habitat [Silva-López,
2009].

Manatees

Antillean manatees (Trichechus manatus manatus) have historically occurred in the ALS,
representing one of the most important areas for manatees in the southern GOM.
Overexploitation reduced their numbers in the 1970s and 1980s and they are now considered
endangered throughout their range in Mexico. However, the rescue of six orphan calves
suggests that manatees may be increasing in the ALS. Historically, the Antillean manatee was
found from northern Veracruz state along the west coast of the GOM to the eastern coast of
the Yucatan peninsula and the Mexico-Belize border [Lluch, 1965, Lefebvre et al., 2001,
Morales-Vela et al., 2005]. However; hunting, water quality degradation, and the destruction
of breeding habitat has caused a decline in the number of manatees [Campbell and Gicca,
1978, Colmenero and Hoz, 1986].
There is little information regarding the life history of manatees in the state of Veracruz.
It is not known if they migrate, as the Florida subspecies (Trichechus manatus latirostris)
does in the United States [Deutsch et al., 2003], or whether they are year-round residents of
their local habitat, as is typical of Antillean manatees in the Yucatan Peninsula of Mexico and
in Belize [Morales-Vela et al., 2000, Self-Sullivan et al., 2003]. Movements of Antillean
manatees in Chetumal Bay, on the east coast of the Yucatan Peninsula, do not appear to be
influenced by cloudiness, atmospheric pressure, or temperature, in contrast to the Florida
manatee that migrates seasonally in response to intra-annual changes in water temperature
[Axis-Arroyo et al., 1998, Deutsch et al., 2003]. However, movements of Antillean manatees
in Chetumal Bay were moderately associated with water salinity (as in Florida), depth and
group structure [Axis-Arroyo et al., 1998]. Manatees in Florida seem to prefer areas with
access to freshwater that they require for osmoregulation. The salinity in the waters of the
ALS decreases with distance from the ocean, and the potential influence of this salinity
gradient on the movements of manatees in the ALS is unknown. Manatees in Nicaragua
undergo seasonal migrations, and their daily movements appear to be influenced by tides,
which may also influence water salinity [Jimenez, 2002]. In the ALS fishermen have reported
that manatees were quite common in the region in the mid-1900s. Even though large scale
406 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

hunting of manatees was not practiced in ALS, the sale of meat in the town market of
Alvarado during the 1970‘s was common [Ortega-Argueta, 1999], and poaching continues to
be an important threat to the species. Studies conducted in the mid 1980s reported the
disappearance of manatees from the ALS [Colmenero, 1984]. Nevertheless, recent reports
from local residents of the ALS, and the incidental capture of manatee calves, have confirmed
their continued occurrence in the Alvarado region [Ortega-Argueta, 1999; Portilla-Ochoa et
al., 1999]. A recent study assessing manatee distribution and habitat utilization found that
manatees could potentially be found in 3150 km2 of lowlands and wetlands in the ALS
(Figure 2) [Ortega-Argueta, 2002]. Habitats selected by manatees include estuaries, mangrove
wetlands and unpopulated areas. The marine zone appears not to be utilized permanently by
manatees, although they may move locally between rivers along the coast through the marine
zone. Threats to the manatees in the ALS include the clearing of land for sugar cane
cultivation, cattle-ranching, coastal urban development, mangrove deforestation, increases in
port and tourism industries in the coastal zone, water pollution, and oil and gas exploration
and exploitation [Ortega-Argueta, 1999, 2002].
Rodriguez-Ibañez [2004] investigated the knowledge, use, and cultural traditions of the
inhabitants of the ALS with respect to the Antillean manatee using oral interviews. She found
a large number of correlations between the inhabitants‘ oral history knowledge of manatee
movements and habitat use with current scientific knowledge as determined by a review of
the literature. Additionally, many inhabitants knew a lot about the hunting, butchering, and
preparing of manatee meat for human consumption. Such hunting has reduced the manatee
population in the ALS to very low levels [Ortega-Argueta et al., 2003].

Figure 2. Classification of manatee habitat within the Alvarado Lagoon System (from Ortega-Argueta,
2002). Most of the best habitat lies in the lagoons along the Limon river and in lagoons between the
Limon and Acula rivers. The Papaloapan river is not good manatee habitat due to its rapid current and
channelizing with dikes that prevent animals from entering and leaving the river easily.
 The Alvarado Lagoon – Environment, Impact, and Conservation 407

During several interview surveys conducted with local inhabitants and fishermen,
besides boat and airplane surveys in 2000, 2005 and 2006 it was revealed that manatees are
common in the ALS around the year [Ortega-Argueta, 2002, Portilla-Ochoa et al., 2006,
2007, Keith et al., 2009]. Manatees are most commonly sighted in the Acula River and
adjacent lagoons, and are rarely sighted in the Limon River and adjacent lagoons (Figure 3).
Most of the interviewees reported that manatees are not as abundant now as compared to
three decades ago, but their numbers have increased in the past few years (Figure 4). Most of
the sightings are of adult animals, although females and calves are infrequently seen (Figure
5). Most sightings occur in the rainy season (Figure 6), and most sightings are unique in the
sense that an animal is usually only seen once, rather than frequently or repeatedly (Figure 6).
Respondents thought that manatees predominantly feed on marsh plants and water hyacinth,
with ―grasses‖ and other emergent plants also being important in the diet (Figure 7). A recent
survey of the ALS using visual, acoustic, and side-scan sonar methods estimated the
abundance of manatees in the ALS at 0.93 manatees/ha ± 0.39 (95% CI) [Serrano-Solis,
N.D.].

Figure 3. Locations of manatee sightings (from both vessels and aircraft), interviews and evidence of
manatee butchering (from Ortega-Argueta, 2002).
408 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

Figure 4. Increase in the number of manatee sightings over the past decade as determined by interviews
with residents of the ALS. Most of the interviewees reported that manatees are not as abundant now as
compared to three decades ago, but their numbers have increased recently. This increment in
observations may reflect a recovery of the manatee population; a more dedicated monitoring effort; or
an increase of the appeal of the species as results of the education and awareness campaigns.

Figure 5. Age-class of manatees sighted in the ALS as determined by interviews with residents. Most of
the sightings are of adult animals, although females and calves are infrequently seen

Figure 6. Seasonality and frequency of manatee sightings in the ALS as determined by interviews with
the residents. Most of the sightings occur in the rainy season and most sightings are unique in the sense
that an animal is usually only seen once, rather than frequently or repeatedly
 The Alvarado Lagoon – Environment, Impact, and Conservation 409

Figure 7. Foods of manatees as reported by residents of the ALS. Respondents thought that manatees
predominantly ate marsh plants and water hyacinth, with ―grasses‖ and other things also being
important in the diet

We also found that the inhabitants of the ALS maximized their use of the manatees killed
in the distant past, including the medicinal use of powdered manatee bones and manatee fat,
and the use of manatee bones and teeth in the production of artifacts. This suggests that
manatees played a significant role in the culture of these riverbank communities in the past. A
majority of those interviewed (82%) said they were interested in protecting animals liberated
near their homes in the ALS. However, several respondents expressed concern that neighbors
would kill released animals and/or that hunting would continue because of lack of
enforcement of the laws [Portilla-Ochoa et al., 2006, 2007, Keith et al., 2009]. Manatee
poaching continues in many areas despite official protection. This illegal activity is still
practiced for a number of reasons: tradition; an appreciation of manatee meat, which is
considered a delicacy; ignorance of national laws and sanctions in force to protect the
manatee, and limited inspection and vigilance by Mexican environmental and regulatory
authorities (Ortega-Argueta, 1999).

CONSERVATION
The coastal wetland lagoon system of Alvarado is one of the most productive such
systems in Veracruz and the third largest wetland in Mexico. A total 350 species of birds have
been registered in the ALS, including the Mexican Duck (Anas diazi), which is undergoing a
slow but marked decline due to habitat destruction and overhunting. The ALS has been
considered a high priority region for conservation [Arriaga-Cabrera et al., 1998; CONABIO,
1998; Dugan, 1993], including recognition by the North American Wetlands Conservation
Council (NWCCA), the International Council for Bird Preservation-Mexico Chapter
(CIPAMEX), and Mexico‘s Commission on Biodiversity (CONABIO). Notable, too, are the
threats, including agricultural encroachment and increasing levels of contamination from
urban wastewater and pesticides. A newly funded program will enable the municipality of
Alvarado and Pronatura Veracruz (local NGO) to strengthen the environmental education
program in Alvarado schools; teach sustainable management techniques to local communities
410 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

and train them to be conservation promoters; and develop wetland-conservation outreach

materials for use by local authorities. A conservation easement will be pursued at a site of
high importance to wetland-associated birds. Partners will work to reduce the effects of cattle
ranching on wetland resources and will continue monitoring resident and migratory birds in
the area. These activities will be coordinated with the newly formed Veracruz State
Committee for Conservation of Wetlands.
One of the most important achievements of our conservation activities in Veracruz was
the nomination of Alvarado lagoon system as a Ramsar Site. On February 4th, 2004, the ALS
was designated Ramsar Site No. 1355 through the efforts of the Institute for Biological
Research (IBR) at the University of Veracruz, and other organizations such as the North
American Wetlands Conservation Council. The area encompasses 2671 km2 that includes
most of our proposed critical manatee habitats and other areas that are crucial to manatee
survival. The ecological description of the site mentions the region‘s importance to this
endangered species. The IBR is taking further actions with the collaboration of local
authorities in order to assure the implementation of protective measures and to establish a
Regional Management Plan for the area. Further information on the ALS Ramsar Site can be
found on the following web page: http://www.ramsar.org/wwd2004_rpt_mexico1.htm.
After several workshops involving specialists and governmental agencies, including the
―Technical Advisory Subcommittee for Manatee Recovery in Mexico‖, it was concluded that
in order to protect the manatees in the ALS from continued poaching, the primary mortality
factor, an education and awareness program should be developed throughout the ALS.
Additional components included an assessment of the current status of manatees in the ALS
and the identification of critical manatee habitats within the ALS [Ortega-Argueta, 1999,
2002, Portilla-Ochoa et al., 2002]. These efforts led to the preparation of a ―Regional Manatee
Recovery Plan in the Wetlands of Alvarado, Veracruz, Mexico‖ [Ortega-Argueta et al., 2001,
2002, 2003], and culminated in 2001 when September 7th was officially declared the
―National Day of the Manatee‖ in Mexico. With the potential for the release of rehabilitated
manatees from the Veracruz Aquarium into the ALS, there is need for continued educational
and informational campaigns to further educate the local community about the need to protect
and conserve manatees and their habitat. Over the intervening years our educational,
conservation, and outreach activities have continued, including informative workshops for
children and adults in the communities within and surrounding the ALS, boat surveys of the
ALS for manatees, interviews with fishermen and others familiar with the ALS and putative
manatee habitats there, and continued celebration of the ―National Day of the Manatee‖
[Ortega-Argueta et al., 2001, 2002, 2003, Portilla-Ochoa et al., 2002,].
The rescue of orphan manatees in the ALS suggested that the population of manatees
might be rebounding, and this has motivated the conservation and education efforts of the
past decade [Ortega-Argueta et al., 2002, 2003]. During this period, six orphan manatees have
been rescued from the ALS and transported to the Veracruz Aquarium in the city of Veracruz,
Mexico. A seventh animal was rescued but subsequently died from a gunshot wound. As the
captive population in the aquarium has grown, they have constructed a new, larger, manatee
pool and viewing area, sufficient to support 4-6 manatees. The possibility that more orphan
manatee calves may be encountered in the future has raised the concern that the aquarium will
no longer be able to continue to accept new orphans without some mechanism to decrease the
total number of animals being cared for there. The ability to release some animals will
increase the Aquarium‘s capability to foster new orphans if and when they should be found.
 The Alvarado Lagoon – Environment, Impact, and Conservation 411

Rehabilitation strategies and sites for release are being discussed in the Manatee Advisory
Committee.
An agency of the government of the state of Veracruz, the ―Papaloapan Development
Council‖ (Consejo de Desarrollo del Papaloapan, CODEPAP) has recently constructed two
concrete-lined tanks suitable for manatee husbandry along the banks of the Acula River in the
central ALS. These tanks were designed and constructed to facilitate the reintroduction of
captive manatees into the ALS. Plans are currently underway to transfer some of the manatees
from the Veracruz Aquarium to these tanks and to begin their transition to a free-ranging
existence. Once the manatees have become accustomed to feeding on the native vegetation,
and have been weaned from their dependence on humans, it is anticipated that they will be
released into an enclosure along the bank of the Acula River, and eventually into their native
habitat. Such husbandry constitutes an opportunity to rehabilitate and release individuals of
one of the most threatened species in Mexico.

CONCLUSION
The Alvarado Lagoon System is a mangrove dominated coastal wetland formed by the
confluence of the Acula, Blanco, Limon and Papaloapan rivers. The ALS is one of the most
productive estuary-lagoon systems in the Mexican GOM. It has a total area of 2800 km2 of
which 258 km2 are covered by water with an average depth of 1.5 m. Vegetation of the ALS
includes diverse ecosystems representative of Mexico´s Gulf coastal plain. Salinity in the
ALS was inversely correlated with rainfall, with highest levels occurring in the dry season
samples (March 2003 and 2005) and lowest levels occurring in the wet season samples
(September 2005). Concentrations of total inorganic carbon did not vary seasonally, while
levels of total organic carbon were higher during the rainy season. A strong correlation
between total mercury and total suspended solids in the water column suggests that
particulate matter may be a carrier phase for mercury within this lagoon system.
Historically, Antillean manatees were found in the ALS and along the west coast of the
Gulf of Mexico to the eastern coast of the Yucatan peninsula and the Mexico-Belize border.
However, hunting, water quality degradation, and the destruction of breeding habitat has
caused a decline in the number of manatees and they are now considered endangered
throughout their range in Mexico. Manatee habitat in the ALS includes estuaries, mangrove
wetlands and unpopulated regions, with a total potential area of 3150 km2.
Interviews with the inhabitants of the ALS reveal important correlations between their
oral history knowledge of manatees with current scientific knowledge. They also knew a lot
about the hunting, butchering, and preparing of manatee meat for human consumption. The
inhabitants maximized their use of the manatee carcass, including the medicinal use of
powdered manatee bones and manatee fat, and the use of manatee bones and teeth in the
artisanal production of artifacts, suggesting that manatees played a significant role in their
culture in the past.
A majority of those interviewed said they were interested in protecting manatees, but
several expressed concern that hunting would continue because of lack of enforcement of the
laws. Manatee poaching continues for a number of reasons including tradition; an
412 Jane L. Guentzel, Enrique Portilla, Alejandro Ortega-Argueta et al.

appreciation of manatee meat that is considered a delicacy; ignorance of national laws and,
and limited vigilance by Mexican environmental and regulatory authorities.
In 2001, September 7th was officially declared the ―National Day of the Manatee‖ in
Mexico. Our educational and informational campaigns have continued in order to educate the
local communities about the need to protect and conserve manatees and their habitat. In 2004,
the ALS was designated Ramsar Site No. 1355 and a ―Regional Manatee Recovery Plan in
the Wetlands of Alvarado‖ was prepared. Over the past decade, six orphan manatees have
been rescued from the ALS and transported to the Veracruz Aquarium in the city of Veracruz.
Two concrete-lined tanks suitable for manatee husbandry have recently been constructed
along the banks of the Acula River in the central ALS. These tanks were designed and
constructed to facilitate the reintroduction of captive manatees into the ALS. Such efforts
constitute an important opportunity to rescue, rehabilitate, and release individuals of one of
the most threatened species in Mexico.
Continuing threats to the ALS include increasing anthropogenic activities both within the
lagoon system and in its surrounding terrestrial areas. Limited waste management planning
and practices have contributed to deterioration of its hydrological characteristics. Overfishing,
manatee poaching, and loss of habitat have lead to a significant deterioration in the quality of
ecosystem services provided by the ALS. Despite the establishment of government policy and
measures to protect the coastal wetlands of ALS, the identified threats continue to menace the
important biodiversity and human well-being of the region.

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G. Montero, & J. Velasco-Toro, (editors). De Padre Río y Madre Mar: Reflejos de la
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Instituto de Investigaciones Biológicas, Universidad Veracruzana.
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(2002). Achievements of the manatee conservation program in Veracruz, Mexico.
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Acuáticos, Mérida, Yuc., México.
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M. & Vasquez-Lopez, H. (2009). Trophic Seasonal Behavior of the Ichthyofauna of
Camaronera Lagoon, Veracruz. Journal of Fisheries and Aquatic Sciences, 4, 75-89.
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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 417-433 © 2011 Nova Science Publishers, Inc.

Chapter 15

ADAPTIVE LAGOON FISHERY

DEVELOPMENT THROUGH SUSTAINABLE
LIVELIHOODS APPROACH: A CASE
STUDY OF CHILIKA LAGOON, INDIA

Shimpei Iwasaki
Research Fellow of Japan Society for the Promotion of Science,
Research Institute for Humanity and Nature, Kyoto University, Japan

ABSTRACT
Fishery resource in the lagoon environment is the primary form of livelihood for
survival and affects lives in different ways. For centuries, fishermen used to keep a
certain harmony with fishery resources in a traditional manner but they have been faced
with various vulnerabilities in managing fishery resources and their related livelihoods.
This chapter presents a case study of fishing communities in Chilika Lagoon (India) with
emphasis on adaptive capacity to respond to changes in the lagoon environment. It
explores pressing constraints and positive strengths of lagoon fishery development by
applying the concept of Sustainable Livelihoods Approach (SLA).
The research is based on five livelihood assets analysis developed by DFID with due
consideration of vulnerability assessment and institutional contexts. Drawing on Chilika
Lagoon experience, the study revealed that vulnerabilities to fishery livelihoods are
affected by climatic and environmental dimensions as well as by socio-economic and
cultural values. The range of pressing constraints for fishing communities covers not just
fishing but also marketing, schooling, social relations, social infrastructure and
environmental and disaster prevention awareness. This exposure posed grave threats in
lowering the capability of people in the choice of lagoon fishery development, leading to
less income generation and its associated byproducts.
In contrast, the study identified several attempts to cope with the underlying root
causes of failure in resource-based development. The Chilika Development Authority
(CDA), for instance, implemented hydrological interventions in 2000, resulting to
fisheries enhancement with a spectacular increase in fish landings. The elaborations
undertaken by CDA also made great contributions to institutional arrangements for
418 Shimpei Iwasaki

watershed management with a concept of participatory micro-watershed management

that has enabled the upper communities to upgrade their socio-economic status as well as
mitigate the impacts of siltation. Importantly, innovative activities which are considered
to be positive strengths of lagoon fishery development have been commonly associated
with the involvement of various stakeholders to adjust to the ecological-social-economic
system in response to actual or expected impacts.
Finally, this chapter draws some suggestions on adaptive strategies for fishery
development in Chilika Lagoon and potential implications to other lagoons all over the
world. The findings in Chilika Lagoon fisheries provide answers to the enquiry on
holistic and integrated measures to sustain lagoon fisheries by putting forward the
principle of SLA.

INTRODUCTION
Our planet‘s essential goods and services consist of the functions of biological diversity.
An ecological sphere rich in variety and endowed with highly-productive ecosystem services
in which fishery resources are present provides attractive benefits. Fishery resource is the
primary form of people‘s livelihood for survival, especially in coastal and lagoon areas. It is a
major source of food protein for human beings representing at least 15 per cent of the average
per capita animal protein intake of more than 2.9 billion people [1]. Significant demands for
fishery resources create employment opportunities for many people around the world [2].
Indeed, the number of fishers including aquaculturists has grown faster than the world‘s
population, and faster than employment in traditional agriculture during the past three
decades [1, 3]. In 2004, an estimated 51 million people were making their entire or partial
living from fish production and capture [4], the great majority of these in Asian countries [1,
3].
The characteristic of fisheries varies to some extent from place to place. However, it is
interesting to note that a significant proportion of fishing population comprises ‗small-scale
fishermen‘, especially from developing countries. It is estimated that there are 51 million
fishermen in the world of whom 50 million (around 98 per cent) are small-scale, subsistence,
or artisanal fishermen [4]. In general, they are continuously living amidst severe poverty.
India, for instance, is one of the best cases to illustrate this situation as the prominent presence
of a ‗caste system‘ (a social structure in which classes are determined by heredity) is deeply
entrenched in defining the societal status of the fishers [5]. In local caste hierarchies, fishing
occupation is regarded low as Shudras or out-of-caste (untouchables) by other higher castes
in different regions of the Indian subcontinent. On this account, the term ‗small-scale
fishermen‘ has been traditionally referred to as a minority group due to its so-called low
socio-economic status in most parts of the world.
Prior to the modern era, it is interesting to note that small-scale fishermen used to keep a
certain harmony with fishery resources as a whole. Many studies have shown that fishing
communities conserved fishery resources in a good condition because of a complicated
traditional system of partitioning fishing activities along low population density and poor
fishing gears [6-10]. In India, a regulatory system of traditional fisheries in a niche space
among the sympatric castes is commonly observed so that the differences in resource use
patterns allowed the caste groups to avoid competitive exclusion [6]. These traditional
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 419

customs at the community level played a great and important role in managing fishery
resources in a sustainable manner.
However, the present situation tends to break or weaken such good customs and practices
in many parts of the world; fishing communities have been faced with difficulties in
managing sound fishery resources due to a wide variety of vulnerabilities such as climate
change, population growth, technological development, market fluctuations, institutional
changes, among others. Revenue-oriented thoughts is a good example that often induce
dominant persons/groups such as government officials and capitalists to apply for destructive
fishing methods or gear practices, accounting for numerous losses of fishery resource stocks.
Such practices destroy fish ecology and then undermine people‘s capacity to adapt to fishing
activities especially for small-scale fishermen. Out of various geographical types of fishery
domain, such situations are particularly applicable to lagoon fisheries. The lagoon is situated
at both extremity of watersheds and sea marine, which are of a dynamic and complex
environmental character: these are transitional ecosystems between land and sea and between
fresh and marine water. With spatial and temporal changes in the lagoon environment, these
areas are physically or climatically subject to various influences not only from their internal
environment but also the adjacent marine and terrestrial places including watershed areas. In
other words, the lagoon ecosystem being influenced by extra-local shocks combined with
rapid anthropogenic pressures tends to increase vulnerable conditions in fish ecology. To
ensure that small-scale fishers can achieve wise use of fishery resources sufficiently over
time, there is a need to explore the vulnerability of lagoon fisheries and its associated
livelihoods in the local context. Thus, this chapter sets out to identify the pressing constraints
and positive strengths of lagoon fishery development through a case study of Chilika Lagoon,
India.

Livelihood Assets

H In order to achieve

Vulnerability Transforming Livelihood

Context S N Structures& Processes Outcomes
Influence
• Shocks & Access STRUCTURES • More
Livelihood Strategies

• Trends income
• Seasonality • Levels of • Increased
P F Government well-being
• Private • Reduced
sector ••Laws vulnerability
Key •
•Policies • Improved
H = Human capital • Culture food security
N = Natural capital •Institutions • More sustainable
F = Financial capital use of natural
S = Social capital PROCESSES resources
P = Physical capital

Source: modified from DFID [16]

Figure 1. Sustainable Livelihoods Framework

420 Shimpei Iwasaki

SUSTAINABLE LIVELIHOODS APPROACH

The term ‗vulnerability‘ is crucial to identify pressing constraints and positive strengths
of fishery operation and related activities in the lagoon environment. The origin of this word
‗vulnerability‘ lies in the Latin vulnus, meaning ‗a wound‘, and vulnerare, ‗to wound‘ [11]. In
particular, Kelly and Adger [11] pointed out that the word vulnerable derives from the late
Latin vulnerabilis which is enlightening and vulnerabilis was the term used by the Romans to
describe the state of a soldier lying wounded on the battlefield, i.e., already injured therefore
at risk from further attack. On the whole, vulnerability can be portrayed in the degree to
which a system is susceptible or unable to cope with negative effects of natural or man-made
variability and extremes. Although a common conceptualization of vulnerability has never
been shared among academic and development practitioners [12-14], it is usually
characterized as some form of the characteristic, extent and frequency of exposures and
sensitivity, and people‘s capacity to adapt to these hazards. Consistent with the
characteristics, Smit and Wandel [13] depicted a basic vulnerability relationship that takes
into account a broad scale of determinants corresponding to three components (exposure,
sensitivity and adaptive capacity) of vulnerability. In the exposed lagoon environment and the
people who are sensitive to varying influential sources of climatic and hydrological changes
at multiple scales, small-scale fishermen need to adapt to the impacts of changes in the
ecological-social-economic systems. Thus, the last third function (adaptive capacity) of
vulnerability is a critical key in building people‘s resilience to the lagoon environment.
With this recognition, this chapter applied the ‗Sustainable Livelihoods Approach (SLA)‘
in an effort to understand the vulnerable contexts of Chilika Lagoon fisheries. SLA represents
a new paradigm of poverty reduction, and is an innovative tool originally developed by
UNDP on the basis of the 1987 UN Environment Summit and Chambers and Conway[15].
SLA provides a way of thinking about livelihoods of poor people in the context of
vulnerability [16]. The application of SLA helps researchers and practitioners identify
pressing constraints and positive strengths of lagoon fishery development with overlaps
between micro and macro links. According to the SLA model developed by DFID [16], the
framework compromises three components: ‗livelihood assets (natural, financial, social,
human and physical capital)‘, ‗vulnerability context (vulnerability analysis)‘ and ‗structure
and process (institutional analysis)‘ (Figure 1). The SLA has been applied flexibly in various
ways, but the framework places high emphasis on the linkages among the three components
so that users are encouraged to draw up the best adaptive strategies called ‗livelihood
strategy‘ with ‗livelihood outcomes‘. However, the SLA has seldom been applied to field
situations especially in the sector of fisheries [17-18]. In this sense, this chapter makes an
enquiry into addressing holistic and integrated measures to sustain lagoon fisheries by
utilizing the principle of SLA.
On the basis of SLA, field surveys were conducted in Chilika Lagoon twice: between
November 2005 and February 2006 and in June 2009. The case study was carried out in eight
fishing communities of Chilika Lagoon with two communities each located in the north,
central south and the outer channel sectors of Chilika Lagoon. The research used both
qualitative and quantitative data, including structural questionnaires, key informants
interviews and secondary data. In this chapter, primary data from structural questionnaires
were collected from 25 fishermen (N=195), 20 women (N=160) and 15 fisher-children
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 421

(N=110) in each fishing community, although in some instances the survey failed to collect
data samplings of 5 fishermen and 10 fisher-children because of the small population in
certain communities. The questionnaires used a multiple-choice format and were compiled
into three sections; general information (age, caste, education, literacy), fishing and marketing
activities and livelihood conditions. In addition, semi-structured interviews with key
informants (government officers, village leaders, NGOs, researchers) were carried out to
validate and complement the information.

PROFILE OF FIELD STUDY SITE (CHILIKA LAGOON)

Chilika Lagoon is the largest brackishwater lagoon in Indian sub-continent, situated at
latitude 19°28‘ and 19°54‘ north and longitude 85°05 and 85°38‘ east (Figure 2). The lagoon
extends from southwest corner of Puri and Khurdra districts to the adjoining Ganjam district
of Orissa state. The pear-shaped lagoon is around 64.3 km long and its width varies from 18
km to 5 km and, is connected to the sea through irregular water channels with several small
sandy and usually ephemeral islands [19]. The average lagoon area is 1,055 sq km which
increases to 1,165 sq km during the rainy season and shrinks to 906 sq km during the summer
season. Chilika Lagoon becomes less saline during the rainy season due to flood waters from
52 rivers and rivulets. It becomes more saline during the dry season as the supply of flood
water is cut off when the south wind begins to blow and saline waters enter from the Bay of
Bengal at high [20]. The lagoon has three hydrologic sub-systems (Mahanadi delta, western
catchments, and the Bay of Bengal) influencing the hydrological regimes as shown in Figure
2. The total inflow of freshwater from the Mahanadi delta has been estimated to be 4,912
million cu.m., accounting for 80 per cent of the total water flow. The maximum discharge of
3,182 million cu.m. comes from Makara River, followed by Bhargavi River (1,108 million
cu.m.) and Luna River (428 million cu.m.) [19]. Meanwhile, the western catchments account
for 20 per cent of the total fresh water flow.
Chilika Lagoon itself can be broadly divided into four sectors (northern, central, southern
and outer channel) with distinctive ecological characteristics in water depth and salinity (see
Figure 2). The lagoon having four distinctive ecological sectors is a unique assemblage of
marine, brackish and freshwater ecosystems with estuarine characteristics. This mixed
combination has endowed it with valuable biodiversity and highly productive ecosystem in
which fishery resources present attractive benefits. The rich lagoon ecosystem supports the
livelihood of more than 200,000 fishermen and thousands of local people who are engaged in
allied fishery business activities including boat operators, food processors, fish merchants and
fish delivery operators [19, 22]. This valuable ecosystem service provides fishery resources
that cater to the needs of Orissa state and other states such as West Bengal, Bihar, Madhya
Pradesh, Tamil Nadu and Kerala states [19]. There are reported to be 127 fishing villages in
Chilika Lagoon with estimated fishery families of 12,363 (ibid). With regard to fishing
occupation, traditional fishermen include seven sub-caste groups: Keuta, Niari, Kartia,
Kandara, Gokha, Tiara and Nolia [23]. Most of them belong to Schedule Caste (SC) and their
societal status is quite low as they belong to the poorest of society.
422 Shimpei Iwasaki

Northern
Sector

Chilika Lagoon
Central
Sector Old Mouth

Outer Channel

New Mouth
Southern
Sector

Catchment along the Sandbbar

Source: modified from Ghosh and Pattnaik [21]

Figure 2. Map of Chilika Lagoon

VULNERABLITY ASSESSMENT THROUGH

LIVELIHOOD ASSETS ANALYSIS
This section sets out to assess fishery vulnerability through livelihood assets analysis
(natural, human, financial, physical and social capital) on the basis of the SLA model
developed by DFID. The research seeks to identify the vulnerable context of each capital with
regard to fishery livelihoods in Chilika Lagoon. It provides better insight into understanding
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 423

the underlying issues of Chilika Lagoon fisheries and then throws light on fishery adaptation
in an appropriate manner.

Natural Capital

More or less, fishery development depends on the availability of fishery resources. On

the point of resource stocks, Chilika Lagoon has experienced severe environmental
deterioration primarily from siltation since the 1980s. In combination with anthropogenic
pressures such as deforestation, overgrazing and industrialization, seasonal climate forces
such as cyclones and floods brought a lot of silt into the lagoon. This caused shutting of the
sea mouth between the sea and lagoon, leading to adverse impacts on the availability of
fishery resources. The closure of the sea mouth affected the salinity level of the lagoon and
prevented exchange of migratory fish species, which account for nearly 80 per cent of lagoon
fisheries catch [24].
In addition, the silt accumulation reduced the water spread area and hindered the
exchange of water between the sea and river, resulting in decreased salinity and lower
availability of fish species in the lagoon. Siltation into the lagoon also encouraged the prolific
growth of freshwater invasive species. The area of Chilika Lagoon dominated by invasive
plants increased 20 sq km in 1972 to 685 sq km in May 2000 [22]. The spread of the invasive
species restricted the feeding as well as the breeding ground of many marketable aquatic
species. As a result, these changes reduced the area of fishing grounds in Chilika Lagoon.
This led to loss of income that renders fishermen more to the brink of poverty. The weed
invasion presented physical difficulties for boat navigation, further undermining people‘s
adaptive capacity to changes in the lagoon environment.

Financial Capital

The livelihoods of fishing communities largely depend on the fisheries from Chilika
Lagoon. Most of them have no secondary occupation, so fishing is the sole source of income.
On the whole, members of fishing boats in Chilika Lagoon are limited to family or
neighbours, and their profits are equally distributed among them. Household incomes per
month in 2005 (N=195) are Indian Rupee (INR) 1,540 (approximately US$ 34) 1 in the lean
season and INR 3,303 (approximately US$ 72) in the harvest season, respectively2. Their
incomes are not sufficient to cover their living expenses in the lean season especially during
the monsoon period because they often cannot go fishing due to extreme rainfall and strong
winds. Maintenance of fishery livelihoods often requires the purchase or repair of fishing
gears, these being high exhaustive goods. Due to this situation, most of the fishermen fall into
indebtedness. The fishermen borrowed money from mahajans – dominant fish merchants (4
per cent) and commission agents (68 per cent) to purchase or repair fishing gears. On the

1
An exchange rate of US$1 = INR 45.85 is used in 2005.
2
Seasonality was purposely divided into two seasons (lean and harvest seasons). The seasonal difference is derived
from amounts and profits of fish and prawn landings; fishermen catch more fishery resources from March to
August and less in the rest of the months.
424 Shimpei Iwasaki

average, the aggregate indebtedness per fishermen amounted to INR 28,506 (approximate
US$ 622) from those lenders in 2005.
Fish merchants seeks to exploit the fishermen in the fish marketing process in
combination with money lending with interest free. The loan provisions are addressed
through purchasing or repairing fishing gears, instead of informal fish trade promises that
debtors shall deal their entire catch with the merchants. This give-and-take system led to the
dominant control of fish merchants resulting to the fishermen selling their catch at lower than
market price. Consequently, the dependency between fishermen and specific fish merchants
pushes fishery households to the brink of indebtedness and led to the nearly-defunct primary
fishery cooperative societies (PFCSs) which stopped managing cooperative fish marketing
and then weakened people‘s unity in lagoon fisheries management [25]. The exploitative
marketing situation drives the fishermen to operate indiscriminate fish catch for survival
which can bring about failures in resource-led development [26].

Social Capital

Perpetual conflicts over fishery resources especially between fishermen and non-
fishermen caste have been observed in Chilika Lagoon. Tracing back the history of Chilika
Lagoon, the traditional fishermen caste has naturally enjoyed fishing as an exclusive legal
right but this situation changed in response to the 1991 guideline which gave rights to non-
fishermen caste as well. It meant legally allowing outsiders to enter the fisheries in limited
areas of Chilika Lagoon while excluding the local fishermen to some extent. Furthermore,
ambiguous demarcation of each fishing ground enabled others to encroach on exclusive
fishing grounds. Many fishing grounds are encircled by trapping nets (khandas) that make it
difficult to adopt multi-strata use of fishing activities in one spot as practiced by the
traditional fishermen caste before. Meanwhile, the decrease in the water spread area due to
siltation (corresponding to natural capital), extensive gherry operation3 and human population
growth push traditional fishermen more to the brink. Those sensitivities and exposures to
decreasing fishing grounds in terms of social and natural dimensions gave rise to perpetual
resource-based conflicts especially between fishermen and non-fishermen caste plaguing
human lives, livelihoods and dignity.

Physical Capital

The physical environment surrounding the fishing communities of Chilika Lagoon is very
poor. The fishermen are forced to make use of unreliable boat jetties attached to raised
ground. Once tremendous climate hazards occur, social infrastructure including fish landing
centers and community roads are easily damaged in part by fallen trees. Villagers stressed
that their fishing equipment tend to be broken or lost. The losses or damages of fishing
equipment lead to suspension of fishing activities as well as require enough money to

3
Gherry is made either of earthen embankment or bamboo and a net enclosure [27-28].
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 425

purchase or repair those materials, which induce them to become more reliant on dominant
fish merchants, in terms of indebtedness.
On the other hand, poor housing conditions make them vulnerable to climatic and
environmental hazards. Some housing with partially-stripped roof can be observed due to a
lack of sufficient household income. In particular, there is no sanitary facility in many parts of
the fishing communities in Chilika Lagoon so that the local people are prone to various water-
borne diseases which are relevant to human capital. Moreover, many people in fishing
communities have less access to medical support because of lack of income and the
remoteness of their village.

Human Capital

Educational status in fishing communities of Chilika Lagoon is low. Instead of attending

school, the boys tend to start fishing to help their families survive. Around 26 per cent of
fishermen including boat members (N=462) had no educational experience while only around
5 per cent fishermen had entered college or university. Most of the fishermen (55 per cent)
dropped out before high school except those who had no educational experience. On this
account, 60 per cent of the people can read and write in their native language (Oriya). Such
characteristics are particularly prominent among women (95 per cent school dropout and 20
per cent literacy rates). The high illiterate population resulted to various constraints on
alternative jobs, health care and formal credit taking that are largely linked to enhancement of
other capital assets. Lower education limits alternative jobs except fishing and related
industries so that there is an increasing trend of fishing population in Chilika Lagoon. It
creates high competition over limited fishery resources and triggers disputes among the
fishermen. Children who have started fishing are more vulnerable to climate variability and
extreme events than the adults, but there is no choice for them but to engage in fisheries. The
root cause for this is mainly attributed to the lack of household income, but also linked to
affairs of formal schooling. Villagers argued that some of children were reluctant to go to
high school because of caste discrimination. Most high school are situated in non-fishing
villages where a sense of caste discrimination strongly prevails leading to one or more
obstacles for entering high school.

ADAPTIVE STRATEGIES FOR LAGOON FISHERY DEVELOPMENT

This section explores adaptive strategies for fishery development in Chilika Lagoon. The
primary goal of SLA is to develop an understanding of the factors that lie behind people‘s
choice of livelihood strategy and then to reinforce the positive aspects as well as mitigate the
pressing constraints toward sustainability (DFID, 1999-16). On the basis of vulnerability
assessment through livelihood assets analysis, Table 1 shows expected fisheries strategies,
showing the impacts on vulnerability and institutional contexts. The key expected adaptive
strategies can be compiled into three components: integrated lagoon fisheries management,
wise use of fishery resources and resilient fishing communities.
426 Shimpei Iwasaki

Table 1. Adaptive Strategies for Fishery Development in Chilika Lagoon by SLA

Livelihood Major Problems Related to Root Causes Adaptive Countermeasures

Assets Fishery Livelihoods
Natural  Decrease of fish species  Soil erosion from upstream  Hydrological interventions
Capital  Decrease of fishing grounds  Closure of sea mouth  Involvement of stakeholders
 Boat navigation trouble  Proliferation of freshwater in watershed management
weeds  Enhancing environmental
 Illegal and destructive awareness
fisheries
Financial  Lack of fishery income  Decrease of fish species  Strategic loan provision for
Capital  High rate of indebtedness  Exploitative marketing fishing equipment
structure
 Resource-based conflicts
Social  Inequitable fish trade  Loan dependency on fish  Revitalization of primary
Capital  Resource-based conflict merchants fishery cooperative societies
 Lower capacity of primary  Proper demarcation of
fishery cooperative societies fishing grounds with rapport
 Ambiguous demarcation of building among relevant
fishing grounds stakeholders
 Improper consensus building
for resource allocation
change of fishing rights
Physical  Poor social infrastructure  Lack of political power  Promotion of disaster
Capital  Loss or damage of fishing  Lack of unity for disaster insurance scheme
equipment prevention  Enhancing disaster
prevention awareness
Human  School dropouts  Less fishery income  Strategic loan provision for
Capital  Increase in fishing  Caste discrimination in education
population schooling  Eradication of racial
 Vulnerable health condition discrimination
especially for fisher-children

Integrated Lagoon Fisheries Management

The domain of lagoon fishery development is largely corresponding to the availability of

fishery resources. However, the ecosystem of Chilika Lagoon was under severe
environmental threat. Importantly, siltation (soil erosion) is identified as among the most
serious environmental problems in combination with climate variability and human pressures.
Siltation from upstream leading to the shrinkage of the water spread area, decrease in salinity
and prolific growth of weed infestation had adverse impacts on the habitat of wildlife
including fishery resources. Indeed, fish landing statistics in several decades showed how
fishing activities were hampered by rapid changes in the lagoon environment especially in the
1990s.
In an effort to solve the serious situation, Chilika Development Authority (CDA), which
was established in 1991, implemented hydrological interventions (e.g., opening of a new
mouth and dredging of water channels) in the year 2000 (see Figure 2). The interventions
were successful and contributed to the dramatic natural restoration. In particular, the opening
of a new mouth exhibited positive impacts on lagoon ecosystem especially fisheries
enhancement with a spectacular increase in fish landings (see Figure 3). Fish landing of
14,053 metric tons in 2003-04 was an all-time record high, compared to the all-time low of
around 1,600 metric tons prior to the interventions. However, it should be kept in mind that
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 427

the technical interventions can be just temporal end-of-pipe measures to cope with siltation.
Together with the overexploitation of fishery resources, there has been a gradual decrease in
fish landing quantities after the hydrological implementation, so additional elaboration was
needed to take into account how to reduce the risk impacts of siltation in a proactive manner.
Under the circumstances, CDA has further adopted and expanded participatory micro-
watershed management projects since 2001 that seek to involve local people in the projects,
in order to mitigate the impacts of siltation caused by climate extreme events combined with
anthropogenic pressures. Greater emphasis has been placed on community participation
including women and the landless or the poor to enhance the win-win situation of livelihood
improvement and soil conservation. On this account, a watershed association was established
in each project site, where members are the local people. In collaboration with relevant
stakeholders, the responsibility of project implementation has been entrusted to the
association. Within the association, the watershed committee implements the day-to-day
activities of the watershed development projects, leading to stronger and better participation
of local residents in the watershed areas. It is responsible for coordination and liaison with the
Gram Panchayat and government agencies concerned to ensure smooth implementation of the
watershed development projects. In this way, CDA acted in a leading role in the coordination
of environmental watershed governance between upstream and downstream communities.
Practices regarded as lagoon fisheries management linking to watershed conservation help
develop a pathway for strengthening adaptive capacity to changes in the lagoon environment.

MT Trend of Fish Landing Quantity from 1929 to 2008

16000
14000 Yearly Average Fish Landing Amounts
12000 3 Years Average Fish Landing Amounts
10000
8000
6000
4000
2000
0
1929 1934 1939 1944 1949 1954 1959 1964 1969 1974 1979 1984 1989 1994 1999 2004

Source. modified from DFGO [29], DFGO and CDA [30], CDA data

Figure 3. Trend of Fish Landing Quantity from 1929 to 2008

Table 2. Total amount of loan availed by PFCSs from

different financial sources (Unit: Indian Rupee)

Bank Government NCDC

Amount of Finance 38,75,150 11,27,500 24,48,960
Amount of Demand 38,75,150 11,27,500 22,18,996
Collection 21,91,284 5,50,696 2,29,366
Balance 16,83,866 5,76,804 19,89,630
Source: ARCSCCB [33]
428 Shimpei Iwasaki

In an effort to maintain (and preferably improve) fish stocks in Chilika Lagoon, there is a
need, therefore, to incorporate fisheries management into sea mouth and watershed
management. Elaborations are needed to enhance or maintain multiple linkages, horizontally
(across space) and vertically (across levels of organization) [31-32]. In this sense, it is of use
to introduce a notion of integrated lagoon fisheries management (ILFM) in which fisheries
management, sea mouth management and lagoon watershed management have to be balanced
towards sustainability.

Wise Use of Fishery Resources

It needs to be mentioned that fishermen tend to operate indiscriminate fish catch. The
underlying cause of illegal and destructive fisheries is partly linked to exploitative fish
marketing structure combined with informal money lending. Thus, enhancing environmental
awareness and strategic loan finance from formal banking institutions are strongly
recommended to eradicate their illegal and destructive activities. In this regard, however,
considerate efforts are required to solve the latter challenge because attempts had already
failed in private and government banks. In the past, these banking institutions provided loans
to the fishermen for the purpose of reducing dependency on fish merchants, but debtors could
easily escape the duty for loan repayment from the lenders while continuing to lie about who
were debtors [33]. Indeed, Table 2 shows that only 57 per cent, 49 per cent and 10 per cent of
total loan amounts were repaid to private banks, government banks and National Cooperative
Development Corporation, respectively [34]. On this account, the formal banking institutions
were forced to withdraw the loan scheme for small-scale fishermen. It created more space for
control of the fish economy by fish merchants combined with informal money lending, which
catalyzed a greater incentive for the fishermen to operate fish catch indiscriminately.
To address this issue, it is helpful to know that there is an innovative approach to loan
finance and cooperative fish marketing developed by the South Indian Federation of
Fishermen Society (SIFFS). SIFFS supported a large number of fishing communities in the
south of India by providing loan finance from banks to each fisherman with due capacity
assessment and introducing automatic deduction of loan repayment from pay through
cooperative fish marketing. Instead of cutting off the loan dependency with fish merchants,
SIFFS encouraged the fishermen to join cooperative fish marketing activities for economic
improvement as well as solution for ‗loan waiver‘. This effort gives a great clue to solve the
loan issue and then bridge the gap between controlled and actual price in Chilika Lagoon (see
Iwasaki [35]).
Furthermore, lagoon fishery development is also largely linked to people‘s access to
fishery resources as well as the presence of resource stocks. Perpetual conflicts over fishery
resources especially between fishermen and non-fishermen caste undermined people‘s
security plaguing human lives, livelihoods and dignity. Except for the outer channel sector,
most of the fishermen strive to stay on boats near their grounds for several days so as not to
allow others to encroach on their fishing grounds4. A sense of insecurity is commonly
observed in Chilika Lagoon [28, 35] that caused the fishermen to do unfavorable fish trade

4
In the outer channel area, fishing grounds were close to the villages because of the productive and eco-sensitive
nature of this area in Chilika lagoon so they are able to monitor encroachments from their villages.
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 429

with commission agents on the boat [36]. Aside from loan finance, it further strengthened fish
transaction with specific commission agents who made adjustments to meet the multiple
needs of fishermen: the commission business was combined with the sale of basic materials
and favourable trade location by boat-to-boat transaction, which made a great contribution to
not only ensuring that fishing grounds are not encroached upon but also saving on their work
and fuel oil in the fish delivery process to buyers. However, the merchants could have a more
incentive to demand exploitative fish trade with the fishermen, irrespective of debt, taking
advantage of insecurity affairs. In an attempt to solve the resource-based conflicts, the
realistic feasible approach may be to precisely define the ambiguous demarcation of leased
grounds. The defective demarcation of each leased ground made by the Orissa government
enabled non-fishermen caste to encroach on leased grounds owned by fishermen caste or to
occupy unauthorized leased grounds inside Chilika Lagoon. Therefore, an appropriate
demarcation of leased grounds is strongly recommended to remove the underlying cause of
resource-based conflicts. Moreover, there is a strong need to develop rapport and consensus
building among all fishermen through deliberate discussions with appropriate rules and
management for common-pool resources in Chilika Lagoon.

Enhancing Resilient Fishing Communities

The practice of fisheries itself is prone to be physically affected by various types of

climate and environmental hazards. Destructive natural hazards that frequently occur in
Chilika Lagoon cause serious damages to fishing communities. In particular, people such as
the aged, disabled, women and children are highly vulnerable. Despite the early age, for
instance, children forced to start fishing are being exposed to severe climate hazards including
strong sunlight and cold winds. There is no alternative for them but to engage in fisheries; the
entrance to schooling is disallowed due mainly to the lack of financial capital. Thus, a
strategic loan provision undertaken by SIFFS may offer one way to improve their livelihoods
and make sure that children are able to go to school and kept in a safe environment. In
addition, another effort needs to be made to eradicate caste discrimination in formal
schooling. Discrimination induces school children to join fisheries despite the fact that its
lifestyle makes them physically vulnerable to climate hazards. Hence, deliberate discussions
on castism among relevant stakeholders are of high importance to promote resilient fishery
development in Chilika Lagoon.
In addition, their physical capital is so low that it will be easily damaged or lost when
disastrous events occur in Chilika Lagoon. On this account, promotion of natural calamity
insurance supported by Department of Fisheries and Animal Resources Development has
been implemented. The insurance scheme enables all people including the poor to mitigate
the sudden shocks of climate variability and extreme events. It was promoted through primary
fishery cooperative societies (PFCSs) which were able to mediate the insurance scheme
between their associated members and the government effectively. Taking into account the
increased intensity and frequency of natural disasters in Orissa state [37], the initiatives will
play a greater role in responding to the direct and indirect effects of climate change in the
long run. There is, of course, negative aspects to be considered. Fishermen do not tend to
adjust themselves to changes in climate and environment variability, even though catastrophic
430 Shimpei Iwasaki

climate extreme events such as cyclones and floods devastate their private and public
property including fishing equipment. Therefore, enhancing disaster prevention awareness
and the sense of unity among the local people is recommended to mitigate the impacts of
climate and environmental hazards.

CONCLUSION
Putting them all together, this chapter sought to put the principle of sustainable
livelihoods approach (SLA) into fishery development in the case study of Chilika Lagoon.
Livelihoods approach with an overlap between micro and macro links reflects a wide variety
of poverty aspects that give a clue to figuring out pressing constraints and positive strengths
of lagoon fisheries development. The findings revealed that the range of fishery
improvements covers not just occupational activities but also multifaceted aspects of fishery
livelihoods that determine the extent of their capacity to adapt to the lagoon environment. The
domain of expected fishery strategies in Chilika Lagoon covers all encompassing aspects
including fishing, marketing, schooling, social cohesion, social infrastructure and
environmental and disaster prevention awareness. The increase in fish species, for instance,
meets an important requirement of capability for lagoon fishery development but is not a
necessary precondition. The dominant fish marketing structure by fish merchants undermines
fishermen‘s capacity to adapt to the ecological-social-economic system while access to
fishing grounds also affects them to a great extent. These vulnerabilities triggered dropouts in
school and caused young people to enter the fishing industry, resulting in an increase in over-
fishing population and subsequent practice of illegal and destructive fisheries. These
interactions may lead to a negative chain of lagoon fishery development unless considerable
efforts are made. Furthermore, the people in fishing communities have been under severe
threats of climate and environmental hazards. Each vulnerability factor among their
livelihood assets influences the extent of their capacity to cope with the downside risks. On
this account, it implies that issues that lie behind fishery development in Chilika Lagoon will
defy any attempt at a quick and simple solution.
In this regard, expected adaptive strategies in Chilika Lagoon fisheries are presented in
Table 1. There are several positive strengths of lagoon fishery development in Chilika
Lagoon. In particular, hydrological interventions and participatory micro watershed
management can be of very significance in maintaining (and preferably improving) the
lagoon environment and fishery resource. In addition, the promotion of disaster insurance and
strategic loan financial schemes helps fishery households, which are largely dependent on
fisheries, in mitigating the impacts of climate and environmental extreme events. Of
particular note is that these innovative efforts are commonly associated with the involvement
of various stakeholders. In this way, further collaborative and cooperative efforts among
relevant stakeholders will be required towards resilient lagoon fishery development.
Finally, the application of SLA is rather new and still evolving, so the research method
has been applied flexibly in various ways by researchers and policy makers. In this chapter,
the analysis related to lagoon fisheries requires more examination of the interaction among
households on how to allocate their own resources and services to family members. In this
 Adaptive Lagoon Fishery Development Through Sustainable Livelihoods… 431

way, a better understanding of lagoon fishery development and their related livelihoods in the
community context can be developed.

ACKNOWLEDGMENT
The author acknowledges the support of a JSPS grant. The author is extremely grateful to
Dr. Ajit Kumar Pattnaik, Chief Executive Officer, CDA for offering his wholehearted
support. He is also thankful to Mr. Durga Prasad Dash, Secretary, Pallishree, for kind
assistance during his stay in Bhubaneswar and Chilika Lagoon.

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 435-455 © 2011 Nova Science Publishers, Inc.

Chapter 16

VERTICAL FLUX OF ICE ALGAE IN A SHALLOW

LAGOON, HOKKAIDO, JAPAN

Yoko Niimura1, Hiroaki Saito2, and Satoru Taguchi*3

1
Tokyo University of Fisheries, Tokyo, Japan
2
Hokkaido National Fisheries Research Institute, Hokkaido, Japan
3
Soka University, Tokyo, Japan

ABSTRACT
A seasonal variability in the vertical flux of ice algae was examined with a multiple
sediment trap during seasonal ice coverage in SaromaKo Lagoon, Hokkaido, Japan. The
multiple sediment traps were moored at 4 m below the water surface and 5 m above the
bottom to collect suspended materials at 7 dayintervals for 64 days from February 4 to
April 8, 1999. Community structure of ice algae and water column phytoplankton
collected with the sediment traps was determined in terms of both cell abundance and cell
volume. For the ice algal community, Odontella aurita was the most dominant in cell
volume, followed by Pleurosigma spp., Achnanthes spp., Detonula confervacea,
Bacteriaosira fagilis, Fragilariopsis spp., and Navicula spp. while Fragilariopsis spp.
and Achnanthes spp. were dominant numerically. Water column phytoplankton were
dominant in descending order of cell volume by Membraneis spp. Thalassiosira spp.
Campylodiscus sp., Chaetoceros spp., Amphora spp., and Dictyocha speculum, and
Alexandrium sp. Mean cell volume ratio of ice algae to total algae with one standard
deviation was 0.30 ± 0.28 and highly variable although a similar ratio based on cell
number was 0.72 ± 0.06. The vertical fluxes of chlorophyll a (Chl a) was estimated from
the volume ratio, and the mean with one standard deviation was 0.90 ± 0.42 mg Chl a
m−2 d−1. This suggests that the ecological role of ice algae in a small embayment should
be considered separately from ecosystem in the high latitudes although a total release of
ice algal carbon from the sea ice into a water column could be similar to one in the high
latitudes and only 3 g C m2 in 65 day ice season. Even during the ice coverage, due to a
lateral transport of phytoplankton through two channels from the Sea of Okhotsk, where
ice coverage was always incomplete, the community structure of released ice algae under

* Corresponding author: staguchi@soka.ac.jp, Tel/Fax: +81-42-691-8002

436 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

the sea ice was modified significantly. A combination of laterally transported water
column phytoplankton and vertically released ice algae into the underlying water column
may play a significant role in the energy transfer to the successful aquaculture of scallops
and oysters as well as other benthos in the shallow coastal water ecosystem.

Key words: cell volume ratio, Chl a, diatoms, resuspension, sediment trap, temporal
variability

INTRODUCTION

Ice Algal Community

Dense algal assemblages are formed at the bottom surface of sea ice and they are
generally called ―ice algal community‖ (e.g., Horner 1985). Ice algal community occupy a
habitat in the brinefilled space between ice crystals, i.e., brine channels or brine pockets. Ice
algal community faces highly variable fluctuations in the physical, chemical, and biological
environment over different temporal and spatial scales. Ice algal biomass in the brine
channels often exceeds biomass found in open water (Legendre et al. 1992). High
accumulation of ice algal biomass is controlled by permeability of the ice that is a critical
factor for supply of nutrients to the ice algal community (e.g., Cota et al. 1987; Smith et al.
1990).
At the same time for the accumulation of algal cells in the sea ice, ice algal community is
continuously released into an underlying water column from the sea ice (e.g., Taguchi et al.
1997b). The release is provided by physical factors such as brine expulsion (Weeks and
Ackley 1986) and water exchange between brine channels and underlying water (Krembs et
al. 2000). The physical factors are likely triggered by temperature change. The released algae
could contribute often to algal biomass in underlying water (Reesburg 1984; Garrison et al.
1987; Michel et al. 1993). Sinking ice algal community transports energy without a
significant loss during the sinking in a water column to benthic community particularly in
high latitudes (e.g., Tremblay et al. 1989). This process is particularly significant for the
shallow coastal waters where the influence of seasonal inputs of organic matters to the
sediments including aquaculture systems could be highly significant (Gutt et al. 1998). In
such regions when sea ice and ice algal community are developed, the sedimentation of ice
algal community has received much attention (Carey 1987) in connection with carbon flow in
the aquatic ecosystem (Vezina et al. 1997).

Sedimentation of Ice Algal Community

Ice algal sedimentation has been recognized as one of the most difficult processes for
quantitative estimation but critical information, particularly in coastal sea ice ecosystem. The
origin of the difficulty is two-fold: (1) resuspension of bottom sediments and (2) mixture
with pelagic phytoplankton. The former can be corrected by a chemical ratio method
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 437

introduced by Gasith (1975), requiring quantitative chemical measurements of ice algal

community, organic matters collected in the sediment trap, and bottom sediments. The latter
has been merely attempted in the past (Leventer and Dunber 1987) because some ice algal
cells are often found in a water column and some phytoplankton are also incorporated into the
sea ice and possible differential dissolution of silica frustules occurs during sedimentation.
Because a taxonomical identification can be employed to distinguish ice algal species from
other epiphytic algae and pelagic phytoplankton in the present study area (e.g., Michell et al.
1997) and any significant dissolution does not occur in a shallow water column due to a
shallow water column, it can provide a reasonable estimate for the vertical flux of ice algal
community. It can be made as long as a significant relationship between cell volume and Chl
a concentration is obtained. Once the relative contribution of ice algal community is
estimated, vertical flux of Chl a related to ice algal community can be obtained by assuming
that a portion of ice algal Chl a in the total Chl a trapped in the sediment traps is similar to the
cell volume ratio of ice algae to total algal cells.

Saroma-Ko Lagoon

The complete freezing of the surface area in Saroma-Ko Lagoon commences in late
January and ice retreat occurs in early April every year (Taguchi and Takahashi 1993)
although the Sea of Okhotsk has never been completely frozen. The winter community of
pelagic phytoplankton prevails in the surface mixed layer in the Sea of Okhotsk. Natural
assemblages of pelagic phytoplankton are extremely suppressed under the complete coverage
by sea ice in Saroma-Ko Lagoon (Michel et a. 1887). Since Saroma-Ko Lagoon is semi-
enclosed water and connected with the Sea of Okhotsk by two channels, the winter
community of pelagic phytoplankton in the Sea of Okhotsk can be transferred by tidal current
through the channels to a water column in Saroma-Ko Lagoon. The tidal current may invade
from the North deep channel and overfill through the South shallow channel during the period
of complete coverage by sea ice. This process may modify the community structure of
phytoplankton assemblage under the sea ice in Saroma-Ko Lagoon. Runoff from Bekanbetsu
River, which is the biggest supply of fresh water and inorganic matters (Nomura et al. 2008),
can affect the current system and sedimentation of organic matters under the sea ice in the
east basin although the maximum runoff occurs one month after the ice season (Takeuchi
1993). All these characteristics related with not only tidal transport of pelagic winter
phytoplankton but also a seasonal sea ice provides a unique situation to study vertical flux of
ice algae in a water column. Observation study with sediment traps has been made in the
present study area in the past (e.g., Michell et al. 1993, Taguchi et al. 1997b), however the
seasonal variability in the vertical flux of ice algal Chl a released from sea ice has remained
clarified. Ice algal community includes several taxonomic groups of algae and is employed to
estimate quantitatively a vertical flux of Chl a specific to ice algal community.
438 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

Objectives

Objectives of this study were (1) to quantify the vertical flux of ice algae based on the
community structure of algae, (2) to determine the temporal variability in the vertical flux of
Chl a during the period of complete coverage of sea ice, and (3) to estimate the annual
vertical fluxes of organic matter related to ice algal community.

MATERIALS AND METHODS

In order to assess the vertical flux of ice algae from sea ice during a complete ice
coverage season of Saroma-Ko lagoon, a multiple sediment trap was moored at a trap station
off the coast of Sakae-ura in Hokkaido (Fig. 1) on January 21 when there was some ice in the
lagoon but before complete ice coverage. The trap held 12 cylinders (8.5 cm inside diameter
and 25.5 cm deep), with each cylinder being open for seven days before the motor drive
closed that cylinder and opened the next cylinder (Taguchi et al. 1997b). Prior to deployment,
each cylinder was filled with a 4 % NaCl solution. The trap array was bottom-anchored, with
the cylinders 4 m below the water surface and 5 m above the bottom as in the previous study
(Taguchi et al. 1997b). The 12 cylinders were sequentially opened for seven days between
January 21 and April 15, 1999.

A
Saroma-ko
Lagoon
44
Latitude (N)

Hokkaido
Hokkaido

42

140 142 144 146

Longitude (E)

B
Sea of Okhotsk

Saroma-Ko
Lagoon

Figure 1. A, Map of Hokkaido, showing the location of Saroma−Ko Lagoon (open circle) and
Monbetsu Tide Gage Station (open square); B, Location of the sediment trap station (filled circle) in
Saroma-Ko Lagoon and the rader station at Tokoro (filled square).
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 439

The hourly data of air temperature was taken from the Radar AMeDAS at Tokoro
(144o06‘E, 44o09‘N, Fig. 1B). The water temperature was continuously observed at the
vicinity of sediment trap station as part of the monitoring system of Saromako Aquaculture
Research Center. The hourly data of tide height was obtained from Monbetsu port, where is
60 km far from Saroma-Ko Lagoon (Fig 1A).
Shortly after the lagoon was ice-free, the sediment trap array was retrieved and taken to
the nearby laboratory. The samples from each cylinder of the sediment trap array were kept at
20oC until time of analysis, when each sample was melted in a cold room and split to four
sub−samples by a Folsom splitter (Sell and Evans 1982). For the determination of chlorophyll
a (Chl a), the first subsamples were filtered onto a Whatman glass fiber filter type GF/F.
Chlorophyll a pigments were extracted by N, Ndimethylfolmamid in opaque vials (Suzuki
and Ishimaru 1990). The concentration of Chl a was measured on a fluorometer (Turner
Designs, Model 10AU) with the method recommended by Holm-Hansen et al. (1965). The
second sub−samples for determination of biogenic silica (BSi) were filtered onto a Millipore
polycarbonate filter with 0.2 µm of pore size. Concentration of BSI was determined
spectrophotometrically by the method of Paasch (1980). All measurements were conducted in
duplicate. The last subsamples were fixed with buffered formalin for microscopic analysis
of the species composition. Taxonomical identification, enumeration, and size (volume)
determination of species were carried out on an inverted light microscopy (Olympus IMT−2).
The subsamples were settled for at least 24 h (Hasle 1978) and minimum of 400 cells was
processed (Lund et al. 1958).
In order to differentiate between ―ice algae‘ and ‗water column phytoplankton‘, on
February 15 and 17, 1999, five ice cores were obtained using a CRREL core sampler (Rand
and Mellor 1985) in addition to water samples at 1 m water depth (using Niskin bottles) in the
vicinity of the sediment trap array. The bottom surface (03 cm) of each core was sectioned
and melted in 3 % NaCl solution to avoid any breakage of cells due to osmotic pressure
(Sime-Ugando et al 1997). The aliquots were processed for microscopic analysis as
mentioned above. Ice algae and water column phytoplankton were identified by the
taxonomic descriptions as provided by Hasle (1973; 1990), Hasle and Syversten (1988),
Poulin and Cardinal (1982; 1983), Medlin and Priddle (1990), Round et al. (1990), Krammer
and Lange-Berta lot (1991), and Tomas (1997). Cell volume of ice algae and phytoplankton
cells were estimated by the methods described in Hillebrand et al. (1999).
The following premises are made in the present study; (1) the allocation of cells as ‗ice
algae‖ or ‗water column phytoplankton‘ as determined from the ice core and water column
studies as described above can be used to separate two groups of algae as recovered in the
cylinders of the seiment trap array; 2) the ratio of cell volumes to cellular Chl a and to BSi are
similar in ‗ice algae‘ as compared to ‗water column phytoplankton‘; 3) daily vertical flux can
calculated by dividing the measured amounts in each cylinder by the number of days each
cylinder was open. Daily vertical flux during the eleventh trap was corrected to the actual
length of ice coverage period because the trap was closed one day earlier than the end of
complete ice coverage.
440 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

10

A
5

Air temperature (oC)

0

-5

-10

-15

-20
-0.6

B
-0.8

-1.0
Water temperature (oC)

-1.2

-1.4

-1.6

-1.8

-2.0
04-Feb

11-Feb

18-Feb

25-Feb

04-Mar

11-Mar

18-Mar

25-Mar

01-Apr

08-Apr

Date

Figure 2. Temporal changes in environmental conditions at Saroma−Ko Lagoon during the period of
complete ice coverage (February 4 to April 8, 1999). A. Changes in air temperature, with regression
line for the data shown by the solid line; B. Changes in water temperature. Vertical lines indicate the
duration of the time period during which each trap-cylinder was open, with the number of the cylinder
shown on the upper abscissa.
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 441

RESULTS

Environmental Conditions Before and After Trap Deployment

Although some sea ice formation was sporadically observed from the end of December
1998, it was not until February 3, 1999, that sea ice completely covered the surface area of
Saroma-Ko Lagoon. The air temperature in the period immediately preceeding deployment of
the sediment trap array was below −10.0 oC during the period of complete ice coverage the air
temperature fluctuated considerably from −15.0 oC to +5.0 oC, with the regression line
showing the general increase from −8 oC on February 4 to −1 oC on April 8 (Fig. 2A). With
increasing air temperature and a strong spring wind, the sea ice disappeared completely on
April 9, 1999 (Kohno, per. comm.). Duration of the complete ice coverage was 65 days.
Overlying snow depth was 10 cm on March 11with 40 cm ice thickness and a 2cmincrease
of sea ice thickness was observed during the data logger deployment from February 10 to
March 11 (Shirasawa, pers. comm.).
Air temperature during the complete ice coverage period fluctuated almost weekly, which
was frequently observed at the southern location in the sea ice ecosystem of Northern
Hemisphere (Fig. 2). Air temperature higher than the mean of −5.0 oC during the ice season
was observed during the forth, sixth, eighth, tenth, and eleventh sediment trap openings. The
coldest air temperature was observed during the fifth sediment trap opening from February 19
to 25.

Date
Mar/04

Mar/11

Mar/18

Mar/25

Apr/01

Apr/08
Feb/04

Feb/11

Feb/18

Feb/25

440

420

400

380
Tide (cm)

360

340

320

300

280
800 1000 1200 1400 1600 1800 2000 2200 2400

Time (hours)

Figure 3. Temporal changes in tide height at Monbetsu port. Hour 817 and 2161 correspond to the first
hour (01:00 am) of February 4 (beginning of Trap 3) and to the last hour (24:00pm) of April 8 (closing
of Trap 11), 1999, respectively.
442 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

Water temperature changed from the positive to negative value on December 22, 1998
and continued to decrease to −1.8 oC on January 10, 1999. During the first three sediment trap
openings from February 4 to 25, the water temperature fluctuated between −1.8 oC and −1.6
o
C and thereafter gradually increased to −0.8oC when the last cylinder was closed on April 8
(Fig. 2B).
The overlying snow depth on the ice was 10 cm on March 1. On March 11 the ice
thickness was 40 cm (Shirasawa, pers. comm.). During the period from February 10 to March
11 the temperature of the ice at 20 cm below the ice surface showed a temporal change from
−3.1 to −1.5 oC, which reflected the increase in air and water temperatures during that time
period.
During the period when the first four cylinders were closed the daily tide change was
relatively large (generally > 100 cm) and variable. During the time of the second half of the
trap deployment, the change in the daily tide showed less variability and was generally < 80
cm (Fig. 3). However, the difference between two periods was not significant.

Table 1. Top seven species of ice algae and water column phytoplankton observed in the
sediment traps in term of cell abundance and cell volume.

Species Maximum cell abundance Maximum cell volume

(106 cells m−2 d−1) (109 cell volume m−2 d−1)
Ice algae
Fragilariopsis spp. 101 10.6
Achnanthes spp. 83.0 25.4
Odontella aurita 13.9 116
Detonula confervacea 8.88 20.7
Navicula spp. 3.54 9.83
Bacterosira fragilis 5.73 13.3
Pleurosigma spp. 0.143 33.5
Water column phytoplankton
Thalassiosira spp. 47.0 392
Chaetoceros spp. 3.41 19.8
Amphora spp. 1.66 4.81
Dictyocha speculumn 1.50 3.04
Membraneis spp. 1.15 969
Alexandrium sp. 0.29 3.17
Campylodiscus sp. 0.29 389

Dominant Species of Ice Algae and Water Column Phytoplankton

Prior to the complete ice coverage, in the first two sediment traps, Thalassiosira spp.
were dominated more than 86 % of water column phytoplankton while Odontella aurita and
Achnanthus spp. were dominated more than 60 % of ice algae. During the complete ice
coverage, diatoms exclusively dominated the top seven species of the ice algal community
with a different descending order between cell density and cell volume (Table 1).
Fragilariopsis spp. were most abundant in term of cell density while in term of cell volume
Odontella aurita was most abundant and followed by Pleurogima spp., Achnanthes spp.,
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 443

Detonula confervacea, Bacterosigma fragilis, Fragilariopsis spp., and Navicula spp. All
these diatom species were also found in the bottom 3-cm sea ice core collected on February
15 and 17, 1999. For water column phytoplankton, diatoms, dinoflagellates, and
silicoflgellates were dominant groups in the top seven species with a different descending
order based on either cell density or cell volume (Table 1). Within a group of diatoms,
volumetrically Membraneis spp. and Thalassiosira spp. were dominated consistently
throughout the complete ice coverage while Campylodiscus sp. was occurred as the second
dominant species only in the tenth sediment trap. For other two groups, Alexandrium sp. was
mainly occurred in the last three sediment traps during the complete ice coverage while
Dictyocha speculumn were occurred throughout the complete ice coverage. Diatoms and
silicoflagellates except for Alexandrium sp. were also observed at < 106 cells m−3 in the water
samples collected 1 m below the bottom surface of sea ice on February 15 and 17, 1999.

Temporal Changes in Cell Volume

Temporal changes in the total cell volume of ice algae and water column phytoplankton
indicated the maximum of 1820 × 109 µm3 m−2 d−1 during the period from March 25 to April
1 (Trap 10) and the minimum of 54 × 109 µm3 m−2 d−1 during the period from March 19 to 25
(Trap 9, Table 2). Total cell volume of ice algae ranged from 148 × 109 µm3 m−2 d−1 during
the period from April 1 to 8 (Trap 10) to 22 × 109 µm3 m−2 d−1 during the period from
February 19 to 25 (Trap 5, Table 2). Temporal changes in cell volume of ice algae was
mainly caused by Odontella aurita which occupied usually more than 50 % of total ice algal
cell volume except for Trap 10 (Fig. 4). In Trap 10, Pleurosigma spp. and Achnanthes spp.
were more abundant than Odontella aurita. Total cell volume of water column phytoplankton
stayed between 250 and 470 × 109 µm3 m−2 d−1 from February 4 to March 11, and thereafter
decreased to about 10 × 109µm3 m−2 d−1, and increased to one higher than 700 × 109 µm3 m−2
d−1 (Table 2).

Table 2. Cell volume (x 109 µm3 m−2 d−1) and relative abundance (%) of ice algae and
water column phytoplankton in Saroma-Ko Lagoon, Hokkaido, Japan. Mean and S.D.
indicate annual mean and one standard deviation, respectively.

Trap Number Duration Cell volume Relative abundance

Total Ice algae Water column Ice algae Water column
phytoplankton phytoplankton
3 Feb 4 to 11 470 122 348 25.9 74.0
4 Feb 12 to 18 544 126 418 23.2 76.7
5 Feb 19 to 25 276 21.6 254 7.87 92.1
6 Feb 26 to Mar 4 527 112 414 21.0 78.0
7 Mar 5 to 11 557 80.1 467 14.6 85.4
8 Mar 12 to 18 55.5 46.0 9.5 82.8 17.2
9 Mar 19 to 25 53.5 38.6 14.7 71.5 28.5
10 Mar 26 to Apr 1 1810 148 1660 8.19 91.8
11 Apr 2 to 8 791 100 691 12.8 87.2
Mean 565 88.3 475 29.8 70.3
± S.D. 526 44.2 494 27.7 27.7
444 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

The cell volume of water column phytoplankton ranged from 1660 × 109 µm3 m−2 d−1
during the period from March 25 to April 1 (Trap 10) to 9.5 × 109 µm3 d−1 during the period
from March 12 to 18 (Trap 9, Table 2). The most striking feature was characterized by two
major groups; Thalassiosira spp. and Membraneis spp. (Fig. 4). The former group always
occurred throughout the observation and dominated at 75 % in Traps 8 and 9 whereas the
latter group disappeared from Traps 8 and 9. Although the maximum and minimum total cell
numbers collected in the sediment traps showed two magnitudes of order difference, relative
abundance of ice algae in the total algae was stayed in a relatively narrow range from 62 %
during the period from April 2 to 8 to 83 % during the period from March 12 to 18 (Fig. 5).

100
Relative abundance of cell volume (%)

80

60

40

20

0
3 4 5 6 7 8 9 10 11

Trap numbers
Odontella
Pleurosigma
Achnannthes
Detonera
Melosira
Pinnularia
Bacterosira
Navicula
others

Figure 4. Temporal changes in species composition of ice algae based on cell volume during the period
of complete ice coverage.
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 445

100

Relative abundance of cell volume (%)

80

60

40

20

0
3 4 5 6 7 8 9 10 11

Trap numbers
Membraneis spp.
Thalassiosira spp.
Campylodiscus sp.
Amphora spp.
Chaetoceros spp.
Alexandrium sp.
Dictyocha
others

Figure 5. Temporal changes in species composition of water column phytoplankton based on cell
volume during the period of complete ice coverage.

Relationship between Cell Volume and Chl A and BSi

A significant relationship was obtained between total cell volume of ice algal community
(× 1010 µm3 m−2 d−1) and water column phytoplankton assemblages and amounts of Chl a or
BSi (mg m−2 d−1) in the sediment traps as Y = 8.6 × 10−11 X + 0.30, r2 = 0.9421, p < 0.01 or Y
= 8.4 × 10−9 X + 39, r2 = 0.9654, p < 0.01, respectively (Fig. 6).
446 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

100

Relative abundance (%) 80

60

40

20

100

80
Relative abundance (%)

60

40

20

0
3 4 5 6 7 8 9 10 11

Trap numbers

Figure 6. Relative abundance of ice algal community and water column phytoplankton based on cell
density (upper panel) and cell volume (lower panel) during the period of complete ice coverage.

Vertical Flux of Chl a and BSi

A vertical flux of ice algal Chl a or BSi, which were calculated by applying a ratio of ice
algal cell volume to total algal volume to total amounts of Chl a or BSi in the sediment traps,
ranged from the maximum of 1.4 mg Chl a m−2 d−1 during the period from February 4 to 11
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 447

(Trap 3) and 127 mg BSi m−2 d−1 during the period from March 26 to April 1 (Trap 10) to the
minimum of 0.18 mg Chl a m−2 d−1 and 17 mg BSi m−2 d−1 during the period from February
19 to 25 (Trap 5), respectively (Fig. 7). A significant relationship was obtained between the
vertical flux of Chl a and BSi as Y = 12.2 × X + 80.5, r2 = 0.8249, p < 0.01.

18

16
Amounts of Chl a in sediment trap

14

12

10

1800

1600
Amounts of BSi in sediment trap

1400

1200

1000

800

600

400

200

0
0 5.0x1010 1011 1.5x1011 2.0x1011

Total cell volume in sediment trap

Figure 7. Relationship between cell volume of ice algae and other algae and chlorophyll a (upper panel)
and BSi (lower panel).
448 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

1.6

Ice algal Chl a flux (mg Chla m d )

-1
1.4

-2
1.2

1.0

0.8

0.6

0.4

0.2

0.0

140
Ice algal BSi flux (mg BSi m d )

120
-1
-2

100

80

60

40

20

0
3 4 5 6 7 8 9 10 11

Trap numbers

Figure 8. Temporal changes in vertical flux of ice algal chlorophyll a (upper panel) and BSi (lower
panel) during the period of complete ice coverage.

DISCUSSION
It has been one of the most difficult problems to estimate a vertical flux of organic matter
in shallow water because resuspension of the organic matter from the bottom is easily
occurred by tidal currents and/or riverine inflow. Although the effect of riverine inflow is at
the minimum during the ice season in Saroma-Ko Lagoon (Takeuchi 1993), a contribution of
water column phytoplankton to the total cell volume in the sediment traps is highly variable
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 449

due to effect of horizontal transport of water from the Sea of Okhotsk. One of the methods to
provide a possible separation of resuspended matter from the newly produced suspended
matter is a chemical ratio method introduced by Gasith (1975). The chemical ratio method is
only applicable to the present study area if the chemical composition of the material in ice
algal layer, sediment trap, and the bottom sediments are significantly different. The eastern
basin of SaromaKo Lagoon where the sediment trap array had been deployed was as shallow
as 9 m although the western basin was deeper than 20 m. A physical structure of the water
column at the present station has been known to have a feature of three layers; the sea ice
layer at the top, pycnocline in the first few meters, and high saline deep water (Taguchi et al.
1997a). The sediment trap array was aimed to locate within this high saline water layer in the
present study so that they were expected to catch the particles which sediment through the
pycnocline. There was also a logistic reason for the deployment depth of sediment trap array
at 4 m depth to avoid the damage caused by the ice floe from the Sea of Okhotsk. Because of
the shallowness, ice algal cells released into a water column reach rapidly the bottom without
any significant changes in the chemical composition as discussed by Michell et al. (1997).
Thick layers of ice algal aggregates or mats are usually observed at the bottom by scuba
divers under the sea ice (Fujiyoshi, pers. comm.) because ice algal aggregates are formed at a
much faster rate than other algae (Riebesell et al. 1991) and a low temperature may slow a
rate of degradation. This feature may explain why different chemical composition is unable to
obtain among the ice algal layer, the sediment trap, and the bottom sediments. The chemical
ratio method may be less applicable to the present unique situation.
Identification of ice algae can be employed to follow the sedimentation process in sea ice
ecosystems such as the present study area. Since a horizontal transport of water from the Sea
of Okhotsk to the water column under the sea ice in Saroma-Ko Lagoon can be occurred by
tidal currents, some pelagic water column phytoplankton but less possibility for ice algae
from the outside of the present study water can be found in the sediment traps. The
sedimentation process of ice algal community under the sea ice in the present study water can
be identified by microscopic determination. This can be supported by the following reasons;
the ice algae inhabited in the Sea of Okhotsk are most likely sunken out of a water column
even they are present in the water column before they are transported to the present water due
to a high sinking rate of ice algae (Levanter 2003) and pelagic water column phytoplankton
can be distinguished positively from the ice algae inhabited in the sea ice of Saroma-Ko
Lagoon. The temporal variability of water column phytoplankton in the sediment traps can be
governed by the abundance and the horizontal transportation rate of pelagic winter
phytoplankton in the Sea of Okhotsk.
The species of ice algae identified in the present study are similar to those observed
previously in the similar area (Takahashi 1981). Ice algal cells have been known to remain
not suspended in the plankton biomass in the present study area (Michel et al. 1997). Certain
ice algal species such as Fragilariopsis species might be able to survive in a water column
under the sea ice (Leventer and Dunbar 1987) but the abundance in a water column was low
as < 1 × 106 cells m−3 in the present study as observed by Michell et al. (1997). Once they are
released into a water column, they reach rapidly the bottom, where they provide a large
quantity of high quality food for the cultured scallops and oysters, which have a grazing
pressure on ice algal cells (Kurata et al. 1991). Zooplankton community in Saroma-Ko
Lagoon mainly consists of microzooplankton, which are too small to feed on ice algal cells
450 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

(Saito and Hattori 1997). The high sinking speed of released ice algal cells without a
significant loss due to zooplankton grazing in a water column also support the direct
relationship between the ice algal community and benthos.
A significant relationship between the total cell volume of both ice algal and water
column phytoplankton and the amounts of balk chlorophyll a or BSi in the sediment trap in
the present study may suggest that a portion of vertical flux of Chl a related with ice algal
community can be estimated from the bulk materials collected in the sediment traps based on
the assumption that a portion of ice algal Chl a or BSi in the bulk Chl a or BSi in the
sediment traps is similar to the cell volume ratio in the present study area. This assumption is
not necessarily relevant for other waters as discussed by Levanter (2003). Both relationships
have a positive intercept on Y-axis which indicates possible bias due to the shrinkage of cell
volume and degradation of Chl a and dissolution of silicate. The estimation of cell volume
based on the preserved samples could be underestimated by 8 % even for diatoms (Montagnes
et al. 1994). It took three months to process the sediment materials so that the latter processes
would be possibly occurred even though the samples were kept frozen in a dark condition.
Any temporal change in the relative abundance of diatoms in the total phytoplankton
could be one of error sources for the cell volume ratio method if their contributions are
extremely low. Although the average relative cell volume contribution of diatoms in the total
algae was about 30 % in the present study area, as long as the relative cell volume
contribution of ice algae is considered, the cell volume ratio method may be less biased by the
temporal change in the relative abundance of ice algae in the total algae. A temporal change
in the relative abundance of cell volume within ice algal cells may influence the sinking speed
of ice algal community (Smayda 1970). However their sinking speed is faster than water
column phytoplankton cells due to a tendency to form aggregate (Riebesell et al. 1991), the
cell volume ratio method should be able to differentiate ice algal Chl a and BSi from the bulk
of Chl a and BSi with a reasonable accuracy. A significant relationship between the estimated
vertical flux of Chl a and BSi may also support the reasonable estimation in the present study.
The high variability in the vertical flux of Chl a and BSi observed in the present study
may indicate that growth condition and their trophic interaction within the ice algal
community are highly variable during the ice season. Variability in the growth condition and
their interaction can be related with air temperature. Higher than 100 × 109 µm3 m−2 d−1 was
usually associated with the air temperature higher than −5 oC except for during the period
from March 12 to18 (Trap 8). The least loss of algal cells from the sea ice observed during
the period from February 9 to 25 (Trap 5) might be caused by the coldest air temperature in
the present study. The coldest air provides a solid structure of the bottom portion of brine and
the accumulation of Chl a and BSi in the growing cells within the sea ice are occurred with a
decreasing available light. The decrease of light is caused by a steady thickening of sea ice
and accumulation of snow on the sea ice and this situation enforces ice algal cells shade
adapted (Obata and Taguchi 2009). This trend to shade adaptation is likely further enforced
by the consistent appearance of large cells such as Odontella aurita because large diatoms in
the ice algal community are subjective to a high package of Chl a per cell (Finkel 2001).
When both air and water temperature are suddenly increased as observed during the period of
last two trap openings, ice algal cells are easily released into a water column (Nomura et al.
2008) so that they cannot take advantage to remain in the brine to grow rigorously. When the
frequent increase of water temperature warmer than −1.6oC is occurred, the sea ice starts
melting and eventually disappeared.
 Vertical Flux of Ice Algae in a Shallow Lagoon, Hokkaido, Japan 451

When the cell ratio method is applied to the trapped materials, which contain sediment
materials associated with not only ice algal community but also non-ice algal community, the
vertical flux of ice algal community can be estimated as long as the ice coverage is
maintained in the present study area. Although a significant relationship between the vertical
flux of ice algal Chl a and BSi estimated in the present study does not necessarily support a
validity of cell ratio method, the slope between them is within a range of BSi:Chl a ratios
observed for nutrient limited and saturate diatoms (Harrison et al. 1977). Although it is
difficult to confirm the validity of our estimates of vertical flux, the comparison with the
previous studies may suggest that our estimates are within their range (Sasaki and Fukichi
1993; Michell et al. 1997; Taguchi et al. 1997b). The high variability in the vertical flux of
Chl a and BSi as indicated by 44-% of coefficient of variation can be related with air
temperature as observed in the variability in the ratios discussed above. The increase in the
vertical flux during the period from March 26 to April 8 (Trap 10) seems to be accompanied
by the increase of air temperature, which subsequently causes the temperature of sea ice to
increase. A laboratory experiment shows that a steady increase of water temperature weakens
the bottom structure of sea ice and subsequently high salinity brines are dropped out due to
the heavy density (Wakatsuchi and Ono 1983). The peak in the vertical flux was also related
with significant increase of air temperature and spring wind at the end of the ice season
(Meteorological Agency of Japan, 1999).
On the scale of days a frequent release of brine has been also observed to be related with
highly variable air and sea ice temperature in the present study area (Nomura et al. 2009). The
unstable fluctuation of air temperature is directly related with the southern location of
SaromaKo Lagoon in the sea ice ecosystem of Northern Hemisphere (Honda et al. 1994).
Ice algal community is one of the most important primary producers in the sea ice
ecosystem and a portion of those is continuously released into a water column even during the
ice growing period as observed in the present study. The species composition of released ice
algal community also varies as ice grows as observed under the high latitude sea ice
(Ishikawa et al. 2001). The released ice algal community has also the important role being
utilized by benthos because the abundance of phytoplankton is low during the duration of ice
coverage. The long−term success in the aquaculture of scallops and oysters in the present
study area may not be maintained without the supply of organic matters derived from the ice
algal community. The ecological significance of the ice algal community in addition to the
primary producer in the sea is the supplier of organic matters to the benthos due to a short
distance from the sea ice at the surface water to the bottom in shallow, coastal water such as
the present study area.
In conclusion, the effects of the re−suspension of organic matters in a water column and
the lateral transport of phytoplankton assemblages always occurs even during the complete
ice coverage and is highly variable; 70 ± 28 % in the present study. Annual supply of ice algal
cells, Chl a, and BSi from sea ice were 3.97 x 109 cells m−2, 58 mg Chl a, and 5.5 g BSi m−2
for 65 days of complete ice coverage duration, respectively. If we assume a plant carbon to
chlorophyll a ratio of 54 (Taguchi et al. 2004), total amounts of plant carbon released from
the sea ice could be about 3.2 g C m−2 per ice season. If about 3-% of organic carbon in total
mass flux is assumed in the present study area (unpublished data), the present estimate is
similar to those observed in high latitudes as summarized by Levanter (2003). The quality of
organic matters related directly with the ice algal community might be highly variable due to
the growth condition and trophic interaction which depend on temperature. When a temporal
452 Yoko Niimura, Hiroaki Saito, and Satoru Taguchi

variation of the energy flow is considered in a shallow, coastal water of sea ice ecosystem, the
re-suspension and lateral transport of phytoplankton should be considered in relation to air
temperature and tide.

ACKNOWLEDGMENTS
We thank H. Hattori and his colleague who helped the deployment of the multiple
sediment traps in the field. This work would not have been completed without logistic support
from Y. Fujiyoshi and N. Kohno. We deeply appreciate K Shirasawa and N. Kohno for
providing data. All facilities for sample analysis were provided by Soka University. This
work was partly supported by the Institute of Low Temperature Science in Hokkaido
University. Critical comment provided by O. Holm-Hansen was extremely constructive and
helpful. All assistance provided by the Scripps Institution of Oceanography, University of
California, San Diego was greatly appreciated.

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In: Lagoons: Biology, Management and Environmental Impact ISBN: 978-1-61761-738-6
Editor: Adam G. Friedman, pp. 457-473 © 2011 Nova Science Publishers, Inc.

Chapter 17

THE EVALUATION OF SOME LIMNOLOGICAL

FEATURES OF THE LAGOON LAKES
IN EUROPEAN PART OF TURKEY

Belgin Çamur-Elipek and Timur Kırgız

Trakya University, Faculty of Science, Department of Biology, Edirne, Turkey

ABSTRACT
Lagoons have perfect hydrodynamic perspective and very sensitive structures. First
of all, the human activities on lagoons have become a major environmental concern. Any
artificial influence to these sensitive areas may cause the destruction of the natural
balance of them.
Turkish coasts have more than 70 lagoon lakes which are formed on about 60 000
ha. area. European part of Turkey which is also named as ―Turkish Thrace‖ is surrounded
by three different seas: The Marmara Sea, The Black Sea, and The Aegean Sea. The
region has a lot of lagoon lakes (such as Lakes Mert and Erikli are located on the coasts
of The Black Sea in Kırklareli province; Lakes Terkos, Küçükçekmece, and
Büyükçekmece are located on the coasts of The Marmara Sea in İstanbul province; and
Lakes Gala, Dalyan, Taşaltı, Işık, Vakıf, and Tuzla are located on the coasts of The
Aegean Sea in Edirne province) which are formed at different types. Therefore, Turkish
Thrace may be considered as a rich area in terms of lagoon lakes. Furthermore, some
lakes are important parts of some National Parks in Turkey.
In this chapter, some limnological features of some lagoon lakes located in European
part of Turkey were evaluated. With this aim, both the results of the previous
limnological studies performed by different researchers (by the authors and/or the others)
since 1987 in some lagoons in the region and the results of the present data on the lakes
which were visited on different dates by the authors at the years 2008 and 2009 for
sampling were evaluated. According to the all data (both from the previous studies and
from the present study) some physicochemical features, salinity levels, some biological
data of the lagoons were gathered in this chapter. Furthermore, rather roughly trophy
levels of the lagoons were determined by the available features which are used to
determine the trophy level of the lakes. In conclusion, this study aimed to gather all data
458 Belgin Çamur-Elipek and Timur Kırgız

on the lagoons in European part of Turkey by making a comparison of their former and
present status.
Consequently, the results from the previous limnological studies performed in some
lagoons in the region (a review); the results from the present data on some features of
some lagoons (a research); limnological evaluation on all of the lagoons in the region (an
evaluation) were provided in the present chapter. Thus, it was provided the whole
limnological documents which have been gathered from the lakes at separate times since
1987.

1. INTRODUCTION
Although they have different forming types, lagoons are generally known as aquatic
ecosystems which are located on coastal areas of marine environments. There are a lot of
factors determining the formation type of a lagoon: the connection type between the mouth of
river and marine environment, amounts and types of the sediment which are carried by flow
of river or tide zone of marine environments. A lagoon may be formed at mouth of a river
(alluvial deposit from river may accumulate at the mouth of the river and settled to water or
alluvial deposit from marine environments may accumulate and settled to the mouth of river),
at delta of a river basin (wetland area may be formed as a lagoon), or at small bay in marine
(alluvial deposit from marine environment may close the bay as a lagoon). Salinity of a
lagoon is determined by both water amount from the river and changes of water from sea. The
salinity of the lagoons ranges from nearly fresh to hyperhaline waters. Therefore lagoons have
saline, brackish, or fresh water and their salinities may change seasonally.
Lagoons and its surrounding areas are used both to provide the agricultural products,
fisheries and other aquatic activities and also to serve to the tourism sector. Lagoons are very
sensitive areas and they are affected by surrounding environments. The physical, chemical,
and biological components of the lagoons differ from one other. Therefore, it is very
important to keep their sustainable use management. With this aim, we have to learn their
hydrobiological structures. Their biological productivities and carrying capacities may change
and thus they do not sustain their specific functions.
A lot of activities belonging to agricultural, industrial, urban, and tourism surrounding of
lagoons may cause deterioration on natural balance of these sensitive areas. These
environmental deteriorations can be observed as some changes in their physicochemical
features.
Lagoons are the most productive areas in the ecosphere. Their productivity amounts are
the highest because of nutrients carried by rivers, and fish production is very high in these
habitats [1]. Nutrient loadings coming from both intent and extent surrounds, they have a
major impact on water quality and ecology. The high nutrient concentrations in the water can
be pointed out that the lagoon has eutrophic character [2]. A lagoon can be considered as
oligotrophic when it has low levels of nutrient concentrations in the water [2]. Mesotrophic
lagoons have medium level of nutrient concentrations in the water [2].
Hydrodynamic parameters can change at each lagoon lake. But it should be monitored its
hydrodynamic parameters to know the situation of yesterday, today, and future‘s of the lake.
Each lake has its own features. It changes as time passes and therefore it should be monitored
periodically.
 The Evaluation of Some Limnological Features of the Lagoon Lakes… 459

Flows, salinity, nutrients, temperature, and other physicochemical features of lagoon, and
discharges, salinity, and water temperature from the rivers and artificial outlets to a lagoon
must be monitored periodically.
Some parameters such as water salinity, temperature, light permeability, conductivity
may be necessary for some modelling aspects in the lagoon. Furthermore, the other some
parameters such as dissolved oxygen, hydrogen sulphide, pH, nutrients, etc. are necessary to
identify the trophy level of a lagoon. Biological parameters such as chlorophyll-a,
phytoplankton, zooplankton, macrophytes, macrozoobenthos, and Ichthyofauna are also
necessary to monitory the trophy level of a lagoon.

2. LAGOON LAKES IN TURKISH THRACE

Turkish Thrace (23764 km2) is located in the north-west of Turkey that is geographically
part of Europe. This part of Turkey is occupying the south-eastern tip of the Balkan
Peninsula. It is surrounded by three different seas: Black Sea in the northeast and by the Sea
of Marmara and the Aegean Sea in the south. It includes several lakes that have traditionally
sustained Turkish coasts have more than 70 lagoon lakes which are formed different forming
types. European part of Turkey which is named as Turkish Thrace has more than 10 lagoons
or lagoon type forming lakes. In this chapter it is given the brief summaries on some
hydrobiological features of the Turkish Thrace lagoons from the studies which have been
performed since 1983 are given. Thus, it is presented a comparative analysis of the lagoon
lakes in Turkish Thrace for the future studies.

2.1. General Knowledge on the Lagoons of Turkish Thrace (Location, Origin

and Hidrography)

A total of 11 lagoon lakes in the European part of Turkey are presented in this chapter
(Figure 1). Some of them have freshwater while they had salty water before. The others have
water range salty to freshwater characters.
Furthermore, some field experiments were carried out in some lagoons in the years 2008
and 2009. Conductivity, pH, and temperature profiles were obtained at several locations in the
lagoons. Depth of each studied lake was also measured and the light permeability of the lakes
was recorded. The water samples which were sampled from the lagoons were availed by
using Ruttner Water Sampler and carried to the laboratory to determine salinity, total
hardness, Mg+2, Ca+2 profiles, some nutrients (NO2-N, NO3-N, SO4-2, PO4-3), dissolved
oxygen, solid suspended material were measured by classical titrimetric and
spectrophotometric methods [3].
460 Belgin Çamur-Elipek and Timur Kırgız

Figure 1. The locations of the lagoon lakes in Turkish Thrace (1:Erikli, 2:Mert, 3:Terkos,
4:Küçükçekmece, 5:Büyükçekmece, 6:Tuzla, 7:Vakıf, 8:Işık, 9:Dalyan, 10:Taşaltı, 11:Gala)

2.1.1. Lake Erikli

This lagoon lake is located between 41˚52'55"N, 27˚59'11"E (Demirköy/Kırklareli) by
length is about 1-1.5 km (Figure 2). It has 43 ha. (0.43 km2) area and most of this area (36.5
ha) is covered by Phragmites austrialis [4]. Its maximum depth is 1.5-1.8 meters [4, 5]. This
lagoon lake is formed by alluvial deposit from Efendi stream. The Black Sea is located on
east of the lake. The forest area behind the lake remains under water level when the water
level rises after excessive flows from the rivers. This area is named as ―Erikli Longos area‖.

Figure 2. Erikli lagoon lake

 The Evaluation of Some Limnological Features of the Lagoon Lakes… 461

Table 1. Some physicochemical characters in Erikli Lake

(İğneada/Kırklareli) (from Güher [4])

Parameters\Months May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr.
Water temp.(0C) 19.7 17.7 20.9 13.8 17.46 19.0 3.6 6.6 5.0 6.3 13.3 22.3
DO. (mg·L-1) 5.56 8.53 6.56 9.00 8.26 7.75 13.34 9.21 9.60 8.54 9.96 7.54
pH 8.19 7.89 8.09 9.33 9.49 9.06 7.80 9.38 7.67 6.66 8.11 7.82
Depth (cm) 111.6 113.3 94.33 76.66 60.00 73.3 125.0 103.3 111.6 130.0 115.0 123.3
Turbidity(cm) 45.0 43.3 61.0 43.3 48.3 56.6 65.0 36.6 81.6 76.6 95.0 115.0
EC (mho·cm-1) 226 300 523 1307 1045 1512 925 485 113 195 476 83
Mg (mg·L-1) 26.3 31.0 - 91.9 148.6 206.5 301.1 25.3 - 39.6 77.2 26.2
Ca (mg·L-1) 66.1 47.4 - 67.6 74.8 136.2 35.2 32.0 - 51.2 68.0 40.2
T.H. (FS)0 33.8 36.6 - 71.8 98.8 153.4 142.0 26.5 - 42.0 65.9 31.1
Cl- (mg·L-1) 392 444 - 1771 3001 3083 5034 2722 - 730 1612 383
NO3-N (mg·L-1) - - - 0.017 0.077 0.056 0.05 0.05 - 0.0002 0.0001 0.37
NO2-N (mg·L-1) - - - 0.012 0.001 0.001 0.001 0.003 - 0.0006 0.0008 0.015
Phosphate (mg·L-1) - - - rare 0.2 0.19 0.19 0.19 - 0.004 0.007 absent
(DO: Dissolved oxygen; EC: conductivity; T.H.: Total hardness)

2.1.1.1. Some Limnological Characters Of Lake Erikli

This lake was studied by Kırgız & Güher [6] and Güher [4] in previous studies to obtain
the some physicochemical features. According to the obtained results by Güher [4], dissolved
oxygen ranged between 5.56-13.34 mg/L, pH ranged between 6.6-9.4, turbidity (light
permeability) ranged between 43-115 cm, conductivity ranged between 83-1512 mho/cm,
magnesium ranged between 26-301 mg/L, calcium ranged between 32-136 mg/L, total
hardness ranged between 31-153 FS0, chloride ranged between 383-5034 mg/L, nitrate ranged
between 0.00018-0.37 mg/L, nitrite ranged between 0.0006-0.015 mg/L, phosphate ranged
between 0.00-0.2 mg/L. The results were showed that in Table 1. Also, in the study by Güher
[4], it was reported that 268105 zooplanktonik organisms in per m3 at average in the lake. In
the study which is performed by Kırgız & Güher [6] in the lake, it was reported that 600
macrozoobenthic individuals in per m2 at average belonging to a total of 11 different taxa [6].
In the studies which were performed in the years 2008 and 2009 in Erikli Lake, it was
found that the temperature 25 0C, pH 7.6, biological oxygen demand (BOD) 7.36 mg/L,
dissolved oxygen 4 mg/L, light permeability 34 cm, conductivity 1300 S/cm, NO3-N 0.76
mg/L, salinity 7.709 ‰, HCO3 6.5 mg/L, H2S 0.213 mg/L, solid suspended material 0.92
mg/L at average. It was also measured the amounts of NO2-N, carbonate, PO4-2 in the lake
during the sampling, but it was not found in any amount.

2.1.2. Lake Mert (Lake Koca)

This lagoon lake is located between 41˚52'09"N, 27˚57'57"E (Demirköy/Kırklareli) by
length is about 2 km (Figure 3). It has an area of 222 ha. area and a most of part of this area
(178 ha.) is covered by Phragmites austrialis [4]. Its maximum depth is 1.5 meters [4]. This
lagoon lake is formed by alluvial deposit from Deringeçit stream [4]. It is separated from the
Black Sea by a little sand area. It is sometimes related with the Sea when the water level rises.
Thus, this area is named as ―Mert (Koca) Longos area‖ when the water level rise and the
woodland area remains under the water. Mert and Erikli longos area have been declared as
―National Park of Iğneada Longos Forests‖ since 2007. The Longos forests (flooded forests)
cover a large area at Erikli and Mert lakes surroundings.
462 Belgin Çamur-Elipek and Timur Kırgız

Figure 3. Mert Lagoon Lake

2.1.2.1. Some Limnological Characters Of Lake Mert

This lake was studied by Kırgız & Güher [6] and Güher [4] in pervious studies to obtain
the some physicochemical features. According to the obtained results by Güher [4], dissolved
oxygen ranged between 6.9-13 mg/L, pH ranged between 7.1-9.2, turbidity (light
permeability) ranged between 40-110 cm, conductivity ranged between 296-2550 mho/cm,
magnesium ranged between 71-903 mg/L, calcium ranged between 53-212 mg/L, total
hardness ranged between 56-290 FS0, chloride ranged between 1285-41178 mg/L, nitrate
ranged between 0.0002-0.55 mg/L, nitrite ranged between 0.0001-0.03 mg/L, phosphate
ranged between 0.00-0.2 mg/L. The results have been showed that in Table 2. Also, in the
study by Güher [4], it was reported that 271919 zooplanktonik organisms in per m3 at average
in Mert lagoon. In the study which was performed by Kırgız & Güher [6], it was reported that
1624 macrozoobenthic individuals in per m2 at average in the lake. These individuals belong
to a total of 10 different taxa [6].

Table 2. Some physicochemical characters in Mert Lake

(İğneada/Kırklareli) (from Güher [4])

Parameters \ Months May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr.
Water temp.(0C) 17.8 19.9 20.1 15.3 12.7 17.6 4 11.6 10 6.3 13.6 18.3
DO. (mg·L-1) 6.9 12.5 9.1 9.1 9.0 7.1 13.0 9.9 8.7 9.5 9.5 8.1
pH 8.1 8.7 9.2 8.63 8.9 8.34 7.95 7.9 7.8 7.17 8.01 7.89
Depth (cm) 125 113 98 71 56 73 116 71 86 108 115 100
Turbidity(cm) 60 48 75 63 56 66 40 43 75 79 110 100
EC (mho·cm-1) 296 900 1023 3525 1985 2550 1125 2235 1350 925 678 586
Mg+2 (mg·L-1) 71.8 903.5 - 505.4 493.6 424.2 374 307.7 - 132.8 274.0 135.4
Ca (mg·L-1) 53.2 136.4 - 181.0 186.6 212.4 47.6 121.4 - 70.9 116.2 81.3
T.H. (FS)0 56 196.4 - 285.3 282.9 290.6 178.3 187.7 - 90.3 171.2 96.6
Cl- (mg·L-1) 1285 5443 - 8927 10114 10346 6580 41178 - 2769 5536 3193
NO3-N (mg·L-1) - - - 0.064 0.073 0.056 0.050 0.050 - 0.0002 0.0004 0.55
NO2-N (mg·L-1) - - - 0.01 0.001 0.001 0.001 0.003 - 0.0001 0.0009 0.034
Phosphate (mg·L-1) - - - rare 0.20 0.19 0.18 0.19 - 0.07 0.005 absent
(DO: Dissolved oxygen; EC: conductivity; T.H.: Total hardness)
 The Evaluation of Some Limnological Features of the Lagoon Lakes… 463

Figure 4. Terkos Lagoon Lake

In the studies which were performed in the years 2008 and 2009 in Mert Lake, it was
found that the temperature is 26 0C, pH 8.6, biological oxygen demand (BOD) 7.06 mg/L,
dissolved oxygen 3 mg/L, light permeability 103 cm, conductivity 2050 S/cm, salinity 9.55
‰, HCO3 5 mg/L, H2S 0.426 mg/L, solid suspended material 1.42 mg/L at average. It was
also measured the amount of NO3-N, NO2-N, carbonate, PO4-2 in the lake during the
sampling, but it was not found.

2.1.3. Lake Terkos (Lake Durusu)

This lagoon forming lake has a surface area of 25-32 km2 (Figure 4). It has a maximum
depth of 11 meters [7]. Its maximum length is 14 km., and width is 6 km. It is located near the
Black Sea coast of Turkey between 40˚19' N, 28˚32' E (Çatalca/İstanbul), and it is one of the
six main drinking water reservoirs of the Istanbul metropolitan area, providing 25% of the
water demand. The lake is fed by Istranca River so its waters are fresh and its salinity is low,
with an average 0.02‰ [7]. Freshwater fish species predominate [8]. The largest river in the
drainage area is Istranca River. This lagoon is formed at the end of Quaternary. Firstly, a bay
has been formed in the Sea. And then, this bay has been separated from the Sea by alluvial
deposit from Istranca River. This lagoon is surrounded by settlements, agricultural areas and
by small forests.

2.1.3.1. Some Limnological Characters Of Lake Terkos

This lake was studied by Çamur-Elipek [7] in pervious study to obtain the
physicochemical features. According to her obtained results, dissolved oxygen ranged
between 8.94-11 mg/L, pH ranged between 7.6-8.5, turbidity (light permeability) ranged
between 65-204 cm, conductivity ranged between 188-309 mho/cm, magnesium ranged
between 3.8-13.7 mg/L, calcium ranged between 41.5-58.1mg/L, total hardness ranged
between 12-20 FS0, chloride ranged between 27.5-38.7 mg/L, nitrate ranged between 0.00-
0.61 mg/L. The results were showed that in Table 3. Also, in the study by Çamur-Elipek [7],
it was reported that 1278 benthic organisms in per m2 at average. These individuals are
belong to a total of 41 different taxa [7].

2.1.4. Lake Küçükçekmece

This lagoon lake is situated at twenty-four kilometers (24 km) southwest away from the
center of Istanbul and adjacent to the Marmara Sea (41º00' N-28º43' E) (Figure 5). It has a
surface area of 15.22 km2 [9]. The lake is 10 km in length and 6 km in its widest part. The
464 Belgin Çamur-Elipek and Timur Kırgız

average depth of the lake is approximately 10 meters and the deepest part is 20 meters near
the southern edge of the lake [10]. A narrow channel connects it to the Marmara Sea in the
southeast and the lake is connected to the Marmara Sea via this channel, but besides sea
water, the main water supply comes from fresh underground springs and several small
streams [11]. Three stream systems feed the lake: Nakkaşdere, Sazlıdere and Ispartakule [12].
The Sazlıdere stream output into the lake is much less due to the damming of this stream in
1995, which formed Sazlıdere Lake [13]. The lack of fresh water which was comes from the
Sazlıdere stream does not affect Küçükçekmece‘s water level due to its connection with the
Marmara Sea [13]. Since the discharge of Nakkaşdere stream was stopped and diverted
offshore to the Marmara Sea by a new pipeline system in 2005, the lake has been fed by the
Ispartakule stream from the northwest, surface runoff from the surrounding areas and by the
sea water from the south [13]. Formerly the water of the lake was saline then it turned to fresh
water by the river discharges [9]. Although, it is separated from the sea by a set, the lake has
brackish water [10].

Figure 5. Küçükçekmece Lagoon Lake

Table 3. Some physicochemical characters in Lake Terkos

(Çatalca/İstanbul) (from Çamur-Elipek [7])

Parameters\Months Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar.
Water temp.(0C) 15.1 20.3 22.6 25.5 25.3 18.1 12.3 13.1 8.52 8.02 7.3 13.9
DO. (mg·L-1) 10.2 11.0 10.2 8.94 9.36 10.0 10.7 10.5 11.0 11.0 11.1 9.59
pH 8.04 8.12 8.09 7.98 8.27 8.32 8.14 8.55 8.39 8.42 7.75 7.64
Depth (cm) 899 871 839 814 749 672 834 565 584 612 724 745
Turbidity(cm) 165 156 118 139 113 65 204 141 178 120 136 155
EC (mho·cm-1) 244 238 283 300 309 229 188 239 260 257 217 243
Mg (mg·L-1) 4.30 4.11 3.86 4.74 7.06 9.75 6.96 12.9 13.0 13.7 9.87 9.29
Ca (mg·L-1) 42.7 43.3 44.4 42.7 42.4 41.6 41.5 45.3 58.1 57.8 52.4 56.7
T.H. (FS)0 12.4 12.5 12.7 12.6 13.5 14.4 13.2 16.6 19.9 20.1 17.1 18
Cl- (mg·L-1) 27.5 31.9 30.3 30.9 37.5 38.7 36.5 38.0 35.8 37.5 32.4 35.9
NO3-N (mg·L-1) 0.12 0.00 0.00 0.61 0.00 0.00 0.04 0.03 0.00 0.00 0.00 0.13
(DO: Dissolved oxygen; EC: conductivity; T.H.: Total hardness)
 The Evaluation of Some Limnological Features of the Lagoon Lakes… 465

Table 4. Some physicochemical characters in Lake Küçükçekmece

(İstanbul) (from Topçuoğlu et al. [11] and Demirci et al. [13])

Parameters / Literatures Topçuoğlu et al. (1999) Demirci et al. (2006).

Salinity (‰) 5.96 (April) -10.20 (October) -
Temperature(°C) 6.6 - 25.8 -
Dissolved oxygen (mg/L) 6.30 (in July)-10.80 (in April) 5.5 - 21
pH 7.00 - 8.36 8.7
Secchi depth (m) 0.3 - 4.0 -
Nitrate (mg/L) 0.2 - 1.9 -
Nitrite(mg/L) 0.002 - 0.136 -
Ammonium (mg/L) 0.10 - 1.30 -
Phosphate (mg/L) 0.73 - 6.60 0.9 – 9.8
Conductivity (mS) - 11.4
COD (mg/L) - 4.4 - 732

2.1.4.1. Some Limnological Characters Of Lake Küçükçekmece

This lake was studied by Topçuoğlu et al. [11] and Demirci et al. [13] in pervious studies
to obtain the physicochemical features. According to Topçuoğlu et al [11] dissolved oxygen
ranged between 6.3-10.8 mg/L, pH ranged between 7-8.3, turbidity (light permeability)
ranged between 30-400 cm, nitrate ranged between 0.2-1.9 mg/L, nitrite ranged between
0.002-0.136 mg/L, phosphate ranged between 0.7-6.6 mg/L, ammonium ranged between 0.1-
1.3 mg/L. Some results were showed that in Table 4. According to Demirci et al [13], the
average pH value is 8.7 for the lake (this value is approximately the same as open sea pH,
which indicates the intrusion of saline sea water from the southern part into the lake converts
it to brackish one), the average high conductivity values (11.4 mS) (is further evidence of the
intrusion of sea water), dissolved oxygen (DO) values are between 5.5 and 21 mg/L,
phosphate concentrations range between 0.1-9.8 mg/L (are far exceeding and unpolluted
surface water), chemical Oxygen Demand (COD) values in the lake show a large value spread
(between 4.4 and 732 mg/l), the total coliform values are at average of 563 per 100 ml (too
high for either drinking water or recreational waters), turbidity is widespread across the lower
levels in the southwest portion and higher near some of the streams (Table 4).

2.1.5. Lake Büyükçekmece

This lagoon lake which is located at north of the Marmara Sea coast (41˚04' N, 28˚34' E)
of Turkey (Çatalca/İstanbul) is the third largest water resource among the six main reservoirs
of a metrapolitan Istanbul, providing 17% water demand [14] (Figure 6). It is 30-35
kilometers to the southwest of Istanbul city center. The lake is formed at the point, where the
river Karasudere flows into the Marmara Sea blocked by the sandbank it created. The lake
has an area of 28.47 km2, it is 7 km long and 2 km wide, and the deepest section is about 8.6
meters. The lake is fed by Karasu stream. After Büyükçekmece Lake is separated from
Marmara Sea by a dam and serve as a reservoir to the city.
466 Belgin Çamur-Elipek and Timur Kırgız

Figure 6. Büyükçekmece Lagoon Lake

Table 5. Some physicochemical characters in Lake

Büyükçekmece (Istanbul) (from Koşal-Şahin [15])

Parameters\Months Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb. Mar. Apr. May.
DO. (mg·L-1) 9.0 10.2 8.9 9.0 10.0 12.0 11.7 10.8 8.8 9.8 7.8 7.4
pH 7.4 7.8 7.6 8.3 7.7 8.2 6.4 7.4 7.4 7.3 7.0 6.8
Turbidity(cm) 132 160 102 80 110 90 120 130 90 70 60 62
EC (mho·cm-1) 446 481 533 503 527 514 472 509 430 467 547 547
T.H. (FS)0 12 12 12 12 12 12 13 18 14 13 13 12
Salinity (‰) 0.02 0.02 0.03 0.02 0.03 0.03 0.03 0.03 0.03 0.03 0.03 0.03
NO2-N (mg·L-1) 1.44 1.54 1.84 0.56 0 0 0 25.34 16.84 26.6 12.54 36.34
NO3-N (mg·L-1) 0.28 0.88 0.52 1.38 0 0.92 0 0 0.40 0 0 0
PO4-3(mg·L-1) 20.9 21.0 21.5 17.4 0.18 0 1.9 14.0 18.5 7.4 0.2 82.3
(DO: Dissolved oxygen; EC: conductivity; T.H.: Total hardness)

2.1.5.1. Some Limnological Characters Of Lake Büyükçekmece

This lake was studied by Koşal-Şahin [15] in pervious study to obtain the
physicochemical features. According to her obtained results, dissolved oxygen ranged
between 7.4-11.7mg/L, pH ranged between 6.4-8.3, turbidity (light permeability) ranged
between 60-132cm, conductivity ranged between 430-547 mho/cm, total hardness ranged
between 12-18 FS0, nitrate ranged between 0.0-1.3 mg/L, nitrite ranged between 0.00-36.3
mg/L, phosphate ranged between 0.00-82.3 mg/L, salinity is 0.03‰ at average. The results
were showed that in Table 5.

2.1.6. Tuzla (Erikli Salt) Lagoon

This lagoon is situated at 40˚37' N, 26˚28' E (Erikli, Enez/Edirne) (Figure 7). It has an
area of 2.2 km2, and 2.1 km length, 1.4 km width. Its maximum depth is about 500 cm. It is
correlated with the Aegean Sea by a narrow channel. Therefore it has very saline water.
 The Evaluation of Some Limnological Features of the Lagoon Lakes… 467

Figure 7. Tuzla Lagoon Lake (Erikli Salt Lagoon)

2.1.6.1. Some Limnological Characters Of Tuzla Lagoon

Up to now, there has been no study on physicochemical features of Erikli Tuzla lagoon.
In this chapter, the first records are provided. It was observed in the studies which were
performed in the years 2008 and 2009 in Tuzla lagoon, it the temperature is 18 0C, pH 7.9,
dissolved oxygen (DO) 2.1 mg/L, light permeability 30 cm, conductivity 280 mho/cm, NO3-
N 11.3 mg/L, salinity 12‰, solid suspended material 2.5 mg/L, calcium 330 mg/L, total
hardness 295 FS0, PO4-3 0.002 mg/L, sulphate 6.10 mg/L at average. It was also measured the
amounts of NO2-N, and Magnesium in the lake during the sampling, but it was not found.

2.1.7. Vakıf Salt Lagoon

This lagoon is situated at 40˚36' N, 26˚15' E (Vakıf, Enez/Edirne) (Figure 8). It has an
area of 1.5 km2, and length of 2.2 km, width of 1 km. Its maximum depth is 100 cm. It is fed
weakly by Balik stream. But, it has salty water.

Figure 8. Vakıf Salt Lagoon Lake

468 Belgin Çamur-Elipek and Timur Kırgız

2.1.7.1. Some Limnological Characters Of Vakıf Salt Lagoon

Up to now, there has been no study on physicochemical features of Vakıf Tuzla lagoon.
In this chapter, the first records are provided. It was observed in the studies which were
performed in the years 2008 and 2009 in Tuzla lagoon, it the temperature 17 0C, pH 7.8,
dissolved oxygen (DO) 2.2 mg/L, light permeability 30 cm, conductivity 270 mho/cm, NO3-
N 12.39 mg/L, salinity 11‰, solid suspended material 2.93 mg/L, calcium 344 mg/L, total
hardness 290 FS0, PO4 0.003 mg/L, sulphate 6.52 mg/L at average. It was also measured the
amount of NO2-N, and Magnesium in the lake during the sampling, but it was not found.

2.1.8. Işık (Bücürmene) Lagoon

This lagoon is situated at 40˚42' N, 26˚03' E (Enez/Edirne) at the South of Dalyan
Lagoon and it has 76 ha. area (about 1 km2) (Figure 9). Its length is 1 km., and width is 1 km.
Maximum depth is 2 meters. It is a coastal lagoon. It has haline water. There is marches on its
north and east portion.

2.1.8.1. Some Limnological Characters Of Işık Lagoon

Up to now, there has been no study on physicochemical features of Işık lagoon. In this
chapter, this is the first record that is provided. Some physicochemical features of the lagoon
were showed at Table 6.

2.1.9. Dalyan lagoon

This lagoon is situated at 40˚42' N, 26˚04' E (Enez/Edirne) (Figure 9). It is formed by
aluvyonal flows from Meriç River. It has an area of 3.7 km2, 5 km. length, and 1.7 km. width
with maximum 2 meters depth. It is a coastal lagoon and has hyperhaline water. The lake is
surrounded by sandy area. It has no macrovegetation on its banks except north-west portion.

2.1.9.1. Some Limnological Characters Of Dalyan Lagoon

Up to now, there has been no study on physicochemical features of Dalyan lagoon. In this
chapter, the first records are provided. Some physicochemical features of the lagoon were
showed at Table 6.

2.1.10. Taşaltı lagoon

This lagoon is situated at 40˚42' N, 26˚05' E (Enez/Edirne) in the South of Dalyan
Lagoon and it has an area of 70 ha. (about 1 km2) (Figure 9). Its length is 1.2 km., and width
is 0.6 km. Maximum depth is 80 cm. It is a coastal lagoon. It has water with medium salty. It
is surrounded by marches.

Table 6. Some observed features of the Işık, Dalyan, and

Taşaltı Lagoons at the years 2008 and 2009

Temp. pH EC. D.O. Ca Mg Sal. T.H. Turb PO4-3 NO2-N NO3-N SO4-2 SSM
0
C mg·L- mg·L- mg·L- ‰ (FS)0 cm mg·L- mg·L- mg·L- mg·L- mg·L-
Dalyan 14 8.3 150 3.4 320 0 7 228 10 0 0.0002 21.58 5.94 1.67
Işık 13 8.4 240 5.1 272 0 10 230 70 0 0 3.76 5.69 2.27
Taşaltı 11 7.9 230 2.8 496 0 10 284 10 0.05 0.22 4.54 3.52 2.24
(EC: conductivity; DO: Dissolved oxygen; Sal.: Salinity; T.H.: Total hardness; SSM: Solid suspended material)
 The Evaluation of Some Limnological Features of the Lagoon Lakes… 469

Figure 9. Işık, Dalyan, and Taşaltı Lagoons

2.1.5.1. Some Limnological Characters Of Taşaltı Lagoon

Up to now, there has been no study on physicochemical features of Taşaltı lagoon. In this
chapter, this is the first record that is provided. Some physicochemical features of the lagoon
were showed at Table 6.

2.1.11. Lake Gala

Lake Gala is 5.6 km2 area, its depth changes between 0.4-2.2 meters and sea level is 2
meters (Figure 10). It is formed as alluvial setted lagoon lake by the Meriç River. Therefore,
this lake has different forming type from the other lagoons which are located on the coasts of
Aegean Sea. During summer, the lake is separeted into two sections because of drying. The
bank of the Lake is accompained by macrovegetation consisting of Phragmites australis and
Typha sp. There are a lot of agricultural areas (essential rice plant) around the lake [16].

Figure 10. Location of Lake Gala

470 Belgin Çamur-Elipek and Timur Kırgız

Table 7. Some physicochemical characters in Lake Gala (Edirne)

(from Çamur-Elipek et al. [17])

Mar. Apr. May Jun. Jul. Aug Sep. Oct. Nov Dec Jan.
pH 8.2 8.4 8.7 8.2 8.3 8.2 8.3 8.4 8.6 8.5 8.4
EC. 145 143 187 163 270 250 310 320 209 250 150
Temp 14.8 17.8 19.3 26.7 27.6 25.6 23.6 19 8.3 9.1 6.2
Ch-a 21.9 15.8 20.0 17.8 16.2 4.8 26.5 20.2 58.3 65.5 18.9
DO 16.3 14.4 17.8 12.8 12.9 11.4 14.9 16.3 12.8 8.6 12.3
Depth 199 111 126 164 128 131 145 109 121 106 156
Turb. 48 48 56 47 76 91 28 51 29 24 38
Mg 67.8 41.4 52.7 69.9 78.8 78.0 98.6 88.4 85.7 87.8 80.5
Ca 96.1 86.0 81.6 52.9 57.7 54.3 52.1 105.8 78.1 69.7 67.5
TH 52 40 42 42 47 46 54 63 55 49 50
NO3N 7.20 4.04 1.80 4.40 1.19 1.88 3.32 0.00 0.01 0.00 0.00
NO2N 0.001 0.00 0.00 0.00 0.00 0.00 0.24 0.02 0.01 0.00 0.00
SO3-3 3.80 3.00 2.80 3.20 3.60 2.50 3.73 4.43 2.53 0.06 2.58
PO4-2 0.01 0.01 0.01 0.06 0.03 0.03 0.03 0.06 0.00 0.01 0.02
(EC: conductivity; DO: Dissolved oxygen; Turb.: turbidity; T.H.: Total hardness)

2.1.11.1. Some Limnological Characters Of Lake Gala

This lake was studied by Çamur-Elipek et al. [17] in pervious study to obtain the
physicochemical features. According to their obtained results, dissolved oxygen ranged
between 8.6-17.8 mg/L, pH ranged between 8.2-8.7, turbidity (light permeability) ranged
between 24-91cm, conductivity ranged between 143-320 mho/cm, magnesium ranged
between 41.4-98.6 mg/L, calcium ranged between 52.1-96.1 mg/L, total hardness ranged
between 40-63 FS0, nitrate ranged between 0.00-7.2 mg/L, nitrite ranged between 0.00-0.24
mg/L, sulphate ranged between 0.06-4.43 mg/L, phosphate ranged between 0.00-0.06 mg/L,
Chlorophyll-a ranged between 4.8-65.5 mg/L. The salinity is 0.02 %0 at average in this lake.
Some results have been showed that in Table 7.
Furthermore, it was reported that zoobenthic organisms were found 1627 individuals in
per m2 at average by Çamur-Elipek et al. [17].

2.3. Evaluation

As a result of some studies which were performed in the lakes in the previous studies,
some of them have showed haline and some of them have showed freshwater characteristics.
It is observed that Erikli and Mert Lagoons which are located on Black Sea coasts have
coastal lagoon features. Their salinity ranged between brackish to salty water (7.709‰ in
Erikli Lagoon, and 9.55‰ in Mert Lagoon). Their vegetation type, shallow, and some
physicochemical features showed that these lagoons have eutrophic-mesotrophic characters.
Kırgız & Güher [6] also supports our findings.
The Lake Terkos has freshwater because of the Istranca River flows. Its salinity is very
low, with an average of 0.02‰ [7]. Freshwater fish species predominate [8]. Although, the
lake was reported to have oligotrophic characters, in the latest study the lake has been
indicated as mesotrophic character [7].
 The Evaluation of Some Limnological Features of the Lagoon Lakes… 471

Küçükçekmece lagoon has ranged brackish to salty waters between 5.96‰ and 10.20‰
salinity. The lagoon has shown some sign of eutrophication, such as cyanobacterial blooms
and deterioration in water quality from late spring to mid-autumn [18]. At present, the lagoon
is used only for fishing and for recreational purposes [9]. Some fishing is possible, but
unfortunately it has been facing a dangerous pollution in the last 20 years because of the
dense human habitat and uncontrolled industrial development [13]. The low Dissolved
oxygen (DO) values would indicate areas where some fish species may be under stress. The
DO supersaturated surface water (unpolluted water DO is about 8.6 mg/L) is a clear
indication of level approaching eutrophication [13]. The Phosphates and Nitrates levels
reported are excessive and it assists algal growth in freshwater lakes [13]. Thus, the lake‘s
water does not even approach safe drinking water standards and can be regarded as a heavily
polluted lake in terms of many parameters like total coliform, turbidity, temperature,
phosphate, DO and COD significant amount of toxic chemicals in the stream [13].
Büyükçekmece is fed by Karasu Stream. Therefore, it has ranged freshwater to weak
salty water between 0.02‰ and 0.03‰ salinity [15]. The lake has showed eutrophic-
mesotrophic characters with the high dissolved oxygen, high nutrient levels, and low light
permeability. There is some fishing but lately the lake has been endangered by the pollution
caused by human settlement and industrial zones.
Tuzla and Vakıf Salt lagoons have showed haline character with 12‰ and 11‰ salinities,
respectively. The Lagoons Işık, Dalyan, and Taşaltı have also saline water with 10‰, 7‰,
and 10‰ salinity, respectively.
Lake Gala has freshwater. The forming type of this lake is different from the others
which are located on the Aegean Sea coasts in Turkish Thrace. It is estimated that this may
explane the differences for some features of the lake from the others. It was also reported
eutrophic characters with measured features [17].
Consequently, it was observed that almost all lagoons in Turkish Thrace are under
treatments of settlements, industrialization, agricultural and other human activities. Therefore,
overloaded nutrient flowing from these areas may affect these sensitive areas negatively.

3. CONCLUSION
Lagoons are very sensitive structures and they are affected by surrounding environments.
Any artificial influence to these sensitive areas and the activities belonging agricultural,
industrial, urban, and tourism surrounding of lagoons may cause to the destruction of the
natural balance of them. First of all, the human activities on lagoons have become a major
environmental concern. To avoid the deformation of the lagoons, we have to learn their
past‘s, today‘s and future‘s balance.

ACKNOWLEDGMENTS
We would like to thank B.Öterler, M.Taş, P.Özkahya, and P.Altınoluk (Trakya
University) for their help during some field studies.
472 Belgin Çamur-Elipek and Timur Kırgız

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Fakültesi, Yayın no 14, III. Baskı, 153 Sayfa, İzmir.
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[5] Seçmen, Ö. & Leblebici, E. (1997). Türkiye Sulak Alan Bitkileri ve Bitki Örtüsü. Ege
Üniversitesi Fen Fakültesi Yayınları No:158, 870s. Bornova/İzmir.
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Erikli Lakes (Kırklareli/İğneada). XII. National Biology Congress, 6-8 July 1994,
Edirne / Turkiye.
[7] Çamur-Elipek, (2003). The Dynamics of Benthic Macroinvertebrates in a Mesotrophic
Lake: Terkos, Turkey‖, Acta Biologica Iugoslavica - Serija D: Ekologija, 38(1-2), 31-
40 .
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öncelikleri sempozyumu, 18-19 Kasım.
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of brackish water lagoon, Küçükçekmece Lake, in northwestern Turkey', Toxicological
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 INDEX

air temperature, 128, 227, 439, 440, 441, 450, 451,

2 452, 453
algae, viii, x, xvi, 73, 76, 77, 79, 80, 84, 85, 86, 91,
20th century, 263, 334
97, 98, 104, 105, 106, 107, 108, 110, 111, 129,
21st century, 367, 432
134, 135, 136, 143, 144, 160, 185, 201, 206, 215,
A 237, 262, 263, 304, 305, 311, 319, 330, 334, 337,
341, 342, 344, 345, 348, 404, 435, 436, 437, 438,
abatement, 291, 293, 294, 297, 343 439, 442, 443, 444, 447, 449, 450, 454, 455, 473
abundance data, 232 Algeria, 180, 359, 363, 369
access, 198, 230, 304, 305, 367, 405, 425, 428, 430, algorithm, 88, 98, 110, 198, 200, 201, 205, 310
431 ALS, xv, 397, 398, 399, 403, 404, 405, 406, 407,
accounting, 173, 419, 421 408, 409, 410, 411, 412
accumulation areas, 100, 105, 106, 190, 192, 198, Alvarado Lagoon System (ALS XE "ALS" ), xv,
206, 207, 208, 306, 308, 309, 317, 320 397, 398
acetic acid, 284, 288, 289, 294, 374 ambient air, 128
acid, vii, xii, xiii, 2, 3, 11, 33, 229, 256, 275, 279, ambient air temperature, 128
280, 281, 284, 285, 288, 289, 290, 294, 297, 348, amine, 19
374 amines, 19
acidic, 281, 291, 297 amino, 8, 11, 282
acidity, 258, 343 amino acid, 8, 11
ACTH, 14, 15, 27 amino acids, 8, 11
ADA, 191 amino groups, 8
adaptation, 28, 109, 111, 366, 423, 431, 433, 450 ammonia, 129, 131, 134, 143
adaptations, 25 ammonium, 258, 263, 267, 358, 452, 465
additives, xii, 279, 280 amplitude, 49, 113, 123, 342
adjustment, 210, 325 anoxia, 41, 143, 258, 275, 357
adrenocorticotropic hormone, 14 antibody, 10
adults, 335, 383, 404, 410, 425 antigen, 10, 16, 17
adverse effects, xi, 140, 219 antioxidant, 30
Africa, xi, 43, 46, 47, 64, 146, 176, 180, 219, 226, apoptosis, 13
242, 245, 261, 262, 263, 271, 272, 276, 359, 360, aquaculture, xi, xiv, xvii, 57, 58, 223, 249, 250, 260,
369 261, 262, 269, 276, 333, 338, 340, 341, 349, 431,
age, 4, 18, 22, 24, 25, 35, 125, 376, 395, 396, 410, 436, 451
421, 429 aquarium, 410
agencies, 365, 410, 427 aquatic environment, vii, 1, 2, 3, 13, 15, 20, 21, 24,
aggregation, 17, 110, 162, 187, 195, 237 33, 37, 41, 115, 267
agriculture, 58, 157, 255, 256, 260, 263, 340, 343, aquatic habitats, 156, 266
344, 352, 362, 363, 418 aquatic life, 400
476 Index

aquatic systems, x, xiii, 90, 103, 114, 116, 144, 185, biodegradation, 298
198, 201, 215, 221, 237, 301, 304, 314, 330, 336, biodiversity, xii, xiv, xv, 42, 114, 115, 144, 154, 157,
352, 356 160, 166, 169, 175, 177, 178, 182, 220, 221, 249,
Argentina, 245, 395 250, 258, 260, 265, 274, 333, 334, 345, 365, 368,
aromatic compounds, 32, 282, 283 370, 397, 404, 412, 421
aromatic hydrocarbons, 7, 23, 67, 281 biogeography, 67, 413
aromatic rings, 284, 292, 294 bioindicators, ix, 31, 46, 64, 107, 153, 154, 155, 176,
aromatics, 291 179, 187, 189, 214, 304, 305, 316
Asia, 71, 176, 177, 242, 260, 384, 432 biological activity, 128, 400
Asian countries, 418 biological control, 217, 331
aspartate, 8, 34 biological processes, 123, 130, 272
assessment, viii, xvi, 2, 4, 18, 20, 24, 26, 28, 30, 36, biomarkers, 3, 5, 13, 14, 17, 20, 24, 25, 26, 29, 30,
37, 39, 65, 67, 116, 120, 136, 144, 146, 147, 156, 31, 33, 34, 36, 37
157, 169, 170, 173, 175, 182, 220, 223, 224, 228, biomasses, viii, 73, 76, 82, 83, 85, 93, 99, 100, 101,
247, 251, 255, 256, 261, 265, 267, 269, 271, 274, 102, 103, 104, 105, 106, 107, 108, 109, 252, 258,
275, 276, 330, 398, 410, 417, 425, 428 327, 357, 367
assessment techniques, 175 biomonitoring, 18, 33
assessment tools, 157 bioremediation, 69
assets, xvi, 176, 417, 420, 422, 425, 430 biosphere, 252
assimilation, 275, 331, 360 Biosphere Reserves, 370
atmosphere, 40, 134, 201, 250 biotic, viii, x, xiv, 2, 18, 40, 41, 58, 77, 100, 115,
atmospheric deposition, 201, 262, 343 141, 154, 160, 170, 178, 180, 181, 215, 240, 352,
atmospheric pressure, 405 361, 364, 365
atoms, 200, 291, 314 biotic factor, 178, 240
authorities, xiv, 285, 351, 352, 353, 363, 364, 365, birds, ix, xvi, 97, 153, 154, 155, 156, 157, 160, 161,
409, 410, 412 162, 166, 167, 169, 170, 171, 172, 173, 178, 179,
awareness, xvi, 362, 408, 410, 417, 426, 428, 430 180, 181, 182, 183, 222, 239, 240, 265, 358, 359,
360, 362, 368, 398, 409
B blood, vii, 2, 3, 4, 9, 10, 11, 12, 14, 16, 18, 22, 31, 35
blood circulation, 9, 14
background information, 370
blood flow, 4
bacteria, 77, 131, 133, 134, 201, 258, 273, 338, 340,
blood monocytes, 16
343, 344, 346
blood supply, 10
bacterial infection, 21
blood vessels, 4, 9, 10
bacterium, 338
Boat, 426
Baltic states, 324
body size, 246
banking, 428
body weight, 4, 10, 21, 23
banks, 48, 49, 51, 55, 144, 254, 287, 362, 373, 411,
bones, 409, 411
412, 428, 468
boreal forest, 415
barriers, 15, 16, 255, 335, 367
Brazil, 33, 34, 43, 47, 49, 51, 64, 65, 67, 70, 151,
base, vii, xii, xiv, 2, 3, 11, 30, 33, 65, 112, 173, 190,
178, 242, 274, 276, 368, 370
191, 192, 193, 194, 199, 200, 204, 206, 207, 254,
breakdown, 3, 6, 173, 357
266, 280, 281, 305, 306, 307, 308, 309, 310, 314,
breeding, 4, 18, 144, 173, 181, 239, 338, 341, 358,
318, 321, 352, 360, 365, 366, 370, 371, 383, 432
361, 405, 411, 423
benefits, xi, 186, 187, 214, 219, 220, 223, 253, 360,
brevis, 402
363, 366, 418, 421
Britain, 35, 175, 243
benthic invertebrates, 179, 239
Brittany, 66
benzene, 282, 283
buffalo, 361, 362
bias, 42, 450
bulk materials, 450
bile, 3, 5, 6, 32
butyl ether, 282
bile duct, 5
buyers, 429
bioaccumulation, 3, 37, 403, 413
by-products, 291, 297, 298
bioassay, 31
bioavailability, 2, 291
 Index 477

changing environment, 56, 472

C chemical characteristics, 41, 243, 254
Chemical oxidation, xii, 279, 280, 294, 297
Ca2+, 12, 13
chemical properties, xii, 252, 280, 285, 296
Cabinet, 268
chemicals, 4, 8, 12, 13, 15, 18, 19, 23, 41, 267, 289,
cadmium, 8, 13, 14, 19, 27, 28, 30, 33, 34, 36, 37,
471
130, 141, 294
Chicago, 245
calcium, 12, 32, 111, 115, 461, 462, 463, 467, 468,
children, 367, 410, 420, 425, 426, 429
470
Chile, 392
calibration, xii, 113, 198, 205, 250, 251, 376, 395
Chilika Lagoon, xvi, 417, 418, 420, 421, 423, 424,
Cameroon, 243
425, 426, 428, 429, 430
campaigns, 158, 256, 408, 410, 412
chlorination, 291, 299
canals, 258
chlorine, 22, 291
candidates, viii, 39
chlorobenzene, 282, 283
capsule, 4, 9
chloroform, 13, 282, 283
carbohydrate, 24
chromatograms, 291
carbohydrate metabolism, 24
chromatography, 299
carbon, xv, xvii, 13, 28, 42, 51, 130, 131, 132, 133,
chromium, 13, 37, 283
134, 136, 137, 143, 148, 229, 246, 253, 262, 280,
CIA, 267
282, 283, 286, 287, 290, 294, 346, 397, 400, 401,
circulation, vii, viii, 9, 14, 39, 40, 43, 46, 49, 51, 55,
403, 411, 435, 436, 451, 453
56, 68, 147, 162, 392
carbon dioxide, 280
cirrhosis, 5
carbon tetrachloride, 13, 28, 42, 282, 283
cities, 57, 334
carcinogen, 36
City, xiii, 52, 67, 263, 280, 287
Caribbean, 262, 269, 412, 413, 414
clarity, x, 85, 97, 98, 107, 110, 113, 185, 187, 237,
case studies, 285
303, 311, 319
case study, xvi, 64, 66, 68, 102, 146, 149, 157, 277,
classes, 24, 162, 250, 287, 321, 341, 404, 418
330, 417, 419, 420, 430, 433
classification, xii, 69, 146, 147, 162, 245, 250, 251,
catabolism, 8, 18
265, 266, 286, 291, 297, 331, 341, 404
catastrophes, 392
clay minerals, 384, 391
catchment, ix, 120, 122, 123, 124, 125, 126, 129,
cleaning, 60
130, 131, 140, 141, 146, 148, 149, 150, 177, 190,
cleanup, 280
198, 227, 276, 305, 308, 358, 363
climate, viii, 41, 73, 74, 182, 223, 253, 263, 264,
catchments, ix, xi, 119, 120, 125, 126, 130, 140, 141,
271, 273, 329, 330, 344, 348, 349, 354, 365, 387,
143, 144, 147, 149, 222, 227, 249, 261, 268, 271,
396, 419, 423, 424, 425, 426, 427, 429, 430, 431,
304, 415, 421
433
catecholamines, 11
climate change, viii, 73, 74, 273, 329, 330, 349, 365,
catfish, 6, 19, 23, 27, 28, 33, 34, 403
396, 419, 429, 431, 433
cation, 373
climates, 395
cattle, xvi, 361, 362, 364, 398, 403, 406, 410
climatic conditions, 41, 237
causal relationship, 4
closure, 128, 129, 136, 137, 138, 423
CCA, 170
clustering, 376
cell biology, 26
CO2, 257, 346
cell death, 5, 13
coal, 287
cell division, 19
coastal ecosystems, xi, 74, 108, 160, 217, 249, 260,
cell membranes, 13
262, 266, 267, 331, 334, 335
cellulose, 58, 216
coastal management, viii, 73, 146, 186, 187, 216
Census, 158, 167, 176, 177
coastal region, 41, 109
Central Europe, 36
coastal zone management, 348, 349
CGL, 174
CoastWeb, viii, 73, 74, 76, 77, 78, 82, 84, 85, 87, 88,
CH3COOH, 288, 289
90, 93, 96, 99, 100, 102, 109, 110, 111
Chaetoceros, xvii, 435, 442
coefficient of variation, 202, 314, 451
chain transfer, 14
collaboration, 361, 364, 410, 427
challenges, 432
478 Index

Colombia, 63, 263 contaminated soil, 284, 300

colonization, 69, 224, 225, 240, 241, 243, 247 contaminated soils, 284
combined effect, 55, 142, 166, 349 contaminated water, 14, 34
commercial, xiv, 138, 141, 142, 245, 265, 280, 285, contamination, ix, xii, 2, 3, 6, 7, 9, 17, 19, 21, 23, 35,
288, 289, 333, 341, 404 53, 66, 73, 74, 75, 99, 104, 105, 116, 141, 142,
communication, 171, 253, 376 146, 147, 275, 280, 296, 343, 409
compaction, 224 Continental, 69, 245, 273, 350
comparative analysis, 145, 166, 459 control group, 19
compatibility, 275 control measures, 258
compensatory effect, viii, 73, 100 controversial, 20
competition, 136, 145, 340, 404, 425 copper, 8, 13, 14, 19, 26, 32, 33, 34, 130, 141
competitors, 183 coral reefs, 262, 270
compilation, 79, 90, 173, 193, 198, 207, 317, 319, correlation, xv, 52, 59, 168, 189, 321, 385, 397, 400,
321, 323 403, 411
complement, 227, 361, 366, 421 correlations, 35, 237, 406, 411
complex interactions, 250 corticosteroids, 27
complexity, 9, 15, 41, 46, 62, 74, 116, 201, 250, 349, corticotropin, 14, 29
365 cortisol, 14, 15, 31, 32
composition, ix, xi, xii, 26, 33, 60, 120, 122, 127, cost, 25, 173, 214, 329, 366
128, 136, 137, 138, 141, 142, 143, 144, 147, 149, covering, 83, 109, 159, 167, 201, 390
155, 157, 159, 161, 174, 200, 217, 219, 222, 224, crabs, 120, 376, 382
240, 244, 254, 270, 274, 275, 280, 286, 314, 331, creosote, 37
359, 372, 383, 395, 439, 444, 445, 449, 451, 452 crises, 41, 251, 265, 271, 347, 394, 396
compounds, vii, xii, 1, 2, 3, 5, 6, 7, 15, 32, 33, 41, Croatia, 43, 71
58, 237, 261, 263, 279, 280, 282, 283, 291, 294, crop, 217, 331
298, 346, 348 cross-validation, 376
comprehension, 61 crude oil, 18, 19, 20
conceptualization, 420 crystals, 436
concordance, 156, 170, 180 cultivation, xvi, 398, 406
conductivity, 158, 229, 459, 461, 462, 463, 464, 465, cultural heritage, 253
466, 467, 468, 470 cultural tradition, 406
conference, 269 cultural values, xvi, 365, 417
configuration, xii, 280, 289 culture, 33, 260, 272, 409, 411, 432
confinement, 47, 49, 53, 54, 55, 56, 57, 58, 65, 66, cumulative percentage, 232
69, 157, 162, 178, 348 cycles, 23, 41, 43, 46, 49, 56, 125, 251, 263, 264,
conflict, 176, 362, 363, 426 276, 331, 338, 348
connective tissue, 4, 9 cycling, 7, 132, 133, 143, 147, 148, 149, 215, 253,
consciousness, 265 270, 344, 345, 347, 356
consensus, 27, 131, 426, 429 cyclones, 372, 423, 430
construction, xiv, 223, 226, 227, 228, 230, 351, 353, cysteine, 8, 13
359, 363 cytochrome, 6, 7, 30, 31, 32, 36, 37
consumers, 170, 264, 356
consumption, 78, 79, 80, 82, 91, 93, 94, 95, 107, D
113, 186, 199, 261, 282, 284, 290, 341, 345, 356,
damages, iv, 253, 281, 424, 429
370, 403, 404, 406, 411
data mining, 329
consumption rates, 107
data set, 229
contact time, 291
database, 41, 302
contaminant, 2, 3, 13, 15, 18, 20, 21, 24, 26, 102,
decomposition, 128, 130, 143, 199, 257, 281, 356,
142, 294, 297
357, 368, 370
contaminants, viii, 3, 4, 18, 20, 21, 23, 24, 25, 28,
decoupling, 241
29, 30, 33, 34, 41, 73, 102, 130, 141, 142, 145,
deduction, 428
167, 186, 216, 279, 282, 330, 335, 338
defecation, 45
contaminated sites, 19, 21
defence, 15, 16, 17, 21, 24, 36
 Index 479

deficiency, 58, 109 diseases, 18, 21, 28, 261, 265, 425
deficit, 51 dispersion, 45, 65, 171, 172
deforestation, 130, 141, 143, 151, 399, 403, 404, disposition, 383, 384, 387
406, 423 dissociation, 348
deformation, 471 dissolved oxygen, 59, 128, 136, 137, 226, 228, 267,
degenerate, 18 273, 346, 358, 459, 461, 462, 463, 465, 466, 467,
degradation, viii, 16, 20, 40, 140, 142, 169, 173, 224, 468, 470, 471
260, 280, 281, 283, 284, 297, 338, 342, 344, 345, diversification, 58, 61
348, 369, 405, 411, 449, 450 diversity, vii, ix, xv, 2, 12, 27, 30, 45, 46, 54, 58, 59,
degradation process, 169, 345 60, 61, 120, 122, 141, 156, 161, 162, 163, 164,
Delta, 61, 149, 176, 178, 180, 182, 261, 274 166, 169, 170, 171, 172, 240, 255, 349, 358, 361,
demography, 167 365, 398, 418
denitrification, 131, 134, 144, 201, 358 DNA, 28
denitrifying, 134, 148 dominance, 43, 46, 48, 52, 59, 96, 97, 146, 162, 240,
Denmark, 36, 77, 111, 244, 276, 324, 330, 337 251, 256, 383
deposition, 12, 19, 116, 130, 149, 201, 221, 224, Doñana National Park, vi, xiv, 371, 372, 373, 385,
230, 262, 283, 343, 359, 372, 387, 389, 391 387, 388, 389, 390, 394
deposits, 71, 221, 222, 245, 361, 383, 387, 388, 389, dosage, 282, 294
392, 393, 394, 395, 396 drainage, 126, 141, 157, 227, 255, 256, 275, 357,
depression, 37, 54, 221 363, 364, 398, 463
desiccation, 260 drinking water, 360, 463, 465, 471
desorption, xii, 134, 280, 281 drought, 41, 360, 398
destruction, xvi, xvii, 10, 17, 18, 41, 362, 398, 405, drying, 42, 354, 364, 469
409, 411, 457, 471 dumping, 41, 223, 225, 245, 363
detectable, 18 durability, 228
detection, 35, 57, 62, 142, 166, 247, 277 dwarfism, 58
detoxification, vii, 1, 3, 4, 8, 17, 23, 25, 31
developed countries, 174 E
developing countries, 223, 418, 431
early warning, viii, 2, 3, 24, 25, 58, 65, 173
development policy, 432
ecological indicators, 62, 176, 182, 341
deviation, xvii, 101, 103, 104, 106, 172, 192, 195,
ecological requirements, 42
196, 197, 199, 202, 208, 232, 291, 315, 316, 321,
ecological restoration, 244, 300
325, 326, 401, 435, 443
ecological roles, 224
diatom assemblages, 271
ecological systems, 156, 271
diatoms, 136, 256, 267, 341, 382, 436, 442, 450,
ecology, x, 62, 67, 69, 78, 82, 109, 114, 115, 116,
451, 452, 453, 454
117, 143, 144, 149, 154, 170, 171, 173, 178, 220,
dichloroethane, 283
228, 241, 256, 270, 271, 272, 331, 340, 366, 370,
diet, 6, 19, 65, 113, 168, 341, 404, 407, 409
394, 405, 419, 458, 472
differential equations, viii, 73, 74
economic damage, 253
diffraction, 373
economic damages, 253
diffusion, viii, x, xiii, 73, 112, 113, 185, 186, 187,
economic development, vii, xiv, 1, 2, 174, 252, 261,
192, 193, 194, 198, 208, 237, 268, 301, 304, 308,
352, 432
309, 315, 318, 328, 346
economic progress, 431
digestion, 3, 18, 65, 95, 289, 290
economic status, xvi, 418
dignity, 424, 428
economic systems, 420
dioxin, 19, 30, 37
economic values, 222, 253, 265, 276
directives, xii, 249, 251, 266
economics, xii, 279
disaster, xvi, 417, 426, 430
ecosystems, vii, viii, ix, xi, xiii, 1, 2, 20, 39, 40, 57,
discharges, 11, 51, 58, 123, 131, 141, 166, 178, 187,
58, 74, 108, 117, 119, 120, 140, 143, 156, 160,
194, 196, 201, 211, 246, 254, 272, 302, 305, 308,
169, 173, 174, 182, 220, 249, 250, 251, 252, 253,
309, 327, 459, 464
256, 257, 260, 262, 264, 265, 266, 267, 269, 331,
discriminant analysis, 376
333, 334, 335, 338, 348, 403, 411, 419, 421, 449,
discrimination, 18, 25, 229, 376, 425, 426, 429
458
480 Index

editors, 29, 215, 246, 247, 413, 414 environmental stress, viii, 4, 14, 17, 20, 21, 23, 37,
education, 144, 408, 409, 410, 421, 425, 426 40, 41, 43, 59, 64, 257
educational experience, 425 environmental stresses, 41
EEA, 337 environmental sustainability, 261
effluent, 19, 20, 21, 22, 26, 31, 223, 269 environmental variables, 142, 159, 160, 161, 170,
effluents, 22, 26, 36, 51, 58, 59, 262, 264, 268 174, 267
Egypt, 43, 62, 68, 69, 261, 274, 394 enzyme, 6, 7, 23, 30
elaboration, 427 enzymes, 6, 7, 8, 12, 27, 28, 34, 116
electrolyte, vii, 2, 3, 11, 27 EPA, 155, 175, 182, 215, 223, 227, 280, 289, 290,
electron, xii, 14, 26, 32, 34, 36, 134, 279, 280, 281, 299, 300, 400, 403, 415
282, 283, 299, 346 epithelia, 13, 14
e-mail, 351 epithelial cells, 7, 12
emigration, 85, 86, 87, 88, 89, 90, 91, 92, 93, 95, 102 epithelium, 5
emission, 187, 210, 324 equilibrium, 222, 240, 250
employment, 362, 418 equipment, 226, 362, 373, 424, 426, 430
employment opportunities, 418 equity, 365
endangered species, 223, 361, 410 erosion, 78, 80, 100, 113, 126, 144, 190, 191, 192,
endocrine, 4, 11, 14, 35, 37 193, 198, 199, 200, 203, 207, 208, 220, 221, 222,
endocrine system, 35 227, 242, 256, 306, 307, 308, 309, 310, 319, 320,
endothelial cells, 7 360, 384, 389, 426
energy, xv, xvii, 6, 23, 24, 41, 53, 54, 96, 123, 126, erythrocytes, 10, 20, 24
165, 222, 244, 356, 372, 383, 384, 387, 389, 390, erythropoietin, 12, 32
391, 394, 397, 398, 436, 452 estrogen, 4
energy input, xv, 397, 398 estuarine environments, 56
energy transfer, xvii, 436 estuarine systems, ix, 153, 154, 182
enforcement, 365, 409, 411 ETA, 306
engineering, 227, 258, 300 ethanol, 42, 229
England, 62, 70, 150 ethics, 246
enlargement, 5, 6, 23 ethylene, 282, 283, 373
environmental awareness, 426, 428 ethylene glycol, 373
environmental change, 42, 62, 68, 155, 156, 223, EU, 109, 156, 157, 214, 266, 329, 337, 338, 341
261, 394 Europe, 36, 71, 176, 183, 263, 268, 280, 334, 335,
environmental characteristics, 145, 157, 163, 223 337, 367, 370, 373, 387, 391, 395, 459
environmental conditions, viii, 15, 39, 46, 57, 59, 64, European Commission, 251, 257, 261, 270
74, 156, 180, 217, 227, 241, 274, 282, 285, 440, European Community, 259, 263, 336
472 European Union, 156, 174, 337, 350
environmental contamination, 9, 17 eutrophic, 84, 120, 178, 250, 251, 254, 257, 260,
environmental degradation, 20, 260, 342 261, 262, 264, 266, 272, 273, 274, 276, 277, 339,
environmental effects, 223 357, 452, 458, 471
environmental factors, xi, xii, 20, 21, 115, 205, 219, evaporation, vii, viii, 39, 41, 43, 51, 53, 126, 128,
250, 251, 330, 340 193, 194, 195, 254, 260, 261, 263, 357
environmental impact, iv, vii, xi, 24, 150, 219, 220, evapotranspiration, 227
221, 224, 228, 247, 267 evidence, xi, 5, 21, 25, 26, 31, 41, 138, 142, 216,
environmental influences, 32 219, 220, 224, 234, 260, 272, 330, 349, 365, 380,
environmental management, xi, xiv, 115, 219, 269, 384, 390, 393, 395, 396, 407, 465
334, 342, 352, 368 evolution, xv, 125, 222, 241, 251, 273, 368, 372,
environmental protection, 266 373, 376, 385, 388, 390, 393, 394, 395, 396
Environmental Protection Agency, 116, 175, 182, excavations, 361
217, 223, 243, 299, 300, 331, 332 exchange rate, 226, 423
environmental quality, viii, xii, 3, 29, 40, 41, 59, exclusion, 418
250, 251, 338, 344 excretion, vii, 2, 3, 6, 12, 29, 30, 260
environmental regulations, 60 exercise, 10, 22, 29, 366
experimental condition, 288
 Index 481

experimental design, 25, 142 fishing, vii, ix, xiv, xvi, 1, 2, 73, 74, 90, 91, 98, 99,
expertise, 25 101, 102, 103, 166, 167, 169, 170, 171, 173, 263,
exploitation, xiv, xvi, 250, 256, 260, 333, 334, 335, 333, 360, 362, 403, 417, 418, 419, 420, 421, 423,
340, 349, 362, 365, 398, 403, 406 424, 425, 426, 428, 429, 430, 431, 432, 433, 471
explosives, 282 fixation, 201, 202, 217, 314, 324, 358
exports, 126, 127 flocculation, 107, 115, 130, 237
exposure, vii, viii, xvi, 1, 2, 3, 4, 5, 6, 7, 8, 12, 13, flooding, xiv, 143, 227, 333, 359, 363, 364, 403
14, 15, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, floods, 360, 423, 430
28, 29, 30, 31, 32, 34, 35, 36, 37, 46, 73, 75, 76, flora, vii, xiv, 1, 2, 143, 150, 156, 223, 226, 265,
96, 190, 191, 195, 196, 214, 240, 254, 417, 420 352, 353, 360, 363, 365
expulsion, 10, 436 flora and fauna, vii, xiv, 1, 2, 143, 150, 265, 352,
external influences, 160 353, 360, 363, 365
extinction, 104 flotation, 42
extraction, 244, 245, 290 fluctuant, 161
exudate, 20 fluctuations, vii, viii, xii, 18, 31, 39, 41, 136, 221,
222, 226, 249, 250, 256, 263, 264, 267, 270, 395,
F 396, 419, 436
fluid, 222, 273
facies, xiv, xv, 121, 371, 372, 373, 375, 377, 378,
food chain, 258, 338
380, 382, 384, 385, 386, 387, 391, 392
food habits, 109
facilitators, 247
food production, 253
FAI, 59, 60
food safety, 338
families, xiv, 136, 337, 352, 354, 404, 421, 425
food web, ix, 114, 117, 134, 153, 154, 155, 162, 170,
family members, 430
172, 173, 179, 180, 181, 182, 260, 264, 271, 277,
farmers, 339, 363
348, 349, 357, 360, 455
farmland, 180
force, 14, 140, 266, 409
farms, 163, 186, 217, 261, 332, 338
Ford, 365, 368
fascia, 64
formaldehyde, 228, 229
fat, 5, 6, 409, 411
formation, 6, 10, 123, 144, 186, 221, 295, 441, 458
fauna, vii, xi, xiv, 1, 2, 46, 59, 60, 70, 131, 141, 143,
formula, 116, 168, 196
145, 147, 148, 150, 177, 219, 223, 224, 225, 228,
fouling, 338, 340, 357
229, 233, 240, 241, 245, 265, 272, 352, 353, 360,
fragments, 48, 51, 377, 378, 382
363, 365, 383, 394
France, xiii, 39, 47, 53, 57, 60, 64, 66, 67, 71, 177,
feces, 260, 405
242, 245, 264, 265, 271, 272, 280, 333, 334, 335,
fertilization, 264
337, 338, 339, 342, 350, 351, 359, 361, 369, 370,
fertilizers, 58, 256
391
fiber, 439
free radicals, 281
fibers, 58
freezing, 437
fidelity, 181, 228, 413
freshwater species, 9, 22, 110, 360, 377
filtration, xiii, 12, 280, 294, 295, 296, 298
frost, 41
financial, 109, 174, 214, 329, 420, 422, 427, 429,
fungi, 77
430
fusion, 6
financial capital, 429
financial support, 109, 174, 214, 329 G
fine suspended particles, 190
Finland, vi, xiii, 77, 99, 212, 213, 225, 301, 302, gasification, 287
303, 304, 305, 306, 307, 308, 309, 310, 311, 312, general knowledge, xii, 249, 251
314, 315, 316, 317, 318, 319, 320, 321, 322, 323, genes, 8
324, 325, 326, 327, 329, 331, 332 genus, 43, 229
fish liver, 3, 4, 5, 7, 8, 23, 27, 31 geography, 243
fisheries, x, xi, xvi, 114, 116, 140, 149, 154, 171, geological history, 222
176, 220, 222, 243, 244, 245, 249, 250, 261, 335, geology, 129, 255, 344
341, 369, 417, 418, 419, 420, 423, 424, 425, 426, geometry, 124, 453
427, 428, 429, 430, 431, 432, 458 Georgia, 66, 272
482 Index

Germany, 71, 280, 324, 368 health, viii, 3, 4, 13, 15, 20, 21, 23, 24, 30, 31, 33,
gill, 29, 34 40, 41, 57, 126, 141, 146, 154, 173, 176, 179,
gland, 14 180, 261, 265, 272, 285, 338, 340, 347, 349, 364,
global climate change, 273 425, 426
global scale, 254 health care, 425
glucose, 11, 33 health condition, 13, 426
glycerol, 229 health status, 41, 340
glycogen, 3, 4, 5, 6, 23 heavy metals, 8, 13, 14, 15, 19, 31, 35, 36, 66, 71,
glycoproteins, 16 141, 149, 173, 277, 283, 338
gonads, 9, 24, 340, 404 height, 128, 306, 373, 439, 441
goods and services, 174, 223, 352, 418 hematocrit, 22
governance, 329, 427 hemoglobin, 22
government policy, xvi, 398, 412 Hepatic lipidosis, 6, 34
governments, 251 hepatic necrosis, 32
grain size, 46, 59, 136, 137, 377, 378, 383, 384 hepatic portal system, 10
granules, 19 hepatocytes, 4, 5, 6, 7, 26, 27, 35, 36
graph, 164 hepatotoxicity, 5, 6, 8
grass, 96, 226 hepatotoxins, 7
grasses, xv, 143, 397, 398, 407, 409 herbicide, 13, 27
grasslands, 395 heredity, 418
gravity, 201, 328 heterogeneity, 41, 142, 145, 149, 162, 166, 276
grazing, 94, 181, 275, 357, 362, 364, 449 heterotrophy, 2725
Great Britain, 35, 243 highlands, 180
Greece, 52, 63, 65, 69, 70, 179, 265 Himmerfjärden Bay, v, x, 185, 187, 188, 190, 191,
green alga, 263, 473 192, 194, 196, 198, 200, 204, 206, 209, 213, 214
groundwater, 48, 178, 263, 272, 273, 300, 360 Histopathology, 4, 19, 26, 34
grouping, 141 history, 3, 36, 67, 116, 117, 138, 167, 222, 243, 245,
growth, 12, 16, 17, 18, 26, 31, 35, 58, 63, 115, 129, 256, 335, 350, 392, 405, 406, 411, 424
131, 135, 143, 144, 189, 206, 216, 250, 256, 257, Holocene, vi, xv, 63, 69, 71, 221, 371, 372, 376, 385,
260, 262, 263, 274, 275, 339, 344, 345, 346, 348, 388, 390, 391, 392, 393, 394, 395, 396
389, 419, 423, 424, 426, 450, 451, 452, 455, 471 homeostasis, 3, 11, 15
growth hormone, 17, 31, 35 homes, 409
growth rate, 135, 339, 344, 345, 348 Hong Kong, 391
GSA, 396 horizontal salinity distribution, 41
guidance, 300, 432 hormone, 3, 14, 15, 31, 35
guidelines, 130, 144, 365 hormones, 11, 12, 14
Guinea, 145, 242 host, 33
Gulf Coast, 394 hot springs, 361
Gulf of Finland, vi, xiii, 212, 213, 301, 302, 303, household income, 425
304, 305, 306, 307, 308, 309, 310, 312, 314, 315, human activity, 163, 223
316, 318, 320, 321, 322, 323, 325, 326, 327, 329, human capital, 425
331 human development, 253
Gulf of Mexico, xv, 150, 262, 338, 397, 398, 399, human health, 15, 173, 261, 265, 285, 338
400, 401, 411, 413 human perception, 265
hunting, xv, 361, 362, 398, 405, 406, 409, 411
H hurricanes, 254, 262, 372
husbandry, 411, 412
habitat quality, 173
hyaline, 46, 48, 50
harbors, 223, 280, 285
hydrocarbons, xiii, 6, 13, 58, 59, 60, 67, 141, 280,
hardness, 459, 461, 462, 463, 464, 466, 467, 468,
282, 283, 285
470
hydrodynamic turnover XE "turnover" time, 43
harmony, xvi, 417, 418
hydrogen, xii, 131, 143, 144, 279, 281, 282, 284,
harvesting, 258, 338, 339
285, 288, 289, 290, 294, 459
hazards, 285, 420, 424, 425, 429, 430
 Index 483

hydrogen peroxide, xii, 279, 281, 282, 284, 285, 288, individuals, vii, 1, 2, 42, 136, 141, 168, 173, 242,
289, 290, 294 340, 365, 382, 383, 403, 404, 411, 412, 461, 462,
hydrological conditions, 181, 274 463, 470
hydrolysis, xii, 280, 281 Indonesia, 260, 272, 395
hydroxide, 271 inducer, 7
hydroxyl, 281, 282, 283, 284, 291 induction, 6, 7, 30
hydroxyl groups, 283 industrialization, 423, 471
hyperplasia, 4, 5, 14, 19 industrialized countries, 280
Hypertrophism, 251 industries, xvi, 57, 186, 216, 223, 285, 304, 344,
hypertrophy, 4, 5, 6, 14 398, 406, 425, 432
hypotension, 27 industry, 263, 284, 334, 363, 430, 432
hypothalamus, 14 inertia, 366
hypothesis, 6, 125, 223 infection, 3, 15, 16, 18, 21, 32
hypoxia, 22, 32, 129, 147, 243 inferences, 156
infestations, 21
I infilling, xv, 123, 143, 228, 372, 390, 391
inflammation, 16, 26
ICAM, 64
infrastructure, xvi, 126, 143, 363, 404, 417, 424,
ice algal community, 436, 437, 442, 445, 446, 449,
426, 430
450, 451, 454
inland aquatic ecosystems, 155
Iceland, 337
innate immunity, 15, 26
ideal, viii, 3, 39, 62, 170
insecticide, 8, 35
identification, 266, 373, 410, 437, 439
insecurity, 428
identity, 431
institutional change, 419
image, 19, 20
institutions, 158, 285, 365, 428
image analysis, 19, 20
integration, 155, 243, 274
imbalances, 18
integrity, x, 13, 20, 28, 35, 141, 154, 156, 157, 167,
imitation, 136, 149, 215, 216, 217, 262, 263, 330,
175, 176, 177, 180, 181, 354
331, 452
interest groups, 364
immigration, 85, 86, 87, 88, 89, 90, 93, 102
interface, ix, xiii, 119, 120, 126, 333, 344
immune function, 32
interference, 14, 15
immune response, 10, 15, 16, 17, 21
Intermittently Closed and Open Lake Lagoons
immune system, 3, 15, 21, 28, 35, 36, 38
(ICOLLs), 120
immunity, vii, 2, 3, 10, 11, 15, 16, 26, 36
internal environment, x, 154, 157, 419
immunocompetent cells, 19
internal processes, 74, 198, 304, 309, 349
immunoglobulin, 27, 32, 35
intervention, 274, 403
immunoglobulins, 10
intestine, 14
immunosuppression, 18
intoxication, 5
impact assessment, 267, 271, 352
intrinsic value, 222
Impact Assessment, 223
invertebrates, 2, 116, 134, 136, 148, 156, 162, 179,
improvements, 29, 60, 213, 430
224, 226, 239, 246, 350, 357, 369
in transition, 29, 266, 267, 277
investment, 21
in vitro, 11, 14, 27
investments, 186, 324, 344
in vivo, 19, 26, 27, 33
ion transport, 13
incidence, 18, 21, 60, 179
ions, xii, 11, 12, 14, 34, 279, 281, 283
income, xvi, 344, 360, 417, 423, 425, 426
Iowa, 29
incompatibility, 334
IPR, 80, 90, 95
independence, 363
Iran, 265
India, vi, xvi, 27, 35, 69, 260, 272, 391, 395, 417,
iron, xii, 17, 18, 131, 134, 255, 271, 279, 281, 282,
418, 419, 428, 431, 432, 433
283, 290, 291, 297, 298, 299, 347
indigenous peoples, 403
irradiation, 283
indirect effect, 136, 429
irrigation, 163, 363
484 Index

islands, ix, xi, 119, 121, 122, 159, 164, 172, 219, lens, 128, 229
222, 230, 239, 240, 255, 421 lesions, 4, 13, 20, 25, 27
isolation, 68, 123, 393 leucocyte, 21
isotope, x, 154, 170, 171, 179, 182 levees, 373, 384
Israel, 62, 71 liberation, 8
issues, vii, viii, xiii, 1, 2, 11, 12, 19, 34, 40, 43, 109, life cycle, 27, 37, 87, 267, 271, 338, 340, 359
157, 172, 174, 216, 304, 333, 348, 423, 430 light, 26, 34, 88, 111, 129, 136, 149, 155, 194, 200,
Italy, xiii, 39, 53, 57, 62, 64, 66, 69, 70, 249, 253, 202, 205, 225, 241, 257, 271, 287, 291, 293, 297,
255, 264, 265, 268, 269, 273, 275, 276, 279, 280, 311, 316, 347, 359, 423, 439, 450, 452, 459, 461,
285, 393 462, 463, 465, 466, 467, 468, 470, 471
Ivory Coast, 49 light conditions, 202, 205, 311, 316
light scattering, 194
J light transmittance, 225
lignin, 58
Japan, vi, xvi, 32, 59, 70, 71, 260, 272, 334, 417,
limestone, 344, 361, 390
435, 443, 451, 453, 454
lipid metabolism, 3
Java, 272, 395
lipid peroxidation, 6, 26
jurisdiction, 266, 335
Lipid peroxidation, 6
juveniles, 19, 31, 33, 45, 335, 340, 341
lipids, 3, 6, 340
K liquid phase, 288, 289, 294, 295
literacy, 421, 425
K+, 12, 13, 14, 33, 374 literacy rates, 425
kidney, vii, 1, 3, 9, 10, 11, 12, 13, 14, 17, 22, 24, 28, Lithuania, 266
30, 31, 32, 33, 34, 35, 36 liver, vii, 1, 3, 4, 5, 6, 7, 8, 9, 17, 18, 19, 21, 23, 24,
kidneys, 13, 18 26, 27, 28, 29, 30, 31, 32, 34, 35, 36, 37
kill, 225, 409 liver cells, 4
kinetic model, 37 liver damage, 8
kinetics, 140, 291 liver disease, 26
livestock, 364
L loans, 428
local authorities, 285, 410
laboratory studies, xii, 7, 279 local community, xiv, 351, 352, 410
laboratory tests, 285 local conditions, 56
Lake Mälaren, 188 localization, 32, 254, 259
lamination, 377, 380, 382 Louisiana, 19, 31, 225, 243, 246, 269
landings, xvi, 417, 423, 426, 432 lying, 260, 335, 363, 420
landscape, ix, xiii, 119, 120, 125, 142, 144, 155, 162, lymph, 9, 17
163, 164, 166, 169, 170, 171, 175, 180, 181, 223, lymph node, 9, 17
333, 354, 363, 403 lymphocytes, 9, 10, 17, 20, 22, 31
landscapes, 155, 415 lymphoid, 9, 10, 11, 19, 22, 32, 33, 34, 35
languages, 335 lymphoid organs, 9, 19, 32, 34, 35
larvae, 21, 93, 114, 137, 170, 264, 339 lymphoid tissue, 9, 10
larval stages, 27
Late Pleistocene, vi, xv, 371, 372, 385, 388, 390, 392 M
Latin America, 266
laws, 409, 411 macroalgae, 97, 98, 99, 117, 149, 150, 160, 180, 251,
leaching, 131 257, 274, 343, 345, 346, 348
lead, 3, 4, 12, 13, 19, 21, 22, 34, 35, 41, 53, 56, 58, macrobenthos, 240, 243, 245, 247
97, 130, 140, 141, 143, 154, 156, 240, 255, 257, macronutrients, 130
403, 412, 424, 430 macrophages, 10, 13, 15, 16, 17, 18, 19, 20, 26, 31,
leakage, 224, 256 35
learning, 366 magnesium, 461, 462, 463, 470
legislation, xiv, 352, 354 magnitude, 90, 126, 291, 294, 346, 366
lending, 424, 428 major issues, xiii, 333
 Index 485

majority, ix, 119, 121, 127, 297, 337, 409, 411, 418 mesoderm, 10
mammal, 361 Metabolic, v, 1, 78, 79, 80
mammals, 4, 5, 6, 7, 8, 16, 97, 361 metabolic pathways, viii, 2, 25
man, 57, 97, 148, 164, 361, 365, 420 metabolism, 3, 5, 6, 8, 17, 23, 24, 28, 30, 36, 116,
mangroves, 67, 135, 260 148, 251, 272, 274
manipulation, 240, 247 metabolites, 6, 12
mapping, 56, 165 metabolized, 7, 58
marches, 468 metabolizing, 27
marginalisation, 354, 366 metal ion, 283
marine benthos, 245, 246 metal ions, 283
marine diatom, 452 metals, x, xiii, 4, 6, 8, 13, 14, 15, 19, 22, 23, 29, 31,
marine environment, 7, 12, 42, 59, 61, 62, 64, 69, 70, 35, 36, 66, 68, 71, 130, 141, 149, 173, 185, 187,
126, 134, 147, 150, 216, 217, 246, 330, 458 277, 280, 283, 294, 301, 303, 338
marine environments, 7, 12, 42, 62, 64, 126, 134, meter, xi, 96, 206, 219, 230
458 methodology, 66, 266, 269, 341
marine fish, 36, 45, 114, 222 methylene chloride, 282, 283
marine species, 383 Mexico, xv, xvi, 150, 175, 176, 245, 246, 247, 262,
marketing, xvi, 417, 421, 424, 426, 428, 430 275, 338, 397, 398, 399, 400, 401, 403, 404, 405,
marrow, 9 409, 410, 411, 412, 413, 414, 415
marsh, xiv, 41, 64, 66, 67, 69, 70, 117, 177, 360, Mg2+, 12, 373
362, 363, 364, 369, 371, 378, 380, 385, 387, 389, Miami, 376
392, 398, 407, 409 microorganism, 16
Maryland, 30 microorganisms, 16, 49
mass XE "mass" -balance model, viii, x, xiii, 73, 74, microscope, 32, 34, 42, 376, 452, 453
75, 76, 78, 100, 109, 185, 186, 193, 198, 214, microscopy, 439
216, 301, 303, 304, 308, 309, 315, 330 Middle East, 176
materials, xvii, 114, 165, 190, 199, 200, 220, 228, migrants, 361
230, 239, 250, 280, 306, 307, 310, 361, 410, 425, migration, viii, 73, 76, 82, 86, 87, 88, 89, 93, 95, 98,
429, 435, 450, 451 102, 107, 109, 245, 255
matrix, 281, 282, 283, 291, 294, 297, 383 mineralization, 193, 226, 254, 298, 346
Mauritania, 392 Ministry of Education, 174, 298
measurement, 173, 201, 454 mission, 364, 367
measurements, 76, 195, 228, 237, 289, 308, 321, missions, x, 185, 186, 189, 211, 212, 213, 413
327, 341, 413, 437, 439 mitochondria, 5, 13
meat, 406, 409, 411, 412 mitogen, 34
median, 19, 83, 111, 112, 192, 195, 196, 199, 204, mixing, viii, x, 41, 51, 58, 73, 150, 185, 186, 192,
208, 313, 315, 321 193, 194, 195, 198, 203, 207, 226, 255, 288, 289,
medical, 425 304, 307, 308, 309, 315, 319
Mediterranean, v, x, xiii, xiv, 33, 34, 45, 46, 47, 53, modelling, 74, 75, 77, 78, 79, 80, 82, 100, 108, 115,
61, 69, 71, 75, 153, 154, 155, 156, 157, 160, 164, 116, 144, 145, 158, 215, 268, 269, 271, 273, 276,
166, 169, 174, 175, 176, 177, 180, 181, 183, 239, 330, 331, 343, 365, 459
254, 256, 261, 263, 264, 265, 269, 270, 271, 273, models, 5, 74, 76, 93, 109, 116, 117, 171, 181, 201,
274, 276, 333, 334, 335, 337, 338, 342, 344, 348, 205, 215, 217, 252, 266, 267, 269, 274, 276, 303,
351, 352, 354, 359, 368, 369, 370, 394, 396 304, 327, 329, 332, 343, 393
Mediterranean climate, 344, 348 moderators, 98, 109, 111, 199, 202, 311
Mediterranean countries, 352 modifications, 21, 46, 58, 76, 110, 256, 267
melanin, 17 moisture, 286, 287, 296, 298
melting, 450, 454 moisture content, 287
membranes, 13, 241 molecular biology, 36
memory, 370 molecular oxygen, 281
mercury, xv, 8, 13, 19, 31, 34, 37, 258, 272, 397, molecular weight, 285
400, 401, 402, 403, 411, 414, 415 molecules, 3, 15, 16, 17, 283, 284
Mercury, 13, 35, 399, 400, 401, 402, 413, 415 morbidity, 173
486 Index

Morocco, 261, 394 nickel, 13, 283

morphological abnormalities, 69 Nigeria, 55
morphological variability, 123 Nile, 32, 61, 261, 274
morphology, viii, ix, 2, 3, 4, 22, 25, 35, 58, 66, 120, nitrates, 264, 267
122, 123, 125, 126, 140, 254, 373, 452, 454 nitrification, 134
morphometric, 20, 21, 28, 75, 190 nitrifying bacteria, 133
mortality, 19, 60, 129, 173, 180, 224, 225, 245, 275, nitrite, 258, 461, 462, 465, 466, 470
346, 410 nitrogen, 29, 51, 109, 117, 129, 130, 131, 134, 147,
mosaic, 181, 354 148, 149, 150, 162, 179, 187, 188, 189, 201, 203,
mosquitoes, 352 204, 206, 211, 212, 215, 216, 261, 262, 263, 264,
motivation, 225 267, 268, 269, 270, 271, 276, 303, 313, 314, 324,
MSW, 111, 193, 194 330, 331, 332, 343, 344, 350, 358, 359, 453
mucosa, 9 nitrogen compounds, 263
mucus, 15, 201 nitrogen fixation, 201
multiple factors, 41 nitrogen gas, 131, 134
multiple regression, 170, 171, 203 N-N, 358
multiple regression analyses, 170 nodes, 9, 17
multiple regression analysis, 203 North Africa, 176, 261, 271, 275, 359, 360
multivariate analysis, 376 North America, 409, 410, 413
multivariate statistics, 229 Norway, 28, 62, 280, 337
NPS, 285
N nutrient concentrations, x, 82, 111, 129, 131, 134,
135, 136, 143, 186, 187, 211, 214, 257, 264, 274,
Na+, 12, 13, 14, 33
277, 304, 307, 314, 458
NaCl, 438, 439
nutrient enrichment, 181, 257
Namibia, 176
nutrient transfer, 356, 357
NAS, 403, 414
nutrients, ix, x, xii, xiii, 6, 41, 52, 68, 74, 78, 111,
native species, 143, 223
119, 120, 126, 129, 130, 140, 141, 143, 155, 159,
NATO, 455
162, 181, 185, 186, 198, 212, 214, 217, 220, 226,
natural compound, 283
228, 237, 246, 249, 250, 251, 254, 256, 260, 261,
natural disaster, 429
262, 263, 264, 267, 270, 272, 274, 301, 302, 327,
natural disasters, 429
332, 335, 344, 356, 359, 360, 436, 454, 458, 459
natural disturbance, 136, 141
nutrition, 36, 46
natural hazards, 429
nutritional imbalance, 18
natural resources, 260, 366
nutritional status, 4, 25
Navicula, xvii, 435, 442, 443, 454
necrosis, 5, 13, 18, 20, 32 O
Necrosis, 5
negative consequences, 365 obstacles, 425
negative effects, 420 oceans, 122, 215, 330, 349
negative relation, 170 ODS, 162
neglect, 354, 366 officials, 419
nephropathy, 29 OH, 281, 283, 298, 299, 300
net migration, 255 oil, xvi, 18, 19, 20, 32, 58, 60, 66, 68, 69, 398, 406,
Netherlands, 37, 175, 176, 177, 179, 180, 182, 183, 429
243, 247, 280, 334 oil spill, 32, 60, 68, 69
neurotransmitters, 17 olefins, 282
neutral, 282 oocyte, 340
neutrophils, 16, 22, 26 openness, 166, 334
New South Wales, 62, 120, 123, 145, 147, 148, 149, operations, xi, xiii, 219, 226, 228, 231, 237, 241,
150, 151, 262 242, 280
New Zealand, 59, 67, 144, 148 opportunities, 418
NGOs, 421, 432 ordinary differential equations, viii, 73, 74
Nicaragua, 405, 413 ores, xiv, 371
 Index 487

organ, vii, 1, 3, 4, 9, 10, 11, 12, 16, 21, 24, 25, 28 peripheral blood, 22
organelles, 5 peritoneal cavity, 26
organic chemicals, 13 permeability, 14, 436, 459, 461, 462, 463, 465, 466,
organic compounds, xii, 7, 33, 41, 58, 279, 283, 294, 467, 468, 470, 471
298 permission, iv, 347
organism, vii, 1, 6, 20, 38, 79, 223, 264 permit, xv, 372, 373
organs, vii, viii, 1, 2, 3, 9, 11, 12, 16, 17, 19, 20, 25, peroxidation, 6, 18, 26
32, 34, 35, 37, 346 peroxide, xii, 280, 281, 282, 284, 285, 288, 289, 290,
osmolality, 12 294
osmotic pressure, 439 personal communication, 376
osmotic stress, 261 Perth, 148
outreach, 410 pesticide, 14, 20, 32, 41, 179, 256
overgrazing, 423 petroleum, xiii, 22, 32, 280, 282, 283, 285, 299
overlap, 57, 61, 157, 172, 430 Petroleum, 299
ox, 6, 74, 100, 107, 133, 134, 136, 201, 237, 404 pH, xii, xv, 29, 41, 46, 57, 128, 131, 135, 136, 148,
oxidation, xii, 255, 258, 279, 280, 281, 283, 284, 228, 237, 256, 257, 267, 276, 279, 280, 281, 282,
285, 288, 291, 292, 293, 294, 296, 297, 298, 344, 283, 284, 286, 287, 288, 289, 290, 291, 294, 295,
377 299, 348, 397, 399, 401, 459, 461, 462, 463, 464,
oxidative reaction, 281 465, 466, 467, 468, 470
oxidative stress, 28 phagocyte, 16, 36
oxygen, 13, 41, 43, 46, 54, 58, 59, 99, 101, 108, 112, phagocytosis, 15, 16, 17
113, 128, 133, 134, 136, 137, 144, 186, 187, 199, phenol, 31
201, 203, 204, 206, 209, 210, 226, 228, 237, 240, Philadelphia, 28, 298, 368
267, 269, 273, 281, 328, 344, 345, 346, 356, 358, phosphate, 12, 134, 166, 228, 229, 237, 271, 347,
459, 461, 462, 463, 464, 465, 466, 467, 468, 470, 461, 462, 465, 466, 470, 471
471 phosphates, 347
oxygen consumption, 186, 199 phosphorous, 254, 261, 263, 264, 267, 276, 358
oyster, 222, 260, 272, 338, 339, 341, 348, 349 photosynthesis, 129, 452
oysters, xvii, 260, 269, 339, 341, 344, 348, 436, 449, phylum, 41
451 physical characteristics, 123
ozone, xii, 279, 281, 282 physical environment, 224, 252, 424
physical features, 125, 126
P physical properties, 246, 396
physical structure, 163, 164, 223, 449
Pacific, 68, 338, 432
physicochemical characteristics, 43, 398
paints, 340
physico-chemical parameters, 241
paleontology, 390
physicochemical properties, 170
parallel, xi, 49, 219, 221, 254, 335, 377, 380, 382
Physiological, 29, 36
parasite, 21
physiology, 6, 12, 17, 22
parasites, 21, 265
pituitary gland, 14
parasitic infection, 18
plankton, viii, 73, 87, 88, 114, 122, 192, 200, 224,
parenchyma, 3, 4, 5, 9, 10, 11, 16
257, 271, 304, 314, 449, 452, 454
partial differential equations, 74
plants, 135, 223, 224, 256, 258, 262, 337, 343, 344,
participants, 367
357, 358, 359, 364, 407, 409, 423
pathogens, 17, 21, 338
plasma levels, 8
pathology, 26
platform, 289
pathways, viii, 2, 25, 160, 352
playing, vii, 1, 2
PCBs, 6, 7, 14, 22, 23, 31, 282, 283, 285, 286, 288,
PM, 78, 115, 187, 215, 228, 311, 326
290, 291, 297, 299
Poland, 324
peat, 222, 240, 361
polar, 453
peptides, 27
policy, xiv, xvi, 182, 270, 336, 341, 352, 360, 364,
percolation, ix, 119, 121
365, 398, 412, 430, 431, 432
perfusion, 4, 7
policy makers, 430
periodicity, 231, 232, 240
488 Index

policymakers, 252 producers, 76, 178, 250, 252, 256, 272, 342, 345,
political power, 426 356, 451
political problems, 261 productivity rates, 254
pollutants, vii, viii, x, xii, xiii, 1, 2, 3, 4, 5, 7, 13, 14, profit, 268
15, 17, 19, 24, 25, 126, 167, 185, 220, 225, 258, project, 109, 214, 223, 224, 227, 228, 229, 230, 231,
276, 279, 280, 281, 282, 283, 284, 285, 287, 288, 232, 239, 240, 247, 261, 266, 300, 329, 337, 344,
295, 298, 301, 338, 340, 359, 360, 365 427
polycarbonate, 439 prolactin, 14, 31
polychlorinated biphenyl, xiii, 6, 7, 179, 280, 282 proliferation, 5, 6, 149, 160, 180, 338, 344
polychlorinated biphenyls (PCBs), 6, 7, 282 proline, 116
polycyclic aromatic hydrocarbon, 7, 23, 281 protected areas, 157, 177, 380
polypeptide, 14 protection, xiv, 120, 144, 157, 222, 226, 251, 253,
polyunsaturated fat, 6 265, 266, 268, 331, 333, 365, 409, 433
ponds, 45, 51, 59, 65, 163, 169, 373, 377, 390, 395 protective mechanisms, 36
pools, 16 proteins, 8, 16
population, viii, ix, 2, 3, 7, 15, 20, 23, 24, 27, 37, 42, proximal tubules, 13, 27
66, 146, 153, 155, 156, 160, 173, 181, 188, 226, PTFE, 288
252, 256, 334, 337, 344, 354, 359, 361, 368, 383, public concern, 342
384, 406, 408, 410, 418, 419, 421, 424, 425, 426, public health, 3, 21
430 public support, 174
population densities, 334 publishing, 71
population density, 42, 226, 418 pulp, 10, 19, 22, 26, 58
population growth, 256, 419, 424 purification, 60, 193, 207, 341
population size, 173 pyrite, 347
population structure, 368, 383, 384
Portugal, 1, 29, 43, 64, 179, 182, 264, 269, 270, 271, Q
273, 274, 275, 337, 371, 392, 394, 395
quantification, 201, 266, 267, 277, 349, 368
positive correlation, 59, 237
quantitative estimation, 436
positive feedback, 345
quartz, 376, 377, 378, 380, 382, 383, 385
positive interactions, 365
Quartz, 379, 380, 384
positive relationship, 237
Queensland, 146, 149, 262, 268
potassium, 281, 283
quotas, 74, 115, 330
poverty, 261, 418, 420, 423, 430
poverty reduction, 420 R
power plants, 223
precipitation, xii, 81, 125, 130, 148, 190, 191, 193, radiation, 262, 348, 373
194, 195, 198, 280, 281, 305, 309, 348, 357, 358, radicals, 281, 282, 284
398, 400 rainfall, 41, 51, 124, 125, 126, 127, 129, 140, 142,
predation, 65, 76, 97, 98, 99, 100, 102, 103, 105, 227, 262, 275, 358, 364, 399, 400, 411, 423
113, 114, 115, 116, 136, 177, 215, 356 raw materials, 361
predators, ix, 80, 81, 82, 116, 117, 138, 144, 153, reactants, 281
154, 171, 173, 179, 183, 252, 404 reaction rate, 282, 283, 284
predictability, 241 reactions, xii, 3, 6, 16, 21, 26, 280, 281, 282, 284,
prediction models, 252 288, 297
predictor variables, 376 reactive oxygen, 13
preparation, iv, 172, 410 reactivity, 21, 282
preservation, 226, 253, 266, 365 reagents, xii, xiii, 279, 280, 281, 285, 288, 289, 294,
prevention, xvi, 417, 426, 430 297
primary data, 420 reality, xiv, 40, 107, 324, 351
Prince William Sound, 116 receptacle, xiv, 333, 335
principles, 87, 214, 432 reception, 361, 362
private banks, 428 recession, 220
probability, 372 recognition, xiv, 16, 71, 285, 352, 409, 420
 Index 489

recommendations, iv, 189, 366 rings, 284, 292, 294

reconciliation, 261 risk, 37, 167, 202, 264, 267, 295, 338, 343, 347, 350,
reconstruction, xiv, 304, 305, 322, 327, 371 363, 366, 400, 420, 427
recovery, xi, 20, 23, 24, 102, 104, 161, 219, 221, risk assessment, 37
225, 234, 240, 245, 257, 325, 408, 413, 414, 415 risks, 24, 202, 206, 213, 258, 430
recovery plan, 414 river basins, 146
recreation, 167, 223 river systems, 125
recreational, vii, 1, 2, 98, 465, 471 root, xvi, 344, 345, 361, 417, 425
recycling, 17, 18, 226, 260, 357, 453 root system, 344, 345
red blood cells, 9, 18, 22 roots, 96, 344, 346, 377, 378
regeneration, 146, 243 routes, 2, 223
regression, 11, 81, 83, 85, 110, 111, 112, 114, 160, routines, 180
170, 171, 195, 201, 203, 205, 206, 303, 304, 310, rowing, 340
314, 316, 318, 440, 441 Royal Society, 63, 145, 244
regression analysis, 203 RPR, 35
regression line, 111, 303, 318, 440, 441 rules, 429
regression model, 114, 171, 304 runoff, xvi, 48, 124, 125, 126, 128, 130, 140, 141,
regulations, xii, xiv, 60, 157, 251, 266, 279, 351, 145, 148, 227, 254, 262, 270, 343, 359, 398, 437,
354, 362 464
regulatory requirements, xii, 279 Russia, 266, 324
rehabilitation, xiv, 173, 351, 354
reintroduction, 411, 412 S
relevance, xi, 21, 249, 250, 253, 265, 276
safe haven, 97
remedial actions, 109, 214
safety, 338
remediation, xii, 23, 25, 265, 279, 284, 287, 294, 300
saline water, 40, 120, 204, 336, 357, 358, 363, 421,
renin, 12, 27
449, 466, 471
repair, 5, 423, 425
salinity levels, xvii, 358, 457
replication, 228
salmon, 5, 22, 26, 32, 35, 36
reproduction, 45, 58, 339, 341, 348, 350
salt concentration, 347
requirements, xii, 42, 221, 230, 266, 279, 284, 334,
salts, 283
354
saltwater, 110, 139, 201, 357, 400
RES, 79
samplings, 421
researchers, xii, xvii, 60, 249, 251, 256, 268, 349,
sanctions, 409
420, 421, 430, 457
sanctuaries, 120, 223
reserves, 360
saturation, 99, 101, 108, 113, 128, 203, 358, 374
residues, 41, 179
scaling, 452
resilience, 250, 420
school, 409, 425, 429, 430
resistance, xiii, 7, 21, 27, 30, 179, 250, 264, 273,
schooling, xvi, 417, 425, 426, 429, 430
277, 280, 298, 337, 365
science, ix, 29, 108, 116, 153, 154, 227, 243, 246,
resolution, 332, 388, 392
268, 270, 273, 274, 365, 366, 367, 368, 369
resource allocation, 426, 433
scientific knowledge, 261, 369, 406, 411
resource management, xiv, 221, 352, 366, 369, 433
scientific papers, 264
resources, vii, xiv, xvi, 2, 24, 134, 164, 166, 223,
scientific publications, 258, 335
224, 228, 245, 256, 258, 260, 261, 266, 268, 271,
scope, 216, 228, 319, 329, 331, 341
299, 300, 333, 334, 348, 349, 352, 354, 360, 362,
sea level, 67, 69, 220, 221, 222, 265, 348, 373, 387,
363, 365, 366, 404, 410, 417, 418, 419, 421, 423,
388, 391, 469
424, 425, 426, 427, 428, 430, 432
seafood, 403
restoration, 29, 144, 174, 181, 182, 220, 227, 230,
sea-level, xv, 67, 222, 261, 265, 372, 393, 395, 396
243, 244, 246, 262, 269, 300, 348, 352, 363, 364,
sea-level rise, 222, 261, 393
426
seasonal changes, 34, 270, 358
retention rate, 78, 86, 87
seasonal flu, 31, 136
reticulum, 5, 6, 18
seasonal growth, 346
rights, iv, 360, 424, 426
seasonality, 170
490 Index

secondary data, 420 social benefits, 363

secrete, 41 social capital, 422
secretion, 14, 15, 29, 32 social development, 363
security, 363, 428 social infrastructure, xvi, 417, 424, 426, 430
sedimentation, viii, x, xiii, 41, 73, 74, 84, 105, 106, social problems, 261
107, 110, 113, 129, 146, 185, 186, 187, 190, 192, social relations, xvi, 417
198, 199, 201, 203, 204, 205, 208, 222, 224, 225, social security, 363
242, 243, 301, 303, 304, 306, 308, 309, 314, 317, social structure, 418
320, 328, 359, 376, 377, 385, 391, 392, 393, 436, society, 222, 267, 421
437, 449, 452, 453, 454, 455 sodium, 281, 283, 288, 289
seeding, 454 soil erosion, 222, 256, 426
selectivity, 114, 294 soil particles, 360
semantics, 273 soil pollution, 268
semi-structured interviews, 421 soil type, 403
Senegalese sole, 9, 28 Solea senegalensis, 9, 28
senescence, 358 solid matrix, 281, 282, 283, 291
sensitivity, 13, 25, 56, 60, 74, 99, 102, 105, 107, 109, solid phase, 288, 289
168, 221, 245, 327, 328, 420 Solomon I, 367
septic tank, 143 solution, 227, 228, 229, 281, 283, 288, 289, 359,
serum, 8, 28, 34 428, 430, 438, 439
services, iv, xiv, 114, 174, 222, 223, 253, 270, 351, solvents, 282
352, 354, 360, 362, 365, 366, 368, 412, 418, 430 sorption, xii, 130, 280, 281
settlements, 157, 256, 265, 403, 463, 471 South Africa, 145, 149, 176
sewage, 20, 21, 31, 51, 58, 59, 129, 141, 143, 188, SPA, 157
189, 217, 264, 358 Spain, vi, x, xiv, 149, 153, 157, 175, 176, 177, 179,
sex, 23 180, 181, 214, 265, 268, 273, 274, 277, 329, 359,
sexuality, 340 371, 372, 373, 382, 391, 392, 393, 394, 395, 396
shade, 450 specialists, 168, 410
shape, 123, 126, 340 specialization, 159, 168
sheep, 361, 362 species richness, 52, 54, 60, 166, 225, 240, 263
shellfish, 45, 338, 341, 343 spectrophotometric method, 459
shelter, 97, 123, 159, 345 spectrophotometry, 290
shoreline, 123, 140, 160, 166, 167, 168, 169, 173, sperm, 11
220, 255, 263, 265 spleen, vii, 1, 3, 9, 10, 16, 17, 18, 19, 20, 21, 22, 24,
shores, 53, 54, 156, 174, 222, 223, 229, 352, 357, 29, 31, 32, 33, 36
368 Spring, 149, 180, 269, 412
shortage, 363 SSI, 21, 22, 23, 24
showing, 9, 10, 48, 50, 163, 314, 321, 340, 344, 399, stability, 147, 246, 277, 285, 365
425, 438, 441 stabilization, 161
shrimp, 45, 59, 65, 222, 402, 403, 432 stakeholders, xiv, xvi, 352, 354, 362, 365, 418, 426,
Siberia, 114 427, 429, 430
signals, ix, 153, 154 standard deviation, xvii, 105, 107, 172, 192, 195,
signs, 2, 20, 240 196, 197, 199, 202, 205, 208, 232, 291, 307, 315,
silica, 437, 439 316, 319, 323, 325, 326, 401, 435, 443
silver, 13, 27 starvation, 18, 26
simulation, 102, 105, 217, 277, 331 state, xii, 4, 16, 77, 102, 136, 166, 187, 210, 213,
simulations, 92, 98, 99, 100, 105, 202, 206, 209, 212, 217, 240, 250, 251, 263, 266, 267, 269, 270, 271,
213, 274, 313, 316, 323, 325 275, 276, 304, 325, 327, 328, 331, 345, 347, 348,
skin, 9, 15, 405 361, 398, 405, 411, 420, 421, 429, 431
sludge, 287, 299 states, 144, 173, 277, 324, 337, 341, 398, 421
smoothing, 84, 88, 111, 113, 157 Statistical Package for the Social Sciences, 376
snakes, 352, 360 statistics, 172, 229, 426, 432
SO42-, 346 steroids, 9
 Index 491

stimulant, 15
stomach, 15, 173 T
storage, 3, 4, 6, 10, 17, 18, 22, 23, 24, 32, 35, 229,
Taiwan, 260, 272, 273
356, 358, 360, 367
tanks, 143, 341, 411, 412
storms, 41, 372, 389
tannins, 129, 134, 135
stormwater, 130, 141
Tanzania, 151
stratification, 41, 48, 51, 53, 55, 56, 65, 128, 194,
taphonomy, 62
198, 203, 304, 307, 382, 384
target, vii, xii, 1, 3, 28, 187, 192, 206, 250, 253, 279,
stress, viii, 3, 4, 5, 14, 17, 18, 20, 21, 24, 25, 26, 27,
282, 284, 285, 298, 304, 310, 316, 327
28, 29, 30, 31, 33, 35, 37, 40, 41, 43, 54, 57, 59,
target variables, 187, 192, 206, 304, 316, 327
61, 62, 64, 65, 66, 96, 109, 112, 141, 151, 168,
taxa, ix, 41, 49, 136, 137, 138, 141, 153, 154, 156,
221, 257, 261, 270, 271, 471
177, 225, 229, 232, 234, 241, 365, 461, 462, 463
stress factors, 14, 37, 168
taxonomic descriptions, 439
stressors, ix, 4, 22, 23, 25, 153, 154, 250, 252, 271,
taxonomy, 43
400, 403
teams, 385
structuring, 277
techniques, 3, 13, 76, 162, 164, 172, 173, 175, 223,
style, 243
258, 267, 376, 409
subgroups, 384, 385
technologies, 275, 298, 299
subsistence, 352, 366, 403, 418
technology, 243, 284
substitutions, 282
tenure, 367
substrate, 59, 224, 240, 403
terraces, 389, 396
substrates, 59, 241, 255
territorial, 336
success rate, 340
testing, 156
succession, 150, 215, 242, 246, 275
tetrachlorodibenzo-p-dioxin, 30, 37
sulfate, xi, 12, 19, 220, 228, 229, 234, 237, 241, 275,
textbook, 115
346
textbooks, 187
sulfur, 148, 229, 346, 347
texture, 66, 390, 391
sulphur, 258, 272
TGF, 17
Superfund, 27, 285
Thailand, 393, 432
supplier, 11, 288, 289, 451
Thalassiosira, xvii, 435, 442, 444, 452
suppression, 6, 15, 21
thoughts, 419
surface area, xv, 47, 51, 53, 123, 124, 125, 130, 195,
threats, xvi, 92, 99, 109, 115, 117, 147, 227, 262,
255, 397, 398, 437, 441, 453, 463
398, 409, 412, 417, 430
surface layer, 42, 51, 128
tidal range_ XE "tidal range" _ formula, 196
surplus, 12, 162
tides, 49, 204, 222, 254, 345, 405
surrogates, 156
time frame, 305
surveillance, 63, 173
time lags, x, 153, 155
survival, xvi, 12, 97, 113, 223, 340, 361, 410, 417,
time series, ix, 42, 153, 154
418, 424
tin, 338
survival rate, 340
tissue, 3, 4, 8, 9, 10, 11, 12, 13, 14, 15, 17, 18, 20,
susceptibility, ix, 21, 120, 122, 140, 147, 225
23, 24, 26, 27, 33, 173, 402
suspensions, 373
tonic, 452, 454
sustainability, 228, 252, 261, 425, 428
tourism, xiv, xvi, 156, 157, 176, 222, 256, 262, 333,
sustainable development, 221, 253, 337, 365
334, 352, 398, 406, 458, 471
Sweden, 73, 99, 102, 116, 185, 211, 216, 217, 301,
toxic contamination, viii, 73, 74, 75, 99, 104
324, 330, 331
toxic effect, vii, 2, 3, 13, 15, 24, 258, 345
swelling, 6, 13
toxic gases, 257
Switzerland, 32, 367
toxic substances, 12, 102, 105, 187, 303
symptoms, 140, 167, 266
toxicity, 5, 6, 7, 8, 15, 19, 28, 30, 37, 225, 291, 295,
syndrome, 166
298
synthesis, 3, 6, 8, 9, 23, 24, 34, 116, 245, 270
toxicology, 12, 24, 28, 29, 30, 37
systemic change, 148
toxin, 5
trace elements, 41, 58, 59, 60, 61, 257
492 Index

tracks, 405 264, 265, 268, 270, 275, 277, 304, 333, 343, 344,
trade, 144, 424, 426, 428 351, 363, 398, 404, 406, 409, 458, 471
traditions, 361, 406 urban areas, 52, 142, 304
traits, 36 urban settlement, 157, 265
transaminases, 8, 24 urbanisation, 130, 140, 143, 148, 334, 344
transformation, 352, 358, 359, 393 urbanization, 157, 177, 262, 352, 403
transgression, xv, 221, 372, 376, 385, 389, 391, 392, urine, 11, 12
393 USA, xiii, 32, 35, 38, 66, 115, 116, 246, 247, 266,
transition metal, 283 275, 279, 280, 285, 287, 289, 298, 299, 300, 368,
transition metal ions, 283 370, 376, 393, 397, 413, 414
transitional coastal waters, 154 UV, 283
transport processes, x, xiii, 78, 185, 186, 189, 190, UV irradiation, 283
201, 206, 214, 215, 222, 245, 301, 316
transportation, 78, 190, 192, 198, 220, 306, 307, 308, V
309, 340, 449
validation, 376, 385
transportation XE "transportation" areas, 78, 190,
valuation, 23
192, 306, 308
variables, ix, x, 74, 76, 77, 80, 81, 82, 102, 109, 119,
treatment, xii, xiii, 20, 22, 187, 188, 189, 195, 211,
120, 137, 141, 142, 149, 151, 153, 155, 157, 158,
213, 253, 256, 262, 270, 280, 281, 282, 285, 287,
159, 160, 161, 170, 171, 174, 187, 192, 193, 204,
288, 289, 290, 291, 294, 295, 296, 298, 343, 344
206, 214, 234, 235, 236, 237, 238, 239, 241, 245,
triggers, 425
254, 256, 267, 304, 307, 314, 315, 316, 327, 348,
trophic classes, 321
376, 385
trophic level, viii, 39, 250, 254, 256, 260, 263, 264
variations, x, xi, 4, 9, 11, 18, 23, 24, 25, 33, 40, 64,
trophic state, xii, 77, 217, 250, 263, 267, 270, 276,
100, 128, 151, 181, 185, 202, 203, 214, 220, 238,
331
239, 241, 246, 262, 271, 274, 294, 312, 345, 372,
turbulence, 186, 198, 309
391, 392
turbulent mixing, 198, 309
vector, 213
Turkey, vi, xvii, 178, 268, 337, 457, 459, 463, 465,
vegetation, 69, 135, 143, 168, 179, 222, 256, 270,
472, 473
356, 357, 358, 362, 364, 377, 383, 403, 404, 411,
turnover, vii, viii, 39, 41, 43, 46, 79, 80, 84, 93, 94,
470
95, 107, 111, 113, 116, 192, 200, 205, 207, 208,
vein, 4
210, 216, 258, 304, 308, 309, 317, 318, 319, 320,
velocity, 110, 126, 195, 196, 198, 199, 306, 308, 309
327, 328, 356, 367
vertebrates, 4, 9, 10, 11, 15, 16, 17, 31
U vessels, 4, 9, 10, 19, 288, 407
Vietnam, 47
U.S. Army Corps of Engineers, 300 viruses, 338, 341
U.S. Geological Survey, 28 vision, 432
UK, 33, 35, 177, 179, 242, 245, 298, 299, 361, 368, vitamin E, 6
369, 392, 394, 395, 431, 432 volatilization, 282
ulcer, 32 vulnerability, xvi, 3, 114, 168, 417, 419, 420, 422,
ultrastructure, 8, 28, 35, 63 425, 430, 431
UN, 247, 365, 420
UNESCO, 64, 245, 246, 247, 253, 267, 272, 353, W
365, 370, 452
waiver, 428
uniform, 142
Wales, 62, 71, 120, 123, 145, 147, 148, 149, 150,
United, 69, 145, 150, 265, 276, 277, 299, 300, 405,
151, 262
413
warning systems, 24
United Kingdom, 145, 150
Washington, 29, 32, 69, 182, 276, 298, 300, 414, 472
United Nations, 276, 277
waste, xiv, xvi, 11, 223, 253, 256, 261, 263, 270,
United States, 69, 299, 300, 405, 413
299, 333, 344, 360, 398, 399, 412
updating, 364
waste management, 399, 412
urban, xiv, xvi, 52, 59, 61, 126, 130, 141, 142, 145,
waste treatment, 253
146, 147, 157, 166, 167, 179, 223, 261, 262, 263,
 Index 493

waste water, 256, 270, 344, 360 226, 241, 247, 253, 263, 265, 267, 268, 269, 271,
wastewater, 59, 157, 241, 269, 343, 344, 409 273, 276, 333, 336, 352, 356, 360, 361, 368, 370,
water ecosystems, 166 371, 373, 390, 393, 398, 406, 411, 412, 414
water policy, 270, 336 wild animals, 226
water quality, vii, ix, xi, 2, 15, 17, 41, 60, 100, 120, wilderness, 363
122, 125, 127, 131, 137, 139, 140, 141, 143, 144, wildlife, vii, 2, 32, 166, 173, 220, 334, 426
148, 150, 187, 219, 220, 221, 225, 226, 228, 229, wind speeds, 227
234, 235, 236, 237, 238, 239, 241, 249, 251, 257, woodland, 180, 461
261, 266, 267, 268, 269, 273, 274, 275, 335, 341, workers, 363
342, 344, 345, 347, 349, 400, 405, 411, 413, 415, working groups, 336
458, 471 worldview, 365
water resources, 261, 363 worldwide, viii, xi, 39, 45, 47, 156, 220, 249, 250,
waterbirds, ix, 153, 154, 155, 156, 160, 161, 162, 255, 258, 259, 265, 266, 268
163, 165, 166, 170, 171, 173, 176, 177, 178, 180,
181, 182, 240, 359 X
watershed, xiii, xvi, 145, 146, 157, 166, 173, 177,
X-ray diffraction, 373
269, 277, 333, 335, 342, 343, 344, 349, 418, 419,
X-ray diffraction (XRD), 373
426, 427, 428, 430
XRD, 373
waterways, 147, 280
wave base, 112, 190, 191, 192, 193, 199, 200, 204, Y
206, 207, 305, 306, 307, 308, 309, 310, 314, 318,
321 Y-axis, 450
weakness, 55, 175 yield, 81, 82, 127, 162, 166, 220, 222, 245, 263, 270,
wealth, viii, 2, 3 297
web, 114, 162, 170, 173, 177, 180, 181, 182, 250, yolk, 5
260, 264, 267, 269, 271, 277, 348, 349, 357, 360, young people, 430
410, 455
weight ratio, 4 Z
well-being, xvi, 340, 398, 412
West Africa, xi, 43, 46, 64, 180, 219, 226, 243, 245, zinc, 8, 14, 33, 34, 37, 130, 141
246, 261, 272, 274, 276, 369 zooplankton, viii, 73, 76, 77, 83, 85, 86, 87, 90, 91,
West Indies, 242, 244, 413 92, 93, 94, 95, 99, 100, 101, 102, 103, 104, 105,
Western Australia, 137, 147, 148 113, 114, 116, 162, 200, 254, 256, 262, 270, 272,
Western Europe, 337 274, 275, 304, 319, 450, 454, 459
wetlands, ix, xiii, xiv, xvi, 153, 154, 156, 157, 159,
169, 173, 174, 175, 176, 177, 178, 179, 181, 183,