Sie sind auf Seite 1von 13

Ecotoxicology (2011) 20:706–718

DOI 10.1007/s10646-011-0612-6

Recolonisation of translocated metal-contaminated sediments

by estuarine macrobenthic assemblages
Anthony A. Chariton • William A. Maher •

Anthony C. Roach

Accepted: 8 February 2011 / Published online: 18 February 2011

Ó Springer Science+Business Media, LLC 2011

Abstract A recolonisation experiment was performed findings showed that the source of the sediments influenced
using sediments from three locations (Nords Wharf, Cockle the composition of the recolonised assemblages, with the
Bay and Warners Bay) along a metal contamination gra- described approach being a powerful tool for examining
dient (Lake Macquarie, Australia). The study aimed to the effects of location-specific sediments under environ-
determine whether the source of the sediments would mentally relevant conditions.
influence the recolonisation of benthic assemblages, pro-
viding additional information regarding the ecological risks Keywords Benthic assemblages  Estuarine sediments 
associated with the more contaminated sediments. Sedi- Recolonisation  Trace metals  Translocation
ments were translocated to two locations within the lake
and retrieved after 22 weeks along with benthic samples
from the surrounding sediments (ambient). Total abun- Introduction
dance was greater in the reference treatment (Nords
Wharf), with this difference being driven by polychaetes, Elevated concentrations of trace metals within estuarine
especially capitellids. In general, univariate metrics were sediments have the potential to modify benthic assem-
similar among the recolonised treatments, although even- blages (Ward and Hutchings 1996; Josefson et al. 2008).
ness and diversity patterns were complex due to significant These changes are often reflected as a decline in diversity,
location-treatment interactions. PERMANOVA analysis richness and evenness due to the loss and reduction of
demonstrated that the Nords Wharf treatments were sig- sensitive taxa concurrent with an increase in the relative
nificantly different from the more contaminated treatments abundance of more resilient and resistant taxa (Warwick
(Cockle Bay and Warner’s Bay) and the ambient assem- 1993; Calabretta and Oviatt 2008). As benthic communities
blages, with no differences being detected among Cockle are continually modified by numerous abiotic and biotic
Bay and Warners Bay assemblages. Collectively, the processes, the correlative models that underpin many of
these studies (survey and gradient) do not permit a direct
link to causality (Luoma 1996). The influences of natural
A. A. Chariton (&)
variability, sampling error, and additional (often unidenti-
Land and Water, CSIRO, Locked Bag 2007, Kirrawee,
NSW 2232, Australia fied) contaminants can also confound the findings of survey
e-mail: studies, reducing our ability to confidently identify and
assess the ecological risks associated with a particular
W. A. Maher
location (Suter and Barnthouse 1993; Batley et al. 2002).
Ecochemistry Laboratory, Institute for Applied Ecology,
School of Health, Design and Science, University of Canberra, In order to clarify correlative studies and to increase our
Canberra 2601, Australia understanding of how contaminants affect benthic commu-
nities, there is a need to test models founded on causality
A. C. Roach
under environmentally relevant conditions. Manipulative
Ecotoxicology and Water Science Section, New South Wales
Department of Environment, Climate Change and Water, field experiments are increasingly being used to test
Lidcombe, NSW 1825, Australia the effects of contaminant(s) on benthic communities

Recolonisation of translocated metal-contaminated sediments 707

(e.g. Morrisey et al. 1996); evaluate bioavailability models In this paper, we employed an experiment to examine if
and biogeochemical assays (e.g. Warren et al. 1998); and recolonization by estuarine macrobenthos would differ in
shed light on location-specific relationships between sediments sourced from three locations along a metal
contaminants and benthos (e.g. Lindegarth and Under- contamination gradient. As the sediments were translocated
wood 2002). Three main approaches are used in location to experimental locations in areas with no known sources
or sediment-specific benthic community studies: (i) the of contaminants, it was hypothesised that assemblages that
translocation of benthic assemblages from reference to recolonised the treatments with greater metal concentra-
contaminated sediments (Lenihan et al. 1995); (ii) the tions would differ in their univariate and multivariate
artificial formulation of sediments which contain con- attributes from those that recolonised the reference treat-
centrations similar to those reported in the field (Linde- ment, as well as those naturally residing within the sedi-
garth and Underwood 2002); and (iii) the translocation of ments adjacent to the experiment. More specifically, it is
contaminated field sediments (Roach et al. 2000). The hypothesised that the more contaminated treatments
third approach, which was utilised in this study, examines (Cockle Bay and Warners Bay) would be less diverse and
differences among the benthic assemblages which recol- rich than the Nords Wharf treatment; with their faunal
onise translocated defaunated sediments, with variations assemblages being dominated by opportunistic taxa such as
in the univariate and multivariate attributes of the recol- deposit-feeding polychaetes (e.g. capitellids and spionids),
onised assemblages used to measure the effect of the reducing the evenness of the communities (Glasby and
treatment. In this study, the latter approach was deemed Underwood 1996; Ward and Hutchings 1996; Warwick
most suitable as it would enable us to examine sediments 2001; Chariton 2005). Whilst it is not inferred that the period
sourced from a specific gradient of interest, encompassing of colonisation would be long enough to create relatively
all of their inherit characteristics, including metal con- stable established assemblages, comparisons between the
centrations, grain size and organic content. recolonised and surrounding (ambient) assemblages were
Lake Macquarie is the largest coastal lagoon lake in performed to examine the level of convergence between the
eastern Australia encompassing a catchment of approxi- recolonised and established assemblages.
mately 622 km-2. The northern perimeter of the lake has
been extensively developed and includes the Pasminco
lead/zinc smelter in Cockle Bay. Many areas in the Materials and methods
southern part of the lake have above background trace
metal and metalloid concentrations in their biota and sed- Sediment collection, transplant locations and design
iments, however, these concentrations are considerably
lower than those reported in the north, with concentrations Ninety litres of sediment were collected from each of three
generally declining along a southern gradient (Batley 1987; locations (Cockle Bay, Warners Bay and Nords Wharf) along
Roach 2005; Chariton 2005). Correlative evidence derived a metal contamination gradient in Lake Macquarie, NSW,
from a gradient study indicated that benthic communities Australia (Fig. 1). Previous work has shown that the fine-
within Lake Macquarie are being modified by trace metals. fraction (\63 lm) of sediments collected from Cockle Bay
Locations with higher concentrations of lead, cadmium and Warners Bay were enriched with a similar mean con-
and zinc contained distinct assemblages which were less centration of cadmium (21–31 mg/kg), lead (250–370 mg/
diverse, rich and even (Chariton 2005). However, addi- kg) and zinc (620–710 mg/kg), however, differences in their
tional factors such as rainfall, habitat structure and larval macrobenthic assemblages were observed (Chariton 2005).
dispersal were potentially confounding or dictating the Sediments from Nords Wharf have been shown to contain
observed patterns along the contaminant gradient. Coupled substantially lower concentrations of cadmium (&2 mg/kg),
with this was the possibility that the observed changes in lead (&26 mg/kg) and zinc (&150 mg/kg) than those
the benthic communities were a response to historic trace from Cockle Bay and Warners Bay, with benthic assem-
metal concentrations, especially dissolved constituents, blages being distinct from those at the other two locations
which have since been significantly reduced, but have (Chariton 2005).
permanently modified the structure of the residing com- Acid-washed plastic spades were used to collect the top
munities. The experimental approach employed in this 10 cm of the sediment. This section is reflective of trace
study is designed to reduce the confounding influence of metal concentrations deposited over the last 15–20 years
sediment location and exposure history. The experiment is (Kilby and Batley 1993), and is a the primary area of
not viewed as a surrogate for gradient studies, but rather as benthic activity. For each location the collected sediments
an additional line of evidence which may be integrated into were placed in 3 9 30 l acid-washed polypropylene vats,
a weight-of-evidence approach for assessing the health of with the sediments evenly distributed between the three
contaminated estuarine sediments. containers. Upon returning to the laboratory, sediments

708 A. A. Chariton et al.

Pb/Zn Smelter water column. The lips of the containers were positioned
to sit approximately 2-cm above the sediment–water
Cockle Bay Bay interface (SWI), using a plastic template to ensure consis-
tency in positioning. Once the surrounding sediments had
settled, the positioning of the containers was checked,
and a diver carefully removed the lids.
After 22 weeks (October 2002), the containers were
covered and retrieved by divers. From each of the containers
an 8-cm deep core (6 cm diameter) was collected and sec-
Swansea tioned vertically. One half of the core was homogenised for
total particulate trace metal analysis with the remainder
sectioned in two (0–2 and 2–8 cm) for acid volatile sulfide/
Location 1 Ocean simultaneously extractable metals (AVS/SEM) analysis.
Each section was immediately wrapped in impermeable
Location 2 plastic wrap, placed in a snap-locked plastic bag with the air
Nords evacuated, stored on ice, and transferred to a freezer within
4 h. The remaining sediment was sieved through a 1 mm
mesh, with the retained benthic fauna fixed in 5% v/v
buffered formalin in seawater solution with a Rose Bengal
0 1 2 3 4 vital stain. Ten cores (10 cm diameter 9 8 cm depth) were
km additionally obtained from surrounding sediments at each
location for benthic identification and numeration (herein
Fig. 1 Map of Lake Macquarie, NSW illustrating the two locations
(1 and 2) used in the sediment translocation experiment, the original referred to as ambient samples). Samples were sorted under
sources of the sediments (Cockle Bay, Warners Bay and Nords a dissecting microscope and keyed to the following taxo-
Wharf) and the location of the lead/zinc smelter nomic groups: polychaetes (family), molluscs (family—
with the exception of the class Polyplacophora), crustaceans
(order), nemerteans (phyla), and sipunculans (phyla).
were defaunated by purging each vat with ultra-high purity
nitrogen gas (BOC Edwards) for a period of 2 h, then Chemical analysis and granulometry
capped with nitrogen and stored at 4°C. After 7 days, three
sub-samples were collected from each vat and examined Total particulate metals (\63 lm)
under a dissecting microscope to ensure that all fauna were
dead. Sub-samples were also obtained for particulate trace The fine fraction of the sediment was obtained by sieving
metal analysis, total organic carbon and grain size oven-dried (45°C for 72 h), homogenised sediments
measurements. through an acid-washed 63-lm nylon mesh. Prior to
Two locations within the South Basin were chosen for homogenisation, all visible vegetative matter and mollusc
the recolonisation experiment, herein referred to as Loca- shells were carefully removed. Concentrated Aristar nitric
tions 1 and 2, enabling the experiments to be conducted in acid (5 ml) (Sigma-Aldrich) was added to sub-samples of
areas with no known sources of contaminants. Experience the homogenised fine sediment (0.15 g), and digested using
from pilot studies also emphasised that minimizing a MDS 2000 microwave oven (CEM Microwave Tech-
potential human interference was an over-riding consider- nology) for 60 min at 100°C. The digested samples were
ation in location choice. Whilst the locations contained diluted with deionized water (Millipore, 18 MX; Milli-Q
relatively different substrates (Location 1, 53% fines; Academic Water System, Millipore Australia) to obtain a
Location 2, 71% fines), recruitment was expected to be final volume of 50 ml. After a 24-h settling period, a 10-ml
driven by water column sources and not the surrounding aliquot of the supernatant was transferred into polyethylene
adult fauna (Santos and Simon 1980; Diaz-Castaneda et al. ICPMS vials for analysis. Dissolved trace metal and met-
1993). alloid concentrations were determined by inductively
In May 2002, the defaunated sediments were transferred into coupled plasma mass spectrometry (ICP-MS) (Perkin-
polyethylene containers (12.2 cm 9 12.2 cm 9 10.0 cm), Elmer Elan 6000) using the method described by Maher
with a porewater collection device (PCD) placed in each et al. (2001). Ten percent of the samples digested and
container. At each location, SCUBA divers placed ten analysed consisted of certified reference materials
containers of each sediment treatment in a random (National Research Council Canada PACS-2 and MESS-1),
sequence into the substrata at 1 m intervals below a 2-m with measured values ±10% of certified values deemed

Recolonisation of translocated metal-contaminated sediments 709

acceptable (PACS-2 Cu = 90.4 ± 0.9% Standard Error Atmosphere, New Zealand (C. Hickey, NIWA, unpub-
(SE), Zn = 93.5 ± 1.1% SE, Cd = 91 ± 0.9% SE, Pb = lished). This approach is based on the collection of pore
91.1 ± 0.9% SE, Ni = 95.1 ± 1.0% SE; MESS-1 Cu = waters via diffusion into membrane-covered QiagenÒ
92.5 ± 0.6% SE, Zn = 92.7 ± 1.4% SE, Pb = 95.3 ± 96-well microplates, hereafter referred to as a porewater
1.4%). All results were corrected using blanks which con- collection device (PCD). PCDs were initially prepared by
stituted 10% of the samples. All implements were soaked for adhering clean 30 lm nylon mesh on to the front of acid-
72 h in a 2% v/v Aristar grade nitric acid solution, and rinsed washed microplates. Once dried, oxygen was removed from
four times with deionised water (Millipore, Milli-Q). the PCDs by placing the units in a nitrogen-filled anaerobic
chamber (Forma Scientific, 1029 aerobic system) for a
Acid volatile sulfides/simultaneously extractable metals minimum of 7 days. Twenty-four hours prior to being
(AVS/SEM) placed into the field, the PCDs were submerged in deoxy-
genated, deionised water and transferred into a vacuum
Three randomly selected samples from each treatment in chamber where the nitrogen was removed from the cells and
each location were analysed for AVS/SEM. For both AVS displaced with deoxygenated deionised water. The PCDs
and SEM analyses, an average was taken from two sub- were immediately wrapped in a non-permeable plastic wrap,
samples from each section (0–2 and 2–8 cm), with replicates and placed back into the anaerobic chamber. The devices
performed on every fifth sample. AVS was determined using were transported to the field in nitrogen filled, airtight con-
a rapid screening method (Simpson 2001). Briefly, tainer, where a PCD was inserted into each experimental
0.02–0.10 g (dry weight equivalent) of sediment was placed container immediately prior to being handled by the divers.
into a centrifuge tube with 50 ml of deoxygenated Milli-Q The PCDs were positioned into the sediment with the first
water and reacted with 5 ml of Methylene Blue reagent row immediately above the sediment–water interface,
(‘Clines reagent’). The sediment solutions were centrifuged enabling measurements to be obtained from this region.
(2 min; 2,500 rpm), allowed to develop for 90 min and then Upon retrieval, stratified dissolved oxygen and pH
measured colorimetrically and quantified at 670 nm using a measurements were immediately obtained from two col-
UV–VIS spectrophotometer (Jasco, UVIDEC-610). SEM umns of wells within each plate using a calibrated Hannah
was determined by inverting &0.4 g of wet homogenised HI9025 microcomputer multi-probe. For trace metal anal-
sediment in 20 ml of 1 M cold HCl for 20 s, with a 2.0 g ysis, the contents of the remaining 10 wells in each row
sub-sample collected concurrently for moisture content were collected by syringe, filtered (0.45 lm Minisart,
determination. Subsequent to settling, 15 ml of the digested Sartorius) and fixed in nitric acid (1% v/v concentrated
supernatant was transferred to a 20 ml polyethylene vial, Aristar grade).
with the dissolved metal concentrations of the filtrate being Porewater samples for trace metal analysis were obtained
determined by inductively coupled plasma atomic emission from composite samples collected from four randomly
spectrometry (ICP-AES) (Spectroflame EOP, Spectro selected PCDs from each treatment at each location. Only
Analytical Instruments). reduced (\-50 mV) waters were collected as the precipi-
tation of iron and manganese oxyhydroxides in oxic pore
Sediment characterisation waters has been shown to artificially inflate metal concen-
trations in similar devices (Teasdale et al. 1995). Determi-
Total organic carbon (TOC) was obtained by analysing nation of trace elements within the porewaters was
0.3 g of ground homogenised sediment on an OI Total performed on a Perkin-Elmer Elan 6000 ICP-MS, using a
Organic Carbon Analyser (Model 1010) calibrated against method adapted from Willie et al. (1998). This method
glucose standards. To remove inorganic carbon, samples employs a ToyopearlÒ AF-Chelate 650 M resin column
were pre-treated with 20 ll of 5% v/v hydrochloric acid. (Tosohass, PA, USA), an iminodiacetic acid resin with a
Samples were wet-sieved with the contents retained on a macroporous methacrylate backbone, as a chelating ion
series of sieves to obtain the following grain size classes: exchanger to sequester the trace elements from the saline
\63 lm (silt/clay); 63 lm–1 mm; and [1 mm. The con- waters, reducing the interference of chlorine-containing
tents of each sieve were oven-dried at 40°C for 48 h, polyatomic species. This technique also preconcentrates the
reweighed and expressed as a percentage calculated on a diluted samples, compensating for their initial low volume
mass/mass basis. and the expected low trace metal concentrations.

Pore water collection and analyses Data analysis

Pore waters were collected using a novel and cost-effective Differences in particulate trace metal concentrations,
approach developed by the National Institute of Water and community indices and the abundances of selected taxa

710 A. A. Chariton et al.

were analysed using a balanced, two-factor ANOVA, with from the lead/zinc smelter. Sediments collected from
the first factor ‘location’ being random, and the second Cockle Bay, the location closest to the smelter, contained
factor ‘treatment’—the sediment treatment—being fixed. higher concentrations of lead, cadmium and zinc than
Three-factor ANOVAs were used to analyse acid volatile the Warners Bay and Nords Wharf sediments. The Nords
sulfides (AVS) and simultaneously extractable metals Wharf sediments, which were sourced from the location
(SEM), with the additional factor being sediment depth furthest from the smelter, had the lowest concentrations of
(0–2 and 2–8 cm). In all biotic analyses, samples from the particulate lead, cadmium and zinc (Table 1). Cockle Bay
ambient sediments were treated as an additional treatment. and Warners Bay sediments had comparable percentages
Homogeneity of variances was tested using Cochran’s of fines (\63 lm), sands (63 lm–1 mm) and gravels
test, where violated, appropriate transformations were ([1 mm), whilst sediments collected from Nords Wharf
performed (Sokal and Rohlf 1995). In cases where datasets had a higher percentage of sand, coupled with a lower
remained heteroscedastic (Cochran’s test: P \ 0.05), percentage of fines (Table 1). Total organic carbon (TOC)
the level of significance was set at P \ 0.01. Student– was similar in the Nords Wharf and Cockle Bay sedi-
Newman–Keuls test (SNK) was used as a post-hoc proce- ments, which were inturn marginally greater than the
dure to evaluate significant differences among means. All Warners Bay sediments (Table 1).
ANOVAs were performed using G-MAV5 (Institute of Concentrations of the trace metals in each sediment
Marine Ecology, Sydney, Australia). treatment were generally unchanged at the end of the
Ordination of the biotic data was by non-metric multi- experiment (Tables 1, 2). No significant differences in the
dimensional scaling (nMDS), using the Primer v5 statisti- mean concentrations of lead (F = 1.50, P = 0.224), zinc
cal package (Plymouth Marine Laboratory). Data were (F = 1.09, P = 0.302), and copper (F = 0.07, P = 0.786)
double square-root transformed prior to analysis, with were detected between translocated sediments of the same
distances between samples measured using Bray-Curtis treatment in Location 1 and 2 (Table 2). Mean concentra-
similarity coefficients (Clarke and Warwick 1994). Dif- tions of cadmium (F = 5.46, P = 0.023) and nickel
ferences in benthic assemblages among treatments were (F = 11.75, P \ 0.001) were significantly higher in the
tested by permutational multivariate analysis of variance sediments translocated to Location 1 (Table 3). However,
(PERMANOVA) (Anderson 2001) on the transformed data these differences were proportionally small, resulting in a 2
with Bray-Curtis dissimilarities between samples. Two- and 6% difference respectively. The Cockle Bay sediments
factor, pair-wise a posteriori tests based on 999 random contained significantly higher concentrations of lead
permutations were used to identifying significant differ- (F = 893; P \ 0.001), cadmium (F = 849; P = 0.001) and
ences among treatments and locations, and their interac- zinc (F = 1977; P \ 0.001) than the Warners Bay sedi-
tions. The Primer v5 SIMPER procedure was performed to ments, which in turn were significantly higher than the
identify which taxa contributed to any differences among Nords Wharf sediments (Tables 2, 3). Although generally
the sediment treatments, including both the translocated low, mean concentrations of nickel were significantly higher
and ambient sediments. in the Nords Wharf sediment than both the Cockle Bay and
Warners Bay sediments (F = 503; P = 0.002), with no
differences being detected between the latter two sediment
Results treatments (Table 3). Copper concentrations within all
treatments were low (Table 2), and did not significantly
Sediment characteristics and trace metal concentrations differ among treatments (F = 21; P = 0.055). Cadmium
was the only trace metal in which a significant interaction
Prior to translocation, the concentrations of metals within between the translocated location 9 sediment source treat-
the sediment treatments reflected their distance of origin ment (location 9 treatment) was detected (F = 5.33;

Table 1 Trace metal concentrations, grain size and total organic carbon in the sediments collected from Nords Wharf, Cockle Bay and Warners
Sediment source Pb (mg/kg) Cd (mg/kg)) Zn (mg/kg) Cu (mg/kg) Ni (mg/kg) \63 lm (%) 63 lm–2 mm (%) [2 mm (%) TOC (%)

Nords Wharf 36 ± 1 1.4 ± \ 0.1 160 ± 3 34 ± 1 5.5 ± 0.2 24 ± 2 71 ± 3 5±2 1.0 ± 0.1
Cockle Bay 260 ± 6 30.7 ± 0.6 550 ± 7 32 ± 1 3.8 ± 0.1 40 ± 3 56 ± 4 4±2 1.0 ± 0.1
Warners Bay 221 ± 4 15.0 ± 0.8 390 ± 5 27 ± 1 3.6 ± 0.1 44 ± 3 53 ± 5 3±1 0.6 ± 0.1
Measurements were obtained from the \63 lm fraction after defaunation and homogenisation, and prior to deployment. Mean ± 1 SE are
presented, all percentages are calculated on a mass/mass basis

Recolonisation of translocated metal-contaminated sediments 711

P \ 0.01), with concentrations in the translocated Cockle





Bay and Warners Bay sediments being greater in Location 1
Table 2 Summary of particulate and porewater trace metal concentrations, SEM and AVS measurements from translocated treatments collected at the completion of the experiment

(Table 3).

[Ni, Cu, Zn, Cd sand Pb]

SEM concentrations were not influenced by depth,

location or their interactions with sediment treatment

NW Nords Wharf, CB Cockle Bay, WB Warners Bay Values for particulate and porewater trace metal concentrations represent the mean (± 1 SE), n.d not detected (\0.1 lg/l)
(Table 3). A significant difference in mean SEM concen-

trations were detected among the sediment treatments



(F = 300; P \ 0.001). Pair-wise comparisons found SEM
concentrations declined in the order Cockle Bay [

Warners Bay [ Nords Wharf (Table 3).


Sediment depth had a significant effect on AVS con-

AVS, SEM, and AVS–SEM values represent mean values (n = 3), SEM–AVS is calculated by subtracting the mean SEM from the mean AVS. SEM =
centrations (F = 15.26; P \ 0.01), with concentrations
1.0 (0.1)

0.4 (0.1)

0.6 (0.1)

1.0 (0.2)

0.5 (0.1)

0.3 (0.1)
being greater in the lower sediments (2–8 cm) (Table 3).
Mean AVS concentrations were greater in the Cockle Bay

sediments both the Warners Bay and Nords Wharf

treatments (F = 15.26; P \ 0.001) (Table 3). With the
0.8 (0.4)

1.6 (0.1)

0.8 (0.3)

1.3 (0.2)

1.2 (0.4)

0.6 (0.2)

exception of Warners Bay surficial sediments (0–2 cm),


mean AVS concentration always exceeded their molar

equivalence of SEM (Table 2). As sulfide forms insoluble
10.3 (3.7)
6.0 (0.6)

1.4 (0.1)

3.9 (0.8)

2.1 (0.6)

1.6 (0.2)

complexes with divalent metals, these results would sug-

gest that a low concentration of labile metals (Di Toro
Porewater metals (lg/l)

et al. 1990).
Redox profiles from the sediment treatments showed an






overall trend of a decline in redox values with sediment

depth (Fig. 2). Oxygen penetration was consistently deeper
0.4 (\0.1)
0.4 (0.1)

0.6 (0.1)

0.2 (0.1)

0.9 (0.6)

0.3 (0.1)

in the Nords Wharf sediments (*4 cm) than the other

translocated sediments. In the Warners Bay sediments, the

oxic layer disappearing within the first centimetre of the

sediment column. Porewater pH generally decreased with
5.3 (0.1)

3.8 (0.1)

3.6 (0.1)

5.0 (0.1)

3.6 (0.1)

3.4 (0.1)

sediment depth, with the pH range of the overlying waters


and porewaters (pH 7.2–7.8) being lower than the main

water body of the lake (pH 8.4) (Fig. 2). The mean pH of
35.1 (1.1)

31.6 (1.3)

25.1 (0.7)

34.3 (0.6)

29.5 (1.2)

26.8 (1.2)

Location 1’s Nords Wharf treatment was greater than the

other treatments and ranged between 7.6 and 7.8 in the first

four centimetres of the sediment column (Fig. 2). At a

sediment depth of 7 cm, all treatments had a mean pH
563 (15)

498 (11)

405 (22)
165 (4)

157 (4)

540 (7)
Total particulate metals (mg/kg)

between 7.3 and 7.5 (Fig. 2).


In all treatments, porewater concentrations for cadmium

were below the detection limit. Concentrations of pore-
1.3 (\0.1)

1.4 (\0.1)
29.8 (1.1)

14.2 (0.4)

26.3 (0.4)

13.0 (0.5)

water lead, zinc and nickel did not vary significantly with
sediment treatment, location or their interactions (Table 3),

although a significant interaction between sediment treat-

ment and location was found in porewater copper con-
233 (7)

195 (4)

224 (2)

194 (8)

centrations (F = 6.25; P = 0.009). Post hoc comparisons

31 (1)

30 (1)

of means found that in Location 1, porewater copper was


significantly greater in the Cockle Bay sediments than the

of sediment

other two treatments.





Univariate measurements of biota



A total of 3,371 individuals were sampled during the


experiment, comprising 40 taxa, including 19 polychaete,

nine gastropod and seven bivalve families. Polychaetes

712 A. A. Chariton et al.

Table 3 Summary of results of analysis of variance for sediment trace metal concentrations, acid volatile sulfide (AVS), simultaneously
extractable metals (SEM) and transformed (log10) porewater metals from the translocated sediments
Variable Location Treatment (sediment) Location 9 treatment Depth Interactions
with depth
(L 9 D;
S 9 D;
L 9 S 9 D)

Particulate lead ns CB [ WB [ NW*** ns na na

Particulate Loc1 [ Loc2* CB [ WB [ NW** CB & WB Loc1 [ Loc2 na na
cadmium Loc1 & Loc2
CB [ WB [ NW
Particulate zinc ns CB [ WB [ NW*** ns na na
Particulate nickel Loc1 [ Loc2 NW [ CB = WB ns na na
SEM ns CB [ WB [ NW*** ns ns ns
AVS ns CB [ WB = NW*** ns 2–8 cm [ 0–2 cm** ns
Porewater lead  ns ns ns na na
Porewater zinc  ns ns ns na na
Porewater copper ns ns Loc1 CB [ WB = NW** na na
Porewater nickel ns ns ns na na
CB Cockle Bay, WB Warners Bay, NW Nords Wharf, Loc1 Location 1, Loc2 Location 2, ns not statistically significant, na not applicable due to
the experimental design
Significant at * P \ 0.05, ** P \ 0.01, *** P \ 0.001. Only significant post hoc comparisons of means (SNK) are displayed
Significance set at P \ 0.01 due to heteroscedasticity

were the most numerically abundant taxon, comprising Whilst there was no difference in diversity at the treat-
over 79% of the total fauna sampled. Mean values of the ment level, however, in Location 1, the Nords Wharf
univariate metrics are graphically presented in Fig. 3 with treatment was less diverse than the Warners Bay treatment
the results of the 2-factor ANOVAs summarized in (Table 4, Fig. 3d). Evenness patterns were also complex.
Table 4. In Location 1, the metal contaminated treatments were
more even (i.e. lower community variation), however, in
Differences among locations in the recolonised Location 2 this difference was restricted to the Warners
assemblages Bay and Nords Wharf treatments (Table 4, Fig. 3d). The
source of the recolonised sediment had no significant
Mean total abundance, and the abundances of polychaetes, influence on taxonomic richness or the mean abundances of
capitellid polychaetes, and crustaceans were significantly molluscs and crustaceans.
greater in Location 1 (Fig. 3, Table 4). Examination of the
interaction terms indicated that in the cases of total abun- Comparisons between ambient and recolonised
dance, polychaetes and capitellids, these differences were assemblages
restricted to the translocated treatments and were not driven
by the sampled ambient (surrounding) sediments. No sig- The total number of organisms sampled in the ambient
nificant differences in richness (d), diversity (H’) or even- sediments was similar in the two locations (Fig. 3,
ness (J’) were found between the two locations (Table 4). Table 4). Ambient sediments contained a significantly
lower mean number of individuals than the translocated
Differences among translocated treatments Nords Wharf treatment (Fig. 3); however, these did not
significantly differ to those observed in the Cockle Bay and
A greater mean number of organisms recolonised the Warners Bay treatments (Table 4).
Nords Wharf treatments than the more metal-enriched The ambient sediments in Location 1 were less diverse
Cockle Bay and Warners Bay treatments (Fig. 3a, than those sampled in Location 2, with the ambient sedi-
Table 4). Analysis at the treatment level (i.e. sediments ments being the least diverse treatment within the latter
sourced from the three locations) and the interaction location (Table 4, Fig. 3b). Assemblages from the ambient
between treatment and location found differences in sediments exhibited a similar level of richness as those
abundances were primarily due to polychaetes, especially from the three translocated treatments (Fig. 3, Table 4).
capitellids (Table 4, Fig. 3e, f). Mean capitellid abundance were similar to those observed

Recolonisation of translocated metal-contaminated sediments 713

reasonable clustering of the treatments on a two-dimen-

Loc 1 Nords Wharf Loc 2 Nords Wharf
Loc 1 Cockle Bay Loc 2 Cockle Bay
sional scale despite their relatively high stresses (Location
Loc 1 Warners Bay Loc 2 Warners Bay 1 stress = 0.25; Location 2 stress = 0.26) (Clarke 1993)
(a) 0
(Fig. 4). In both locations, replicates from the translocated
Nords Wharf sediments showed a higher degree of aggre-
-1 gation than the other treatments, indicating a lower degree
of variation among the benthic assemblages within this
-2 treatment. In Location 2, the position of the replicates from
the ambient sediments in the ordination plots for both
Depth (cm)

locations suggests that the ambient assemblages are dis-
similar to the translocated assemblages, although this trend
was not clearly evident in Location 1.
-5 PERMANOVA based on the Bray-Curtis distances
detected a significant difference among treatments (PER-
-6 MANOVA F = 4.62, P \ 0.001) and locations (PER-
MANOVA F = 3.22, P \ 0.001), with the differences
-7 among treatments varying with location (PERMANOVA
-250 -200 -150 -100 -50 0 50 100 150
F = 1.59, P = 0.027). Differences between the recolon-
Redox (mV) ised assemblages in the Cockle Bay and Nords Wharf,
Warners Bay and Nords Wharf, Cockle Bay and Warners
(b) 0
Bay sediments were the same regardless of location;
however, differences between the Cockle Bay and ambient
treatments were only observed in Location 2 (Table 5).
Depth (cm)

-3 Composition of communities within the translocated

and ambient sediments

SIMPER analysis found the highest mean Bray-Curtis
dissimilarity in Location 1 was between the recolonised
-6 fauna in the Nords Wharf treatment and the surrounding
ambient fauna (Table 6). This difference was primarily
-7 due to the relatively higher abundances of capitellids,
7.0 7.2 7.4 7.6 7.8 8.0
spionids, nereids and isopods in the Nords Wharf treat-
pH ment, and oweniids in the ambient sediment. In Location 1,
Fig. 2 Mean a redox (mV) and b pH profiles obtained from the the recolonised assemblages in both the Cockle Bay and
porewaters of the translocated sediments at the completion of the Warners Bay treatments were almost equally dissimilar to
experiment. Loc 1 Location 1; Loc 2 Location 2 the Nords Wharf assemblages. The Nords Wharf treatment
contained greater proportions of capitellids, nereids,
in the metal-contaminated treatments, and consequently, eunicids and spoinids, with increased presence of oweniids
significantly lower than the Nords Wharf treatment. being indicative of both metal contaminated treatments.
Comparisons between the ambient and recolonised treat- The most dissimilar assemblages in Location 2 were the
ments produced complex interactions between location and Warners Bay and ambient assemblages. This was due to the
treatment for the metrics diversity, evenness and poly- presence of lucinids and decapods in the Warners Bay
chaete abundances, with no definitive trends being evident. treatment, and the relatively greater abundances of capi-
No significant differences in the mean abundances of tellids and mytilids in the ambient sediments. The Nords
molluscs and crustaceans were detected between the Wharf treatment contained relatively greater abundances of
ambient and recolonised assemblages. capitellids, spoinids, decapods, nereids than the metal-
contaminated treatments. In contrast to Location 1, owe-
Multivariate measurements of biota niids were relatively more abundant in the Nords Wharf
treatment than the Warners Bay treatment, with no trend in
The two-dimensional nMDS ordination plots of the biotic this taxon being observed between the Nords Wharf and
data for the experiments in both locations showed Cockle Bay treatments.

714 A. A. Chariton et al.

Fig. 3 Mean total abundances

and community measurements
per recolonization container in
each treatment for each
location. Bars represent means
(±1 SE)

Discussion for the most part these were either location specific or in
disagreement with those initially hypothesised. As pre-
The aim of this study was to experimentally test if recruited dicted, the recolonised assemblages differed from those
benthic assemblages within the metal-contaminated loca- sampled from the surrounding (ambient) established
tions of Lake Macquarie (Cockle Bay and Warners Bay) communities.
were being altered in manner which would be reflected by The relatively greater total abundance in the reference
changes in their univariate attributes and community treatment (Nords Wharf) was predominantly due to
composition. Low porewater metal concentrations and the opportunistic polychaetes, most notably, capitellids. This
physico-chemical profiles suggest that the procedures used response was consistent with a ‘protracted pulse’ pertur-
to prepare the sediments were appropriate for the creation bance resulting from the exploitation of the sediment due to
of treatments representative of their sourced locations an increase in resources (Glasby and Underwood 1996).
(Chariton 2005). The multivariate analysis clearly dem- Capitellids are commonly viewed as archetypical oppor-
onstrated that the assemblages which recolonised the metal tunists due to their ability to exploit environments which
enriched treatments (Cockle Bay and Warners Bay) dif- are unpredictable or contain ephemeral resources (Grassle
fered from the Nords Wharf reference treatment. Whilst and Grassle 1976). The finding here suggests that oppor-
some differences in the univariate attributes were observed, tunistic polychaetes were either preferentially recolonising

Recolonisation of translocated metal-contaminated sediments 715

Table 4 Summary of results of from two-factor analysis of variance for community indices and the abundances of selected taxa sampled in the
translocated and ambient sediments from Locations 1 and 2 in Lake Macquarie
Variable Location Treatment Location 9 treatment

Total abundance Loc1 [ Loc2*** NW [ CB = WB = AM** ns

Diversity (H’) ns ns NW Loc2 [ Loc1; Am Loc1 [ Loc2**
Loc1 WB [ NW; Loc2 NW = CB = WB [ AM
Taxa richness (d) ns ns ns
Evenness (J’) ns ns NW Loc2 [ Loc1; AM Loc1 [ Loc2*
Loc1 CB = WB = AM [ NW; Loc2 WB [ NW = AM
Polychaete abundance Loc1 [ Loc2*** ns NW & CB & WB Loc1 [ Loc2**
Loc1 NW [ WB = CB [ AMB; Loc2 NW [ CB = WB = AM
Capitellid abundance Loc1 [ Loc2*** NW [ CB = WB = AM* ns
Molluscs abundance ns ns ns
Crustacean abundance Loc1 [ Loc2** ns ns
Loc1 Location 1, Loc2 Location 2, NW Nords Wharf, CB Cockle Bay, WB Warners Bay, AM Ambient sediments
Significant at * P \ 0.05, ** P \ 0.01, *** P \ 0.001. Only significant post hoc comparisons of means (SNK) are displayed

Table 5 Multivariate pair-wise comparisons of assemblages among

treatments within Locations 1 and 2, Lake Macquarie
Location Sediment treatment t P

Location 1 Nords Wharf vs. Cockle Bay 1.73 0.002

Nords Wharf vs. Warners Bay 2.06 \0.001
Nords Wharf vs. Ambient 2.29 <0.001
Cockle Bay vs. Warners Bay 0.98 0.490
Cockle Bay vs. Ambient 1.34 0.067
Warners Bay vs. Ambient 1.90 <0.001
Location 2 Nords Wharf vs. Cockle Bay 1.50 0.011
Nords Wharf vs. Warners Bay 1.85 <0.001
Nords Wharf vs. Ambient 2.17 <0.001
Cockle Bay vs. Warners Bay 1.21 0.193
Cockle Bay vs. Ambient 2.25 <0.001
Warners Bay vs. Ambient 2.17 <0.001
Bold P values indicate significant results where P \ 0.05

the Nords Wharf sediments, or were being subjected to

lower rates of mortality, avoidance or emigration than the
fauna in the Cockle Bay and Warners Bay sediments.
It was hypothesised that assemblages sampled from the
treatments with high trace metal concentrations would be
less taxonomically rich and diverse, and more even than
the Nords Wharf treatment, with such responses being
indicative of a contaminant-induced ‘protracted-press per-
turbation’ (Glasby and Underwood 1996). However, these
hypotheses were not supported, with richness remaining
unaffected by sediment treatment, and diversity and
evenness patterns being ambiguous. Whilst mollusc and
crustacean abundances did not decline in response to
Fig. 4 Two dimensional nMDS ordination plots for the recolonisa- treatments, SIMPER analysis found representatives from
tion experiments in Location 1 (a) and Location 2 (b) both taxonomic groups aided discrimination between the

716 A. A. Chariton et al.

Table 6 Summary of SIMPER analyses for comparisons between significantly different treatments
Location Sediment treatment Dissimilarity (%) Five major taxa contributing to dissimilarities

Location 1 Nords Wharf vs. Ambient 55.70 Spionidae, Capitellidae, Eunicidae, Cirratulidae Oweniidae
Warners Bay vs. Ambient 54.74 Capitellidae, Isopoda, Spionidae, Oweniidae, Nereididae
Nords Wharf vs. Warners Bay 48.13 Capitellidae, Oweniidae, Eunicidae, Isopoda, Nereididae
Nords Wharf vs. Cockle Bay 48.04 Oweniidae, Capitellidae, Nereididae, Eunicidae, Spionidae
Location 2 Warners Bay vs. Ambient 68.04 Capitellidae, Spionidae, Lucinidae, Decapoda, Mytlidae
Cockle Bay vs. Ambient 67.97 Capitellidae, Oweniidae, Spionidae, Tellinidae, Mytlidae
Nords Wharf vs. Warners Bay 60.36 Capitellidae, Nereididae, Oweniidae, Spionidae, Decapoda
Nords Wharf vs. Ambient 60.05 Oweniidae, Nereididae, Spionidae, Decapoda, Mytlidae
Nords Wharf vs. Cockle Bay 56.66 Capitellidae, Spionidae, Decapoda, Nereididae, Trochidea

reference and metal contaminated treatments. From the While the recolonisation experiment was designed to
relatively small pool of manipulated trace metal studies, overcome some of the confounding issues associated with
marked response in univariate indices has only been the gradient study (Chariton 2005), the experiment was not
demonstrated in studies using treatments with highly ele- void of confounding factors. As the Nords Wharf treatment
vated concentrations of trace metals in either or both the was a reference sediment and not a true control, it is not
sediment and porewaters (Hansen et al. 1996; Watzin possible to establish if other differences other than trace
and Roscigno 1997). For example, Trannum et al. (2004) metal concentrations, e.g. grain size, were influencing the
observed significant changes in the composition of response of the treatments. Although statistical differences
assemblages with copper concentrations between 400 and in grain size occurred between the metal-contaminated
1,500 mg/kg. In studies using trace metal concentrations and reference treatments, these differences were not pro-
closer to those employed here (e.g. Lindegarth and nounced, i.e. sandy versus silty. However, when the present
Underwood 2002), univariate responses have generally study is viewed in concert with the findings of benthic
been unresponsive or temporally and spatially complex. surveys (Chariton 2005), bioaccumulation and environ-
The findings of the current study support the commentary mental chemistry studies (Roach et al. 2008), there is
of Johnston and Roberts (2009), who emphasised that considerable evidence to suggest that the concentrations of
community metrics cannot be solely used to derive eco- metals within Cockle Bay and Warners Bay are sufficient
toxicological lines of evidence as they do not convey to induce some level of ecological and biological
pertinent information on taxa loss and replacement. dysfunction.
The multivariate analysis clearly showed that recolon- In order to employ recolonisation experiments as a
ised assemblages in the Nords Wharf treatments were location or sediment-specific risk assessment tool, it is
distinct from those sourced from Cockle Bay and Warners essential that the translocated treatments remain represen-
Bay, with the latter two treatments containing similar tative of sediments from the source locations. The use of
assemblages. For the most part, it was the relative abun- nitrogen gas to defaunate the sediments appears to have
dances of the dominant biota (e.g. capitellids, spionids, and created treatments with similar metal concentrations and
isopods), and not their presence or absence which lead to physico-chemical qualities to those found in Lake Mac-
these differences. Consequently, there were few taxa which quarie (Chariton 2005). At the end of the experiment,
were indicative of either the reference or metal-contami- particulate trace metal concentrations were generally sim-
nated treatments. Nereids were a notable exception, with ilar to initial concentrations, indicating minimal loss of
this taxa being relatively common in the Nords Wharf metals or deposition from the ambient substrate. Trace
treatment, and all but absent in the both metal-contami- metals appear to have remained in their sediment-bound
nated treatments. Nereids have frequently been shown to be phases as porewater metals were low in all treatments,
sensitive to metals (Dean 2009), and have been observed to including those treatments that had high molar equiva-
be more populous in Nords Wharf than the other locations lences of SEM than AVS. The physico-chemical mea-
(Chariton 2005). Other pronounced differences observed in surements of the pore waters indicated that the sediments
Lake Macquarie, e.g. higher abundances of amphipods and had reached a state typical of biologically irrigated sedi-
nephytids at Nords Wharf, were not observed in the ments, with an identifiable oxic layer penetrating into the
recolonisation experiment. sediment column followed by a dramatic decline in the

Recolonisation of translocated metal-contaminated sediments 717

redox potential of the porewaters (Jörgensen and Revsbech Clarke KR (1993) Non-parametric multivariate analyses of changes in
1985). In the case of the Nords Wharf sediments, the community structure. Aust J Ecol 18:117–143
Clarke KR, Warwick RM (1994) Changes in marine communities: an
greater level of biological activity resulted in a deeper oxic approach to statistical analysis and interpretation. Plymouth
layer and greater infiltration of the overlying waters as Marine Laboratory, Plymouth
indicated by the porewaters pH and redox status being Dean HK (2009) The use of polychaetes (Annelida) as indicator
closer to that of the overlying waters (Marinelli and species of marine pollution: a review. Rev Biol Trop 56:11–38
Di Toro DM, Mahony JD, Hansen DJ, Scott KJ, Hicks MB, Mayr SM,
Boudreau 1996). Redmond MS (1990) Toxicity of cadmium in sediments: the role
The present study demonstrated that defaunated sedi- of acid volatile sulfide. Environ Toxicol Chem 9:1487–1502
ments sourced from locations with high trace metal con- Diaz-Castaneda V, Frentier S, Arenas V (1993) Experimental
centrations were colonised by different faunal assemblages re-establishment of soft-bottom community: utilization of mul-
tivariate analysis to characterize different benthic recruitments.
to sediments sourced from a location with lower concen- Estuar Coast Shelf Sci 37:387–402
trations. While no single approach can provide a confident Glasby TM, Underwood AJ (1996) Sampling to differentiate between
and robust assessment of the ecological status of a loca- pulse and press perturbations. Environ Monit Assess 42:241–252
tion, when coupled with field surveys and/or toxicological Grassle JP, Grassle JF (1976) Sibling species in the marine pollution
indicator Capitella (Polychaeta). Science 192:567–569
data, manipulative translocation experiments provide an Hansen DJ, Mahony JD, Berry WJ, Benyi SJ, Corbin JM, Pratt SD, Di
additional line of ecological information which can be Toro DM, Abel MB (1996) Chronic effect of cadmium in
integrated into a weight-of-evidence approach for assess- sediments on colonization by benthic marine organisms: an
ing the risks associated with contaminated sediments evaluation of the role of interstitial cadmium and acid-volatile
sulfide in biological availability. Environ Toxicol Chem
(Batley et al. 2002). The translocation technique used in 15:2126–2137
this experiment is simpler and more accurate than spiking Johnston EA, Roberts DA (2009) Contaminants reduce the richness
with a complex mixture of contaminants, and incorporates and evenness of marine communities: a review and meta-
other chemicals which may not have been foreseen. Def- analysis. Envion Poll 157:1745–1752
Jörgensen BB, Revsbech NP (1985) Diffusive boundary layers and
aunation and homogenisation under anoxic conditions the oxygen uptake of sediments and detritus. Limnol Oceanogr
appears to provide sediment treatments with biogeo- 30:111–122
chemical conditions similar to that observed in the field. Josefson AB, Hansen JL, Asmund G, Johansen P (2008) Threshold
Furthermore, as the approach focuses on recolonisation, it response of benthic macrofauna integrity to metal contamination
in West Greenland. Mar Poll Bull 56:1265–1274
examines the potential toxicity of metals on assemblages Kilby GW, Batley GE (1993) Chemical indicators of sediment
in a different state of organisation to that of established chronology. Aust J Mar Freshw Res 44:635–643
field assemblages, providing a different alternative per- Lenihan HS, Kiest KA, Conlan KE, Slattery PN, Konar BH, Oliver JS
spective of how metals may be modifying in situ (1995) Patterns of survival and behaviour in Antarctic benthic
invertebrates exposed to contaminated sediments: field and
assemblages. laboratory bioassay experiments. J Exp Mar Biol Ecol
Acknowledgments The authors wish to thank the NSW Environ- Lindegarth M, Underwood AJ (2002) A manipulative experiment to
mental Trust and the Australian Post-graduate Awards for their evaluate predicted changes in intertidal, macro-faunal assem-
financial support, Frank Krikowa (University of Canberra) for the blages after contamination by heavy metals. J Exp Mar Biol Ecol
trace metal analyses, Dr Graeme Batley (CSIRO) for his editorial 274:41–64
comments on the manuscript, and the numerous staff and students Luoma SN (1996) The developing framework of marine ecotoxico-
who assisted in sampling. logy: pollutants as a variable in marine ecosystems? J Exp Mar
Biol Ecol 200:29–55
Maher WA, Forster S, Krikowa F, Snitch P, Chapple G, Craig P
(2001) Measurements of trace elements and phosphorus in
References marine animal and plant tissue by low-volume microwave
digestion and ICP-MS. At Spectrosc 22:361–370
Anderson MJ (2001) A new method for non-parametric multivariate Marinelli RL, Boudreau BP (1996) An experimental and modelling
analysis of variance. Austral Ecol 26:32–46 study of pH and related solutes in an irrigated anoxic coastal
Batley GE (1987) Heavy metal speciation in waters, sediment and sediment. J Mar Res 54:939–966
biota from Lake Macquarie, New South Wales. Aust J Mar Morrisey DJ, Underwood AJ, Howitt L (1996) Effects of copper on
Freshw Res 38:591–606 the faunas of marine soft-sediments: an experimental field study.
Batley GE, Burton GA, Chapman PM, Forbes VE (2002) Uncertain- Mar Biol 125:199–213
ties in sediment quality weight-of-evidence (WOE) assessments. Roach AC (2005) Assessment of metals from Lake Macquarie, New
Hum Ecol Risk Assess 8:1517–1547 South Wales, Australia, using normalisation models and sedi-
Calabretta CJ, Oviatt CA (2008) The response of benthic macrofauna ment quality guidelines. Mar Environ Res 50:453–472
to anthropogenic stress in Narragansett Bay, Rhode Island: a Roach AC, Jones AR, Murray A (2000) Using benthic recruitment to
review of human stressors and assessment of community assess the significance of contaminated sediments: the influence
conditions. Mar Poll Bull 56:1680–1695 of taxonomic resolution. Environ. Pollut 112:1–13
Chariton AA (2005) Responses in estuarine macrobenthic inverte- Roach AC, Maher WA, Krikowa F (2008) Assessment of metals in
brate assemblages to trace metal contaminated sediments. PhD fish from Lake Macquarie, New South Wales, Australia. Arch
thesis, University of Canberra Environ Contam Toxicol 54:292–308

718 A. A. Chariton et al.

Santos SL, Simon JL (1980) Marine soft-bottom establishment near a lead smelter, Spencer Gulf, South Australia. Mar Ecol
following annual defaunation: larval or adult recruitment? Mar Prog Ser 135:123–135
Ecol Prog Ser 2:235–241 Warren LA, Tessier A, Hare L (1998) Modelling cadmium accumu-
Simpson SL (2001) A rapid screening method for acid-volatile lation by benthic invertebrates in situ: the relative contribution of
sulphides in sediments. Environ Toxicol Chem 20:2657–2661 sediment and overlying water reservoirs to organism cadmium
Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of concentrations. Limnol Oceanogr 43:1442–1454
statistics in biological research, 3rd edn. W.H. Freeman, New Warwick RM (1993) Environmental studies on marine communities:
York pragmatical considerations. Aust J Ecol 18:63–80
Suter GW, Barnthouse LW (1993) Assessment concepts. In: Suter Warwick RM (2001) Evidence for the effects of metal contamination
GW (ed) Ecological risk assessment. Lewis Publishers, London, on the intertidal macrobenthic assemblages of the Fal Estuary.
pp 21–47 Mar Pollut Bull 42:145–148
Teasdale PR, Batley GE, Apte SC, Webster IT (1995) Pore water Watzin MC, Roscigno PR (1997) The effects of zinc contamination
sampling with sediment peepers. Trends Anal Chem 14:250–256 on the recruitment and early survival of benthic organisms in an
Trannum HC, Olsgard F, Skei JM, Indrehus J, Øverås S, Eriksen J estuary. Mar Pollut Bull 34:443–455
(2004) Effects of copper, cadmium and contaminated harbour Willie SN, Iida Y, McLaren JW (1998) Determination of Cu, Ni, Zn,
sediments on recolonisation of soft-bottom communities. J Exp Mn, Co, Pb, Cd and V in seawater using flow injection ICP-MS.
Mar Biol Ecol 310:87–114 At Spectrosc 19:67–72
Ward TJ, Hutchings PA (1996) Effects of trace metals on infaunal
composition in polluted intertidal and subtidal marine sediments