Sie sind auf Seite 1von 9

Ecological Indicators 45 (2014) 130–138

Contents lists available at ScienceDirect

Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Approaching a functional measure of vulnerability in marine


ecosystems
Francisco Arreguín-Sánchez ∗ , Thelma Mónica Ruiz-Barreiro
Centro Interdisciplinario de Ciencias Marinas del Instituto Politécnico Nacional, Apartado Postal 592, La Paz 23000, Baja California Sur, Mexico

a r t i c l e i n f o a b s t r a c t

Article history: Ecosystem vulnerability is a major concern for management purposes, especially when directed toward
Received 1 May 2013 conservation and sustainable exploitation. We estimate the relative vulnerability of selected marine-
Received in revised form 25 January 2014 ecosystems in the Gulf of Mexico through simulation experiments based on trophic models. The same
Accepted 2 April 2014
perturbation pattern was applied to different functional groups at different trophic levels. Perturbation
consisted of increasing biomass extraction for a single group up to 98% at a constant rate over 50 years.
Keywords:
The ratio Ascendency to Capacity of Development, A/C, was estimated as a measure of ecosystem order.
Ecosystem vulnerability
The maximum negative difference respect to the initial A/C represents the gain of entropy. The slope of
Order
Entropy
the relationship between entropy gained and the trophic level provides an estimate of the relative vul-
Trophic webs nerability of the ecosystem. This was applied to five ecosystems in the Gulf of Mexico: Florida coral reef;
Fisheries management Mexican coastal lagoon, Terminos Lagoon; and three continental shelves, the northern Gulf of Mexico,
USA; Yucatan and the Campeche Sound, Mexico. The pattern of vulnerability among ecosystems is related
to ecosystem complexity. The coral reef exhibited a lower slope, corresponding to higher vulnerability,
which is related to higher connectivity, production efficiency, and net ecosystem production. Increas-
ingly higher slopes, corresponding to lower vulnerability, followed a gradient from the coral reef to the
continental shelves to the least vulnerable system, the coastal lagoon. Middle trophic levels contribute
to higher vulnerability. This interpretation is supported by the concept of energy flows within trophic
networks. The relevance of these findings for management is discussed.
© 2014 Elsevier Ltd. All rights reserved.

1. Introduction with the particular problems to be addressed. Here, we are con-


cerned with the vulnerability of marine-ecosystems represented by
Ecosystem vulnerability is a major concern for human society trophic models and with exploring the internal processes in these
for a variety of reasons. Particularly critical is the need to cope with systems. For this purpose, we define vulnerability as the sensitivity
variability and uncertainty in the use and management of natural of an ecosystem to stresses, perturbations or damage that may alter
resources. Several approaches to estimating and addressing vulner- the dynamic ecological balance. Sensitivity is related to the effect
ability can be found in the literature, including studies that warn of of such perturbations, which is a function of ecosystem organiza-
certain species’ extinction vulnerability (Dulvy et al., 2003; Graham tion and functioning. Our measure of vulnerability is based on the
et al., 2011), identify vulnerable marine areas (Zacharias and Gregr, thermodynamic concept of entropy.
2005), propose strategies to cope with climate change (Luers et al., The exploitation of natural living resources in an ecosystem (e.g.,
2003; Eriksen et al., 2005; Romieu et al., 2010), or provide method- fishing) results in the removal of biomass, thus altering ecosys-
ological approaches to evaluate risks or formulate management tem function and organization. Although exploitation creates some
policies (Helpern et al., 2007; De Lange et al., 2010; Teck et al., level of stress, if the perturbation does not affect the natural
2010). renewal rate of the exploited species, then the species and the
The concept of vulnerability may be defined differently in any of ecosystem will respond by recovering the lost biomass and restor-
these areas of research, and these variable definitions are associated ing their energy flows to maintain their dynamic balance; this
process is known as resilience, which is strongly related to the con-
cept of sustainability (Ulanowicz, 2011a; Ulanowicz et al., 2009;
∗ Corresponding author. Tel.: +52 612 1230350; fax: +52 6121225322. Turner et al., 2003). The self-organization process represents the
E-mail addresses: farregui@ipn.mx, francisco.arreguinsanchez@gmail.com natural dynamics through which an ecosystem maintains order. If
(F. Arreguín-Sánchez). the perturbation alters the natural renewal rate, then the biomass

http://dx.doi.org/10.1016/j.ecolind.2014.04.009
1470-160X/© 2014 Elsevier Ltd. All rights reserved.
F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138 131

of the exploited species cannot be recovered at the state previous sense, entropy will rise. The energy in reserve is called the Over-
to the perturbation, and the energy flows in the trophic web can- head (Ulanowicz, 1986) and is represented by the difference C − A.
not be restored and the system enter in a self-organization process. Our goal is to estimate the ecosystem entropy (or loss of order)
Even if the ecosystem’s self-organization processes act to promote generated by perturbing certain functional groups and to charac-
recovery, the result will be an unbalanced state, generating entropy. terize ecosystem-vulnerability patterns for its potential use in a
Under this framework, sustainability is a dynamic process that management framework.
maintains a balance between order and entropy (Ulanowicz, 2009,
2011b), and vulnerability is related to increasing entropy. 2. Materials and methods
Our purpose is to explore the dynamics behind the order-
entropy balance to address the following questions: how does a To estimate changes in the ascendency and the capacity of
system react to a stressor based on its organization and function? development of a given ecosystem, a simulation experiment was
How can we measure internal processes to evaluate vulnerabil- designed using trophic models constructed with the suite of pro-
ity, especially in exploited ecosystems? Understanding internal grams Ecopath with Ecosim (Pauly et al., 2000; Christensen and
ecosystem processes related to vulnerability is critical to formally Walters, 2004). The experiment consisted of perturbing selected
estimate the probability of success of management decisions. functional groups at different trophic levels (Table 1) in an ecosys-
Ecosystem functioning refers to attributes related to energy tem model and measuring the ecosystem response to these
flows and to the way in which an ecosystem uses and distributes perturbations in terms of A and C. The perturbations consisted of
energy (Ulanowicz, 1986); being a measure of the activity of the gradually extracting biomass from 0% to 98% of the initial biomass
system, or its metabolism (Mageau et al., 1995). In general terms, at a constant rate over a 50-year period. The functional groups to be
numerous authors have argued that ecosystem-based management perturbed were selected covering the whole range of trophic levels
must focus on preserving ecosystem health, that is, on preserving an and taking care that groups between ecosystems were as similar
ecosystem’s function, organization and resilience (Costanza, 1992, as possible and from comparable trophic levels. For demonstration
2012; Costanza and Mageau, 1999; Mageau et al., 1998; Ulanowicz, purposes, we assumed that the current ecosystem model can be
1980), understanding organization as a measure of the number and used as baseline against which to compare ecosystem attributes
diversity of interactions between the components of an ecosystem, after being disturbed, in which order and entropy were balanced.
and resilience, as the ability of a system to maintain its structure Several functional groups were selected within each ecosystem
and pattern of behavior in presence of stress (Mageau et al., 1995). (Table 1), but only one group was perturbed at a time.
This goal could be referred to as maintaining ecosystem order, or The perturbation (P) of a functional group was applied according
the dynamic balance between order and entropy, assuming entropy to the relationship
to be a measure or indicator of ecosystem degradation.  I

Ulanowicz (1986) provided a theoretical framework to describe P= [1 − exp -(I + M)]
(I + M)
ecosystem properties based on energy flows in trophic networks;
and following Ulanowicz (2009) the ratio A/C (Ascendency, A, over where I is the instantaneous impact rate and M is the instantaneous
Capacity of Development, C) provides a measure of ecosystem natural mortality rate, both on an annual basis, and P expresses the
order. Ascendency is described by proportion of the biomass extracted for a given impact rate.
   The simulation outputs consisted of estimates of the ecosys-
Tij T• • tem ascendency and capacity of development for each perturbed
A= Tij log
Ti,• T• j functional group based on the yearly perturbation rate. These esti-
ij
mates were used to calculate order (A/C) and entropy (1 − A/C).
where i,j represent the prey (resources) and predator (consumer), Additionally, a negative deviation of the order from its initial state
respectively; T represents the energy flows; and • is the sum of the (A/Csim < A/Cini ) was assumed to represent a gain in entropy and
energy flows of the prey or predators, with Ti,• being the flows from consequently a trend toward ecosystem deterioration. The results
one prey species to all of its predators T•,j being the total consump- for different functional groups within each ecosystem were ana-
tion of a predator species summed over all of its prey, and T•• being lyzed and compared to those from other ecosystems.
the total flow occurring in the system. As test cases, we used trophic models of five ecosystems within
The Capacity of Development of the ecosystem is a measure the Gulf of Mexico: the northern Gulf (Browder, 1993) and a
of the maximum ascendency that the ecosystem can reach and is Florida coral reef (Venier and Pauly, 1997), both in the United
represented by States; and the Yucatan continental shelf (Arreguín-Sánchez, 2000),
   the Campeche Sound (Zetina-Rejón and Arreguín-Sánchez, 2003)
Tij and Terminos Lagoon (Manickchand-Heileman et al., 1998), all in
C= Tij log
T•• Mexico.
ij
For correlations we used the reduced major axis (RMA) lin-
Ascendency represents the organized power of the system, and ear regression (Hofman et al., 1986; Leduc, 1987; Smith, 2009),
the magnitude of the energy (power) flowing within the ecosystem in which the fitting process assumes both variables are measured
toward particular ends. Ascendency also depicts the density of links with error, in contrast with the conventional linear egression anal-
in the system implying the ability of self-organization to direct itself ysis where only the dependent variable is assumed to be measured
to the mature and fully developed stage The Development Capacity with error (Fig. 1).
is the upper limits of the Ascendency and represents the whole
capacity of information within the system boundary and indicates 3. Results
the complexity of the system’s activities (Ulanowicz, 1986; Chen
et al., 2010). For each ecosystem, we selected functional groups at different
In our context, if we consider A/C to be a measure of ecosystem trophic levels to be perturbed (Table 1). The perturbation rate, rep-
order, then 1 − A/C is a measure of ecosystem entropy. In terms of resenting the proportion of biomass extracted, was applied to each
ecosystem dynamics, a system can maintain order if it has enough functional group using the Ecosim model (Walters et al., 1997),
energy in reserve to deal with perturbations. When this energy is and the results were expressed in terms of changes in the ascen-
exhausted, the ecosystem will lose some order; in a thermodynamic dency, capacity and order (A/C) of the ecosystem. For example, Fig. 2
132 F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138

2.1
2.1
2.4
2.4
2.4
2.5
2.7
2.9
2.9
3.3
1.0
TL
Functional groups (FG) selected for simulated perturbation in each ecosystem, indicating the corresponding trophic level (TL). Numbers after FG indicate the total functional groups for each ecosystem. For location see Fig. 1.

Other macroinvertebrates
Terminos Lagoone (LT)

Microcrustaceans
Phytoplankton

Zooplankton

Anchovies

Snappers
Mojarras
Shrimp
FG (20)

Porgies

Catfish
Grunts
2.1
2.3
2.8

3.3
3.4
3.9

4.2
1.0

3.0

4.0
TL
Campeche Soundd (CS)

Fig. 1. Locations of the ecosystems selected as test cases in the Gulf of Mexico.
(1) Northern Gulf of Mexico, (2) Coral Reef, (3) Continental shelf of Yucatan, (4)
Phytoplankton

Campeche Sound, (5) Terminos Lagoon. For details about ecosystem models see
Zooplankton

Table 1.
Sea turtles

Octopuses

Groupers
Snappers
Mojarras
Shrimp
FG (25)

Grunts

Sharks
Yucatan continental shelfc (YCS)

2.2
2.4

3.3
3.4
3.5
3.5
4.1
4.1
4.6
4.6
4.9
1.0
2.0

3.0
TL

Microcrustaceans
Other mollusks
Phytoplankton

Red groupers
Zooplankton

Octopuses
Penaeidae

Snappers
Mojarras
FG (21)

Porgies

Grunts

Sharks
Crabs

Jacks
2.4
2.8
2.8
2.9

3.5
3.7
3.9
3.9
4.1
4.3
1.0
2.0

3.0
TL

Fig. 2. Changes in ascendency in the Terminos Lagoon ecosystem as a function of


increasing perturbation rate.
Mid-water piscivores
Small reef herbivores

Small reef carnivores

Large reef carnivores


Large planktivores
Worms, mollusks

shows the changes in ascendency with increasing perturbation


Coral reefb (CR)

Large groupers
Phytoplankton

Cephalopods
Zooplankton

rate for selected functional groups in the Terminos Lagoon ecosys-


Crustaceans
Sea turtles

tem. Ascendency measures ecosystem organization (Ulanowicz,


FG (20)

Sharks

1986), the ecosystem trajectories exhibited increasing organization


when catfish, mojarra, zooplankton and shrimp were perturbed
but decreasing organization when the remaining functional groups
were perturbed.
Northern Gulf of Mexicoa (NGM)

Fig. 3 represents the changes in order (A/C) with gradually


2.1
2.5
3.1
3.3
3.8
1.0
TL

increasing perturbation rate in the Terminos Lagoon and Yucatan


continental shelf ecosystems. For Terminos Lagoon, a clear trend
Zetina-Rejón and Arreguín-Sánchez (2003).

toward decreasing order emerged when phytoplankton were per-


Pelagic predators

turbed. When shrimp, zooplankton and other macro-invertebrates


Manickchand-Heileman et al. (1998).
Phytoplankton

Crabs, shrimp

were perturbed, the system gained order. For the Yucatan con-
Zooplankton

tinental shelf, a loss of order was evident when phytoplankton


Mackerels
FG (14)

and zooplankton were perturbed. In all cases, although ascendency


Sharks

(Fig. 2) and order (Fig. 3) decreased gradually, larger changes were


Arreguín-Sánchez (2000).
Venier and Pauly (1997).

apparent when approximately 40% (±15%) of the biomass of a given


functional group was extracted for the five study cases.
Browder (1993).

Fig. 4 shows the relationship between order and entropy for the
Group number

Yucatan continental shelf ecosystem. The magnitude of change dif-


fered depending on the functional group perturbed. The magnitude
of change was clearly greater for low trophic levels; the pertur-
Table 1

bation of phytoplankton and zooplankton generated the highest


1
2
3
4
5
6
7
8
9
10
11
12
13
14
a

entropy, followed by the perturbation of high trophic-level groups


F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138 133

perturbed than high TLs. Points in Fig. 5 represent the entropy


gained by an ecosystem when a trophic level (independent vari-
able in the figure) is perturbed; so, for example, a loss of biomass
of 80% in a low trophic level, will generate higher entropy in the
system than the same perturbation on a high trophic level. This is
because low trophic levels are the basis of the food web, and this
is also the reason because all the slopes are negative. Since slopes
indicate the trend over all the perturbed trophic levels, they can be
interpreted as the amount of entropy that a system can gain after
a perturbation. Since vulnerability is defined as the capability to
be damaged after an event, then slopes express the relative vul-
nerability of an ecosystems respect to others. The different slopes
among ecosystems suggest vulnerability is an intrinsic attribute
of the ecosystems. Because the dependent variable is the entropy
gained by the ecosystem after the perturbation of a functional
group (represented by trophic levels), the slope can be considered
an holistic index of vulnerability. Thus, a lower slope represents
higher ecosystem vulnerability because the values for TLs exhibit
high gain of entropy. In contrast, a higher slope represents lower
vulnerability because only low TLs perturbed produce high entropy,
while high TLs perturbed exhibit lower entropy. The slopes of these
relationships were computed using the reduced major axis (RMA)
linear regression (Hofman et al., 1986; Leduc, 1987; Smith, 2009),
assuming both variables are measured with error.
The weighted estimated entropy was computed as the ratio
(A/Csim < A/Cini )/(A/Cmax < A/Cmin ) where numerator was explained
above and denominator represents the total magnitude of change
in order due to perturbation. Note that symbol “<” is used to select
only those measures that provokes increase in entropy, avoiding
those cases where entropy reduced. When such ratio if related to
Fig. 3. Changes in the order (A/C) of the Terminos Lagoon ecosystem (a) and the the trophic level perturbed, the relative contribution of each func-
Yucatan continental shelf ecosystem (b) as a function of increasing perturbation rate. tional group to vulnerability can be observed. Fig. 5 (bottom) shows
Trajectories below the initial A/C value represent a loss of order and consequently a that contribution of middle trophic levels perturbed to ecosys-
degrading ecosystem.
tem vulnerability is higher, coinciding with concept of key species
(Scotti and Jordán, 2010; Livi et al., 2011) referred to the central
such as red groupers, porgies, penaeids, octopuses, jacks and sharks. role of the species in the middle of the food web in the dynamics
Other impacted groups did not generate entropy when perturbed. of ecosystems (Table 2).
The entropy is computed as the maximum negative difference The relative vulnerability of each ecosystem (i.e., the slopes of
in order between the simulated and initial states (A/Csim < A/Cini ). the relationships in Fig. 5) was associated with certain topological
This represents the entropy gained when a functional groups is and functional ecosystem attributes. Fig. 6 shows the relationships
perturbed, being an unweighted estimator since is independent of with connectance, net system production (NSP), the ratio of pri-
the total magnitude of change in order generated by the perturba- mary production to respiration (P/R), and the ratio of respiration
tion. This entropy gained was related to the trophic level (TL) of the to biomass (R/B). Even when none of the relationships were sta-
perturbed group. All of the slopes were negative (Fig. 5 top), indi- tistically significant (Table 3) (most likely due to the few degrees
cating that, in proportion, low TLs generated higher entropy when of freedom), clear tendencies were evident. For example, higher

Fig. 4. Changes in the order (A/C) of the Yucatan continental shelf ecosystem as a function of entropy [1 − (A/C)] when selected functional groups were perturbed. The
middle point in the left panel indicates the current state of the ecosystem. The right panel represents a magnified view around the middle point to highlight relatively small
deviations. Rightward trajectories indicate increasing entropy, assumed to represent ecosystem deterioration. Numbers represent functional groups listed in Table 1. Because
all of the lines fall within the same space in the graph, each line was lagged by 0.5 units over the Y-axis to facilitate analysis.
134 F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138

Table 2
Parameters of the reduced major axis linear regressions for each ecosystem between the logarithm of the entropy gained (after the perturbation of a functional group) and
the trophic level of the perturbed group.

Ecosystem a b r2 p F df RMSr

Terminos Lagoon −0.1584 −1.6228 0.7812 <0.001 28.562 9 0.4947


N Gulf of Mexico 0.3294 −1.5034 0.7523 0.025 12.147 5 0.9639
Campeche Sound 0.5006 −1.3784 0.6171 0.007 12.892 9 1.0293
Yucatan continental shelf −0.4052 −1.0036 0.5133 0.004 12.653 13 1.1428
Florida coral reef −0.5952 −0.2972 0.3622 0.038 5.678 11 0.4048
All ecosystems 0.3545 −1.3364 0.5225 <0.001 37.2095 35 1.2439

a and b, regression parameters; r2 , determination coefficient; p, probability of significance (p < 0.05); F, ANOVA test statistic; df, degrees of freedom; RMSr, root mean square
of the residual error.

Fig. 5. The relationship between relative entropy (the logarithm of the entropy gained after the perturbation of a functional group) and trophic level (pictures on top). Linear
trends are used to show the tendency of a gradient of slopes that appears to be related to complexity of ecosystems (see Fig. 6). The fitting parameters are shown in Table 2.
The slopes are considered an index of the relative vulnerability. Pictures on the bottom show the weighted entropy (the ratio of entropy gained over total change of order
over the whole range of perturbation). It can be observed that functional groups on the middle of the food web (intermediate trophic levels) have the higher contribution to
entropy and then vulnerability of ecosystems. Black dots represent functional groups that produced a gain in entropy when perturbed; open dots are groups that contribute
with loss of entropy when perturbed. LT, Terminos Lagoon (coastal lagoon); NGM, Northern Gulf of Mexico (continental shelf, soft bottom); CS, Campeche Sound (continental
shelf, soft bottom); CSY, Yucatan continental shelf (hard bottom); CRF, coral reef of Florida.

Fig. 6. Relationships between relative vulnerability and selected ecosystem attributes for five ecosystems of the Gulf of Mexico. For the interpretation of these relationships,
see the text.
F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138 135

Table 3 its maximum possible organization but will be highly fragile. From
Parameters of the reduced major axis linear regressions between relative vulnera-
this perspective, the A/C ratio clearly indicates the degree of order
bility (slopes in Table 3 and selected ecosystem attributes (treated as independent
variables and shown at the head of each column). R/B, respiration/biomass ratio; of the system.
PP/R, primary production/respiration ratio; NSP, net system production; and Con- Overhead, like ascendency and the capacity of development,
nectance, connectivity. has several components based on the destination of the energy
Parameters R/B PP/R NSP Connectance
flows: import, export, respiration and internal flows. Assuming
that exports and imports are balanced or that their magnitude
a 1.7102 0.5493 0.5999 −0.9669
is zero and that respiration represents dissipated energy (i.e.,
b −0.0641 0.1871 0.0002 6.8672
r2 0.5555 0.6131 0.7431 0.6247 energy that is not involved in production), the energy in reserve is
p 0.148 0.117 0.06 0.112 derived from internal flows and is represented by the redundancy
F 3.7491 4.7535 8.6755 4.9931 of flows, which also expresses ecosystem resilience (Ulanowicz
df 4 4 4 4
et al., 2009; Costanza, 2012). According to Ulanowicz et al. (2009),
RMSr 0.5212 0.4629 0.3426 0.4516
the resilience, self-organization capacity and sustainability of an
a and b, regression parameters; r2 , determination coefficient; p, probability of sig- ecosystem are related concepts. From the perspective of the redun-
nificance. None of the relationships was statistically significant (p < 0.05) due to the
few degrees of freedom.
dancy of flows, this energy in reserve represents the probability that
a unit of energy will move to any given destination in the food web
ecosystem vulnerability was related to high complexity in terms when necessary to compensate for energy loss and maintain the
of connectance, ecosystem efficiency (P/R) and net system produc- dynamic balance. This probability is associated with uncertainty
tion (NSP), resulting in positive slopes, but was inversely related to that depends on the organization of the system and on the part
energetic cost (R/B). The behavior of these ecosystem attributes is of the ecosystem (food web) that is perturbed. When a system is
well known in ecology (Odum, 1971; Margalef, 1974). disturbed, the energy flows become more uncertain relative to the
state of dynamic balance. This increased uncertainty is associated
4. Discussion with redundancy. Thus, the difference between the uncertainty of
the disturbed state and that of the state of dynamic balance repre-
The current concern about ecosystem vulnerability is supported sents the increase in entropy. In our experiments, if we compute the
by the possible negative consequences of ecological changes for the values of order (A/C) and entropy (1 − A/C) for the state of dynamic
availability and use of ecosystem goods and services. Vulnerability balance, then the negative difference in A/C measures the effect of
studies are generally based on the assumption that ecosystems are the disturbance or the entropy gained due to the disturbance.
in a state of dynamic balance, and this assumption is necessary In our simulations, not all of the functional groups in an
for reference or comparative purposes. In thermodynamic terms, ecosystem generate entropy when perturbed. For example, Fig. 4
dynamic balance does not imply a steady state; within certain lim- shows that entropy decreases when some groups are disturbed.
its, variability is accepted as part of ecosystem dynamics. Outside Which groups will generate or reduce entropy when perturbed
of these limits, a disturbed state is considered to exist. This vari- depends on the intrinsic organizational characteristics of the
ation represents the stochastic processes of the interaction of the ecosystem. However, identifying the groups whose perturbation
dynamics between populations and ecosystem levels which could will tend to generate entropy in the ecosystem is important
be globally characterized as “natural stochastic noise” where the because this knowledge can facilitate precautionary management,
significant perturbations will incorporate additional noise outside thus preventing undesired effects on the ecosystem. For example,
such natural limits. Stochastic population dynamics and its effect if a group whose perturbation will generate entropy is heavily
on ecosystems have been approached by Powell and Boland (2009) exploited, then managers should establish measures to control
and Livi et al. (2011), who demonstrate the need of explicit study this exploitation. Also, in this context, a given species cannot
of variability. In our context, even when we do not approach to be expected to behave identically in two different ecosystems.
an assessment of this variability, its characterization represents Therefore, different management schemes must be formulated
the knowledge of the processes behind the dynamic balance that based on the species’ role in each ecosystem.
govern ecosystem evolution. Regarding the relationship between the relative increase in
Additionally, we focus our approach to vulnerability under a entropy due to perturbation and the TL of the perturbed group,
thermodynamic framework, characterized by the flows of energy our results show a general pattern of negative slopes, indicating
in the food web; that is, on the ecosystem metabolism. However that disturbances at lower TLs cause higher entropy compared to
the maintenance of ecosystem order do not depends only on these disturbances at higher TLs. From a food-web perspective, lower
energy flows, there are other mechanisms relevant to ecosystem TLs perturbed, through their direct and indirect connections, have
functioning such as pollination, planktonic larvae dispersion, etc., stronger effects on the organization of the network. In particu-
that are critical to maintain populations and ecosystem order in lar, lower TLs serve as the energy sources (or are near the energy
consequence. sources) for the ecosystem. However, Fig. 4 clarifies that the dif-
Our purpose here is to show, in a deterministic way, a ference in order (represented by the length of the vector) is larger
functional measure of vulnerability based in ecosystem thermo- for lower TLs perturbed than for high TL’s. This is because for low
dynamic processes, supported theoretically through the dynamics trophic level the higher intrinsic growth rate provoke a quick recov-
of metabolism, but we are not including the study of stochastic pro- ery causing a delay in the effect of disturbance. This is not the
cesses or mechanisms independent of energy flows that could be case for high TL’s, where slower growth rate does not permit a
of relevance for the maintenance of order of the ecosystem. recovery of production in the short time. This relationship suggests
Ulanowicz (1986) proposed that in terms of energy flows in the the hypothesis that this difference is a measure of the ecosystem’s
food web, ascendency represents ecosystem organization weighted resistance to perturbation, with higher TLs being less resistant to
by the total system flow (as a measure of magnitude), while perturbation. This hypothesis is consistent with reports in the lit-
overhead represents the energy in reserve within an ecosystem, erature regarding the sensitivity of ecosystems to overexploitation
being the sum of both (A and O) an estimate of the capacity of at high TLs (e.g., Pauly et al., 1998).
development or the maximum ascendency that an ecosystem can Furthermore, the gain in entropy indicates that ecosystems
reach. Therefore, if the energy in reserve is fully utilized for the respond differently according to the role of each functional group
organization and function of the system, the ecosystem will achieve in the organization of the ecosystem (Fig. 5, bottom). Therefore,
136 F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138

Table 4
Ecosystem statistics for the ecosystems selected as test cases. References are given in Table 1.

Terminos Lagoon Coral reef Campeche Sound N Gulf of Mexico Yucatan


continental shelf

Sum of all consumption 631.326 51,699.52 1679.565 1343.571 1050.104


Sum of all exports 2219.128 32,119.74 3651.79 430.096 1.933
Sum of all respiratory flows 368.262 24,904.01 1016.901 789.668 602.295
Sum of all flows into detritus 2684.243 58,816.88 4742.73 761.404 394.637
Total system throughput 5903 167,540 11,091 3325 2049
Sum of all production 2724 45,590 4994 1505 691
Calculated total net primary production 2587.39 30,123.75 4668.702 1219.764 454.228
Total primary production/total respiration 7.026 1.21 4.591 1.545 0.754
Net system production 2219.128 5219.738 3651.801 430.096 −148.067
Total primary production/total biomass 9.819 5.002 44.757 33.821 6.972
Total biomass/total throughput 0.045 0.036 0.009 0.011 0.032
Total biomass (excluding detritus) 263.519 6021.917 104.312 36.065 65.152
Connectance index 0.402 0.346 0.281 0.209 0.278
System Omnivory Index 0.187 0.242 0.172 0.134 0.195
Net system production/connectance index 5520.22 15,085.95 12,995.73 2057.88 −532.62
Respiration/biomass 1.40 4.14 9.75 21.90 9.24
Production/biomass 10.34 7.57 47.88 41.73 10.61

the gain in entropy is a measure of the sensitivity of the ecosystem immediate consequences, one that patterns resulting from our
to perturbation. According to some authors (e.g., De Lange et al., experiments are not directly applicable to testing hypotheses about
2010), vulnerability incorporates three aspects: exposure, which biodiversity, although the concept on how to address an anal-
here corresponds to the perturbation rate; sensitivity, which repre- ysis under this approach may be analogous to that proposed
sents the effect or impact; and resilience, which is described above. here. Second, the response of ecosystems to disturbances is typi-
According to these definitions, the information contained in the cally characterized by resilience, and the dynamics of vulnerability
slopes shown in Fig. 5, strongly suggests that these slopes provide associated ecosystem resilience may be somewhat different from
a relative measure of ecosystem vulnerability. choosing to work with functional groups or species, particularly
Fig. 5 suggests a gradient of slopes; the coral reef ecosys- regarding the redundancy of flows, central point resilience analysis
tem has the lowest slope (meaning higher vulnerability), followed (Ulanowicz, 2009). Moreover, analysis of order and entropy corre-
by the Yucatan continental shelf (characterized by hard-bottom sponds to a holistic ecosystem in such a manner that the inference
communities), Campeche Sound (a continental shelf characterized about particular species likely requires more information than that
by soft-bottom communities), northern Gulf of Mexico (a conti- provided in this analysis.
nental shelf ecosystem), and Terminos Lagoon (a coastal lagoon) The approach to the study of vulnerability in this holistic per-
which presents the lower vulnerability. The relationships for all spective, offers possibilities to support resource management and
ecosystems are significant (p < 0.05), suggesting the tendency of the conservation in terms of sustainability of the ecosystem, under
gradient is valid with the slope magnitude being inversely related the theoretical framework proposed by Ulanowicz (2002), rather
to vulnerability. than for individual species or groups. The concept of sustainability
To confirm that the pattern of relative vulnerability (i.e., the involves changes in populations and the ecosystem that are man-
slope gradient) shown in Fig. 5 is ecologically meaningful, we ifested in their function and organization (and where appropriate
evaluated the relationships between the slopes estimated from structure), and as a natural entity maintains a dynamic response
our simulations and selected ecosystem attributes reported by the tending to thermodynamic balance, which is in turn manifested as
authors who developed the ecosystem models (Table 1). The results variability eventually defining the evolution of ecosystems. In this
of these tests confirm our interpretations regarding ecosystem vul- sense, knowledge of the vulnerability associated with sustainability
nerability because they are consistent with ecological concepts in the context of use of living natural resources serve as reference to
found in the literature. For example, coral reef systems tend to be set strategies for resource management, which is properly defined
more vulnerable, and some of their attributes that are positively as adaptive management.
related to our vulnerability estimate include high connectivity, high In a broader context some of the results of the vulnerability anal-
production efficiency relative to energetic costs, and higher costs ysis can be of practical interest. For example, the significant changes
per unit of biomass. These indices correspond to the highest net in ascendency (organization) and in the order of the ecosystem, at a
production of coral reef ecosystems, as shown in Table 4. disturbance level of 40% (±15%), is an indication of a threshold level
In the experimental design we only consider changes in biomass for biomass extraction (e.g. for fishing), a harvesting level that pre-
and trophic flows, but not the changes in topology of the ecosystem. serves the integrity of the ecosystem (Figs. 2 and 3). This condition
The immediate consequence is that observed patterns of vulnera- is comparable to the concept of balanced harvesting mentioned by
bility do not necessarily apply to cases where there is reduction or Garcia et al. (2011, 2012), Zhou et al. (2010), Bundy et al. (2005),
increase in the number of species (nodes or functional groups). Sim- where the first of them suggested, under the criterion of maximum
ilarly, perturbations considered only for individual groups, but not biomass available in the ecosystem, a balanced harvest rate near to
for simultaneous disturbances. It was felt that such scenarios could 40%, as an average for 36 ecosystems analyzed.
multiply, mask or compensate some ecosystem-level processes. In Moreover, the vulnerability analysis let us identify functional
both cases, although the conceptual consideration of how to esti- groups that, when disturbed, promote gain in entropy, assumed
mate vulnerability is probably appropriate, the patterns of change here as analogous to ecosystem deterioration, and by contrary,
associated with topological changes of food webs, or the combined functional groups whose disruption cause no such deterioration.
effects between groups and intensities of disturbance should still This allows to define two aspects directly related to resource man-
be characterized. agement; on the one hand, the recognition, observation and control
Furthermore, in the case studies authors used functional groups, over those species which can cause ecosystem degradation; and
but not isolated species to build trophic models. This has two secondly, recognize that a given species can play a different role
F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138 137

in different ecosystems; which means that particular manage- of Mexico. J. Fish Boil. 53 (Suppl. A), 143–153, http://dx.doi.org/10.1111/
ment strategies should be developed for each ecosystem. In the j.1095-8649.1998.tb01024.x.
Bundy, A., Fanning, P., Zwanenburg, K.C.T., 2005. Balancing exploitation and conser-
Gulf of Mexico, for example, might cite the case of red snap- vation of the eastern Scotian Shelf ecosystem: application of a 4D ecosystem
per, Lutjanus campechanus, an economically highly appreciated exploitation index. ICES J. Mar. Sci. 62, 503–510, http://dx.doi.org/10.1016/
species in the entire gulf, with severe problems of overfishing j.icesjms.2004.12.008.
Browder, J., 1993. A pilot model of the Gulf of Mexico continental shelf. In: Chris-
in the Northern Gulf of Mexico; and also highly exploited in the tensen, V., Pauly, D. (Eds.), Trophic Models of Aquatic Ecosystems, vol. 26.
southern Gulf of Mexico, in the Campeche Sound and in the con- ICLARM Conference Proceedings, pp. 279–284.
tinental shelf of Yucatan. Even when the last two ecosystems are Chen, S., Fath, B.D., Chen, B., 2010. Information indices from ecological network
analysis for urban metabolic system. Proc. Environ. Sci. 2, 720–724.
neighbors, Arreguín-Sánchez and Manickchand-Heileman (1998)
Christensen, V., Walters, C.J., 2004. Ecopath with Ecosim: methods, capabili-
demonstrated the differential role of L. campechanus in ecosys- ties and limitations. Ecol. Model. 172, 109–139, http://dx.doi.org/10.1016/
tems and the management implications. This principle could also j.ecolmodel.2003.09.003.
Costanza, R., 1992. Toward an operational definition of ecosystem health, 239–256.
be applied for L. campechanus stock in the Northern Gulf of Mexico,
In: Constanza, R., Norton, B., Haskell, B.D. (Eds.), Ecosystem Health: New Goals
or even for other species. for Environmental Management. Island Press, Washington, DC, p. 281.
In practical terms, from a holistic context, knowledge of limits Costanza, R., Mageau, M., 1999. What is a healthy ecosystem? Aquat. Ecol. 33 (1),
of disturbance levels, measured through the loss of biomass (e.g. 105–115, http://dx.doi.org/10.1023/A:1009930313242.
Costanza, R., 2012. Ecosystem health and ecological engineering. Ecol. Eng. 45,
fishing), and the contribution of the functional groups to ecosys- 24–29, http://dx.doi.org/10.1016/j.ecoleng.2012.03.023.
tem vulnerability, and consequently to ecosystem deterioration De Lange, H.J., Sala, S., Vighi, M., Faber, J.H., 2010. Ecological vulnerability in risk
including the critical levels of disturbance, could permit the design assessment – a review and perspectives. Sci. Total Environ. 48, 3871–3879,
http://dx.doi.org/10.1016/j.scitotenv.2009.11.009.
of ecosystem-level strategies for resource management, in consis- Dulvy, N.K., Sadovy, Y., Reynolds, J.D., 2003. Extinction vulnerability in
tence with sustainability and ecosystem health criteria. marine populations. Fish Fisheries 4 (1), 25–64, http://dx.doi.org/10.1046/
j.1467-2979.2003.00105.x.
Eriksen, S.H., Brown, K., Kelly, P.M., 2005. The dynamics of vulnerability:
5. Conclusions locating coping strategies in Kenya and Tanzania. Geogr. J. 171, 287–305,
http://dx.doi.org/10.1111/j.1475-4959.2005.00174.x.
Garcia, S.M., Kolding, J., Rice, J., Rochet, M.J., Zhou, S., Arimoto, T., Beyer, J., Borges,
Vulnerability of an ecosystem can be measured through L., Bundy, A., Dunn, D., Graham, N., Hall, M., Heino, M., Law, R., Makino, M.,
metabolic changes expressed by flows of energy in trophic Rijnsdorp, A.D., Simard, F., Smith, A.D.M., Symons, D. (Eds.), 2011. Selective
networks. Ecosystem order is measured by the A/C ratio Fishing and Balanced Harvest in Relation to Fisheries and Ecosystem Sustaina-
bility. Report of a Scientific Workshop Organized by the IUCN-CEM Fisheries
(A = Ascendency, C = Capacity) and the inverse 1 − (A/C) represents Expert Group (FEG) and the European Bureau for Conservation and Develop-
entropy. These measures can be estimated through the ecosys- ment (EBCD) in Nagoya (Japan), 14–16 October 2010. IUCN and EBCD, Gland,
tem dynamics, where gain in entropy is of particular importance Switzerland and Brussels, Belgium, p. iv + 33.
Garcia, S.M., Kolding, J., Rice, J., Rochet, M.J., Zhou, S., Arimoto, T., Beyer, J.E., Borges,
since represents ecosystem deterioration. Under simulation exper- L., Bundy, A., Dunn, D., Fulton, E.A., Hall, M., Heino, M., Law, R., Makino, M.,
iments, when different functional groups are perturbed, some of Rijnsdorp, A.D., Simard, F., Smith, A.D.M., 2012. Reconsidering the consequences
them cause increase in entropy but other can cause increase in of selective fisheries. Science 335 (6072), 1045–1047.
Graham, N.A.J., Chabanet, P., Evans, R.D., Jennings, S., Letourneur, Y., Mac-
order. The slope between the gained entropy and trophic levels of Neil, M.A., McClanahan, T.R., Öhman, M.C., Polunin, N.V.C., Wilson, S.K.,
groups perturbed is interpreted as a measure of the relative ecosys- 2011. Extinction vulnerability of coral reef fishes. Ecol. Lett. 14, 341–348,
tem vulnerability; whose magnitude was found the be inversely http://dx.doi.org/10.1111/j.1461-0248.2011.01592.x.
Helpern, B.S., Selkoe, K.A., Micheli, F., Kappel, C.V., 2007. Evaluating and ranking the
related to complexity, showing, for ecosystems of the Gulf of
vulnerability of global marine ecosystems to anthropogenic threats. Conserv.
Mexico, a higher vulnerability for coral reefs, and lower for coastal Biol. 21 (5), 1301–1315, http://dx.doi.org/10.1111/j.1523-1739.2007.00752.x.
lagoons. This behavior is supported by general theory of trophic Hofman, M.A., Laan, A.C., Uylings, H.B.M., 1986. Bivariate linear models in neurobio-
networks. We discuss that this knowledge can be of relevance logy: problems of concept and methodology. J. Neurosci. Methods 18, 103–114,
http://dx.doi.org/10.1016/0165-0270(86)90114-7.
for living resources management; for example, a disturbance level Leduc, D.J., 1987. A comparative analysis of the reduced major axis tech-
(reduction of biomass) of 40% (±15%) can be taken as an indica- nique of fitting lines to bivariate data. Can. J. For. Res. 17 (7), 654–659,
tor of threshold level for biomass extraction (e.g. by fishing), after http://dx.doi.org/10.1139/x87-107.
Livi, C.M., Jordán, F., Lecca, P., Okey, T.A., 2011. Identifying key species in
such level, the loss of order (vulnerability increase) change sharply. ecosystems with stochastic sensitivity analysis. Ecol. Model. 222, 2542–2551,
This criterion is consistent with the ecosystem balanced harvesting http://dx.doi.org/10.1016/j.ecolmodel.2010.09.025.
concept reported in literature. The study of vulnerability as repre- Luers, A.L., Lobell, D.B., Sklar, L.S., Addams, C.L., Matson, P.A., 2003. A method
for quantifying vulnerability, applied to the agricultural system of the Yaqui
sented here permits the design of ecosystem-level strategies for Valley, Mexico. Glob. Environ. Change 13, 255–267, http://dx.doi.org/10.1016/
sustainable resources management. S0959-3780(03)00054-2.
Mageau, M.T., Costanza, R., Ulanowicz, R.E., 1995. The development and initial test-
ing of a quantitative assessment of ecosystem health. Ecosyst. Health 1 (4),
Acknowledgements 201–213.
Mageau, M.T., Costanza, R., Ulanowicz, R.E., 1998. Quantifying the trends expected
in developing ecosystems. Ecol. Model. 112 (1), 1–22, http://dx.doi.org/
Authors thank support through the projects SEP-CONACYT 10.1016/S0304-3800(98)00092-1.
(104974, 155 900), Gulf of Mexico LME (GEFMEX-09001), ANR- Manickchand-Heileman, S., Arreguín-Sánchez, F., Lara-Domínguez, A.L., Soto, L.,
CONACYT (111465), and SIP-IPN (20131266, 20144037). Also 1998. Energy flow and network analysis of Terminos Lagoon, SW Gulf
of Mexico. J. Fish Biol. 53 (Suppl. A), 179–197, http://dx.doi.org/10.1111/
thanks to the Ecopath Research and Development Consortium to j.1095-8649.1998.tb01026.x.
facilitate models’ files. FAS thanks the National Polytechnic Insti- Margalef, R., 1974. Ecología. Omega, Barcelona, pp. 951.
tute for its support through the EDI and COFAA programs, and TMRB Odum, E.P., 1971. Fundamentals of Ecology, 3rd ed. Saunders Co, PA, London, pp.
574.
thanks CONACyT by scholarship received. Authors dedicate this Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., Torres Jr., F., 1998. Fishing
contribution to the memory of Dr. Daniel Lluch Belda (1942–2014). down marine food webs. Science 279, 860–863, http://dx.doi.org/10.1126/
science.279.5352.860.
Pauly, D., Christensen, V., Walters, C., 2000. Ecopath, ecosim, and ecospace as tools
References for evaluating ecosystem impact of fisheries. ICES J. Mar. Sci. 57, 697–706,
http://dx.doi.org/10.1006/jmsc.2000.0726.
Arreguín-Sánchez, F., 2000. Octopus–red grouper interaction in the exploited Powell, C.R., Boland, R.P., 2009. The effects of stochastic population dynamics on
ecosystem of the northern continental shelf of Yucatan, Mexico. Ecol. Model. food web structure. J. Theor. Biol. 257, 170–180, http://dx.doi.org/10.1016/
129 (2), 119–129, http://dx.doi.org/10.1016/S0304-3800(00)00218-0. j.jtbi.2008.11.006.
Arreguín-Sánchez, F., Manickchand-Heileman, S., 1998. The trophic role of lut- Romieu, E., Welle, T., Schneiderbauer, S., Pelling, M., Vinchon, C., 2010. Vulnerabil-
janid fish and impacts of their fisheries in two ecosystems in the Gulf ity assessment within climate change and natural hazard contexts: revealing
138 F. Arreguín-Sánchez, T.M. Ruiz-Barreiro / Ecological Indicators 45 (2014) 130–138

gaps and synergies through coastal applications. Sustain. Sci. 5, 159–170, Ulanowicz, R.E., 2011a. The central role of information theory in ecology. In: Dehmer,
http://dx.doi.org/10.1007/s11625-010-0112-2. M., Emmert-Streib, F., Mehler, A. (Eds.), Towards an Information Theory of
Scotti, M., Jordán, F., 2010. Relationships between centrality indices and trophic Complex Networks: Statistical Methods and Applications. Springer, New York,
levels in food webs. Commun. Ecol. 11 (1), 59–67, http://dx.doi.org/10.1556/ http://dx.doi.org/10.1007/978-0-8176-4904-3.
ComEc.11.2010.1.9. Ulanowicz, R.E., 2011b. Quantitative methods for ecological network analysis and
Smith, R.J., 2009. Use and misuse of the reduced major axis for line-fitting. Am. J. its application to coastal ecosystems. Treatise Estuar. Coast. Sci. 9, 35–57,
Phys. Anthropol. 140, 476–486, http://dx.doi.org/10.1002/ajpa.21090. http://dx.doi.org/10.1016/B978-0-12-374711-2.00904-9.
Teck, S.J., Halpern, B.B.S., Kappel, C.V., Micheli, F., Selkoe, K.A., Crain, C.M., Martone, Venier, J., Pauly, D., 1997. Trophic dynamics of a Florida keys coral reef ecosys-
R., Shearer, C., Arvai, J., Fischhoff, B., Murray, G., Neslo, R., Cooke, R., 2010. Using tem. In: Lessios, H.A., Macintyre, I.G. (Eds.), Proceedings 8th International Coral
expert judgment to estimate marine ecosystem vulnerability in the California Reef Symposium, Smithsonian Tropical Research Institute, Panamá, vol. 1, pp.
current. Ecol. Appl. 20 (5), 1402–1416, http://dx.doi.org/10.1890/09-1173.1. 915–920.
Turner, I.I.B.L., Kasperson, R.E., Matsone, P.A., McCarthy, J.J., Corell, R.W., Chris- Walters, C., Christensen, V., Pauly, D., 1997. Structuring dynamic models of exploited
tensen, L., Eckley, N., Kasperson, J.X., Luers, A., Martello, M.L., Polsky, C., ecosystems from trophic mass-balance assessments. Rev. Fish. Biol. Fisher. 7 (2),
Pulsipher, A., Schiller, A., 2003. A framework for vulnerability analysis in 139–172, http://dx.doi.org/10.1023/A:1018479526149.
sustainability science. Proc. Natl. Acad. Sci. U.S.A. 100 (14), 8074–8079, Zacharias, M.A., Gregr, E.J., 2005. Sensitivity and vulnerability in marine environ-
http://dx.doi.org/10.1073/pnas.1231335100. ments: an approach to identifying vulnerable marine areas. Conserv. Biol. 19
Ulanowicz, R.E., 1980. An hypothesis on the development of natural communities. J. (1), 86–97, http://dx.doi.org/10.1111/j.1523-1739.2005.00148.x.
Theor. Biol. 85 (2), 223–245, http://dx.doi.org/10.1016/0022-5193(80)90019-3. Zetina-Rejón, M.J., Arreguín-Sánchez, F., 2003. Flujos de energía y estructura trófica
Ulanowicz, R.E., 1986. Growth and Development: Ecosystem Phenomenology. de la Sonda de Campeche, Suroeste del Golfo de México. In: Wakida Kusunoki,
Springer-Verlag, New York, USA. A., Solana Sansores, R., Uribe Martínez, J.A. (Eds.), Memorias del III Foro de
Ulanowicz, R.E., 2002. The balance between adaptability and adaptation. BioSystems Camarón del Golfo de México y del Mar Caribe. INP-SAGARPA y Gob. del Estado
64, 13–22, http://dx.doi.org/10.1016/s0303-2647(01)00170-8. de Campeche, México, pp. 55–62.
Ulanowicz, R.E., Goerner, S.J., Lietaer, B., Gomez, R., 2009. Quantifying sustainability: Zhou, S., Smith, A.D.M., Punt, A.E., Richardson, A.J., Gibbs, M., Fulton, E.A., Pascoe, S.,
resilience, efficiency and the return of information theory. Ecol. Complex. 6, Bulman, C., Baylissa, P., Sainsbury, K., 2010. Ecosystem-based fisheries manage-
27–36, http://dx.doi.org/10.1016/j.ecocom.2008.10.005. ment requires a change to the selective fishing philosophy. Proc. Natl. Acad. Sci.
Ulanowicz, R.E., 2009. The dual nature of ecosystem dynamics. Ecol. Model. 220 (16), U.S.A. 107 (21), 9485–9489, http://dx.doi.org/10.1073/pnas.0912771107.
1886–1892, http://dx.doi.org/10.1016/j.ecolmodel.2009.04.015.

Das könnte Ihnen auch gefallen