ICES Journal of Marine Science, 62: 453e458 (2005)
doi:10.1016/j.icesjms.2004.12.004
Ecological indicators based on fish biomass distribution
along trophic levels: an application to the
Terminos coastal lagoon, Mexico
Atahualpa Sosa-López, David Mouillot, Thang Do Chi,
and Julia Ramos-Miranda
Sosa-López, A., Mouillot, D., Do Chi, T., and Ramos-Miranda, J. 2005. Ecological
indicators based on fish biomass distribution along trophic levels: an application to the
Terminos coastal lagoon. e ICES Journal of Marine Science, 62: 453e458.
Cumulative relative biomass trophic level spectra (BTLS) are constructed for the fish
community of a tropical coastal lagoon in Mexico to analyse spatio-temporal patterns as
a potential ecosystem indicator of multifactor impacts. Data were based on monthly trawl
surveys over a single year carried out eighteen years apart. The spectra show significant
differences between the two periods, indicating major shifts in the trophic structure of the
system. Specifically, biomass of the omnivorous, estuarine species in the middle of the
foodweb (originally dominating) has been replaced by carnivorous and herbivorouse
detritivorous species. As a consequence, the initial sigmoid shape of the BTLS has tended
to become more linear. However, interpretation of the causes involved remains unclear. It is
suggested that this potential indicator of trophic status of the fish community reflects
a combination of interacting driving forces acting simultaneously in the lagoon: (i)
increased marine conditions as well as artificial reefs constructed in adjacent zones may
enhance biomass of marine predators and detritivorous species; (ii) attenuation of estuarine
influences may lead to decreasing biomass of estuarine generalist species; and (iii) the
establishment of a marine protected area may increase predator biomass, causing a decline
in prey biomass.
Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: coastal lagoon, cumulative relative biomass trophic level spectra, fish diet,
habitat impact, marine protected area, shrimp-trawl survey.
A. Sosa-López and J. Ramos-Miranda: Centro de Ecologı́a, Pesquerı́as y Oceanografı́a de
Golfo de México (EPOMEX), Universidad Autónoma de Campeche, Av. Agustı́n Melgar
s/n, Campeche, México 24030. D. Mouillot and T. Do Chi: UMR CNRS-UMII 5119,
‘‘Ecosystemes Lagunaires’’ cc 093, Université Montpellier II, 340595 Montpellier Cedex 5,
France. Correspondence to A. Sosa-López: tel: C52 9818 111600; fax: C52 9818 119800;
e-mail: atahsosa@uacam.mx.
Introduction
Among the long list of human influences on aquatic
ecosystems, climate change, exchange of biota, habitat
degradation, and fishing activities are important (Murawski, 2000; Nystrom et al., 2000; Jackson et al., 2001;
Hughes et al., 2003). Fishing-induced changes in abundance and spatial distribution of fish can have vital impacts
on species interactions (Garrison and Link, 2000), and the
trophic structure of a system in general. Therefore,
studying the spatial and temporal evolution of fish
communities may help to understand the impact of
anthropogenic activities.
Owing to their position between terrestrial, freshwater,
and marine interfaces, coastal lagoons, like estuaries or
1054-3139/$30.00
coastal wetlands, belong to the Critical Transition Zones
that provide essential ecosystem services to human
populations (Levin et al., 2001). Coastal lagoon areas
constitute 13% of the world’s coastline and are highly
productive (Knoppers, 1994). However, many of them are
under severe anthropogenic stress. Protected areas where
fishing and other human activities are regulated may
provide an ecosystem-level experimental framework to
study the persistence and stability of communities, and to
detect both direct and indirect effects of fishing (Mangel,
2000; Tuck and Possingham, 2000). Further, monitoring
reserves and adjacent unprotected areas over long periods
allows the differentiation of fishing effects from long-term
changes associated with other anthropogenic and natural
disturbances (Shears and Babcock, 2003).
Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
454
A. Sosa-López et al.
The Terminos lagoon is such a coastal lagoon (and
a marine protected area since the 1990s) in the southern
Gulf of Mexico (18e19(N 91e92(W), characterized by
various habitats that have been modified through many
years of human activities. During the past 20 years, the
lagoon has faced many anthropogenic impacts, specifically
in relation to the oil industry, human population growth,
deforestation of wetlands and mangroves, artificial reef
construction, and fishing activities on the adjacent shelf, as
well as changes in hydrological conditions, such as an
increase in salinity and temperature (Flores-Hernández
et al., 2000).
Trophodynamics represent a key component of the
functional role of the fish compartment in an ecosystem
(Cruz-Escalona et al., 2000; Hajisamae et al., 2004), and
trophic level is frequently applied as a simple descriptor of
the position of individual species in a foodweb (Froese
et al., 1992). Our objectives are (i) to present a new
ecological indicator of shifts, based on the fish biomass
distribution across trophic levels, (ii) to evaluate its spatial
and temporal variations in the Terminos lagoon, and (iii) to
discuss its ability to discriminate between several anthropogenic impact sources.
Material and methods
The analysis is based on monthly shrimp-trawl surveys
conducted within the Terminos lagoon (Figure 1) from
February 1980 to April 1981 (18 stations; Yáñez-Arancibia
and Day, 1988; Yáñez-Arancibia et al., 1988, 1993), and
from October 1997 to March 1999 (23 stations; RamosMiranda, 2000). For comparative assessments over space
and time, 17 stations (stratified by habitat units; YáñezArancibia and Day, 1988; Ramos-Miranda, 2000, Figure 1)
were selected; they had been fished throughout the period
FebruaryeJanuary in both 1980/1981 and 1998/1999.
Fish were identified to species level, counted, and
weighed to the nearest 0.1 g. Because direct observations
of diet compositions were not available, trophic level (TL)
was based on the FishBase ‘‘ecology table’’ (Pauly and
Christensen, 1995; Pauly et al., 2002; Froese and Pauly,
2003). This table provides information on TL for fish
species on the basis of reported diet composition by weight
or volume from stomach content studies, and also from
their food items. Although estimates based on detailed diet
composition data are obviously desirable (Froese et al.,
1992; Froese and Pauly, 2003), the TL of predators may
also be estimated (TL#) using a randomized re-sampling
routine based on the TL of food items that have been
observed in stomachs of a species or are otherwise known
to be eaten by that species. Applying this method for
species with known diet composition yielded the following
simple linear regression: TL Z 1.154TL#ÿ0.6 (r2 Z 0.76,
p ! 0.05). To standardize the results, this regression was
applied when TL was not known and only TL# was
available.
Because spatio-temporal dependence between years was
assumed and the data did not conform to normal distributions, we performed a univariate Wilcoxon signed-rank test
to analyse the biomass data (kg per sampling unit) by
species, and assessed the statistical significance of a change
Figure 1. Study area and location of the sampling sites: zones AeE refer to habitats described by Yáñez-Arancibia et al. (1988) and
Ramos-Miranda (2000); areas marked with vertical and inclined lines represent artisanal fishing and artificial reef areas, respectively.
Ecological indicators in Mexico’s Terminos coastal lagoon
(increase or decrease) of each species’ biomass between the
two periods.
Fish biomass-TL spectra were then constructed by
combining species by 0.5 TL interval for each zone
(AeE), and for each period. Mean TL values were compared
between years for each zone using a non-parametric
ManneWhitney Z-test. Finally, cumulative relative biomass
spectra along the TL gradient (BTLS) were smoothed by
weighted least squares (McLain, 1972). A Kolmogorove
Smirnov test (Zar, 1997) was performed between years, by
zone and for the pooled biomass across zones, to assess
differences in the general shape of the BTLS.
Results
According to the Wilcoxon signed-rank test, and of a total
of 106 fish species recorded, the biomass of 18 species
decreased significantly (11 with a p of !0.01; 7 with a p of
!0.05), and the biomass of 17 increased significantly (7
with a p of !0.01; 10 with a p of !0.05) between the two
periods analysed. In addition, 16 species were caught only
during the first period and 27 only during the second.
Trends for species representing the highest biomasses
caught are shown in Figure 2. Among the species that
increased were common predators such as Synodus foetens,
Trichiurus lepturus, and Centropomus parallelus. Biomass
of detritivorous gerreid species such as Diapterus rhombeus
and Eugerres plumieri also increased significantly. Species
that decreased in biomass mostly belonged to the TL range
Synodus foetens (4.5)
CARNIVORY
Trichiurus lepturus (4.45)
Centropomus parallelus (4.28)
Bairdiella chrysura (4.0)
Bairdiella ronchus (3.65)
Menticirrhus saxatilis (3.58)
Achirus lineatus (3.58)
Cynoscion nebulosus (3.5)
Citharichthys spilopterus (3.5)
Urolophus jamaicensis (3.42)
Chilomycterus schoepfi (3.3)
Arius felis (3.29)
Sphoeroides testudineus (3.24)
Eucinostomous argenteus (3.14)
Acanthostracion quadricornis (3.02)
HERBIVORY - DETRIVORY
Diapterus rhombeus (2.89)
Eugerres plumieri (2.6)
Cetengraulis edentulus (2.0)
0
1980/81
1998/99
15
30
45
60
75
90
105
TOTAL BIOMASS (kg)
Figure 2. Total biomass by year for species with an annual
biomass R 1 kg that have shown significant changes (numbers in
parenthesis indicate trophic level).
455
between 3 and 4 (Acanthostracion quadricornis, Sphoeroides testudineus, Arius felis, Chilomycterus schoepfi,
Citharichthys spilopterus, Achiurus lineatus, and Cynoscion nebulosus). In contrast to other sciaenid species,
Bairdiella chrysoura also showed a negative trend.
Differences between mean TL during the two periods
were significant (ManneWhitney; p ! 0.05) for all zones
except D (Figure 3): an increase was observed for zone C,
and decreases in zones A, B, and E. Results for the pooled
biomass largely follow the increase in zone C, because of
its large biomass (average 158 kg). The lowest biomass was
in zone E (34 kg), followed by zones D (37 kg), A (39 kg),
and B (87 kg). The biomass decreased by R 50% in zones
B, C, and D, whereas zones A and E exhibited a small
increase. Pooled biomass decreased from 430 to 286 kg.
The cumulative relative biomass trophic level spectra
(BTLS) showed highly significant (p ! 0.001) differences
in shape between years for zones B to E, and significant
(p ! 0.05) differences for zone A and the pooled biomass
(Figure 4). The general tendency in most zones was
a change from a strong sigmoid pattern during the first
period to a more linear pattern during the later period,
especially for zones B and D. The BTLS for the pooled
biomass exhibits the same trend, but less markedly because
of the strong influence of zone C and its high biomass.
Discussion
Based on the results of the analysis (Figures 3 and 4), there
have been marked changes in the trophic structure of the
Terminos lagoon fish community within little more than
a decade, indicating a re-allocation of biomass from species
characterized by intermediate trophic levels to carnivorous
and herbivorousedetritivorous species. Although not
shown, we did not find a strong seasonal signal in the
BTLS, suggesting that the shape is consistent across short
periods. This would make it a robust ecological indicator of
the trophic structure in the fish community and long-term
changes therein.
According to Ley et al. (1994), estuarine fish are
generally omnivorous, sharing common resources and
being flexible in their exploitation of temporary peaks in
prey populations. Many of the most abundant Terminos
lagoon fish are typically mid-trophic level, estuarine
species, and their decline between the periods investigated
is largely responsible for the overall reduction in fish
biomass (Figures 2 and 3). In zone C, the increase of marine
predatory species was more pronounced than in the zones
under the influence of river run-off (A and E), and along the
inner island (B). Zones A and E appear to follow the
patterns of gradually decreasing trophic level of global
catches (Pauly et al., 1998). This might be explained by
increasing bycatch in the intensive artisanal shrimp fishery
that is developing on the western continental shelf adjacent
to the lagoon, or by the change in hydrological conditions
456
A. Sosa-López et al.
125
100
ZONE A
Mean ± s.d.
(*)
1980/81 3.41 ±0.35
1998/99 3.21 ±0.41
ZONE B
Mean ± s.d.
(**)
1980/81 3.15 ±0.48
1998/99 3.12 ±0.72
ZONE D
Mean ± s.d.
ZONE E
Mean ± s.d.
(**)
1980/81 3.53 ±0.47
1998/99 3.27 ±0.56
ZONE C
Mean ± s.d.
(**)
1980/81 3.00 ±0.58
1998/99 3.17 ±0.63
75
25
0
125
100
75
1980/81 3.41 ±0.46
1998/99 3.43 ±0.85
POOLED
Mean ± s.d.
(**)
1980/81 3.16 ±0.55
1998/99 3.21 ±0.64
280
240
200
160
120
50
80
25
Pooled catch(kg)
Total catch (kg)
50
40
0
0
2
2.5
3
3.5
4
4.5
2
2.5
3
3.5
4
4.5
2
2.5
3
3.5
4
4.5
Trophic level
Figure 3. Biomass trophic level spectra (*, **: significant differences at p ! 0.05 and p ! 0.01, respectively, using two-sample
ManneWhitney test; grey bars, 1980e1981; white bars, 1998e1999).
Further, the increased influence of marine conditions
may have enhanced the entry of marine predatory species
(especially snappers and small schoolers) in the eastern part
of the lagoon ecosystem, as well as the construction of
that seem to show that the amount of seawater entering the
lagoon is increasing (Flores-Hernández et al., 2000). This
may have restricted the distribution of estuarine species
largely to the zones under influence of river run-off.
ZONE A
100
ZONE B
ZONE C
75
50
25
p<0.001
p<0.05
p<0.001
0
Accumulated
100
ZONE D
ZONE E
POOLED
75
50
25
0
p<0.001
2
2.5
3
3.5
4
4.5
p<0.001
2
2.5
3
3.5
4
4.5
p<0.05
2
2.5
3
3.5
4
4.5
Trophic level
Figure 4. Cumulative relative biomass trophic level spectra (circles, continuous lines, 1980e1981; squares, dashed lines, 1998e1999;
lines smoothed by weighted least-squares method; significant shape differences based on the KolmogoroveSmirnov two grouped-samples
test).
Ecological indicators in Mexico’s Terminos coastal lagoon
artificial reefs constructed on the eastern coastal shelf, as
has been reported for other coastal areas (Santos and
Monteiro, 1998).
The significant increase of detritivores (gerreids) might
be a response to a loss of submerged vegetation either
caused by physical disturbance by intensive shrimp trawling
during the 1980s (cf. Rueda and Defeo, 2003), or by toxic
pollutants drained into the lagoon (Chesworth et al., 2004).
Although the loss of submerged vegetation has not been
well studied in the lagoon, the increase in gerreids accords
with the expected fish community adjustment in response to
high fishing pressure (Albaret and Laë, 2003). Also, the
significant decrease of species associated with submerged
vegetation (e.g. S. testudineus and A. quadricornis) points in
this direction, because they appear to be sensitive to organic
waste (Connolly, 1999). However, there is an obvious need
to study abundance and distribution of seagrass beds and
mangrove forests, to clarify relationships between fish and
habitat changes in the area.
We have assumed that most fish inhabiting the lagoon are
juveniles that use it as a nursery area and do not exhibit
major trophic changes. This assumption is consistent with
the view that herbivorous fish species do not change trophic
status during ontogeny, although carnivorous fish may feed
on gradually larger prey (at correspondingly higher trophic
levels), before they migrate out to the open sea (Cocheret
de la Morinière et al., 2003).
Based on the results presented and the history of the
Terminos lagoon, the trophic status of the fish community
appears to reflect the forces acting upon the system
simultaneously. Three types of force can be distinguished:
(i) those enhancing biomass of marine predators and
detritivorous species (increased marine conditions, artificial
reefs, and trophic adjustment after intensive fishing); (ii)
those leading to a decrease in the biomass of estuarine
generalist species (attenuation of estuarine conditions,
fishing pressure on the adjacent estuarine shelf); and (iii)
those favouring an increase in predator biomass and
subsequent decrease of prey (marine protected areas;
Macpherson et al., 2002; Salomon et al., 2002).
Although the BTLS has not allowed us to draw firm
conclusions about whether the ecological status of the
lagoon has recovered or even improved, the indicator might
be useful for tracking changes in the trophic structure that
reach beyond simple changes in mean trophic level. The
different shapes observed might elucidate the array of
effects of ecosystem disturbances that are acting simultaneously, but interfere with ecological processes at different
trophic levels, then spread through the system by triggering
top-down or bottom-up controls. This clearly deserves
a more thorough evaluation before shapes can be linked to
specific impacts. Now that it is a marine protected area, the
Terminos lagoon may be a good experimental area to
continue such investigations. Also, the approach might
provide other ecologists with an opportunity to address
a variety of questions on changes and differences in
457
community structure, and their relationships with environmental and human influences.
Acknowledgements
The authors thank the IOC-SCOR Working Group 119,
organizers of the symposium, as well as UMR CNRS-UMII
5119, ‘‘Ecosystemes Lagunaires’’ Université Montpellier
II, for financial support. We also thank Tropical Fisheries
Resources area from EPOMEX, University of Campeche,
for permission to use the 1997e1999 database. Valuable
comments from two referees greatly helped to improve the
manuscript.
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