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Estuarine, Coastal and Shelf Science xx (2006) 1e8
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Feeding ecology and trophic relationships of fish species in the
lower Guadiana River Estuary and Castro Marim e Vila Real
de Santo António Salt Marsh
Rita Sá*, Constança Bexiga, Pedro Veiga, Lina Vieira, Karim Erzini
Centro de Ciências do Mar (CCMAR), Universidade do Algarve, 8000-117 Faro, Portugal
Received 1 February 2005; accepted 18 October 2005
Abstract
In this study we analyze the feeding ecology and trophic relationships of some of the main fish species (Soleidae, Moronidae, Mullidae,
Sparidae, Mugilidae, and Batrachoididae) of the lower Estuary of the Guadiana River and the Castro Marim e Vila Real de Santo António
Salt Marsh. We examined the stomachs of 1415 fish caught monthly between September 2000 and August 2001. Feeding indices and coefficients
were determined and used along with the results of multivariate analysis to develop diagrams of trophic interactions (food webs). Results show
that these species are largely opportunistic predators. The most important prey items are amphipods, gobies (Gobiidae), shrimps (Palaemon
serratus and Crangon crangon), and polychaete worms. The lower Estuary and associated salt marshes are important nurseries and feeding
grounds for the species studied. In this area, it is therefore important to monitor the effects of changes in river runoff, nutrient input, and temperature that result from construction of the Alqueva Dam upstream.
Ó 2006 Elsevier Ltd. All rights reserved.
Keywords: stomach contents; trophic guilds; multivariate analysis; Guadiana Estuary
1. Introduction
Studies of feeding habits and diet are the key to understanding many aspects of the biology, ecology, physiology, and behaviour of fish (Rosecchi and Nouaze, 1987; Gonçalves and
Erzini, 1998). Given the inherent difficulties of in situ observation of feeding habits of particular species, the analysis of
stomach contents has become the most widely used method
for studying the diet of fish (Valente, 1992). Stomach content
analysis has been used to describe the diet of individual fish
belonging to a population, to examine ecological niche overlap
and competition between predators (Lawror, 1980; Graham
and Vrijenhoek, 1988), investigate intra- and inter-specific interactions (Forney, 1977), and determine the role of a species
in the food chain (Hyslop, 1980; Valente, 1992); such analysis
* Corresponding author.
E-mail address: [email protected] (R. Sá).
0272-7714/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2006.05.038
plays an important role in multi-species fisheries models
(Gulland, 1977, 1983; Caddy and Sharp, 1988; Daan, 1989;
Hislop et al., 1991).
Fish have the potential for integrating different aspects of
their habitat(s) at spatial and/or temporal scales because of
their mobility and longevity. Thus, fish diet reflects the available prey, and a fish can be considered a sampling tool whereby
the stomach contents represent a sample of the prey items
available in the aquatic environment (Wootton, 1990).
To date, there are no studies of the feeding ecology and trophic interactions of fish species of the Guadiana River Estuary,
despite the fact that this is the most important river in southern
Portugal, with a catchment area of approximately 67,000 km2
(González, 1995). In 2002, the Alqueva dam was completed,
creating the largest man-made lake in Europe, with a storage
capacity of 4.1 109 m3. The volume of this dam represents
an increase of approximately 43% in terms of the water retained in dams along the Guadiana River. It is possible that
the dam has a significant impact on the biota of the downstream
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estuary and salt marshes due to the expected reduction in mean
flow (60% of the 50-year mean), nutrients, and organic matter
as well as changes in the seasonal flow and a decrease in extreme flow events (Charneca and Silva, 2003; Erzini, 2005).
The present study took place within the framework of
a baseline study of the ichthyofauna of the lower Estuary of
the Guadiana River and the Castro Marim e Vila Real de Santo
António Salt Marsh prior to completion of the Alqueva dam.
The objective is to study the feeding ecology of some of the
main fish species over an annual cycle, to investigate trophic
interactions, and to evaluate the importance of the lower estuary and salt marsh as habitats and feeding grounds for the different species. The data obtained will be essential for
monitoring the impacts of the Alqueva dam on the fish and
fisheries of the lower estuary, the salt marsh, and adjacent
coastal waters.
2. Materials and methods
2.1. Study area
This study took place in the lower Estuary of the Guadiana
River, which originates in Spain, at 37 090 e37 400 N, 7 150 e
7 400 W. Morales-Gonazález (1995) and Chı́charo et al.
(2001) divided the estuary in three zones: low, middle and
high. The high estuary is defined as the freshwater section
where the salinity is zero; the middle estuary corresponds to
the transition zone where the water is brackish most of the
time; and the low estuary has a salinity similar to that of the sea.
The lower estuary can be divided into two main habitat
types: the salt marsh and the main river channel (Fig. 1).
The Castro Marim Salt Marsh on the Portuguese side and
the Ayamonte Salt Marsh on the Spanish side are protected
areas with nature reserve status. These salt marshes are important wintering grounds for many bird species, especially
waders, and are important spawning and nursery grounds for
numerous fish, mollusc, and crustacean species (Veiga et al.,
in this issue).
2.2. Sampling procedures and data analysis
Two different types of equipment were used for sampling:
a beach seine in the salt marsh and an otter trawl in the
main channel (Veiga et al., in this issue). The beach seine
was used in the salt marsh because of the confined nature of
the area and shallow depths, while the otter trawl was more
suitable for sampling the deep channel where currents were often strong. Sampling took place at night and low tide during
the last quarter of the lunar phase at six locations in the lower
estuary and four locations in the Castro Marim Salt Marsh. We
sampled on a monthly basis from September 2000 until August 2001.
Sampled fish were taken to the laboratory where they were
identified, counted, measured, and weighed. Stomachs were
removed and contents preserved in 4% buffered formalin for
later identification. Diet characterization was based solely on
the stomach contents to avoid overestimation of prey with
Fig. 1. Map of sampling sites in the lower Guadiana River and Castro Marim e
Vila Real de Santo António Salt Marsh. G e Guadiana river, CM e Castro
Marim Salt Marsh (adapted from Bexiga, 2002).
exoskeletons or other hard structures. The relative importance
of each prey item in the diet was expressed as a percent of numerical abundance (CN%), occurrence of food items in stomachs (CF%), and weight (CP%) (Hyslop, 1980).
Multivariate analyses were performed using the statistical
package PRIMER (Clarke and Warwick, 1994). For these
analyses, prey was grouped and data were root transformed,
as appropriate for percentage data (Platell and Potter, 2001).
We then calculated pairwise Bray-Curtis similarity coefficients, which provide a measure of dietary overlap (Marshall
and Elliott, 1997). Cluster analysis (using group-average linking based on Bray-Curtis similarities) was used to define trophic groups (guilds). The importance of prey taxa within
different guilds was assessed by SIMPER analysis, which determines those prey taxa responsible for the grouping of species categories in terms of Bray-Curtis mean similarity.
3. Results
Samples (1415 stomachs) were collected in all months from
September 2000 to August 2001 with the exception of December 2000. The sampling months were grouped by season for
posterior analysis. Taxonomic groups and corresponding species are provided in Table 1. As the number of stomachs per
species was not very high, the data were analysed by taxonomic group and in some cases by and between the most
representative species (n > 50).
The two species of soles (Soleidae) were grouped because
cluster analysis based on mean CN% for seasonal data shows
a high degree of similarity (93%), with no significant
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Table 1
Species of fishes of the lower Estuary of the Guadiana River. The most important species are italicized
Taxonomic Group Species
Number of
individuals
Percentage
Group Total Group Total
Soleidae
Moronidae
Mullidae
Sparidae
Mugilidae
Batrachoididae
Solea senegalensis
50
Solea vulgaris
57
Dicentrachus labrax
78
Dicentrarchus punctatus
5
Mullus surmeletus
125
Diplodus annularis
2
Diplodus bellottii
1
Diplodus sargus
119
Diploduds vulgaris
59
Sparus aurata
9
Spondyliosoma cantharus 17
Chelon labrosus
6
Liza aurata
26
Liza ramada
58
Liza saliens
6
Mugil cephalus
8
Halobatrachus didactylus 774
107
83
125
207
104
774
46.7
53.3
94.0
6.0
100.0
1.0
0.5
57.5
28.5
4.3
8.2
5.8
25.0
55.8
5.8
7.7
100.0
3.6
4.1
5.6
0.4
8.9
0.1
0.1
8.5
4.2
0.6
1.2
0.4
1.9
4.1
0.4
0.6
55.3
difference in the diet of the two soles (ANOSIM: r ¼ 0.057,
p ¼ 0.61). The main differences were due to Tanaidacea,
which according to SIMPER analysis accounted for 53.7%
of the dissimilarity of 22.56 between the two species. The
European sea bass (Dicentrarchus labrax) and the spotted
3
sea bass (Dicentrarchus punctatus) were the only representatives of the Moronidae sampled in this study. Only one species
of red mullet (Mullidae; Mullus surmuletus) and one species of
toadfish (Batrochoididadae; Halobatrachus didactylus) were
analysed. Although we studied six species of sea breams of
the family Sparidae, only Diplodus sargus and Diplodus vulgaris were caught in adequate numbers. Cluster analysis based
on mean seasonal values of CN% showed that the six species
of sea breams had a relatively high coefficient of similarity
(57%); however, significant differences in diet were found
(ANOSIM: r ¼ 0.204, p ¼ 0.03), with Amphipoda being the
prey item contributing most (14.2%) to the observed dissimilarity of 66.9 (Table 3).
The stomach contents of the grey mullets (Mugilidae) consisted only of undifferentiated organic matter. As these data
represent only one prey category, they cannot be analysed in
terms of feeding coefficients or by multivariate analysis, however, given the relatively large number of individuals analysed
(104) and the importance of mullets in the Estuary and Salt
Marsh, these data were included for the purposes of the overall
analysis.
Diet indices are provided in Tables 2 and 3. The analysis of
data for all fish predators showed significant differences
between the predator groups/species (ANOSIM: r ¼ 0.60,
p ¼ 0.01). As evident in Fig. 2, there are two main groups
of predators, with one comprising red mullet (Mullidae) and
soles (Soleidae), and the other Lusitanian toadfish
Table 2
Number coefficient (CN%), weight coefficient (CP%), frequency coefficient (CF%), feeding coefficient (Q), and Index of Relative Importance (IRI) of the identified
prey for Soleidae and Mullidae. The feeding coefficient (Q) was used to evaluate the relative importance of the different prey items in the diet: principal prey are in
italics, while secondary prey are in bold and occasional prey are in normal font
Prey
Actinaria
Amphipoda
Bryozoa
Carcinus maenas
Cereastoderme spp.
Cirripedia
Crangon crangon
Echinoidea
Gastropoda
Gobiidea
Holothuroidea
Insecta
Isopoda
Modiolus barbatus
Natantia n.i.
Others Bivalvia
Others Brachuyra
Others Curstacea
Others Teleostei
Teleostei eggs
Palaemon serratus
Pinnotheres pisum
Plant
Polychaeta
Tanaidacea
Soleidae
Mullidae
CN%
CW%
CF%
Q
IRI
CN%
CW%
CF%
Q
IRI
3.5
<0.1
3.3
0.1
11.6
73.0
0.3
30.0
22.4
2198.4
18.9
85.3
45.0
1613.6
4689.3
1.4
76.7
19.8
99.1
0.9
80.3
16.4
7605.0
17.2
14124.8
338.3
5.0
6.8
1.4
0.2
5.0
0.3
7.9
2.7
13.8
5.0
37.3
82.5
2.7
0.4
10.0
1.0
30.9
4
Table 3
Number coefficient (CN%), weight coefficient (CP%), frequency coefficient (CF%), feeding coefficient (Q), and Index of Relative Importance (IRI) for Moronidae, Sparidae, and Batrachoididae. The feeding
coefficient (Q) was used to evaluate the relative importance of the different prey items in the diet: principal prey are in italics, secondary prey are in bold, and occasional prey are in normal font
Prey
Sparidae
<0.1
1.1
<0.1
0.4
8.7
0.8
49.3
4.3
2.2
428.3
249.3
1.7
39.1
7.5
30.1
293.3
1403.8
3.2
8.9
8.6
28.2
104.0
15.4
2.4
0.2
0.1
7.5
3.2
2.3
0.3
117.2
8.0
2.4
0.6
6.5
1.4
19.2
0.4
1.2
14.2
<0.1
4.4
23.6
1.1
1.1
9.7
<0.1
5.2
335.2
0.4
6.0
365.7
8.3
4.7
15.1
38.9
195.5
3.6
0.8
9.7
3.0
42.5
IRI
Batrachoididae
CN%
CW%
CF%
Q
IRI
CN%
CW%
CF%
Q
IRI
0.3
52.7
2.2
<0.1
14.0
<0.1
0.3
15.4
2.1
<0.1
736.7
0.1
0.1
1026.2
4.7
15.9
0.2
10.9
3.1
175.2
5.3
1.7
0.3
0.3
1.1
0.1
0.1
0.6
3.5
3.6
0.2
2.7
0.2
8.3
1.8
10.5
0.1
0.1
2.1
2.3
4.8
0.2
0.1
0.1
0.5
0.1
<0.1
<0.1
0.5
0.5
0.2
0.3
<0.1
<0.1
0.1
2.8
<0.1
<0.1
69.4
6.2
6.6
2.1
1.4
1.7
2.1
0.3
0.7
1.7
4.5
4.5
1.4
6.3
1.0
0.7
4.2
6.6
0.3
0.3
21.7
13.6
25.3
0.3
<0.1
<0.1
0.5
<0.1
<0.1
<0.1
1.7
1.7
<0.1
0.9
<0.1
0.1
0.2
29.8
<0.1
<0.1
143.8
14.1
6.7
4.0
0.5
0.8
3.3
0.1
0.1
1.1
18.2
18.4
0.6
19.2
0.2
5.8
7.9
88.7
<0.1
<0.1
1550.1
115.4
14.3
1.1
39.2
1.1
17.9
1.9
559.2
1.2
957.3
4.3
15.3
0.4
4.5
1.3
19.8
0.2
69.0
0.5
393.7
0.3
22.3
13.5
25.5
302.1
913.7
2.6
0.2
3.3
0.5
9.2
0.5
0.1
0.7
0.5
7.3
8.3
8.2
0.4
0.3
1.5
0.2
<0.1
<0.1
0.8
0.1
28.1
1.4
9.0
0.1
0.1
0.4
<0.1
1.0
0.2
1.0
0.6
4.9
1.2
7.4
0.8
0.6
2.5
0.4
<0.1
<0.1
0.5
0.1
204.6
11.6
73.4
<0.1
<0.1
0.7
<0.1
0.5
<0.1
1.4
0.4
172.0
11.3
126.9
0.4
0.2
5.0
0.1
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Actinaria
Amphipoda
Bryozoa
Carcinus maenas
Cereastoderme spp.
Cirripedia
Crangon crangon
Echinoidea
Gastropoda
Gobiidea
Holothuroidea
Insecta
Isopoda
Modiolus barbatus
Natantia n.i.
Others Bivalvia
Others Brachuyra
Others Curstacea
Others Teleostei
Teleostei eggs
Palaemon serratus
Pinnotheres pisum
Plant
Polychaeta
Tanaidacea
Moronidae
CN%
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Fig. 2. Dendrogram based on average CN% for predators. Sol e Soleidae,
Mor e Moronidae, Mul e Mullidae, Spar e Sparidae, Bat e Batrachoididae.
(Halobatrachus didactylus), Dicentrarchus labrax, and the
Sparidae (Table 4). The latter group has greater feeding plasticity compared to the red mullet and soles, with the highly opportunistic Lusitanian toadfish, although benthic by nature,
being similar to the demersal sea bass and sea breams in terms
of diet. Table 3 shows that the soles and red mullet are the
predator groups that differ the least in terms of their diets,
while soles and European bass differ most.
As evident in Fig. 3, the diets of soles did not differ significantly over different seasons (coefficient of similarity of
91%). This was also the case for the red mullets, where the
clusters based on the mean CN% had a coefficient of similarity
of 68% (Fig. 5). For the sea basses, the main difference was
between spring and other seasons, with a coefficient of similarity of approximately 37% (Fig. 4). The sea bream (Fig. 6)
and Lusitanian toadfish (Fig. 7) diets during autumn differed
Table 4
SIMPER analysis results for total number of prey by predator. Mean dissimilarities are presented in parentheses for the combinations: Sol (Soleidae), Mor
(Moronidae), Mul (Mullidae), Sp (Sparidae), Bat (Batrachoididae)
Predators
Prey
Contribution
(%)
Cumulative
(%)
Sol & Mor (89.67)
Tanaidacea
Amphipoda
C. crangon
Polychaeta
Insecta
C. maenas
Polychaeta
C. crangon
Tanaidacea
P. serrratus
Amphipoda
Amphipoda
Tanaidacea
Polychaeta
Amphipoda
Amphipoda
Tanaidacea
Amphipoda
Insecta
Amphipoda
e
16.76
16.02
13.50
11.96
10.49
10.17
28.42
19.26
16.44
12.12
11.65
27.07
15.13
11.31
10.97
10.06
12.44
10.07
10.82
16.99
e
16.76
32.78
46.28
58.24
68.73
78.90
28.42
47.68
64.12
76.23
87.88
27.07
15.13
26.44
10.97
10.06
12.44
22.51
10.82
16.99
e
Sol & Mul (54.85)
Mor & Mul (71.66)
Sol & Sp (78.18)
Mor & Sp (76.92)
Mul & Sp (70.25)
Sol & Bat (83.11)
Mor & Bat (60.00)
Mul & Bat (73.48)
Sp & Bat (59.65)
5
Fig. 3. Dendrogram based on CN% for Soleidae. W: winter, Sp: spring.
from those during spring and summer, with a separation of
the two main clusters at similarities of approximately 55%
and 70%, respectively.
Comparison of the diets from five locations along a gradient
in the lower Estuary showed no significant differences for any of
the main taxonomic groups. The ANOSIM results were as follows: soles: r ¼ 0.154, p ¼ 0.79; sea basses: r ¼ 0.022,
p ¼ 0.52; red mullets: r ¼ 0.0, p ¼ 0.53; sea breams:
r ¼ 0.078, p ¼ 0.67; and Lusitanian toadfish: r ¼ 0.052,
p ¼ 0.65.
Fig. 8 contains a summary of the trophic relationships in
the lower Guadiana Estuary based on the diet analysis and
the classification of prey items as preferential or secondary.
Overall, the most important prey items for the ichthyofauna
of the lower Estuary of the Guadiana River are Amphipoda,
Carcinus maenas, Cerastoderma spp., Crangon crangon, Gobiidae, other Teleosts, fish eggs, Pelaemon serratus, plant
material, and Polychaeta.
4. Discussion
The multivariate analysis used in this study is similar to the
approach taken by Baldó and Drake (2002) in studying the fish
feeding habits of the Guadalquivir River Estuary in southern
Fig. 4. Dendrogram based on CN% for Moronidae. A: autumn, W: winter, Sp:
spring, Su: summer.
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Fig. 5. Dendrogram based on CN% for Mullidae. Su: summer, A: autumn.
Spain. The authors based their analysis on the traditional numeric, gravimetric, and frequency of occurrence indices, and
came to the conclusion that because of the degree of correlation, all were suitable for describing the structure of the community in terms of feeding.
In general, diet composition in terms of the main prey items
did not differ significantly over the course of the year, indicating that populations of the main prey species in the Guadiana
Estuary and Castro Marim Salt Marsh are fairly stable and
available year-round. The main prey species are amphipods,
Crangon crangon, Gobiidae, Pelaemon serratus, and polychaete worms: taxonomic groups that are common in
estuaries.
Although Tanaidacea were relatively important numerically
and in terms of frequency of occurrence, polychate worms
dominated the diet of Soleidae in terms of weight. These findings are in agreement with those of other studies on the feeding ecology of Solea vulgaris that reported Polychaeta,
Crustacea, and Mollusca to be the most important prey items
(Braber and DeGroot, 1973; Quiniou, 1978; Ramos, 1981; Lagardère, 1987; Costa, 1988; Henderson et al., 1992; Darnaude
et al., 2001).
Although sea basses (Moronidae) clearly showed a preference for the shrimp Crangon crangon, there was some variability in the diet, as reported previously (Anthouard et al.,
Fig. 6. Dendrogram based on CN% for Sparidae. Sp: spring, A: summer, Su:
autumn.
Fig. 7. Dendrogram based on CN% for Batrachoididae. Sp: spring, W: winter,
A: autumn.
1993; Begout Anras, 1995; Boujard et al., 1996). Sea bass
are highly adaptable and opportunistic feeders, preying on
whatever prey is particularly abundant (Boulineau-Coatanea,
1969; Kennedy and Fitzmaurice, 1972; Arias, 1980; Aranda
et al., 1999).
The diet of red mullet had little diversity, consisting almost
exclusively of small crustaceans, especially Crangon crangon.
Other authors have reported greater prey diversity: Bentes
(1996) for red mullet from the Algarve coastal zone, and
Gharbi and Ktari (1979) and Azouz (1974) in the Mediterranean. In the Guadiana River, the abundance of C. crangon
may be such that red mullets have no need to seek other prey.
The sea breams (Sparidae) are versatile predators that can
be considered omnivores or carnivores (Gonçalves and Erzini,
1998), feeding mainly on small prey. The observed seasonal
changes in the simple feeding coefficients can be explained
by the variation in temperature, with significant decreases in
feeding for temperatures below 16 C (Wassef and Eisawy,
1985). The ingestion of plant material, whether accidentally
along with other food (Gonçalves and Erzini, 1998) or deliberately as reported for Diplodus sargus juveniles (Whitehead
Fig. 8. Trophic relations based on the feeding coefficient (Q). Preferential prey
are indicated by bold arrows and secondary prey by hatched arrows.
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et al., 1984) distinguishes these species from all others in the
Estuary and Salt Marsh. Furthermore, Mann and Buxton
(1992) partly attribute the success of D. sargus in a wide variety of habitats to its capacity for the consumption of algae,
sea grasses, and associated epibenthic organisms.
The Lusitanian toadfish is an abundant and voracious predator that occupies the top of the estuarine food chain and plays
an important role in community structure and function (Costa
et al., 2000; Costa, 2004). Being demersal and of low mobility
(Whitehead et al., 1984), it feeds primarily on other demersal
and benthic species, namely Carcinus maenas, Gobiidae, and
Crangon crangon. These findings are in agreement with those
of Costa et al. (2000), Sobral (1981), and Costa (2004), who
reported that crabs are always the most important prey, while
fish and shrimp are of secondary importance.
The Guadiana lower Estuary and associated Salt Marsh are
important habitats for fish, especially as nurseries for juveniles
of a wide variety of marine species (Bexiga, 2002; Veiga et al.,
in this issue). The high observed densities are probably due to
the primary production and bacterial production resulting from
increased nutrient loading, organic matter loading, and estuarine stratification, and the refuge from predation afforded by
the high turbidity conditions associated with greater sediment
loads (Kimmerer, 2002a,b).
The favorable conditions outlined above may change with
the construction of the Alqueva dam, completed in 2002, creating the largest man-made lake in Europe. Changes in the
mean and seasonal flows and a reduction in extreme flow
events associated with operation of the dam are important in
terms of significant offshore and alongshore transport of freshwater, organic material, nutrients and sediments (LNEC,
2003). Peak flows will now occur from January to April instead of November to February, and there will be substantial
reductions in river flow from November to January. The new
water flow regime will result in a shift of peak flows to the
spring, coinciding with rather than preceding the spawning periods of many species that use the Estuary. The changes
brought about by the construction of the Alqueva dam, including a reduction in the nutrient and organic material input into
the Estuary and Salt Marsh, as well as possible changes in water temperature (Petts, 1989), are likely to have a significant
impact on the fish species, especially the planktivorous fish.
Although it is too early to know for sure, short to medium
term impacts are likely at the community level, especially in
terms of species composition (key prey), community structure,
and inter- and intra-specific relations (Sale, 1985; Ward and
Stanford, 1987). Thus, it is important to continue monitoring
the composition of the fish community and the diets of the
main species of the lower Estuary and Salt Marsh of the
Guadiana River.
5. Conclusions
Due to relatively low habitat diversity and depths in the
Guadiana Estuary compared to adjacent coastal zones, considerable overlap might be expected in terms of resource use by
similar species, however, this is not generally the case.
7
Although there was some overlap for very abundant prey species, involving opportunistic feeding by some predators, interspecific competition was not significant. The fish species of
the Guadiana Estuary are representative of a wide range of
ecological niches and have characteristically high trophic flexibility. The use of the Estuary and the Salt Marsh by the studied species is largely related to reproductive strategies, with
these habitats serving as important nurseries during the first
year of life.
The most important prey species in the Guadiana River Estuary and Castro Marim Salt Marsh are amphipods, shrimps
(Crangon crangon and Pelaemon serratus), gobies (Gobiidae),
and polychaete worms. These species may be sensitive to
changes in the ecosystem resulting from the construction of
the Alqueva dam, especially a reduction in the input of organic
material and changed river flow. Changes in the trophic structure may have a significant effect on the fish communities of
the lower Estuary and Salt Marsh.
Acknowledgements
This study was funded in part by the INAG as part of project ‘‘Estudo das condiç~oes ambientais no estuário do rio
Guadiana e zonas adjacentes’’. We would especially like to
thank Dr. A. Canário for coordinating the Universidade of
the Algarve component and the fishermen who carried out
the beach seining and trawling.
References
Anthouard, M., Kentouri, M., Divanach, P., 1993. An analysis of feeding activities of sea-bass (Dicentrarchus labrax, Moronidae), raised under different lighting conditions. Ichtyophysiologica Acta 16, 59e73.
Aranda, A., Sánchez-Vázquez, F.J., Madrid, J.A., 1999. Influence of water
temperature on demand-feeding rhythms in sea bass. Journal of Fish Biology 55, 1029e1039.
Arias, A., 1980. Crescimiento, régimen alimentario y reproducción de la dorada (Sparus aurata L.) y del robalo (Dicentrarchus labrax L.) en los esteros de Cádiz. Investigación Pesquera, Barcelona 44, 59e83 (in Spanish).
Azouz, A., 1974. Les fonds chalutables de la région nord de la Tunisie. 2. Potentialités de la pêche, écologie et répartition bathymétrique des poissons.
Bulletin de l’Institut National Scientifique et Technique d’Océanographie
et de Pêche de Salammbô 3, 29e94 (in French).
Baldó, F., Drake, P., 2002. A multivariate approach to the feeding habits of
small fishes in the Guadalquivir Estuary. Journal of Fish Biology 61,
21e32.
Begout Anras, M., 1995. Demand-feeding behaviour of sea bass kept in ponds:
diel and seasonal patterns, and influences of environmental factors. Aquaculture International 3, 186e195.
Bentes, L., 1996. Crescimento, reproduç~ao ecologia alimentar de Mullus surmuletus L. 1758, Salmonete, na Costa Sudoeste de Portugal. Licenciatura
thesis, Universidade do Algarve, Faro, Portugal, unpublished (in
Portuguese).
Bexiga, C.M.S., 2002. Comunidade ictiológica estuarina do Guadiana e Sapal
de Castro Marim. MSc thesis, Universidade do Algarve, Faro, Portugal,
unpublished (in Portuguese).
Boujard, T., Jourdan, M., Kentouri, M., Divanach, P., 1996. Diel feeding activity and the effect of time-restricted self-feeding on growth and feed conversion in European sea bass. Aquaculture 139, 117e127.
Boulineau-Coatanea, F., 1969. Régime alimentaire du bar (Dicentrarchus
labrax, Serranidae). Sur la côte atlantique bretonne. Bulletin du Museum
d’Histoire Naturelle, série 2 (41), 1106e1122 (in French).
ARTICLE IN PRESS
+
8
MODEL
R. Sá et al. / Estuarine, Coastal and Shelf Science xx (2006) 1e8
Braber, L., DeGroot, S.S., 1973. The food of five flat fish species (Pleuronectiformes) in the Southern North Sea. Netherlands Journal of Sea Research
6, 163e172.
Caddy, J.F., Sharp, G.D., 1988. An Ecological Framework for Marine Fishery
Investigations. FAO Fisheries Technical Paper 283, 152.
Charneca, N., Silva, S., 2003. Estudo das condiç~oes ambientais do estuário do
rio Guadiana e zonas adjacentes. 3a Fase, Relatório 224/03 e NTI. LNEC
(Laboratório Nacional de Engenharia Civil), Lisboa, 267 p (in Portuguese).
Chı́charo, M.A., Chı́charo, L.M., Galv~ao, H., Barbosa, A., Marques, M.H.,
Andrade, J.P., Esteves, E., Miguel, C., Gouveia, C., Rocha, C., 2001. Status
of the Guadiana Estuary (south Portugal) during 1996e1998: an ecohydrological approach. Aquatic Ecosystem Health 4, 73e90 (in Portuguese).
Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities: an Approach to Statistical Analysis and Interpretation. Natural Environmental
Research Council, Plymouth.
Costa, M.J., 1988. Écologie alimentaire des poisons de l’estuaire du Tage.
Cybium 12, 301e320 (in French).
Costa, J.L., 2004. A biologia do xarroco, Halobatrachus didactylus (Bloch and
Schneider, 1801), e o seu papel na estruturaç~ao e funcionamento das comunidades em que se insere; referência especial à populaç~ao do estuário do
Mira. Ph.D. dissertation, University of Lisbon, Lisbon, Portugal, unpublished, 925 p. (in Portuguese).
Costa, J.L., Silva, G., Almeida, P.R., Costa, M.J., 2000. Activity and diet of
Halobatrachus didactylus (Bloch and Schneider, 1801) adults in the Tagus
Estuary. Thalassas 16, 21e25.
Daan, N., (Ed.) 1989. Data Base Report of the Stomach Sampling Project,
1981. ICES Co-operative Research Report, 164, International Council
for the Exploration of the Sea, Copenhagen, 144 p.
Darnaude, A.M., Harmelin-Vivien, M.L., Salen-Picard, C., 2001. Food partitioning among flatfish (Pisces: Pleuronectiforms) juveniles in a Mediterranean coastal shallow sandy area. Journal of the Marine Biological
Association of the United Kingdom 81, 119e127.
Erzini, K., 2005. Trends in North Atlantic (Portugal) landings: evaluating the
relative importance of fisheries and environmental variables. Fisheries
Oceanography 14, 195e209.
Forney, J.L., 1977. Evidence of inter- and intra-specific competition as factor
regulating walleye (Sitzostedion vitem vitem) biomass in Oneida lake, New
York. Journal of the Fisheries Research Board of Canada 34, 1812e1820.
Gharbi, H., Ktari, H., 1979. Régime alimentaire des rougets (Mullus barbatus
Linnaeus, 1758 et Mullus surmuletus Linnaeus, 1758) du golfe de Tunis.
Bulletin de l’Institut National Scientifique et Technique d’Oceanographie
et de Pêche de Salammbô 1-4, 41e52 (in French).
Gonçalves, J.M.S., Erzini, K., 1998. Feeding habits of the two-banded sea
bream (Diplodus vulgaris) and the black sea bream (Spondyliosoma cantharus) (Sparidae) from the south-west coast of Portugal. Cybium 22,
245e254.
González, J.A.M., 1995. Sedimentologı́a del estuario del rı́o Guadiana (S.O.
España-Portugal). Industrias Quimicas y Basicas de Huelva e Universidad
de Huelva (in Spanish).
Graham, J.H., Vrijenhoek, R.C., 1988. Detrended correspondence analysis of
dietary data. Transactions of the American Fisheries Society 117, 29e36.
Gulland, J.A., 1977. Goals and Objectives of Fishery Management. FAO Fisheries Technical Paper 166, 14.
Henderson, P.A., James, D., Holmes, R.H.A., 1992. Trophic structure within
the Bristol Channel: seasonality and stability in Bridgewater Bay. Journal
of the Marine Biological Association of the United Kingdom 72, 675e690.
Hislop, J.R.G., Robb, A.P., Bell, M.A., Armstrong, D.W., 1991. The diet and
food consumption of whiting (Merlangius merlangus) in the North Sea.
Journal of Marine Science 48, 139e156.
Hyslop, E.J., 1980. Stomach contents analysis: a review of methods and their
applications. Journal of Fish Biology 17, 411e429.
Kennedy, M., Fitzmaurice, P., 1972. The biology of bass, Dicentrarchus
labrax, in Irish waters. Journal of the Marine Biological Association of
the United Kingdom 52, 557e597.
Kimmerer, W.J., 2002a. Effects of freshwater flow on abundance of estuarine
organisms: physical effects or trophic linkages? Marine Ecology Progress
Series 243, 39e55.
Kimmerer, W.J., 2002b. Physical, biological and management responses to variable freshwater flow into the San Francisco Estuary. Estuaries 25, 1275e1290.
Lagardère, J.P., 1987. Feeding ecology and daily food consumption of common sole, Solea vulgaris Quensel, juveniles on the French Atlantic coast.
Journal of Fish Biology 30, 91e104.
Lawror, L.R., 1980. Overlap, similarity and competition coefficients. Ecology
61, 245e251.
Mann, B.Q., Buxton, C.D., 1992. Diets of Diplodus sargus capensis and
Diplodus cervinus hottentotus (Pisces: Sparidae) on the Tsitsikamma coast,
South Africa. Koedoe 35, 27e36.
Marshall, S., Elliott, M., 1997. A comparison of univariate and multivariate numerical and graphical techniques for determining inter- and intraspecific
feeding relationships in estuarine fish. Journal of Fish Biology 51, 526e545.
Morales-Gonazález, J.A., 1995. Modelo de interacción de las corrientes de
marea en la desembocadura del estuario mesomareal del Rı́o Guadiana,
(S.O. España-Portugal). Geogaceta 18, 83e87 (in Spanish).
Petts, G.E., 1989. Perspectives for ecological management of regulated rivers.
In: Gore, J.A., Petts, G.E. (Eds.), Alternatives in Regulated River Management. CRC Press, Boca Raton, Florida, pp. 3e24.
Platell, M.E., Potter, I.C., 2001. Partitioning of food resources amongst 18 abundant benthic carnivorous fish species in marine waters on the lower coast of
Australia. Journal of Experimental Marine Biology and Ecology 261, 31e54.
Quiniou, L., 1978. Les poissons demersaux de la Baie de Douarnenez. Alimentation et ecologie. In: Thèse 3ème cycle, 224. Université de Bretagne
Occidentale (in French).
Ramos, J., 1981. Régimen y comportamiento alimentario del lenguado (Solea
solea L.) (Pises, Soleidae). Informes Técnicos del Instituto de Investigación Pesquera 83, 3e15 (in Spanish).
Rosecchi, E., Nouaze, Y., 1987. Comparison de cinq indices alimentaires
utilisés dans l’analyse des contenus stomacaux. Revue Travailles Institut
Pêches Maritimes 49, 111e123 (in French).
Sale, M.J., 1985. Aquatic ecosystem response to flow modification: an overview of the issues. In: Olson, F. (Ed.), Small Hydropower and Fisheries,
Symposium Proceedings. American Fisheries Society, Bethesda, Maryland, pp. 25e31.
Sobral, D., 1981. Contribuiç~ao para o estudo da ictiofauna bentónica do
estuário do rio Sado. Licenciatura thesis, University of Lisbon, Lisbon,
Portugal, unpublished (in Portuguese).
Valente, A.C.N., 1992. A alimentaç~ao natural dos peixes (métodos de estudo).
Instituto de Zoologia Dr Augusto Nobre, Universidade do Porto. Série
Monografias, 4 (in Portuguese).
Veiga, P., Vieira, L., Bexiga, C., Sá, R., Erzini, K. Structure and temporal
variations of fish assemblages of the Castro Marim Salt Marsh, southern
Portugal. Estuarine, Coastal and Shelf Science, in this issue.
Ward, J.A., Stanford, J.A., 1987. The ecology of regulated streams: past
accomplishments and directions for future research. In: Craig, J.F.,
Kemper, J.B. (Eds.), Regulated Streams: Advances in Ecology. Plenum
Press, New York, pp. 391e409.
Wassef, E.A., Eisawy, A., 1985. Food and feeding habits of wild and reared
gilthead bream Sparus aurata L. Cybium 9, 233e242.
Whitehead, P.J.P., Bauchot, M.-L., Hureau, J.-C., Nielsen, J., Tortonese, E.,
1984. Fishes of the North-Eastern Atlantic and the Mediterranean. Volumes I, II and III. Unesco, 1473 pp.
Wootton, R.J., 1990. Ecology of Teleost Fishes. Chapman and Hall, UK.
404 pp.