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Estuaries

Vol. 26, No. 4A, p. 938–948

August 2003

Food Availability and the Feeding Ecology of Ichthyofauna of a Ria Formosa (South Portugal) Water Reservoir SOFIA GAMITO1,*, ANA PIRES1, CRISTINA PITA2, and KARIM ERZINI2 1

Instituto do Mar (IMAR), Faculdade de Cieˆncias do Mar e do Ambiente, Universidade do Algarve, Campus de Gambelas, 8000-117 Faro, Portugal 2 Centro de Cie ˆncias do Mar (CCMAR), Faculdade de Cieˆncias do Mar e do Ambiente, Universidade do Algarve, Campus de Gambelas, 8000-117 Faro, Portugal ABSTRACT: The feeding habits of several fish species in a water reservoir of the Ria Formosa, Portugal, that has similar ecological characteristics to the outside tidal channels, were studied and compared with food availability. The gilthead seabream (Sparus aurata), the most abundant fish species, mainly selected gastropods and bivalves, although occasionally fish and small crustaceans such as tanaids, ostracods, and cumaceans were also selected. Polychaetes, although abundant in the environment, were not particularly selected by any of the fish species studied. The diets of all the species studied were characterized by a large variety of prey, allowing them to survive in environments of low diversity and poor stability, such as coastal lagoons. These fish are largely benthic feeders, essentially eating the epimacroinvertebrates and endomacroinvertebrates and, occasionally, fish. Diplodus vulgaris and Diplodus annularis preferentially selected gastropods and small crustaceans. Spondyliosoma cantharus generally preyed on crustaceans, including the highly mobile epifauna, the mysids, and decapods. Halobatrachus didactylus and Anguilla anguilla, had very diversified diets that included fish. Mullus barbatus were found to have selected all groups of crustaceans and also bivalves. Wrasses, gobies, and Diplodus sargus, all small-sized fish, singled out small crustaceans, gastropods, and bivalves. The Sparids were the least specialized predators, with broader niches than the other species. They preferentially selected molluscs, which were abundant in the environment. A large overlap of diets was observed and competition may be important when fish biomass is high.

The Ria Formosa in south Portugal is the westernmost formation in an almost continuous series of wetlands that run eastwards along the Gulf of Cadiz. It is a true barrier islands system, comprised of mainland, backbarrier lagoons, inlet deltas, barrier islands, and shoreface (Pilkey et al. 1989). The Ria Formosa extends for about 55 km, has an area of 160 km2, and is an important wetland area considered in the Ramsar Convention (Carp 1972; Ramsar site 212—http://www.ramsar.org/profilespportugal.htm) and as a Special Bird Protection Area by Community Directive 79/ 409/ EEC (European Economic Community). The ecological characteristics of the water reservoirs in the salinas and fish farms of the Ria Formosa are similar to those of the tidal channels, being extensions of the latter and dependent on the water renewal regime (Gamito 1994). Because of their size, these reservoirs are ideal sites for ecological studies. The feeding habits of the main fish species occurring in the water reservoir of a fish farm in the Ria Formosa near Olha˜o were studied, along with food availability. The reservoir had a daily water renewal, making it comparable to the tidal channels of the large and complex Ria Formosa lagoonal system. The objective was a complete study of the trophic relationships, with si-

Introduction Estuaries and coastal lagoons are characteristically highly productive and important as nursery grounds for fish and crustacean species, including many commercially valued species. Recruitment may be determined in part by trophic interactions, including competition and predation. In most cases little is known about ecosystem structure and functioning, especially in spatial and temporal terms (Paine 1996). The study of the feeding ecology of the main species, including prey abundance and prey selectivity, is an important first step to a more holistic understanding of the ecosystem and may provide a basis for improved management and conservation. Some studies on the feeding habits of coastal and lagoonal benthic feeding fish have been carried out, but these studies have generally focused on a few species of one family, and contain little or no information on food availability (Arias 1980; Ferrari and Chieregato 1981; Eisawy and Wassef 1984; Roblin and Brusle 1984; Wassef and Eisawy 1985; Rosecchi 1987; Drake and Arias 1989; Laffaille et al. 2001; Pita et al 2002). * Corresponding author: tele: 1 351 289 800976; fax: 1 351 289 818353; e-mail: [email protected]. Q 2003 Estuarine Research Federation

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Food Availability and Feeding, Ria Formosa

multaneous sampling of food availability (benthic invertebrates) and the feeding preferences of the fish predators, of this small-sized water reservoir. The preferential selection of food items by each group of fish, fish diet overlap, and niche breadth were analyzed. METHODS The water reservoir of the Aquamarim fish farm near Olha˜o, with an area of more than 1 ha, was divided with a 2 cm mesh net that was fixed at the bottom to prevent large fish from crossing from one side to the other. Only one side of the water reservoir, with an approximate area of 0.6 ha and a mean depth of 2 m, was studied. Abiotic and biotic parameters were monitored and analyzed during a period of 19 mo: May 1996–September 1997. All the sampling was done in the morning, between 0930 and 1230 hrs. Water samples were collected twice a month, during neap and spring tides. The water temperature, salinity, dissolved oxygen, and biochemical oxygen demand (BOD5) were determined with portable probes (temperature and salinity with a Electronic Switchgear probe, oxygen with a WTW Microprobe Oximeter OXI 196). Winkler bottles were kept in an incubation chamber for 5 d, at 208C for BOD determination. The macrobenthic fauna and the suprabenthos were collected every month, with the macrobenthos comprising the endofauna and the epifauna with small mobility, and the suprabenthos considered here as the highly mobile fauna, such as mysids, shrimps, crabs, and small fish that live near the bottom surface. The first group was collected with a corer and the sediment sieved with a 0.5 mm mesh sieve. Eight randomly placed corers of 0.01 m2 were used for each sampling session: 4 in the middle of the reservoir and 4 near the edge. The organisms were identified to the species level, counted, measured and the biomass and secondary production determined. The organisms were dried for 48 h at 608C, and burnt at 4508C, for 3 h. The production of the most abundant species was determined by the increment summation method (Winberg 1971) and the other species through production-to-biomass ratios taken from previous studies done at the Ria Formosa (Sprung 1994a). Two random sledge hauls were carried out at the same locations, covering an area of approximately 5.6 m2 each. A 50 cm wide, hand-pushed sledge equipped with a 1 mm mesh size net was used to collect fauna in the layer of water 0–20 cm above the bottom (adapted from Cunha et al. 1999). The organisms were identified, counted, measured, and weighed (dry weight). Every 3 mo, three samples of water were taken for pigment

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analysis and for zooplankton quantification. The chlorophyll a (chl a) and phaeopigments were determined by fluorometric analysis (Welschemeyer 1994). Samples of approximately 20 l of water were poured through a 60 mm mesh filter, and the organisms quantified. All organisms in every cell of a counting chamber, observed under a compound microscope, were counted and grouped in broad zooplanktonic groups. The biomass of these groups was determined using the conversion factors compiled by Sprung (1994b). Fish were captured by beach seine, hook and line, and, on the last occasion, gill net. Most of the sampling was carried out by repeated seining with a 50 m beach seine with a small mesh size. Given the relatively small area of the reservoir, the selective characteristics and length of the beach seine, good estimates of standing stock were expected. Fishing took place in August and December 1996, February 1997, and on a monthly basis May through October 1997. All fish were identified, measured (total length) to the nearest half cm, and weighed to the nearest g. Due to the low captures during June, July, and August 1997, the gut content analysis was not performed for those months. In October, the gut content analysis was also not performed due to the capture technique applied, the gill net, which implies that the fish remain in the nets during a long period of time. The gut content analysis was carried out with fish from 5 of the 9 sampling occasions, corresponding to the beach seine captures. The alimentary tracts of the most abundant fish species were removed immediately after harvesting and individually stored in 70 % alcohol. Whenever possible, a minimum of 10 fish from each species were analyzed on each sampling occasion. A total of 490 tracts were observed. Data relative to fewer than three fish per group, or to fish with a very different length or weight from the rest of the group, were not further analyzed. Although all prey were identified to the species level whenever possible, for simplicity, the data was organised in large taxonomic-functional groups as follows, A: small Crustacean: Tanaidacea, Ostracoda, and Cumacea; B: Amphipoda, Isopoda, and Insecta; C: Mysidacea; D: Decapoda; E: Gastropoda; F: Bivalvia; G: Annelida and Nemertina; H: Pisces. The biomass of each group of items, in dry weight, was estimated by multiplying the number of each prey species or taxa by their mean weight (estimated from macrofauna and suprabenthos data). Almost all prey items were broken into small pieces, making it impossible to estimate their weight by direct weighing. The macrofauna and suprabenthos data was organised in the same large taxonomic-functional groups, converting the ash-free dry weights

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TABLE 1. Observed mean values of chlorophyll a (mg m23) and biomass values of zooplanktonic groups (dry weight mg m23). May 1996

July 1996

October January 1996 1997

April 1997

July 1997

Chlorophyll a

1.5

1.6

0.6

2.9

1.1

1.1

Zooplankton Crustacea Bivalvia Gastropoda Polychaeta Total

2.7 0.1 1.0 0.0 3.8

70.2 1.5 38.1 0.2 110.0

62.1 0.1 11.1 0.1 73.4

4.7 0.2 1.1 0.0 6.0

26.7 0.4 1.3 4.6 33.0

33.6 0.7 1.8 1.7 37.7

the Ivlev index for our analysis since it had the least disparities when compared with the Wilcoxon’s test results (Kohler and Ney 1982). A dendrogram was constructed based on the Morisita index, with the unweighted pair group average agglomerative method (UPGMA; NTSYS-PC software, version 2.02). A principal components analysis was applied to the biomass gut contents matrix; after centering, each group of food items was weighted by its standard deviation (CANOCO for Windows, version 4.0). Spearman rank correlations were used to compare diets among species and within species and also among fish diets and food availability (SPSS for Windows, version 11.0). Fig. 1. Variation of the water temperature (8C) and salinity (psu) in the water reservoir, and variation of the dissolved oxygen and biochemical oxygen demand (BOD5; ppm) in the water reservoir.

(AFDW) into dry weights. The mollusc data is shell-free dry weight. For counting and biomass determination purposes, fragments of a particular species were considered to be one individual, with the exception of when two heads or two tails of the same species were clearly seen. The average number of prey individuals per tract (Nm, considering only the tracts with prey) and the Vacuity index (VI 5 number of fish of each species with empty tracts, expressed as a percentage of the total number of fish of each species, for each sampling occasion) were calculated. The proportion of prey biomass for each group of fish was determined, as was the proportion of the biomass of each food item in the environment. All the biomass values were in dry weights. We calculated the Ivlev prey electivity index, Hulbert’s standardized niche breadth, and the simplified Morisita index of diet overlap (Krebs 1998). Electivity values above 0.3 or below 20.3 were assumed to indicate selection. The Wilcoxon’s two-sided, signed-rank test, recommended by Kohler and Ney (1982), could not be applied to our data. We chose

Results From April 1996 to September 1997 the water temperature varied between 128C and 278C and the salinity between 27.2 and 37.4 psu (Fig. 1). The dissolved oxygen concentration varied between 4.2 and 10.8 ppm, and the BOD5 varied between 0.7 and 6.2 ppm. The lowest chl a concentration found was 0.5 mg m23 and the highest was 3 mg m23. Copepods were the zooplanktonic group best represented, both in numbers and in biomass. The total biomass of zooplankton varied between 3.8 and 110 mg dry weight m23 (Table 1). The Annelids, mainly composed of polychaetes, were the most abundant macrofauna group, with a mean density close to 4,000 indiv m22, followed by the gastropods, with a mean density of approximately 2,000 indiv m22. The total mean density of macrofauna was 9,200 indiv m22, and their mean annual biomass was 7.3 g AFDW m22 (with an annual production of 22.3 g AFDW g m22 yr21). The mean density of suprabenthos was 52 indiv m22, with biomass varying between 0.01 and 0.9 g wet weight m22 (between 0.002 and 0.17 g dry weight m22). The mysids were the most abundant group, with densities higher than 200 indiv m22 in May 1997. The dry weights of macrofauna and suprabenthos, organized in the same wide taxonomicfunctional groups used for fish gut contents analysis, are presented (Table 2).

274 89 15 0 5,960 3,618 6,289 28 0 16,272 150 48 16 28 1,582 2,377 5,840 60 21 10,122 311 101 15 2 5,982 4,106 3,346 88 0 13,951 76 54 94 6 55 2,135 3,707 117 0 6,245 88 22 19 40 192 3,150 5,180 142 0 8,832 175 109 13 4 1,372 4,967 6,309 9 47 13,005 116 124 3 31 1,574 5,435 7,211 69 95 14,659 38 26 9 54 537 2,055 9,260 31 8 12,017 93 48 8 77 383 1,337 7,204 19 0 9,169 67 53 5 18 1,018 2,131 9,450 40 8 12,789 536 76 0 32 734 1,982 11,949 0 47 15,357 139 214 25 38 1,367 2,417 6,081 4 47 10,333 84 267 14 33 1,915 439 1,866 54 8 4,680 A B C D E F G H Other Total

196 459 7 13 1,504 1,098 7,791 12 0 11,081

September 1997 August 1997 July 1997 June 1997 May 1997 April 1997 March 1997 February 1997 January 1997 December 1996 November 1996 October 1996 September 1996 August 1996 Group

TABLE 2. Variation of macrofauna and suprabenthos biomass (mg dry weight m22). A: Tanaidacea, Ostracoda, and Cumacea; B: Amphipoda, Isopoda and Insecta; C: Mysidacea; D: Decapoda; E: Gastropoda; F: Bivalvia; G: Annelida and Nemertini; and H: Pisces. Other: other taxa (Actiniaria, Ophiuroidea, Chaetognatidae, Tunicata).

Food Availability and Feeding, Ria Formosa

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The gilthead seabream (Sparus aurata) was the species with the highest total biomass, with 28 % of the total catches, followed by two other Sparid fish, the black seabream (Spondyliosoma cantharus) and the two-banded seabream (Diplodus vulgaris). The total fish catch for August 1996–October 1997 was 218 kg ha21 (22 g wet weight m22 or 5.9 g dry weight m22). In 1997, the total fish catch was 145 kg ha21 (14.5 g wet weight m22 or 3.9 g dry weight m22), with the black seabream dominating, followed by the gilthead seabream (Table 3). Almost all fish had eaten something with the exception of Anguilla anguilla, which presented high emptiness indices (Table 4), and also, occasionally, some Sparidae species. The mean number of prey per tract varied considerably and the fish species seemed to actively select small gastropods, such as Bittium reticulatum and Hydrobia ulvae, bivalves, and, for some species, crustaceans. Polychaetes, although abundant in the environment (Table 2), were not preferentially selected. No olygochaetes or nemerteans were found in the gut contents. S. aurata preferentially consumed gastropods and bivalves, as well as small crustaceans such as tanaids, ostracods, and cumaceans (Table 4), although the small- and medium-sized individuals also selected fish. S. cantharus generally chose crustaceans, including the mysids, decapods, and the highly mobile epifauna. Diplodus annularis were found mostly to have selected small crustaceans, and some gastropods. Halobatrachus didactylus and A. anguilla had low mean numbers of prey per tract, but a very diversified diet. Mullus barbatus were found to have selected all groups of crustaceans, and also molluscs. Wrasses, gobies, and Diplodus sargus, all small-sized fish, preferentially ate small crustaceans, gastropods, and bivalves. D. vulgaris had a similar diet to these three groups of fish, although avoiding bivalves. Six groups of fish with high diet overlap were detected (Fig. 2). These groups can also be easily seen in Fig. 3. Group I (Labridae [December 1996] and S. cantharus [February 1997]) showed a highly diverse diet, preferentially eating small crustaceans, amphipods, and isopods, as well as gastropods. Group II (various species of Sparidae, Labridae, and A. anguilla) essentially consumed gastropods, but also some bivalves, amphipods, and isopods. Group III (S. aurata, D. annularis, H. didactylus, and Gobidae) essentially ate gastropods and bivalves. Group IV (S. aurata, A. anguilla, M. barbatus, Gobidae, and D. sargus) fed mainly on bivalves and also Annelids. Group V (H. didactylus and A. anguilla) had a highly diverse diet and also consumed the highly mobile fauna like decapods and fish. Finally, group VI (S. cantharus and D. an-

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S. Gamito et al.

TABLE 3. Total fish catch and catches in 1996 and 1997 in the Ria Formosa water reservoir, by family and species. 1996 Family

Anguillidae Atherinidae Batrachoididae Belonidae Clupeidae Engraulidae Gobiidae Labridae Moronidae Moronidae Mugilidae Mullidae Sparidae Sparidae Sparidae Sparidae Sparidae Sparidae Sparidae Sparidae Sparidae Soleidae

Species

Anguilla anguilla (L.) Atherina sp. Halobatrachus didactylus (Schneider) Belone belone (L.) Sardina pilchardus (Walbaum) Engraulis encrasicholus (L.) Dicentrarchus labrax (L.) Dicentrarchus punctatus (Bloch) Mullus barbatus L. Dentex dentex (L.) Diplodus annularis (L.) Diplodus sargus (L.) Diplodus vulgaris (Saint-Hilaire) Pagellus acarne (Risso) Pagellus erythrinus (L.) Sarpa salpa (L.) Sparus aurata L. Spondyliosoma cantharus (L.) Solea senegalensis Kaup

Common Name

European eel Boyer’s sand smelt Lusitanian toadfish Garfish European sardine European anchovy Gudgeon Wrasse Common seabass Spotted seabass Mullet Red mullet Common dentex Annular seabream White seabream Twobanded seabream Axillary seabream Common pandora Salema Gilthead seabream Black seabream Sole Total kg/ha

nularis) was characterized by a preference for several groups of crustaceans. Figure 2 shows that although annelids were the dominant group in the environment, they were consumed by only some fish, essentially from groups III and IV. No seasonal trend could be detected among the species of fish. According to Hurlbert’s niche breadth, groups II, III, and IV contained the less specialized fish species. Although these fish had essentially selected only gastropods and bivalves, these are abundant in the environment. Groups I, V, and VI, which correspond to fish species with more diversified diets, are more specialized, having selected items that are not very abundant in the environment. Highly significant correlations were observed among the several classes of S. aurata (within seasons and sizes) and among almost all fish from the previous described groups II, III, and IV (Table 5). S. cantharus presented significant negative correlations with some fish from those groups. In May 1997, this species had eaten large amounts of Mysidacea, an item that was not preferentially selected by most of the fish studied, and that is not very abundant in the environment. Occasionally, some fish presented significant correlations with environment-food availability. That can be due, for some of them, as it happens with S. aurata, to the fact that they only had eaten 3 or 4 different items

Wet Weight (g)

1997 %

992 137 3,171

2.3 0.3 7.2

349 2,076 4,100

0.8 4.7 9.3

687 187

1.6 0.4

1,180

2.7

6,474

14.7

1,193 22,205 649 531 43,930 73

2.7 50.5 1.5 1.2

Wet Weight (g)

4,186 789 4,363 152 7,610 433 3,354 1,534 17 319 7,752 3,746 961 6,889 4,605 7,413 59 97 128 13,957 18,041 433 86,835 145

Total %

4.8 0.9 5.0 0.2 88 0.5 3.9 1.8 0.0 0.4 8.9 4.3 1.1 7.9 5.3 8.5 0.1 0.1 0.1 16.1 20.8 0.5

Wet Weight (g)

5,177 925 7,534 152 7,610 782 5,430 5,634 17 319 8,438 3,934 961 8,068 4,605 13,886 59 97 1,321 36,162 18,690 964 130,765 218

%

4.0 0.7 5.8 0.1 5.8 0.6 4.2 4.3 0.0 0.2 6.5 3.0 0.7 6.2 3.5 10.6 0.0 0.1 1.0 27.7 14.3 0.7

of food, creating a large number of zeros in the comparisons with the environmental data. Discussion The small variation in salinity indicates that the water reservoir has good water exchange, even during the neap tides. The occasional occurrence of low dissolved oxygen values or high BOD5 values indicates some instability of the ecosystem. This is usual in these small lagoons where there is an excessive production of organic matter that can be followed in extreme situations by the total consumption of oxygen and massive mortalities of the fauna and flora (Krom et al. 1985). Although no direct comparisons were made with other sites in the Ria Formosa, a review of other studies suggests that the water reservoir is broadly comparable in terms of a variety of parameters and environmental characteristics to the surrounding tidal channels and other lagoons: mean chlorophyll a concentrations (by Assis et al. 1984; Cunha and Massapina 1984; Falca˜o et al. 1991), the mean density of zooplankton (Arias and Drake 1987), zooplankton composition (Sprung 1994b), zooplankton biomass (Cunha and Massapina 1984), benthos (Gamito 1994; Cunha et al. 1999; Lock and Mees 1999), fish composition (Monteiro et al.1987, 1990; Monteiro 1989), and fish production (Cle´ment and Rigaud 1986; Gamito 1994, 1997).

February 1997 February 1997 February 1997 February 1997 Total February

May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 May 1997 Total May

September 1997 September 1997 September 1997 September 1997 September 1997 September 1997 Total September

DanF GOBF SauFM ScaF

AanM DanM DsaM DvuM GOBM HdiM LABM MbaM SauML SauMM SauMS ScaM

AanS HdiS MbaS SauSL SauSM SauSS

Total

December 1996 December 1996 December 1996 December 1996 December 1996 Total December

AanD GOBD HdiD LABD SauDL

1996 1996 1996 1996 1996 1996 August

Date

August August August August August August Total

AanA DanA DvuA HdiA SauAL ScaA

Code

A. anguilla H. didactylus M. barbatus S. aurata—L S. aurata—M S. aurata—S

A. anguilla D. annularis D. sargus D. vulgaris Gobiidae H. didactylus Labridae M. barbatus S. aurata—L S. aurata—M S. aurata—S S. cantharus

D. annularis Gobiidae S. aurata—M S. cantharus

A. anguilla Gobiidae H. didactylus Labridae S. aurata—L

A. anguilla D. annularis D. vulgaris H. didactylus S. aurata—L S. cantharus

Species

476

10 6 10 3 15 12 56

12 7 15 8 9 16 17 15 4 78 3 31 215

8 11 21 19 59

10 20 10 20 27 87

4 14 20 9 3 9 59

n

34 19 20 35 18 13

34 16 11 18 12 17 11 18 35 16 6 14

14 13 15 14

37 12 16 12 34

32 16 26 14 35 16

L

2.4 4.4 2.2 1.2 1.8 1.2

7.5 2.4 2.3 1.6 1.4 2.9 1.4 1.5 1.7 1.1 2.1 1.5

1.3 1.6 1.4 1.9

6.7 1.4 2.3 2.2 3.6

3.7 1.2 2.7 1.5 0.5 0.6

Lstd

52,246

72 124 102 555 86 27 5,754

63 70 28 83 20 83 21 76 545 58 3 38 13,210

45 26 45 38 2,319

79 21 72 30 667 20,528

51 72 319 49 606 65 10,436

W

19.8 105.2 24.1 73.7 27.4 6.5

49.0 26.3 15.8 20.3 6.6 61.4 7.0 21.7 117.6 14.5 2.5 15.9

15.6 8.7 14.4 20.3

44.8 6.4 29.8 17.0 221.7

16.2 17.4 86.9 15.3 19.5 8.3

Wstd

Nm

40.0 3 0.0 4 10.0 17 33.3 119 0.0 49 0.0 34 Environment:

16.7 5 0.0 66 6.7 11 0.0 169 11.1 5 12.5 6 11.8 37 0.0 16 0.0 171 5.1 74 0.0 19 0.0 58 Environment:

25.0 33 9.1 4 0.0 36 5.3 15 Environment:

10.0 1 10.0 2 10.0 3 5.0 55 11.1 326 Environment:

50.0 27 28.6 32 30.0 40 11.1 6 0.0 24 11.1 200 Environment:

%VI

1.0 0.0 0.9 0.0 0.9 0.6 0.5 0.7 21.0 20.7 21.0 1.0 0.3 0.8 20.5 0.7 21.0 20.9 20.7 0.5

0.0 0.2 0.3 0.2 0.6 20.7 0.6 0.8 20.8 20.2 0.6 0.1 1.0

21.0 21.0 0.0 21.0 20.8 0.1 1.7

0.9 0.9 0.7 21.0 21.0 21.0 0.1

0.5 20.3 0.4 21.0 21.0 20.1 20.2 20.1 21.0 20.6 21.0 1.0 0.2

21.0 0.7 20.3 1.0 0.1

21.0 0.6 20.5 1.0 0.2

0.9 20.2 0.5 1.0 0.3

21.0 21.0 21.0 21.0 21.0 ,0.1

1.0 0.9 0.9 1.0 0.0 0.4

21.0 0.9 21.0 0.9 21.0 0.5

21.0 21.0 21.0 21.0 21.0 21.0 ,0.1

1.0 21.0 21.0 21.0 21.0 1.0 0.8 0.8 21.0 21.0 21.0 0.9 0.5

21.0 21.0 21.0 21.0 0.4

21.0 21.0 1.0 21.0 21.0 0.1

D

21.0 21.0 21.0 21.0 21.0 21.0 0.7

C

21.0 21.0 21.0 21.0 21.0 21.0 0.3

0.6 0.7 0.3 0.1 20.1 0.7 5.7

B

0.6 0.9 0.5 20.2 21.0 0.9 1.8

A

20.6 20.8 21.0 20.1 20.2 20.2 36.6

0.6 0.9 0.8 0.9 0.8 0.8 0.9 0.3 0.9 0.9 0.8 20.7 2.2

0.9 0.5 0.9 0.7 4.5

0.8 0.7 20.6 0.6 0.8 8.0

0.3 20.4 0.3 0.0 0.1 21.0 40.9

E

G

20.5 20.8 20.6 20.9 20.9 21.0 38.6

20.8 20.6 20.5 20.9 20.6 20.8 20.9 20.6 21.0 21.0 21.0 20.9 58.6

20.5 0.1 0.1 20.1 0.2 20.3 20.1 0.3 0.2 0.2 0.4 21.0 35.7 0.5 20.3 0.6 0.5 0.5 0.5 22.2

21.0 20.4 21.0 20.8 77.1

21.0 21.0 20.9 21.0 21.0 73.9

21.0 21.0 21.0 21.0 21.0 21.0 39.9

0.0 0.5 0.2 21.0 17.1

21.0 0.4 20.5 0.1 0.0 16.7

21.0 21.0 20.2 0.5 0.7 21.0 9.4

F

21.0 1.0 21.0 21.0 0.8 0.8 0.2

0.9 21.0 0.6 21.0 21.0 0.9 21.0 21.0 21.0 0.2 21.0 20.1 1.6

21.0 21.0 21.0 0.9 0.3

21.0 21.0 1.0 21.0 1.0 0.3

21.0 21.0 21.0 0.9 21.0 21.0 1.1

H

TABLE 4. Groups of fish considered for gut content analysis. Fish codes are used in subsequent tables and figures. Number of fish (n), mean total length (L, cm) and standard deviation (Lstd), mean wet weight (W, g) and standard deviation (Wstd), percentage Vacuity Index (%VI), mean number of prey (Nm), and Ivlev index for each food item (varies from 21 to 11). Bold: Ivlev values above 0.3, indicating preference; Italics: Ivlev values below 20.3, indicating avoidance. Prey item codes, A, B, . . . , H, as in Table 2. Environment: observed percentage of macrofauna and suprabenthos. (Sparus aurata: S: small; M: medium, L: large).

Food Availability and Feeding, Ria Formosa

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S. Gamito et al.

Fig. 2. a) Fish gut contents—dendrogram of Morisita index based on relative biomasses of food items, b) Hurlbert’s niche breadth measure, based on fish gut contents and food availability, c) Percentage of biomasses in gut contents, and d) in the environment (prey item codes as in Table 2 and fish species codes as in Table 4).

Fig. 3. Projection of food items and fish on the first two axes of principal components analysis based on the biomass gut contents matrix. Cumulative percentage: axis 1: 40.7 %, axes 1 and 2: 72.1 %. Groups I–VI are based in Morisita’s index (prey item codes as in Table 2 and fish species codes as in Table 4).

All the fish caught were also reported by Monteiro (1989) and Monteiro et al. (1987, 1990) in their study of the ichthyofauna of the Ria Formosa. The species composition and relative abundances encountered in the water reservoir are comparable to those of individual beach seine stations sampled by Monteiro (1989), with a clear dominance of sea breams (Sparidae). The total fish biomass of 218 kg ha21 was high. If we consider that the first two samplings were carried out with 50 m beach seines in 1996 (Table 3), with the objective of catching all the large predators, the total catch of 148 kg ha21 in 1997 can be broadly compared to the annual fish production under local extensive aquaculture regimes, resulting from the small fish that were not originally caught or from those that repopulated the reservoir. Cle´ment and Rigaud (1986) point to a maximum value of 150 kg ha21 yr21. In certain places with favorable environmental conditions, an estimated production of 300 kg ha21 yr21 has been observed (Gamito 1994). According to an ecological model already developed for similar places (Gamito 1997), the maximum expected yield of gilthead in places with good environmental conditions and relatively low

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34

AanA DanA DvuA HdiA SauAL ScaA AanD GOBD HdiD LABD SauDL DanF GOBF SauFM ScaF AanM DanM DsaM DvuM GOBM HdiM LABM MbaM SauML SauMM SauMS ScaM AanS HdiS MbaS SauSL SauSM SauSS Envir.

**

*

2

**

1

1

* ** *

1 ** **

3

*

** ** *

* **

1 * **

4

* *

—*

*

*

*

*

1 *

5

*

*

*

* *

* **

**

1

6

*

1

7

*

1

8

*

*

*

*

** ** **

1

9

*

**

1

10

*

1

11

*

*

*

** ** ** **

1 * * **

12

**

** —

*

*

**

1

16

*

**

1

13

* * 14

17

*

**

15

*

1

* **

*

1

**

** —*

**

** * ** **

1

**

*

** ** *

1 *

** ** * * 18

**

* *

1

A D F M S

** * * * 19

* —* *

**

*

1

1 ** * * ** A

20

** * *

**

*

**

1

1 * ** ** D

21

1

1 ** * F

22

*

*

1

1 * M

23

1 *

1 S

24

** * *

1 * ** —* *

25

* ** **

*

1 * —*

* * ** * 26

1 —

27

— —

1

* 28

**

1

29

*

1

30

1 1 * * ** 31

32

1 **

33

1 1 34

TABLE 5. Spearman Rank correlations among fish gut contents (biomasses) and between fish and food availability (environment—last row). Fish species codes as in Table 4. Small triangular matrix: rank correlations among environmental sampling occasions (A: August 1996, D: December 1996; F: February 1997; M: May 1997; S: September 1997). *: significant correlation at the 0.05 level (2 tailed test; **: significant correlation at the 0.01 level; —*; and —**: significant negative correlations; n 5 8).

Food Availability and Feeding, Ria Formosa

945

946

S. Gamito et al.

benthic biomass should not exceed 10 g m22 (100 kg ha21). If we consider all the Sparidae caught in the water reservoir we get a figure of 140 kg ha21, which means that, according to the model, the amount of food available would not be enough to support the fish populations. The fish caught in 1996 may correspond in part to the production of fish from the previous year. If we only consider data from 1997, we get a figure of 87 kg ha21, which is near the upper limit of 100 kg ha21. It seems that the water reservoir has conditions similar to those observed in the tidal channels of the Ria Formosa and other lagoonal systems, but lower macrofauna biomass that may perhaps not be sufficient to support the large biomass of fish present. The results indicate that S. aurata, particularly the larger individuals, selected hard-bodied prey such as gastropods and bivalves, confirming the observations of Arias (1980) and Gamito et al. (1997). The smaller fish were also found to have eaten large quantities of soft-bodied prey, such as small crustaceans like tanaids, ostracods, and cumaceans. Some classes of S. aurata also selected fish. Rosecchi (1987) found gilthead to be the most specialized of the 4 species of sparids studied, singling out bivalve molluscs and, secondarily, crustaceans (decapods and annelids) in the open sea and fish and crustaceans in the lagoons. The author did not give any food availability data for the two environments. On the other hand, Ferrari and Chieregato (1981) found in a study of gilthead juveniles that the most important prey items in the diet were those that were most abundant in the environment, indicating non-selectivity. This was consistent with the conclusions of Wassef and Eisawy (1985), who reported that the gilthead was a generalist feeder, taking whatever is available. D. vulgaris mainly selected gastropods and small crustaceans, such as tanaids, ostracods, and cumaceans. Gonc¸alves and Erzini (1998) indicate that the diet of this fish consists of a wide range of small prey, that are often very common in the environment (polychaetes, ophiuroids, and amphipods). Rosecchi (1987) considered this species to be an opportunist predator, capturing large quantities of crustaceans and, occasionally, a large mollusc or echinoderm. In the French lagoons this fish mostly ate fish and, as secondary prey, crustaceans. D. annularis mainly selected small crustaceans and selected other crustaceans on occasion, such as amphipods and isopods, and also gastropods. Rosecchi (1987) found amphipods to be the preferred prey, both in the open sea and in lagoons. The larger individuals from the sea also opted for molluscs as prey of choice. S. cantharus generally selected crustaceans, including the highly mobile epifauna, the mysids,

and decapods, even though Gonc¸alves and Erzini (1998) concluded that the diet of this species was characterized by polychaetes, amphipods, and hydrozoans, along with gastropods and decapods. They concluded that, as with other sparids, the black seabream is an opportunistic feeder and an omnivore. H. didactylus and A. anguilla had very diversified diets that varied over time. Only the small crustaceans were not selected by these two species. Lecomte-Finiger (1983) has shown that eels are carnivorous and consume benthic-invertebrates such as amphipods and isopods. The author found that eels generally feed in the night and afternoon, which might explain the high VIs found in this study, as the fish were all captured in the morning. Cardenas (1977) also found that the diet of H. didactylus was extremely varied and dependent on the size of the fish and the food available to it. In Greece, polychaetes were the dominant prey of M. barbatus in the Iraklion Sea (Labropoulou 1997), while in the Aegean Sea crustaceans, polychaetes, and fish predominated (Vassilopoulou and Papaconstantinou 1997). The results of our study were similar to the findings of Caragitsou and Tsimenidis (1982) for the Thracian Sea, who found that decapods, polychaetes, mysids, and amphipods were found to be of most importance in the dietary habits of M. barbatus, while cumaceans, copepods, and bivalves were considered as secondary food. All the species studied were characterized by a wide variety of diets, which allows them to survive in environments of low diversity and poor stability such as coastal lagoons. They are largely benthic feeders, essentially eating the epimacrofauna and endomacrofauna, while some, such as S. cantharus and H. didactylus, also feed on the suprabenthos. Almost all the tracts examined contained some vegetable material, such as small pieces of seagrass and macroalgae. It is difficult to decide if these had been selected or ingested together with invertebrates. The annelids, although abundant in the water reservoir, were apparently not selected by the fish. Several reasons for this can be pointed out, including that the annelids can be more quickly digested than the other preys and they are harder to quantify. Sometimes only small pieces were found in the guts and they were considered to be only one individual, when in fact they can correspond to several individuals. The fish may not have selected them since most of the annelids were very small-sized organisms, and were buried in the sediment, making them inaccessible or non-compensatory from an energetic point of view. The gastropods were actively selected on almost all occasions, except during the first and last observations in Au-

Food Availability and Feeding, Ria Formosa

gust 1996 and September 1997, when their relative availability in the environment were high. Six groups of fish with overlapping diets were detected. S. aurata were dominant in groups II, III, and IV, and were independent of size or season, consuming essentially gastropods and bivalves. D. annularis, D. vulgaris, and D. sargus were generally included in the same three groups denoting the same preferences, but with some particular preferences already previously described. Gobiidae were included in groups III and IV, showing preference for molluscs and also annelids. M. barbatus was included in group IV, being characterized by having consumed mainly bivalves and annelids. The majority of the species included in groups II, III, and IV had broader niches then the ones from the other three groups because they had selected items that were relatively abundant in the environment. S. cantharus, A. anguilla, and H. didactylus were almost all included in groups I, V, and VI— the groups that showed the more diverse diets— and were feeding from all the groups of food considered, including the mobile fauna such as mysidacea, decapods, and fish. As most of their prey were not very abundant in the environment, the niche breadth of most of these species was small, indicating that they can be considered specialized predators. A great overlap in diets was observed among the various species suggesting the existence of possible interspecific and intraspecific competition as described by Tokeshi (1999). When food is scarce, a negative effect on development may occur, together with an increase in mortality rates. Poor condition of some fish, which looked rather thin, was noticeable during fish harvesting. The present joint analysis of food selectivity, food availability, diet overlap, and niche breadth allowed the clarification of the relationships among the fish species and is an ecological approach that leads to a better understanding of the structure and the dynamics of the Ria Formosa lagoon ecosystem. Monitoring of fish feeding may be a useful tool for integrated studies, in particular in lagoon systems such as the Ria Formosa Natural Park where the objective is sustainable development in the face of increasing pressure from population growth, fisheries, and aquaculture. Extensive aquaculture, which is less harmful to the environment than the intensive form, may for example be optimized by controlling the relative proportions and numbers of the different species in relation to the available natural prey. The data obtained in this study can also be used for the development of eco-trophic models.

947

ACKNOWLEDGMENTS Thanks are due to Dr. Jorge Santinha and Aquamarim for allowing us to use their facilities for all our field work. Joa˜o Reis and many others helped us with the field work, mainly during fish harvesting. We are grateful for the criticism and helpful comments of two anonymous reviewers. This research was supported by the Fundac¸a˜o para a Cieˆncia e Tecnologia, project PBIC/C/MAR/2226/95.

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