Factors determining the structure of sh 81communities in Pantanal lagoons (MS, Brazil)

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1 Fisheries Management and Ecology, 2001, 8, 173±186 Factors determining the structure of sh 81communities in Pantanal lagoons (MS, Brazil) Y. R. SU AREZ UEMS/Unidade de Ivinhema, Ivinhema ± MS, Brazil M. PETRERE Jr UNESP ± Departamento de Ecologia, Rio Claro ± SP, Brazil A. C. CATELLA Embrapa/Pantanal, Corumba ± MS, Brazil Abstract The sh communities of lagoons in the Nhecolaà ndia Pantanal were studied to determine the factors which are responsible for the composition and abundance of species. Fishes were collected in 19 lagoons during August 1997, after their isolation from the River Negro, using beach seines ( m; 2 mm mesh). A total of 51 species were collected. In the lagoons, or in parts with dense macrophytes, a screened box trap was used. Fishing was also accomplished with hooks of several sizes. Species richness was estimated by the jack-knife procedure, after adjustment to the log-normal distribution and with von Bertalan y's equation (asymptotic). The most important factors in the community organization were macrophyte cover, piscivore abundance and depth of the lagoons. The role of these habitats in the Pantanal ecosystem was discussed. KEYWORDS: Brazil, sh communities, oodplains, lagoons, Pantanal. Introduction Floodplain environments are highly productive and support important inland shing activities (Goulding 1980; Bayley & Petrere 1989). They are spawning grounds and nursery grounds for many shes, as a result of the diversity of habitats, supplying food and shelter against predators (Goulding 1979; Lowe-McConnell 1987). Pantanal is an alluvial plain in the centre of South America, with a oodplain of about km 2 (Alho, Lacher Jr. & GoncË alves 1988). There is a diversi ed ora and fauna, in the varied aquatic habitats such as rivers, intermittent creeks, lagoons and swamps (MouraÄ o 1989). The ooding pattern is of fundamental importance for the ichthyofauna of the Pantanal. The area and residence time of water in the surrounding lands determines habitat availability and the food of the shes, thus a ecting their abundance (Catella 1992). Correspondence: Yzel R. Su arez, UEMS/IVINHEMA, Av. Brasil no. 679, Centro. CEP ±000, Ivinhema (MS), Brazil ( suarezyr@uol.com.br) Ó 2001 Blackwell Science Ltd 173

2 174 Y. R. SU AREZ ET AL. Although the importance of sh in this ecosystem is well recognized, few studies have attempted to characterize the sh communities and to elucidate the processes responsible for their composition and abundance (Catella 1992; Catella & Petrere 1996). The objectives of this paper were to: ± establish whether sh species composition and abundance are determined by the `species pool' in the lagoons during the connection period or if the characteristics of these lagoons in uence this organization; ± which are the most important factors that determine the distribution and abundance of the sh species; ± using presence/absence data and the cumulative increase of species as a function of the number of lagoons sampled, what would be the total richness of species in the lagoons of the Pantanal of Nhecolaà ndia area. Materials and methods A total of 19 lagoons were sampled during August 1997, in the Pantanal of Nhecolaà ndia, CorumbaÂ, MS (Fig. 1). These lagoons are visited by aquatic birds for shelter and mainly for feeding in the dry season. At least 32 species out of the 656 of all bird species listed for the Pantanal, feed exclusively upon sh (Coutinho, Campos, MouraÄ o & Mauro 1997). The area of the lagoons studied ranges from 179 to m 2, with depth from 0.3 to 2 m and distance from River Negro from 0.1 to 34 km. Macrophyte cover varied from 1 to 97% of the lagoon area and the river isolation varied from 2 to 13 weeks. A trap specially developed to catch sh in areas covered with aquatic macrophytes was used for sampling. The trap consisted of two 2-m long, 1-m wide and 1-m deep rectangular iron frames, with the bottom and sides of the trap covered with a 2-mm mesh mosquito screen. For sh sampling the trap was manoeuvred under the vegetation in a collapsed state, with the side walls folded under the upper frame. Soon after, the upper frame was lifted quickly above the surface, trapping sh in the box thus formed. In areas without or with little vegetation, a m, 2-mm mesh beach seine and shhooks of di erent sizes were used. Fishes were identi ed according to Britski, Silimon & Lopes (1999). The lagoons were grouped using the simple matching coe cient (presence/absence of species) and the Morisita±Horn index based on percentage abundance (Krebs 1999), to verify similarities on composition and abundance of sh species. The simple matching coe cient (S SM ) is expressed as: S SM ˆ a b = a b c d where a is the number of common species in lagoons A and B; b, the number of species in lagoon B but not in lagoon A; c, the number of species in lagoon A but not in lagoon B and d, number of species absent in both lagoons The Morisita±Horn index (C ij ) is expressed as: C ij ˆ Xn k X ki ; X kj, X X 2 ki =N 2 i X X 2 kj N 2 j! N i N j

3 FISH COMMUNITIES IN PANTANAL LAGOONS 175 Figure 1. Location of the study area: Nhecolaà ndia Pantanal in Mato Grosso do Sul State, Brazil. Shaded area represents extent of Negro River high inundation oodplain. where X ki, X kj are the number of individuals of species k in lagoons i and j; N i, the total number of individuals in lagoon i; N j, total number of individuals in lagoon j. The simple matching coe cient was used because it is sensitive to double absences. Once the lagoons are connected, any sh will decide in which lagoon it will remain. A given species may also not choose either of the two lagoons if none is suitable. They were also grouped by their characteristics (depth, area, distance from the main river, macrophyte covering, piscivore abundance in weight and isolation time) using the Bray± Curtis' coe cient, as a metric and the unweighted pair group method average (UPGMA) as the clustering method. The cophenetic coe cient of correlation was calculated in order to assess the appropriateness of the dendrograms. The Bray±Curtis coe cient (B) is expressed as: B ˆ X Y ij Y ik. X Yij Y ik

4 176 Y. R. SU AREZ ET AL. where Y ij is the lagoon characteristic i in lagoon j; Y ik, the lagoon characteristic i in lagoon k. Similarity matrices were compared using the Mantel test (Mantel 1967). Species richness was estimated by the jack-knife procedure (Heltshe & Forrester 1983) and by tting the log-normal distribution (Krebs 1999). The lagoons were randomized generating 50 groups of one, two, ¼, 19 lagoons, to calculate the asymptote richness. The average richness, for each of the 50 randomizations, was plotted as cumulative richness as a function of the number of sampled lagoons. These results were adjusted to the von Bertalan y growth equation, using an algorithm of non-linear regression. The species frequency of occurrence (FO) was calculated according to: FO ˆ Number of lagoons with the species i = Number of lagoons 100 If FO is ³ 50%, the species is termed a primary species; if 25% FO 50%, the species is termed a secondary species; if FO 25%, the species is termed an incidental species. The relative abundance of the 14 primary species and the already mentioned characteristics of the lagoons were used in the communities ordering through Canonical Correspondence Analysis (CCA). CCA scatterplots describe the ecological associations between the samples and species along an environmental gradient (Jongman, Ter Braak & Van Tongeren 1995). A Monte Carlo simulation procedure was also performed (1000 permutations) to test the statistical signi cance of the variable e ects in the observed distribution (Manly 1994). Results Characiformes was the most represented order by number, weight and number of species. However, its dominance was less accentuated in a number of species (Table 1). A total of individuals were recorded representing 51 species (Table 2). The ve most abundant species represented 86% of all individuals collected. The Characidae family represented 92% of the individuals. Of these, Odontostilbe calliura represented 59.7% of the individuals, followed by Psellogrammus kennedyi (11.1%). There are more incidental species (51%) than primary species (27%) and secondary species (22%). Of the 51 species, 14 occurred in one lagoon and 6 occurred in two lagoons. This community mainly consists of adults of small sized sh species and not by juveniles of large sized species. Table 1. Relative number of species (RNSP), relative abundance by number (RANI) and relative abundance weight (RAWT) for the sh orders in 19 lagoons of the Nhecolaà ndia Pantanal, August 1997 Order RNSP RANI RAWT Characiformes Siluriformes Perciformes Synbranchiformes

5 FISH COMMUNITIES IN PANTANAL LAGOONS 177 Table 2. List of species and their respective number of individuals, weight (g) and frequency of occurrence (FO) sampled in 19 lagoons of the Nhecolaà ndia Pantanal, August Species Authorities Number Weight (g) FO (%) Characiformes Characidae Aphyocharax anisitsi Eigenmann & Kennedy Astyanax bimaculatus Linnaeus Acestrorhynchus pantaneiro Menezes Aphyocharax paraguayensis Eigenmann A. rathbuni Eigenmann Bryconamericus exodon Eigenmann Characidium a. zebra Eigenmann Gymnocorymbus ternetzi Boulenger Hyphessobrycon eques Steindachner Holoshestes pequira Steindachner Hemigrammus ulreyi Boulenger Metynnis maculatus Kner M. mola Eigenmann & Kennedy Markiana nigripinnis Perugia Moenkhausia sanctae- lomena Steindachner Odontostilbe calliura Boulenger O. microdon Eigenmann Psellogrammus kennedyi Eigenmann Piaractus mesopotamicus Rolmberg ± ± 5.26 Pygocentrus nattereri Kner ± ± Roeboides paranensis Pignalberi Serrasalmus spilopleura Kner Triportheus nematurus Kner Curimatidae Curimatopsis myersi Vari Erythrinidae Erythrinus erythrinus Schneider Hoplias malabaricus Bloch Lebiasinidae Pyrrhulina australis Eigenmann & Kennedy Rivulidae Rivulus punctatus Boulenger Perciformes Cichlidae Apistogramma borellii Regan Aequidens plagiozonatus Kullander Bujurquina vittata Heckel Cichlassoma dimerus Heckel Crenicichla edithae Ploeg Gymnogeophagus balzanii Perugia

6 178 Y. R. SUÂ AREZ ET AL. Table 2. (Continued) 8 Species Authorities Number Weight (g) FO (%) Siluriformes Aspredinidae Amaralia hypsiura Kner Auchenipteridae Parauchenipterus striatulus Steindachner Callichthyidae Corydoras hastatus Eigenmann & Eigenmann Hoplosternum littorale Hancock Hoplosternum pectorale Boulenger H. personatus Ranzani Doradidae Anadoras weddellii Castelnau Hypopomidae Hypopomus sp Hypopomus sp Loricariidae Lyposarcus anisitsi Eigenmann & Kennedy Hypostomus sp Loricariithys platymetopon IsbruÈ cker & Nijsen Gymnotidae Gymnotus gr. carapo Linnaeus Sternopygidae Eigenmannia trilineata Lopez & Castello E. virescens Valenciennes Synbranchiformes Synbranchidae Synbranchus marmoratus Bloch Lagoons were more similar in the composition of species when a quantitative coe cient was used (Fig. 2; cophenetic correlation r ˆ 89.9; P < 0.01) than when a simple matching coe cient was used (Fig. 3; cophenetic correlation r ˆ 92.7; P < 0.01). Using the Morisita±Horn coe cient, six of the 19 lagoons studied (B. Anhuma 2, B. Sede, B. PocË o, B. Anhuma 1, B. Logrador, B. Alegria) were similar in the abundance of the species, a pattern that does not occur with the coe cient of simple matching. The lack of grouping of the two similarity coe cients was veri ed by the Mantel test (r ˆ 0.103; P ˆ 0.29). The Mantel test showed that there was no correlation between the similarity among species abundance of the communities (Morisita±Horn) and the geographical distance (km) between the lagoons (r ˆ 0.073; P ˆ 0.37). However, signi cant correlation existed between the similarity matrix calculated with the species abundance in lagoons and the matrix of their physical characteristics (r ˆ )0.293; P ˆ 0.008). Closer lagoons tended to be more similar in species composition (simple matching) (r ˆ 0.470; P < 0.001), but the

7 FISH COMMUNITIES IN PANTANAL LAGOONS 179 Figure 2. Similarity dendrogram (Morisita±Horn) of the sh communities in the 19 lagoons studied at the Nhecolaà ndia Pantanal, August Figure 3. Similarity dendrogram (simple matching) of the sh communities in the 19 lagoons studied at the Nhecolaà ndia Pantanal, August 1997.

8 180 Y. R. SU AREZ ET AL. similarity among the lagoons based on physical characteristics does not in uence the composition of species (r ˆ )0.088; P ˆ 0.23). At the level of 60% similarity the lagoons separated into 4 groups using the Morisita± Horn coe cient (Fig. 2), while for the coe cient of simple matching the ponds were divided into 11 groups, with 9 groups represented by just a single lagoon (Fig. 3). The higher the number of sh species in lagoons the lower the similarity in species composition (Fig. 3). The estimated species richness for lagoons of the Nhecolaà ndia Pantanal as tted by log-normal distribution was of 63 species. With the jack-knife the estimated richness was 64 species (CI (0.05%): 56±71). The asymptotic richness, estimated by von Bertalan y's equation was 50 species (CI (0.05%): 48±52) (Fig. 4), according to: Richness ˆ 50:44 1 exp 0:224 number of lagoons Š: The rst three axes of the CCA explained 40.2% of the variation of the species abundance. The rst axis explained 23.5% of the variation based on macrophyte cover and piscivore abundance. The second axis was associated mainly with lagoon depth and it explained 9.9% of the variation. The third axis explained 6.8% of variation and it was associated with lagoon area (Fig. 5; Table 3). Monte Carlo simulation showed that only axes 1 and 3 were signi cant. Discussion The ichthyofauna of South American rivers is characterized by the dominance of Characiformes over Siluriformes (Lowe-McConnell 1987; Agostinho 1993). However, in lagoons and dams this dominance is intense (Cordiviola de Yuan 1980; Bonetto, Rolda n& Vero n 1981; Castro & Arcifa 1987; Verõ ssimo 1994; Okada 1995). Verõ ssimo (1994), studying the icthyofauna of lagoons of the oodplain of the Parana river attributed this to Figure 4. Mean number of species as a function of the number of lagoons sampled in the Nhecolaà ndia Pantanal.

9 FISH COMMUNITIES IN PANTANAL LAGOONS 181 Figure 5. Scatterplot of the rst two axis of the Canonical Correspondence Analysis of the sh species in the Nhecolaà ndia Pantanal lagoons. The arrows indicate the importance of the environmental variables. Table 3. Canonical Correspondence Analysis (CCA) for the sh communities in the lagoons of the Nhecolaà ndia Pantanal, August 1997 Axis 1 Axis 2 Axis 3 Canonical coe cients for the standardized variables Macrophyte cover (%) ) )0.220 Depth )0.213 )0.316 Lagoon area )0.280 )0.034 )0.317 Piscivores (%) )0.428 River distance ) )0.125 Isolation time )0.109 ) Correlation among groups of variables Macrophyte cover (%) ) )0.038 Depth )0.472 )0.440 Lagoon area )0.329 )0.303 )0.508 Piscivores (%) )0.251 River distance ) Isolation time ) Statistical summary for the rst 2 axes Eigenvalue Explained variation (%) Species/environment correlation Monte Carlo simulation (1000 permutations) P

10 182 Y. R. SU AREZ ET AL. the small Characiformes being able to exploit oxygen in the upper layers of the water column. The present study con rmed this high dominance. In the Nhecolaà ndia lagoons, 51 (19%) of the 263 sh species listed to the Pantanal oodplain were found (Britski et al. 1999). Although the relationship between the number of species number of sample lagoons quickly approaches the asymptote (k ˆ lagoons ±1 ), suggesting that a small number of lagoons is su cient to represent Nhecolaà ndia sh diversity, other considerations are in order: in the present study it was observed that a large number of incidental species (51%), albeit these were rare representing only 0.49% of individuals. This is responsible for the di erences identi ed in the simple match groupings (Fig. 3), and it can be interpreted as a complementary measure of the b diversity (between habitats), provided that a high frequency of incidental species indicates a large di erence in the composition of species between the lagoons. This suggests that it is necessary to preserve several lagoons and di erent habitats to assure the survival of a viable number of individuals for conservation purposes. However, although the lagoons were di erent in species composition, the abundance of the main species leads to a tighter grouping of the ponds, as shown by the dendrogram using the Morisita±Horn formula. The lagoons with low richness tend to be more similar in their simple matching coe cients. This raises two hypotheses regarding the diversity in these ponds: (1) the low similarity observed among the lagoons using the simple matching coe cient is mainly a function of the di erence in richness and not of species abundance; (2) the lagoons with low richness and most similarities in species composition, are those that endured larger stress caused by drought and retained the most resistant species. In comparison, those that revealed greatest diversity were the deepest ones and had been isolated from the river more recently. MouraÄ o, Ishii, & Campos (1988) studied the ichthyofauna of Nhecolaà ndia Pantanal lagoons, and Catella (1992) found 75 species in Baõ a da OncË a, a perennial marginal lake of Aquidauana River, Pantanal, and they concluded that richness is a result of the lake±river connection (distance, height, continuance and frequency of the connection), water quality and lake area. In the present study neighbouring lagoons tended to be more alike in species composition (simple matching), but they were not more similar in the species abundance (Morisita±Horn). These results suggest that the species composition is determined by the `pool' of available species during the period in which the lagoons are connected. However, the characteristics of each lagoon (depth, macrophyte cover, macrophyte dominant species) will determine the abundance of the species. This was con rmed by the CCA. Jackson & Harvey (1989) veri ed a negative correlation between sh community structure and the geographical distance between lakes of the Ontario region. Jackson & Harvey also veri ed that lakes in the same region presented similarities in typology (ph, depth and area). In the Orinoco oodplain ponds, Rodrõ guez & Lewis (1997) veri ed that the similarity among the sh communities was not signi cantly correlated with the geographical distance. They commented that the morphometry of each lake allied to the predator/prey interaction, would be the main factors responsible for the community structure, independent of the distance between the ponds. Catella (1992) observed in Baõ a da OncË a a low similarity between the communities during two serial isolation periods

11 FISH COMMUNITIES IN PANTANAL LAGOONS 183 (1988, 1989), and changes in numerical dominant species (Moenkhausia dichroura and Auchenipterus nigripinnis), but they represented species with the same dietary habits. This suggests that the arrangement of the species may be a function of the resources available, and the lagoon can be exploited by di erent combinations of ecologically equivalent species. The results of the CCA indicated that macrophyte cover and piscivorous abundance were the most important biotic factor structuring sh communities. Tejerina-Garro, Fortin & Rodriguez (1998) demonstrated that water transparency and maximum lake depth were the most important factors structuring the sh communities in oodplain lagoons of the Araguaia river in Brazil. Besides these two factors, Rodrõ guez & Lewis (1997) suggested the piscivory as another determining trait in the Orinoco oodplain. It was anticipated that this study would contribute to understanding the role ecological factors play in structuring the sh communities of these habitats. This knowledge is important in the decision making about community management (e.g. to decide which species may be collected for aquarium trade) and land use. The jack-knife species richness estimator is positively biased (Heltshe & Forrester 1983). In the present work, its 95% estimated con dence interval (56±71 species) overlapped with the estimate by the log-normal model (63) suggesting that the list of species in the lagoons (51) may be incomplete. Therefore, these estimates are considered more realistic than the asymptotic richness value (50). Bastos & MouraÄ o (1986), studying the composition of sh species in the lagoons of the Nhumirim farm (Nhecolaà ndia Pantanal), made four collections of sh from a number of lagoons, and identi ed 53 species. Welcomme (1985) commented that the best habitats for sh feeding rarely coincide with the best for reproduction, resulting in seasonal migrations between these areas. During ooding in the Pantanal, the sh species invade the oodplain in search of food. The moment the level of the rivers begins to drop, there is the inverse migration back to 83 the main channel (Ferraz de Lima 1986). Verõ ssimo (1994) and Okada (1995) found that with isolation, the water recedes and sh density increases together with biotic and abiotic pressures, although Catella (1992) detected an opposite trend. There can be drastic changes in some physical and chemical water characteristics (e.g. reduced oxygen), quickly killing the less tolerant species (Verõ ssimo 1994; Okada 1995). In this study, some lagoons were far from the river, so they may dry out completely before the next ood. Catella (1992) suggested that the species that remain are represented by: (1) individuals that did not return (or did not have the opportunity) to the river before isolation; (2) species that would exhibit some adaptation to the pool characteristics (e.g. hypoxia, presence/absence of sheltering macrophytes, desiccation), and therefore may be able to survive until the next ood. However, in the present set of lagoons there are some which do not dry out sustaining sh populations, whose characteristics allow the survival of a small number of species among the 263, that would possibly explain the low diversity. It has been veri ed that the Nhecolaà ndia lagoons hosts mainly species of small size and not small specimens of large species, but what is the role of these lagoons in the Pantanal? Probably, one important function is to provide an amenable habitat for these small-sized shes, easily caught in shallow waters by aquatic birds and reptiles, mainly in the dry season. In contrast, Catella (1992) remarks that marginal lagoons as Baõ a da OncË a

12 184 Y. R. SU AREZ ET AL. (perennial and deeper) shelter these small forms in the dry season, providing potential prey for predatory sh when the lake connects to the river. These lagoons are more important as feeding locations for aquatic mammals than for birds and reptiles. The sh communities of these lagoons are not exploited by subsistence nor commercial sheries. They are only exploited by shermen looking for bait for sport sheries, mainly the tuvira (Gymnotus gr. carapo), which lives in macrophyte roots. In this activity the macrophytes are frequently brought to the lagoon margin, destroying this important habitat. It has been increasing since the 1980s as a result of intensi cation of sport shing in the Pantanal. During 1979±1981, there were an estimated ± sport shermen (Silva 1986), but this reached in 1995, being responsible for a catch of 960 t, representing 69% of the total catches in the Pantanal of Mato Grosso do Sul State (Catella, Albuquerque, Peixer & Palmeira 1999). Although the sh fauna is diverse, with a great potential for aquarium trade, with some species already scattered all over the aquarist world, e.g. Hyphessobrycon eques ( ˆH. callistus) and Gymnocorymbus ternetzi, there is no regular exploitation of these sh. Future management of these species requires knowledge of their habitats and the environmental factors structuring sh communities. There is an important question. If most of the lagoons dry out every year killing the vast majority of its sh, would it not be worthwhile collecting the ornamental sh just before they are lost? The habitats studied are intimately related to the main river and su er from any in uence of possible alterations in the channel. The most severe threat to the whole Pantanal ecosystem is the proposed Paraguay±Parana water-way, for grain and cattle 84 transport from Brazil's Centre-west (Cunha 1998). The project will alter the ow regime, as a result of dredging, deepening and widening of channel, rock removal, embankments, etc. There is considerable debate about the social bene t of such a dramatic environmental impact, compared with a possible railway connecting the South Cone. Other threats are hydroelectric reservoirs in the upland, as Manso reservoir, which also interfere with water regime; levees for drying out the oodplain for cattle raising; river siltation because of inappropriate land occupation in the high plateau and the use of pesticides. Acknowledgments This paper is a part of a dissertation submitted by YRS to the Universidade Federal de Mato Grosso do Sul (UFMS) as a partial requirement for a Master Degree in Ecology and Conservation advised by MPJ. We thank CAPES, UNESP, EMBRAPA/CPAP and CNPq for the nancial support and thank Gary R. Su arez and Robson de Souza for the help in the eld work. We also thank EMBRAPA/CPAP for use of the eld station at Leque Farm and laboratory facilities during this project. References Agostinho A.A. (1993) ConsideracË oä es sobre a ictiofauna das principais bacias hidrograâ cas Brasileiras. Encontro Brasileiro de Ictiologia, 10, Anais, SBI/USP, pp. 287±301.

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