Trophic Structure of Fish Assemblages from Mamore´ River Floodplain Lakes

Trophic structure of ﬁsh assemblages from Mamore´ River ﬂoodplain lakes (Bolivia)

Pouilly M, Yunoki T, Rosales C, Torres L. Trophic structure of fish M. Pouilly1,2, T. Yunoki3, assemblages from Mamore´ River floodplain lakes (Bolivia). C. Rosales2, L. Torres3 Ecology of Freshwater Fish 2004: 13: 245–257. Ó Blackwell 1Institut de Recherche pour le De´veloppement Munksgaard, 2004 (IRD), France, 2Instituto de Ecologıá, Universidad Mayor de San Andres, La Paz, Bolivia, 3Univer- Abstract – The fish assemblage of the floodplain of the Mamore´ River sidad Tećnica del Beni, Trinidad, Bolivia (Bolivia) was estimated in eight lakes, corresponding to four habitat types, situated on an environmental gradient related to the river distance: lakes situated near the river, in the forested floodplain, at the floodplain edge and lakes isolated in the savanna. This paper documents the diet of 71 fish species (among the 140 recorded) and compares the taxonomic and trophic structure of fish assemblages between four lake types. The diet analysis was conducted to determine five trophic guilds: algivores/iliophages, herbivores, zooplanktivores, invertivores and piscivores. The taxonomic and trophic structures of the fish assemblages were not similar in the different lake types of the Mamore´ River. The trophic structure of assemblages showed a coarse pattern of dominance of algivores/iliophages Key words: Bolivia; river floodplain; tropical and invertivores, but different situations were observed in relative freshwater fishes; distribution pattern; diet abundance of the trophic groups in relation to the spatial position of the lakes (except for piscivores). Lakes close to the river appeared more Marc Pouilly, Institut de Recherche pour le De´veloppement (IRD), Universite´ Lyon 1, UMR favourable to the microphages (algivores/iliophages, zooplanktivores) CNRS 5023 Ecologie des Hydrosyste`mes although remote lakes appeared more favourable to the macrophages Fluviaux, 43, Bd du 11 Novembre 1918, Bat. (invertivores, herbivores). These results support the general idea that fish Forel, 69622 Villeurbanne Cedex, France; distribution follows a pattern linked to the ecology of the species, and e-mail: [email protected] related to environmental characteristics of the lakes. Accepted for publication April 13, 2004

Un resumen en espan˜ol se incluye detra´s del texto principal de este artı´culo.

Until now little evidence exists about patterns of Introduction organization of neotropical fish assemblages in rela- The ecology of neotropical freshwater fishes has tion to environmental characteristics. Several studies, received increasing attention over the past 2 decades. based on taxonomic structure, lead to discordant However, the knowledge is still fragmented and results on the existence of a pattern and on the concentrated on a few major contributions coming parameters that control the fish distribution (Marlier from the central Amazon, Parana´ and more recently 1968; Bonetto et al. 1970; Cordiviola de Yuan 1980; from Orinoco. Little attention was paid to the Upper Rodrı´guez & Lewis 1997; Henderson & Crampton Amazon system. Because of the great ecological 1997). But it is likely that, even if taxonomic diversity and complexity of the structure and dynamics differences do not exist, ecological patterns of distri- of the Amazon and because of the current paucity of bution should exist. For example, Rodrı´guez & Lewis information, generalization of the species ecological (1997) demonstrated a pattern of piscivorous fish characteristics remains premature and needs to be distribution controlled by water transparency. reinforced. Researches that focus on new investigation This paper documents the diet of the most abundant areas should address basic ecology objectives, before fish species of the Mamore´ River floodplain lakes. The or at the same time as they look at more explicative or taxonomic and trophic structure of the fish assem- predictive goals. blages were determined in eight lakes corresponding

245 Pouilly et al. to four ecological situations ranging from lakes occurs at the end of the wet season (December to situated near the Mamore´ River to lakes isolated in April) and can last as long as 3 or 4 months with a the savanna. The objective was to test the hypothesis potential extension of ca. 150,000 km2 (Loubens et al. that taxonomic and trophic structures of fish assem- 1992). blages are influenced by the position of the lake in the The lakes studied in the present paper correspond to floodplain. four different ecological situations. Six corresponded to oxbow lakes and were situated in the forest gallery, at varying distances from the Mamore´ River. Materials and methods Mamore´ River Study area Two oxbow lakes situated near the Mamore´ River A 2-year fishing survey was undertaken in eight lakes (Tiuco and Verdun 1) were about 10 years old with a situated in the central Mamore´ River floodplain (near morphology similar to the river channel, and with a the city of Trinidad, latitude 14°30¢S–14°52¢S, longi- water depth varying from 17 m during high waters to tude 64°51¢W–65°01¢W; Fig. 1). The Mamore´ River 4 m during low waters. They were connected to the is one of the main tributaries of the Madeira, that Mamore´ River by the way of a short channel (<100 m). drains white waters (Sioli 1964) from the south Bolivian Andes. In the plain of Beni, the Mamore Forest River flows on a landscape dominated by savanna with Two oxbow lakes situated in the middle of the forested some patches of forest confined to the elevated part of floodplain (Siquero and Verdun 2) were more than the plain, and some forest galleries along the rivers. 20 years old with a water depth varying from 8 m Local climatic conditions are marked by the alterna- during high waters to 1 m during low waters. They tion of a wet (October to March) and a dry season were connected to the Mamore´ River by the way of a (April to September). A big annual flood generally small temporal tributary that drains the savanna and

Fig. 1. Study area in the Mamore´ River ﬂoodplain, Bolivia.

246 Trophic structure of Bolivian fish assemblages the floodplain. The channel distance is over 1 km long from the Museo Nacional de Historia Natural of La and flowed through one or two other lakes before Paz, and at the Museum National d’Histoire Naturelle reaching the Mamore´ River. of Paris (Lauzanne & Loubens 1985; Lauzanne et al. 1991). Edge Two oxbow lakes situated at the forested floodplain Fish diet analysis and trophic classification edge (Potrero and Florida) were estimated to be more than 50 years old. The water depth varied between Estimation of diet was based on the analysis of 4 m during high waters and 0.5 m during low waters. stomach contents of fishes covering a range of sizes Florida was connected only by inundation although that we assumed to correspond to the adult stage. After Potrero was connected by the way of a short channel identification of the fish, stomachs were extracted by that converged with a small temporal tributary. They dissection. Empty stomachs or stomachs with almost were situated more of 4 km from the Mamore´ River. fully digested contents were excluded from further analysis. The contents of the remaining stomachs were Savanna examined under a microscope and items were separ- The last two lakes (Coitarama and Suarez) are ated into seven categories: soft substrate; algae or situated in the savanna adjacent to the annual periphyton; aquatic or terrestrial vegetation, fruits or floodplain. They were estimated to be more than seeds; zooplankton (cladocers, rotifers or copepods); 100 years old. The water depth varied from 1 to aquatic invertebrates; terrestrial invertebrates; fish. 2 m throughout the years. During regular hydrologic Invertebrate categories (terrestrial and aquatic) corres- cycles they were isolated all the year round, but ponded mainly to insect prey. The soft substrate connections are probable during strong hydrologic category did not correspond to a biological feeding cycles. resource. It is likely that fish that ingest soft substrate Lakes close to the river may be subjected to are in fact consuming periphyton and algae, which are whitewater invasion (Loubens et al. 1992; Iban˜ez aggregated in the substrate and/or other associated 2000), and are largely influenced by the variations of microorganisms. However, the soft substrate category water level. On the contrary, endogenous waters, local was retained as an indicator for a particular benthic rainwater with characteristics intermediate between feeding. white and blackwaters (Sioli 1964), supply lakes In order to obtain a general qualitative diet for the remotely situated from the river (Loubens et al. 1992; species, results were expressed by the occurrence Iban˜ez 2000). Savannah lakes are less influenced by method (Hyslop 1980). The relative importance of an water level variations (Pouilly et al. 1999). item in the diet was estimated by the number of stomachs that contained that item divided by the total number of nonempty stomachs analysed in the partic- Fish sampling ular species. This method is adapted to describe Fish were sampled using 13 gillnets with a wide range general food habits at an interspecific level and to of mesh sizes (25 m long · 2 m high, mesh size: 10, define broad trophic groups. 15, 20, 25, 30, 35, 40, 50, 60, 70, 80, 90 and 110 mm). In order to show relative level of diet specialization Sampling was conducted during eight periods from of the species, diet breadth was estimated using 2 1 March 1998 to March 2000. For each sampling, Levin’s standardized index Bi j Pij À 1 1 ¼ ½ð Þ À gillnets were left in place for 2 h in the evening n 1 À , where Pij is the proportion of the food (17.00–19.00 hours) and for 2 h in the morning ðcategoryÀ Þ j in the diet of species i, and nPis the number (05.00–07.00 hours) for gillnets of small mesh size of categories (Hurlbert 1978). B 0 indicates a (10–50 mm), and all the night (17.00–07.00 hours) for species that feed only on one food ¼category; B 1 the other mesh size. They were placed near the shore indicates a species that feed equally on all the food¼ and their locations were approximately the same categories. Fish species diets were compared and throughout the study. grouped by cluster analysis (UGPMA algorithm) on an Captured fishes were fixed in buffered formalde- Euclidean distance matrix derived from species scores hyde (4%), transported to the laboratory and then along the four first axis of a correspondence analysis preserved in buffered alcohol (75%). They were of species-food items table. The correspondence identified to the species level (or to genus when analysis is an ordination method, based on chi-square systematic knowledge was inadequate for reliable metric, recommended for analysis of occurrence data identification of the species). Identifications were (Legendre & Legendre 1998). The first few axes based on voucher specimens left by previous system- (generally the first three or four) model the majority of atic research projects at the Trinidad fish collection variation of the matrix (Winemiller 1991) and extract (CIRA-UTB), at the Coleccioń Boliviana de Fauna the main components of ordination of the matrix.

247 Pouilly et al. Analyses were performed using ADE software two lakes situated on the floodplain edge (Chaetobran- (http://pbil.univ-lyon1.fr/ADE-4). Data concerning chus flavescens Heckel), and two species were absent 48 species comes from a previous work (Pouilly only from these two lakes [Mylossoma aureum et al. 2003). (Agassiz), Pellona castelnaeana Valenciennes]. Phe- nacogaster sp. was recorded only in the two lakes from the forested floodplain. Seven Siluriformes species were Taxonomic and trophic structure present in the four lakes situated near the Mamore´ River Taxonomic structure was estimated by the presence– and were absent from the other four lakes [Ageniosus absence data of the species in the lakes. A Jaccard sp., Centromochulus sp., Opsodoras sp., Sturisoma index was used to calculate a pairwise matrix of nigrirostrum Fowler, Pseudohemiodon laticeps taxonomic similarity between the eight lakes, and a (Regan), Ancistrus sp., Calophysus macropterus (Lich- cluster analysis (UPGMA algorithm) was performed to tenstein)]. classify the lakes according to their taxonomic similarity. Analysis was performed using ADE software. Diet composition and classification Relative densities of each trophic group were used to compare the trophic structure between lakes. They were Diet varied among the species (Table 2) and cluster estimated by compiling the CPUE of species showing at analysis allowed five groups of species showing general least five individuals captured and two occurrences. similar diet profiles to be distinguished: algivores/ Detail presentation of the CPUE by lake and sampling iliophages, herbivores, zooplanktivores, invertivores, date will be presented on a future analysis. Relative piscivores (Fig. 3). Each group showed one or two densities of trophic groups were transformed as arcsine dominant diet items but the estimated diet breadth (B) (p0.5) to fit better statistical assumptions. indicates that algivores/iliophages present the higher food specialization (B 0.130) and invertivores the lower (B 0.319; anova¼ test with a P < 0.001; Results Table 2). The¼ invertivores group showed a wide range of diet based on a high level of consumption of aquatic Taxonomic composition invertivores, except for five species that were more A total of 140 species were captured (Table 1). specialized on terrestrial invertebrates. For example, Characiformes (46% of the species) and Siluriformes Auchenipterus nuchalis (Spix & Agassiz) appeared to (34%) dominated the assemblage. Gymnotiformes be specialized on aquatic invertebrates (B 0.055), (7%), Perciformes (7%) and Clupeiformes (3%) were Thoracocharax stellatus (Kner) on terrestrial¼inverte- secondary taxonomic groups. The species richness of brates (B 0.1), although Sternopygus macrurus the lakes ranged from 70 to 99 species. There were (Bloch & Schneider)¼ feeds equally on aquatic inverte- fewer species in the lakes of floodplain edge and brates, vegetation and fish (B 0.595). savanna and more in the four lakes closed to the Of the 71 analysed species¼ (Table 2), 25 (35%) Mamore´ River (Table 1). depended mainly on vegetal resources (algae or Species composition of the assemblages appeared macrovegetation) and 46 (65%) on animal resources. spatially structured according to lake type (Fig. 2). The Omnivorous species, consuming both animal and cluster analysis of the similarities of species occurrence vegetal resources, occurred in all the guilds, but only (Jaccard coefficient) grouped the lakes in accordance seven species show a co-dominance (more than 50% with their spatial position. The first hierarchical distinc- of occurrence of one item) between both resources tion separated savanna lake assemblages from the [Opsodoras sp., Eigenmannia virescens (Valenci- assemblages of annual floodplain lakes. The second ennes, 1842), Mylossoma duriventre (Cuvier), Marki- distinction separated the assemblage of floodplain edge ana nigripinnis (Perugia), Ctenobrycon spilurus lakes from the assemblages of four other annual (Valenciennes), Sternopygus macrurus (Bloch & floodplain lakes. Twenty-four species were present in Schneider), Pimelodella spp.] all eight lakes and 21 species were present in only one lake (Table 1). Five species were present only in the two Trophic structure savanna lakes [Metynnis maculatus (Kner), Apteronotus albifrons (Linnaeus), Crenicichla cf. semicincta Steind- Trophic quantitative structure of the assemblages achner, Satanoperca jurupari (Heckel), Platydoras was based on the density of 103 species (Table 1). costatus (Linnaeus)] and five were absent only from Diet classification of the species that were not these two lakes [Parecbasis cyclolepis (Eigenmann), included in the diet analysis was estimated from Rhaphiodon vulpinus Spix & Agassiz, Engraulidae, bibliographic references related to the species or Auchenipterus nuchalis (Spix & Agassiz), Epapterus sometimes to different species from the same genus dispilurus Cope]. One species was present only in the (Appendix 1).

248 Trophic structure of Bolivian ﬁsh assemblages

Table 1. Occurrence and total abundance of 140 species captured in eight ﬂoodplain lakes of the Mamore´ River (Bolivia). Species are listed according to taxonomic classiﬁcation.

Lake type

Mamore´ River Forested ﬂoodplain Floodplain edge Savanna Species Total code Order/family Species, authority Tiuco Verdun 1 Siquero Verdun 2 Florida Potrero Coitarama Suarez abundance

Beloniformes BELSP Belonidae Potamorrhaphis cf. eigenmanni 1 0 0 0 0 1 1 0 3 Miranda-Ribeiro, 1915 Characiformes ACEAL Acestrorhynchidae Acestrorhynchus spp. 1 1 1 1 1 1 1 1 387 LEOFR Anostomidae Leporinus friderici friderici 1 1 1 1 1 1 1 1 86 (Bloch, 1794) LEOTR Anostomidae Leporinus trifasciatus 0 0 0 1 0 0 0 0 1 Steindachner, 1876 RHYMI Anostomidae Rhytiodus microlepis 1 1 1 1 1 1 0 1 107 Kner, 1858 SCHFA Anostomidae Schizodon fasciatus Spix & 1 1 1 1 1 1 1 1 154 Agassiz, 1829 AGOSP Characidae Agoniates cf. anchovia 1 0 1 0 0 0 0 0 9 Eigenmann, 1914 APYAN Characidae Aphyocharax anisitsi Eigenmann 0 0 0 0 1 1 1 0 338 & Kennedy, 1903 BRYSP Characidae Brycon cf. cephalus 1 0 0 0 0 0 1 0 3 (Gu¨nther, 1869) CHXGI Characidae Charax gibbosus 1 1 1 1 1 0 1 1 21 (Linnaeus, 1758) ROBAF Characidae Roeboides afﬁnis 1 1 1 1 1 1 1 1 968 (Gu¨nther, 1868) EUCSP Characidae Roeboides biserialis 1 0 0 0 0 1 0 0 11 (Garman, 1890) ROBMY Characidae Roeboides myersii Gill, 1870 1 1 1 1 1 1 1 1 277 PIBME Characidae Piabucus melanostomus 0 0 0 0 0 0 0 1 3 Holmberg, 1891 ASYAB Characidae Astyanax abramis 0 0 1 0 0 0 1 0 2 (Jenyns, 1842) ASXBI Characidae Astyanax bimaculatus 0 0 0 0 1 0 1 1 48 (Linnaeus, 1758) CTEPI Characidae Ctenobrycon spilurus 1 1 0 1 1 1 1 1 183 (Valenciennes, 1850) GYCTE Characidae Gymnocorymbus ternetzi 0 0 1 0 0 0 1 0 2 (Boulenger, 1895) HEGSP Characidae Hemigrammus sp. 0 0 1 0 0 0 0 0 4 MARNI Characidae Markiana nigripinnis 0 0 0 1 1 0 1 1 35 (Perugia, 1891) MOEDI Characidae Moenkhausia dichroura 1 1 1 1 1 1 1 1 11748 (Kner, 1858) PAECY Characidae Parecbasis cyclolepis 1 1 1 1 1 1 0 0 431 Eigenmann, 1914 PHGSP Characidae Phenacogaster sp. 0 0 1 1 0 0 0 0 4 TRPAL Characidae Triportheus albus Cope, 1872 1 1 1 1 1 1 1 1 1336 TRPAN Characidae Triportheus angulatus 1 1 1 1 1 1 1 1 1834 (Spix & Agassiz, 1829) TRICU Characidae Triportheus culter (Cope, 1872) 1 0 0 0 0 0 0 0 3 TRISP Characidae Triportheus sp. 0 1 1 0 0 0 0 1 4 COLMA Characidae Colossoma macropomum 1 1 1 0 1 1 1 0 35 (Cuvier, 1818) METHY Characidae Metynnis hypsauchen 0 0 1 0 0 1 1 1 13 (Mu¨ller & Troschel, 1844) METMA Characidae Metynnis maculatus 0 0 0 0 0 0 1 1 30 (Kner, 1858) MYETI Characidae Myleus tiete (Eigenmann & 0 0 1 0 0 0 1 1 3 Norris, 1900) MYLAU Characidae Mylossoma aureum 1 1 1 1 0 0 1 1 32 (Agassiz, 1829) MYLDU Characidae Mylossoma duriventre 1 1 1 1 1 1 1 1 157 (Cuvier, 1818)

249 Pouilly et al.

Table 1. Continued.

Lake type River

Mamore´ River Forested ﬂoodplain Floodplain edge Savanna Species Total code Order/family Species, authority Tiuco Verdun 1 Siquero Verdun 2 Florida Potrero Coitarama Suarez abundance

PIRBR Characidae Piaractus brachypomus (Cuvier, 1818) 0 0 0 0 1 1 1 0 4 PYGNA Characidae Pygocentrus nattereri Kner, 1858 1 1 1 1 1 1 1 1 397 SERCO Characidae Serrasalmus compressus Je´gu, 1 1 1 1 1 1 1 1 21 Leaõ & Santos, 1991 PRSEI Characidae Serrasalmus eigenmanni Norman, 1929 1 0 1 1 0 1 1 1 115 SEREL Characidae Serrasalmus elongatus Kner, 1858 1 0 1 1 0 1 1 0 23 SERHO Characidae Serrasalmus hollandi Eigenmann, 1915 1 1 1 1 1 1 1 1 372 SERRH Characidae Serrasalmus rhombeus 1 1 1 1 1 1 1 1 474 (Linnaeus, 1766) SERPI Characidae Serrasalmus spilopleura Kner, 1858 0 0 1 0 1 0 1 1 37 POPCO Characidae Poptella compressa (Gu¨nther, 1864) 0 1 1 0 1 1 1 1 235 STTCR Characidae Stethaprion crenatum Eigenmann, 1916 0 1 1 1 1 1 1 1 163 TETAR Characidae Tetragonopterus argenteus Cuvier, 1816 0 1 1 1 0 0 1 0 7 CUASP Curimatidae Curimata sp. 1 0 0 0 0 0 1 1 27 CUEAI Curimatidae Curimatella alburna 1 1 1 1 1 1 1 1 1069 (Mu¨ller & Troschel, 1844) CUEDO Curimatidae Curimatella dorsalis 0 0 1 0 0 0 0 1 55 (Eigenmann & Eigenmann, 1889) CUEOC Curimatidae Curimatella immaculata 1 1 1 0 0 0 0 0 38 (Fernańdez-Ye´pez, 1948) CUEME Curimatidae Curimatella meyeri (Steindachner, 1882) 1 1 1 1 0 1 1 1 131 CUESP Curimatidae Curimatella sp. 1 1 0 0 0 0 1 1 431 POTAL Curimatidae Potamorhina altamazonica 1 1 1 1 1 1 1 1 135 (Cope, 1878) POTLA Curimatidae Potamorhina latior 1 1 1 1 1 1 1 1 2058 (Spix & Agassiz, 1829) PSEAM Curimatidae Psectrogaster amazonica 0 0 1 1 1 1 1 0 95 Eigenmann & Eigenmann, 1889 PSECU Curimatidae Psectrogaster curviventris 1 1 1 1 1 1 1 0 119 Eigenmann & Kennedy, 1903 PSERU Curimatidae Psectrogaster rutiloides (Kner, 1858) 1 1 1 1 1 1 1 0 395 PSESP Curimatidae Psectrogaster sp. 0 1 1 0 0 0 0 0 2 STISP Curimatidae Steindachnerina sp. 1 1 0 0 1 0 0 0 14 CYNGI Cynodontidae Cynodon gibbus Spix & Agassiz, 1829 1 0 0 1 0 1 1 0 29 HYDSC Cynodontidae Hydrolycus scomberoides 1 1 1 1 1 1 1 0 65 (Cuvier, 1816) RAPVU Cynodontidae Rhaphiodon vulpinus 1 1 1 1 1 1 0 0 69 Spix & Agassiz, 1829 HOEUN Erythrinidae Hoplerythrinus unitaeniatus 0 0 0 0 0 0 1 0 1 (Agassiz, 1829) HOPMA Erythrinidae Hoplias malabaricus (Bloch, 1794) 1 0 1 1 1 1 1 1 132 TORST Gasteropelecidae Thoracocharax stellatus (Kner, 1858) 1 1 1 1 1 0 0 0 21 EIGME Hemiodontidae Anodus elongatus Agassiz, 1829 1 1 1 1 1 1 1 1 938 PYRSP Lebiasinidae Pyrrhulina vittata Regan, 1912 0 0 0 0 1 0 0 0 1 PRONI Prochilodontidae Prochilodus nigricans 1 1 1 1 1 1 1 1 133 Spix & Agassiz, 1829 Clupeiformes PELCA Pristigasteridae Pellona castelnaeana 1 1 1 1 0 0 1 1 187 Valenciennes, 1847 PELFL Pristigasteridae Pellona flavipinnis (Valenciennes, 1836) 1 1 1 1 1 1 0 1 968 ANHSP Engraulidae Anchoviella cf. carrikeri Fowler, 1940 0 0 0 1 0 0 0 0 2 ENGSP Engraulidae Engraulidae sp. 1 1 1 1 1 1 0 0 1701 Gymnotiformes ADOSA Apteronotidae Adontosternarchus sachsi 0 1 1 1 0 1 0 0 73 APTAL Apteronotidae Apteronotus albifrons (Linnaeus, 1766) 0 0 0 0 0 0 1 1 9 STNSP Apteronotidae Sternarchorhynchus sp. 0 0 1 0 0 0 0 0 2 GYMCA Gymnotidae Gymnotus carapo Linnaeus, 1758 0 0 0 0 1 1 1 0 4 HYPSP Hypopomidae Brachyhypopomus 0 1 0 1 0 1 0 1 15 cf. brevirostris (Steindachner, 1868) RHPRO Rhamphichthyidae Rhamphichthys rostratus 0 1 1 0 1 1 0 1 19 (Linnaeus, 1766)

250 Trophic structure of Bolivian ﬁsh assemblages

Table 1. Continued.

Lake type River

Mamore´ River Forested ﬂoodplain Floodplain edge Savanna Species Total code Order/family Species, authority Tiuco Verdun 1 Siquero Verdun 2 Florida Potrero Coitarama Suarez abundance

DISCO Sternopygidae Distocyclus conirostris 0 0 0 0 0 0 0 1 1 (Eigenmann & Allen, 1942) EAIUM Sternopygidae Eigenmannia humboldtii 1 1 0 1 0 1 0 1 52 (Steindachner, 1878) EAIVI Sternopygidae Eigenmannia virescens 0 1 1 1 1 1 1 1 259 (Valenciennes, 1842) STOMA Sternopygidae Sternopygus macrurus 1 1 1 0 1 1 0 1 29 (Bloch & Schneider, 1801) Perciformes ASNCR Cichlidae Astronotus crassipinnis (Heckel, 1840) 1 0 0 0 0 0 0 0 2 CHAOR Cichlidae Chaetobranchopsis orbicularis 1 0 1 0 0 0 0 1 3 (Steindachner, 1875) CHAFL Cichlidae Chaetobranchus ﬂavescens 0 0 0 0 1 1 0 0 2 Heckel, 1840 AEQSP Cichlidae Aequidens sp. 0 0 0 0 0 0 1 0 1 BATSP Cichlidae Crenicichla sp. 0 0 0 0 0 0 0 1 1 CICMO Cichlidae Cichla monoculus Spix & Agassiz, 1831 1 0 0 0 0 0 1 1 19 CRISE Cichlidae Crenicichla cf. semicincta 0 0 0 0 0 0 1 1 3 Steindachner, 1892 SATJU Cichlidae Satanoperca jurupari (Heckel, 1840) 0 0 0 0 0 0 1 1 4 PACTR Sciaenidae Pachypops triﬁlis 1 0 0 0 0 0 0 0 1 (Mu¨ller & Troschel, 1848) PLGSQ Sciaenidae Plagioscion squamosissimus 1 1 1 1 1 1 1 0 492 (Heckel, 1840) Pleuronectiformes ACHAC Achiridae Achirus achirus (Linnaeus, 1758) 1 0 0 0 0 0 0 0 1 Rajiformes POASP Potamotrygonidae Potamotrygon cf. motoro 0 1 1 0 1 1 1 1 17 (Mu¨ller & Henle, 1841) Siluriformes AGEBR Ageneiosidae Ageneiosus inermis (Linnaeus, 1766) 1 1 1 1 0 1 0 0 72 AGEMA Ageneiosidae Ageneiosus brevis Steindachner, 1881 0 1 1 1 0 1 0 0 384 AGESP Ageneiosidae Ageneiosus sp. 1 1 1 1 0 0 0 0 14 AGEUC Ageneiosidae Ageneiosus ucayalensis Castelnau, 1855 0 0 1 0 0 0 0 0 11 TYMSP Ageneiosidae Tympanopleura sp. 1 1 1 1 1 0 0 0 246 SIASP Aspredinidae Bunocephalus sp. 0 0 1 0 0 0 0 0 1 AUCNU Auchenipteridae Auchenipterus nuchalis 1 1 1 1 1 1 0 0 289 (Spix & Agassiz, 1829) CENSP Auchenipteridae Centromochlus sp. 1 1 1 1 0 0 0 0 144 ENTBE Auchenipteridae Entomocorus benjamini 0 1 1 1 1 1 1 1 307 Eigenmann, 1917 EPADI Auchenipteridae Epapterus dispilurus Cope, 1878 1 1 1 1 1 1 0 0 124 PAUST Auchenipteridae Trachelyopterus striatulus 0 1 1 0 1 1 1 1 68 (Steindachner, 1877) TATAU Auchenipteridae Tatia aulopygia (Kner, 1858) 0 0 1 0 0 0 0 0 1 BROSL Callichthyidae Brochis splendens (Castelnau, 1855) 0 1 1 1 0 0 0 0 44 CORSP Callichthyidae Corydoras sp. 0 1 1 1 0 0 0 0 64 DIALO Callichthyidae Dianema longibarbis Cope, 1872 0 0 1 0 1 0 0 0 5 HOSLI Callichthyidae Hoplosternum littorale (Hancock, 1828) 0 0 0 0 1 0 0 0 3 HOSTO Callichthyidae Megalechis thoracata 0 0 1 1 1 0 1 0 27 (Valenciennes, 1840) ANAWE Doradidae Anadoras weddellii (Castelnau, 1855) 0 0 0 1 1 1 0 0 19 ASDAS Doradidae Astrodoras asterifrons (Kner, 1853) 0 0 1 0 0 0 0 0 1 DORSP Doradidae Doras sp. 1 1 1 1 1 1 1 1 178 OPSSP Doradidae Opsodoras sp. 1 1 1 1 0 0 0 0 120 PLACO Doradidae Platydoras costatus (Linnaeus, 1758) 0 0 0 0 0 0 1 1 10 PSDNI Doradidae Oxydoras niger (Valenciennes, 1821) 1 0 0 0 1 1 1 1 30 PTEGR Doradidae Pterodoras granulosus 1 0 1 0 0 0 0 1 4 (Valenciennes, 1821) TRYPA Doradidae Trachydoras paraguayensis 1 1 1 1 1 1 0 1 114 (Eigenmann & Ward, 1907)

251 Pouilly et al.

Table 1. Continued.

Lake type River

Mamore´ River Forested ﬂoodplain Floodplain edge Savanna Species Total code Order/family Species, authority Tiuco Verdun 1 Siquero Verdun 2 Florida Potrero Coitarama Suarez abundance

PIESP Heptapteridae Pimelodella spp. 1 1 1 1 1 1 1 1 721 HYTJO Loricariidae Hypoptopoma joberti 1 1 1 1 1 1 1 1 3644 (Vaillant, 1880) HYSSP Loricariidae Hypostomus sp. 1 0 1 0 1 1 1 1 18 PTYMU Loricariidae Pterygoplichthys sp. 1 0 1 1 1 1 1 1 129 HENAC Loricariidae Hemiodontichthys acipenserinus 0 0 0 1 0 1 1 1 15 (Kner, 1853) RINLA Loricariidae Rineloricaria cf. lanceolata 0 1 1 0 0 1 0 1 7 (Gu¨nther, 1868) STUNI Loricariidae Sturisoma nigrirostrum Fowler, 1940 1 1 1 1 0 1 0 0 107 LOASI Loricariidae Loricaria cf. simillima Regan, 1904 1 1 1 1 0 1 0 1 119 LOIMA Loricariidae Loricariichthys maculatus (Bloch, 1794) 1 1 1 1 1 1 1 1 164 PSHLA Loricariidae Pseudohemiodon laticeps 1 1 1 1 0 0 0 1 43 (Regan, 1904) ANCSP Loricariidae Ancistrus sp. 1 1 1 1 0 0 0 0 7 HESPL Pimelodidae Hemisorubim platyrhynchos 1 1 1 0 0 1 1 1 8 (Valenciennes, 1840) LEIMA Pimelodidae Leiarius marmoratus (Gill, 1870) 0 0 0 0 0 1 0 0 1 PHREM Pimelodidae Phractocephalus hemioliopterus 0 1 0 0 0 0 0 0 1 (Bloch & Schneider, 1801) PIMFL Pimelodidae Pimelodina ﬂavipinnis 0 1 0 0 0 0 0 0 1 Steindachner, 1876 PIUMA Pimelodidae Pimelodus gr. maculatus-blochi 1 1 1 1 1 1 1 1 479 PINPI Pimelodidae Pinirampus pirinampu 1 1 1 1 0 1 0 0 46 (Spix & Agassiz, 1829) PSLFA Pimelodidae Pseudoplatystoma fasciatum 1 1 1 1 0 1 1 1 28 (Linnaeus, 1766) PSLTI Pimelodidae Pseudoplatystoma tigrinum 1 0 1 0 1 1 1 0 24 (Valenciennes, 1840) SORLI Pimelodidae Sorubim lima 1 1 1 1 1 1 0 1 196 (Bloch & Schneider, 1801) HYAED Pimelodidae Hypophthalmus edentatus 1 1 1 1 1 1 1 1 109 Spix & Agassiz, 1829 HYAMA Pimelodidae Hypophthalmus marginatus 1 1 1 1 1 1 0 1 166 Valenciennes, 1840 CAOMA Pimelodidae Calophysus macropterus 1 1 1 1 0 0 0 0 84 (Lichtenstein, 1819) Lake species richness 83 81 99 79 70 79 76 75

In all the lakes, assemblages were co-dominated Discussion by algivores/iliophages and invertivores while piscivores were secondary. Herbivores and zooplankti- The fish assemblage of the Mamore´ River floodplain vores appeared in low density. However, the trophic lakes included 140 of the 327 species compiled by structure of the assemblages appeared to be modified Lauzanne et al. (1991) in the Mamore´ River water- according to the lake type (Fig. 4). All the trophic shed. These species belonged mainly to orders Char- groups, except piscivores, showed a significant aciformes and Siluriformes and secondary to the variation in relative abundance between the four Gymnotiformes, Perciformes and Clupeiformes. This lake types (anova test with a P < 0.012, P 0.536 is almost a general pattern in the South American for piscivores). Assemblages of the lakes ¼situated freshwaters (Lowe-Mc Connell 1987; Rodrı´guez & near the Mamore´ River and in the middle of the Lewis 1990; Pouilly et al. 1999). forested floodplain possessed a higher density of The 140 species of the Mamore´ River floodplain algivores/iliophages and a lower density of herbiv- lakes showed a pattern of distribution marked by the ores. In contrast, assemblages of the lakes situated influence of the lake’s position on the floodplain. The in the savanna and at the edge of the floodplain assemblages appeared more similar between lakes showed a higher density of invertivores and a lower from the same position rather than between lakes density of zooplanktivores. Piscivores were of the from different positions. The major faunal difference same importance in all the lakes. appeared between the floodplain lake and savanna

252 Trophic structure of Bolivian ﬁsh assemblages

Fig. 2. Clustering of fish assemblages of eight lakes from Mamore´ River floodplain (Bolivia) calculated by a UPGMA algorithm on a matrix of Jaccard similarity index. lakes. This result could be the product of the the Mamore´ River. This result is concordant with the isolation of the latter. During the flood, oxbow lakes observations of Soares et al. (1986) for the fish assem- of forested floodplain are connected, although blage of the central Amazonian whitewater floodplain, savanna lakes stay isolated. Flood provides water and indicated, for the both systems, an under-utilisation homogenisation (Pouilly et al. 1999) and connections of macrophyte items. In contrast, in the nutrient poor favourable for species exchange in all the six oxbow Machado river, Goulding (1980) observed a broad lakes studied. Differences in lake characteristics may partitioning of food resources between herbivores, also explain the restricted distribution of some carnivores and microphages but concluded that forest species (Marlier 1968; Lowe-Mc Connell 1987; material is the essential resource for the fish assemblage. Henderson & Crampton 1997). However, the faunal In the Mamore´ River floodplain, despite the general specificity (number of exclusive species) between pattern of dominance, differences were observed in the lake types was relatively low. Among the 140 species relative abundance of the trophic groups that could be captured, only 10 species were exclusive to savanna coarsely related to water chemistry and lake charac- or to oxbow floodplain lakes. Accordingly, Hender- teristics. Lakes close to the river may be subjected to son & Crampton (1997), in a comparison of white whitewaters invasion, and are assumed to be nutrient- and blackwater Upper Amazon lakes, reported that rich and support a high primary production. They are many species were caught in both habitats and that largely influenced by the variations of water level that the habitats differ essentially in the relative abun- constrain the development of littoral floating mead- dance of species. Machado-Allison (1990) also noted ows, and thus limit the terrestrial supplies to the wet that different habitats of the floodplain could be season. Correlatively, these lakes appeared to be more seasonally or permanently used by a same species. favourable to the microphagous species (algivores/ These results seem to indicate that fish distribution iliophages, zooplanktivores) that are directly depend- patterns could be more evident at quantitative level ent on primary production. In contrast, lakes remote rather than at qualitative level. from the river showed higher relative density of The five trophic guilds (algivores/iliophages, herbi- macrophages (invertivores and herbivores), except vores, zooplanktivores, invertivores and piscivores) piscivores. They possessed characteristics that are determined in this study correspond to a large range of assumed to be more favourable to these species rather categories presented in other Amazonian fish trophic to microphages (poor nutrient water, surrounding studies (Marlier 1968; Kno¨ppel 1970; Goulding 1980; vegetation, habitat stability). As estimation of Soares et al. 1986). The same five guilds were deter- resources availability is difficult and then often mined and discussed in a previous work including the 48 neglected in trophic studies of Amazonian fish most abundant species (Pouilly et al. 2003). assemblage (Soares et al. 1986), links between habitat Globally, there is a dominance of algivores/iliophag- characteristics, resource availability and fish trophic es, invertivores and piscivores in the floodplain lakes of structure remain to be tested at both the regional and

253 Pouilly et al.

Table 2. Diet composition and breadth (B, Levin’s standardised index) of 71 fish species of the Mamore´ River floodplain lakes (Bolivia) expressed by relative occurrence of seven food categories. Soft substrate (MUD); algae or periphyton (ALG); aquatic or terrestrial vegetation, fruits or seeds (VEG); zooplankton (cladocers, rotifers or copepods, ZOO); aquatic invertebrates (AIN); terrestrial invertebrates (TIN); fish (FISH). Species are grouped according to cluster analysis results (Fig. 3). Values in bold correspond to values up to 50%.

Species code No. of stomachs MUD ALG VEG ZOO AIN TIN FISH B

Zooplanktivores AGEMA 39 0.00 0.00 0.00 97.44 23.08 0.00 0.00 0.075 EPADI 8 0.00 0.00 0.00 87.50 25.00 12.50 0.00 0.142 HYAMA 17 0.00 23.53 5.88 58.82 11.76 0.00 11.76 0.315 HYAED 7 0.00 42.86 14.29 57.14 28.57 0.00 0.00 0.389 APYAN 95 0.00 30.53 2.11 89.47 97.89 9.47 0.00 0.305 Algivores/iliophagesà RHYMI 26 0.00 88.46 11.54 0.00 3.85 7.69 0.00 0.091 CUEDO 15 0.00 100.00 0.00 0.00 0.00 0.00 0.00 0.000 PSEAM 51 0.00 100.00 0.00 0.00 0.00 0.00 0.00 0.000 ENGSP 68 5.88 95.59 0.00 0.00 7.35 0.00 0.00 0.047 STISP 14 14.29 100.00 0.00 0.00 0.00 0.00 0.00 0.047 STUNI 52 9.62 100.00 0.00 0.00 0.00 0.00 0.00 0.032 HYTJO 70 5.71 92.86 0.00 0.00 0.00 1.43 0.00 0.026 PSERU 118 5.08 98.31 0.00 0.00 0.00 0.85 0.00 0.020 LOIMA 25 28.00 88.00 12.00 0.00 16.00 0.00 0.00 0.220 EIGME 144 25.69 90.28 0.00 4.17 6.94 0.00 0.00 0.137 PTYMU 8 50.00 25.00 12.50 0.00 0.00 0.00 12.50 0.318 POTAL 38 55.26 52.63 2.63 5.26 0.00 0.00 0.00 0.215 PSHLA 20 70.00 100.00 0.00 0.00 0.00 0.00 0.00 0.157 CUEOC 10 90.00 100.00 0.00 0.00 0.00 0.00 0.00 0.166 CUEAI 165 70.91 68.48 3.03 0.00 0.00 0.00 0.00 0.181 PRONI 27 37.04 66.67 3.70 0.00 0.00 7.41 0.00 0.207 CUEME 9 44.44 66.67 11.11 0.00 0.00 0.00 0.00 0.214 PSECU 60 58.33 80.00 11.67 0.00 5.00 0.00 0.00 0.235 POTLA 211 40.76 77.73 0.00 5.21 0.00 0.00 0.00 0.163 Piscivores§ AGESP 7 14.29 0.00 14.29 14.29 0.00 0.00 85.71 0.179 ACEAL 51 1.96 1.96 1.96 0.00 0.00 3.92 96.08 0.035 HYDSC 10 0.00 0.00 10.00 0.00 10.00 10.00 90.00 0.119 RAPVU 12 0.00 0.00 8.33 0.00 8.33 8.33 91.67 0.097 SERRH 76 0.00 1.32 5.26 0.00 10.53 7.89 94.74 0.094 PLGSQ 80 0.00 0.00 5.00 0.00 15.00 2.50 90.00 0.086 CAOMA 28 0.00 3.57 14.29 0.00 7.14 3.57 85.71 0.119 PELCA 43 0.00 0.00 9.30 0.00 4.65 4.65 93.02 0.070 SERHO 90 0.00 2.22 11.11 1.11 6.67 2.22 90.00 0.092 HOPMA 28 21.43 10.71 0.00 0.00 3.57 7.14 71.43 0.213 PINPI 8 0.00 0.00 0.00 0.00 25.00 25.00 62.50 0.242 TYMSP 55 1.82 1.82 9.09 5.45 16.36 18.18 67.27 0.291 PRSEI 32 0.00 6.25 21.88 0.00 34.38 9.38 59.38 0.374 PYGNA 87 0.00 2.30 32.18 1.15 5.75 12.64 62.07 0.275 PELFL 120 0.00 0.00 2.50 3.33 52.50 6.67 66.67 0.231 ROBAF 154 0.00 1.30 0.65 9.74 55.19 2.60 61.69 0.246 ROBMY 33 0.00 0.00 0.00 6.06 75.76 18.18 42.42 0.261 Herbivores– METMA 6 0.00 0.00 100.00 0.00 16.67 33.33 0.00 0.163 SCHFA 43 2.33 30.23 74.42 0.00 4.65 0.00 0.00 0.154 COLMA 14 7.14 7.14 71.43 0.00 7.14 0.00 21.43 0.214 DORSP 58 18.97 79.31 82.76 12.07 34.48 5.17 1.72 0.450 LEOFR 10 0.00 50.00 80.00 0.00 10.00 20.00 10.00 0.340 Invertivores PAUST 18 0.00 5.56 11.11 0.00 33.33 55.56 27.78 0.412 STTCR 68 0.00 10.29 32.35 0.00 32.35 64.71 1.47 0.353 POPCO 52 1.92 0.00 28.85 0.00 25.00 69.23 7.69 0.298 TRPAL 94 0.00 8.51 31.91 3.19 26.60 74.47 2.13 0.321 TORST 4 0.00 0.00 0.00 0.00 25.00 75.00 0.00 0.100 HOSTO 7 0.00 28.57 0.00 28.57 100.00 0.00 0.00 0.187 CENSP 32 0.00 0.00 9.38 0.00 87.50 28.13 0.00 0.138 AUCNU 26 0.00 3.85 0.00 3.85 96.15 7.69 0.00 0.055 PAECY 26 3.85 30.77 3.85 0.00 76.92 0.00 3.85 0.176 CORSP 18 0.00 27.78 11.11 5.56 94.44 5.56 0.00 0.185 ADOSA 27 0.00 18.52 3.70 7.41 85.19 3.70 0.00 0.138

254 Trophic structure of Bolivian ﬁsh assemblages

Table 2. Continued.

Species code No. of stomachs MUD ALG VEG ZOO AIN TIN FISH B

ASXBI 4 0.00 25.00 25.00 0.00 75.00 25.00 0.00 0.333 BROSL 7 0.00 14.29 14.29 0.00 85.71 14.29 0.00 0.179 TRYPA 25 12.00 4.00 24.00 16.00 96.00 4.00 0.00 0.230 OPSSP 27 11.11 40.74 48.15 11.11 77.78 0.00 0.00 0.412 EIAVI 57 0.00 52.63 42.11 5.26 91.23 14.04 3.51 0.388 MYLDU 18 5.56 11.11 44.44 5.56 38.89 5.56 0.00 0.389 MARNI 13 0.00 23.08 61.54 0.00 38.46 23.08 7.69 0.451 CTEPI 16 0.00 6.25 50.00 6.25 62.50 6.25 6.25 0.313 STOMA 4 0.00 25.00 50.00 0.00 50.00 25.00 50.00 0.595 PIESP 52 19.23 0.00 73.08 3.85 28.85 21.15 25.00 0.473 PIUMA 140 0.71 25.71 23.57 5.00 53.57 37.14 37.14 0.644 ENTBE 91 0.00 0.00 7.69 43.96 58.24 31.87 0.00 0.357 MOEDI 241 0.41 8.30 5.81 26.56 60.17 46.06 0.41 0.389 TRPAN 277 0.36 19.86 20.94 9.75 55.96 53.79 1.44 0.463

Mean value: 0.245; à0.130; §0.178; –0.264; 0.319.

Fig. 3. Clustering of 71 fish species of the Mamore´ River floodplain lakes (Bolivia) according to their diet similarities calculated by a UPGMA algorithm on a matrix of Euclidean distances derived from species scores on the four first axis of a correspondence analysis of Table 2. See Table 1 for species codes.

255 Pouilly et al.

3. El ana´lisis de la dieta logra clasificar a las especies en cinco grupos tro´ficos: algı´voras/ilio´fagas, herbı´voras, zooplancto´fagas, insectı´voras y piscı´voras. 4. La estructura taxono´mica y tro´fica de las comunidades no es similar en las diferentes lagunas de la llanura de inundacioń del Rıó Mamore´. La estructura tro´fica de las comunidades presenta una dominancia general de las especies algı´voras/ilio´fagas y insectı´voras, pero existen variaciones en la abundancia relativa de los grupos tro´ficos en funcioń de la posicioń espacial de las lagunas (excepto por el grupo de los piscı´voros). Las lagunas cercanas al rıó parecen ma´s favorables a las especies micro´fagas (algı´voras/ilio´fagas, zooplancto´fagas), aunque las lagunas ma´s alejadas parecen ser ma´s favorables a las macro´fagas (insect- ´ıvoras, herbı´voras). 5. Estos resultados apoyan la idea general que la distribucioń de Fig. 4. Mean ± SE arcsine transformed relative abundance of los peces sigue un patroń relacionado a la ecologıá de las trophic group in four categories of floodplain lakes of the especies y esta´ de acuerdo a las caracterı´sticas ambientales de Mamore´ River (Bolivia). Mamore´: lakes Tiuco (n 8 sampling las lagunas. date) and Verdun 1 (n 5); forest: lakes Siquero¼(n 8) and Verdun 2 (n 5); edge: lakes¼ Potrero (n 8) and Florida¼(n 5); savanna: lakes¼ Suarez (n 8) and Coitarama¼ (n 5). ¼ Acknowledgements ¼ ¼ This work was part of the BIOBAB project (aquatic biodiver- sity in the Bolivian Amazon basin) developed by IRD, the the local scale. These relationships could help to Instituto de Ecologıá from La Paz University and the Centro de Investigacioń de los Recursos Acua´ticos from Trinidad Uni- explain the differences of herbivore abundance versity. Alfredo Parada from Trinidad University, Jean Louis between the assemblages. Menou and Lionel Christiaen from IRD, helped with logistics, In the Mamore´ River system, temporal variations in fieldwork and identification of specimens. Guido Miranda, biological community composition between high and Gustavo Alvarez y David Kopp helped with fish diet evalua- low water level seem to be non negligable (Pouilly et al. tion. We would like to thank G. Miranda (La Paz) and P.A. 1999). The results presented above suggest that the 140 Hulley (Captown) for language corrections. fish species also showed a pattern of distribution marked by the influence of the lake type on the floodplain. The References differences exist at both taxonomic level (presence/ absence of species) and trophic level (relative abun- Bonetto, A., Cordiviola de Yuan, E. & Pignalberi, C. 1970. dance of trophic groups). Distribution patterns of Nuevos datos sobre poblaciones de peces en ambientes neotropical fish have been explored among a variety lenı´ticos permanentes del Parana´ medio. Physis 30: 141– of water bodies and are generally associated to water 154. chemistry or lake characteristics (Marlier 1968; Lowe- Boujard, T., LeBail P.Y. & Planquette, P. 1988. Donneés biologiques sur quelques espe`ces continentales de Guyane Mc Connell 1987; Henderson & Crampton 1997; Française d’intereˆt piscicole. Aquatic Living Resources 1: Rodrı´guez & Lewis 1997). But these studies generally 107–113. are concerned only at the taxonomic level. Our results Burgess, W.E. 1989. An atlas of freshwater and marine support the idea that fish distribution follows a pattern catfishes: a preliminary survey of the Siluriformes. Neptune linked to the ecology of the species and related to City, New Jersey: T.F.H. Publications. environmental characteristics of the lakes. A future Cordiviola de Yuan, E. 1980. Campanã limnologica ‘Keratella analysis will determine the physical parameters that I’ en el rıó Parana´ medio: taxocenoses de peces de ambientes could explain this observed pattern. lenı´ticos. Ecology (Argentina) 4: 103–113. Dos Santos, G.M. 1990. Pesca e Ecologia dos peixes de Rondoˆnia. Manaus, AM, Brasil: Fundaçaõ Universidade do Resumen Amazonas, 228 pp. Ge´ry, J. 1977. Characoids of the world. Neptune city, New 1. La comunidad de peces de la llanura de inundacioń del Rıó Jersey: T.F.H. Publications, 672 pp. Mamore´ (Bolivia) fue estudiada en ocho lagunas, correspondi- Goulding, M. 1980. The fishes and the forest. Exploration in endo a 4 tipos de ha´bitat, ubicadas en un gradiente ambiental Amazon Natural History. Berkeley, CA: University of relacionado a la distancia al rıó: lagunas en relacioń directa al California Press, 280 pp. rıó, en el medio del bosque de galerıá, en el l´ımite del bosque de Henderson, P.A. & Crampton, G.R. 1997. A comparison of fish galerıá, y aisladas en la sabana. diversity and abundance between nutrient-rich and nutrient- 2. Este articulo presenta la dieta de 71 especies de peces (sobre poor lakes in the Upper Amazon. Journal of Tropical Ecology 140 colectadas) y compara la estructura taxono´mica y tro´fica de 13: 175–198. las comunidades entre los 4 tipos de lagunas.

256 Trophic structure of Bolivian ﬁsh assemblages

Hurlbert, S.H. 1978. The measurement of niche overlap and Sioli, H. 1964. General features of the limnology of Amazonia. some relatives. Ecology 59: 67–77. Verhandlungen Internationale Vereinigung fur Theoretische Hyslop, E.J. 1980. Stomach contents analysis. A review of und Angewandte Limnologie 15: 1053–1058. methods and their applications. Journal of Fish Biology 17: Smith, N.J.H. 1981. Man, fishes, and the Amazon. New York: 411–429. Columbia University Press. Iban˜ez, C. 2000. Composicioń de la comunidad de zooplancton Soares, M.G.M., Almeida, R.G. & Junk, W.J. 1986. The trophic en ocho lagunas de la planicie de inundacioń del rıó Mamore´. status of the fish fauna in Lago Camaleaõ, a macrophyte Thesis de Licenciatura. La Paz, Bolivia: UMSA La Paz dominated floodplain lake in the middle Amazon. Amazoni- University. 85 pp. ana 9: 511–526. Kno¨ppel, H.A. 1970. Food of central Amazonian fishes, Winemiller, K.O. 1991. 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In: Developments in environmental modelling, Vol. 20: Amster- References dam: Elsevier: 853 pp. Species code Guildes (species referenced if different) Loubens, G., Lauzanne, L. & Le Guennec, B. 1992. Les ANCSP Algivores/iliophages Dos Santos 1990 milieux aquatiques de la re´gion de Trinidad (Beńi, Amazonie HYSSP Algivores/iliophages Dos Santos 1990 bolivienne). Revue d’Hydrobiologie Tropicale 25: 3–21. LOASI Algivores/iliophages Dos Santos 1990 (L. cataphracta) Lowe-Mc Connell, R.H. 1987. Ecological studies in tropical RINLA Algivores/iliophages Dos Santos 1990 fish communities. In: Cambridge tropical biology series. CUASP Algivores/iliophages Dos Santos 1990 CUESP Algivores/iliophages Dos Santos 1990, Cambridge: Cambridge University Press, 382 pp. Soares et al. 1986 Machado-Allison, A. 1990. Ecologia de los peces de las areas AGEBR Piscivores/carnivores Dos Santos 1990, inundables de los llanos de Venezuela. Intercienca 15: 411–423. Marrero & Taphorn 1991 Marlier, G. 1968. 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Journal of Fish Biology 52: Dos Santos 1990 PSLTI Piscivores/carnivores Goulding 1980, Smith 1981, 556–569. Novoa et al. 1984, Novoa, D., Ramos, F. & Cartaya, E. 1984. Las pesquerias Boujard et al. 1988, artesanales del rio Orinoco sector Caicara-Cabruta. Parte I. Dos Santos 1990 Memorias de la Sociedad de Ciencias Naturales ’La Salle’, SERCO Piscivores/carnivores Table 2: SEREL, SERPI, Caracas XLIV: 163–215. SERRH, SERHO Planquette, P., Keith P. & LeBail, P.Y. 1996. Atlas des poissons SEREL Piscivores/carnivores Dos Santos 1990 SERPI Piscivores/carnivores Dos Santos 1990 d’eau douce de Guyane. Paris: IEGB -MNHN, INRA, CSP, SORLI Piscivores/carnivores Dos Santos 1990 Ministe`re de l’Environnement, Tome 1, 429 pp. PLACO Invertivores/omnivores Dos Santos 1990 Pouilly, M., Iban˜ez, C., Guttierez, M. & Yunoki, T. 1999. POASP Invertivores/omnivores Dos Santos 1990 Funcionamiento ecolo´gico de las lagunas de la zona de PSDNI Invertivores/omnivores Burgess 1989 inundacioń del rıó Mamore´ (Beni – Bolivia). Revista APTAL Invertivores/omnivores Dos Santos 1990 Boliviana de Ecologıá 6: 41–54. DIALO Invertivores/omnivores Dos Santos 1990 TETAR Invertivores/omnivores Dos Santos 1990 (T. chalceus) Pouilly, M., Lino, F., Bretenoux, J.-G. & Rosales, C. 2003. EAIUM Invertivores/omnivores Table 2: EIAVI Dietary-morphological relationships in a fish assemblage of HENAC Invertivores/Omnivores Burgess 1989 the Bolivian Amazonian floodplain. Journal of Fish Biology HYPSP Invertivores/omnivores Me´rigoux & Ponton 1998 62: 1137–1158. (Brachyhypopomus beebei) Rodrı´guez, M.A. & Lewis, W.M.J. 1997. Structure of fish RHPRO Invertivores/omnivores Planquette et al. 1996 assemblages along environmental gradients in floodplain lakes METHY Herbivores/omnivores Marlier 1968, of the Orinoco river. Ecological Monographs 67: 109–128. Dos Santos 1990 MYLAU Herbivores/omnivores Dos Santos 1990, Rodrı´guez, M.A. & Lewis, W.M.J. 1990. Diversity and species Soares et al. 1986 composition of fish communities of Orinico floodplain lakes. National Geographic Research 6: 319–328.

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