Dietary´–Morphological Relationships in a Fish Assemblage of the Bolivian Amazonian Floodplain

Journal of Fish Biology (2003) 62, 1137´–1158 doi:10.1046/j.1095-8649.2003.00108.x,availableonlineathttp://www.blackwell-synergy.com

Dietary´–morphological relationships in a fish assemblage of the Bolivian Amazonian floodplain

M. POUILLY*†‡, F. LINO†, J.-G. B RETENOUX* AND C. ROSALES† *Institut de Recherche pour le De´veloppement (IRD), Universite´ Lyon 1, Laboratoire d’Ecologie des Hydrosyste`mes Fluviaux, 43, Bd du 11 Novembre 1918, F-69622 Villeurbanne Cedex, France and †Instituto de Ecologı´a, Universidad Mayor de San Andre´s, Bolivia, CP 10077, La Paz, Bolivia

(Received 24 January 2002, Accepted 7 April 2003)

Morphological correlates of diet were examined in 48 species of freshwater fishes from floodplain lakes in the central part of the Mamore´River (Bolivian Amazon). The species were classified, according to the percentage occurrence of seven food items, into eight broad trophic categories: mud feeders, algivores, herbivores, terrestrial invertivores and omnivores, carnivores, zooplanktivores, aquatic invertivores and piscivores. There were significant relationships between the diet and morphology of the fishes even when the effect of taxonomical relatedness between species was eliminated. Relative gut length was the main morphological variable used to order species on a carnivore to mud feeder gradient. Standard length and head and mouth size were the morphological variables most closely associated with prey size. Mud feeder, algivore and piscivore species appeared as the most dietary and morphologically specialized. These results support both the hypotheses that species morphology influences the diet and that morphological similarity is conserved even in comparison with taxonomically unrelated species. # 2003 The Fisheries Society of the British Isles Key words: Bolivia; diet; ecomorphology; river floodplain; tropical freshwater fishes.

INTRODUCTION A correlation between morphological attributes and diet has been sought in testing ecomorphological hypotheses in fish assemblages. The results of studies on diet and morphological relationships in temperate and tropical river fish assemblages, however, have excluded the idea of a general pattern. Some studies have revealed strong relationships between diet and morphology (Gatz, 1979; Wikramanayake, 1990; Winemiller et al., 1995; Piet, 1998; Hugueny & Pouilly, 1999; Xie et al., 2001) while others found relatively weak and indistinct relationships (Grossman, 1986; Douglas & Matthews, 1992; Motta et al., 1995; Winemiller & Adite, 1997). Some relationships between morphological attributes and diet have been encountered repeatedly, e.g. gut length is frequently positively

‡Author to whom correspondence should be addressed. Tel.: þ33 4 72446299; fax: þ33 4 72431141; email: [email protected] 1137 # 2003 The Fisheries Society of the British Isles 1138 M. POUILLY ET AL. correlated with herbivory, gill raker length is often associated with the consumption of plankton and fish size (and related head and mouth size) is com- monly associated with prey size. Relationships also exist between morphological attributes and feeding behaviour, e.g. the orientation of the mouth and the position of the eyes are linked with the position of the fish relative to its food (Gatz, 1979). At present, even though many studies have reported strong relationships between species ecology and morphology, no powerful predictive model exists for fish assemblages. This discrepancy may be partially due to the importance of fish behaviour in determining the type of prey that can be used (Grossman, 1986), the relatively high level of opportunism in freshwater fish species (Hugueny & Pouilly, 1999), the influence of phylogeny on limiting morphological adaptation (Douglas & Matthews, 1992; Motta et al., 1995) and the selection of morphological and dietary variables. Ecomorphological hypotheses include two main considerations: (1) species morphology is likely to be similar within an ecological group and to differ between ecological groups depending on the nature of the resource used and the strategy developed by the species to use it and (2) the morphological variations correspond to a response to selective pressure and result in the phenomenon of convergence: ‘morphological similarity of phylogenetically unrelated species’ (Winemiller, 1991). The present study investigated the trophic ecology and morphology of 48 dominant fish species inhabiting lakes of the floodplain of the Mamore´ River, one of the principal drainages of the Bolivian Amazon.

MATERIALS AND METHODS

STUDY AREA The Bolivian Amazonian plain is situated in the upper watershed of the Madera River, one of the primary tributaries of the Amazon River (Fig. 1). The majority of this territory (c. 550 000 km2) comprises the ‘Llanos de los Moxos’ (province of Beni), a landscape dominated by savannah with some patches of forest confined to the higher part of the plain, and forest galleries (bands of vegetation) along the rivers. The Mamore´River drains the south Bolivian Andes and >85% of the Moxos savannah area, and corresponds to a large floodplain system with a potential flood extension of c. 150 000 km2 (Denevan, 1980). Local climatic conditions are marked by the alternation of a wet season (October to March) and a dry season (April to September). A substantial annual flood (maximum flow in the main channel in February 1987 was 8010 m3 s1) generally occurs at the end of the wet season (December to April) and can last as long as 3 or 4 months (Loubens et al., 1992). The study area is situated in the central part of the Mamore´River (between 14300 and 14520 S and 64510 and 65010 W) near the city of Trinidad (capital of Beni province). Loubens et al. (1992) described the aquatic habitats of the Mamore´River floodplain. The study site included eight lakes in the central Mamore´River floodplain that corresponded to four different ecological habitats: oxbow lakes at three locations (near the river, in the middle of the forest ‘band’ and at the limit between forest and savannah) and savannah lakes. Pouilly et al. (1999) presented a preliminary description of limnological parameters, plankton and fish communities.

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 DIET AND MORPHOLOGY OF AMAZONIAN FISHES 1139

82° 78° 74° 70° 66° 62° 58° 54° 50°

12°

8°

4°

0° Amazon Basin

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8° Rio Madera

12° Beni Study area Rio Mamoré

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0 500 1000 km Bolivia 20° Projection Lambert’s Azimuthal

FIG. 1. Map of the Amazon watershed showing the Bolivian part of the upper Madera basin (Beni plain and Andes) and the study area in the central Mamore´River.

FISH SAMPLING Fishes were sampled using 13 gillnets (25 m long and 2 m depth) with a wide range of mesh sizes (10, 15, 20, 25, 30, 35, 40, 50, 60, 70, 80, 90 and 110 mm). Sampling was conducted during eight periods between March 1998 and March 2000. For each sampling (lake and period), gillnets were left in place for 2 h in the evening (1700´–1900 hours) and for 2 h in the morning (0500´–0700 hours). They were placed near the shore and their locations were approximately the same throughout the study. Captured fishes were preserved in buffered formaldehyde (4%), transported to the laboratory and then placed in buffered alcohol (75%). They were identified at the species level (or at the genus level if systematic knowledge was inadequate). Identification was based on voucher specimens left by a previous systematic research programme (Lauzanne & Loubens, 1985; Lauzanne et al., 1991) at the Trinidad fish collection (CIRA-UTB), the Museo Nacional de Historia Natural, La Paz and at the Muse´e National d’Histoire Naturelle, Paris. The 48 species analysed represented 89% of the total number of individuals captured during the study (M. Pouilly, unpubl. data). Species were selected in order to present a broad range of systematic groups. The 48 species studied belonged to five main orders (Characiformes, Siluriformes, Gymnotiformes, Perciformes and Clupeiformes) and represented 18 families out of the 26 registered during the study (six families of

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Characiformes out of eight collected; seven families of Siluriformes out of nine; two families of Gymnotiformes out of five; one family of Perciformes out of two; two families of Clupeiformes out of two collected). Changes in fish diet and morphology depend on the stage of development and the size of the fish (Me´rigoux & Ponton, 1998). Consequently, for each species, a range of sizes that were assumed to correspond to the adult stage was studied. All the fishes included in the morphological analysis were also used for the analysis of diet. In order to optimize the estimation of diet in a given species, however, extra fishes captured were included in the diet analysis.

FISH DIET ANALYSIS Estimation of diet was based on the analysis of stomach contents. After identification of the fish, the stomach was extracted by dissection. Empty stomachs or stomachs with almost fully digested contents were eliminated. The contents of the remaining stomachs were examined under a microscope and items were separated into seven categories: soft substratum (MUD); algae or periphyton (ALG); aquatic or terrestrial vegetation, fruits or seeds (VEG); zooplankton (cladocerans, rotifers or copepods, ZOO); aquatic invertebrates (AIN); terrestrial invertebrates (TIN); fishes (FISH). The invertebrate categories (terrestrial and aquatic) mainly corresponded to insect prey. The soft substratum category did not correspond to a biological feeding resource. It is likely that fishes that ingest soft substratum are in fact consuming periphyton and algae aggregated to the substratum and other associated microorganisms. Soft substratum, however, was conserved as an indicator for a particular feeding habit. Following Sibbing & Nagelkerke’s (2001) classification, implicit prey size categories were used for the interpretation: ALG ¼ MUD < ZOO < AIN ¼ TIN < VEG < FISH. In order to obtain a general qualitative diet for a given species, results were expressed by the occurrence method. The relative frequency of an item in the diet was estimated by the number of stomachs that contained that item divided by the total number of non- empty stomachs analysed in that particular species.

MORPHOLOGICAL MEASUREMENTS Following the results of other authors who have examined fish ecomorphology (Gatz, 1979; Watson & Balon, 1984; Winemiller, 1991) and especially diet ecomorphology (Motta et al., 1995; Piet, 1998; Hugueny & Pouilly, 1999), 10 morphological variables associated with prey capture and feeding strategy were selected and were measured on 26´–30 individuals of each species. Quantitative morphological variables were entered as a ratio of standard length (LS) in the analysis in order to reduce the allometric (size- dependency) effect and to standardize data for body size differences (Winemiller, 1991). The 10 variables were: LS, the distance from the tip of the snout to the last vertebra; relative head length (HEAD), the ratio between head length (distance from the tip of the snout to the posterior edge of the opercle) and LS; relative mouth height (MOHE), the ratio between mouth height at maximum extension and LS. These three variables were assumed to be directly linked with prey size: fish with a larger head and mouth gap are able to handle larger prey (Gatz, 1979). These variables were expected to be positively correlated with larger items (VEG, AIN, TIN and FISH) and negatively correlated with smaller items (ALG, ZOO and MUD); mouth orientation (MORI), coded following Watson & Balon (1984) and Hugueny & Pouilly (1999) (1, dorsal; 2, terminal; 3, ventrally oblique; 4, ventral). The position of the mouth was assumed to indicate the position of food relative to the fish (Gatz, 1979; Hugueny & Pouilly, 1999). Fishes with a dorsal or a terminal mouth were assumed to obtain their food from the pelagic area (ZOO, TIN and FISH), while fishes with a ventral mouth were thought to feed on benthic resources (ALG, MUD and AIN); relative eye diameter (EYDI), the ratio of the horizontal diameter of the eye and LS. Eye size was assumed to be positively correlated with the importance of vision for feeding (Gatz, 1979). It may also indicate vertical position in the water column, because species that inhabit deeper water tend to have smaller eyes

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(Wikramanayake, 1990); eye vertical position (EYPO), the ratio between the vertical distance from the middle of the eye to the lower limit of the head and the total head depth measured at eye level. EYPO was expected to indicate the foraging position of the species in the water column. Nektonic fishes were assumed to have lateral eyes, while benthic fishes were expected to have more dorsally located eyes (Gatz, 1979; Hugueny & Pouilly, 1999); teeth (TEETH) are considered to be a good index of diet (Gatz, 1979), but no simple measure exists and different coding systems based on number and shape have been proposed (Gatz, 1979; Motta et al., 1995). The number and shape of the premaxillar and mandibular teeth were combined into one code to describe the mode of intake of the diet [0, lack of teeth (associated with suction or snapping up of passive prey); 1, few teeth (<50) of conical, insiciform or multicuspidal shape (associated with biting or tearing); 2, numerous teeth (>50), filiforms (associated with scraping); 3, band of numerous teeth (associated with suction or snapping up of active prey)]; number of gill rakers on the first gill arch (GRNU) and relative maximum length of gill rakers on the first gill arch (GRLE), the ratio of the length of the longest gill raker of the first gill arch and LS. GRNU and GRLE were assumed to be positively linked with filtration activity and indirectly indicated planktivorous species (Motta et al., 1995); relative length of the digestive tract (GUTL), the ratio between the total length of the digestive tract and LS. GUTL was assumed to be higher in herbivores and detritivores, and lower in carnivores (Gatz, 1979; Hugueny & Pouilly, 1999).

STATISTICAL ANALYSIS Fish diets were compared and grouped by cluster analysis of the trophic distance matrix (UPGMA algorithm; Legendre & Legendre, 1998). Trophic distances between the 48 species were calculated from species scores along the three first axes of a correspondence analysis (explaining 76% of the total variability) of the species-food items table (Table I). Correspondence analysis is an ordination method, based on w2, recommended for analysis of occurrence data (Legendre & Legendre, 1998). The first few axes (generally the first three or four) model the majority of variation of the matrix (Winemiller, 1991) and extract the main components of ordination of the matrix. In order to show the relative level of diet specialization of the species, diet breadth of a 2 1 1 given species was estimated by Levin’s standardized index Bi ¼ [(ÆjPij) 1](n 1) where Pij is the proportion of prey j in the diet of predator i and n is the number of prey categories (Hurlbert, 1978). The index ranges from 0 (diet specialized on few prey items) to 1 (generalist diet). Relationships between fish diet and morphology were studied by canonical correspondence analysis, a non-linear ordination method specially adapted to explore unimodal relationships (CCA, Ter Braak, 1986). CCA is a correspondence analysis in which the axes are a linear combination of explanatory variables (morphological variables). It allows measurement of the amount of variation in the trophic data that can be explained by the linear combination of the morphological variables. The statistical significance of the diet´–morphology correlations extracted by the CCA was estimated by a permutation test (1000 simulations). Diet´–morphology relationships could be an artifact derived from the phylogenetic distance between the species (Winemiller, 1991; Douglas & Matthews, 1992; Hugueny & Pouilly, 1999). Phylogenetic distances were not available for all Amazonian freshwater fish groups. Following Hugueny & Pouilly (1999), the phylogenetic link between two species was approximated by means of an ordinal taxonomic distance. A value of 1 was set for congeneric species, 1´5 for consubfamilial species, 2 for confamilial species, 3 for species from the same order and 4 for species from different orders. Statistical comparisons of data matrices were performed in order to quantify the agreement between the diet, morphology and taxonomy of the fish. The non-parametric Mantel test was used to evaluate the null hypothesis which assumes that the distance among fishes in one matrix is not correlated with the corresponding distance in another matrix (Legendre & Legendre, 1998). By extension, a similar procedure could be performed to evaluate the partial correlation between two matrices while controlling for the effect of a third one

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TABLE I. Diet composition and breadth (Levin’s index, B) of 48 fish species in the central Mamore´River expressed by % occurrence of seven food categories. MUD, soft substratum; ALG, algae and periphyton; AIN, aquatic invertebrates; TIN, terrestrial invertebrates; ZOO, zooplankton; FISH, fishes; VEG, aquatic and terrestrial vegetation. Species are ordered according to the results of cluster analysis (see Fig. 2). See Table IV for species abbreviations

Number of Species code stomachs MUD ALG VEG INT INA ZOO FISH B

Zooplanktivores HYAMA 17 0´00 23´53 5´88 0´00 11´76 58´82 11´76 0´315 ENTBE 91 0´00 0´00 7´69 31´87 58´24 43´96 0´00 0´357 APYAN 95 0´00 30´53 2´11 9´47 97´89 89´47 0´00 0´305 AGEBR 39 0´00 0´00 0´00 0´00 23´08 97´44 0´00 0´075 Mud feeders POTAL 38 55´26 52´63 2´63 0´00 0´00 5´26 0´00 0´215 CUEAI 165 70´91 68´48 3´03 0´00 0´00 0´00 0´00 0´181 PSHLA 20 70´00 100´00 0´00 0´00 0´00 0´00 0´00 0´157 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 0´00 0´00 5´21 0´00 0´163 Algivores RHYMI 26 0´00 88´46 11´54 7´69 3´85 0´00 0´00 0´091 PSEAM 51 0´00 100´00 0´00 0´00 0´00 0´00 0´00 0´000 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 1´43 0´00 0´00 0´00 0´026 ENGSP 68 5´88 95´59 0´00 0´00 7´35 0´00 0´00 0´047 LOIMA 25 28´00 88´00 12´00 0´00 16´00 0´00 0´00 0´220 ANOME 144 25´69 90´28 0´00 0´00 6´94 4´17 0´00 0´137 Herbivores LEOFR 10 0´00 50´00 80´00 20´00 10´00 0´00 10´00 0´340 DORSP 58 18´97 79´31 82´76 5´17 34´48 12´07 1´72 0´450 SCHFA 43 2´33 30´23 74´42 0´00 4´65 0´00 0´00 0´154 Terrestrial invertivores and omnivores STTCR 68 0´00 10´29 32´35 64´71 32´35 0´00 1´47 0´353 POPCO 52 1´92 0´00 28´85 69´23 25´00 0´00 7´69 0´298 TRPAL 94 0´00 8´51 31´91 74´47 26´60 3´19 2´13 0´321 PAUST 18 0´00 5´56 11´11 55´56 33´33 0´00 27´78 0´412 PIUMA 140 0´71 25´71 23´57 37´14 53´57 5´00 37´14 0´644 TRPAN 277 0´36 19´86 20´94 53´79 55´96 9´75 1´44 0´463 MOEDI 241 0´41 8´30 5´81 46´06 60´17 26´56 0´41 0´389 Aquatic invertivores OPSSP 27 11´11 40´74 48´15 0´00 77´78 11´11 0´00 0´412 EIAVI 57 0´00 52´63 42´11 14´04 91´23 5´26 3´51 0´388 MYLDU 18 5´56 11´11 44´44 5´56 38´89 5´56 0´00 0´389 CTEPI 16 0´00 6´25 50´00 6´25 62´50 6´25 6´25 0´313 TRYPA 25 12´00 4´00 24´00 4´00 96´00 16´00 0´00 0´230 CENSP 32 0´00 0´00 9´38 28´13 87´50 0´00 0´00 0´138 BROSL 7 0´00 14´29 14´29 14´29 85´71 0´00 0´00 0´179 AUCNU 26 0´00 3´85 0´00 7´69 96´15 3´85 0´00 0´055

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PAECY 26 3´85 30´77 3´85 0´00 76´92 0´00 3´85 0´176 ADOSA 27 0´00 18´52 3´70 3´70 85´19 7´41 0´00 0´138 Carnivores PYGNA 87 0´00 2´30 32´18 12´64 5´75 1´15 62´07 0´275 TYMSP 55 1´82 1´82 9´09 18´18 16´36 5´45 67´27 0´291 SEREI 32 0´00 6´25 21´88 9´38 34´38 0´00 59´38 0´374 ROBMY 33 0´00 0´00 0´00 18´18 75´76 6´06 42´42 0´261 ROBAF 154 0´00 1´30 0´65 2´60 55´19 9´74 61´69 0´246 PELFL 120 0´00 0´00 2´50 6´67 52´50 3´33 66´67 0´231 Piscivores HOPMA 28 21´43 10´71 0´00 7´14 3´57 0´00 71´43 0´213 SERRH 76 0´00 1´32 5´26 7´89 10´53 0´00 94´74 0´094 PLGSQ 80 0´00 0´00 5´00 2´50 15´00 0´00 90´00 0´086 SERHO 90 0´00 2´22 11´11 2´22 6´67 1´11 90´00 0´092 CAOMA 28 0´00 3´57 14´29 3´57 7´14 0´00 85´71 0´119 ACEAL 51 1´96 1´96 1´96 3´92 0´00 0´00 96´08 0´035

(Smouse et al., 1986). In the present case, to factor out the taxonomic effect, a partial Mantel statistic was calculated between the matrices of residuals of morphology and taxonomy on the one hand and between diet and taxonomy on the other (Douglas & Matthews, 1992; Hugueny & Pouilly, 1999). Statistical significance was estimated by a permutation test (1000 simulations). Because of the multiple comparisons, the Bonferroni technique was used to assign the level of significance (a ¼ 0´05, divided by 3 ¼ 0´017) (Douglas & Matthews, 1992). The trophic distance matrix was the same as in cluster analysis. Similarly, the morphological distances were generated using species scores on the first three axes (explaining 73´8% of total variability) of a principal component analysis on the correlation matrix of morphological data (Winemiller, 1991; Douglas & Matthews, 1992).

RESULTS

DIET COMPOSITION AND CLASSIFICATION Diet varied among the species, and cluster analysis allowed eight groups of species showing similar diet profiles to be identified (Table I and Fig. 2); zooplanktivores: Hypophthalmus marginatus Valenciennes, Entomocorus benjamini Eigenmann, Aphyocharax anisitsi Eigenmann & Kennedy and Ageneiosus brevis Steindachner fed primarily (>40%) on zooplankton. Ageneiosus brevis appears as the only species that is highly specialized in the consumption of zooplankton, whereas the other species completed their diet with aquatic invertebrates (E. benjamini and A. anisitsi) or algae (H. marginatus and A. anisitsi). Diet breadth (Levin’s index, B) reflected the difference in specialization. It was equal to 0´075 for A. brevis and ranged between 0´305 and 0´357 for the other three species; mud feeders: Potamorhina altamazonica (Cope), Potamorhina latior (Spix & Agassiz), Curimatella alburna (Mu¨ller & Troschel), Pseudo- hemiodon laticeps (Regan) and Psectrogaster curviventris Eigenmann & Kennedy showed a similarly specialized diet based on algae and soft substratum associated with a low diet breadth (B between 0´16 and 0´24); algivores: Rhytiodus

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 1144 M. POUILLY ET AL.

HYAMA ENTBE Zooplanktivores APYAN AGEBR RHYMI PSEAM STUNI HYTJO Algivores ENGSP LOIMA ANOME POTAL CUEAI Mud feeders PSHLA PSECU POTLA LEOFR DORSP Herbivores SCHFA STTCR POPCO TRPAL PAUST Terrestrial invertivores PIUMA TRPAN MOEDI OPSSP EIAVI MYLDU CTEPI TRYPA Aquatic invertivores CENSP BROSL AUCNU PAECY ADOSA PYGNA TYMSP SEREI Carnivores ROBMY ROBAF PELFL HOPMA SERRH PLGSQ SERHO Piscivores CAOMA ACEAL

FIG. 2. Cluster analysis dendrogram (UPGMA algorithm) of trophic distances between 48 fish species in the central Mamore´River floodplain. (See Table IV for species abbreviations.) microlepis Kner, Psectrogaster amazonica Eigenmann & Eigenmann, Sturisoma nigrirostrum Fowler, Hypoptopoma joberti (Vaillant), Engraulidae, Loricari- ichthys maculatus (Bloch) and Anodus melanopogon Agassiz fed exclusively on algae associated with a low diet breadth (B between 0´00 and 0´2); herbivores: Leporinus friderici friderici (Bloch), Doras sp. and Schizodon fasciatus Spix & Agassiz fed on vegetation and algae. Leporinus friderici friderici and Doras sp. also consumed invertebrates (AIN and TIN) but only as a small proportion of their diet. These food items were probably complementary or resulted from feeding on aquatic macrophytes. Diet breadth reflected the difference in specialization between species of this group (B ¼ 0´15 for S. fasciatus and B > 0´34 for the two other species); terrestrial invertivores and omnivores: Stethaprion crenatum Eigenmann, Poptella compressa (Gu¨nther), Triportheus albus Cope, Triportheus angulatus (Spix & Agassiz), Parauchenipterus striatulus (Steindachner), Pimelodus gr. maculatus-blochii Valenciennes and Moenkhausia dichroura (Kner)

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 DIET AND MORPHOLOGY OF AMAZONIAN FISHES 1145 mainly fed on invertebrates and especially on terrestrial invertebrates. They also consumed other items such as fishes (P. striatulus and P. maculatus-blochii), zooplankton (M. dichroura) and vegetation (S. crenatum, P. compressa, T. albus, T. angulatus and P. maculatus-blochii). Although these species shared a high rate of consumption of TIN, they also presented noticeable variations in their complementary diet that resulted in this group being classified as omnivores. The diet breadth (B between 0´3 and 0´64) confirmed that no species presented a high level of specialization in the consumption of terrestrial invertebrates; aquatic invertivores: Opsodoras sp., Eigenmannia virescens (Valenciennes), Mylossoma duriventre (Cuvier), Ctenobrycon spilurus (Valenciennes), Trachy- doras paraguayensis (Eigenmann & Ward), Centromochlus sp., Brochis splendens (Castelnau), Auchenipterus nuchalis (Spix & Agassiz), Parecbasis cyclolepis Eigenmann and Adontosternarchus sachsi (Peters) fed predominantly on aquatic invertebrates (>60% of occurrence except in the case of M. duriventre). It was possible, however, to distinguish two trends. Trachydoras paraguayensis, Cen- tromochlus sp., B. splendens, A. nuchalis, P. cyclolepis and A. sachsi had a highly specialized diet (>75% of occurrence of AIN and secondary resources <31%). Conversely, Opsodoras sp., E. virescens, M. duriventre and C. spilurus consumed vegetation as a complementary resource (>40% of occurrence for the four species) as well as algae (>40% of occurrence for Opsodoras sp. and E. virescens). Diet breadth confirmed the distinction between a group of five more specialized species (B between 0´06 and 0´18) and four species with a more omnivorous diet (B between 0´32 and 0´41). Trachydoras paraguayensis was in an intermediate position between the two trends (B ¼ 0´23); carnivores: Pygo- centrus nattereri Kner, Tympanopleura sp., Serrasalmus eigenmanni (Norman), Roeboides myersii Gill, Roeboides affinis (Gu¨nther) and Pellona flavipinnis (Valenciennes) consumed fishes as their primary resource (42´–68% of occurrence) and invertebrates (S. eigenmanni, R. myersii, R. affinis and P. flavipinnis) or vegetation (P. nattereri and S. eigenmanni) as their main complementary resource. Diet breadth reflected the distinction between the two groups. Three more specialized species (R. myersii, R. affinis and P. flavipinnis) presented a lower diet breath (B between 0´23 and 0´26) with two co-dominant resources (FISH and AIN). The three other species (P. nattereri, S. eigenmanni and Tympanopleura sp.), which were less specialized, presented a higher diet breath (B between 0´28 and 0´37); piscivores: Serrasalmus rhombeus (L.), Serrasalmus hollandi Eigenmann, Plagioscion squamosissimus (Heckel), Calophysus macropterus (Lichtenstein) and Acestrorhynchus cf. altus Menezes comprised a specialized group (B between 0´1 and 0´12) with a high percentage of fish consumption (>85%). Hoplias malabaricus (Bloch) was also associated with this group but presented secondary consumption of soft substratum and algae, and thus a higher diet breadth (B ¼ 0´21).

DIET´–MORPHOLOGY RELATIONSHIPS The CCA revealed a significant relationship between diet and morphology (P < 0´01, tested with 1000 permutations). Interpretation was conducted on the three first axes, accounting for 90´5% of the total diet variation explained by the morphological variables (Table II). The fraction of variation of each food item

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TABLE II. Results of canonical correspondence analysis (CCA) between diet and morphology of 48 fish species of the Mamore´River

Axis 1 Axis 2 Axis 3

Variance of dietary data (%)23´914´67´6 Cumulated variance of dietary data 38´546´1 Variance of diet´–morphology relationship (%)46´828´715´0 Cumulated variance of diet´–morphology relationship 75´590´5 Canonical Eigenvalue CCA 0´46 0´28 0´15 Diet´–morphology relationship (r2)0´71 0´58 0´52

explained by morphology was 32´4% for terrestrial invertebrates, 38´4% for zooplankton, 44´8% for aquatic invertebrates, 45´8% for vegetation, 57´6% for algae, 58´4% for fishes and 68´2% for soft substratum. These results showed that terrestrial invertebrate and zooplankton consumption had the lowest associations with morphology. Conversely, soft substratum, algae and fishes appeared to be consumed by species that had more specific morphology. The axes derived from the CCA provided a geometric space that highlighted the distribution pattern of species according to the relation between their morphology and diet. Mud feeders and algivores were distributed in the right part of the first CCA graph (scatter plots of axes 1 and 2) and were associated with a large relative gut length (GUTL), which thus appeared as the most important morphological variable to distinguish microphagous species (mud feeders and algivores) from the others (Fig. 3). Carnivores and piscivores were mainly distributed in the upper left part of the first CCA graph (Fig. 3). These species were characterized by large size (LS), mouth height (MOHE) and head length (HEAD). Zooplanktivores were positioned on the upper left part of the second CCA graph (scatter plots of axes 2 and 3, Fig. 4). They were mainly characterized by a higher number of gill rakers of larger size. Herbivores that consumed macrophytic vegetation tended to be positioned on the lower left part of the second CCA graph, and were characterized by a larger eye diameter. Invertivores were mostly positioned on the lower left part of the CCA graphs but did not show clear differentiation that could be linked to a particular morphological feature. Teeth characteristics (TEETH) appeared to be of secondary importance and showed a negative correlation with consumption of mud and algae. This result indicated that the codification used enabled species without teeth (consuming mud or algae) to be approximately distinguished from the others. Eye position (EYPO) and mouth orientation (MORI) also appeared as secondary morphological features to explain fish diet, and presented no clear pattern associated with consumption of a particular diet item. In the species ordination diagram, species were positioned at the centroid of their morphological attributes (Figs 3 and 4). Their positions showed overall similarity with the diet classification resulting from the cluster diagram (Fig. 2). Some species, however, appeared positioned with a morphology that did not correspond to their observed diet. For example, P. nattereri was located at the extremity of the two first axes and thus appeared to be more morphologically

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 DIET AND MORPHOLOGY OF AMAZONIAN FISHES 1147

Axis 2 FISH (a)

MOHE L S

MUD HEAD EYPO

GUTL MORI TEETH ALG Axis 1

EYDI GRLE GRNU INT VEG

INA

ZOO

PYGNA Axis 2 PLGSQ (b)

HOPMA

PELFL ACEAL SERRH

POTAL SERHO SEREI POTLA PSECU CAOMA LOIMA PAUST ENGSP PIUMA ROBMY STUNI ANOME STTCR TRYPA Axis 1 PSEAM PSHLA SCHFA RHYMI CUEAI TRPAN OPSSP AGEBR CENSP TRPAL LEOFR HYAMA POPCO MYLDU ADOSA APYAN EIAVI DORSP TYMSP HYTJO PAECY BROSL ROBAF ENTBE MOEDI

AUCNU

CTEPI

FIG. 3. Graphical output of the axes 1 and 2 of canonical correspondence analysis (CCA) linking diet (seven food items) and morphology (10 attributes) of 48 fish species of the central Mamore´River. Ordination plots for morphological attributes and food items (a) and species (b) are presented separately to avoid cluttering. Species are presented by diet categories: , zooplanktivores; *, mud feeders; , algivores; ~, herbivores; &, terrestrial invertivores; &, aquatic invertivores; , carnivores; , piscivores. (See Tables I and IV for abbreviations.)

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 1148 M. POUILLY ET AL.

Axis 3 ZOO (a)

MOHE

GUTL GRNU GRLE TEETH

ALG FISH EYPO Axis 2 INT INA MORI MUD HEAD

VEG

L S

EYDI

HYAMA Axis 3 AGEBR (b)

HYTJO

ENGSP STUNI

ENTBE ANOME HOPMA TYMSP ROBMY PYGNA ROBAF PAUST APYAN STTCR AUCNU PIUMA CENSP SERHO MOEDI Axis 2 PSHLA CAOMA ACEAL PAECY ADOSA PELFL CUEAI SERRH TRPAN PSECU POPCO TRPAL PSEAM LOIMA DORSP POTAL CTEPI RHYMI SEREI EIAVI POTLA OPSSP PLGSQ BROSL MYLDU TRYPA

LEOFR

SCHFA

FIG. 4. Graphical output of the axes 2 and 3 of canonical correspondence analysis (CCA) linking diet (seven food items) and morphology (10 attributes) of 48 fish species of the central Mamore´River. Ordination plots for morphological attributes and food items (a) and species (b) are presented separately to avoid cluttering. Species are presented by diet categories (see Fig. 3). (See Tables I and IV for abbreviations.)

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 DIET AND MORPHOLOGY OF AMAZONIAN FISHES 1149

TABLE III. Correlation coefficient and probabilities for Mantel test and partial Mantel test on diet, morphology and taxonomy distances matrix between 48 fish species of the Mamore´River

Covariable r (Mantel) P*

Diet´–morphology 0´263 0´006 Diet´–taxonomy 0´102 0´025 Morphology´–taxonomy 0´406 0´001 Diet´–morphology Taxonomy 0´244 0´011

*Bonferroni-adjusted probability ¼ 0´017 (0´05 divided by 3). specialized for piscivory than other species that eat a higher proportion of fishes. Sturisoma nigrirostrum was located at the extremity of the second axis, and could thus be considered as morphologically specialized for detritivory despite the fact its diet is based on algae. Two carnivorous species Tympano- pleura sp. and R. affinis were located in a pool of invertivores and zooplanktivores distributed in the lower left part, and thus appeared to not present a high correlation with any of the morphological variables. The result of Mantel and partial Mantel tests showed the correlation coefficient between the trophic, morphologic and taxonomic distances matrix to be significant, except for the diet and taxonomy comparison (P ¼ 0´025, evaluation by a test of 1000 permutations, Table III). Trophic distances between species were positively correlated with morphological distances. Morphological distances were also positively correlated with taxonomic distances, suggesting that the observed diet´–morphology relationships may be the result of a taxonomic link between species. The partial Mantel test using taxonomic distance as a covariate showed that the diet´–morphology relationship was still significant (P ¼ 0´011) when controlling for the effect of taxonomy.

DISCUSSION

DIET COMPOSITION AND CLASSIFICATION Forty-eight fish species of the Mamore´River floodplain were classified into eight trophic categories: mud feeders, algivores, herbivores, terrestrial invertivores and omnivores, aquatic invertivores, zooplanktivores, carnivores and piscivores. The trophic categories defined in this study correspond to a large range of categories presented in other Amazonian fish trophic studies (Marlier, 1968; Kno¨ppel, 1970; Soares, 1979; Goulding, 1980; Soares et al., 1986). The high level of taxonomic diversity of the Mamore´River floodplain (c. 140 species, 26 families) corresponds to a high level of trophic diversity even when only the most abundant species are taken into consideration. ‘Forest feeders’ is the only main category absent from the present data that is generally represented in the Amazon by herbivorous species such as Colossoma macropomum

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 1150 M. POUILLY ET AL.

(Cuvier). Although this species is present in the central Mamore´region (Lauzanne et al., 1991), it was not abundant in the present sampling. From the point of view of species-specific diet, it is difficult to compare studies, not only because of differences in methodology but also because the patterns of resource availability are not presented. Species that present a broad distribution and a rather specialized diet, however, are generally consistently classified. Species belonging to the Curimatidae are widely recognized as micro- phytophages and classified as detritivores (Soares et al., 1986) or mud feeders (Goulding, 1980) or separated, as in the present results, into mud feeders and phytophages (Marlier, 1968). Species of the genus Hypophthalmus have been shown to be zooplanktivores (Marlier, 1968; Carvalho, 1980). Species of the genus Leporinus and S. fasciatus are described as herbivorous species (Soares et al., 1986) or omnivores (Goulding, 1980). Rhytiodus microlepis is classified as algivorous by Soares et al. (1986). A majority of piscivorous species have also been described as specialized and as having an unvarying diet dominated by fish prey: A. cf. altus (Menezes, 1969), H. malabaricus (Soares et al., 1986) and P. squamosissimus (Goulding, 1980). Species that are highly omnivorous are also classified consistently, such as species of the genera Triportheus and Pimelodus (Goulding, 1980; Soares et al., 1986). A majority of the fishes analysed in the Mamore´River floodplain were shown to have a diet (at the general level of classification used here) similar to other South American systems including white, clear and black waters. Food resource availability is likely to be different in each kind of system, so it may be assumed that fish diet not only depends on the availability of different food items but also on the capacity of fishes to capture and make use of this food. Apparently, specialized species do not modify their diet from one system to another, but the global trophic structure of the assemblage seems to change with the system. For example, the fish assemblage of the Machado River, a clear-water tributary of the Madeira River, is highly supported by forest resources and shows a broad partitioning between microphages, carnivorous and herbivorous species (Goulding, 1980). In the present results, as in the white waters of the central Amazon (Soares et al., 1986), the herbivores tended to be under-represented, although microphages (algivores and mud feeders) and carnivores (invertivores and piscivores) included the majority of the species.

DIET´–MORPHOLOGY RELATIONSHIPS The 48 fish species analysed had taxonomical links ranging from intra-genus to inter-order. Unfortunately, no reliable phylogenies exist for South American fishes and thus the analysis had to be based on the less reliable data of taxonomic relatedness. Weathers & Siegel (1995), however, indicated that ‘if a data set is reasonably diverse phylogenetically (i.e. has a high ratio of number of clades to number of species) and exhibits a reasonably strong correlation, phylogenetic analysis is unlikely to alter conclusions’. Thus, as the analysis showed high taxonomic diversity (five orders and 18 families for 48 species), it is likely that integration of taxonomic relatedness rather than phylogenies would give reliable conclusions with respect to the effect of evolutionary relationships.

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 DIET AND MORPHOLOGY OF AMAZONIAN FISHES 1151

Three main associations between morphology and fish diet emerged from the results. Among the 10 morphological variables analysed, relative gut length appeared to be the main feature broadly associated with fish diet. Relative gut length was positively and strongly associated with herbivory and iliophagy and negatively with carnivory, as has been reported in various fish assemblages (Paugy, 1994; Winemiller & Adite, 1997; Piet, 1998; Hugueny & Pouilly, 1999) and among species belonging to the same family (Fryer & Ilies, 1972). Besides gut length, the second main trend corresponded to a positive link between carnivory and prey size and the morphological variables LS, HEAD and MOHE. This association has also been reported in various fish assemblages (Gatz, 1979; Wainwright & Richard, 1995; Piet, 1998; Hugueny & Pouilly, 1999). Finally, the third main association was the positive link between gill raker length and number and zooplankton consumption (Motta et al., 1995). Other patterns presented in the literature were not at all or only weakly validated in the results. In the CCA results, mouth orientation, eye diameter and eye position appeared as a weak descriptor of fish diet. Benthic fishes generally tend to possess dorsally positioned eyes and a ventrally orientated mouth, while pelagic fishes have laterally positioned eyes and an upward orientated mouth (Gatz, 1979; Watson & Balon, 1984; Winemiller et al., 1995; Hugueny & Pouilly, 1999). The Curimatidae, which includes a majority of benthic feeding species characterized by a terminal mouth and lateral eyes, is an exception to this generalization. A majority of Curimatidae species, however, have evolved to a benthic detritivorous diet (Ge´ry, 1977) and display other adaptations, like a lack of teeth and a long intestine adapted to detritivory, that indirectly indicate benthic feeding. Hugueny & Pouilly (1999) noted a similar case of Mormyridae benthic feeding species that did not have dorsally positioned eyes. Gatz (1979) linked eye size to the importance of vision in feeding and it is likely that sight is important in foraging and in the capture of animal food and especially in piscivory. Among the species analysed, eye size appears to be greatly influenced by taxonomy, as 80% of the species with an EYDI above the mean were Characiformes (Table IV) which consequently limits the ecological interpretation of this character in the data. The results call attention to the fact that the selection of morphological variables is one of the major difficulties in ecomorphological analysis. In particular, other morphological variables than those examined could play important roles in food selection and ingestion and consequently a failed correlation does not necessarily indicate that there is no morphological correlation with diet. Morphological variables, categories of diet items and statistical methods used are generally different and specific to individual studies. Even though the situations analysed were different, the three main associations observed in the present study remain generally valid, and thus point to a strong trend towards the matching of an organism’s morphology to its theoretical or potential diet. Increase in gut length, in the size and number of gill rakers, and in the size of the mouth and head appear as constant adaptations resulting from a specialized herbivore, plantkivore and piscivore diet. Consequently, it is recommended that these morphological features should not be avoided in diet ecomorphological studies.

# 2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 62, 1137´–1158 1152

TABLE IV. Classification, standard length (range in parentheses) and mean values (S.D. in parentheses where appropriate) of nine morphological parameters for 48 fish species of the Mamore´River. HEAD, relative head length; MOHE, relative mouth height; MORI, mouth orientation; EYPO, eye vertical position; TEETH, type of dentition; EYDI, relative eye diameter; GRNU, number of gill rakers on

# the first gill arch; GRLE, relative maximum length of gill rakers on the first gill arch; GUTL, relative length of the digestive tract 03TeFseisSceyo h rts Isles, British the of Society Fisheries The 2003 HEAD MOHE EYPO EYDI GRLE 2 2 2 LS 10 10 10 10 10 GUTL Order, Family Species Code n (range) (S.D.) (S.D.) MORI (S.D.) TEETH (S.D.) GRNU (S.D.) (S.D.)

Characiformes Anostomidae Leporinus friderici LEOFR 30 130´3 2´76 5´53 25´97 17´71 25 1´21 1´37 friderici (Bloch) (54´8´–195) (0´18) (1) (1´16) (0´91) (0´34) (0´24) Rhytiodus microlepis RHYMI 26 126´8 2´72 6´64 25´79 17´1 32 1´89 1´85 POUILLY M. Kner (77´8´–197´7) (0´17) (1´3) (0´92) (1´3) (1´2) (0´17) Schizodon fasciatus SCHFA 26 172´6 2´46 5´55 25´18 16´98 17 1´24 1´65 Spix & Agassiz (80´5´–277´7) (0´36) (1´23) (0´67) (1´54) (0´31) (0´43) Characidae Aphyocharax anisitsi APYAN 30 54´7 2´83 10´53 25´64 29´99 20 3´03 1´21 Eigenmann & Kennedy (50´–58´6) (0´15) (0´56) (0´33) (0´29) (0´35) (0´1) Triportheus albus Cope TRPAL 30 105´2 2´36 8´86 25´9 18´06 44 1´18 1´09 AL. ET ora fFs Biology Fish of Journal (91´2´–159´2) (0´1) (1´33) (0´63) (0´45) (0´25) (0´13) Triportheus angulatus TRPAN 30 100 2´66 8´84 1´56´23 18´61 43 2´53 1´31 (Spix & Agassiz) (54´–148) (0´21) (0´8) (0´29) (1´04) (0´34) (0´19) Acestrorhynchus cf. ACEAL 30 157´5 2´94 13´75 26´45 16´24 27 0´88 1´03 altus Menezes (92´–241´5) (0´26) (1´94) (0´54) (0´63) (0´13) (0´17) Roeboides affinis ROBAF 30 63´1 2´64 11´19 1´55´32 1916 3´68 0´69 (Gu¨nther) (51´1´–116´4) (0´27) (1´74) (0´53) (0´63) (0´63) (0´17) Roeboides myersii Gill ROBMY 30 88´8 2´88 13´43 26´4 19´74 26 6´02 0´93 2003, (63´5´–134´2) (0´14) (1´71) (0´48) (0´66) (0´56) (0´14) Parecbasis cyclolepis PAECY 30 54´7 2´71 10´1 26´34 19´96 26 3´29 0´8 62, Eigenmann (51´7´–65´4) (0´22) (1´15) (0´77) (0´88) (0´65) (0´14) 1137 Poptella compressa POPCO 30 64´2 2´77 11´51 25´35 110´96 20 2´75 0´92

´ ´´ ´ ´ ´ ´ ´ ´ ´ –1158 (Gu¨nther) (365–832) (165) (249) (064) (215) (061) (02) # 03TeFseisSceyo h rts Isles, British the of Society Fisheries The 2003

Stethaprion crenatum STTCR 30 45´7 3´06 15´6 1´55´49 112´44 23 3´04 1´08 Eigenmann (41´3´–49´8) (0´15) (1´21) (0´54) (0´51) (0´31) (0´27) Ctenobrycon spilurus CTEPI 30 42´9 2´45 8´61 24´76 110´59 19 2´04 0´96 ITADMRHLG FAAOINFISHES AMAZONIAN OF MORPHOLOGY AND DIET (Valenciennes) (38´6´–49´5) (0´44) (1´08) (0´43) (0´44) (0´45) (0´16) Moenkhausia dichroura MOEDI 30 55´8 2´44 10´84 25´36 19´78 25 3´39 0´82 (Kner) (47´–63´9) (0´29) (0´77) (0´43) (0´53) (0´36) (0´12) Curimatidae Curimatella alburna CUEAI 30 96´2 2´73 7´75 25´12 010´14 26 0´73 10´06 (Mu¨ller & Troschel) (87´6´–118´5) (0´13) (0´56) (1´04) (0´97) (0´15) (2´09) Potamorhina POTAL 30 119´9 3´49 10´42 25´4 08´75 0— 9´03 altamazonica (Cope) (81´76´–174) (0´5) (1´75) (0´72) (0´91) (2´26) Potamorhina latior POTLA 30 126´7 3´38 9´46 1´55´78 08´07 0— 8´04 (Spix & Agassiz) (71´8´–154´6) (0´27) (1´92) (0´51) (0´78) (2´21) Psectrogaster amazonica PSEAM 30 71 3´49 12´1 25´74 010´97 96 0´82 1´58 ora fFs Biology Fish of Journal Eigenmann & Eigenmann (60´2´–102´5) (0´31) (1´07) (0´41) (0´51) (0´17) (0´17) Psectrogaster curviventris PSECU 30 109´3 3´23 10´07 25´76 09´26 0—10´27 Eigenmann & Kennedy (63´–158´4) (0´19) (1´32) (0´66) (1´07) (2´8) Erythrinidae Hoplias malabaricus HOPMA 30 150´9 3´24 16´82 26´34 1624 2´19 1´07 (Bloch) (63´4´–223´3) (0´73) (2´98) (0´66) (0´84) (0´57) (0´2) Hemiodontidae Anodus melanopogon ANOME 30 135´6 3´38 9´77 25´57 06´65 105 6´96 1´77 Agassiz (78´7´–175´5) (0´26) (1´93) (0´49) (0´77) (0´61) (0´3) Serrasalmidae Mylossoma duriventre MYLDU 30 110 2´91 7´88 25´1 19´23 21 2´9 1´96 2003, (Cuvier) (64´4´–150´2) (0´23) (0´97) (0´42) (0´84) (0´38) (0´43) Serrasalmus eigenmanni SEREI 30 118´9 3´24 12´94 25´95 19´04 18 1´28 2´00 62, (Norman) (66´9´–154´8) (0´2) (2´01) (0´83) (0´63) (0´21) (0´88) 1137 Pygocentrus nattereri PYGNA 30 133´7 3´84 20´03 16´37 18´3 18 2´12 1´64 ´´ ´ ´ ´ ´ ´ ´ ´ ´ Kner (105 3–202 5) (0 18) (1 3) (1 9) (0 9) (0 59) (0 31)

–1158 Serrasalmus hollandi SERHO 23 84´5 3´85 14´46 15´66 19´68 32 1´27 1´23 Eigenmann (39´5´–146´2) (1´32) (1´84) (2´21) (2´54) (0´4) (0´18) Serrasalmus rhombeus (L.) SERRH 30 98´5 3´73 14´94 16´27 19´3 11 1´33 1´22 (37´9´–142´5) (0´2) (2´62) (0´39) (1´05) (0´39) (0´21) 1153 1154

TABLE IV. Continued overleaf #

03TeFseisSceyo h rts Isles, British the of Society Fisheries The 2003 HEAD MOHE EYPO EYDI GRLE 2 2 2 LS 10 10 10 10 10 GUTL Order, Family Species Code n (range) (S.D.) (S.D.) MORI (S.D.) TEETH (S.D.) GRNU (S.D.) (S.D.)

Clupeiformes Clupeidae Pellona flavipinnis PELFL 30 153´2 2´78 15´21 17´61 18´53 27 3´96 0´81 (Valenciennes) (138´3´–183´2) (0´12) (1´3) (0´56) (0´61) (0´39) (0´13) Engraulidae Engraulidae ENGSP 30 141´4 3´03 13´13 24´74 05´19 87 6´29 2´61

(124´–177) (0´12) (1´51) (0´99) (0´41) (0´55) (0´43) POUILLY M. Gymnotiformes Apteronotidae Adontosternarchus ADOSA 30 152´4 1´3 3´76 27´58 01´26 0— 0´5 sachsi (Peters) (105´3´–189´3) (0´14) (0´41) (0´47) (0´17) (0´12) Sternopygidae Eigenmannia virescens EIAVI 30 221´5 1 2´37 26´2 31´79 14 0´71 0´36 (Valenciennes) (123´4´–608´7) (0´21) (0´67) (0´58) (0´45) (0´26) (0´07)

Perciformes AL. ET ora fFs Biology Fish of Journal Sciaenidae Plagioscion PLGSQ 30 249´8 3´38 13´03 26´87 25´94 15 4´47 0´93 squamosissimus (Heckel) (185´2´–347) (0´16) (1´9) (0´45) (0´46) (0´4) (0´16) Siluriformes Ageneiosidae Ageneiosus brevis AGEBR 30 59´8 2´85 11´71 33´75 34´04 26 2´89 0´96 Steindachner (56´4´–65´7) (0´15) (0´65) (0´75) (0´42) (0´22) (0´13) Tympanopleura sp. TYMSP 30 84´9 2´91 9´05 43´88 35´66 19 1´87 1´06 (68´5´–108´1) (0´4) (0´82) (0´73) (0´84) (0´25) (0´14) Auchenipteridae Auchenipterus nuchalis AUCNU 30 128´4 2´09 7´38 23´14 14´91 33 2´27 1´13 2003, (Spix & Agassiz) (87´5´–148´4) (0´22) (0´95) (0´51) (0´71) (0´45) (0´16) Centromochlus sp. CENSP 30 66´1 2´8 9´16 25´32 37´6 80´23 1´33 62, (54´7´–76´5) (0´23) (1´07) (0´5) (1´02) (0´12) (0´26) 1137 ´ –1158 # 03TeFseisSceyo h rts Isles, British the of Society Fisheries The 2003

Entomocorus benjamini ENTBE 27 61 2´82 9´71 24´04 37´48 18 2´22 0´99 Eigenmann (54´1´–70´2) (0´46) (1´27) (0´68) (0´64) (0´29) (0´12) FISHES AMAZONIAN OF MORPHOLOGY AND DIET Parauchenipterus PAUST 30 140´5 2´9 9´56 25´21 33´97 80´48 1´18 striatulus (Steindachner) (103´–165´6) (0´25) (1´11) (0´53) (0´38) (0´12) (0´21) Callichthyidae Brochis splendens BROSL 25 46´7 3´48 6´23 45´96 18´68 15 1´11 1´48 (Castelnau) (37´3´–65´8) (0´43) (0´91) (0´51) (1´01) (0´19) (0´21) Doradidae Doras sp. DORSP 30 56´3 3´11 8´18 36´11 07´98 14 1´44 2´09 (46´4´–110´1) (0´15) (1´16) (0´55) (0´61) (0´44) (0´45) Opsodoras sp. OPSSP 29 64´2 3´23 6´69 47´59 06´79 11 1´55 1´12 (43´3´–84´6) (0´3) (0´69) (0´5) (0´6) (0´23) (0´17) Trachydoras paraguayensis TRYPA 27 96´6 2´93 6´79 47´69 08´1 14 0´64 1´74

ora fFs Biology Fish of Journal (Eigenmann & Ward) (84´3´–116´1) (0´3) (0´89) (0´52) (0´96) (0´16) (0´24) Hypophthalmidae Hypophthalmus HYAMA 30 195´6 3´04 10´54 22´21 02´87 246 6´4 1´46 marginatus Valenciennes (107´–272) (0´28) (2´96) (0´38) (0´51) (0´99) (0´36) Loricariidae Hypoptopoma joberti HYTJO 30 70´5 3´14 8´32 43´09 25´63 84 1´73 8´33 (Vaillant) (61´4´–79´6) (0´18) (1´68) (0´53) (0´6) (0´21) (1´56) Loricariichthys maculatus LOIMA 30 168´4 2´31 5´34 48´01 13´07 21 0´47 1´79 (Bloch) (84´3´–230´9) (1´49) (0´56) (0´48) (0´58) (0´11) (0´4) Pseudohemiodon laticeps PSHLA 30 137´5 1´74 4´7 48´18 12´94 12 0´48 1´45 2003, (Regan) (84´3´–199´8) (0´15) (0´72) (0´64) (0´34) (0´13) (0´23) Sturisoma nigrirostrum STUNI 30 121´7 2´31 5´16 47´46 22´61 68 0´57 7´09 62, Fowler (88´7´–188´7) (0´16) (0´38) (0´58) (0´23) (0´13) (0´62)

1137 Pimelodidae Calophysus macropterus CAOMA 26 169´5 2´43 6´54 37´92 12´86 25 2´03 1´04 ´´ ´ ´ ´ ´ ´ ´ ´

´ (Lichtenstein) (1186–2417) (011) (135) (047) (052) (021) (02) –1158 Pimelodus gr. maculatus- PIUMA 30 73 4´14 8´38 36´54 37´35 24 3´1 1´05 blochii Valenciennes (51´2´–112´7) (5´32) (1´22) (0´68) (0´71) (0´81) (0´22) 1155 1156 M. POUILLY ET AL.

Several authors have noted that piscivorous and detritivorous species have the most highly specialized morphology (Piet, 1998; Hugueny & Pouilly, 1999; Sibbing & Nagelkerke, 2001; Xie et al., 2001). The other diets (invertivore and omnivore) seem to require a lower level of morphological specialization at least for the features analysed. At the level of assemblage, the trophic composition may thus play a role in determining the degree of correlation between diet and morphology. Studies that concluded the existence of a strong relationship generally include specialized piscivores, detritivores and planktivores (Piet, 1998; Hugueny & Pouilly, 1999; Sibbing & Nagelkerke, 2001; Xie et al., 2001). In contrast, studies that include a majority of invertivore or omnivore and generalist species concluded the existence of a relatively weak relationship between diet and morphology (Douglas & Matthews, 1992; Motta et al., 1995; Winemiller & Adite, 1997). The results suggest significant relationships between diet and morphology in the most abundant fish species of the Mamore´River, even when the taxonomical´– morphological relationships between species were eliminated. This conclusion supports the ecomorphological hypothesis and its two main arguments, first that species morphology is associated with their diet (Wainwright & Richard, 1995) and second that morphological similarity is conserved even in the comparison of taxonomically unrelated species (Winemiller, 1991). Ecomorphological diversification in an assemblage is a function of the richness of species (Winemiller, 1991). Accordingly, the results obtained in the Mamore´River floodplain could be related to the relatively high trophic and taxonomic diversity and especially to the presence of species with specialized diet requiring particular morphological features.

This work was part of the BIOBAB project (aquatic biodiversity in the Bolivian Amazon basin) developed by IRD, the Instituto de Ecologıá from La Paz University (Universidad Mayor de San Andre´s) and the Centro de Investigacioń de los Recursos Acua´ticos’ of Trinidad University (Universidad Tećnica del Beni). We thank these institutions for their support. J.G. Bretenoux was a student at the French Polytechnic School. T. Yunoki, A. Parada from Trinidad University and J.L. Menou from IRD helped with logistics, fieldwork and identification of specimens. We would also like to thank B. Hugueny (IRD) for reviewing the manuscript and L. Torres (Trinidad University) for his helpful participation in the BIOBAB project.

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