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Flood pulse influence on the feeding ecology of two Amazonian auchenipterid catfishes

ABSTRACT

We assessed the flood pulse effect on the diet composition, trophic niche breadth, and the amount of food intake of two Amazonian auchenipterids with different feeding strategies. Sampling was carried out quarterly (from April/2012 to January/2014) on the middle Xingu River, using gillnets. We measured specimens for standard length and total weight. The specimens’ stomachs were removed, weighed, and had their contents identified. We analyzed 360 stomachs of Auchenipterus nuchalis and 584 of Tocantinsia piresi. The diet of A. nuchalis was mainly composed of aquatic insects and crustaceans, while T. piresi fed on fruits and seeds. The diet composition of both species varied seasonally, but only T. piresi changed its trophic niche breadth in response to hydrological changes, becoming more specialist during the higher water periods (filling and flood). Both species also showed differences in their amount of food intake between hydrological periods, with A. nuchalis feeding more intensely in lower water periods (ebb and dry), while T. piresi in the higher water periods. We evidenced different responses to the hydrological periods for the related species. We emphasize that studies considering the relationship between flood pulse and feeding ecology of the organisms are essential to understanding river floodplain systems’ dynamics.

Keywords:
Amazon basin; Diet; Niche breadth; Siluriformes; Xingu River

RESUMO

Avaliamos o efeito do pulso de inundação na composição da dieta, amplitude de nicho trófico e quantidade de alimento ingerido de dois auchenipterídeos amazônicos com diferentes estratégias alimentares. Os espécimes foram amostrados trimestralmente entre abril/2012 e janeiro/2014 no médio rio Xingu, utilizando malhadeiras. Estes foram mensurados quanto ao comprimento padrão e peso total. Os estômagos dos espécimes foram removidos, pesados e seu conteúdo identificado. Analisamos 360 estômagos de Auchenipterus nuchalis e 584 de Tocantinsia piresi. A dieta de A. nuchalis foi predominantemente composta por insetos aquáticos e crustáceos, enquanto para T. piresi frutos e sementes predominaram. A composição da dieta de ambas as espécies variou sazonalmente, mas apenas para T. piresi a amplitude de nicho trófico variou entre períodos hidrológicos, sendo mais especialista nos períodos de águas altas (enchente e cheia). Ambas as espécies diferiram na quantidade de alimento ingerido entre os períodos hidrológicos, sendo maior para A. nuchalis nos períodos de águas baixas (vazante e seca) e para T. piresi nos períodos de águas altas. Evidenciamos diferentes respostas à variação hidrológica pelas espécies. Enfatizamos que estudos considerando a relação entre a dinâmica do pulso de inundação e a ecologia alimentar dos organismos é fundamental para um melhor entendimento da dinâmica das planícies de inundação.

Palavras-chave:
Amplitude de nicho; Bacia Amazônica; Dieta; Rio Xingu; Siluriformes

INTRODUCTION

Flood pulse is the main ecological driver of freshwater floodplain rivers (Junk et al., 1989Junk W, Bayley P, Sparks R. The flood pulse concept in river-floodplain systems. Can J Fish Aquat. 1989; 106(1):110-27.; Thomaz et al., 2007Thomaz SM, Bini LM, Bozelli RL. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia . 2007; 579(1):1-13. https://doi.org/10.1007/s10750-006-0285-y
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). Many terrestrial and aquatic organisms depend on this hydrological dynamic for food supply, breeding, and shelter (Ocock et al., 2014Ocock JF, Kingsford RT, Penman TD, Rowley JJL. Frogs during the flood: Differential behaviours of two amphibian species in a dryland floodplain wetland. Austral Ecol. 2014; 39(8):929-40. https://doi.org/10.1111/aec.12158
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; Robinson, Pizo, 2017Robinson V, Pizo MA. A floodplain with artificially reversed flood pulse is important for migratory and rare bird species. Rev Bras Ornitol. 2017; 25(3):155-68. https://doi.org/10.1007/BF03544394
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; Bayley et al., 2018Bayley PB, Castello L, Batista VS, Fabré NN. Response of Prochilodus nigricans to flood pulse variation in the central Amazon. R Soc Open Sci. 2018; 5(6):172232. https://doi.org/10.1098/rsos.172232
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). These organisms have developed specific behavioral strategies to use periodically available habitats and resources during high and low water periods (Alho, Sabino, 2012Alho CJR, Sabino J. Seasonal Pantanal Flood Pulse: Implications for biodiversity conservation - a review. Oecologia Australis. 2012; 16(4):958-78. https://doi.org/10.4257/oeco.2012.1604.17
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; Naus, Reid Adams, 2018Naus CJ, Reid Adams S. Fish nursery habitat function of the main channel, floodplain tributaries and oxbow lakes of a medium-sized river. Ecol Freshw Fish. 2018; 27(1):4-18. https://doi.org/10.1111/eff.12319
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). For fish fauna, the flood pulse plays a significant role in reproduction and feeding strategies (Bailly et al., 2008Bailly D, Agostinho AA, Suzuki HI. Influence of the flood regime on the reproduction of fish species with different reproductive strategies in the Cuiabá River, Upper Pantanal, Brazil. River Res Appl. 2008; 24(9):1218-29. https://doi.org/10.1002/rra.1147
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; Luz-Agostinho et al., 2008Luz-Agostinho KDG, Agostinho AA, Gomes LC, Júlio HF. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná River floodplain. Hydrobiologia . 2008; 607(1):187. https://doi.org/10.1007/s10750-008-9390-4
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; Barbosa et al., 2018Barbosa TAP, Rosa DCO, Soares BE, Costa CHA, Esposito MC, Montag LFA. Effect of flood pulses on the trophic ecology of four piscivorous fishes from the eastern Amazon. J Fish Biol. 2018; 93(1):30-39. https://doi.org/10.1111/jfb.13669
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), as well as in their assemblage structure (Barbosa et al., 2015Barbosa T, Benone N, Begot T, Gonçalves A, Sousa L, Giarrizzo T et al. Effect of waterfalls and the flood pulse on the structure of fish assemblages of the middle Xingu River in the eastern Amazon basin. Braz J Biol. 2015; 75(3 suppl 1):78-94. https://doi.org/10.1590/1519-6984.00214BM
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; Fitzgerald et al., 2018Fitzgerald DB, Sabaj Perez MH, Sousa LM, Gonçalves AP, Rapp Py-Daniel L, Lujan NK et al. Diversity and community structure of rapids-dwelling fishes of the Xingu River: Implications for conservation amid large-scale hydroelectric development. Biol Conserv. 2018; 222:104-12. https://doi.org/10.1016/j.biocon.2018.04.002
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). In the tropics, the high fish diversity is accompanied by a high diversity of ecological strategies, presenting different responses to these periodic environmental changes (Lowe-McConnell, 1987Lowe-McConnell RH. 1987. Ecological studies in tropical fish communities. Cambridge Tropical Biology Series. Cambridge University Press: Cambridge. 382 p).

New foraging areas become available during flood periods, and so do new food resources, such as fruits, seeds, and terrestrial insects that drop into the water from the forest canopy while others become more difficult to find (Lowe-McConnell, 1987Lowe-McConnell RH. 1987. Ecological studies in tropical fish communities. Cambridge Tropical Biology Series. Cambridge University Press: Cambridge. 382 p; Correa, Winemiller, 2014Correa SB, Winemiller KO. Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest. Ecology. 2014; 95(1): 210-24. https://doi.org/10.1890/13-0393.1
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; Castello, Macedo, 2016Castello L, Macedo MN. Large-scale degradation of Amazonian freshwater ecosystems. Global Change Biol. 2016; 22(3):990-1007. https://doi.org/10.1111/gcb.13173
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). The more extensive availability of energetically rich food resources in the high-water periods is advantageous for many fish species that explore the floodplains for feeding (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. Berkeley, CA: University of California Press; 1980. 280p.; Correa et al., 2007Correa SB, Winemiller KO, López-Fernández H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience. 2007; 57(9):748-56. https://doi.org/10.1641/B570907
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; Mortillaro et al., 2015Mortillaro JM, Pouilly M, Wach M, Freitas CEC, Abril G, Meziane T. Trophic opportunism of central Amazon floodplain fish. Freshw Biol. 2015; 60(8):1659-70. https://doi.org/10.1111/fwb.12598
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; Costa-Pereira, 2017Costa-Pereira R. An overview on the effects of fish consumption on seed germination: Pitfalls, challenges, and directions. Aquat Bot. 2017; 140:34-37. https://doi.org/10.1016/j.aquabot.2017.01.005
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). Based on the Optimal Foraging Theory (MacArthur, Pianka, 1966MacArthur R, Pianka E. On optimal use of a patchy environment. Am Nat. 1966; 100(916):603-09. https://doi.org/10.1086/282454
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), the organism tends to have a more specialized diet searching for food that optimizes their energy gain during this period. For instance, invertivorous and frugivorous species have their diet based mainly on allochthonous resources (Freitas et al., 2011Freitas TMS, Almeida VHC, Valente RM, Montag LFA. Feeding ecology of Auchenipterichthys longimanus (Siluriformes: Auchenipteridae) in a riparian flooded forest of Eastern Amazonia, Brazil. Neotrop Ichthyol . 2011; 9(3):629-36. https://doi.org/10.1590/S1679-62252011005000032
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). Contrary, in the low water periods, the diet of these trophic groups becomes predominantly dependent on autochthonous food items (Lopes et al., 2017Lopes DA, Vieira KRI, Silva Mota R, Souza MRF, Santos Costa FE, Paiva F. Opportunistic diet of Triportheus nematurus (Characiformes: Triportheidae) in Southern Pantanal ponds: influences of temporal availability and abundance of resources. Acta Sci Biol Sci. 2017; 39(4):441-47. https://doi.org/10.4025/actascibiolsci.v39i4.36391
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). Thus, the flood pulse has a tangible role in fish’s ecology (Junk et al., 1989Junk W, Bayley P, Sparks R. The flood pulse concept in river-floodplain systems. Can J Fish Aquat. 1989; 106(1):110-27.), especially in their feeding strategies adjustment for a more efficient use of available resources (MacArthur, Pianka, 1966MacArthur R, Pianka E. On optimal use of a patchy environment. Am Nat. 1966; 100(916):603-09. https://doi.org/10.1086/282454
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).

Knowledge about the feeding dynamics of the fish species may provide an essential baseline for understanding their role in aquatic ecosystems (Winemiller, 1989Winemiller KO. Patterns of variation in life history among South American fishes in seasonal environments. Oecologia. 1989; 81(2):225-41. https://doi.org/10.1007/BF00379810
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), and such ecological data are desirable for environmental conservation. While the influence of hydrological cycles on the feeding strategies of fish is well-documented (Mérona et al., 2001Mérona B de, Santos GM dos, Almeida RG de. Short term effects of Tucuruí Dam (Amazonia, Brazil) on the trophic organization of fish communities. Environ Biol Fishes. 2001; 60(4):375-92. https://doi.org/10.1023/A:1011033025706
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; Prudente et al., 2016Prudente BS, Carneiro-Marinho P, Valente RM, Montag LFA. Feeding ecology of Serrasalmus gouldingi (Characiformes: Serrasalmidae) in the lower Anapu River region, Eastern Amazon, Brazil. Acta Amaz. 2016; 46(3):259-70. https://doi.org/10.1590/1809-4392201600123
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; Dary et al., 2017Dary EP, Ferreira E, Zuanon J, Röpke CP. Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotrop Ichthyol. 2017; 15(4):e160173. https://doi.org/10.1590/1982-0224-20160173
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), this knowledge is far from being comprehensive, given the high fish diversity in the Neotropical region, especially in the Amazon Basin (Reis et al., 2016Reis RE, Albert JS, Di Dario F, Mincarone MM, Petry P, Rocha LA. Fish biodiversity and conservation in South America. J Fish Biol . 2016; 89(1):12-47. https://doi.org/10.1111/jfb.13016
https://doi.org/10.1111/jfb.13016...
). For Auchenipteridae catfishes, for instance, the knowledge gaps on feeding habits [see Raunkiæran shortfalls in Hortal et al. (2015Hortal J, de Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu Rev Ecol Evol Syst. 2015; 46(1):523-49. https://doi.org/10.1146/annurev-ecolsys-112414-054400
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)] are noteworthy, and information about their diet is still accumulating with every new study published (Freitas et al., 2021Freitas TMS, Stropp J, Calegari BB, Calatayud J, De Marco P, Montag LFA et al. Quantifying shortfalls in the knowledge on Neotropical Auchenipteridae fishes. Fish Fish. 2021; 22(1):87-104. https://doi.org/10.1111/faf.12507
https://doi.org/10.1111/faf.12507...
).

The Xingu River is an important tributary on the right bank of the Amazon River, widely known for its complex geomorphology resulting in rapids and anastomosing channels (Fitzgerald et al., 2018Fitzgerald DB, Sabaj Perez MH, Sousa LM, Gonçalves AP, Rapp Py-Daniel L, Lujan NK et al. Diversity and community structure of rapids-dwelling fishes of the Xingu River: Implications for conservation amid large-scale hydroelectric development. Biol Conserv. 2018; 222:104-12. https://doi.org/10.1016/j.biocon.2018.04.002
https://doi.org/10.1016/j.biocon.2018.04...
). It also harbors a fish diversity with high rates of endemism (Dagosta, De Pinna, 2019Dagosta FCP, De Pinna M. The fishes of the Amazon: distribution and biogeographical patterns, with a comprehensive list of species. Bull Am Mus Nat Hist. 2019; 2019(431):1-163. https://doi.org/10.1206/0003-0090.431.1.1
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), many of them important in artisanal fisheries (Issac et al., 2015Isaac VJ, Almeida MCD, Cruz REA, Nunes LG. Artisanal fisheries of the Xingu River basin in Brazilian Amazon. Braz J Biol . 2015; 75(3):125-37. https://doi.org/10.1590/1519-6984.00314BM
https://doi.org/10.1590/1519-6984.00314B...
) and ornamental fish trade (Ramos et al., 2015Ramos FM, Araújo MLG, Prang G, Fujimoto RY. Ornamental fish of economic and biological importance to the Xingu River. Braz J Biol . 2015; 75(3):95-98. https://doi.org/10.1590/1519-6984.02614BM
https://doi.org/10.1590/1519-6984.02614B...
). The species of the present study, the auchenipterids Auchenipterus nuchalis (Spix & Agassiz, 1829) and Tocantinsia piresi (Miranda Ribeiro, 1920), are among the most abundant species of the middle Xingu River, being considered relevant ecological models to advance the understanding of the effect of river fluviometric dynamics on the trophic ecology of fish in this region. In addition, these species were also considered a target species in the Basic Environmental Plan, which is used to support mitigation and compensatory actions for environmental impacts identified during the environmental licensing process for the construction of the Belo Monte Dam. In previous studies, A. nuchalis and T. piresi were described as insectivorous (Pouilly et al., 2004Pouilly M, Yunoki T, Rosales C, Torres L. Trophic structure of fish assemblages from Mamoré River floodplain lakes (Bolivia). Ecol Freshw Fish . 2004; 13(4):245-57. https://doi.org/10.1111/j.1600-0633.2004.00055.x
https://doi.org/10.1111/j.1600-0633.2004...
; Mérona, Vigouroux, 2006Mérona B, Vigouroux R. Diet changes in fish species from a large reservoir in South America and their impact on the trophic structure of fish assemblages (Petit-Saut Dam, French Guiana). Ann Limnol - Int J Limnol. 2006; 42(1):53-61. https://doi.org/10.1051/limn/2006006
https://doi.org/10.1051/limn/2006006...
) and insectivorous/frugivorous (Carvalho, Kawakami, 1984Carvalho FM, Kawakami ER. Aspectos da Biologia de Tocantinsia depressa (Siluriformes, Auchenipteridae). Amazoniana. 1984; 8(3):327-37. http://hdl.handle.net/21.11116/0000-0004-6E55-2
http://hdl.handle.net/21.11116/0000-0004...
; Dary et al., 2017Dary EP, Ferreira E, Zuanon J, Röpke CP. Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotrop Ichthyol. 2017; 15(4):e160173. https://doi.org/10.1590/1982-0224-20160173
https://doi.org/10.1590/1982-0224-201601...
), respectively. Considering that this region was recently affected by one of the most controversial hydropower plants in the Amazon, the Belo Monte (concluded in November 2015), our research provides novel ecological data before the complete Xingu River damming.

In this sense, we aimed to evaluate how the water level variation in the middle Xingu River affects the feeding ecology of A. nuchalis and T. piresi. We expected a higher contribution of allochthonous resources in the diet composition, lower niche breadth, and greater feeding intensity during high water periods for both species.

MATERIAL AND METHODS

Study area. The study was carried out on the middle Xingu River (03º12’52”S 52º11’23”W) - a right-bank tributary of the Amazon River - and in their tributaries Bacajá River (03º45’12”S 51º34’59”W) and Iriri River (03º49’33”S 52º41’36”W) (Fig. 1). Known as “Volta Grande”, this section of the Xingu River basin is characterized by clear water with high flow over a bedrock. This region presents a marked fluviometric variation, with water levels increasing by 5 m during the flood season, creating larges floodplain areas. During the studied period (from April 2012 to January 2014), the local monthly precipitation and water level ranged from 10.8 mm to 478.3 mm (INMET, 2014Instituto Nacional de Meteorologia (INMET). Banco de dados meteorológicos para ensino e pesquisa. 2014.) and 245 cm to 737 cm (ANA, 2018Agência Nacional de Águas (ANA). Rede Hidrometeorológica Nacional [Internet]. 2018. Available from: http://www.snirh.gov.br/gestorpcd/Mapa.aspx
http://www.snirh.gov.br/gestorpcd/Mapa.a...
), respectively. Thus, we considered four distinct hydrological periods: flood (between March and May), ebb (June-August), dry (September-November), and filling (December and February), as previously defined by Freitas et al. (2015Freitas TMS, Prudente BS, Oliveira V, Oliveira MNC, Prata EG, Leão H et al. Influence of the flood pulse on the reproduction of Tocantinsia piresi (Miranda Ribeiro) and Auchenipterus nuchalis (Spix & Agassiz) (Auchenipteridae) of the middle Xingu River, Brazil. Braz J Biol . 2015; 75(3 suppl 1):158-67. https://doi.org/10.1590/1519-6984.00114BM
https://doi.org/10.1590/1519-6984.00114B...
). These hydrological periods were herein used as a proxy to flood pulse dynamics (Fig. S1 ).

FIGURE 1
| Study area on the middle Xingu River (Eastern Amazon, Brazil). The black dots represent the sampling sites, and the arrows indicate the direction of the water flow. Black triangle = Altamira municipality; black star = Belo Monte Dam.

Sampling sites. Fishes were sampled quarterly between April 2012 and January 2014, totaling eight field expeditions, with each hydrological season being assessed twice. We defined ten areas separated by approximately 40 km in the fluvial distance (Fig. 1), which, when sampled quarterly results in 80 sampling sites (ss). In each sampling site, three sets of gillnets of monofilament nylon (meshes of 2, 4, 7, 10, 12, 15, and 18 cm) with 100 m-long and two m-height (each) were disposed for twelve hours and harvested every six hours. When sampled alive, the specimens were anesthetized using clove oil (Fernandes et al., 2017Fernandes IM, Bastos YF, Barreto DS, Lourenço LS, Penha JM. The efficacy of clove oil as an anaesthetic and in euthanasia procedure for small-sized tropical fishes. Braz J Biol . 2017, 77(3):444-50. https://doi.org/10.1590/1519-6984.15015
https://doi.org/10.1590/1519-6984.15015...
).

Standard length (SL, cm), total weight (WT, g), and stomach weight (WS, g) were measured for all collected specimens of A. nuchalis and T. piresi. Voucher specimens were fixed in 10% formalin solution for approximately 48h, transferred to 70% ethanol, and deposited at the Laboratório de Ictiologia de Altamira (LIA), Universidade Federal do Pará (UFPA), municipality of Altamira, Pará State, Brazil, under the code: LIA 363 for A. nuchalis and LIA 383 for T. piresi.

Stomach contents were identified to the lowest taxonomic level possible using specialized literature (Costa et al., 2006Costa C, Ide S, Simonka CE. Insetos imaturos: Metamorfose e identificação. Ribeirão Preto: Holos; 2006.; Hamada, Ferreira-Keppler, 2012Hamada N, Ferreira-Keppler RL. Guia ilustrado de insetos aquáticos e semiaquáticos da Reserva Florestal Ducke. Manaus: EDUA - Universidade Federal do Amazonas; 2012.) and expert assistance, and weighed (precision of 0.001 g). For each food item, the frequency of occurrence (FO%; Hyslop, 1980Hyslop EJ. Stomach contents analysis-a review of methods and their application. J Fish Biol . 1980; 17(4):411-29. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
https://doi.org/10.1111/j.1095-8649.1980...
) and mass percentage (M%; Hynes, 1950Hynes HBN. The food of fresh-water sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius), with a review of methods used in studies of the food of fishes. J Anim Ecol. 1950; 19(1):36. https://doi.org/10.2307/1570
https://doi.org/10.2307/1570...
) were calculated, and then combined into the Alimentary Index (Ai%; changed from Kawakami, Vazzoler, 1980Kawakami E, Vazzoler G. Método gráfico e estimativa de índice alimentar aplicado no estudo de alimentação de peixes. Bol Inst Ocean. 1980; 29(2):205-07. https://doi.org/10.1590/S0373-55241980000200043
https://doi.org/10.1590/S0373-5524198000...
), which attributed the importance of each item in the fish diet. The Ai% was calculated by the equation, Ai%=FO%×M%/FO%×M%×100. Food items were grouped into ten categories: Algae, Aquatic insects, Arachnids, Crustaceans, Fish, Fruit and seeds, Mollusks, Other plant fragments (e.g., branches, leaves, and flowers), Terrestrial insects, and Terrestrial vertebrates, which also had their respective values of Ai% calculated.

Data analysis. For both species, variation in diet composition between hydrological periods was assessed using a Principal Coordinates Analysis (PCoA) based on a Bray-Curtis similarity matrix of the log-transformed categorical Ai% values and tested using a global and pairwise Permutational Multivariate Analysis of Variance (PERMANOVA). This analysis was followed by a similarity percentage analysis (SIMPER) to determine the diet category responsible for diet dissimilarity among the hydrological periods. For PCoA and PERMANOVA, we grouped the different years in the hydrological periods, considered only hydrological periods represented by at least three sampling sites and sampling sites with at least two non-empty stomachs, minimal numbers required to carry out the statistical test and obtain the alimentary index, respectively.

To verify if the origin of the resource consumed by the species varied between hydrological periods, food items were grouped into autochthonous (originates from the aquatic environment) and allochthonous resources (from the terrestrial environment), and then had their alimentary index (Ai%) calculated. These values were visually examined against the hydrological period.

Trophic niche breadth was assessed by testing homogeneity of dispersion in diet composition (PERMDISP, Permutational Analysis of Multivariate Dispersion), a dissimilarity-based multivariate extension of Levene’s test (Anderson et al., 2008Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: Primer-E; 2008.). This test is based on the ANOVA F statistic, which compares the average distances from observed values and their centroid. Greater dispersion values indicate greater niche amplitude. PCoA, PERMANOVA, and PERMDISP analyses were performed in the statistical software PRIMER 6 (Clarke, Gorley, 2006Clarke KR, Gorley RN. PRIMER v6: User Manual/ Tutorial. Plymouth: Primer-E ; 2006.) with PERMANOVA+1.0.3 package (Anderson et al., 2008Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: Primer-E; 2008.).

Differences in the total amount of food intake between hydrological periods were evaluated using the Repletion Index (RI%), given by the equation RI%=WS/WT×100 (Santos, 1979Santos EP. Dinâmica de populações aplicada à pesca e piscicultura. São Paulo: HUCITEC; 1979.), where WS is the stomach weight and WT is the total weight. Considering that these data did not meet the assumptions of parametric tests, RI% values were tested using a Kruskal-Wallis (H) test followed by a Mann-Whitney pairwise comparison test (Zar, 2010Zar JH. Biostatistical Analysis. 5th ed. New Jersey: Prentice Hall; 2010.). Finally, the relationship between the amount of ingested food (RI% values) and average fluviometric quotas [obtained from ANA (2018)] was assessed based on a beta regression analysis (using betareg package in R environment). It assumes that response variables are proportions or percentages values and are beta distributed (Cribari-Neto, Zeileis, 2010Cribari-Neto F, Zeileis A. Beta regression in R. J Stat Softw. 2010; 34(2):1-24. https://doi.org/10.18637/jss.v034.i02
https://doi.org/10.18637/jss.v034.i02...
). Visual inspection of the residuals validated the betareg model. Finally, empty stomachs were not considered in any previous analysis. All statistics tested were carried out considering a significance level of 0.05 (Zar, 2010Zar JH. Biostatistical Analysis. 5th ed. New Jersey: Prentice Hall; 2010.).

RESULTS

A total of 360 stomachs of A. nuchalis and 584 T. piresi were analyzed, of which 221 and 333 had stomach content, respectively. The standard length of T. piresi ranged from 9.3 to 46.0 cm (mean = 31.3; standard deviation = 5.3), and for A. nuchalis ranged from 8.1 to 19.5 cm (mean = 12.4; standard deviation = 2.0). Based on the criteria of sampling site selection (see Material and methods), the diet composition was analyzed considering 16 sampling sites for A. nuchalis and 28 sampling sites for T. piresi. The number of stomachs and sampling sites assessed by season/year for A. nuchalis and T. piresi are shown in Tabs. 1-2, respectively.

TABLE 1
| Alimentary Index (Ai%) of food items in the diet of Auchenipterus nuchalis from the Xingu River, Eastern Amazon, Brazil. n = number of stomachs evaluated. ss = number of sampling sites. The food categories are shown in bold.

TABLE 2
| Alimentary Index (Ai%) of food items in the diet of Tocantinsia piresi from the Xingu River, Eastern Amazon, Brazil. n = number of stomachs evaluated. ss = number of sampling sites. The food categories are shown in bold.

The diet of A. nuchalis was composed of 27 food items (Tab. 1), primarily autochthonous items such as aquatic insects (76.0 Ai%) and crustaceans (16.5 Ai%). The first two axes of the principal coordinate analysis (PCoA) explained 53.4% and 29.1% of the total variation in the diet composition of A. nuchalis, respectively (Fig. 2A). We observed variation in diet composition among the hydrological periods (Pseudo-F = 3.303, p = 0.012), with a significant difference between dry and filling seasons (p = 0.024). According to the SIMPER analysis, the average dissimilarity between these seasons was equal to 71.52%. It was mainly influenced by the consumption of crustaceans (percentage of contribution = 30.78%), followed by aquatic insects (30.69%) and terrestrial insects (27.57%). The contribution of the other categories was less than 11%.

FIGURE 2
| Graphic representation of the Principal Coordinates Analysis (PCoA) of the diet composition of Auchenipterus nuchalis (A) from the Xingu River (Eastern Amazon, Brazil). Colors represent the hydrological seasons: flood (blue), dry (red), and filling (green). The contribution of the main food items is expressed according to the circle size (B - terrestrial insects; C - aquatic insects; and D - crustaceans). The purple color represents an overlap of dry and flood samples.

The diet of A. nuchalis was predominantly composed of crustaceans during the dry season in 2012 (99.77 Ai%) (Fig. 2B) and aquatic insects during the dry season in 2013 (99.99 Ai%), while in the filling season in 2013 and 2014 the diet was composed by aquatic insects (62.64 and 75.0 Ai%, respectively), and terrestrial insects (25.46 and 22.96 Ai%, respectively) (Figs. 2C, D). During the food season in 2012 and 2013, the diet was mainly composed by aquatic insects (59.20 and 90.29 Ai%, respectively). The ebb was not included in the PERMANOVA analysis because it was represented by only two sampling sites (Tab. 1). In this period, we analyzed 13 stomachs of A. nuchalis, recording a diet mainly composed of crustaceans (94.35 Ai%). No specimen of A. nuchalis was caught in the ebb 2013.

For T. piresi, the diet was composed of 30 food items (Tab. 2), with high consumption of fruit and seeds (98.17 Ai%). The first two axes of PCoA explained 58.4% and 20.2% of the diet composition of T. piresi, respectively (Fig. 3A). As for A. nuchalis, the diet of T. piresi differed between hydrological periods (Pseudo-F = 6.073, p = 0.001) (Tab. 3). Differences in diet composition were observed between flood and ebb season (p = 0.0332) and between filling and ebb season (p = 0.009). The SIMPER analysis evidenced an average dissimilarity of 65.41% between flood and ebb season, which was influenced essentially by the consumption of fruits and seeds (percentage contribution = 29.50%), followed by fishes (19.73%) and aquatic insects (17.75%). The average dissimilarity between filling and ebb season was 60.59%, with a higher percentage contribution from the consumption of fruits and seeds (28.90%), followed by aquatic insects (17.73%) and fishes (17.29%). The other categories presented a percentage contribution of less than 15.5%

FIGURE 3
| Graphic representation of the Principal Coordinates Analysis (PCoA) of the diet composition of Tocantinsia piresi (A) from the Xingu River (Eastern Amazon, Brazil). Colors represent the hydrological seasons: flood (blue), ebb (yellow), and filling (green). The contribution of the main food items is expressed according to the circle size (B - fruits and seeds; C - aquatic insects; and D - fish).

TABLE 3
| Statistical values for the diet composition (PERMANOVA and PERMDISP) of Auchenipterus nuchalis and Tocantinsia piresi from the Xingu River, Eastern Amazon, Brazil. *Statistical differences.

Although fruits and seeds were predominant in all hydrological seasons (Fig. 3B), the diet of T. piresi in the ebb 2013 was mainly composed of aquatic insects (91.95 Ai%) (Fig. 3C). The dry season was not considered in the PERMANOVA analysis; only two sampling sites (and four stomachs) represented the dry 2012 (Tab. 2). In this period, the diet was composed of fish (37.57 Ai%) (Fig. 3D), aquatic insects (37.40 Ai%), and terrestrial insects (24.87 Ai%). We caught no specimen of T. piresi in the dry 2013.

Regarding the origin of the food items, the diet of A. nuchalis was composed of 80% of autochthonous items throughout the studied period (Fig. 4A). On the other hand, the diet of T. piresi was highly changeable during the study period. During the higher water periods (flood and filling periods) and the ebb 2012, the diet of T. piresi was composed of more than 90% of allochthonous items. Elseways, autochthonous items were the primary food source (more than 90%) during the dry 2012 and ebb 2013 (Fig. 4B).

FIGURE 4
| Alimentary index (Ai%) values of the autochthonous (dark gray) and allochthonous (light gray) items of the diet of Auchenipterus nuchalis (A) and Tocantinsia piresi (B) from the Xingu River (Eastern Amazon, Brazil). The dotted line represents the fluviometric variation. Asterisks indicate the months which was not obtained the minimal specimens numbers required to obtain the alimentary index.

Differences in trophic niche breadth between hydrological periods (PERMDISP analysis) were not significant for A. nuchalis (F = 0.192, p = 0.828), but were significant for T. piresi (F = 6.151, p = 0.006), with differences between flood and ebb seasons (t = 5.619; p = 0.001), and ebb and filling (t = 3.187; p = 0.005) (Tab. 3). The PERMDISP result of T. piresi suggests a more specialist feeding strategy during the flood and filling seasons (centroid distance; cd = 0.103 and 0.191, respectively), against a more generalist feeding habit in the ebb season (cd = 0.425) (Tab. 3). The dry season was not considered in the PERMDISP analysis based on the sampling site selection criteria.

The amount of food eaten (RI%) by A. nuchalis differed in relation to the hydrological periods assessed (H6, 0.05 = 33.95; p < 0.001; Fig. 5B). The highest levels of feed intensity were registered during the dry 2012 (mean RI% = 0.50; standard deviation = 0.74) and dry 2013 (0.32 ± 0.61), and the lowest values of RI% were in the flood 2012 (0.07 ± 0.06) and flood 2013 (0.08 ± 0.15). However, differences were only observed when we compared the RI% values of dry 2013 with the periods filling 2013 (p = 0.001), flood 2013 (p < 0.001), and filling 2014 (p = 0.004) (Tab. 4).

FIGURE 5
| Variation in the Repletion Index (RI%) of Auchenipterus nuchalis (A-C) and Tocantinsia piresi (B-D) from the Xingu River (Eastern Amazon, Brazil). Black line represents the linear regression model (C-D).

TABLE 4
| Pairwise comparison of Repletion Index (RI%) of Auchenipterus nuchalis and Tocantinsia piresi from the Xingu River, Eastern Amazon, Brazil. *Statistical differences.

For T. piresi, RI% values also differed between hydrological periods (H6, 0.05 = 68.76; p < 0.001; Fig. 5B). The highest levels of feed intensity were registered during the flood 2012 (mean RI% = 4.38 ± 4.33) and filling 2014 (2.66 ± 2.64), and the lowest values of RI% were in the dry 2012 (0.05 ± 0.05) and flood 2013 (0.35 ± 0.35). During the flood 2012, this species presented a higher feeding intensity when compared to almost all studied periods, except ebb 2012 and filling 2014 (all p < 0.05; see Tab. 4). Repletion values also differed between filling 2014 and dry 2012 (p = 0.020), and filling 2012 (p < 0.001) (Tab. 4).

Additionally, the beta regression model showed a weak relationship between the feeding intensity and fluviometric quota for both species. The RI% values of A. nuchalis were negatively related to the fluviometry (estimate = -0.001, Z = -2.873, df = 3, p = 0.004; Pseudo R²= 0.061) (Fig. 5C). Otherwise, the RI% values of T. piresi were positively related to the fluviometry (estimate = 0.001, Z = 3.853, df = 3, p < 0.001; Pseudo R²= 0.062) (Fig. 5D). The highest feeding intensity was registered in the flood 2012 (mean RI% = 4.38 ± 4.33) and filling 2014 seasons (mean RI% = 2.66 ± 2.64), and the lowest values of RI% were in the dry 2012 season (mean RI% = 0.05 ± 0.05) and ebb 2012 period (mean RI% = 0.35 ± 0.35). The Fig. 6 shows an infographic summary of the results obtained herein.

FIGURE 6
| Infographic summarizing the feeding ecology of Auchenipterus nuchalis and Tocantinsia piresi from the Xingu River, Eastern Amazon, Brazil.

DISCUSSION

The diet analysis revealed an invertivorous habit for Auchenipterus nuchalis, feeding primally on autochthonous insects and crustaceans, and can be considered an invertivore species, predominantly consuming invertebrates of autochthonous origin, with higher food intake during dry seasons. For Tocantinsia piresi, the feeding habit was omnivorous, with a predominantly frugivorous habit, manly during the high water periods, and aquatic insects and fish during the low water periods. This fact highlighted a specialized trophic niche breadth of T. piresi during the flood season and generalist habits during the low water periods. Additionally, the highest food intake also occurred in higher water periods.

The insectivorous diet of A. nuchalis observed in the present study was also recorded in the central Amazon floodplains, in the confluence of the Amazon and Negro rivers (Mérona, Rankin-de-Mérona, 2004Mérona B de, Rankin-de-Mérona J. Food resource partitioning in a fish community of the central Amazon floodplain. Neotrop Ichthyol . 2004; 2(2):75-84. https://doi.org/10.1590/S1679-62252004000200004
https://doi.org/10.1590/S1679-6225200400...
), as well as in the lower Tocantins River, which is affected by the Tucuruí Dam in the Eastern Amazon (Mérona et al., 2001Mérona B de, Santos GM dos, Almeida RG de. Short term effects of Tucuruí Dam (Amazonia, Brazil) on the trophic organization of fish communities. Environ Biol Fishes. 2001; 60(4):375-92. https://doi.org/10.1023/A:1011033025706
https://doi.org/10.1023/A:1011033025706...
). In the latter study, changes in the diet composition of A. nuchalis occurred because of the reservoir closure; before the dam closure, the diet was insectivore, and after the river closure, the feeding habit of this species changed to that of an unspecialized carnivore (Mérona et al., 2001Mérona B de, Santos GM dos, Almeida RG de. Short term effects of Tucuruí Dam (Amazonia, Brazil) on the trophic organization of fish communities. Environ Biol Fishes. 2001; 60(4):375-92. https://doi.org/10.1023/A:1011033025706
https://doi.org/10.1023/A:1011033025706...
). Likewise, the tendency of a frugivorous feeding habit recorded in the present study for T. piresi was previously described in a mid-course of the Teles Pires River (Tapajós basin), where the species showed a predominance in the consumption of vascular plants and fish (Dary et al., 2017Dary EP, Ferreira E, Zuanon J, Röpke CP. Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotrop Ichthyol. 2017; 15(4):e160173. https://doi.org/10.1590/1982-0224-20160173
https://doi.org/10.1590/1982-0224-201601...
). These studies reinforce the variety of feeding habits among auchenipterids fishes.

Both species varied their diet composition in response to changes in hydrological periods. However, the flood pulse had a different influence on the feeding ecology of these auchenipterids. The more significant interaction between the aquatic and terrestrial ecosystem promoted by the rising of the water level (Junk et al., 1989Junk W, Bayley P, Sparks R. The flood pulse concept in river-floodplain systems. Can J Fish Aquat. 1989; 106(1):110-27.) did not increase allochthonous sources in the diet of A. nuchalis. However, we presume that the floodplain areas formed by the river flooding may affect the abundance, distribution, and life cycle of many benthic macroinvertebrate assemblages, including the prey species consumed by A. nuchalis, such as aquatic insects and crustaceans (McClain, 2002McClain ME. The ecohydrology of South American rivers and Wetlands. Florida, USA: International Association of Hydrological Sciences; 2002.; Wantzen et al., 2016Wantzen KM, Marchese MR, Marques MI, Battirola LD. Invertebrates in Neotropical Floodplains. In: Batzer D, Boix D, editors. Invertebrates in Freshwater Waterlands. Cham: Springer International Publishing; 2016. p.493-524. https://doi.org/10.1007/978-3-319-24978-0_14
https://doi.org/10.1007/978-3-319-24978-...
; Piniewski et al., 2017Piniewski M, Prudhomme C, Acreman MC, Tylec L, Oglęcki P, Okruszko T. Responses of fish and invertebrates to floods and droughts in Europe. Ecohydrology. 2017; 10(1):e1793. https://doi.org/10.1002/eco.1793
https://doi.org/10.1002/eco.1793...
). In contrast, changes in the feeding ecology of T. piresi can be directly associated with local flood pulse. This species fed profusely on fruits and seeds of terrestrial plants in the periods of higher water levels, during which several plant species are bearing mature fruit (Maia, Jackson, 2000Maia LMA, Jackson MB. Morphological and growth responses of woody plant seedlings to flooding of the central Amazon floodplain forests. SIL Proceedings, 1922-2010. 2000; 27(4):1711-16. https://doi.org/10.1080/03680770.1998.11901534
https://doi.org/10.1080/03680770.1998.11...
). This allochthonous resource is considered an important energy source for many Amazonian fishes (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. Berkeley, CA: University of California Press; 1980. 280p.; Correa et al., 2007Correa SB, Winemiller KO, López-Fernández H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience. 2007; 57(9):748-56. https://doi.org/10.1641/B570907
https://doi.org/10.1641/B570907...
). In this context, T. piresi consumes as many fruits as possible during the floods to store energy for gonadal maturation, which occurs at the lower water periods (Freitas et al., 2015Freitas TMS, Prudente BS, Oliveira V, Oliveira MNC, Prata EG, Leão H et al. Influence of the flood pulse on the reproduction of Tocantinsia piresi (Miranda Ribeiro) and Auchenipterus nuchalis (Spix & Agassiz) (Auchenipteridae) of the middle Xingu River, Brazil. Braz J Biol . 2015; 75(3 suppl 1):158-67. https://doi.org/10.1590/1519-6984.00114BM
https://doi.org/10.1590/1519-6984.00114B...
). In the dry season, when seeds and fruits are no longer available, T. piresi inhabit burrows in riverbed rocks (Freitas et al., 2015) and change the diet to aquatic insects and fish.

Other auchenipterid species has also been studied concerning the trophic ecology and the flood pulse dynamics; Auchenipterichthys longimanus (Günther, 1864) had more food intake in the flood period when fruits were abundant (Freitas et al., 2011Freitas TMS, Almeida VHC, Valente RM, Montag LFA. Feeding ecology of Auchenipterichthys longimanus (Siluriformes: Auchenipteridae) in a riparian flooded forest of Eastern Amazonia, Brazil. Neotrop Ichthyol . 2011; 9(3):629-36. https://doi.org/10.1590/S1679-62252011005000032
https://doi.org/10.1590/S1679-6225201100...
); Trachelyopterus galeatus (Linnaeus, 1766) consumed mainly allochthonous items during the flood period such as terrestrial insects and fruits (Santos, 2005Santos ACA. Ecologia alimentar do molé, Trachelyopterus galeatus Linnaeus, 1766 (Siluriformes, Auchenipteridae), em trechos inferiores dos rios Santo Antônio e São José (Chapada Diamantina, Bahia). Sitientibus Sér Ciênc Biol. 2005; 5:93-98.; Garcia et al., 2020Garcia DAZ, Tonella LH, Alves GHZ, Vidotto-Magnoni AP, Benedito E, Britton JR, Orsi ML. Seasonal and habitat variations in diet of the invasive driftwood catfish Trachelyopterus galeatus in a Neotropical river basin, Brazil. J Appl Ichthyol. 2020; 36(3):26-335. https://doi.org/10.1111/jai.14035
https://doi.org/10.1111/jai.14035...
); and Ageneiosus apiaka Ribeiro, Rapp Py-Daniel & Walsh, 2017 shifted from aquatic insects to crustaceans when the water level starts to rise (Dary et al., 2017Dary EP, Ferreira E, Zuanon J, Röpke CP. Diet and trophic structure of the fish assemblage in the mid-course of the Teles Pires River, Tapajós River basin, Brazil. Neotrop Ichthyol. 2017; 15(4):e160173. https://doi.org/10.1590/1982-0224-20160173
https://doi.org/10.1590/1982-0224-201601...
). Despite the studies mentioned above, information on how hydrological changes affect feeding ecology of auchenipterid species remains scarce (e.g., Andrian, Barbieri, 1996Andrian IF, Barbieri G. Espectro alimentar e variações sazonal e espacial na composição da dieta de Parauchenipterus galeatus Linnaeus, 1766 (Siluriformes, Auchenipteridae) na região do reservatório de Itaipu, PR. Rev Bras Biol. 1996; 56:409-22.; Santos, 2005Santos ACA. Ecologia alimentar do molé, Trachelyopterus galeatus Linnaeus, 1766 (Siluriformes, Auchenipteridae), em trechos inferiores dos rios Santo Antônio e São José (Chapada Diamantina, Bahia). Sitientibus Sér Ciênc Biol. 2005; 5:93-98.; Freitas et al., 2011Freitas TMS, Almeida VHC, Valente RM, Montag LFA. Feeding ecology of Auchenipterichthys longimanus (Siluriformes: Auchenipteridae) in a riparian flooded forest of Eastern Amazonia, Brazil. Neotrop Ichthyol . 2011; 9(3):629-36. https://doi.org/10.1590/S1679-62252011005000032
https://doi.org/10.1590/S1679-6225201100...
).

Many studies highlight the importance of flooded areas, their vegetation for aquatic communities, the diversity of different food and/or prey items available in these temporary habitats, and the flexibility in fish responses to spatial and temporal patterns in food source availability (Mortillaro et al., 2015Mortillaro JM, Pouilly M, Wach M, Freitas CEC, Abril G, Meziane T. Trophic opportunism of central Amazon floodplain fish. Freshw Biol. 2015; 60(8):1659-70. https://doi.org/10.1111/fwb.12598
https://doi.org/10.1111/fwb.12598...
; Pereira et al., 2017Pereira LS, Tencatt LFC, Dias RM, de Oliveira AG, Agostinho AA. Effects of long and short flooding years on the feeding ecology of piscivorous fish in floodplain river systems. Hydrobiologia . 2017; 795(1):65-80. https://doi.org/10.1007/s10750-017-3115-5
https://doi.org/10.1007/s10750-017-3115-...
; Pool et al., 2017Pool T, Holtgrieve G, Elliott, McCann K, McMeans B, Rooney N et al. Seasonal increase in fish trophic niche plasticity within a flood-pulse river ecosystem (Tonle Sap Lake, Cambodia). Ecosphere 2017; 8(7):e01881. https://doi.org/10.1002/ecs2.1881
https://doi.org/10.1002/ecs2.1881...
; Barbosa et al., 2018Barbosa TAP, Rosa DCO, Soares BE, Costa CHA, Esposito MC, Montag LFA. Effect of flood pulses on the trophic ecology of four piscivorous fishes from the eastern Amazon. J Fish Biol. 2018; 93(1):30-39. https://doi.org/10.1111/jfb.13669
https://doi.org/10.1111/jfb.13669...
). The role of the flood pulse is also associated with other ecological aspects worldwide, such as the increase of fish recruitment during periods with higher water levels (Linhoss et al., 2012Linhoss AC, Muñoz-Carpena R, Allen MS, Kiker G, Mosepele K. A flood pulse driven fish population model for the Okavango Delta, Botswana. Ecol. Model. 2012; 228:27-38. https://doi.org/10.1016/j.ecolmodel.2011.12.022
https://doi.org/10.1016/j.ecolmodel.2011...
) and structuring fish assemblages (Gomes et al., 2012Gomes LC, Bulla CK, Agostinho AA, Vasconcelos LP, Miranda LE. Fish assemblage dynamics in a Neotropical floodplain relative to aquatic macrophytes and the homogenizing effect of a flood pulse. Hydrobiologia. 2012; 685(1):97-107. https://doi.org/10.1007/s10750-011-0870-6
https://doi.org/10.1007/s10750-011-0870-...
; Barbosa et al., 2015Barbosa T, Benone N, Begot T, Gonçalves A, Sousa L, Giarrizzo T et al. Effect of waterfalls and the flood pulse on the structure of fish assemblages of the middle Xingu River in the eastern Amazon basin. Braz J Biol. 2015; 75(3 suppl 1):78-94. https://doi.org/10.1590/1519-6984.00214BM
https://doi.org/10.1590/1519-6984.00214B...
). Specific effects in local assemblages, or species, are far away from being fully unraveled.

Concerning niche breadth, only T. piresi presented a distinct feeding strategy between hydrological periods. During the flood period, the more specialist habit was determined by higher consumption of a single food item (fruits). Besides a high energetic value (Goulding, 1980Goulding M. The fishes and the forest: explorations in Amazonian natural history. Berkeley, CA: University of California Press; 1980. 280p.; Correa et al., 2007Correa SB, Winemiller KO, López-Fernández H, Galetti M. Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience. 2007; 57(9):748-56. https://doi.org/10.1641/B570907
https://doi.org/10.1641/B570907...
), the larger availability of fruits also requires a lower energy investment during foraging when compared with other food items, such as fish or macroinvertebrates. For A. nuchalis, the lack of distinctiveness in feeding strategies between hydrological seasons is due to the prevalence of feeding on aquatic invertebrates during the most of hydrological periods, except for ebb and dry of 2012. We believe that the more generalist feeding habit of A. nuchalis may balance the energy investment in foraging required during active searches for aquatic insects and crustaceans.

The amount of food eaten by A. nuchalis and T. piresi reinforces the distinct trophic behavior between these two auchenipterids. Auchenipterus nuchalis increased feeding intensity during the dry and ebb seasons, the period of which aquatic insects and/or crustaceans have their density and distribution limited to the river channel (Junk et al., 1989Junk W, Bayley P, Sparks R. The flood pulse concept in river-floodplain systems. Can J Fish Aquat. 1989; 106(1):110-27.), which may facilitate their capture by these predators. Although this pattern is often described for piscivorous species (Luz-Agostinho et al., 2008Luz-Agostinho KDG, Agostinho AA, Gomes LC, Júlio HF. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Paraná River floodplain. Hydrobiologia . 2008; 607(1):187. https://doi.org/10.1007/s10750-008-9390-4
https://doi.org/10.1007/s10750-008-9390-...
; Prudente et al., 2016Prudente BS, Carneiro-Marinho P, Valente RM, Montag LFA. Feeding ecology of Serrasalmus gouldingi (Characiformes: Serrasalmidae) in the lower Anapu River region, Eastern Amazon, Brazil. Acta Amaz. 2016; 46(3):259-70. https://doi.org/10.1590/1809-4392201600123
https://doi.org/10.1590/1809-43922016001...
; Barbosa et al., 2018Barbosa TAP, Rosa DCO, Soares BE, Costa CHA, Esposito MC, Montag LFA. Effect of flood pulses on the trophic ecology of four piscivorous fishes from the eastern Amazon. J Fish Biol. 2018; 93(1):30-39. https://doi.org/10.1111/jfb.13669
https://doi.org/10.1111/jfb.13669...
), it can be extrapolated for aquatic invertebrate’s feeders. On the other hand, T. piresi showed a higher feeding intensity during the flood season due to a greater intake of seeds and fruits. Well-documented studies report the relationship between terrestrial plant fruits and fish diet (Freitas et al., 2011Freitas TMS, Almeida VHC, Valente RM, Montag LFA. Feeding ecology of Auchenipterichthys longimanus (Siluriformes: Auchenipteridae) in a riparian flooded forest of Eastern Amazonia, Brazil. Neotrop Ichthyol . 2011; 9(3):629-36. https://doi.org/10.1590/S1679-62252011005000032
https://doi.org/10.1590/S1679-6225201100...
; Correa, Winemiller, 2014Correa SB, Winemiller KO. Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest. Ecology. 2014; 95(1): 210-24. https://doi.org/10.1890/13-0393.1
https://doi.org/10.1890/13-0393.1...
). During the high-water periods occur the fruitification of many floodplain trees (Maia, Jackson, 2000Maia LMA, Jackson MB. Morphological and growth responses of woody plant seedlings to flooding of the central Amazon floodplain forests. SIL Proceedings, 1922-2010. 2000; 27(4):1711-16. https://doi.org/10.1080/03680770.1998.11901534
https://doi.org/10.1080/03680770.1998.11...
; Ferreira, Parolin, 2007Ferreira LV, Parolin P. Tree phenology in Central Amazonian Floodplain forests: effects of water level fluctuation and precipitation at community and population level. Pesquisas série Botânica. 2007, 58:139-56.), which are frequently eaten and dispersed by fishes (Correa, Winemiller, 2014Correa SB, Winemiller KO. Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest. Ecology. 2014; 95(1): 210-24. https://doi.org/10.1890/13-0393.1
https://doi.org/10.1890/13-0393.1...
; Freitas et al., 2018Freitas TMS, Prudente BS, Oliveira V, Oliveira MNC, Prata EG, Leão H et al. Influence of the flood pulse on the reproduction of Tocantinsia piresi (Miranda Ribeiro) and Auchenipterus nuchalis (Spix & Agassiz) (Auchenipteridae) of the middle Xingu River, Brazil. Braz J Biol . 2015; 75(3 suppl 1):158-67. https://doi.org/10.1590/1519-6984.00114BM
https://doi.org/10.1590/1519-6984.00114B...
).

The present study highlights that many aspects of the fish ecology are influenced by the natural flood pulse, making it challenging to plan a general prediction of the impacts on local river hydrological alterations (e.g., by dams and removal of riparian vegetation) (Junk et al., 1989Junk W, Bayley P, Sparks R. The flood pulse concept in river-floodplain systems. Can J Fish Aquat. 1989; 106(1):110-27.; Bayley et al., 2018Bayley PB, Castello L, Batista VS, Fabré NN. Response of Prochilodus nigricans to flood pulse variation in the central Amazon. R Soc Open Sci. 2018; 5(6):172232. https://doi.org/10.1098/rsos.172232
https://doi.org/10.1098/rsos.172232...
). Even within a single taxonomic group, such as Auchenipteridae, we evidenced heterogeneity of ecological strategy in response to the flood pulse. Consequently, these species take part in different ecosystem functions, which need to be considered when discussing biodiversity and ecosystem conservation.

In this context, we believe that A. nuchalis and T. piresi present different responses to the environmental changes caused by the Belo Monte Dam built concluded in November 2015. In general, river damming results in many negatives disturbs in aquatic ecosystems dynamic such as water flow changes, blocks animal movements, disrupts downstream transport of nutrients, softening of the seasonal foods, and decreasing floodplains productivity (Castello, Macedo, 2016Castello L, Macedo MN. Large-scale degradation of Amazonian freshwater ecosystems. Global Change Biol. 2016; 22(3):990-1007. https://doi.org/10.1111/gcb.13173
https://doi.org/10.1111/gcb.13173...
; Winemiller et al., 2016Winemiller KO, McIntyre PB, Castello L, Fluet-Chouinard E, Giarrizzo T, Nam S et al. Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science. 2016; 351(6269):128-29. https://doi.org/10.1126/science.aac7082
https://doi.org/10.1126/science.aac7082...
). For the fish fauna, the reduction of the flood pulse dynamic in the dam reservoir may diminish the availability of seeds and fruit for frugivorous populations (T. piresi in our case), as well as threaten seed dispersal processes (Galetti et al., 2008Galetti M, Donatti CI, Pizo MA, Giacomini HC. Big fish are the best: Seed dispersal of Bactris glaucescens by the pacu fish (Piaractus mesopotamicus) in the Pantanal, Brazil. Biotropica. 2008; 40(3):386-89. https://doi.org/10.1111/j.1744-7429.2007.00378.x
https://doi.org/10.1111/j.1744-7429.2007...
). There is a better chance that aquatic insects and crustaceans will maintain their population dynamics (Principe, 2010Principe RE. Ecological effects of small dams on benthic macroinvertebrate communities of mountain streams (Córdoba, Argentina). Ann Limnol - Int J Limnol . 2010; 46(2):77-91. https://doi.org/10.1051/limn/2010010
https://doi.org/10.1051/limn/2010010...
; Piniewski et al., 2017Piniewski M, Prudhomme C, Acreman MC, Tylec L, Oglęcki P, Okruszko T. Responses of fish and invertebrates to floods and droughts in Europe. Ecohydrology. 2017; 10(1):e1793. https://doi.org/10.1002/eco.1793
https://doi.org/10.1002/eco.1793...
) and their availability for invertivorous organisms. However, there is already evidence of a decline in the abundance and diversity of aquatic insects because of environmental changes caused by river damming (e.g., physical-chemical parameters of water) (Romero et al., 2021Romero GQ, Moi DA, Nash LN, Antiqueira PA, Mormul RP, Kratina P. Pervasive decline of subtropical aquatic insects over 20 years driven by water transparency, non-native fish and stoichiometric imbalance. Biol Lett. 2021, 17(6):20210137. https://doi.org/10.1098/rsbl.2021.0137
https://doi.org/10.1098/rsbl.2021.0137...
). Such adverse effects in fish populations have been reported for the Tucuruí reservoir (Tocantins River), where A. nuchalis is still frequently collected, and T. piresi is one of the species considered locally extinct (Mérona et al., 2001Mérona B de, Santos GM dos, Almeida RG de. Short term effects of Tucuruí Dam (Amazonia, Brazil) on the trophic organization of fish communities. Environ Biol Fishes. 2001; 60(4):375-92. https://doi.org/10.1023/A:1011033025706
https://doi.org/10.1023/A:1011033025706...
). Finally, we emphasize that studies considering the relationship between flood pulse and feeding ecology of the organisms are essential to better understand the dynamics of river-floodplain systems. It becomes even more crucial considering the current habitat modifications that are continually being planned in many South American river basins (Winemiller et al., 2016Winemiller KO, McIntyre PB, Castello L, Fluet-Chouinard E, Giarrizzo T, Nam S et al. Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science. 2016; 351(6269):128-29. https://doi.org/10.1126/science.aac7082
https://doi.org/10.1126/science.aac7082...
).

Thus, besides filling existing knowledge gaps on the ecological relationships between fish species and the environment, our findings also highlight the potential impacts on aquatic systems caused by the Belo Monte and could be used in future comparisons and conservation and management of regional fish species. We also encourage further research in the study area to track and elucidate the effects caused by the Belo Monte in the fish diet and their population dynamics.

All in all, our results demonstrate that a seasonal variability of the diet of two auchenipterid catfishes may be linked to the flood pulse. However, the hydrological variations may be causing different effects on the feeding ecology of these two phylogenetic-related fish species. Even though the flood pulse affects the diet composition of both species, the feeding strategy (niche breadth) and feeding intensity of A. nuchalis were not affected by the local flooding dynamic and showed a more generalist feeding strategy than T. piresi. The more significant influence of the Xingu River flood pulse in the feeding ecology of T. piresi over A. nuchalis also allows us to infer about distinct responses of the species to anthropogenic disturbances on the natural hydrological regimes, such as the construction of the Belo Monte dam. To better understand the resistance capacity of these populations to anthropogenic disturbance requires the knowledge of many other ecological aspects, such as behavior and interspecific relationships, which should be considered in future studies.

ACKNOWLEDGMENTS

The authors are grateful to Norte Energia, LEME, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Finance code 001) (LFAM - process 88881.119097/2016-01), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; LFAM - process 302406/2019-0) for financial support. We also thank all the members of the IctioXingu CNPq Research Group. To Dr. Alistair John Campbell for English review.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Freitas TMS, Prudente BS, Montag LFA. Flood pulse influence on the feeding ecology of two Amazonian auchenipterid catfishes. Neotrop Ichthyol. 2022; 20(1):e210103. https://doi.org/10.1590/1982-0224-2021-0103

Edited by

Rosemara Fugi

Publication Dates

  • Publication in this collection
    28 Mar 2022
  • Date of issue
    2022

History

  • Received
    13 June 2021
  • Accepted
    09 Nov 2021
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br