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Diet of an Assemblage of Four Species of Turtles (Podocnemis) in the Rio Uatumã, Amazonas, Brazil

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Diet of an Assemblage of Four Species of Turtles (Podocnemis) in the Rio Uatumã, Amazonas, Brazil Copeia 108, No. 1, 2020, 103–115 Diet of an Assemblage of Four Species of Turtles (Podocnemis) in the Rio Uatuma˜, Amazonas, Brazil Fernando L. R. Cunha1,2, Rafael Bernhard3, and Richard C. Vogt1 The structure and functioning of freshwater turtle communities remain understudied topics, especially in tropical regions where biodiversity is higher. The objective of our study was to compare the diets of Podocnemis erythrocephala, P. expansa, P. sextuberculata, and P. unifilis living in syntopy in Amazonas, Brazil. We tested for qualitative and quantitative variations in the way different species used the same available food resources. We collected fresh stomach flushings from all turtles captured in trammel nets in three lakes in 2012. Sampling was conducted in the four distinct tropical seasons: beginning of rainy season (rising water), peak of rainy season (rapidly rising water), end of rainy season (highest flooded forest water level), and dry season (when water levels were receding). We tested the hypothesis that different food items are available in different quantities at different times of the year due to the seasonality of fruiting trees and other plants in response to the wet and dry conditions. We examined whether food items consumed were related to turtle body size and if there was feeding niche overlap among species. Podocnemis sextuberculata consumed the least amount of food by volume, while P. expansa consumed the highest diversity of food items. All four species are primarily herbivorous, and their diets were composed mainly of fruits and seeds (85.4% mean proportion by volume). Genipa americana (Rubiaceae) was most important in the diet of all species, except in P. sextuberculata. We found some evidence of seasonal differences in the consumption of some plant species. Body size did not influence qualitative (diversity of food items eaten) or quantitative variation of food items (volume), except in P. erythrocephala for which we detected a significant linear relationship between carapace length and the volume of stomach contents. The highest food niche overlap was between P. expansa and P. unifilis, and the lowest niche overlap was between P. erythrocephala and P. sextuberculata. Turtles tended to partition food resources more in areas that had more species feeding in syntopy than in areas with fewer syntopic species. A estrutura e o funcionamento de comunidades de tartarugas de a´gua doce permanecem sendo topicos´ pouco estudados, especialmente em regioes˜ tropicais onde a biodiversidade e´ alta. O objetivo do nosso estudo foi comparar as dietas de Podocnemis erythrocephala, P. expansa, P. sextuberculata, P. unifilis vivendo em sintopia no Amazonas, Brasil. Nos´ testamos as varia¸coes˜ qualitativas e quantitativas no modo em que as diferentes especies´ usaram os mesmos recursos alimentares dispon´ıveis. Nos´ coletamos amostras dos conteudos´ estomacais, por meio de lavagens,de todas as tartarugas capturadas, utilizando-se as redes do tipo malhadeiras feiticeiras em tresˆ lagos no ano de 2012. Amostragem foi conduzida nas quatro diferentes esta¸coes˜ tropicais: come¸cando pela esta¸ca˜o chuvosa (a´guas subindo), pico da esta¸ca˜o chuvosa (a´guas subindo rapidamente), fim da esta¸ca˜o chuvosa (maior n´ıvel de a´gua nas florestas alagadas) e esta¸ca˜o seca (quando o n´ıvel das a´guas estava diminuindo). Nos´ testamos a hipotese´ que diferentes itens alimentares esta˜o dispon´ıveis em diferentes quantidades em diferentes epocas´ do ano devido a` sazonalidade de frutifica¸ca˜o das a´rvores e outros vegetais em resposta a`s condi¸coes˜ de umidade e seca. Nos´ testamos se os itens alimentares consumidos estavam relacionados com o tamanho corporal das tartarugas e se havia sobreposi¸ca˜o de nicho alimentar entre as especies.´ Podocnemis sextuberculata consumiu a menor quantidade de alimento por volume, enquanto P. expansa consumiu a maior diversidade de itens alimentares. Todas as quatro especies´ sa˜o primariamente herb´ıvoras e suas dietas foram compostas principalmente por frutos e sementes (85,4% de propor¸ca˜omedia´ por volume). Genipa americana (Rubiacea) foi o item mais importante na dieta de todas as especies,´ com exce¸ca˜odeP. sextuberculata.Nos´ encontramos alguma evidenciaˆ de diferen¸cas sazonais no consumo de algumas especies´ vegetais. Tamanho corporal na˜o teve influenciaˆ na varia¸ca˜o qualitativa (diversidade dos itens alimentares consumidos) nem na varia¸ca˜o quantitativa dos itens alimentares (volumes), exceto em P. erythrocephala, para a qual nos´ detectamos uma rela¸ca˜o linear significativa entre comprimento de carapa¸ca e volumes dos conteudos´ estomacais. A maior sobreposi¸ca˜o de nicho alimentar foi obtida entre P. expansa e P. unifilis, e a mais baixa entre P. sextuberculata e P. erythrocephala. Tartarugas tendem a particionar mais os recursos alimentares em a´reas em que ha´ mais especies´ se alimentando em sintopia do que em a´reas com menos especies´ sintopicas.´ ESOURCE partitioning studies describe the patterns our understanding about the instability of food chains that occur in interacting communities of animals (Goodyear and Pianka, 2011). The structure and function- R and help to understand factors that cause these ing of freshwater turtle communities remain understudied partitioning patterns (Schoener, 1977). The availability of topics, even though the basics of population ecology are food items in a habitat is the principal limiting factor for a known. More studies are needed, especially from tropical forager (Perry and Pianka, 1997), and understanding the regions where turtle species richness and diversity are high degree of variation of diets in natural populations increases (Luiselli, 2008). 1 CEQUA, CBIO, Instituto Nacional de Pesquisas da Amazonia,ˆ Av. Andre´ Araujo´ 2936, Petropolis,´ CEP 69.067-375 Manaus, Amazonas, Brazil; Email: (RCV) [email protected]. Send reprint requests to RCV. 2 Programa de Pos-gradua¸´ ca˜o em Biologia de A´ gua Doce e Pesca Interior, Instituto Nacional de Pesquisas da Amazonia,ˆ Av. Andre´ Araujo´ 2936, Petropolis,´ CEP 69.067-375, Manaus, Amazonas, Brazil. 3 Centro de Estudos Superiores de Tefe,´ Estrada do Bexiga, 1085, Bairro Jerusalem, CEP10 69470-000, Tefe,´ Amazonas, Brazil. Submitted: 6 September 2018. Accepted: 17 December 2019. Associate Editor: J. D. Litzgus. Ó 2020 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CE-18-117 Published online: 03 March 2020 104 Copeia 108, No. 1, 2020 Luiselli (2008) reviewed 26 published studies on resource Conservation and management of species of Podocnemis in partitioning in freshwater turtle communities worldwide the Brazilian Amazon have revolved around protecting the finding that among the four resource dimensions studied nesting beaches; this is not enough if their feeding habitats (macrohabitat, microhabitat [basking sites], food, and time), and the plant species they feed on are not also protected. It is basking site was the most important dimension (80%), important to document which plant species and which parts followed by food resource dimension (70%). Many Neotrop- of the plants the turtles feed on and to understand the ical species of freshwater turtles in Mexico (Legler and Vogt, nutritional quality of the plants used by turtles. These results 2013) and the Brazilian Amazon (Vogt, 2008) do not ever will be important not only for turtle management and bask, some are completely nocturnal, and others never leave protection of flooded forests in natural areas, but they can the water, even to nest; thus, we expect to find higher indices also inform the provision of food plants where these turtles of food partitioning or foraging habitat in these species. Most are farmed for meat production. There are 60 large hydro- species of turtles are generalist omnivores (Lagler, 1943; Vogt electric dams programmed to flood forests along most of the and Villarreal-Benitez, 1997; Legler and Vogt, 2013) and use rivers in the Amazon Basin (Fearnside, 2006); we must the resources that are the most abundant and easily delineate the flooded forests to be protected for turtle accessible in their habitat. Dietary studies have shown that foraging habitat before they are gone. To our knowledge, turtles change their preferences both quantitatively and ours is the first study of the feeding behavior of four qualitatively at different times of the year depending on freshwater turtle species of the same genus in the same the seasonality of the food resources available (Mahmoud, locality. 1968; Dreslik, 1999; Alcalde et al., 2010). Variation in food items consumed among turtle populations from different MATERIALS AND METHODS habitats reflects the diverse resource options available in Turtles were collected in the Uatuma˜ Sustainable Develop- these habitats (Lagler, 1943; Fach´ın-Tera´n et al., 1995; Perez-´ ment Reserve (424,430 ha), in the municipalities of Sa˜o Santigosa et al., 2011). Body size also influences turtle Sebastia˜odoUatuma˜ and Itapiranga, Amazonas, Brazil feeding behavior (Mahmoud, 1968; Bury, 1986; Vogt and (Ferreira, 2009). The reserve is located in the lower third of Villarreal-Benitez, 1997), and in turn, feeding behavior the Uatuma˜ River Basin, a tributary of the Amazon River, influences body size. For example, in kinosternid turtles, downstream from Manaus. The climate of the region is individuals that eat more animal protein grow larger, and classified by Koppen(1931)asAmazoniantropicalmon-¨ megacephaly evolves in populations in which individuals soon (meaning that there
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