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 are periods of extensive rainfall; feed on mollusks (Vogt and Guzman, 1988; Iverson, 1999). Peel et al., 2007). Turtles were captured using trammel nets Food habits of sympatric species can be linked through (Vogt, 1980) during four months in 2012, representing the spatial and temporal variation of resource availability, as well four annual seasons: January (rising water, beginning of as through interactions among the foraging species (Vitt and rainy season), April (rising water, height of rainy season), Zani, 1998). Patterns of resource partitioning can facilitate June (highest water levels, end of rainy season), and August coexistence of several species in the same habitat (Vogt and (dry season) in three oxbow lakes in the RDS Uatuma˜: Guzman, 1988). Calabar, Maracarana, and Jaraoaca´ (Fig. 1). Each turtle When resources are limited, interspecific interactions may captured was identified to species and sexed (if mature), affect the abundances of coexisting species depending on the marked with individual notches in the marginal scutes level of overlap of the resources that are partitioned (Cagle, 1939), measured for total straight-line carapace (Schoener, 1983; Aresco, 2010); in areas of unlimited food length with calipers, and the stomach was flushed with resources, resource partitioning is not expected to occur. Low water (Legler, 1977) before being released at the site of values of niche overlap may be interpreted as evidence of capture. Stomach contents were preserved in 70% ethanol resource partitioning (Lindeman, 2000), such that species are and stored in individually marked plastic tubes. We feeding on different food items (Toft, 1985). Food is followed the ethical directions suggested by the American considered one of the principal components of the niche in Society of Ichthyologists and Herpetologists for the treat- studies of sympatric species (Pianka, 1973; Schoener, 1974). ment of reptiles and amphibians (ASIH, 2004). Few of the studies that compare resource use in turtle Stomach flushings were separated into four categories communities use food niche overlap coefficients or null with the use of a dissection microscope: plant, animal, models for the analysis of pseudo-communities (Lindeman, mineral, and unidentified material. Plant material was 2000; Luiselli, 2008). Studies of the four species of Podocnemis separated into seven subcategories: fruits and seeds, stems in the Brazilian Amazon show that they are primarily and shoots, leaves, flowers, roots, miscellaneous (small herbivorous; however, the differences in diet and niche portions of everything else that appeared to be from plants), overlap among sympatric members of this genus are unclear and unidentified plant material. Animal material was (Ojasti, 1971; Almeida et al., 1986; Fach´ın-Tera´n et al., 1995; separated into vertebrate and invertebrate categories. Min- Balensiefer and Vogt, 2006), and the four species do not eral material was considered sediment (this included sand usually occur in syntopy. and rocks). The Uatuma˜ River, a clear water river, is the only river Stomach contents were analyzed quantitatively by vol- system where all four species of Podocnemis occur in syntopy; ume (Hyslop, 1980). After identifying and separating the thus, we investigated the diets and resource partitioning stomach contents, each group of items was measured among these species at this locality. We compared variation volumetrically (to 0.01 ml) by water displacement in a in diet with turtle body size to test the hypothesis that graduated cylinder to 0.01 ml. Qualitative analysis was through indices of food consumption, food may be a limiting made to the lowest taxonomic level possible using special- factor for the coexistence of these four species. ists of the taxonomic group and specific literature (Maia, Cunha et al.—Amazon turtle diet 105

Fig. 1. (A ) Location of Reserva de Desenvolvimento Sustenta´vel (RDS) Uatuma˜ in the state of Amazonas, Brazil. (B) Points where nets were set to capture turtles in lakes (C) Calabar, (D) Maracarana, and (D) Jaraoaca´.

2001; Wittmann et al., 2010). Since some turtle species were meet the assumptions of normality. Third, we used Non- captured in low numbers in some seasons, we only analyzed metric Multidimensional Scaling (NMDS; Kruskal, 1964) to

niche overlap when we had at least three individuals of each test whether qualitative differences in food items were related species. to body size in each species of Podocnemis. NMDS provides a graphical representation of similarity in ordinal space Data analysis.—Frequency of occurrence (frequency of (Gotelli and Ellison, 2011), and is an iterative method that stomachs that had each type of food category) and uses several repetitions to arrive at the result and each time proportion of volume were determined for each category, generates a partial result that will be used in the subsequent subcategory, and food item. The Index of Relative iteration. The first step is to create an array of distances and Importance (IRI) was calculated to show which food items random points on a graph of n dimensions (usually two or were most represented in the diet of each species (Bjorndal three), then the Euclidean distance between each of the pairs et al., 1997 adapted from Hyslop, 1980). From this of points is calculated to create another array, and finally the analysis, we obtained a ranking of the food items in order first array is correlated with the second and checked for of decreasing importance. We used the formula IRI ¼ 100 * similarities, resulting in a STRESS index (Standardized (FO*V)/R (FO*V), where FO ¼ frequency of occurrence for Residual Sum of Squares) that serves as a test of goodness each category and V ¼ proportion of volume for each of fit. A lower STRESS value (small percentage value) indicates category. greater similarity and better fit (Legendre and Legendre, We used the nonparametric Kruskal-Wallis (H) test to 1998). In our study, we used two dimensions and generated determine if there were differences in the volume of stomach contents among the four species of Podocnemis and if there 10,000 random points. NMDS analyses were performed using were spatial and seasonal inter- and intraspecific variations in the total volumes of 11 food subcategories (Table 1) and with the volumes of the food items consumed. To test if there were all the food items found in all species, with the exception of differences in the volumes between pairs of species and inter unidentified material. First, the ordination was made with all and intra specific sexual variations, we used the Mann- the species of turtles and then differentiated by sex, location, Whitney (U) test. The volumes of the stomach flushings of and season of all individuals of Podocnemis spp. The two axes the four species were pooled to test if total volume differed generated were extracted from the scores that were tested by among seasons, localities, and between sexes. means of linear regression with variable: carapace length. We examined the potential relationships between diet and NMDS analyses were conducted in the statistical program R body size in several ways. First, we used the coefficient of (R Core Team, 2012) using the Vegan bundle (Oksanen, variation (r2) to explain the proportion of the variation in the 2011). y variable (total volume of stomach contents) attributable to To investigate interspecific differences in feeding over- the variation in the x variable (carapace length; Gotelli and lap, we used the technique of null models, which Ellison, 2011). We used a 5% significance level. Second, to generates random iterative simulations of pseudocomun- test the relationship between carapace length and total ities. These data are then put into an array of resource use volume of the stomach contents of each species, we used a (Gotelli and Graves, 1996; Lindeman, 2000), where we simple linear regression with log transformed data (log10)to used the index of Pianka (1973) represented by the 106 Copeia 108, No. 1, 2020

Table 1. Percent volume (V) and frequency of occurrence (FO) of the categories and subcategories found in the diet of the four species of Podocnemis in the RDS Uatuma˜, Amazonas. P. erythrocephala P. expansa P. sextuberculata P. unifilis

V% FO% V% FO% V% FO% V% FO%

Categories Plant material 96.8 90.9 98.7 90.2 96.8 68.4 99.5 88.9 Animal material 3.1 27.3 0.5 26.8 1.4 5.3 0.1 8.3 Mineral material — — ,0.1 2.4 — — ,0.1 2.8 Unidentified 0.1 18.2 0.8 21.9 1.8 36.8 0.3 19.4 Subcategories Fruits and seeds 88.7 81.8 83.7 87.8 89.8 52.6 79.5 72.2 Stems and shoots 2.0 54.5 3.6 56.1 2.7 10.5 2.5 58.3 Flowers — — ,0.1 9.8 — — ,0.1 2.8 Leaves 0.1 9.1 2.7 46.3 0.7 10.5 12.1 58.3 Roots — — ,0.1 2.4 — — — — Miscellaneous 5.9 18.2 7.6 19.5 3.3 5.3 3.6 16.7 Unidentified plant material — — 1.0 24.4 0.2 5.3 1.7 8.3 Vertebrates 1.4 27.3 0.3 12.2 — — 0.1 8.3 Invertebrates 1.7 18.2 0.2 24.4 1.4 5.3 ,0.1 2.8 Sediment — — ,0.1 2.4 — — ,0.1 2.8 Unidentified 0.1 18.2 0.8 21.9 1.8 36.8 0.3 19.4 following formula: The ordination of food items and subcategories of food items did not reveal any patterns among the turtle species (Figs. 3, Xn 4). Similarly, the analysis of subcategories of food items was PijPik not related to turtle carapace length (r2 ¼ 0.016; P ¼ 0.11) for Ø ¼ sffiffiffiffiffiffiffiffiffiffiffiffiffii¼1 jk Xn Xn the first axis of ordination. However, the analysis of all the P2 P2 ij ik food items had a significant relationship to carapace length i¼1 i¼1 (r2 ¼ 0.027; P ¼ 0.05), in this case for the second axis of ordination. Where P represents the proportion of food item i used, n is the number of food items, and j and k represent the two Variation in volume of stomach contents among turtle species species being compared. The total volumes of all of the food and sexes.—Paired comparisons of the volumes of stomach items identified for all four turtle species were included in contents between turtle species differentiated P. sextuberculata this analysis. Niche overlap (Øjk) can range from zero (no from the other three species (P. erythrocephala U ¼ 151, P ¼ overlap) to one (complete overlap); this index was calculated 0.04; P. expansa U ¼ 619, P , 0.01; and P. unifilis U ¼ 205.5, P for each turtle species pair. We used the Niche Overlap ¼ 0.02). Module Eco Sim 7.0 (Gotelli and Entsminger, 2001), with The relative volume of stomach contents of females did 1000 random points for this analysis. not vary among the four species (H ¼ 6.25; P ¼ 0.10). Podocnemis expansa differed from P. unifilis (U ¼ 194; P , RESULTS 0.05). Podocnemis expansa and P. sextuberculata did not differ. Volume of stomach contents and turtle carapace length.—We There was a difference in the relative volume of stomach flushed the stomachs of 130 individual turtles, obtaining contents of males among species (H ¼ 340 8.65; P ¼ 0.03), stomach contents from 107: 41 P. expansa (30 females and 11 with P. sextuberculata differing from P. expansa (U ¼ 109; P ¼ males), 36 P. unifilis (9 females, 26 males, and 1 subadult), 19 0.03) and P. unifilis (U ¼ 82; P ¼ 0.01) but not P. erythrocephala P. sextuberculata (6 females and 13 males), and 11 P. (U ¼ 77; P ¼ 0.07). erythrocephala (3 females and 8 males). Only in Jaraoaca´ Lake did we collect all four species of Podocnemis. Podocnemis Taxonomic appraisal of stomach flushings.—Plant material expansa, as expected because of its larger size, had the greatest represented a mean of 98.0% of the total volume of the total volume of stomach contents (mean ¼ 7.166.4 ml), stomach contents collected from the four species of Podocne- followed by P. unifilis (4.966.4 ml), P. erythrocephala (3.562.9 mis and was present in 84.6% of the stomach contents ml), and P. sextuberculata (2.3065.0 ml). The relative volume examined. The diet of Podocnemis was composed primarily of of stomach contents differed among the four species of fruits and seeds (85.4% by volume [mean]) and was present Podocnemis (H ¼ 14.43; P , 0.01). Carapace length of P. in a mean of 73.6% of the stomach contents (Table 1). erythrocephala was positively related to the volume of Overall, we found 56 different types of food items in the diet stomach contents (Fig. 2A). Carapace length of individuals of the four species of Podocnemis studied (Appendix 1). of P. expansa was not related to variation in volume of plant Podocnemis expansa had the greatest number of items (49), or animal material in their stomachs. followed by P. unifilis with 26 items, P. erythrocephala with 19 items, and P. sextuberculata with 14 food items. We identified Influence of turtle body size on resources eaten.—We did not 20 different types of fruits and seeds. Seven were identified to find qualitative differences in diet in relation to body size. species, three others to genus, and one to family level Cunha et al.—Amazon turtle diet 107

Fig. 2. Relationship between total volume of stomach contents and straight line carapace length of individuals of (A) Podocnemis erythrocephala (n ¼ 11), (B) P. expansa (n ¼ 41), (C) P. sextuberculata (n ¼ 19), and (D) P. unifilis (n ¼ 36), in RDS Uatuma˜, Amazonas.

(Appendix 1). Eight different morphotypes of fruits and seeds Pouteria sp. was present in 36.8% of the turtles, representing were found in the diet of P. expansa, two in P. unifilis, and one 26.4% of the total volume of the stomach flushings from all in P. erythrocephala (Appendix 1). We were unable to identify of the turtles sampled (Appendix 1). Poaceae was found in nine of these morphotypes of fruits and seeds; which the diet of 10.5% of the individuals of Podocnemis sextubercu- corresponded to 1.2% of the volume of P. erythrocephala, lata sampled, representing 17% of the volume and the third 2.1% in P. expansa, and 4.5% in P. unifilis. Podocnemis expansa most common item consumed. Leaves were present in the had the greatest number of types of fruits and seeds (18), stomach contents of all four turtle species. Leaves composed followed by P. unifilis (10), P. erythrocephala (9), and P. 12.1% of the volume of stomach contents of P. unifilis sextuberculata (4). Amanoa oblongifolia (Euphorbiaceae) and (Appendix 1). Five types of leaves were separated from P. Genipa americana (Rubiaceae) were the only plant species that erythrocephala, P. expansa, and P. unifilis. Leaves were found in occurred in all four species of Podocnemis. 27.8% of the sample P. unifilis. Unidentified leaves were Genipa americana (Jenipapo) was abundant in the diet of all found in 47.2% of the stomach contents of P. unifilis sampled four species, and it was the most important food in their diet (Appendix 1). Unidentified shoots and stems were found in except in P. sextuberculata, for which it was the second most all species and were present in 58.3% of the individuals of P. important food item (IRI; Appendix 1). Even though Amanoa unifilis, 56.1% of P. expansa, 54.5% of P. erythrocephala, and oblongifolia was in the diet of all four species, its representa- only 10.5% of P. sextuberculata. Stems and shoots were fifth in tion varied from 3rd in rank in P. erythrocephala and P. rank in P. expansa, P. unifilis, and P. sextuberculata, and sixth in expansa,to7th in P. sextuberculata, and 9th in P. unifilis. Fruits P. erythrocephala (Appendix 1). and seeds of Macrolobium acaciifolium, Eugenia inundata, and The small amount of animal material within the stomach Pouteria sp. were found in P. sextuberculata. Macrolobium contents included a diverse array of taxa: six orders of insects, acaciifolium was the second most common item found in two orders of fishes, decapods, arachnids, sponges, and parts 24.4% of the stomachs of P. expansa sampled. Pouteria sp. of reptiles. Scales and vertebral bones of fishes were found in occupied the second rank in Podocnemis erythrocephala, found all turtle species except P. sextuberculata. Perciforms were in 18.2% of the individuals sampled, Pouteria sp. was also found in P. expansa and P. unifilis, while siluriforms were only found in 44.4% of the Podocnemis unifilis.InP. sextuberculata, found in P. expansa (Appendix 1). Fish parts represented only 108 Copeia 108, No. 1, 2020

Fig. 4. Non-metric Multidimensional Scaling (NMDS) of the total Fig. 3. Non-metric Multidimensional Scaling (NMDS) of the total volume of food items found in the four species of Podocnemis in the volume of the subcategories of food items found in the four species of RDS Uatuma˜, Amazonas. P. erythrocephala (square), P. expansa ˜ Podocnemis in the RDS Uatuma, Amazonas. Podocnemis erythroce- (circle), P. sextuberculata (triangle), and P. unifilis (diamond). The phala (square), P. expansa (circle), P. sextuberculata (triangle), and P. STRESS similarity index ¼ 0.099. STRESS ¼ Standardized Residual Sum unifilis (diamond). The STRESS similarity index ¼ 0.020. STRESS ¼ of Squares; the lower the value of STRESS, the better the data fit. Standardized Residual Sum of Squares; the lower the value of STRESS, the better the data fit (Legendre and Legendre, 1998). The STRESS value here is lower than that in Figure 4, suggesting that the use of Seasonality and comparisons of volumes of stomach contents subcategories of food items was more important for distinguishing the among species and localities.—The most common fruits and feeding habits among these four turtle species than the volume of seeds observed during the different seasons (Appendix 1) general food items. were Amanoa oblongifolia and Macrolobium acaciifolium, which occurred in the stomach contents of P. expansa in all a mean volume of 0.2% in the species of Podocnemis studied. seasons. Genipa americana was found in P. erythrocephala, P. Parts of insects were found in all four turtle species, but they expansa, and P. unifilis only during the first season. Oriza was represented only 0.1% of the mean volume. The orders found only in the first season in P. sextuberculata and P. Ephemeroptera, Hemiptera, Odonata, and Orthoptera were unifilis. Most of the fruits and seeds present in the stomachs found in the stomach contents of P. expansa, while P. of turtles were found in all three lakes except for Eugenia erythrocephala and P. expansa had coleopterans in their diets. inundata, which only occurred in the diet of turtles captured Hymenopterans were found in P. expansa and P. sextuberculata in Maracarana Lake. (Appendix 1). Decapods were found in all turtle species, The relative volumes of P. expansa and P. unifilis differed in shrimp were found in all species except P. unifilis. Crabs were season three (U ¼ 47; P ¼ 0.03; Table 2). In season four, only found in P. erythrocephala. Arachnids and sponges were volume of stomach contents differed among the four turtle found in P. expansa (Appendix 1). species (H ¼ 19.64; P , 0.01). Unidentified matter was found in all turtle species, but it When comparisons were made between pairs of species, made up a small percentage of the material consumed. the volume of stomach contents of P. sextuberculata differed Endoparasites occurred in the stomachs of all species. from the other three species (P. erythrocephala U ¼ 77, P ¼ Nematophila grandis was present in 27.3% of the stomachs 0.02; P. expansa U ¼ 221, P , 0.01; and P. unifilis U ¼ 27, P , of P. erythrocephala and 14.6% of P. expansa, while the 0.01). The volumes of P. expansa and P. erythrocephala also nematode Spinitectus sp. was found in 61.1% of individuals of differed (U ¼ 41; P ¼ 0.047). In Jaraoaca´ Lake, the relative P. unifilis, 54.5% of P. erythrocephala, 26.8% of P. expansa, and volume of stomach contents differed among the four species 5.3% of P. sextuberculata. (H ¼ 9.75; P ¼ 0.02), P. sextuberculata differed from P.

Table 2. Indices of food niche overlap for the four species of Podocnemis. First analyzing total overlap, followed by each of the lakes sampled and months collected in 2012 in the RDS Uatuma˜, Amazonas. Species Total Jaraoaca´ Maracarana Calabar Jan Apr Jun Aug

P. erythrocephala x P. expansa 0.756 0.749 — — — — — 0.674 P. erythrocephala x P. sextuberculata 0.453 0.001 — — – — — 0.002 P. erythrocephala x P. unifilis 0.715 0.086 — — – — — 0.645 P. expansa x P. sextuberculata 0.655 0.003 0.781 0.017 ,0.001 — 0.674 0.014 P. expansa x P. unifilis 0.852 0.152 0.818 0.868 — 0.619 0.224 0.871 P. sextuberculata x P. unifilis 0.766 0.010 0.873 0.010 — — 0.208 0.007 Cunha et al.—Amazon turtle diet 109 erythrocephala (U ¼ 51; P ¼ 0.01), P. expansa (U ¼ 66; P , 0.01), unifilis was found to have a linear relationship between the and P. unifilis (U ¼ 2; P ¼ 0.03). In Calabar and Maracarana carapace length and the consumption of fruits and seeds, lakes, we did not collect any P. erythrocephala with stomach while the consumption of fish decreased with the turtle body contents. In Maracarana Lake, there was no difference in the size (Fach´ın-Tera´n et al., 1995). volumes of stomach contents among the three turtle species We found that in the RDS Uatuma˜, P. sextuberculata had a (H ¼ 2.65; P ¼ 0.27). However, we did find a difference in tendency to use a smaller quantity of food compared to the volume of stomach contents among the three species in other species of Podocnemis. The structure of the stomach of Calabar Lake (H ¼ 8.05; P ¼ 0.02): P. sextuberculata differed P. sextuberculata is different from the herbivore stomachs of from P. expansa (U ¼ 60; P ¼ 0.01) and P. unifilis (U ¼ 362 20.5; the other species of Podocnemis andmorelikethatof P ¼ 0.02). Peltocephalus, an omnivore (Magalha˜es et al., 2014). Perhaps the structure of the stomach does not allow for adequate Overlap of food niche.—The greatest overlap in food niche was flushing, or more likely, this species does not retain food in between P. expansa and P. unifilis (Øjk ¼ 0.852), and the lowest its stomach as long as the other species. For this reason, the index of overlap was between P. erythrocephala and P. quantities flushed out are smaller. Stomach flushing in turtles sextuberculata (Øjk ¼ 0.453; Table 2). In summary, when each is successful because turtles swallow everything whole or in of the localities was analyzed separately, in Jaraoaca´ Lake, large bites; they do not chew their food and digestion takes where we captured all four species of Podocnemis, we found place in the small intestine (Bjorndal and Bolten, 1993). the lowest indices of niche overlap. In contrast, the greatest Thus, the stomach is a big reservoir waiting to be emptied indices of overlap were found in Maracarana Lake, where we into the small intestine. The herbivorous species have an did not collect P. erythrocephala; this locality had the greatest elongated caecum in the intestine to help digest plant food niche overlap between P. sextuberculata and P. unifilis material, thus digestion and movement through the gut is (Table 2). slower and may be the reason for better results flushing their stomachs (Legler, 1977). Podocnemis sextuberculata can endure DISCUSSION long periods without feeding during the dry season (Fach´ın- Volume of stomach contents and turtle carapace length.—We Tera´n, 1999). did not find a relationship between the volume of stomach Eisemberg et al. (2017) reviewed the studies on the diet of contents and the carapace length of this turtle dataset of four Amazonian river turtles published over the last 40 years, sympatric species collected in four different seasons. Perhaps comparing the effects of body size, phylogeny, season, and this is because the carapace lengths of the turtles captured habitat. They found no correlation between maximum were relatively uniform, since when using trammel nets the carapace size and plant material consumed. Most studies maximum size of the turtle captured is determined by the were conducted during the low-water season when turtles are mesh size of the outer wall, and the minimum size is easier to sample. Seven studies collected data in more than controlled by the mesh size of the inner wall. Thus, we one season; P. unifilis and P. expansa were found to consume compared a more uniform size of turtle from all four species; more fruits by volume in the rising water and high-water large P. expansa were not allowed into the net and small seasons. Independent of the study region, more plant juveniles of all species passed through the inner mesh of the material was consumed during the high-water season. Ten net. Thus, if there is a feeding difference between hatchlings studies compared diet between sexes, and 60% of these or small juveniles, our study was not designed to detect it. studies found dietary differences related to sex. They The relative volume of stomach contents differed among the suggested that future studies should report frequency of four species of Podocnemis. Carapace length of P. erythroce- occurrence, percent volume, and specify dietary items to the phala was positively related to the volume of stomach lowest possible taxonomic level, as well as the parts of the contents (Fig. 2A). Carapace length of the other three species plant consumed. Eisemberg et al. (2017) suggested that was not related to variation in volume of plant or animal dietary studies should test for differences in size, sex, season, material in their stomachs (Fig. 2B, C, D). Possibly the reason and area. We followed these suggestions in our study, but we for this difference was the smaller sample size for P. did not find dietary differences between the sexes, similarly erythrocephala. to 40% of the studies reviewed.

Influence of turtle body size on resources eaten.—We did not Variation in the volume of stomach contents among the species find any influence of turtle body size on food items and sexes.—In P. expansa, fruits and seeds made up 83.7% of consumed. The use of different food resources by Pelomedusa the total volume of the stomach contents; Genipa americana subrufa in Nigeria, Africa also was not related to sizes of the and Macrolobium acaciifolium were the most common plants turtles studied, with the exception that turtles smaller than found in their diet. Ojasti (1971) noted that 86% of the diet 15 cm did not use the same food items as the larger turtles of this species in Venezuela was composed of fruits. Besides (Luiselli et al., 2011). The lack of a relationship between reconfirming this information, Almeida et al. (1986) and volume of the stomach contents and carapace length of P. Figueroa et al. (2012) identified Macrolobium acaciifolium erythrocephala in our study could have been affected by small among the plants most eaten by individuals of P. expansa in sample size; volumes collected for this species in the Rio Para´, Brazil as well as in the Colombian Amazon. This plant Negro were much higher (Vogt, unpubl. data). The lack of a species also proved to be a large component of the diet of relationship between the carapace length and the volume of Peltocephalus dumerilianus in the Rio Negro Amazonas (De La plant material and animal material in P. expansa is corrobo- Ossa et al., 2011). Schongart¨ et al., (2005) noted that M. rated by Balensiefer and Vogt (2006), who analyzed the items acaciifolium is the dominant legume in the Amazon Basin, consumed by P. unifilis, and they likewise did not find a occurring in flooded forests with a great variation in the relationship. However, in the Guapore´ River, Rondonia,ˆ P. concentration of nutrients in different regions, and is used by 110 Copeia 108, No. 1, 2020 many animals in different regions of the Amazon Basin. fruits and seeds between the two studies could be that a large Macrolobium sp. was abundant in the rio Uatuma˜ in the area portion of the plant material in his study could not be inundated by the Balbina reservoir (Walker et al., 1999). identified (40.2%). In P. unifilis, we found an abundance of Within the turtles studied, P. sextuberculata appeared to the fruits and seeds of Pouteria sp., as has been encountered have the most specialized diet. It used the fruits and seeds of in the diet of this species in other regions of the Amazon Poaceae in large quantities, making up 43.4% of the total Basin (Almeida et al., 1986; Fach´ın-Tera´netal.,1995). volume of food consumed. This result corroborates that of Fruits of Genipa americana are important in the diet of all Fach´ın-Tera´n (1999), who found 91% of the food eaten by P. species studied in the RDS Uatuma˜. Genipa sp. were identified sextuberculata was seeds and 86% of the food was species of as part of the diet in other turtle studies as well: P. expansa Poaceae. The low proportion of animal material present in (Almeida et al., 1986; Figueroa et al., 2012), P. sextuberculata the diet of our study species (mean 1.33% of volume of (Almeida et al., 1986), P. unifilis (Almeida et al., 1986; Portal stomach contents) corroborates the findings of Fach´ın-Tera´n et al., 2002), and in terrestrial species (Rueda-Almonacid et et al. (1995) and Balensiefer and Vogt (2006), who found al., 2007). The intense use of this fruit may be because it 1.2% and 0.8%, respectively, in studies of Podocnemis spp. in fruits throughout the year (Almeida et al., 1986). The texture the Brazilian Amazon. We found P. unifilis to consume a of this fruit is also softer than other fruits, facilitating smaller quantity of insects than was found in the incidental consumption and digestion. Since plant material does not consumption verified by Fach´ın-Tera´n et al. (1995). seem to be a limited resource, the turtles do not compete for or partition this resource. Seasonality and comparisons of volumes of stomach contents among species and localities.—It is interesting that Amanoa Overlap of food niche.—We found a great overlap in the food oblongifolia and Macrolobium acaciifolium occurred in the niches of the four syntopic turtle species studied. This result stomach contents of P. expansa in all seasons, suggesting that is similar to that obtained by Bjorndal et al. (1997) in a study even though they are in the same lakes as the other species, of the diet of three sympatric species of Pseudemys in Florida, they may be foraging in different microhabitats. Other USA; they attributed this great overlap to the unlimited species such as Genipa americana and Oriza were seasonally abundance of food in the study area. Alcalde et al. (2010) also found in the stomach contents only in the first season. Most found a reduced overlap in the diets of two species of turtles of the fruits and seeds present in the stomachs of turtles were from different genera. Lindeman (2000) analyzed the overlap found in all three lakes except for Eugenia inundata, which in feeding behavior in Graptemys ouachitensis, G. pseudogeog- only occurred in the diet of turtles captured in Maracarana raphica, Pseudemys concinna, and Trachemys scripta in Ken- Lake, suggesting that this plant has a more restricted tucky, USA; he found the greatest overlap between species in distribution or availability. The relative volumes of stomach the same genus. We did not capture any P. erythrocephala in contents differed in different seasons among the species in Maracarana Lake, suggesting that this species does not seasons one, three, and four, suggesting that the availability inhabit this lake, or that the population is very small. But of food for each species may be limited in their foraging areas in this locality, we found a greater overlap in the food even though they are in the same lakes. consumed by the three species captured, compared to When comparisons were made between pairs of species, Jaraoaca´ Lake, where we captured all four species. Within the volume of stomach contents of P. sextuberculata differed the analyses of null models, lower overlap can be interpreted from the other three species, perhaps because it is more as resource partitioning (Lindeman, 2000). In this manner, omnivorous than the other species. The volumes of P. we verified a tendency for greater resource partitioning in expansa and P. erythrocephala also differed, which is not localities that had a higher number of species feeding than in surprising considering the vast differences in their overall localities with fewer species feeding. The results of food niche size and foraging methods (Vogt, 2008). overlap among the four species of Podocnemis analyzed in our In Jaraoaca´ Lake, the relative volume of stomach contents study showed that the greatest differences in feeding were differed among the four species. Podocnemis sextuberculata found between P. erythrocephala and P. sextuberculata, while differed from P. erythrocephala, P. expansa, and P. unifilis.In the diets of P. expansa and P. unifilis were not very different Maracarana Lake, there was no difference in the volumes of from each other. stomach contents among P. sextuberculata, P. expansa, and P. unifilis, suggesting that availability of forage plants was not Implications for conservation and management.—In RDS limited. However, in Calabar Lake there was a difference in Uatuma˜, all the species of Podocnemis present in Brazil occur the volume of stomach contents among these three species, in sympatry, and they feed primarily on fruits and seeds in suggesting that all habitats might not be equal in the the flooded forests of the reserve. Our data identify the plants availability of forage plants. These differences may be caused important to maintain these turtle species in their natural by the rising and falling water levels. habitat, and can become part of the management plan for turtles in this reserve, noting priority feeding areas. These Taxonomic appraisal of stomach flushings found in these turtle data can also be used for developing commercial food for species.—Fruits and seeds are the basis of the diet of the four captive rearing of turtles in turtle farms using natural turtle species analyzed in our study, corresponding to 88.7% vegetation rather than a commercial feed created from of the volume of the stomach contents of P. erythrocephala; agricultural products such as is done for chickens and fishes. the most common plant species were Genipa americana and Turtles have evolved eating these plants, not corn and Pouteria sp. Santos Junior´ (2009) also noted that 47.7% of the soybeans. Non-selective clear cutting of flooded forest areas food eaten by P. erythrocephala was composed of fruits and for agricultural practices could be responsible for the decline seeds, and similarly noted that Pouteria sp. was important in of these species in many areas in the Amazon Basin; these the diet of this species. The difference in the proportion of flood plain forests have high nutrient soil deposits and are Cunha et al.—Amazon turtle diet 111 coveted by farmers for growing crops during the dry season. Laboratory Research published by the American Society of These areas are also the prime feeding areas for podocnemid Ichthyologists and Herpetologists (2004). Claudia Keller is turtles, and the absence of turtles along the lower Amazon thanked for helping to rewrite the manuscript in English. River Basin may be the result of destroying their feeding habitat rather than outright overuse of adult turtle stocks or LITERATURE CITED their eggs. Studies must be undertaken to designate flooded forest areas that are being used by populations of turtles to Alcalde, L., N. N. Derocco, and S. D. Rosset. 2010. Feeding have these habitats protected from clear cutting. Although in syntopy: diet of Hydromedusa tectifera and Phrynops animals made up less than 1% of the volume of the stomach hilarii (Chelidae). Chelonian Conservation and Biology 9: contents in all of the species studied, these particles may be 33–44. important for turtles to obtain trace elements that are not Almeida, S. S., P. G. S. Sa´, and A. Garcia. 1986. Vegetais available in the plants they consume. Our capture method utilizados como alimento por Podocnemis (Chelonia) na was important in collecting a nearly uniform size of all four Regia˜o do Baixo Rio Xingu (Para´-Brasil). Boletim do Museu species of turtles, and it was not affected by an attraction to Paraense Em´ılio Goeldi, Botaˆnica 2:199–211. dead animals as is often the case when baited hoop traps or Aresco, M. J. 2010. Competitive interactions of two species fyke nets are used. For this reason, we collected more realistic of freshwater turtles, a generalist omnivore and an data of what the turtles eat without having a bias for dead herbivore, under low resource conditions. Herpetologica fishes in the stomach contents or differentially attracting 66:259–268. turtles to trap bait as in other studies of turtles in this family ASIH. 2004. Guidelines for Use of Live Amphibians and (Perez-Ema´ ´n and Paolillo, 1997). Reptiles in Field and Laboratory Research. Second edition, Notice that because nematodes were found in all species of Revised by the Herpetological Animal Care and Use the turtles we studied, the practice of veterinarians in zoos to Committee (HACC) of the American Society of Ichthyol- automatically deparisitize incoming animals may not be a ogists and Herpetologists. Committee Chair: Steven J. good idea in herbivorous turtles, which often have a high Beaupre, Members: Elliott R. Jacobson, Harvey B. Lilly- load of nematodes as well as microorganisms in their small white, and Kelly Zamudio. intestines to help them break down and digest plant Balensiefer, D. C., and R. C. Vogt. 2006. Diet of Podocnemis material. unifilis (Testudines, Podocnemididae) during the dry Because stomach flushing analysis is only a snapshot of season in the Mamiraua´ Sustainable Development Reserve, what the turtle ate in the hours before it was captured, this Amazonas, Brazil. Chelonian Conservation and Biology 5: 312–317. may vary throughout the year depending on the availability of resources, and since the food available for these four Bjorndal, K. A., and A. B. Bolten. 1993. Digestive efficien- species of turtles appears to be in unlimited supply and cies in herbivorous and omnivorous freshwater turtles on highly diverse, future studies should attempt to compare plant diets: Do herbivores have a nutritional advantage? isotope values in these turtles to unmask any subtle Physiological and Biochemical Zoology 66:384–395. differences that are not apparent from stomach flushing. Bjorndal, K. A., A. B. Bolten, C. J. Lagueux, and D. R. Since food does not appear to be a limited resource, it may be Jackson. 1997. Dietary overlap in three sympatric conge- that the four species of Podocnemis do not need to partition it. neric freshwater turtles (Pseudemys) in Florida. Chelonian Lovich et al. 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Appendix 1. Numeric parameters of the food items found in the stomach flushings of Podocnemis spp. in the Reserva de Desenvolvimento Sustenta´vel Uatuma˜, Amazonas. FO: frequency of occurrence (%); V: percent volume (%); IRI: index of Relative Importance; r: ranking; ni: not identified. P. erythrocephala P. expansa P. sextuberculata P. unifilis

FO V IRI r FO V IRI r FO V IRI r FO V IRI r

FRUITS AND SEEDS Bignoniaceae Handroanthus barbatus — — — — 9.76 6.61 2.66 8 — — — — — — — — (E. Mey.) Mattos Euphorbiaceae Amanoa oblongifolia 36.36 5.66 7.73 3 41.46 7.98 13.65 3 5.26 2.88 1.01 7 16.67 3.05 1.44 9 Mull.¨ Arg. Hevea spruceana (Benth.) 9.09 4.11 1.40 8 9.76 7.41 2.98 7 — — — — — — — — Mull.¨ Arg. Fabaceae Macrolobium acaciifolium 18.18 9.00 6.15 4 24.39 15.19 15.28 2 — — — — 13.89 4.95 1.95 7 (Benth.) Benth. Lecythidaceae Eschweilera sp. — — — — — — — — — — — — 5.56 6.75 1.06 10 Malpighiaceae Heteropterys orinocensis 9.09 0.13 0.04 16 14.63 0.29 0.17 17 — — — — — — — — (Kunth) A. Juss. Myrtaceae Eugenia inundata DC. 9.09 13.37 4.57 5 7.32 3.44 1.04 11 — — — — 2.78 0.45 0.03 16 Poaceae Poaceae 1 — — — — — — — — 10.53 17.04 11.96 3 — — — — Oryza — — — — 12.19 0.34 0.17 18 36.84 26.38 64.83 1 11.11 0.20 0.06 15 Rubiaceae Genipa americana L. 54.54 23.40 47.96 1 26.83 28.20 31.22 1 5.26 43.51 15.28 2 44.44 47.19 59.44 1

Sapotaceae Pouteria sp. 18.18 31.37 21.43 2 34.15 7.33 10.33 4 — — — — 44.44 11.59 14.59 2 Morphotype 1 9.09 0.51 0.18 12 2.44 0.07 ,0.01 30 — — — — — — — — Morphotype 2 — — — — 4.88 3.14 0.63 14 — — — — — — — — Morphotype 3 — — — — 4.88 0.27 0.05 21 — — — — — — — — Morphotype 4 — — — — 4.88 0.15 0.03 23 — — — — 8.33 0.79 0.19 12 Morphotype 5 — — — — 2.44 0.10 0.01 28 — — — — — — — — Morphotype 6 — — — — 2.44 0.33 0.03 22 — — — — — — — — Morphotype 7 — — — — 9.76 0.20 0.08 20 — — — — — — — — Morphotype 8 — — — — 7.32 0.53 0.16 19 — — — — — — — — Morphotype 9 — — — — — — — — — — — — 2.78 0.11 0.01 17 Fruits and seeds ni 27.27 1.18 1.21 9 21.95 2.14 1.94 10 — — — — 16.67 4.47 2.11 6 LEAVES Fabaceae — — — — 14.63 0.39 0.24 16 — — — — 11.11 0.58 0.18 13 cf. Myrtaceae — — — — 2.44 0.03 ,0.01 33 — — — — — — — — Eudicotyledone — — — — 29.27 0.71 0.86 13 — — — — 27.78 5.95 4.68 4 Monocotyledone — — — — 4.88 0.04 0.01 29 5.26 0.69 0.24 9 2.78 0.01 ,0.01 25 Leaves ni 9.09 0.13 0.04 16 36.58 1.57 2.37 9 5.26 0.02 0.01 12 47.22 5.54 7.41 3 SHOOTS AND STEMS Cyperaceae — — — — 2.44 0.01 ,0.01 39 — — — — — — — — Shoots and stems ni 54.54 2.01 4.11 6 56.10 3.60 8.33 5 10.53 2.75 1.93 5 58.33 2.53 4.17 5 FLOWERS — — — — 9.76 0.06 0.02 24 — — — — 2.78 0.06 ,0.01 18 ROOTS — — — — 2.44 0.03 ,0.01 33 — — — — — — — — MISC 18.18 5.91 4.04 7 19.51 7.57 6.09 6 5.26 3.32 1.17 6 16.67 3.60 1.70 8 UNIDENT. PLANT — — — — 24.39 1.03 1.03 12 5.26 0.23 0.08 11 16.67 1.70 0.80 11 MATERIAL Cunha et al.—Amazon turtle diet 115

Appendix 1. Continued. P. erythrocephala P. expansa P. sextuberculata P. unifilis

FO V IRI r FO V IRI r FO V IRI r FO V IRI r

VERTEBRATES Perciformes Cichlidae — — — — 2.44 0.01 ,0.01 39 — — — — 2.78 0.02 ,0.01 24 Crenicichla sp. — — — — 2.44 0.16 0.02 27 — — — — — — — — Perciformes ni — — — — 2.44 0.07 0.01 30 — — — — — — — — Siluriformes Pimelodidae — — — — 2.44 0.03 ,0.01 33 — — — — — — — — Siluriformes ni — — — — 2.44 ,0.01 ,0.01 44 — — — — — — — — Fishes ni 9.09 1.29 0.44 10 — — — — — — — — 5.56 0.02 ,0.01 22 Reptiles 18.18 0.08 0.05 15 2.44 ,0.01 ,0.01 44 — — — — — — — — Testudines — — — — — — — — — — — — 2.78 0.06 ,0.01 18 INVERTEBRATES Insects Coleoptera 9.09 1.29 0.44 10 4.88 0.02 ,0.01 36 — — — — — — — — Ephemeroptera — — — — 2.44 ,0.01 ,0.01 44 — — — — — — — — Hemiptera — — — — 2.44 ,0.01 ,0.01 44 — — — — — — — — Odonata — — — — 2.44 ,0.01 ,0.01 44 — — — — — — — — Orthoptera — — — — 2.44 0.07 0.01 30 — — — — — — — — Hymenoptera — — — — 2.44 0.01 ,0.01 39 — — — — — — — — Hymenoptera/Formicidae — — — — 4.88 ,0.01 ,0.01 39 5.26 0.02 0.01 12 — — — — Insecta ni — — — — 9.76 0.05 0.02 25 5.26 0.02 0.01 12 2.78 0.03 ,0.01 23 Decapoda Decapoda shrimp 9.09 0.21 0.07 14 2.44 ,0.01 ,0.01 44 5.26 1.33 0.47 8 — — — — Decapoda crab 9.09 0.26 0.09 13 — — — — — — — — — — — — Decapoda ni — — — — — — — — — — — — 2.78 0.01 ,0.01 26

Arachnida — — — — 2.44 0.02 ,0.01 37 — — — — — — — — Porifera — — — — 2.44 0.01 ,0.01 39 — — — — — — — — SEDIMENT — — — — 2.44 0.02 ,0.01 37 — — — — 2.78 0.06 ,0.01 18 UNIDENTIFIED Morphotype 10 9.09 0.05 0.02 18 7.32 0.06 0.02 26 31.58 1.35 2.85 4 2.78 0.0 ,0.01 21 UNIDENTIFIED 9.09 0.05 0.02 18 17.07 0.71 0.50 15 5.26 0.46 0.16 10 16.67 0.26 0.12 14