Trophic Ecology of Physalaemus ephippifer (Anura, Leptodactylidae) in Eastern Amazonia

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1 Trophic Ecology of Physalaemus ephippifer (Anura, Leptodactylidae) in Eastern Amazonia Author(s): Lenise Chagas Rodrigues and Maria Cristina dos Santos-Costa Source: Journal of Herpetology, 48(4): Published By: The Society for the Study of Amphibians and Reptiles DOI: URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 Journal of Herpetology, Vol. 48, No. 4, , 2014 Copyright 2014 Society for the Study of Amphibians and Reptiles Trophic Ecology of Physalaemus ephippifer (Anura, Leptodactylidae) in Eastern Amazonia LENISE CHAGAS RODRIGUES 1,3 AND MARIA CRISTINA DOS SANTOS-COSTA 2 1 Programa de Pós-Graduação em Zoologia, Universidade Federal do Pará and Museu Paraense Emílio Goeldi, Belém, Pará, Brazil 2 Laboratório de Ecologia e Zoologia de Vertebrados, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém, Pará, Brazil ABSTRACT. One of the main aspects of natural history is trophic ecology, which affects survival and population size. In the present study, we registered the contribution of prey types to the diet of Physalaemus ephippifer and tested for differences in diet according to sex and season (rainy and dry) of three populations of P. ephippifer in eastern Amazonia. We analyzed frequency of occurrence, trophic amplitude, feeding overlap, and food importance index for each prey category. We analyzed 102 specimens (69 males and 33 females) and observed that the most important prey categories were termites and ants. The most important prey category for females during rainy season included coleopteran larvae, whereas during dry season the most important prey category was termites. In both seasons, the most important prey category for males was ants. We did not observe any seasonal or sexual variation in the diet of P. ephippifer. On the other hand, during the rainy season, coleopteran larvae and termites were the most important prey categories for females, which have a more nutritious diet than males. Increase in nutritional value of the diet of females coincided with the reproductive period, when females would require a greater amount of energy for gamete production. Spatial, temporal, and trophic dimensions, which allow us to infer foraging behavior and habitat use, are considered the most important ecological attributes of species (Pianka, 1973; Davic, 1991; Donnelly, 1991). Thus trophic ecology may be considered one of the main aspects of natural history and a factor that regulates population size (Duellman and Trueb, 1994; Vitt and Caldwell, 2009). As populations grow, there is increase in competition for trophic resources, and as a consequence some species use their habitat differentially (spatially or temporally), thereby reducing competition (Lima and Magnusson, 1998; Caldwell and Vitt, 1999). Such variation in habitat use is important, as it promotes resource partitioning and reduces diet overlap, thus allowing species and conspecifics to coexist (Duellman and Trueb, 1994; Gordon, 2000; Vitt and Caldwell, 2009; Khanaposhtani et al., 2012). Anurans are considered opportunistic and generalist predators and also key species in trophic chains, acting as both predators and prey. Diet of anurans includes mainly insects, especially Formicidae, Isoptera, and Coleoptera (Parmelee, 1999; Santana and Juncá, 2007; Sugai et al., 2012). When anurans eat insects, they also ingest their exoskeletons, which are difficult to digest. However, digestion of exoskeletons may be facilitated through ingestion of minerals and plant material, allowing greater absorption of nutrients from the prey (Anderson et al., 1999; Santos et al., 2004). The wide range of prey in the diet of anurans is a result of foraging strategies, influenced by morphological, physiological, and behavioral features of a given species (Duellman and Trueb, 1994) and availability and quality of prey in the habitat (Toft, 1980; Galatti, 1992; Santana and Juncá, 2007). Also, environmental conditions (e.g., climatic seasonality) and availability may lead to changes in the diet of anurans. For example, in a study conducted in western Amazonia, Toft (1980) observed that leaf-litter anurans eat smaller prey items during the dry season; larger prey are eaten during the rainy season. Similar results were observed in northeastern Brazil, where Santos et al. (2004) observed an increase in the number of prey items consumed by Hypsiboas albomarginata (Hylidae) and Physalaemus cuvieri (Leptodactylidae) during the wet season. 3 Corresponding Author. lenise.rodrigues@yahoo.com.br DOI: / Anurans of the Leptodactylidae family usually forage in leaf litter (Vitt and Caldwell, 2009). According to Toft (1981), leaflitter anurans may be divided into two groups according to their foraging strategy: 1) active foragers, which feed on small and abundant prey; 2) sit-and-wait foragers, which feed on lessabundant but larger prey. So, foraging behavior of anurans may be inferred from prey items observed in their diet. For example, if a species feeds mainly on Formicidae and Isoptera (small and abundant prey), one may infer that the species is an active forager (Toft, 1981; Santana and Juncá, 2007). Forty-five species of the genus Physalaemus (Leptodactylidae) are distributed in South America, from southern Venezuela to central Argentina. However, only two species occur in Brazilian Amazonia (Frost, 2013). One of them is Physalaemus ephippifer, which is a diurnal and nocturnal small leaf-litter anuran, distributed from the mouth of the Amazon River (Brazil) through the Guianas to Venezuela (Frost, 2013). Reproduction occurs during the rainy season, both in open and forested areas, and eggs are laid in foam nests on temporary ponds (Hödl, 1990a,b; Vitt and Caldwell, 2009). Despite the knowledge on some aspects of the natural history of P. ephippifer (i.e., reproduction, habitat use), trophic ecology of this species is unknown. Studies focusing on trophic ecology may provide valuable information for the understanding of population dynamics of this species. Therefore, we conducted this study to answer the following questions: 1) What is the contribution of different prey types to the diet of P. ephippifer? 2) Do individuals feed differently according to sex and season? MATERIAL AND METHODS Study Area. We analyzed specimens collected from three localities in Brazilian Amazonia: Belém, Santa Bárbara do Pará, and Tailandia. ˆ Individuals from Belém were collected at the Utinga Ecological Park (UEP), a 1,340-ha protected area covered mainly by dense terra-firme rain forest. In UEP there are also pastures, roads, and buildings between two lakes, Bolonha Lake and Agua Preta Lake (SEMA, 2013). Specimens from Santa Bárbara were collected in Gunma Ecological Park (GEP), a forest area of 540 ha mainly covered by dense terra-firme rain forest, with canopy trees of over 25 m in height and an understory dominated by palms. In GEP, there are also areas of floodplain and secondary forest. In Tailândia, specimens were collected in

3 DIET OF PHYSALAEMUS EPHIPPIFER 533 FIG. 1. Map of northeast Pará, Brazil showing the localities where specimens of Physalaemus ephippifer were collected: Belém (B), Santa Bárbara do Pará (SB) and Tailândia. the property of the AGROPALMA Company. The property is covered by dense terra-firme rain forest (64,000 ha) and oil-palm plantations of the species Elaeis guianensis (39,000 ha). Belém, Santa Bárbara do Pará, and Tailandia ˆ are located in the northeast of the Brazilian state of Pará (Fig. 1). Local climate is humid equatorial, with a marked rainy season between December and May (mean rainfall mm) and a period of reduced precipitation between June and November (mean rainfall mm) (Albuquerque et al., 2010). Mean annual temperature is approximately 278C; the average relative humidity oscillates around 90% (CPTEC/INPE, 2013). Data Collection. Collected specimens were sacrificed through overdose of Xylocaine, fixed in 10% formalin, and then preserved in 70% alcohol. We made a ventral incision and removed the digestive tracts (stomachs and intestines). Contents in digestive tracts were removed, identified to the lowest taxonomic level with help of experts, dried and weighed on an analytical balance (Shimadzut), and stored in 92% alcohol. Some individuals analyzed from Belém and Santa Bárbara do Pará belong to the herpetological collection of Museu Paraense Emílio Goeldi. Data Analysis. Diet of P. ephippifer was characterized by frequency of occurrence, trophic amplitude, feeding overlap, and food importance index. Minerals and plant material were not considered as food items, so they were excluded from our analysis. To observe which items were part of the diet of P. ephippifer, we calculated frequency of occurrence of each prey (FO i ) (Hynes, 1950). Frequency of occurrence is calculated as the number of occurrences of each prey type divided by the number of digestive tracts containing any food item, obtained by the following formula: FO i = f i N 100 where i is the resource category; f i is the number of digestive tracts containing prey i; andn is the total number of digestive tracts analyzed. We calculated trophic amplitude (B a ) according to Levin s standardized index (Krebs, 1999). This index ranges from 0, when a species feeds only on one prey type (specialist predators), to 1, when a species feeds similarly on different prey types (generalist predators). We calculated trophic amplitude of P. ephippifer according to season (rainy and dry) and sex (males and females). To obtain trophic amplitude we used the following formula: 1 P - 1 p 2 B a = i n - 1 where i is the resource category; p i is the proportion of individuals that fed on prey i; and n is the number of resource categories used by the species. To quantify resource partitioning between sexes in different seasons, we calculated feeding overlap (O) (Pianka, 1973). High values of O indicate high feeding overlap, whereas low values of O indicate low feeding overlap. We calculated feeding overlap between males and females of P. ephippifer and between seasons (rainy and dry). To obtain feeding overlap, we used the following formula: X n i O jk = O kj = p ijp ik qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi Xn i p X n ij 2 i p ik 2 where i is the resource category; j and k are the sexes (male and female) or the seasons (rainy and dry); p ik is the proportion of prey type i in the diet of k; and p ij is the proportion of prey type in the diet of j. Thereafter we tested the significance of P values performing Monte Carlo randomization test with 1,000 permu-

4 534 L. C. RODRIGUES AND M. C. SANTOS-COSTA TABLE 1. Frequency of occurrence (FO i ) of plant material and minerals in the digestive tracts of males and females of Physalaemus ephippifer in eastern Amazonia. Males Females Total n FO i (%) n FO i (%) n Plant material and minerals Plant material Minerals tations using EcoSim 7 software. Two random matrices were generated (one for data on males and females, and one for data on rainy and dry seasons) and then compared with the real data matrices. For each prey type we calculated the food importance index (FI i ) (adapted from Kawakami and Vazzoler, 1980) and verified which food item was the most important to the diet of P. ephippifer according to sex and season. We obtained FI values for each food category for females collected during the rainy season (FR), females collected during the dry season (FD), males collected during the rainy season (MR), and males collected during the dry season (MD). Food importance index was TABLE 2. Frequency of occurrence, weight, and food importance index of prey items in the digestive tracts of individuals from three populations of Physalaemus ephippifer in eastern Amazonia (n: total number of individuals that fed on prey i; FO i : frequency of occurrence of prey i; W: total weight of prey i; FI i : food importance index of prey i). n FO i (%) W (g) FI i Arachnida Acari Araneae Crustacea Isopoda Myriapoda Chilopoda Diplopoda Insecta Blattaria Coleoptera (imago) Coleoptera (larvae) Chrysomelidae (pupa) Collembola Diptera (imago) Diptera (larvae) Hemiptera (imago) Hemiptera (nymph) Homoptera Hymenoptera (non Formicidae) Formicidae Isoptera (imago) Isoptera (nymph) Lepidoptera (larvae) Odonata (imago) Odonata (larvae) Orthoptera Mollusca Pulmonata Others Egg (not identified) TABLE 3. Food importance index of the most important prey categories in the diet of three populations of Physalaemus ephippifer in eastern Amazonia (FR: females from the rainy season; FD: females from the dry season; MR: males from the rainy season; MD: males from the dry season). obtained by the following formula: FR FD MR MD Arachnida Acari Araneae Crustacea Isopoda Myriapoda Chilopoda Diplopoda Insecta Blattaria Coleoptera (imago) Coleoptera (larvae) Chrysomelidae (pupa) Collembola Diptera (imago) Diptera (larvae) Hemiptera (imago) Hemiptera (nymph) Homoptera Hymenoptera (non Formicidae) Formicidae Isoptera (imago) Isoptera (nymph) Lepidoptera (larvae) Odonata (imago) Odonata (larvae) Orthoptera Mollusca Pulmonata Others Egg (not identified) FI i = %FO i %P X%FO i %P 100 where i is the food category; %FO i is the frequency of occurrence of prey i; and %P is the frequency of weight of prey i. We used square-root transformation on FI data and built a similarity matrix based on Bray Curtis coefficients. Thereafter we performed a one-way analysis of similarities with 95% significance level between indices grouped into classes according to sex and season. After that we performed a metric multidimensional scaling analysis to observe variations in the diet of P. ephippifer. Analyses of the FI i were performed using Primer 6 software. RESULTS We analyzed 102 specimens of P. ephippifer (69 males, 33 females) and recorded 25 prey categories in digestive tracts. Approximately 18% (15 males, 4 females) of the digestive tracts were empty or contained only minerals or plant materials (or both), and so they were excluded from our analysis of the FI i. Minerals and plant material were frequent in the stomachs of P. ephippifer (81.5%; 83 specimens) (Table 1).

5 DIET OF PHYSALAEMUS EPHIPPIFER 535 FIG. 2. Metric multidimensional scaling (MDS) showing a group of males that have high diet similarity. Empty circles = females; full circles = males. Stress = 0. Broken line indicates diet similarity of Physalaemus ephippifer in 82% of prey categories consumed. FR: females from rainy season; FD: females from dry season; MR: males from rainy season; MD: males from dry season. Isoptera and Formicidae were the most frequent prey categories in the diet of P. ephippifer (Table 2). Males ate mainly Formicidae during both seasons (rainy and dry). In addition, during the rainy season the second and third most important items in the diet of males were Isoptera and Araneae, whereas during the dry season these were Araneae and Isoptera (Table 3). During the rainy season, females ate mainly Coleoptera larvae, followed by Formicidae and Isoptera. On the other hand, during the dry season females ate mainly, in decreasing order, Isoptera, Formicidae, and Orthoptera (Table 3). Trophic amplitude of P. ephippifer was 0.19, revealing diet specialization of the species. When we analyzed separately seasons and sexes, we also observed diet specialization. During the rainy season, trophic amplitude was 0.26 and during the dry season it was In addition, females (B a = 0.15) exhibited a more specialized diet than males (B a = 0.27). Feeding overlap between sexes was high (O = 0.94), as well as among individuals during rainy and dry seasons (O = 0.97). Data randomizations differed significantly between observed and expected values of male and female data (P [observed < expected] = and P [observed > expected] = 0.000). Similarly, data randomizations between observed and expected values of rainy and dry seasons differed significantly (P [observed < expected] = and P [observed > expected] = 0.000). According to FI analysis, diet of P. ephippifer did not differ between sexes (R = 1; P = 0.33) or between seasons (R =-0.75; P = 1). However, although no statistical significance was observed, we observed a group of males that had higher diet similarity (Fig. 2). DISCUSSION Diet of P. ephippifer includes a variety of arthropods, which indicates a generalist diet. However, some prey types (e.g., ants, termites) were more important for both males and females during rainy and dry seasons. Similar results were reported for Physalaemus cf. cicada (Santana and Juncá, 2007) and P. cuvieri (Santos et al., 2004). In both studies, the authors observed that Isoptera and Formicidae were the most important items in diet. On the other hand, in the case of P. ephippifer, two other prey categories were found frequently in digestive tracts: adult coleopterans and spiders. When we analyzed sexes and seasons separately, we found variation in the general pattern of P. ephippifer diet. Diet of males included mainly ants and termites, but also spiders as a secondary prey type, especially during the dry season. The high consumption of ants and termites by all individuals may be related to the wide availability of those resources in the sampled areas, facilitating consumption of such abundant prey (Davidson et al., 2003). In the case of females, we observed high consumption of termites, but also ants and orthopterans as secondary prey types during the dry season. However, during the rainy season, females consumed mainly prey with high nutritional value (i.e., coleopteran larvae and termites) (Redford and Dorea, 1984; Marconi et al., 2002). Female anurans need to store a larger proportion of fat, which is used as an energy source for gamete production during the reproductive period (Duellman and Trueb, 1994; Biavati et al., 2004; Forti et al. 2011) that occurs during the rainy season for most species in Amazonia, including P. ephippifer (Hödl, 1990a,b). As a general pattern, anurans that are active foragers feed on many small abundant prey types, whereas sit-and-wait foragers feed on few, larger, and less-abundant prey (Toft, 1980; Duellman and Trueb, 1994). According to this theory, then, P. ephippifer may be considered an active and opportunistic predator, catching small and abundant prey, but also catching larger and less-abundant prey. The diet of P. ephippifer varied according to intrinsic (e.g., morphology, physiology, and behavior) or extrinsic factors (e.g., changes in habitat use, prey availability) (Toft, 1980; Duellman and Trueb, 1994). During the dry season in the Amazon, the mass of invertebrates decreases (Toft, 1980), and as a consequence availability of this resource also decreases, which can be observed in the diet of anurans. As invertebrates are less abundant during the dry season, anurans feed on a wider range of prey to supply their nutritional needs (Toft, 1980). On the other hand, the opposite occurs during the rainy season when invertebrates are more abundant, allowing anurans to forage on specific prey types (Toft, 1980), as we observed with trophic amplitude values for P. ephippifer. Despite differences in contribution of prey types to diet and different needs between sexes, we found low trophic amplitude and high feeding overlap between sexes during both rainy and dry seasons. High feeding overlap should lead to increased competition for food, as most items are consumed by all individuals (Gordon, 2000). However, prey abundance and changes in habitat use reduce the risk of inter- and intraspecific competition for food (Toft, 1980; Kuzmin, 1995; Cajade et al., 2010; Sabagh et al., 2012), in addition to the fact that some invertebrates (e.g., ants) are abundant in tropical forests (Davidson et al., 2003). The specialized diet of P. ephippifer explains the lack of significant variation in the diet of males and females in different seasons. Trophic niche partitioning avoids possible intraspecific competition for food, as observed by Forti et al. (2011). In their study, they observed that males of Ameerega braccata eat mainly ants, whereas females eat mainly termites. On the other hand, species that have a highly specialized diet do not exhibit such variation throughout the year or among sexes, as observed in Ameerega flavopicta (Biavati et al., 2004). Ingestion of plant material is considered accidental in some cases, especially when its frequency of occurrence is very low (Klaion et al., 2011). However, in the case of P. ephippifer, ingestion of mineral and plant material may not be accidental as

6 536 L. C. RODRIGUES AND M. C. SANTOS-COSTA their frequency of occurrence was high. Some studies suggest that ingestion of minerals may facilitate the digestion of invertebrate exoskeletons (Anderson et al., 1999; Santos et al., 2004). On the other hand, ingestion of high proportions of plant material may indicate folivory or frugivory (Das, 1996; Silva and Britto-Pereira, 2006), helping individuals to eliminate gastrointestinal parasites and/or being a source of other nutrients (if digested) and water, thus avoiding water loss (Anderson et al., 1999). We conclude that P. ephippifer is an opportunist forager, and a specialist predator of ants and termites, but also ingests spiders and coleopteran adults and larvae. The consumption of coleopteran larvae and termites is higher among females, coinciding with their reproductive period. Acknowledgments. We are grateful to CNPq for financial support; IBAMA-ICMBIO for permission to collect specimens through license 12420; A. 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Journal of Herpetology 15: VITT, L. J., AND J. P. CALDWELL Herpetology: An Introductory Biology of Amphibians and Reptiles. Academic Press, USA. Accepted: 26 January APPENDIX 1 Accession Numbers of Herpetological Collection of Museu Paraense Emílio Goeldi. Physalaemus ephippifer MPEG 859; MPEG 862; MPEG 865; MPEG 866; MPEG 870; MPEG 878; MPEG 880; MPEG 881; MPEG 882; MPEG 883; MPEG 885; MPEG 886; MPEG 1439; MPEG 1441; MPEG 1442; MPEG 1460; MPEG 3133; MPEG 6125; MPEG 6126; MPEG 6127; MPEG 6128; MPEG 16026; MPEG 19354; MPEG 19359; MPEG 19378; MPEG 19381; MPEG 19388; MPEG 19395; MPEG 19403; MPEG 19404; MPEG 19673; MPEG 19674; MPEG 19682; MPEG 19705; MPEG 29276; MPEG 29277; MPEG 29278; MPEG 29279; MPEG 29280; MPEG 29289; MPEG 29290; MPEG 29293; MPEG 29294; MPEG 29299; MPEG 29300; MPEG 29301; MPEG 29302; MPEG 29303; MPEG 29305; MPEG 29307; MPEG 29309; MPEG 29310; MPEG 29311; MPEG