Trophic Dynamics of Three Sympatric Anuran Species in a Soybean Agroecosystem from Santa Fe Province, Argentina
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HERPETOLOGICAL JOURNAL 20: 261–269, 2010 Trophic dynamics of three sympatric anuran species in a soybean agroecosystem from Santa Fe Province, Argentina Paola M. Peltzer1, Andrés M. Attademo1,2, Rafael C. Lajmanovich1, Celina M. Junges1, Adolfo H. Beltzer2,3 & Laura C. Sanchez4 1Cátedra de Ecotoxicología, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral-CONICET, Argentina 2Facultad de Ciencia y Tecnología, Universidad Autónoma de Entre Ríos (UADER), Argentina 3Instituto Nacional de Limnología (INALI-CONICET), Argentina 4Centro de Investigación Científica y Transferencia de Tecnología a la Producción (CICYTTP-CONICET), Materi y España, Argentina The conversion of forests to agroecosystems presents a challenge for biodiversity conservation. In this study, the feeding habits of three species of anurans (Rhinella fernandezae, Odontophrynus americanus and Physalaemus albonotatus) were compared between a soybean field and a native forest in Santa Fe Province, Argentina. Our dietary assessment is based on 124 individuals (47 R. fernandezae, 45 O. americanus and 32 P. albonotatus). Lepidopteran larvae were the predominant item in anuran diets from the soybean field, whereas collembola, isopods and snails prevailed in the diets from forests. Generally, the three anuran species shifted their diets as prey differs in the two environments, but R. fernandezae and P. albonotatus maintained a preference for a few prey types. Mean niche overlap in the soybean field was smaller than expected by chance, suggesting that the three anuran species are competing for limited resources. Trophic studies on other native anurans in agroecosystems should be a priority in conservation efforts due to their potential use as natural control agents, as well as for assessing the consequences of the broad conversion of natural forest to agricultural use in our region and throughout the world. Key words: diet, agriculture, trophic niche, Rhinella fernandezae, Odontophrynus americanus, Physalaemus albonotatus INTRODUCTION Rhinella fernandezae (Bufonidae), Odontophry- nus americanus (Cycloramphidae) and Physalaemus iets of amphibian species depend on intrinsic and albonotatus (Leiuperidae) are widespread anurans in Dextrinsic factors, such as morphological constraints north-eastern and central Argentina (Frost, 2009), where related to life-history stage, size, specialization, foraging they are frequently found in natural habitats (grasslands, mode, diet plasticity, presence or absence of competitors flooded areas, savannahs, ponds) as well as in human- and changes in resource availability due to human-medi- modified environments. Despite their well-known life ated habitat alterations (Anderson et al., 1999; Kupfer et histories (Aquino et al., 2004a,b; Narváes et al., 2004; al., 2005; Lima et al., 2010). Although numerous studies Sanchez & Busch, 2008), few studies have been con- on diet composition and feeding strategies have been con- ducted on their feeding ecology in different environments ducted in native forests and areas with few anthropogenic (Lajmanovich et al., 2003; Attademo et al., 2005, 2007b). activities (Peltzer & Lajmanovich, 1999; Duré & Kehr, This study examines the feeding habits of sympatric 2004; Araújo et al., 2007; Crawford et al., 2009; Dietl et populations occurring in a soybean field and a natural al., 2009), only a few have focused on agroecosystems forest, with emphasis on prey consumption, prey impor- (Hirai & Matsui, 1999; 2000; Attademo et al., 2005). In tance categories and trophic interactions between species. view of the gradual advance of agricultural land, a major We discuss the importance of trophic strategies and prey challenge is to understand the ecological mechanisms by composition in determining the influence of human-al- which a large number of species coexist and how resourc- tered environments such as agroecosystems on anuran es are shared. Although trophic segregation is one of the communities, highlighting the potential use of amphib- main mechanisms structuring anuran assemblages (e.g. ians as potential biological control agents. Basso, 1990; López et al., 2005), trophic niches might in- teract with other aspects such as structural heterogeneity MATERIALS AND METHODS (Suazo-Ortuño et al., 2007). In Argentina, modern agriculture has led to the ex- Study area pansion of cultivated areas, thus exerting an increasing The study area is located in mid-eastern Argentina (Fig. pressure on natural habitats (Paruelo et al., 2005; Peltzer 1), a part of the Espinal ecoregion (Burkart et al., 1999). et al., 2006). In agroecosystems, native anurans may play Mean annual rainfall is 800 mm and mean annual tem- an important role in controlling insect pests while avoid- perature is 18 ºC. The area is dominated by large areas of ing the negative side-effects of pesticides (Attademo et intensively managed agricultural land (cultivated mainly al., 2005; 2007a,b). with soybean and rice, followed by maize, sorghum and Correspondence: P.M. Peltzer, Ciudad Universitaria (FBCB-UNL), Pje. El Pozo, s/n. 3000, Santa Fe, Argentina. E-mail: [email protected] 261 P.M. Peltzer et al. Diet analysis Individuals containing at least one prey item were in- cluded in the overall analysis. Food items were identified to the most detailed taxonomic level possible using a binocular microscope; the number of items per digestive tract was also recorded. We measured each prey item’s maximum length (L) and width (W) using digital cali- pers to the nearest 0.01 mm. For partially digested prey, we estimated length by measuring width and then using predetermined length–width regressions from intact prey (Hirai & Matsui, 2001). Intra-environment diet analysis For each taxon, we calculated the frequency of occur- rence (FO%) and numeric percentage (N%) in accordance with the methodology of Lescure (1971). Volumes (V) of each prey item were estimated using the formula for an ellipsoid (Dunham, 1983). These three parameters were considered in determining the prey importance index pro- posed by Biavati et al. (2004) of each prey category in the Fig. 1. Location of sampling sites in mid-eastern diet of each species in each environment. Argentina: soybean field (A) and native forest (B). Trophic diversity. Trophic diversity was calculated using Hurlbert’s PIE (probability of interspecific encounter) in- dex (Hurlbert, 1971). The index ranges from zero to one and represents the probability that two randomly select- ed individual prey will be of different taxa (Olzewiski, 2004). We calculated the PIE index for each species in each environment using 1000 random permutations in the EcoSim program (Gotelli & Entsminger, 2007). We standardized the number of individuals as the lowest prey wheat), and interspersed with remnant wetlands and flu- abundance in the anuran species recorded. Niche breadth vial forests (Arturi, 2006; Peltzer et al., 2006). was calculated using the index of Levins (1968). The in- Landsat 7 (+ ETM) satellite imagery provided by the dividual estimations of prey were summed at random, Comisión Nacional de Actividades Espaciales (30 × 30 giving the accumulated trophic diversity (hk) (Hurtubia, m pixel resolution) was used for visual selection of the 1973), a value that was used to determine the minimum sites – a soybean field (100 ha) and a native forest (40 ha, sample of digestive tracts required to evaluate sample 5 km away from any agroecosystem) – based on, first, the representatives (e.g. Peltzer & Lajmanovich, 2002; López presence of at least one pond with water during the study et al., 2005). One way analysis of variance (ANOVA) fol- period, and second, the lack of a significant altitudinal lowed by Tukey–Kramer post hoc multiple tests was used gradient. Surveys were conducted during the period of to determine interspecific differences in prey size. soybean growth (December 2005 – March 2006). Feeding overlap. We calculated dietary overlaps using Sampling Pianka’s index (Pianka, 1973). Overlap values of 1.0 Adult R. fernandezae (RF: Anura, Bufonidae), O. indicate identical diets or food volume, whereas over- americanus (OA: Anura, Cycloramphidae) and P. al- lap values of 0 indicate total dissimilarity in food items. bonotatus (PA: Anura, Leiuperidae) were collected Overlap values were arbitrarily set at the following levels: from soybean (30º20'53"S; 59º58'34"W) and forest high (>0.7), intermediate (0.4–0.7) or low (<0.4). (30º18'43"S; 59º59'42"W) sites following the methodol- ogy of Greenberg et al. (1994). All specimens captured Prey importance and predator–prey association. To deter- were euthanased and fixed according to ASIH et al. (2001) mine the importance of each prey category in the pooled protocols. We obtained gastrointestinal contents using a gastrointestinal tracts of each species in each environ- stereomicroscope for preservation in 70% ethanol and ment, we applied the formula of Biavati et al. (2004): deposition in the entomological collection of the Facultad I=(FO%+N%+V%)/3 de Bioquímica y Ciencias Biológicas of the Universidad Nacional del Litoral, Argentina. We recorded snout–vent where F% is the occurrence percentage, N% is the nu- length (SVL) of each anuran to the nearest 0.1 mm. A con- meric percentage and V% is the volumetric percentage. dition factor (CF), expressed as 100 × [body weight (g)]/ To obtain a multidimensional representation of the [length (cm)]3 was calculated (Bagenal & Tesch, 1978). predator–prey associations in soybean and forest sites a A t-test was used to compare CF