Diet of Leptodactylus ocellatus
Transcripción
Diet of Leptodactylus ocellatus
Herpetology Notes, volume 2: 9-15 (2009) (published online on 16 February 2009) Diet of Leptodactylus ocellatus (Anura: Leptodactylidae) from a cacao plantation in southern Bahia, Brazil Mirco Solé1*, Iuri R. Dias1, Erika A. S. Rodrigues1, Euvaldo Marciano-Jr1, Samuel M. J. Branco1, Kaoli P. Cavalcante1 and Dennis Rödder2,3 Abstract. We studied the diet of Leptodactylus ocellatus in a cacao plantation in southern Bahia state, Brazil and compared our results with data available from populations inhabiting natural and human modified habitats. Stomachs of 117 specimens were flushed whereby 77 stomachs revealed at least one prey item. Our results indicate that L. ocellatus consumes a great variety of food items at the study site, whereby Lepidoptera larvae, Coleoptera and Araneae dominated its diet. The presence of vertebrates including Teleostei and Anura in the diet revealed in previous studies was confirmed, although these items made up only minor parts of the diet. The index of relative importance showed that the diet of L. ocellatus was dominated by Lepidoptera larvae, followed by Coleoptera and Araneae. The Levins index observed in our samples was 8.51 and the standardized Shannon-Weaver index was 0.56. Apparently, the structure of the trophic niche of L. ocellatus is not affected by habitat alteration. The present study provides evidence for the opportunistic feeding behaviour and broad trophic niche breadth of L. ocellatus. Keywords. Amphibia, diet, trophic niche, cacao plantation, predation. Introduction Trophic interactions are a crucial component of life history strategies and contribute to the population regulation (Duellman and Trueb, 1994; Wells, 2007). In the Neotropics, habitat loss is still the primary threat to amphibian populations (Young et al., 2001; Stuart et al., 2004). Other indirect effects associated to landscape fragmentation may cause alteration of trophic interactions, due to changes in microclimate, causing abundance variations in available prey items, what might contribute to the decline of amphibians (Carey et al., 2001; Young et al., 2001). A profound knowledge about trophic relationships in tropical communities is essential for the development of successful conservation strategies. An assessment of possible shifts in trophic niches of species inhabiting natural and human altered habitats is currently lacking for the vast majority of anuran taxa. The family Leptodactylidae is distributed from the extreme southern USA throughout tropical Mexico, Central America and South America (Frost et al., 2006), 1 Department of Biological Sciences, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna, km 16, 45662-000 Ilhéus, Bahia, Brazil; e-mail: [email protected] 2 Zoological Research Museum Alexander Koenig, Department of Herpetology, Adenauerallee 160, 53113 Bonn, Germany 3 Trier University, Department of Biogeography, 54286 Trier, Germany * corresponding author whereby the genus Leptodactylus currently comprises 76 species mainly distributed in South America (Frost, 2008). Compared to other members of the genus, Leptodactylus ocellatus (Fig. 1) is a large nocturnal frog, which is widely distributed throughout South America east of the Andes (Cei, 1980). The species inhabits all varieties of ponds, rivers and even lakes and can often be found in strongly anthropogenized areas. Heyer, Caramaschi and de Sá (2006) recently designated a neotype for this species and stated that there are both reproductive and molecular differences that suggest the presence of more than one species under the name L. ocellatus. Regarding L. ocellatus, previous studies have mainly dealt with growth, reproductive (Vaz-Ferreira and Gehrau, 1975), behavioral aspects (Strüssmann et al., 1984), food habits of tadpoles (Lajmanovich, 1994) and juveniles (Lajmanovich, 1996). The diet of L. ocellatus has been studied in several Neotropical countries (Strüssmann et al., 1984; Teixeira and Vrcibradic, 2003; França, Facure and Giaretta, 2004; Maneyro et al., 2004; Sanabria, Quiroga and Acosta, 2005) and in several populations the species has been found to be a potential predator of amphibians (Teixeira and Vrcibradic, 2003; França, Facure and Giaretta, 2004; Sanabria, Quiroga and Acosta, 2005). Our study provides data on the diet of L. ocellatus from a cacao plantation in southern Bahia. We report some prey categories that have not been previously identified as part of the frog’s diet and we discuss our data with 10 available data from both natural and human modified habitats in Uruguay, Peru, the Brazilian Pantanal and the Brazilian states of Espírito Santo, Minas Gerais and Rio Grande do Sul. Material and methods Sampling Frogs were collected manually from December 2006 to April 2007 at night (from 20:00 to 22:00) near a temporary pond (Fig. 2A) and a small stream (Fig. 2B) in a cocoa plantation (5 ha), which is located behind the campus of the Universidade Estadual de Santa Cruz (14°47’45’’S, 39°10’20’’W), municipality of Ilhéus, southern Bahia, Brazil. In the cacao plantations of southern Bahia the shelter of trees of the original Atlantic rainforest vegetation is used to shade the cacao trees. This shading allows the plantation to conserve similar humidity indexes as the less impacted Atlantic forest patches. Faria et al. (2007) found these plantations to harbor over 81% of the amphibian diversity found in not anthropogenized forests. Frogs were captured and transferred to the nearby laboratory. Snout-vent length (SVL; to nearest 0.1 mm) and mouth width (MW) were measured using a digital caliper. Body mass (BM; to nearest 0.1g) was recorded using a digital balance. Each frog’s stomach was flushed following the methodology proposed by Solé et al. (2005) and specimens were released at the capture site during the same night, about two to four hours after having been captured. Stomach contents were transferred Figure 1. Leptodactylus ocellatus, adult female. Mirco Solé et al. to vials, fixed in 70% ethanol and later analyzed under a stereomicroscope. Prey items were classified following order level, with exception of Hymenoptera, which were classified as Formicidae and Non-Formicidae. Completely preserved items were measured and had their volume calculated using V 4S L § W · ¨ ¸ 3 2© 2 ¹ 2 the formula for ellipsoid bodies (Griffith and Mylotte, 1987): with L = prey length and W = prey width. If partially digested body parts were retrieved, the regression formulae proposed by Hirai and Matsui (2001) were used to estimate the original prey size, followed by the volume calculation using the above mentioned formula. For regression analyses XLSTAT 2008 (www.addinsoft.de) was used. To meet statistical assumptions prey volume was log+1 transformed (Zar, 1999). ������������� The index of relative importance (IRI) was applied as a measure that reduces bias in description of animal dietary data. It was introduced by ������������������������������������������������������ Pianka, Oliphant and Iverson (1971)������������������� and Pianka (1973): IRI t ( POt )( PI t PVt ) where POt is the percentage of occurrence (100 x number of stomachs contained t item / total number of stomachs), PIt is the percentage of individuals (100 x total number of individuals of t in all stomachs/total number of individuals of all taxa in all stomachs), and PVt is the percentage of volume (100 x total volume of individuals of t in all stomachs/total Diet of Leptodactylus ocellatus from Southern Bahia, Brazil volume of all taxa in all stomachs). In order to compare the trophic niche breath the standardized Shannon-Weaver entropy index J was used (Weaver and Shannon, 1949): J H log(n) whereby, H ¦ pi log( pi ) pi is the relative abundance of each prey category, calculated as the proportion of prey items of a given category to the total number of prey items (n) in all compared studies. To calculate the trophic niche breadth, the Levins index (B) was used (Krebs, 1989): 1 B ¦ pi2 where pi = fraction of items in the food category i; range = 1 to N. Results A total of 117 frogs were captured including predominately adult and subadult specimens measuring from 32.01 mm to 142.29 mm SVL (mean ± SD 91.33 ± 15.05 mm; Fig. 3) and with a weight of 8.27–159.25 g (mean ± SD 85.63 ± 31.35 g). Mouth width measured 13.99 to 38.52 mm (mean ± SD 30.60 ± 4.33 mm). Data on the diet of L. ocellatus at the study area are 11 summarized in Table 1. A total number of 77 stomachs revealed at least one prey item and 38 stomachs were empty. The mean number of prey items per stomach was 7.52 ± 9.46 (min= 1; max= 44). Volume of prey items ranged from 1.02 – 25481.11 mm3 (mean ± SD 634.56 ± 2915.79 mm3). Most frequent prey items were Lepidoptera larvae (N= 304, N%= 53.52), followed by Araneae (N= 39, N%= 6.87) and Diptera larvae (N= 35, N%= 6.16). Regarding the frequency of occurrence, Lepidoptera larvae, Araneae, and Coleoptera were most important (each F= 21, F%= 27.27). Lepidoptera larvae (V= 113317.7 mm3, V%= 63.15), Coleoptera (V= 16492.2 mm3, V%= 9.19) and Hemiptera (V= 13291.3 mm3, V%= 7.14) resulted to be the most important prey categories in terms of volume. The index of relative importance showed that the diet of L. ocellatus was dominated by Lepidoptera larvae (IRI = 3182.07), followed by Coleoptera (IRI = 394.72) and Araneae (IRI= 276.53). S������������� imple linear regression analyses revealed no significant relationships between SVL or mouth width of L. ocellatus and prey volume, minimum lengths of prey items and maximum length of prey items in our study (Fig. 4). The Levins index observed in our samples was 8.51 and the standardized Shannon-Weaver index was 0.56. Figure 2. Study site. Temporary pond (A) and small stream (B), where specimens of Leptodactylus ocellatus were collected. 12 Discussion Our sample was biased toward adults, which were frequently found on the margins of the temporary pond and the small river in open areas as well as in denser vegetation, whereas juveniles were rare suggesting microhabitat segregation between adults and juveniles. A similar observation was reported from a pit fall survey in Uruguay, where most of the juveniles of L. ocellatus were found far away from ponds (Maneyro, pers. comm.). Dietary composition as observed in our study was similar to those reported for conspecific populations by Stüssmann et al. (1984) ������������������������������������� ������������������������������ in Pará (Brazil), Lajmanovich ������������ (1996) in Paraná (Argentina), Teixeira and Vrcibradic (2003) in Espírito Santo (Brazil), França, ������������������� Facure and Giaretta (2004) in Minas Gerais (Brazil), ����������� Maneyro et al. ���������������������������������������������� (2004) in Maldonado Department (Uruguay), and Sanabria, Quiroga and Acosta (2005) in east Argentina where Coleoptera, Formicidae, Araneae and Orthoptera made up major parts, and small percentages of ingested vertebrates were also found. Presence of vertebrates in the diet of anurans is mainly restricted to large species and was previously reported for several Leptodactylus species including L. labyrinthicus (Cardoso and Sazima, 1977; França, Facure and Giaretta, 2004), L. wagneri (Duellman, 1978), and L. chaquensis (Duré, 1999) besides L. ocellatus. Teixeira and Vrcibradic Mirco Solé et al. (2003) found, respectively, one specimen of the anurans Hypsiboas albomarginatus, Leptodactylus ocellatus and Physalaemus crombiei and one fish (Poecilia vivipara) ingested by specimens of L. ocellatus studied in Espírito Santo, Brazil. Maneyro et al. (2004) detected three anuran specimens ingested by Uruguayan L. ocellatus, França, Facure and Giaretta (2004) found adult anuran specimens (each one Leptodactylus funarius, Rhinella granulosa and one unidentified hylid) and tadpoles in stomachs of L. ocellatus at Minas Gerais, and Sanabria, Quiroga and Acosta (2005) found six bufonids in stomach contents of Argentinean specimens. All studies revealed that vertebrates commonly make up only minor parts of the diet of L. ocellatus. Terrestrial invertebrates usually dominate the diet of most anurans, even in those species which are aquatic or semiaquatic (e.g. Hirai and Matsui, 2001; Stewart and Sandison, 1972). However, the presence of completely aquatic organisms such as belostomatid beetle (Teixeira and Vrcibradic, 2003), fishes and tadpoles (França, Facure and Giaretta, 2004; Teixeira and Vrcibradic, 2003; this study) in the diet suggest that L. ocellatus occasionally forage in the water and might be even capable of capturing prey under water as reported for one other neotropical frog (Solé and Miranda, 2006). The presence of decapod crustaceans as stomach content observed during our study is another hint for Figure 3. Relative frequency of SVL classes in Leptodactylus ocellatus. 13 Diet of Leptodactylus ocellatus from Southern Bahia, Brazil Table 1. Prey types consumed by Leptodactylus ocellatus (N= 117) from a cacao plantation in southern Bahia, Brazil. N= number of prey items; N%= percentage of total number; F= frequency of occurrence; F%= relative frequency of occurrence; V= volume in mm3; V%= relative volume in mm3; IRI= index of relative importance. Prey items Annelida Mollusca Oligochaeta N N% F F% V V% IRI 3 0.53 1 1.30 1547.43 0.86 1.81 Bivalvia 1 0.18 1 1.30 27.91 0.02 0.25 Gastropoda 2 0.35 2 2.60 32.07 0.02 0.96 Crustacea Decapoda 1 0.18 1 1.30 415.50 0.23 0.53 Arachnida Acari 4 0.70 4 5.19 6.20 0.00 3.68 Araneae 39 6.87 21 27.27 5872.86 3.27 276.53 Opiliones 34 5.99 17 22.08 4966.85 2.77 193.27 Chilopoda 6 1.06 6 7.79 1817.31 1.01 16.12 Diplopoda 13 2.29 12 15.58 2396.84 1.34 56.49 394.72 Myriapoda Insecta Coleoptera 30 5.28 21 27.27 16492.24 9.19 Dermaptera 1 0.18 1 1.30 39.93 0.02 0.26 Diptera 6 1.06 3 3.90 189.12 0.11 4.53 Diptera Larvae 35 6.16 4 5.19 8059.32 4.49 55.34 Hemiptera 12 2.11 9 11.69 13291.25 7.41 111.28 Hymenoptera (Formicidae) 17 2.99 13 16.88 596.11 0.33 56.14 Hymenoptera (Non-Formicidae) 27 4.75 18 23.38 3275.38 1.83 153.79 Isoptera 13 2.29 3 3.90 909.82 0.51 10.89 4 0.70 4 5.19 432.94 0.24 4.91 304 53.52 21 27.27 113317.74 63.15 3182.07 Lepidoptera Lepidoptera Larvae Odonata Orthoptera 1 0.18 1 1.30 2971.56 1.66 2.38 13 2.29 8 10.39 2165.12 1.21 36.32 Pisces Teleostei 1 0.18 1 1.30 226.02 0.13 0.39 Amphibia Anura (tadpole) 1 0.18 1 1.30 379.50 0.21 0.50 100 173 179429.02 100 4563.15 Plant Remains Total 38 568 this sporadic feeding behavior. Decapods were not previously reported as part of the diet in L. ocellatus. Plant remains were detected in half of the examined stomachs. The ingestion of plants is generally considered accidental in anurans (Brandão et al. 2003; Solé and Pelz, 2007), but folivory (Das, 1996) or frugivory (������������������������������������������������������� Silva and Britto-Pereira, 2006) have been reported for a few species. During our studies we retrieved a seed of a jack tree (Artocarpus heterophyllus) from one of the examined frog stomachs. The seed measured 31.37 mm in length and 17.81 mm in width, and the mouth width of the frog was 32.14 mm. Rotting jackfruits are usually covered by a wide variety of arthropods, and we do not know if the ingestion of this seed by the frog was accidental while preying on the arthropods or intentional. Other studies reported that SVL and mouth width was 49.35 100 significantly correlated with prey size and volume (França, Facure and Giaretta, 2004; Maneyro et al., 2004). However, in our study simple linear regression analyses revealed no significant relationships between SVL or mouth width of L. ocellatus and prey volume, minimum lengths of prey items and maximum length of prey items in our study (Fig. 4). Since variation in size was low in our sample (Fig. 3), it is likely that the failure to detect significant relationships between SVL (and mouth width) and prey size was caused by the high proportion of adult specimens included. Maneyro et al. (2004) and França, Facure and Giaretta (2005) sampled frogs in different habitats including a higher proportion of juveniles enhancing size variation. The Levins index (8.51) observed in our samples was most similar to those obtained from population of L. ocellatus analyzed in a human altered lagoon in Espírito 14 Mirco Solé et al. Figure 4. Simple linear regression analyses revealed no significant relationships between SVL and prey volume (log(Vol); R2= 0.000, p= 0.970; 4A), maximum length of prey items (R2= 0.002, p= 0.747; 4B) and minimum lengths of prey items (R2= 0.012, p= 0.419; 4C) and mouth width and prey volume (R2= 0.002, p= 0.704; 4D), maximum length of prey items (R2= 0.002, p= 0.718; 4E) and minimum lengths of prey items (R2= 0.018, p= 0.326; 4F). Santo (8.52, Teixeira and Vrcibradic, 2003), whereas values in other studies were slightly lower (7.74, França, Facure and Giaretta, 2004; 7.26, ���������������������� Maneyro et al., 2004; 7.40, ����������������������������������������� Sanabria, Quiroga and Acosta, 2005������� ). The standardized Shannon-Weaver index observed in our study was 0.56. It was slightly lower than reported in other studies (0.71, Teixeira and Vrcibradic, 2003; 0.74 França, Facure and Giaretta, 2004������������������������ ; 0.66, Maneyro et al., 2004; 0.63 Sanabria, ����������������������������������������� Quiroga and Acosta, 2005������� ). The observed differences may be attributed to differences in body size and/or prey availability in the studied habitats. However, the available data suggest that differences in trophic niche breadth and prey diversity in the diet of L. ocellatus inhabiting natural and human modified habitats are small. ����������������������������������������������� Apparently, the structure of the trophic niche of L. ocellatus is not affected by habitat alteration. Acknowledgements We are grateful to the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) for issuing necessary permits (No. 10830-1 (IBAMA-SISBIO) and Licença permanente 13708-1 (ICMBio)). Raul Maneyro, Axel Kwet and Vincenzo Mercurio kindly improved the manuscript with many valuable suggestions. Work of IRD was funded by FAPESB, EARS by ICB-UESC, EMJ by PIBIC-CNPq and DR by “Graduiertenförderung des Landes Nordrhein-Westfalen”. References Brandão, R. A, Garda, A., Braz, V., Fonseca, B. (2003). Observa�������� tions on the ecology of Pseudis bolbodactyla (Anura, Pseudidae) in central Brazil. Phyllomedusa 2, 3-8. Cardoso, A.J., Sazima, I. (1977): Batracofagia na fase adulta e larvária da ra-pimenta Leptodactylus labyrinthicus (Spix, 1824). Anura, Leptodactylidae. Ciência e Cultura 29, 11301132. Carey, C., Heyer, W.R., Wilkinson, J., Alford, R.A., Arntzen, J.W., Halliday, T., Hungerford, L., Lips, K.R., Middleton, E.M., Orchard, S.A., Rand, A.S. (2001): Amphibian declines and environmental change: Use of remote-sensing data to identify environmental correlates. Conservation Biology 15, 903-913. Cei, J.M. (1980): Amphibians of Argentina. 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