Herpetology Notes, volume 8: 157-160 (2015) (published online on 10 April 2015)

Diet of the striped snouted treefrog squalirostris (Anura: ) in southern Brazil

Rebecca N. Kittel1,* and Mirco Solé2

Abstract. The diet of 54 specimens of the striped snouted (Lutz, 1925) from southern Brazil was examined by flushing of stomach contents. We found 35 prey items and recorded their frequency of occurrence and percent of diet. About half of the prey items in the diet consisted of insects (54%), and within Insecta, Diptera (32%) was the major order represented. In addition to insects, S. squalirostris fed on Arachnida (37%), Gastropoda (6%), and Clitellata (3%).

Key Word. Brazil; stomach flushing; Scinax; stomach contents.

Introduction of anurans will help to understand its feeding ecology (Duellman & Trueb 1994; Teixeira & Vrcibradic 2003), The diet of anurans is generally influenced by but also the life history of the anurans. It can help to morphological traits, such as body size or size of identify environmental conditions and therefore mouth (Biavati et al. 2004), physiological factors, such alterations as well as conservation strategies (Batista et as energy demand (Grayson et al. 2005), and by the al. 2011). availability of food resources in the environment (Lopez Tree (Hylidae) are widely distributed all over et al. 2009), but also by environmental changes (Solé the world, except for the Arctic and Antarctic regions. et al. 2009), seasonality (Maragno 2011), and hunting The subtropical northeast of Rio Grande do Sul, the strategy (Maneyro & da Rosa 2004). For example, it has Araucarian Plateau, has been considered an anuran been shown that larger individuals consume larger prey hotspot (Kwet 2001), and thus a perfect locality for in larger quantities (Biavati et al. 2004; Sanabria et al. studies on frog ecology (Solé & Pelz 2007; Dietl et al. 2005; Lopez et al. 2009). 2009). The majority of are generalist invertebrate predators (Rodrigues et al. 2004; Lopez et al. 2009). Material and Methods However, some taxa (e.g., Dendrobatidae) are specialised on a specific type of prey (Biavati et al. 2004; Wells Study site 2007). As a result, amphibians play an important role The study was carried out in the Center for Research in both aquatic and terrestrial ecosystems by controlling and Conservation of Nature Pró-Mata (-29.466667, - populations of many organisms (Peltzer & Lajmanovich 50.166667; 900 m as.l.) of the São Francisco de Paula 1999; Toledo et al. 2007; Wells 2007). Knowing the diet District in northeastern Rio Grande do Sul, southern Brazil. Anurans were collected near a temporary pond surrounded by Campo and a permanent pond surrounded by forest. Approximate pond sizes varied depending on seasonality between 10 m2 and 100 m2. 1 Graduate School of Agricultural Science, Kobe University, Rokkodai 1, Nada, Kobe 657-8501, Japan Sampling 2 Department of Biological Sciences, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado, km 16, 45662-900 Within one hour of collection between February and Ilhéus, Bahia, Brazil April 2005, the frogs were brought to the lab where * Corresponding author email: [email protected] the snout-vent length (SVL) was measured, all frogs 1 Table 1. Diet of the 22 specimens of S. squalirostris with stomach content. N gives the 158 2 number of prey items found in total and as a percentage, where some frogsRebecca hold multiple N. Kittel & Mirco Solé 3 items. F states the number of frogs containing these prey items (frequency of prey items Table 1. Diet of the4 22 found)specimens in total of S.and squalirostris as a percentage. with IRI stomach shows content.the Index N of gives Relative the numberImportance, of prey important items found in total and as a percentage, where some frogs hold multiple items. F states the number of frogs containing these prey items (frequency of prey 5 prey items are in bold. items found) in total and as a percentage. IRI shows the Index of Relative Importance, important prey items are in bold. 6

Prey N N (%) F F (%) Vol Vol (%) IRI Annelida: Clitellata 1 2.86 1 3.33 - - - Arachnida: Araneae 13 37.14 10 33.33 0.92 12.74 27.74 Hexapoda: Insecta - - - Blattodea 1 2.86 1 3.33 1.36 18.84 8.34 Coleoptera 3 8.57 3 10.00 0.41 5.68 8.08 Collembola 2 5.71 2 6.67 0.2 2.77 5.05 Diptera 6 17.14 5 16.67 1.74 24.10 19.30 Heteroptera 1 2.86 1 3.33 - - - Homoptera 2 5.71 2 6.67 2.4 33.24 15.21 Hymenoptera 1 2.86 1 3.33 0.18 2.49 2.89 Lepidoptera (caterpillar) 1 2.86 1 3.33 - - - Orthoptera 1 2.86 1 3.33 - - - Plecoptera 1 2.86 1 3.33 0.01 0.14 2.11 Mollusca: Gastropoda 2 5.71 1 3.33 - - - total 35 100.00 30 100.00 7.22 100.00 7 8 9 10 11 weighed, and their stomachs flushed without harming nMDS them (Solé et 12 al. 2005). The stomach contents were Diet overlap among Scinax species was analysed preserved in 70%13 ethanol. After these procedures, the using an Non-metric multidimensional scaling (nMDS) frogs were released where they were captured. Stomach approach as implemented in the package “vegan” in R contents were identified under a stereomicroscope. (R Development Core Team 2008; Oksanen et al. 2015). The amount of possible distortion (fit between rank Analyses order and predicted dissimilarities) in a plot is measured The volume of prey items were calculated using the by stress. Lower stress values (<0.2) indicate that the following formula for ellipsoid bodies (Griffiths & nMDS plot is a good representation of dissimilarities Mylotte 1987): (Quinn & Keough 2002). We used a Bray-Curtis ordination to quantify the degree of stress.

Results - 1 - where l represents the length of prey items and w the During the study 54 specimens were captured, with width. If only indigestible or incompletely digested snout to vent length (SVL) measurements ranging from body parts remained, we used a regression formula 22.4 to 28.2 mm, the body weight varied from 0.5 to (Hirai & Matsui 2001) to estimate the original prey 1.15 g. Although the flushing of the frog’s stomachs size. The index of relative importance was calculated happened quickly after the capture, 12 frogs (22%) had for each prey category in the diet (Biavati et al. 2004) a completely empty stomach and 20 frogs (37%) had with the formula: various plant materials in the stomachs, but no prey. The remaining 22 frogs (40%) had 35 prey items in total in their stomachs, comprising Insecta (54.3%), Arachnida (37.1%), Mollusca (5.7%), or Annelida (2.9%), percent among all prey items. The Insecta were where F% is the frequency of occurrence, N% the represented by 10 orders (see Tab 1), and within the numeric percentage, and V% the volumetric Insecta, the numerical percentages were as following: percentage. Diptera (32%), Coleoptera (16%), Collembola (11%), Diet of the striped snouted treefrog in southern Brazil 159

dominated by Araneae and Blattodea (Solé & Pelz 2007) (see Fig.2). Interestingly S. argyreornatus had a completely different prey spectrum. The dominant prey were ants (Formicidae), followed by Isopoda (Teixeira & Roeder 2007). This is interesting, because Formicidae form a part or the majority of diets of other anuran species, not restricted just to leaf litter frogs (Vitt & Caldwell 1994; Caldwell 1996; Hirai & Matsui 1999, 2001; Dietl et al. 2009). Lastly, the diet of S. squalirostris is very similar to another treefrog species Dendropsophus minutus (Solé & Pelz 2007), which has a prey content of 24% of all studied specimens. Dendropsophus minutus Figure 1. Relationship between weight of S. squalirostris specimens with stomach conetent and the volume of animal feeds mostly on Araneae, Diptera, and Homoptera and prey. the similar prey preferences might be due to the size and habitat preference. Based on the prey found in the stomachs and the ecological prey guilds as defined by Teixeira and Roedder (Teixeira & Roedder 2007), S. squalirostris appears to be an active hunter, consuming actively flying animal prey. This finding, however, Homoptera (11%), Blattodea (5%), Heteroptera (5%), needs to be verified by further investigations of the prey Hymenoptera (5%), Lepidoptera (5%), Orthoptera availability (Maneyro & da Rosa 2004). A long spawning (5%), and Plecoptera (5%). We calculated the relative period in anurans results in regular feeding events (Solé importance of all taxa and the top prey items were & Pelz 2007). Kwet (2001) indicates that the spawning Arachnida, Diptera, and Homoptera. The average prey of S. squalirostris takes place from September to April, volume increased with individual body weight (Fig. 1). The nMDS analysis shows a stress value of 0.08.

Discussion Two previous studies have examined the stomach content of three Scinax species, S. argyreornatus, S. granulatus, and S. perereca (Solé & Pelz 2007; Teixeira & Roedder 2007). The percentage of frogs with prey in their stomachs in this study (40%) is similar to that of previous studies; S. granulatus 36% and S. perereca 34%, however, S. argyreornatus had 83%. Although the amount of prey items in this study of the diet of S. squalirostris appears to be low with 35 prey items found in 22 stomachs containing prey items, it appears to be an average amount compared to 30 prey items found in S. granulatus, and 32 prey items found in S. perereca (Solé & Pelz 2007). In general the diet seems to be similar among the species, except for S. argyreornatus which’s stomach content differed much (Teixeira & Roeder 2007) (see Fig.2).

Figure 2. An nMDS ordination plot, showing the different diet The diet of S. granulatus comprised mostly Insecta, preferences of the four Scinax species. Numbers in the plot are with Coleoptera and Homoptera being the major orders. for the invertebrate classes or in case of insects, the orders: 1: Additionally, specimens of S. granulatus had Acari and Annelida; 2: Arachnida; 3: Crustacea; 4-15 Insecta (Blattodea, Isoptera in their stomach (Solé & Pelz 2007), which Coleoptera, Collembola, Diptera, Heteroptera, Homoptera, were absent in S. squalirostris. had Hymenoptera, Isoptera, Lepidoptera, Odonata, Orthoptera, less variable stomach contents, in which the prey was Plecoptera); 16: Mollusca; 17: Myriapoda. 160 Rebecca N. Kittel & Mirco Solé covering the time-frame of this study. package=vegan. Peltzer, P.M. & Lajmanovich, R.C. (1999): Análisis trófico en dos Acknowledgements. We thank Tatiana Miranda, Lars Krieger, poblaciones de (Anura: Hylidae) de Argentina. Kerstin Ewald, and Camila Both for their help during field work. Alytes 16: 84-96. We appreciate the facilities provided by the IMA staff of the Quinn, G.P. & Keough, M.J. (2002) Experimental Design and Data PUCRS and the financial support from the Landesstiftung Baden- Analysis for Biologists. Cambridge: Cambridge University Württemberg received by RNK to conduct the field work. Thanks Press. to John Jennings (Uni Adelaide) for comments on an earlier version R Development Core Team. (2008) R: A language and environment of the manuscript. for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Rodrigues, D.J., Uetanabro, M., & Rado, C.P.A. (2004): Seasonal References and ontogenetic variation in diet composition of Leptodactylus Batista, R.C., De-Carvalho, C.B., Freitas, E.B., Franco, S.C., podicipinus (Anura, Leptodactylidae) in the southern Pantanal, Batista, C.C., Coelho, W.A., & Faria, R.G. (2011): Diet of Brazil. Revista Española de Herpetología 18: 19-28. Rhinella schneideri (Werner, 1894) (Anura: Bufonidae) in the Sanabria, E.A., Quiroga, L.B., & Acosta, J.C. (2005): Dieta Cerrado, Central Brazil. Herpetology Notes 4: 17-21. de Leptodactylus ocellatus (Linnaeus, 1758) (Anura: Biavati, G.M., Wiederhecker, H.C., & Colli, G.R. (2004): Diet Leptodactylidae) en un humedal del oeste de Argentina. Revista of Epipedobates flavopictus (Anura: Dendrobatidae) in a Peruana de Biología 12. Neotropical Savanna. Journal of Herpetology 38: 510-518. Solé, M., Beckmann, O., Pelz, B., Kwet, A., & Engels, W. (2005): Caldwell, J.P. (1996): The evolution of myrmecophagy and its Stomach-fushing for diet analysis in anurans: an improved correlates in poison frogs (Family Dendrobatidae). Journal of protocol evaluated in a case study in Araucaria forests, southern Zoology 240: 75-101. Brazil. Studies on Neotropical Fauna and Environment 40: 23- Dietl, J., Engels, W., & Solé, M. (2009): Diet and feeding 28. behaviour of the leaf-litter frog Ischnocnema henselii (Anura: Solé, M., Dias, I.R., Rodrigues, E.A.S., Marciano-Junior, E., Brachycephalidae) in Araucaria rain forests on the Serra Geral Branco, S.M.J., Cavalcante, K.P., & Rödder, D. (2009): Diet of of Rio Grande do Sul, Brazil. Journal of Natural History 43: Leptodactylus ocellatus (Anura: Leptodactylidae) from a cacao 1473-1483. plantation in southern Bahia, Brazil. Herpetology Notes 2: 9- Duellman, W.E. & Trueb, L. (1994) Biology of amphibians. 15. Baltimore & London: John Hopkins University Press. Solé, M. & Pelz, B. (2007): Do male tree frogs feed during the Grayson, K.L., Cook, L.W., Todd, M.J., Pierce, D., Hopkins, W.A., breeding season? Stomach flushing of five syntopic hylid species Gatten Junior, R.E., & Dorcas, M.E. (2005): Effects of prey in Rio Grande do Sul, Brazil. Journal of Natural History: 1-7. type on specific dynamic action, growth, and mass conversion Teixeira, R.L. & Roedder, D. (2007): Diet, foraging strategy efficiencies in the horned frog, Ceratophrys cranwelli. and reproduction of Scinax argyreornatus (Miranda-Ribeiro, Comparative Biochemistry and Physiology 141: 298-304. 1926) from a mountainous region of the Atlantic rainforest in Hirai, T. & Matsui, M. (1999): Feeding habits of the pond frog, southeastern Brazil. Herpetozoa 19: 161-173. Rana nigromaculata, inhabiting rice fields in Kyoto, Japan. Teixeira, R.L. & Vrcibradic, D. (2003): Diet of Leptodactylus Copeia: 940-947. ocellatus (Anura; Leptodactylidae) from coastal lagoons of Hirai, T. & Matsui, M. (2001): Attempts to estimate the original southeastern Brazil. Cuadernos de Herpetología 17: 111-118. size of partly digested prey recovered from stomachs of Japanese Toledo, L.F., Ribeiro, R.S., & Haddad, C.F.B. (2007): Anurans as anurans. Herpetological Review 32: 14-16. prey: an exploratory analysis and the size relationships between Kwet, A. (2001) Frösche im brasilianischen Araukarienwald: predators and their preys. Journal of Zoology 271: 170-177. Anurengemeinschaft des Araukarienwaldes von Rio Grande Vitt, L.J. & Caldwell, J.P. (1994): Resource utilization and guild do Sul: Diversität, Reproduktion und Ressourcenaufteilung. structure of small vertebrates in the Amazon forest leaf litter. Münster: Natur und Tier-Verlag. Journal of Zoology 234: 463-467. Lopez, J.A., Scarabotti, P.A., Medrano, M.C., & Ghiradi, R. Wells, K.D. (2007) The ecology and behavior of amphibians. (2009): Is the red spotted green frog Hypsiboas punctatus Chicago: University Chicago Press. (Anura: Hylidae) selecting its preys? The importance of prey availability. Revista de Biologia Tropical 57: 847-857. Maneyro, R. & da Rosa, I. (2004): Temporal and spatial changes in the diet of Hyla pulchella (Anura, Hylidae) in southern Uruguay. Phyllomedusa 3: 101-113. Maragno, F.P.S., F.L. (2011): Diet of Rhinella scitula (Anura, Bufonidae) in the Cerrado, Brazil: the importance of seasons and body size. Revista Mexicana de Biodiversidad 82: 879-886. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, Accepted by Diogo Provete M.H.H., & Wagner, H. (2015): vegan: Community Ecology Package. R package version 2.2-1. http://CRAN.R-project.org/