Herpetology Notes, volume 6: 603-606 (2013) (published online on 13 December 2013)
Predation of Odontophrynus americanus (Anura: Odontophrynidae) by the invasive species Lithobates catesbeianus (Anura: Ranidae) in an Araucaria Forest remnant in Southern Brazil Peterson Trevisan Leivas1*, Marcoandre Savaris2, Silvana Lampert2 and Elaine Maria Lucas3
Biological invasions are one of the most complex social-environmental problems in the world. Their negative impacts affect the economy and biodiversity of several countries (McNeely et al., 2001; Vilà et al., 2009). Impacts on biodiversity can be direct (e.g., predation and competition) and indirect (pathogens transmission) on the native species (White, Wilson and Clarke, 2006; McGeoch et al., 2010). These effects lead to population decline and species dislocation and, consequently, alterations in the native community structures (Desprez-Loustau, Robin and Buée, 2007; Kenis et al., 2009). Lithobates catesbeianus (Shaw, 1802) (American Bullfrog) is a native anuran from North America introduced in more than 40 countries due to its economic potential (Ficetola, Thuiller and Miaud, 2007). In Brazil, the species was introduced in the 1930s in the state of Rio de Janeiro, and currently it has a broad distribution in the country, especially in the southern and southeastern Atlantic Forest (Giovanelli, Haddad and Alexandrino, 2008; Both et al., 2011; Loyola et al., 2012). The American Bullfrog is one of the 100 species with greatest invasive potential in the world (Lowe et
Universidade Federal do Paraná (UFPR), Programa de PósGraduação em Ecologia e Conservação. Caixa Postal 19020, CEP 81531-980, Curitiba, Paraná, Brazil. 2 Universidade Federal do Paraná (UFPR), Departamento de Zoologia. Caixa Postal 19020. CEP 81531-980, Curitiba, Paraná, Brazil. 3 Universidade Comunitária da Região de Chapecó, Programa de Pós-Graduação em Ciências Ambientais. CEP 89809-000, Chapecó, Santa Catarina, Brazil. * Corresponding author. E-mail:
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al., 2004; GISP, 2012). It is responsible for the decline of anuran populations at global and local scales, due to direct and indirect effects on native species (e.g., predation, competition and pathogens transmission) (Kupferberg, 1997; Wu et al., 2005; Schloegel et al., 2009). The knowledge on biological aspects and impact of L. catesbeianus in the Brazilian fauna is incipient and restricted to reproductive (Kaefer, Boelter and Cechin, 2007; Leivas, Fávaro and Moura, 2012), interspecific acoustic interference (Both and Grant, 2012) and feeding biology (e.g., diet, trophic niche and reports of vertebrate predation) in natural environments (Boelter and Cechin, 2007; Silva et al., 2009; Leivas, Leivas and Moura, 2012). Given this scenario, we present a report of predation of the native species Odontophrynus americanus (Duméril & Bibron, 1841) by the invasive species L. catesbeianus in a Protected Area in Brazil. We recorded the event at the Reserva Particular do Patrimônio Natural Maragato (RPPN; -28.2413666667°, -52.45732777778°, 626 m a.s.l; DATUM=WGS84), Passo Fundo, Rio Grande do Sul, Brazil. The area has 41.56 ha and is in the Araucaria Plateau (Planalto das Araucárias), transitioning to the Missions Plateau (Planalto das Missões), with predominance of smooth hills “slightly rugged” landscape (Martinez, Prestes and Noetzold, 2009). On March 25th 2011 during a nocturnal survey under heavy rain in the margin of a lake, we observed L. catesbeianus preying on O. americanus in a chorus of that latter species. The specimen of O. americanus had only the hind legs outside the mouth of the predator and was emitting distress call (Figures 1a and 1b). After removing O. americanus from L. catesbeianus mouth, we released the prey and euthanized L. catesbeianus following norms of the Federal Council of Veterinary Medicine (Resolution 714).
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Figure 1. A) and B) Lithobates catesbeianus preying on Odontophrynus americanus. C) and D) Adult O. americanus partially swallowed by L. catesbeianus; second and third individuals of O. americanus recorded in the stomach of L. catesbeianus after ventral sectioning, respectively.
After euthanasia, we desiccated L. catesbeianus for analysis of stomach content. We found two more individuals of O. americanus (Figure 1c and 1d). The specimen of L. catesbeianus had 132.63 mm in snoutvent length (SVL) and 170.87 g in body mass (BM). Individuals of O. americanus found in the stomach of L. catesbeianus had 40.53 mm SVL and 11.28 g BM and 45.91 mm SVL and 16.84 g BM, respectively. Specimens are housed in the Herpetological Collection of the Institute of Biological Sciences of the Universidade de Passo Fundo (n° 2739, 2740 and 2741). Predation of L. catesbeianus on vertebrates (e.g., fishes, snakes, birds, reptiles and mammals) was recorded in different place in the world (Lee, 1969; Gollob, 1978; Campbell and Ryder, 2004; Wu et al.,
2005). In Brazil, it was recorded the predation of fishes, snakes (Camargo Filho et al., 2008; Leivas, Leivas and Moura, 2012) and small native amphibians as hylids and microhylids (Boelter and Cechin, 2007; Silva et al., 2009) in natural environments, as well as large species like Rhinella abei (Baldissera-Jr, Caramaschi & Haddad, 2004) (Bufonidae) and Leptodactylus latrans (Linnaeus, 1758) (Leptodactylidae) (Leivas, Leivas and Moura, 2012). Males of Odontophrynus americanus call after heavy rains and the species has fossorial habits, occurring in forested areas and natural fields of Southern and Southeastern Brazil (Hiert and Moura, 2007; this study). This specie was already known as a food item for L. catesbeianus in the state of Rio Grande do Sul (two
Predation of Odontophrynus americanus by Lithobates catesbeianus individuals) (Boelter and Cechin, 2007). However, the predatory behavior recorded in this study, in which L. catesbeianus was preying sequentially on individuals of O. americanus in a chorus have never been described before. This opportunistic behavior comes from the feeding tactic of the species, classified as a convenience generalist predator (Toledo, Silva and Haddad, 2007). Our results, along with the knowledge on vertebrate predation both in Brazil and in the world (Wu et al., 2005; Boelter and Cechin, 2007; Silva et al., 2009; Leivas, Leivas and Moura, 2012) reinforce that L. catesbeianus has a strong negative direct effect to predation on native species. We emphasize the need for long-term studies to gather more data about this phenomenon described here. We argue that more effective action plans that aim to control/eradicate this species from natural habitats of the Araucaria Forest and protected areas with great biodiversity are necessary. Acknowledgements. We thank the Private Reserve of Natural Heritage Maragato (Reserva Particular do Patrimônio Natural Maragato – RPPN) and the Post-graduation Programs in Zoology and Ecology and Conservation of the Universidade Federal do Paraná for facilitating this study. We also thank CNPq and CAPES for the fellowships granted to Marcoandre Savaris, Silvana Lampert and Peterson T. Leivas.
References Boelter, R.A., Cechin, S.Z. (2007): Impact of the bullfrog diet (Lithobates catesbeianus Anura, Ranidae) on native fauna: case study from the region of Agudo, RS, Brazil. Natureza & Conservação 5: 115-123. Both, C., Lingnau, R., Santos-Jr., A., Madalozzo, B., Lima, L.P., Grant, T. (2011): Widespread Occurrence of the American Bullfrog, Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae), in Brazil. South American Journal of Herpetology 6: 127-134. Both, C., Grant, T. (2012): Biological invasions and the acoustic niche: the effect of bullfrog calls on the acoustic signals of white-banded tree frogs. Biology Letters 8: 714-716. Camargo Filho, C.B., Costa, H.C., Silva, E.T., Ribeiro Filho, O.P., Feio, R.N. (2008): Lithobates catesbeianus (American Bullfrog) prey. Herpetological Review 39: 338. Campbell, R.W., Ryder, G.R. (2004): Field observations of bullfrog (Rana catesbeina) prey in British Columbia. Wildlife Afield 1: 61-62. Desprez-Loustau, M.L., Robin, C., Buée, M. (2007): The fungal dimension of biological invasions. Trends in Ecology and Evolution 22: 472-480. Giovanelli, J.G.R., Haddad, C.F.B., Alexandrino J. (2008): Predicting the potential distribution of the alien invasive American bullfrog (Lithobates catesbeianus) in Brazil. Biological Invasions 10: 585-590.
605
GISP (2012): The global invasive species programme. Available at: http://www.gisp.org/. Last accessed on 12 September 2013. Gollob, T. (1978): Bullfrogs preying on cedar waxwing. Herpetological Review 9: 47-48. Ficetola, G.F., Thuiller, W., Miaud, C. (2007): Prediction and validation of the potential global distribution of a problematic alien invasive species - the American bullfrog. Diversity and Distribution 13: 476-485. Hiert, C., Moura, M.O. (2007): Anfíbios do Parque Municipal das Araucárias, Guarapuava, Paraná, 1° edição. Guarapuava, Editora Unicentro. Kaefer, I.L., Boelter, R.A., Cechin, S.Z. (2007): Reproductive biology of the invasive Bullfrog Lithobates catesbeianus in southern Brazil. Finnish Zoological and Botanical Publishing Board 44: 435-444. Kenis, M., Auger-Rozenberg, M.A., Roques, A., Timms, L., Péré, C., Cock, M.J.W., Settele, J., Augustin, S., Lopez-Vaamonde, C. (2009): Ecological effects of invasive alien insects. Journal Biological Invasion 11: 21-45. Kupferberg, S.J. (1997): Bullfrog (Rana catesbeiana) invasion of a California river: the role of competition. Ecology 78: 17361751. Lee, D.S. (1969): Notes on the feeding behavior of the cavedwelling bullfrogs. Herpetologica 25: 211-212. Leivas, P.T., Fávaro, L.F., Moura, M.O. (2012): The Reproductive Biology of the Invasive Lithobates catesbeianus (Amphibia: Anura). Journal of Herpetology 46: 153-161. Leivas, P.T., Leivas, F.W., Moura, M.O. (2012): Diet and trophic niche of Lithobates catesbeianus (Amphibia: Anura). Zoologia 29: 405-412. Loyola, R.D., Nabout, J.C., Trindade-Filho, J., Lemes, P., UrbinaCardona, J.N., Dobrovolski, R., Sagnoria, M.D., Diniz-Filho, J.A.F. (2012): Climate change might drive species into reserves: a case study of the American bullfrog in the Atlantic Forest Biodiversity Hotspot. Alytes 29: 61-74. Lowe, S.J., Browne, M., Boudjelas, S., De Poorter, M. (2004): 100 of the World’s Worst Invasive Alien Species: A selection from the Global Invasive Species Database. Auckland, New Zealand, IUCN, SSC and ISSG. Martinez, J., Prestes, N.P., Noetzold, R. (2009): Os ambientes do papagaio-charão (Amazona pretrei): fisionomia e estrutura da vegetação. In: Biologia da Conservação, p. 105-138. Martinez, J., Prestes, N.P., Org., Passo Fundo, Editora UPF. McGeoch, M.A., Butchart, S.H.M., Spear, D., Marais, E., Kleynhans, E.J., Symes, A., Chanson, J., Hoffmann, M. (2010): Global indicators of biological invasion: species numbers, biodiversity impact and policy responses. Diversity and Distributions 16: 95-108. McNeely, J.A., Mooney, H.A., Neville, L.E., Schei, P., Waage, J.K. (2001): A global strategy on invasive alien species. IUCN Gland, Switzerland, and Cambridge, UK. Schloegel, L.M., Picco, A.M., Kilpatrick, A.M., Davies, A.J., Hyatt, A.D., Daszak, P. (2009): Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biological Conservation 142: 1420-1426. Silva, E.T., Reis, E.P., Feio, R.E., Filho, O.P.R. (2009): Diet of the invasive frog Lithobates catesbeianus (Shaw, 1802) (Anura:
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Ranidae) in Viçosa, Minas Gerais state, Brazil. South American Journal of Herpetology 4: 286-294. Toledo, L.F., Silva, R.R., Haddad, C.F.B. (2007): Anurans as prey: an exploratory analysis and size relationships between predators and their prey. Journal of Zoology 271: 170-177. Vilà, M., Basnou, C., Pysek, P., Josefsson, M., Genovesi, P., Gollasch, S., Nentwig, W., Olenin, S., Roques, A., Roy, D., Hulme, P.E., Partners, D. (2010): How well do we understand the impacts of alien species on ecosystem services? A panEuropean, cross-taxa assessment. Frontiers in Ecology and the Environment 8: 135-144. White, E.M., Wilson, J.C., Clarke, A.R. (2006): Biotic indirect effects: a neglected concept in invasion biology. Diversity and Distributions 12: 443-455. Wu, Z., Li, Y., Wang, Y., Adams, M.J. (2005): Diet in introduced bullfrogs (Rana catesbeiana): Predation on and diet overlap with native frogs on Daishan Island, China. Journal of Herpetology 39: 668-674.
Accepted by Diogo Provete