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First Report of Predation by Calyptocephalella Gayi Upon the Invasive Species Xenopus Laevis (Amphibia, Anura, Calyptocephalellidae and Pipidae)

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First Report of Predation by Calyptocephalella Gayi Upon the Invasive Species Xenopus Laevis (Amphibia, Anura, Calyptocephalellidae and Pipidae) Herpetology Notes, volume 9: 171-173 (2016) (published online on 24 August 2016) First report of predation by Calyptocephalella gayi upon the invasive species Xenopus laevis (Amphibia, Anura, Calyptocephalellidae and Pipidae) Marta Mora1, 2, *, Javiera Constanzo-Chávez1, Juan Contardo2 and Antonieta Labra1,3,4 The helmeted water toad, Calyptocephalella gayi One important source of diseases potentially affecting (Duméril & Bibron, 1841), is a species endemic to Chile C. gayi comes from its sympatric occurrence with the and found in lakes, streams, and rivers from Coquimbo African clawed frog, Xenopus laevis, one of the worst to the Los Lagos region (Correa et al., 2011). It is a big alien species in the world (Lowe et al., 2000), presently and robust anuran that can reach a weight of 1.2 Kg worldwide distributed (Tinsley et al., 2015). This species and 30 cm of snout-vent length (SVL) (Lobos et al., is considered a threat for native amphibians, because it 2013). Currently, it is classified as Vulnerable by the acts as a biological vector of infectious diseases such IUCN (Veloso et al., 2010), and the major threats that as the chytrid fungus, Batrachochytrium dendrobatidis the species faces are the habitat loss, diseases, climate (Weldon et al., 2007), and parasites (Kupermann et al., change and its overexploitation (Vélez, 2014). For 2004). Moreover, available data indicate that native frog many years, it was collected for human consumption species decline when sharing microhabitat with X. laevis and for physiological experimentation (Hermosilla and (Lillo et al., 2011). In Chile, Solís et al. (2010) reported Acuña, 2004). Due to the increased overexploitation, the presence of the chytrid fungus in feral populations Chile prohibited its capture (Vallejos and Pizarro, 2004), of X. laevis, and Lobos et al. (2013) indicated that X. and it is a protected species in Chile since 1988 (Glade, laevis is a potential predator of native amphibian larvae, 1983). In addition, some conservation measures were which may reduce the population sizes of C. gayi. The established, such as the development of legal farming African clawed frog was introduced in Chile around to supply the local demands of the gastronomic market. 1970 to be used in pregnancy test, but also became In 2009 an ex-situ conservation program was started part of pet trade. Some individuals were released into to gather information on the biology and reproduction nature, and the species became quickly established of this species, for successful and sustainable farming and dispersed very rapidly (Lobos et al., 2013). In fact, (Vélez and Acuña, 2012). Unfortunately, illegal hunting since the first reported wild population of X. laevis in continues. 1973, in a restricted area of the Metropolitan region of Chile (Veloso and Navarro, 1988), the species is now known from an area that covers more than 21.200 km2, from Coquimbo to the O’Higgins region (Lobos et al., 2013). 1 ONG Vida Nativa, Santiago, Chile. The scarce information available on the natural history 2 Programa de Magíster en Áreas Silvestres y Conservación de of C. gayi, motivated us to start a monitoring program for la Naturaleza, Universidad de Chile, Santiago, Chile. this species with the aim to obtain relevant knowledge 3 Instituto de Ciencias Biomédicas, Facultad de Medicina, to improve the conditions for this species and reduce its Universidad de Chile, Casilla 70005, Correo 7, Santiago, vulnerability. Chile. Our study is carried out in an estuary of central Chile, at 4 Department of Biosciences, Centre for Ecological and Evolutionary Synthesis. University of Oslo, P.O.Box 1066 Villa Alemana, Valparaíso region, Chile (19S 277786E Blinder, N-0316, Oslo, Norway. and 6341650S), which has a Mediterranean climate. * Corresponding author e-mail: [email protected] The catchment basins where C. gayi inhabits are also 172 Marta Mora et al. Fig. 1. Calyptocephalella gayi with an African clawed frog in its mouth. A. Side view, B. Dorsal view. Photographs by Marta Mora. home to the native amphibian species Pleurodema diet to consume this common prey. Moreover, Rivero thaul, the invasive frog Xenopus laevis, an endemic (2010) determined that under experimental conditions fish Cheirodon pisiculus and one exotic fish Gambusia adults of C. gayi fed X. laevis larvae grew and increased affinis. Individuals of C. gayi were collected with in weight. dip nets, and then measured, photographed, stomach Presently, data on the prevalence of B. dendrobatidis, flushed, marked with a nano chip (Trovan ®Nano an important cause of amphibians mortality (Pasmans transponder ID100), and then released at the collecting et al., 2000), in X. laevis show that it is higher in Chile point, which is georeferenced. On 28 April 2016 at than in populations from other regions, such as those 11:30 h, we captured an adult of C. gayi (18 cm SVL, from Africa (24% vs. 2.7%, respectively; Solís et al., 536 gr of weight) with a live adult of X. laevis (4 cm 2010). Under this context, the fact that C. gayi includes SVL, 13 gr of weight) in its mouth (Fig. 1). X. laevis in its diet might result in an easy infection with It was previously reported that X. laevis can exhibit this fungus by direct contact (Piotrowski et al., 2004). skin secretions as antipredator mechanism that induce, Therefore, it is highly relevant to keep monitoring C. at least in some snake species, an involuntary oral gayi in this area of study, controlling the presence of dyskinesia that allows the frog to escape from the X. laevis and testing for the presence of emerging predator (Barthalmus and Zielinski, 1988; Barthalmus, diseases. 1989). We did not notice any similar effect in the individual of C. gayi, which suggests that, if present, Acknowledgement The study was authorized by the Servicio this antipredatory mechanism may not be effective with Agrícola y Ganadero (Resolution No. 1790/2016). We thank all predators. Hendrik Müller for pre-reviewing the manuscript. This is the first report of C. gayi eating X. laevis, and therefore, it is unclear how frequent X. laevis is part of C. References gayi diet. However, by considering that this species has Barthalmus, G.T. (1989): Neuroleptic modulation of oral a voracious appetite (Cei, 1962), it is likely that X. laevis dyskinesias induced in snakes by Xenopus skin mucus. may constitute a common prey of this frog, particularly Pharmacology Biochemistry and Behavior 34: 95–99. considering that X. laevis can reach high densities of 0,51 Barthalmus, G.T., Zielinski, W.J. (1988): Xenopus skin mucus induces oral dyskinesias that promote escape from snakes. ind/m2 (Ross et al., 2015). Moreover, close to our study Pharmacology Biochemistry and Behavior 30: 957–959. 2 site, the densities of X. laevis can reach up to ~14 ind/m Correa, C., Cisternas, J., Correa-Solís, M. (2011): Lista comentada (Mora et al. unpubl. data). Potentially, the high densities de las especies de anfibios de Chile (Amphibia: Anura). Boletín of X. laevis may determine that C. gayi switches its de Biodiversidad de Chile 6: 1– 21. First report of predation by Calyptocephalella gayi upon the invasive Xenopus laevis 173 Glade, A. (1983): Libro Rojo de los Vertebrados Terrestres Laguna El Peral, Región de Valparaíso. Biodiversidata 3: 41–– Chilenos. Santiago, Chile, Corporación Nacional Forestal. 44. Hermosilla, I., Acuña, P. (2004): Crianza en cautividad de la rana Solís, R., Lobos, G., Walker, S., Fisher, M., Bosch, J. (2010): grande chilena Caudiverbera caudiverbera (Linnaeus, 1758). Presence of Batrachochytrium dendrobatidis in feral populations In: Cría en Cautividad de Fauna Chilena, p.105–122. Iriarte, of Xenopus laevis in Chile. Biological Invasions 12: 1641– A., Tala, C., González, B., Zapata, B., González, G., Maino, 1646. M., Eds., Santiago, Chile, Servicio Agrícola Ganadero, Parque Tinsley, R., Stott, L., Viney, M., Mable, B., Tinsley, M. (2015): Metropolitano, Zoológico Nacional, Facultad de Ciencias Extinction of an introduced warm-climate alien species, Xenopus Veterinarias y Pecuarias and Universidad de Chile. laevis, by extreme weather events. Biological Invasions17: Kuperman, B., Matey, V., Fisher, R., Ervin, E., Warburton, M., 3183–3195. Bakhireva, L., Lehman, C. (2004): Parasites of the African Vélez, C. M., Acuña, P. (2012): Avances en el manejo ex situ de clawed frog, Xenopus laevis, in Southern California, U.S.A. Calyptocephalella gayi (rana grande chilena). In: Conservación Comparative Parasitology 71: 229–232. de Anfibios de Chile, p. 77–82. Soto-Azat, C., Valenzuela- Lillo, F., Faraone, F., Lo Valvo, M. (2011): Can the introduction of Sánchez, A., Eds., Santiago, Chile, Universidad Nacional Xenopus laevis affect native amphibian populations? Reduction Andrés Bello. of reproductive occurrence in presence of the invasive species. Vélez, C.M. (2014): Manejo en Cautiverio de la Rana Grande Biological Invasions 13: 1533–1541. Chilena, Calyptocephalella gayi (Duméril & Bibron, 1841), 1st Lobos, G. (2004): Historia natural del sapo africano Xenopus laevis Edition. 6antiago, Chile, Universidad Santo Tomás. en Chile. In: Antecedentes sobre la Biología de Xenopus laevis y Veloso, A., Formas, R., Gerson, H. (2010): Calyptocephalella gayi. su Introducción en Chile, p. 49 –65. Solís, R., Lobos, G., Iriarte, The IUCN, Red list of threatened species. Version 2010.3. <www. A., Eds., Santiago, Chile, Servicio Agrícola y Ganadero and iucnredlist.org>. Accessed on 20 July 2016. Universidad de Chile. Weldon, C., De Villiers, A., Preez, D. (2007): Quantification of the Lobos, G., Jaksic, F.M. (2005): The ongoing invasion of the African trade in Xenopus laevis from South Africa, with implications for clawed frog (Xenopus laevis) in Chile, causes of concern. biodiversity conservation. African Journal of Herpetology 56: Biodiversity and Conservation 14: 429–439. 77–3. Lobos, G. (2012): Estatus de la invasión del sapo africano Xenopus laevis en Chile. In: Conservación de Anfibios de Chile, p. 49–54. Soto–Azat,– C., Valenzuela-Sánchez, A., Eds., Santiago, Chile, Universidad Nacional Andrés Bello.
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