first report of predation by calyptocephalella gayi upon

3
The helmeted water toad, Calyptocephalella gayi (Duméril & Bibron, 1841), is a species endemic to Chile and found in lakes, streams, and rivers from Coquimbo to the Los Lagos region (Correa et al., 2011). It is a big and robust anuran that can reach a weight of 1.2 Kg and 30 cm of snout-vent length (SVL) (Lobos et al., 2013). Currently, it is classified as Vulnerable by the IUCN (Veloso et al., 2010), and the major threats that the species faces are the habitat loss, diseases, climate change and its overexploitation (Vélez, 2014). For many years, it was collected for human consumption and for physiological experimentation (Hermosilla and Acuña, 2004). Due to the increased overexploitation, Chile prohibited its capture (Vallejos and Pizarro, 2004), and it is a protected species in Chile since 1988 (Glade, 1983). In addition, some conservation measures were established, such as the development of legal farming to supply the local demands of the gastronomic market. In 2009 an ex-situ conservation program was started to gather information on the biology and reproduction of this species, for successful and sustainable farming (Vélez and Acuña, 2012). Unfortunately, illegal hunting continues. One important source of diseases potentially affecting C. gayi comes from its sympatric occurrence with the African clawed frog, Xenopus laevis, one of the worst alien species in the world (Lowe et al., 2000), presently worldwide distributed (Tinsley et al., 2015). This species is considered a threat for native amphibians, because it acts as a biological vector of infectious diseases such as the chytrid fungus, Batrachochytrium dendrobatidis (Weldon et al., 2007), and parasites (Kupermann et al., 2004). Moreover, available data indicate that native frog species decline when sharing microhabitat with X. laevis (Lillo et al., 2011). In Chile, Solís et al. (2010) reported the presence of the chytrid fungus in feral populations of X. laevis, and Lobos et al. (2013) indicated that X. laevis is a potential predator of native amphibian larvae, which may reduce the population sizes of C. gayi. The African clawed frog was introduced in Chile around 1970 to be used in pregnancy test, but also became part of pet trade. Some individuals were released into nature, and the species became quickly established and dispersed very rapidly (Lobos et al., 2013). In fact, since the first reported wild population of X. laevis in 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 km 2 , from Coquimbo to the O’Higgins region (Lobos et al., 2013). The scarce information available on the natural history of C. gayi, motivated us to start a monitoring program for this species with the aim to obtain relevant knowledge to improve the conditions for this species and reduce its vulnerability. Our study is carried out in an estuary of central Chile, at Villa Alemana, Valparaíso region, Chile (19S 277786E and 6341650S), which has a Mediterranean climate. The catchment basins where C. gayi inhabits are also 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 Mora 1, 2, *, Javiera Constanzo-Chávez 1 , Juan Contardo 2 and Antonieta Labra 1,3,4 1 ONG Vida Nativa, Santiago, Chile. 2 Programa de Magíster en Áreas Silvestres y Conservación de la Naturaleza, Universidad de Chile, Santiago, Chile. 3 Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Casilla 70005, Correo 7, Santiago, Chile. 4 Department of Biosciences, Centre for Ecological and Evolutionary Synthesis. University of Oslo, P.O.Box 1066 Blinder, N-0316, Oslo, Norway. * Corresponding author e-mail: [email protected]

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Page 1: First report of predation by Calyptocephalella gayi upon

The helmeted water toad, Calyptocephalella gayi (Duméril & Bibron, 1841), is a species endemic to Chile and found in lakes, streams, and rivers from Coquimbo to the Los Lagos region (Correa et al., 2011). It is a big and robust anuran that can reach a weight of 1.2 Kg and 30 cm of snout-vent length (SVL) (Lobos et al., 2013). Currently, it is classified as Vulnerable by the IUCN (Veloso et al., 2010), and the major threats that the species faces are the habitat loss, diseases, climate change and its overexploitation (Vélez, 2014). For many years, it was collected for human consumption and for physiological experimentation (Hermosilla and Acuña, 2004). Due to the increased overexploitation, Chile prohibited its capture (Vallejos and Pizarro, 2004), and it is a protected species in Chile since 1988 (Glade, 1983). In addition, some conservation measures were established, such as the development of legal farming to supply the local demands of the gastronomic market. In 2009 an ex-situ conservation program was started to gather information on the biology and reproduction of this species, for successful and sustainable farming (Vélez and Acuña, 2012). Unfortunately, illegal hunting continues.

One important source of diseases potentially affecting C. gayi comes from its sympatric occurrence with the African clawed frog, Xenopus laevis, one of the worst alien species in the world (Lowe et al., 2000), presently worldwide distributed (Tinsley et al., 2015). This species is considered a threat for native amphibians, because it acts as a biological vector of infectious diseases such as the chytrid fungus, Batrachochytrium dendrobatidis (Weldon et al., 2007), and parasites (Kupermann et al., 2004). Moreover, available data indicate that native frog species decline when sharing microhabitat with X. laevis (Lillo et al., 2011). In Chile, Solís et al. (2010) reported the presence of the chytrid fungus in feral populations of X. laevis, and Lobos et al. (2013) indicated that X. laevis is a potential predator of native amphibian larvae, which may reduce the population sizes of C. gayi. The African clawed frog was introduced in Chile around 1970 to be used in pregnancy test, but also became part of pet trade. Some individuals were released into nature, and the species became quickly established and dispersed very rapidly (Lobos et al., 2013). In fact, since the first reported wild population of X. laevis in 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).

The scarce information available on the natural history of C. gayi, motivated us to start a monitoring program for this species with the aim to obtain relevant knowledge to improve the conditions for this species and reduce its vulnerability.

Our study is carried out in an estuary of central Chile, at Villa Alemana, Valparaíso region, Chile (19S 277786E and 6341650S), which has a Mediterranean climate. The catchment basins where C. gayi inhabits are also

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

1 ONG Vida Nativa, Santiago, Chile.2 Programa de Magíster en Áreas Silvestres y Conservación de

la Naturaleza, Universidad de Chile, Santiago, Chile.3 Instituto de Ciencias Biomédicas, Facultad de Medicina,

Universidad de Chile, Casilla 70005, Correo 7, Santiago, Chile.

4 Department of Biosciences, Centre for Ecological and Evolutionary Synthesis. University of Oslo, P.O.Box 1066 Blinder, N-0316, Oslo, Norway.

* Corresponding author e-mail: [email protected]

Page 2: First report of predation by Calyptocephalella gayi upon

Marta Mora et al.172

home to the native amphibian species Pleurodema thaul, the invasive frog Xenopus laevis, an endemic fish Cheirodon pisiculus and one exotic fish Gambusia affinis. Individuals of C. gayi were collected with dip nets, and then measured, photographed, stomach flushed, marked with a nano chip (Trovan ®Nano transponder ID100), and then released at the collecting point, which is georeferenced. On 28 April 2016 at 11:30 h, we captured an adult of C. gayi (18 cm SVL, 536 gr of weight) with a live adult of X. laevis (4 cm SVL, 13 gr of weight) in its mouth (Fig. 1).

It was previously reported that X. laevis can exhibit skin secretions as antipredator mechanism that induce, at least in some snake species, an involuntary oral dyskinesia that allows the frog to escape from the predator (Barthalmus and Zielinski, 1988; Barthalmus, 1989). We did not notice any similar effect in the individual of C. gayi, which suggests that, if present, this antipredatory mechanism may not be effective with all predators.

This is the first report of C. gayi eating X. laevis, and therefore, it is unclear how frequent X. laevis is part of C. gayi diet. However, by considering that this species has a voracious appetite (Cei, 1962), it is likely that X. laevis may constitute a common prey of this frog, particularly considering that X. laevis can reach high densities of 0,51 ind/m2 (Ross et al., 2015). Moreover, close to our study site, the densities of X. laevis can reach up to ~14 ind/m2 (Mora et al. unpubl. data). Potentially, the high densities of X. laevis may determine that C. gayi switches its

diet to consume this common prey. Moreover, Rivero (2010) determined that under experimental conditions adults of C. gayi fed X. laevis larvae grew and increased in weight.

Presently, data on the prevalence of B. dendrobatidis, an important cause of amphibians mortality (Pasmans et al., 2000), in X. laevis show that it is higher in Chile than in populations from other regions, such as those from Africa (24% vs. 2.7%, respectively; Solís et al., 2010). Under this context, the fact that C. gayi includes X. laevis in its diet might result in an easy infection with this fungus by direct contact (Piotrowski et al., 2004). Therefore, it is highly relevant to keep monitoring C. gayi in this area of study, controlling the presence of X. laevis and testing for the presence of emerging diseases.

Acknowledgement The study was authorized by the Servicio Agrícola y Ganadero (Resolution No. 1790/2016). We thank Hendrik Müller for pre-reviewing the manuscript.

References

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Fig. 1. Calyptocephalella gayi with an African clawed frog in its mouth. A. Side view, B. Dorsal view. Photographs by Marta Mora.

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Accepted by Hendrik Müller