Herpetology Notes, volume 13: 641-644 (2020) (published online on 05 August 2020)

Predation on Colombian Endemic Frog Rheobates palmatus (Werner, 1899) (Anura: Aromobatidae) by the Terciopelo Viper Bothrops asper (Garman, 1884) (Squamata: Viperidae)

Cristhian Londoño-Quiceno1,*, Sergio Escobar-Lasso1, Juan Camilo Zuluaga-Isaza1, and Luis Santiago Caicedo-Martínez1

Understanding the inter-individual, inter-species, and Eastern hillside of the Central mountain range, Norcasia inter-trophic level interactions in which amphibians municipality, Caldas department, Colombia. participate is crucial to recognise their role within natural The Palm Rocket Frog R. palmatus (Werner, 1899), ecosystems and to carry out accurately conservation and is endemic to Colombia, distributed in the Central and management programs (Wells, 2010; Zipkin et al., 2020). Eastern mountain ranges, in the inter-Andean river Amphibians are one of the few groups of vertebrates that valley of Magdalena, in the Caribbean region, and in are capable of link trophic webs in terrestrial and aquatic the La Macarena high hill from 350 to 2520 m (Jerez ecosystems since they play a vital role both as predators and Yara-Contreras, 2018; Acosta-Galvis, 2019; IUCN, and as prey (Wells, 2010). Predation is an important 2019). The Palm Rocket Frog is a diurnal species with ecological phenomenon that allows the understanding semi-aquatic habits, considered as being fast frogs of amphibians’ defensive strategies (Escobar-Lasso and during daytime, when they are actively foraging (IUCN, González-Duran, 2012) regarding the morphology and 2019). They are commonly found diving and swimming ecology of each animal (Greene, 1988). This process in rocky creeks and small puddles or perched on nearby is divided into six phases: localisation, identification, rocks (Marín-Martínez and Rojas-Morales, 2016: approach, subjugation, ingestion, and digestion (Toledo IUCN, 2019). These frogs are much less active at night, et al., 2011). when they are hidden under the leaf litter, rock crevices, During the last years, frog species have suffered severe or inside small cave-like structures (Lüddecke, 1999). declines, mainly in the tropic ecosystems (Becker et During herpetological surveys conducted on 22 al., 2007). Since the abundance of frogs in the tropics January, 2020 at a creek known locally as Soto, Norcasia is quite high, the decline of their populations has been municipality, Caldas department, Eastern hillside of documented to produce a “coextinction” cascade effect the Central mountain range, Colombia (5.5769°N, in other taxa, primarily snakes (Zipkin et al., 2020). To -74.9413°W, 630 m; WGS84), a juvenile of Terciopelo understand the population declines of endangered and Viper Bothrops asper (Viperidae) was observed feeding endemic frog species, it is essential to know their role in on a post-metamorphic individual of Palm Rocket Frog the food webs of the ecosystems in which they inhabit R. palmatus (Aromobatidae) at 10:00 h. The predation (Blanco-Torres et al., 2020a,b). Therefore, the aim of event took place on a rock located at 35 cm from the this work is to describe for the first time the predation edge of the creek, which is surrounded by a fragment of event on the Colombian endemic frog Rheobates tropical rain forest (Fig. 1A). The predation event was palmatus by the Terciopelo viper Bothrops asper, in the observed when the snake had already ingested half of the frog’s body (Fig. 1B). The localisation, identification, approach, and subjugation phases were not observed throughout the predation event. The taxonomic identity of the prey was possible by a careful observation of the frog’s body that was outside the snake’s mouth. The 1 Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Caldas, Calle 65 # 26- ingestion process observed lasted for about four minutes 10, A. A. 275, Manizales, Colombia. (Fig. 1B-F) and the snake remained motionless once the * Corresponding author. E-mail: [email protected] ingestion process finished (Fig. 1G). 642 Cristhian Londoño-Quiceno et al.

Figure 1. Predation on the Colombian Endemic Frog Rheobates palmatus by the Terciopelo Viper Bothrops asper in the Eastern hillside of the Central mountain range, Norcasia municipality, Caldas department, Colombia. (A) Habitat where the predation event was recorded, the red arrow indicates where the snake was located. (B) Start of the ingestion process. (C-F) Ingestion process. (G) End of ingestion and start of the digestion process. Photographs: Juan Camilo Zuluaga Isaza. Predation on Colombian Endemic Frog Rheobates palmatus by the Terciopelo Viper 643

The Terciopelo Viper B. asper (Garman, 1884), is Acknowledgments. We especially thank to the research agreement distributed from Mexico throughout Central America between Caldas University (VIP Code: 201010027713) and to the north of South America, found from sea level to ISAGEN S.A. E.S.P. (Agreement number 33/45) for funding the research project “Monitoring of the wild vertebrate fauna in the 1975 m (Sasa et al., 2009; Díaz-Ricaurte et al., 2018). areas of influence of productive centres of ISAGEN in the East of In Colombia, the species is found in the sub-Andean the Department of Caldas”. forest, in the dry forest of the Caribbean region, in the rain forest of the Pacific region and, in the inter- References Andean valleys of Cauca and Magdalena rivers (Díaz- Acosta Galvis, A.R. (2019): Lista de los Anfibios de Colombia. Ricaurte et al., 2018). The Terciopelo Viper prefers wet Available at: http://www.batrachia.com Accessed on 17 March environments and is present in a wide range of habitats 2020). and life zones with different degrees of intervention Becker, C.G., Fonseca, C.R., Haddad, C.F.B., Batista, R.F., Prado, (Greene and Campbell, 1992). The species seems to be P.I. (2007): Habitat split and the global decline of amphibians. opportunistic, due to it exhibits great plasticity in the use Science 318: 1775–1777. of prey resources (Sasa et al., 2009), consuming preys Blanco-Torres, A., Bonilla, M.A., Cagnolo, L. (2020a): Habitat modification effects on anuran food webs in the Colombian as centipedes, lizards, snakes, fishes, rodents, birds, and tropical dry forest. Food Webs 22: e00133. anurans (Sasa et al., 2009). The species is usually more Blanco-Torres. A., Duré, M.I., Bonilla, M.A., Cagnolo, L. (2020b): active at night than during the daytime; however, during Predator–prey interactions in anurans of the tropical dry forests the day they can exit of their refuge and assume a “sit- of the Colombian Caribbean: A functional approach. Biotropica and-wait” ambush posture that is characteristic of many 00: 1–8. vipers (Greene and Campbell, 1992). Bothrops asper Boada, C., Salazar, D., Lascano, A.F., Kuch, U. (2005): The diet of Bothrops asper (Garman, 1884) in the Pacific lowlands of has been recorded preying upon eleven anuran species: Ecuador. Herpetozoa 18: 77–79. Rhinella horribilis, Craugastor fitzingeri, Leptodactylus Díaz-Ricaurte, J.C., Cubides-Cubillos, S.D., Ferreto, B. (2018): savage, L. bolivianus, Lithobates forreri, L. vaillanti, Bothrops asper (Garman, 1884). Catálogo de anfibios y reptiles L. warzewitzchi, Eleutherodactylus sp. Pristimantis de Colombia 4: 8–22. achatinus, Smilisca phaeota, S. sordida (Greene, 1997; Escobar-Lasso, S., González-Duran, G.A. (2012): Strategies employed by three Neotropical frogs (Amphibia: Anura) to Boada et al., 2005; Sasa et al., 2009; Toledo et al., avoid predation. Herpetology Notes 5: 79–84. 2007). Therefore, the predation event over R. palmatus Greene, H.W. (1988): Antipredator mechanisms in reptiles. Biology is considered a new prey item in the diet of B. asper. of the Reptilia 16: 1–152. Anurans are preyed upon by different species of Greene, H.W. (1997): Snakes: The Evolution of Mystery in Nature. vertebrates. In reptiles, there are records of predation Berkeley: University of California Press. by crocodilian, lizards, snakes, and turtles (Toledo et Greene, H.W., Campbell, J.A. (1992): The future of pitvipers. In: Biology of the Pit Vipers, p 421–427. Campbell, J.A., Brodie, al., 2007). Compared with all other vertebrate groups, E.D. Eds., Selva, Tyler. snakes are the main predators of anurans, as is referred IUCN SSC Amphibian Specialist Group. (2019): Rheobates to in about 45% of the reports of predation (Toledo et al., palmatus. The IUCN Red List of Threatened Species 2019. 2007). To date, there are reports of only two predators Available at: http://dx.doi.org/10.2305/IUCN.UK.2019- of post-metamorphic individuals of R. palmatus, being 3.RLTS.T55124A85893845.en. Accesses on 17 March 2020. both invertebrates: a mygalomorphic spider Xenesthis Jerez, A., Yara-Contreras, C. (2018). Rheobates palmatus (Werner, 1899) Catálogo de Anfibios y Reptiles de Colombia 4: 68–68. immanis (Marín-Martínez and Rojas-Morales, 2016), Lüddecke, H. (1999): Behavioral aspects of the reproductive and a Whip-Spider Heterophrynus sp. (Zuluaga-Isaza et biology of the Andean frog Colostethus palmatus (Anura: al., 2020). Hence, this work discloses the third known Dendrobatidae). Revista de la Academia Colombiana de predator for R. palmatus. Moreover, this work discloses Ciencias Exactas, Físicas y Naturales 23: 303–316. the first known record of a vertebrate predating upon R. Marín-Martínez, M., Rojas-Morales, J.A. (2016): Predation palmatus. Predators of eggs, tadpoles and metamorphic by a mygalomorphic spider Xenesthis immanis (Araneae: Theraphosidae) on a stream-dwelling frog, Rheobates palmatus individuals of R. palmatus are still unknown. Surely, (Anura: Aromobatidae). IRCF Reptiles and Amphibians 23: however, each of the larval stages of the species is 175–177. involved in a complex trophic web that needs to be Sasa, M., Wasko, D.K., Lamar, W.W. (2009): Natural history of the untangled to carry out accurately conservation and Terciopelo Bothrops asper (Serpentes: Viperidae) in Costa Rica. management plans for the species. Toxicon 54: 904–922. Toledo, L.F., Ribeiro, R.S., Haddad, C.F. (2007): Anurans as prey: an exploratory analysis and size relationships between predators 644 Cristhian Londoño-Quiceno et al.

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Accepted by Clarissa Canedo