Understanding the inter-individual, inter-species, and inter-trophic level interactions in which amphibians participate is crucial to recognise their role within natural ecosystems and to carry out accurately conservation and management programs (Wells, 2010; Zipkin et al., 2020). Amphibians are one of the few groups of vertebrates that are capable of link trophic webs in terrestrial and aquatic ecosystems since they play a vital role both as predators and as prey (Wells, 2010). Predation is an important ecological phenomenon that allows the understanding of amphibians’ defensive strategies (Escobar-Lasso and González-Duran, 2012) regarding the morphology and ecology of each animal (Greene, 1988). This process is divided into six phases: localisation, identification, approach, subjugation, ingestion, and digestion (Toledo et al., 2011).

During the last years, frog species have suffered severe declines, mainly in the tropic ecosystems (Becker et al., 2007). Since the abundance of frogs in the tropics is quite high, the decline of their populations has been documented to produce a “coextinction” cascade effect in other taxa, primarily snakes (Zipkin et al., 2020). To understand the population declines of endangered and endemic frog species, it is essential to know their role in the food webs of the ecosystems in which they inhabit (Blanco-Torres et al., 2020a,b). Therefore, the aim of this work is to describe for the first time the predation event 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.

The Palm Rocket Frog R. palmatus (Werner, 1899), is endemic to Colombia, distributed in the Central and Eastern mountain ranges, in the inter-Andean river valley of Magdalena, in the Caribbean region, and in the La Macarena high hill from 350 to 2520 m (Jerez and Yara-Contreras, 2018; Acosta-Galvis, 2019; IUCN, 2019). The Palm Rocket Frog is a diurnal species with semi-aquatic habits, considered as being fast frogs during daytime, when they are actively foraging (IUCN, 2019). They are commonly found diving and swimming in rocky creeks and small puddles or perched on nearby rocks (Marín-Martínez and Rojas-Morales, 2016: IUCN, 2019). These frogs are much less active at night, when they are hidden under the leaf litter, rock crevices, or inside small cave-like structures (Lüddecke, 1999).

During herpetological surveys conducted on 22 January, 2020 at a creek known locally as Soto, Norcasia municipality, Caldas department, Eastern hillside of the Central mountain range, Colombia (5.5769°N, -74.9413°W, 630 m; WGS84), a juvenile of Terciopelo Viper Bothrops asper (Viperidae) was observed feeding on a post-metamorphic individual of Palm Rocket Frog R. palmatus (Aromobatidae) at 10:00 h. The predation event took place on a rock located at 35 cm from the edge of the creek, which is surrounded by a fragment of tropical rain forest (Fig. 1A). The predation event was 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 ingestion process observed lasted for about four minutes (Fig. 1B-F) and the snake remained motionless once the ingestion process finished (Fig. 1G).

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

1 Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Caldas, Calle 65 # 26-10, A. A. 275, Manizales, Colombia.

* Corresponding author. E-mail: cristhian.lq.88@gmail.com

Cristhian Londoño-Quiceno et al.642

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.

The Terciopelo Viper B. asper (Garman, 1884), is distributed from Mexico throughout Central America to the north of South America, found from sea level to 1975 m (Sasa et al., 2009; Díaz-Ricaurte et al., 2018). In Colombia, the species is found in the sub-Andean forest, in the dry forest of the Caribbean region, in the rain forest of the Pacific region and, in the inter-Andean valleys of Cauca and Magdalena rivers (Díaz-Ricaurte et al., 2018). The Terciopelo Viper prefers wet environments and is present in a wide range of habitats and life zones with different degrees of intervention (Greene and Campbell, 1992). The species seems to be opportunistic, due to it exhibits great plasticity in the use of prey resources (Sasa et al., 2009), consuming preys as centipedes, lizards, snakes, fishes, rodents, birds, and anurans (Sasa et al., 2009). The species is usually more active at night than during the daytime; however, during the day they can exit of their refuge and assume a “sit-and-wait” ambush posture that is characteristic of many vipers (Greene and Campbell, 1992). Bothrops asper has been recorded preying upon eleven anuran species: Rhinella horribilis, Craugastor fitzingeri, Leptodactylus savage, L. bolivianus, Lithobates forreri, L. vaillanti, L. warzewitzchi, Eleutherodactylus sp. Pristimantis achatinus, Smilisca phaeota, S. sordida (Greene, 1997; Boada et al., 2005; Sasa et al., 2009; Toledo et al., 2007). Therefore, the predation event over R. palmatus is considered a new prey item in the diet of B. asper.

Anurans are preyed upon by different species of vertebrates. In reptiles, there are records of predation by crocodilian, lizards, snakes, and turtles (Toledo et al., 2007). Compared with all other vertebrate groups, snakes are the main predators of anurans, as is referred to in about 45% of the reports of predation (Toledo et al., 2007). To date, there are reports of only two predators of post-metamorphic individuals of R. palmatus, being both invertebrates: a mygalomorphic spider Xenesthis immanis (Marín-Martínez and Rojas-Morales, 2016), and a Whip-Spider Heterophrynus sp. (Zuluaga-Isaza et al., 2020). Hence, this work discloses the third known predator for R. palmatus. Moreover, this work discloses the first known record of a vertebrate predating upon R. palmatus. Predators of eggs, tadpoles and metamorphic individuals of R. palmatus are still unknown. Surely, however, each of the larval stages of the species is involved in a complex trophic web that needs to be untangled to carry out accurately conservation and management plans for the species.

Acknowledgments. We especially thank to the research agreement between Caldas University (VIP Code: 201010027713) and ISAGEN S.A. E.S.P. (Agreement number 33/45) for funding the research project “Monitoring of the wild vertebrate fauna in the areas of influence of productive centres of ISAGEN in the East of the Department of Caldas”.

References

Acosta Galvis, A.R. (2019): Lista de los Anfibios de Colombia. Available at: http://www.batrachia.com Accessed on 17 March 2020).

Becker, C.G., Fonseca, C.R., Haddad, C.F.B., Batista, R.F., Prado, P.I. (2007): Habitat split and the global decline of amphibians. Science 318: 1775–1777.

Blanco-Torres, A., Bonilla, M.A., Cagnolo, L. (2020a): Habitat modification effects on anuran food webs in the Colombian tropical dry forest. Food Webs 22: e00133.

Blanco-Torres. A., Duré, M.I., Bonilla, M.A., Cagnolo, L. (2020b): Predator–prey interactions in anurans of the tropical dry forests of the Colombian Caribbean: A functional approach. Biotropica 00: 1–8.

Boada, C., Salazar, D., Lascano, A.F., Kuch, U. (2005): The diet of Bothrops asper (Garman, 1884) in the Pacific lowlands of Ecuador. Herpetozoa 18: 77–79.

Díaz-Ricaurte, J.C., Cubides-Cubillos, S.D., Ferreto, B. (2018): Bothrops asper (Garman, 1884). Catálogo de anfibios y reptiles de Colombia 4: 8–22.

Escobar-Lasso, S., González-Duran, G.A. (2012): Strategies employed by three Neotropical frogs (Amphibia: Anura) to avoid predation. Herpetology Notes 5: 79–84.

Greene, H.W. (1988): Antipredator mechanisms in reptiles. Biology of the Reptilia 16: 1–152.

Greene, H.W. (1997): Snakes: The Evolution of Mystery in Nature. Berkeley: University of California Press.

Greene, H.W., Campbell, J.A. (1992): The future of pitvipers. In: Biology of the Pit Vipers, p 421–427. Campbell, J.A., Brodie, E.D. Eds., Selva, Tyler.

IUCN SSC Amphibian Specialist Group. (2019): Rheobates palmatus. The IUCN Red List of Threatened Species 2019. Available at: http://dx.doi.org/10.2305/IUCN.UK.2019- 3.RLTS.T55124A85893845.en. Accesses on 17 March 2020.

Jerez, A., Yara-Contreras, C. (2018). Rheobates palmatus (Werner, 1899) Catálogo de Anfibios y Reptiles de Colombia 4: 68–68.

Lüddecke, H. (1999): Behavioral aspects of the reproductive biology of the Andean frog Colostethus palmatus (Anura: Dendrobatidae). Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales 23: 303–316.

Marín-Martínez, M., Rojas-Morales, J.A. (2016): Predation by a mygalomorphic spider Xenesthis immanis (Araneae: Theraphosidae) on a stream-dwelling frog, Rheobates palmatus (Anura: Aromobatidae). IRCF Reptiles and Amphibians 23: 175–177.

Sasa, M., Wasko, D.K., Lamar, W.W. (2009): Natural history of the Terciopelo Bothrops asper (Serpentes: Viperidae) in Costa Rica. 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

Predation on Colombian Endemic Frog Rheobates palmatus by the Terciopelo Viper 643

and their prey. Journal of Zoology 271: 170–177.Toledo, L.F., Sazima, I., Haddad, C.F. (2011): Behavioural defences

of anurans: an overview. Ethology Ecology and Evolution 23: 1–25.

Wells, K.D. (2010): The ecology and behavior of amphibians. University of Chicago Press.

Zipkin, E.F., DiRenzo, G.V., Ray, J.M., Rossman, S., Lips, K.R. (2020): Tropical snake diversity collapses after widespread amphibian loss. Science 367: 814–816.

Zuluaga-Isaza, J.C., Escobar-Lasso, S., Llanos-Arias, C.A., Londoño, C. (2020): Predation on Colombian Endemic Frog Rheobates palmatus (Werner, 1899) (Anura: Aromobatidae) by a Whip-Spider Heterophrynus sp. (Amblypygi: Phrynidae). Herpetology Notes 13: 231–233.

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Accepted by Clarissa Canedo