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Herpetology Notes, volume 12: 1023-1025 (2019) (published online on 23 October 2019)

Predation of Cobra Naja samarensis Peters, 1861 on the invasive Cane Toad Rhinella marina (Linnaeus, 1758) in Davao City,

Denni Dominique A. Ravalo1,#, Jacky Roselle D. Gersava1,#, Jasmin E. Alojado1, Marion John Michael M. Achondo1,2, and Lief Erikson D. Gamalo1,2,*

Naja samarensis Peter, 1861 commonly known as the this species was documented to compete with three “Samar cobra,” is endemic to the Philippine , native frog species in the lowlands (Rana cancrivora, recorded in Dinagat, , , , , Polypedates leucomystax and Kaloula conjuncta Samar, and categorized by the IUCN as Least negrosensis) in terms of breeding sites (Joshi, 2011). Concern (Sy et al., 2009; Leviton et al., 2014; Sanguila It is now widely distributed from to the et al., 2016). This venomous snake is a relatively long of Mindanao (Diesmos et al., 2015). According to species characterized as having dark brown to black Diesmos et al. (2006), this species thrives in degraded back colour with a trace of a light lateral line at least habitats, human-modified environments, agricultural anteriorly below the throat and first five ventrals are plantations and artificial ponds at low elevations. yellow (Leviton et al., 2014). It is common in the Mammals and reptiles (including snakes) prey upon R. country and inhabits a wide range of habitats from marina (Oliveira et al., 2017). However, evidence on tropical moist forest to modified habitats including rice the specific predators of this invasive anuran species fields, pineapple plantations, coconut groves, and rural in the Philippines is limited. One documented case villages from 0 to 800 meters above sea level (Sy et al., was the predation of the invasive toad by an endemic 2009). It is known to feed on small mammals and less crocodile by Groffen et al. (2018). They recorded a frequently on reptiles and frogs (Sen Nag, 2018) but juvenile Crocodylus mindorensis currently, there are no studies of reporting the species Schmidt, 1935 with the R. marina in its mouth. There in feeding poisonous toads such as Rhinella marina was no concrete evidence however, supporting their (Linnaeus, 1758). conclusion on the predation success of the crocodile to In the country, invasive species are a major threat the poisonous toad. The findings were solely based on to native flora and fauna. An example is the most their observation that there was no dead toad nor a dead common invasive anuran- R. marina, humans initially crocodile in the area in the subsequent days. introduced this species to control agricultural pests In this paper, we report the first case of R. marina in the Philippines (Diesmos et al., 2006). However, inside the gut of N. samarensis from Davao City, Philippines. We obtained a dead N. samarensis (snout- vent length = 88 cm), on the premises of Bureau of Plant Industry located in Bago Oshiro, Davao City (7.0795° N, 125.4949° E) killed by security guards on 1 Department of Biological Sciences and Environmental 22 January 2019 at 10:02 PM (Fig. 1A,C). The guards Studies, College of Science and Mathematics, University of killed the venomous snake as a precautionary act in the Philippines Mindanao, Mintal, Tugbok District, Davao case of potential attack. Prior to killing, the guards City, Philippines described the snake as aggressive and does not show 2 Wildlife-Human Interaction Studies, Ecological Research and unusual behaviour and may probably inhabiting patches Biodiversity Conservation Laboratory, University of the of vegetation along the agroecosystem within the area. Philippines Mindanao, Mintal, Tugbok District, Davao City, Philippines After a thorough observation, our team brought the * Corresponding author. E-mail: [email protected] animal to the University of the Philippines Mindanao # DD Ravalo and JR Gersava contributed equally to this work. Zoology Laboratory. The specimen was dissected 1024 Denni Dominique A. Ravalo et al.

Figure 1. A dead Samar cobra (A & C) found in Bureau of Plant Industry located in Bago Oshiro, Davao City. Inside its digestive organ (B) was a partially digested Rhinella marina (Linnaeus, 1758) confirmed by morphological characterization, such as the presence of warts, its colour (D), and measurements.

and the contents of the stomach were examined. The items. This behaviour facilitates the bioregulation of alien digestive organ only contained what evidently was populations and expands the availability of food sources a toad (Fig. 1B), still with discernible characteristics for the native fauna (Goodenough, 2010). In addition, matching R. marina species. Its head was completely the shifting diet preference benefits native prey species. digested, while substantial signs of deterioration were However, this behaviour towards invading species is evident over the body. Fortunately, the body size, limb often futile and detrimental for the predators. Feeding structures, squatty appearance, presence of warts and on R. marina fits within this narrative. When threatened, the markings on the remaining parts of its carcass with the parotid glands of R. marina release bufotoxin, as a measured morphometrics (thigh- 4 cm, tibia- 3.7 cm defence mechanism. Ingestion of this bufotoxin have and forearm length of 2.5 cm) were sufficient to provide been reported in Australia to immediately induce lethal an initial identification (Fig. 1D). These observations effects on snakes, lizards, marsupials, crocodiles, and conform to the description of Alcala (1986) on the R. dogs (Shine, 2010). Powerful chemical defences may marina in the Philippines. deter predators such that R. marina populations are Li et al. (2011) stated that native predators actually capable of increasing populations in an unregulated prefer alien species in their diet over non-alien prey manner. Fortunately, there are predators that are resistant Predation of Samar Cobra on the invasive Cane Toad in Davao City, Philippines 1025 to bufotoxin, including some snake species (Oliveira et Groffen, J., van der Ploeg, J., Telan, S. P., van Weerd, M. al., 2017). The condition of the anuran discovered inside (2018): Rhinella marina. Predation by a Philippine crocodile. the stomach of the found cobra indicates that it had been Herpetological Review 49(3): 520–521. Joshi, R.C. (2011): Invasive alien species (IAS): Concerns and eaten long before the snake died. This finding suggests status in the Philippines. Philippine Rice Research Institute that Samar Cobra is possibly resistant to the bufotoxin (PhilRice) Maligaya, Science City of Muñoz, Nueva Ecija 11: and is, therefore, a possible predator of R. marina in the 1–23. Philippines. Leviton, A.E., Brown, R.M., Siler, C.D., Tashjian, J., Oulehla, M., Voris, H. (2014): The dangerously venomous snakes of the Acknowledgement. We thank the Bureau of Plant Industry, Philippine Archipelago, p. 473–530. California Academy of the Local Government Unit of Bago Oshiro, Davao City, the Sciences, California. Department of Environment and Natural Resources Region XI Li, Y., Ke, Z., Wang, S., Smith, G.R., Liu, X. (2011): An exotic for the support and permission to study, and the Department of species is the favorite prey of a native enemy. PLoS One 6(9): Science and Technology for the scholarship and financial support p.e24299. to D.D. Ravalo. We would also like to acknowledge Prof. Elsa Sen Nag, Oishimaya. (2018): How Many Types of Cobras are May D. Baron for reviewing the paper. There? Which Species Are Most Venomous? Retrieved from https://www.worldatlas.com/articles/how-many-types-of- References cobras-are-there-and-which-species-are-most-venomous.html. Oliveira, S., Silva, D., Fachi, M., Morais, A.R. (2017): Predation on Alcala, A.C. (1986): Guide to Philippine flora and fauna. Vol. X. Rhinella mirandaribeiroi (Gallardo, 1965) (Anura; Bufonidae) Amphibians and reptiles. Natural Resource Management Center, by a snake from Central Brazil. Herpetology Notes 10: 151– Ministry of Natural Resource Management Center, Ministry of 155. Natural Resources and the University of the Philippines, Manila, Sanguila, M.B., Cobb, K.A., Siler, C.D., Diesmos, A.C., Alcala, Philippines, 195. A.C., Brown, R.M. (2016): The amphibians and reptiles of Diesmos, A.C., Diesmos, M.L., Brown, R. (2006): Status and Mindanao Island, southern Philippines, II: the herpetofauna of distribution of alien invasive frogs in the Philippines. Journal of northeast Mindanao and adjacent islands. ZooKeys 624: 1–132. Environmental Science and Management 9(2): 41–53. Shine, R. (2010): The ecological impact of invasive cane toads Diesmos, A.C., Watters, J.L., Huron, N.A., Davis, D.R., Alcala, (Bufo marinus) in Australia. The Quarterly Review of Biology A.C., Crombie, R.I., Afuang, L.E., Gee-Das, G., Sison, R.V., 85(3): 253–291. Sanguila, M.B., Penrod, M.L. (2015): Amphibians of the Sy, E., Custodio, C., Gonzalez, J.C., Delima, E.M. (2009): Naja Philippines, part I: checklist of the species. Proceedings of the samarensis. The IUCN Red List of Threatened Species 2009: California Academy of Sciences 62(20): 457–539. e.T169763A6670726. http://dx.doi.org/10.2305/IUCN.K.2009- Goodenough, A. (2010): Are the ecological impacts of alien species 2.RLTS.T169763A6670726.en misrepresented? A review of the “native good, alien bad” philosophy. Community Ecology 11(1): 13–21.

Accepted by Colin Strine