Philander Opossum) Predation on a Coral Snake (Micrurus Nigrocinctus

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Mammalia 72 (2008): 350–351 2008 by Walter de Gruyter • Berlin • New York. DOI 10.1515/MAMM.2008.031

Short Note

Four-eyed opossum (Philander opossum) predation on a coral snake (Micrurus nigrocinctus)

Mario J. Go´mez-Martıńez1,*, Allan Gutierrez2 P. opossum eating coral snakes or other venomous and Fabrice DeClerck1 species. Micrurus nigrocinctus is a medium-sized coral snake 1 Department of Agriculture and Agroforestry, with females attaining a maximum length of 1150 mm CATIE 7170, Turrialba, Costa Rica, and males between 500 and 750 mm. According to e-mail: [email protected] Savage (2002), the species is common in lowland and 2 Programa de Biologıá, Universidad Nacional premontane forests, in pastures, coffee farms and urban Autońoma de Nicaragua, Managua, Nicaragua gardens. *Corresponding author The observation documented here was made in June 2007 in a riparian forest fragment in a pasture dominated landscape of Matigua´s, Nicaragua (128 539 250 N858 169 380 W). The site is a heavily fragmented landscape where Keywords: Bothrops; human-dominated landscape; only 14% of the original forest cover remains (Useche neurotoxin; Nicaragua; pasture; riparian. 2007); however, these forest fragments remain heavily connected via a complex system of riparian forests, live fences, and pastures with high tree densities ()35 individuals ha-1). Our observation took place while conduct- The four-eyed opossum (Philander opossum) is a Neo- ing a survey of reptiles and amphibians of forested and tropical marsupial that ranges from east-central Mexico non-forested riparian corridors bordered by pastures with to northeastern Argentina (Castro-Arellano et al. 2000). P. high and low tree densities. Throughout this study, con- opossum has been registered in every country of Central ducted from March to August of 2007, a total of 18 snake America, where it inhabits tropical evergreen forests and species and 31 individuals, including two species of false secondary growth, but it has also been observed in crop- coral snakes (Erythrolamprus mimus and Pliocercus lands. The species is terrestrial and is most commonly euryzonus) and a single species of true coral snake found near streams or moist areas (Reid 1998). The spe- (Micrurus nigrocinctus) were observed. Two individuals of cies predominantly forages on the ground and middle E. mimus, one individual of P. euryzonus, and three indi- canopy layers (Handley 1976). P. opossum is agile and viduals of M. nigrocinctus were observed during 600 h quick; some authors have stated that it appears more of sampling effort along 30 km of transect. Out of the six alert than other didelphids (Nowak 1991). Depending on individuals, five were found in riparian forests regardless the reference, the species is reported as primarily carni- of whether the adjacent pasture had high tree cover or vorous (Emmons and Feer 1990), omnivorous (Hershko- not. One individual of E. mimus was found 5 m from the vitz 1997) and frugivorous-insectivorous (Atramentowicz streambed in a pasture with high tree density, and refers 1986). Castro-Arellano et al. (2000) report a variety of to the case documented here. food items forming its diet, including fruit, corn, nectar, frogs, small mammals, reptiles, amphibians, birds and On June 4th 2007 at 19:00 h, we began a 50-m tran- their eggs, insects, crustaceans, snails, earthworms and sect in a riparian forest with an adjacent pasture of low carrion. tree density. We initiated our transect searching for Castro-Arellano et al. (2000) provide the most recent amphibians and reptiles when we observed a P. opossum and complete review of P. opossum ecology, behavior 4 m to the side of the transect, raking leaves, turning over and natural history, but do not refer to the species con- logs and stones searching for prey. The opossum con- suming venomous species, nor do the authors make any tinued down the stream where we lost sight of it. We references to interactions between P. opossum and ven- sighted the opossum 10 min later approximately 4 m omous snakes. However, resistance of South and Central from the riverbank. At this time, we observed the opos- American marsupials against viper venoms, especially sum removing leaf litter and excavating a small hole from from the genus Bothrops, the genus responsible for the which the tail of a coral snake (M. nigrocinctus) was pro- greatest number of snakebite fatalities regionally, has truding. The opossum began to pull the snake from the been recorded by Jurgilas et al. (2003) who isolated a hole, biting it along the full length of its body and grasp- snake venom metalloproteinase inhibitor from P. opos- ing it with its claws (Figure 1). As we approached and sum serum. However, the venom used was from B. jara- began to take photos, the opossum became momentarily raca whose venom is hemorrhagic, in contrast to the distracted and lost grasp of the still living coral that neurotoxic venom of Micrurus. No references regarding momentarily escaped into the hole. The opossum man- resistance of P. opossum to Micrurus venom has been aged to recapture the coral before it had completely found. Nor were we able to find reports referring to escaped and continued to withdraw the coral from the

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M.J. Go´mez-Martı´nez et al.: Four-eyed opossum predation on a coral snake 351

ground, and retreated upslope for a couple of meters. We left the snake in place and continued the transect. The total observation time from the second sighting of the opossum until its departure was less than 15 min. There are no known reports of P. opossum predation on coral snakes. However, there is a report of Didelphis albiventris predation on the pitviper B. jararaca in captiv- ity, where the adult and juvenile opossums were observed killing and ingesting the snakes after biting them in the head and neck region (Oliveira and Santori 1999). Because the opossum became tired of our pres- ence, we were unable to observe whether its killing of the snake was for consumption, or to possibly maintain a nesting area free of potential threat to its young, though we assume the former. The opossum was apparently unconcerned by the warning coloration of the coral. Figure 1 Philander opossum individual removing a coral snake Jurgilas et al. (2003) noted that the species is immune from a streamside burrow in a pasture dominated landscape of to the hemotoxin of Bothrops, which begs the question Matigua´s, Nicaragua. whether the species is also immune to the neurotoxins of Micrurus, or whether it relies primarily on its agility to hole, biting it as it removed it, and placing it to the side. avoid being bitten? Once the snake was fully extracted, the opossum bit the snake and quickly hopped to a new position in an appar- ent evasive measure to avoid the snake’s head. At this Acknowledgements point the snake was still alive, though its movements were slower, probably severely wounded. The snake did Funding for the research cited in this article came from a gen- continue to attempt escape. The opossum moved the erous grant from the World Bank-Bank Netherlands Partnership snake down slope towards the streambed. By the time Program ‘‘The impact of improved cattle management practices we were able to catch up with the opossum, the snake on biodiversity conservation’’. had been killed. During our observation time, we never saw the opossum being bit by the snake despite at least two attempted strikes, nor did we see the opossum bite References the snake’s head. We took a final photo (Figure 2) show- ing the opossum with the snake. Judging by the esti- Atramentowicz, M. 1986. Dynamique de population chez trois mated 110 cm estimated length of the coral and marsupiaux, didelphides de Guyane. Biotropica 18: 136–149. indications by Savage (2002) that males of the species Castro-Arellano, C., H. Zarza and R.A. Medellı´n.2000. Philander attain lengths between 500 and 750 mm, we concluded opossum. Mammal. Spec. 638: 1–8. that this individual was an adult female. The opossum Emmons, L.H. and D.E. Feer. 1990. Neotropical rainforest moved into the dry streambed where it disappeared for mammals. A field guide. The University of Chicago Press, Chicago, IL. 298 pp. approximately 3 min. When we were able to see the Handley, C.O. 1976. Mammals of the Smithsonian Venezuelan opossum for a final time, the snake’s head had been project. Brigham Young Univ. Sci. Bull., Biol. Ser. 20: 1–91. removed. At this time, the opossum left the snake on the Hershkovitz, P. 1997. Composition of the family Didelphidae morphology and behavior of the included four-eyed pouched opossums of the genus Philander Tiedemann, 1808. Fieldia- na: Zool., New Ser. 86: 1–103. Jurgilas, P.B., A.G.C. Neves-Ferreira, G.B. Domont and J. Perales. 2003. PO41, a snake venom metalloproteinase inhibitor isolated from Philander opossum serum. Toxicon 42: 621–628. Nowak, R.M. 1991. Walker’s mammals of the world, 5th ed. Johns Hopkins University Press, Baltimore, MD. 642 pp. Oliveira, M.E. and R.T. Santori. 1999. Predatory behavior of the opossum Didelphis albiventris on the pitviper Bothrops jararaca. Stud. Neotrop. Fauna Environm. 34: 72–75. Reid, F. 1998. A field guide to the mammals of Central America and southeast Mexico. Oxford University Press, Oxford. 334 pp. Savage, J.M. 2002. The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. The University of Chicago Press, Chicago, IL. 954 pp. Useche, D.C. 2007. Diseno de redes de conectiviad para la conservacion y restauracion del paisaje en Nicaragua, Cen- Figure 2 Parting shot as Philander opossum prepares to leave troamerica. CATIE Master’s Thesis. Tropical Agricultural with its kill. In this photo the Micrurus nigrocinctus has been Research and Higher Education Center, Turrialba, Costa dispatched. Rica. 233 pp.