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Notes on the Diet of the Pigmy Coral Snake Micrurus Dissoleucus (Cope, 1860) in Northern Colombia (Serpentes: Elapidae)

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Notes on the Diet of the Pigmy Coral Snake Micrurus Dissoleucus (Cope, 1860) in Northern Colombia (Serpentes: Elapidae) Herpetology Notes, volume 8: 39-41 (2015) (published online on 10 March 2015) Notes on the diet of the Pigmy Coral Snake Micrurus dissoleucus (Cope, 1860) in northern Colombia (Serpentes: Elapidae) Miguel Arévalo-Páez, Andrés Camilo Montes-Correa*, Efraín Rada-Vargas, Liliana Patricia Saboyá-Acosta and Juan Manuel Renjifo Snakes are vertebrates with morphological and Solorzano, 2005). Micrurus venoms are significantly biochemical specializations, such as constriction and more toxic to the preferred prey species than to non- venom injection for the capture and digestion of prey prey species (da Silva and Aird, 2001). However, little is (Hardy, 1994; Hayes and Duvall, 1991). The group known about the feeding ecology of Neotropical Coral also presents some morphological adaptations, such as Snakes, probably because of the burrowing habits of cranial kinesis and expandable skin that allow them to the species, making it difficult to be observed in field swallow preys that are equal to or even larger than their (Cavalcanti et al. 2010). own body size (Greene, 1997). The Pigmy Coral Snake Micrurus dissoleucus Previous observations indicate that some ophidians (Cope, 1860), is the smallest species of the genus (e.g. some species of the genera Agkistrodon, Atractaspis, (250-400 mm SLV), displays a triad-arranged colour Clelia, Cylindrophis, Drymarchon, Lampropeltis, pattern and is distributed throughout Panamá, Chocó, Micrurus, and Ophiophagus) commonly consume other lower Magdalena River, and Caribbean lowlands of snakes (ophiophagy) (Wall, 1921; Evans, 1948; Rose, Colombia and Venezuela up to the Orinoco delta. 1962; Hurter, 1893; Delia, 2009). Some ophiophagus This cryptozoic snake is often found in soils of dry species such as Clelia equatoriana (Amaral, 1924) ecosystems as thornscrub and deciduous tropical forests constrict their prey as a strategy of submission (Rojas- (Roze, 1966, 1996; Campell and Lamar, 1989), and Morales, 2013). Others, such as the coral snakes, are its venom is characterized by a predominant myotoxic highly venomous and subdue their prey by inoculating activity causing damage to the muscle fibers, interfering toxins (Greene, 1984; Gold et al., 2002). neurotransmission (Renjifo et al., 2012). The only prey The New World Coral Snakes are a monophyletic record for the Pigmy Coral Snake is a Cope’s Jungle- group, containing the genera Micrurus, Leptomicrurus, runner Ameiva bifrontata Cope, 1862 (Roze, 1996). and Micruroides (Slowinski, 1995), of which Micrurus is The objective of this study is to provide data on the diet the most diverse with a distribution range from southern of M. dissoleucus based on specimens from Colombia United States of America to northern Argentina. These and, therefore, contribute to the knowledge of its diet snakes are commonly known as ophiophagus (Campbell composition. All specimens listed in this contribution and Lamar, 1989; Roze, 1996). Their diet includes other are deposited in the reptile collection of the Centro snakes, lizards, legless lizards, worm lizards, caecilians de Colecciones Biológicas de la Universidad del and freshwater eels (Cunha and Nascimento, 1978; Magdalena (CBUMAG:REP). Roze, 1983; Greene, 1984; Sazima and Abe, 1991; In May 2013, at the campus of the Universidad del Magdalena, city of Santa Marta, Department of Magdalena, Colombia (11°13’18.31” N, 74°11’08.80 W, 21 m elevation), we collected a dead juvenile female of M. dissoleucus melanogenys (Cope, 1860) (CBUMAG: Grupo de Investigación en Manejo y Conservación de Fauna, REP:00088, total length – TL – without head = 181 mm). Flora y Ecosistemas Estratégicos Neotropicales (MIKU), Reptiles, Universidad del Magdalena, Santa Marta, The coral snake contained in its stomach a Whitenose Colombia. Blind Snake Liotyphlops albirostris (Peters, 1857) * Corresponding author: [email protected] (CBUMAG:REP:00046; SVL=121 mm). The prey 40 Miguel Arévalo et al. Figure 1. Size relationship between the Micrurus dissoleucus (181 mm TL) (CBUMAG:REP:00088) and the Liotyphlops albirostris (121 mm LT) (CBUMAG:REP:00048) (A). M. dissoleucus (CBUMAG:REP:00066) feeding on a Black Blind Snake (B). Phyllodactylus ventralis (CBUMAG:REP:00231) regurgitated by a Micrurus dissoleucus (CBUMAG:REP:00057) (C). Micrurus dissoleucus swallowing a Leptodeira annulata with a size very similar to its own (D). Photos by LP Saboyá-Acosta (A) and JM Renjifo (B, C, D). measured ca. 66% of the predator’s TL (excluding the Leptodeira annulata (Linnaeus, 1758) with a TL very head of the coral snake and the tail of the blind snake) similar to its own (Fig. 1D). (Fig. 1A). Other coral snakes also show snakes or other legless In the same city, in Ziruma hills (11°12’47.37’’ N, animals as common preys. Other ophioform prey items 74°13’7.15’’ W), we collected two specimens of M. (i.e., snakes and amphisbaenians) were previously dissoleucus melanogenys (CBUMAG:REP:00057 and recorded for Micrurus albicintus Amaral, 1925, CBUMAG:REP:00066). The specimen CBUMAG: Micrurus ancoralis Jan, 1872, Micrurus corallinus REP:00066 was photographed while feeding on a Black Merrem, 1820, Micrurus ibiboboca (Merrem, 1820), Blind Snake Epictia goudotii (Duméril and Bibron, Micrurus lemniscatus (Linnaeus, 1758), and Micrurus 1844) (Fig. 1B). Additionally, due to the stress caused by paraensis Cunha and Nascimento, 1973 (Marquez and being transported, the specimen CBUMAG:REP:00057 Sazima, 1997; Martins and Oliveira, 1998; Cisneros- regurgitated a Margarita Leaf-toed Gecko Phyllodactylus Heredia, 2005; Souza et al., 2011; Cavalcanti et al., ventralis (O´Shaughnessy, 1875) (CBUMAG: 2012). The most similar previous record is M. ibiboboca REP:00231; SVL=ca. 50 mm) (Fig. 1C). Finally, eating L. annulata (Cavalcanti et al., 2012). The dietary we observed and photographed in the city of Cúcuta, records of M. dissoleucus suggest that this species Department of Norte de Santander (7°51’36.48”N, can take advantage of several preys available in its 72°31’29.74”W) a non-collected specimen of M. d. microhabitat and that, probably, snakes are common dissoleucus (Cope, 1860) swallowing a Cat-Eyed Snake items in its diet. Notes on the diet of the Pigmy Coral Snake in northern Colombia 41 Acknowledgments. Thanks are due to Fernando Castro-Herrera, Roze, J.A. (1983): New World Coral Snakes (Elapidae): a Camila Renjifo, Victor Acosta-Chavez, and anonymous reviewers taxonomic and biological summary. Memórias do Instituto for their contributions on this manuscript. Butantan 46: 305-338 Roze, J.A. (1996): Coral snakes of the America: Biology, References Identification and Venoms. Florida, Krieger Publishing Company. Campbell, J.A., Lamar, W.W. (1989): The Venomous Reptiles of Sazima, I., Abe, A.S. (1991): Habits of five Brazilian snakes with Latin America. Ithaca, Cornell University Press. coral-snake pattern, including a summary of defensive tactics. Cavalcanti, L.B.Q., Santos-Protázio, A., Albuquerque, R.L., Pedro, Studies on Neotropical Fauna and Environment 26: 159-164. C.K.B., Mesquita, D.O. (2012): Death of a coral snake Micrurus Slowinski, J.B. (1995): A phylogenetic analysis of the New World ibiboboca (Merrem, 1820) (Elapidae) due to failed predation coral snakes (Elapidae: Leptomicrurus, Micruroides, and on bigger prey: a cat-eyed night snake Leptodeira annulata Micrurus) based on allozymic and morphological characters. (Linnaeus, 1758) (Dipsadidae). Herpetology Notes 5: 129-131. Journal of Herpetology 29 (3): 325-338. Cisneros-Heredia, D. F. (2005): Predation upon Amphisbaena Solórzano, A. (2005): A fish prey found in the coral snake Micrurus fuliginosa LINNAEUS, 1758 by Micrurus ancoralis (JAN, alleni (Serpentes: Elapidae) in Costa Rica. Revista de Biología 1872). Herpetozoa 18: 93-94. Tropical 53: 227-228. Cunha, O.R., Nascimento, F.P. (1978): Ofídios da Amazônia. Souza, S.M., Junqueira, A.B., Jakovac, A.C.C., Assunção, P.A., X. As cobras da região leste do Pará. Museu Paraense Emílio Correia, J.A. (2011): Feeding behavior and ophiophagous Goeldi. 31: 1-218. habits of two poorly known Amazonian coral snakes, Micrurus Da Silva, N., Aird, S.D. (2001): Prey especifity, comparative albicinctus Amaral 1926 and Micrurus paraensis Cunha and lethality and compositional differences of coral snakes venoms. Nascimento 1973 (Squamata, Elapidae): Herpetology Notes 4: Comparative Biochemistry and Physiology 128: 425-456. 369-372. Delia, J. (2009): Another crotaline prey item of the Neotropical Wall, F. (1921): Ophidia Taprobanica or the snakes of Ceylon. snake Clelia clelia (Daudin 1803). Herpetology Notes 2: 21-22 Colombo, Cottle, Government Printer. Evans, H.E. (1948): Clearing and staining small vertebrates, in toto, for demonstrating ossification. Turtox News 26: 42–47. Gold, B.S., Dart, R.C., Barish, R.A. (2002): Bites of venomous snakes. New England Journal of Medicine 347: 357-356. Greene, H.W. (1984): Feeding behavior and diet of the eastern coral snake (Micrurus fulvius) in northern peninsular Florida. Herpetologica 37: 213-228. Greene, H.W. 1997 Snakes. The evolution of Mystery in Nature. Berkeley, University of California Press. Hardy, D.L. (1994): A re-evaluation of suffocation as the cause of death during constriction by snakes. Herpetological Review 25: 45-47. Hayes, W. K., Duvall, D. (1991): A field study of prairie rattlesnake predatory strikes. Herpetologica 47:78-81. Hurter, J. (1893): Catalogue of Reptiles and Batrachians found in the Vicinity of St Louis, Missouri. Academy of Science of Saint Louis 6: 251–261 Martins, M., Oliveira, M.E. (1998): Natural history of snakes in forests of the Manaus region. Central Amazonia, Brazil. Herpetological Natural History 6: 78-150. Renjifo, C., Smith, E.N., Hodgson, W.C., Renjifo, J.M., Sánchez A., Acosta, R., Maldonado, J.H., Riveros, A. (2012). Neuromuscular activity of the venoms of the Colombian coral snakes Micrurus dissoleucus and Micrurus mipartitus: An evolutionary perspective. Toxicon 59: 132–142. Rojas-Morales, J.A. (2013): Description of ophiophagy in Clelia equatoriana (Amaral, 1924) (Serpentes: Dipsadidae) in captivity. Herpetology Notes 6: 425-426 Rose, W. (1962): The Reptiles and Amphibians of Southern Africa. Cape Town, Maskew Miller Ltd. Roze, J. A. (1966): La Taxonomía y Zoogeografía de los Ofidios de Venezuela.
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