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Parasitising the Texas Indigo Snake Drymarchon Melanurus Erebennus (Cope, 1861) in Nuevo Leon and Tamaulipas, Northeast Mexico

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Parasitising the Texas Indigo Snake Drymarchon Melanurus Erebennus (Cope, 1861) in Nuevo Leon and Tamaulipas, Northeast Mexico Herpetology Notes, volume 14: 765-767 (2021) (published online on 10 May 2021) A new record of the tongue worm Kiricephalus coarctatus (Diesing, 1850) parasitising the Texas indigo snake Drymarchon melanurus erebennus (Cope, 1861) in Nuevo Leon and Tamaulipas, northeast Mexico Manuel de Luna1, Roberto García-Barrios1, Daniel Montoya-Ferrer1, and Gerardo Cuéllar-Rodríguez1,* Central American Indigo Snakes Drymarchon parasites: flukes (Platyhelminthes: Trematoda; 16 adults melanurus (Duméril, Bibron & Duméril, 1854) are in the mouth and throat area), spiny headed worms diurnal colubrids that inhabit the American continent (Acanthocephala; around 300 cystacanths were found from southern Texas (USA) in the Atlantic versant, and embedded in the tissue of the caudal area), and tongue southern Sonora (Mexico) in the Pacific versant, south worms (Pentastomida; 2 adult females were found inside throughout northeastern, western and southern Mexico, the lung). The snake was deposited in the Herpetological Central America, as far south as Venezuela, Ecuador, and Collection of the Facultad de Ciencias Biológicas of extreme northwestern Peru in northern South America the Universidad Autónoma de Nuevo León (UANL) (Wüster et al., 2001; Cisneros-Heredia, 2006; Heimes, and given the voucher #8450, whereas the parasites 2016). There are five recognised subspecies (Uetz et al., were deposited in the Entomology Lab of the Facultad 2019) of which the Texas Indigo Snake Drymarchon de Ciencias Forestales at UANL, the tongue worms in melanurus erebennus (Cope, 1861) is found in Texas in particular were given the voucher FCF-PARAS001. the USA as well as in eastern Coahuila, Nuevo Leon, On 14 August 2020, another adult male D. m. erebennus northern Hidalgo, northern Queretaro, San Luis Potosi, (around 180 cm in total length) was found dead on the Tamaulipas, and northern Veracruz in Mexico (Smith, road near “La Bocatoma” (23.0149ºN, -99.1246ºW; 1941 as Drymarchon corais; Heimes, 2016). WGS 1984) in the municipality of Gómez Farías, state Several species of helminths that use D. melanurus of Tamaulipas, northeast Mexico. The specimen was as a host have been identified, mainly roundworms collected and necropsied. It was found to have mammal (Nematoda) and flukes (Platyhelminthes: Trematoda) hair in its stomach and only hosted tongue worms (Paredes et al., 2008 as D. corais), but also the tongue (Pentastomida) as parasites: one adult female was found worm Railletiella furcocercum (Diesing, 1839) inside the lung, and several infective cysts were found (Pentastomida: Railletiellida: Railletiellidae) (Ali et al., in the stomach lining, but it is unknown if they belong 1984 as D. corais; Paredes et al., 2008 as D. corais). to the same species of tongue worm. The snake and the On 6 August 2018, an adult male D. m. erebennus (233 tongue worms (the adult female and three cysts) were cm in total length) was found dead due to anthropogenic deposited in the aforementioned collections and given causes near “Rancho La Palma” (25.6761ºN, - the voucher #8511 and FCF-PARAS013, respectively. 99.4597ºW; WGS 1984) in the municipality of Los All three adult female tongue worms were identified as Ramones, state of Nuevo Leon, northeast Mexico. The specimen was collected and necropsied. It lacked Kiricephalus coarctatus (Diesing, 1850) (Porocephalida: stomach contents and hosted three different kinds of Porocephalidae): the family was identified using the key present in Brues and Melander (1932), the genus was identified using the keys of Fain (1961) and Self (1969), and finally, the species was identified comparing the 1 Universidad Autónoma de Nuevo León, Manuel L. Barragán specimens with the diagnoses present in Riley and Self Avenue, Ciudad Universitaria, San Nicolás de los Garza, (1980). The tongue worms of the genus Kiricephalus are Nuevo León 66455, México. unusual in that their life cycle involves three vertebrate * Corresponding author. E-mail: [email protected] hosts: an amphibian, lizard or mammal as the first © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. intermediate host, a snake as the second intermediate 766 Manuel de Luna et al. in the state of Nuevo Leon (Paredes et al., 2008). The record for Tamaulipas here described represents a new state record for this species of tongue worm. Acknowledgments. We are very thankful to Jorge Madrazo Fanti who helped us obtaining the second specimen. We also thank the reviewers Katya Ortiz and Sergio Armando Alanís, as well as the anonymous reviewers who contributed to the betterment of this publication. References Ali, J.H., Riley, J., Self, J.T. (1984): A revision of the taxonomy of pentastomid parasites (genus Railletiella Sambon, 1910) from American snakes and amphisbaenians. Systematic Parasitology 6: 87–­97. Bernarde, P. S., Abe, A. S. (2010): Food habits of snakes from Espigão do Oeste, Rondônia, Brazil. Biota Neotropica 10: 167–­173 Brock, A.P., Gallagher, A.E., Walden, H.D.S., Owen, J.L., Dunbar, Figure 1. Female tongue worms Kiricephalus coarctatus M.D., Wamsley, H.L., et al. (2012): Kiricephalus coarctatus found in the lung of an adult male Texas Indigo Snake in an eastern indigo snake (Drymarchon couperi); endoscopic Drymarchon melanurus erebennus from Los Ramones, state removal, identification, and phylogeny. Veterinary Quarterly 32: 107–­112. of Nuevo León, Mexico. Graph paper (millimetres) to provide Brues, C.T., Melander, A.L. (1932): Classification of insects. A key scale. Photo by Manuel de Luna González. to the known families of insects and other terrestrial arthropods. Order Pentastomida. Bulletin of the Museum of Comparative Zoology Harvard College 73: 579–­581. host, and an ophiophagous snake as the definitive host Christoffersen, M.L., De Assis, J.E. (2013): A systematic (Riley and Self, 1980). monograph of the recent Pentastomida, with a compilation of This record expands the knowledge of parasite-host their hosts. Zoologische Mededelingen 87: 1–­206. interaction involving K. coarctatus since it is the first Cisneros-Heredia, D.F. (2006). Reptilia, Colubridae, Drymarchon recorded observation in D. melanurus. Other hosts of melanurus: filling distribution gaps. Check List 2: 20–­21. Cunha, O.R. d., Nascimento, F.P. d. (1978): Ofídios da Amazônia this tongue worm are known (Riley and Self, 1980; X. As cobras de regiâo leste do Pará. Publicacãos Avulsas Museu Rego, 1981; Christoffersen and De Asis, 2014); among Paraense Emílio Goeldi 31: 1–­218. these are the Eastern Indigo Snake Drymarchon couperi Fain, A. (1981): Les pentastomides de l’Afrique Centrale. Annales (Holbrook, 1842) from North America, and the Yellow Musée Royale de l’Afrique Centrale Sciences Zoologiques 92: Tailed Indigo Snake Drymarchon corais (Boie, 1827) 1–­115. from South America (Riley and Self, 1980; Foster et Foster, G.W., Moler, P.E., Kinsella, J.M., Terrell, S.P., Forrester, al., 2000; Brock et al., 2012; Christoffersen and De D.J. (2000): Parasites of eastern indigo snakes (Drymarchon Asis, 2014). These species are known to be generalist corais couperi) from Florida, U.S.A. Comparative Parasitology 67: 124–­128. predators with ophiophagous preferences (Cunha and Hardy, L.M., McDiarmid, R.W. (1969): The amphibians and Nascimento, 1978; Bernarde and Abe, 2010; Prudente et reptiles of Sinaloa, Mexico. University of Kansas Publications, al., 2014). Given that the diet of D. melanurus (Zweifel museum of Natural History 18: 39–­252. and Norris, 1955; Hardy and McDiarmid, 1969; Platt et Heimes, P. (2016): Herpetofauna Mexicana Vol 1: Snakes of al., 2016) is similar to those of D. corais and D. couperi, Mexico. Edition Chimaira, Frankfurt. it is not surprising that K. coarctatus is found in all three Paredes-León, R., García-Prieto, L., Guzmán-Cornejo, C., León- species. Règagnon, V., Pérez, T.M. (2008): Metazoan parasites of Kiricephalus coarctatus has been reported previously Mexican amphibians and reptiles. Zootaxa 1904: 1–­166. Platt, S.G., Rainwater, T.R., Meerman, J.C., Miller, S.M. (2016): in Mexico parasitising the snakes Pituophis deppei Notes on the diet, foraging behavior, and venom of some snakes (Duméril, 1853), Coluber constrictor Linnaeus, 1758 in Belize. Mesoamerican Herpetology 3: 162–­170. and Micrurus sp. (as Micrurus fulvius) in the state of Prudente, A.L. d. C., Menks, A.C., da Silva, F.M., Maschio, G.F. Estado de Mexico, as well as Pantherophis emoryi (2014): Diet and reproduction of the western indigo snake (Baird and Girard, 1853) (as Pantherophis guttatus) Drymarchon corais (Serpentes: Colubridae) from the Brazilian A new record of Kiricephalus coarctatus parasitising the Texas indigo snake 767 Amazon. Herpetology Notes 7: 99–­108. Rego, A.A. (1981): Notas sobre alguns pentastomídeos de répteis. Memorias do Instituto Oswaldo Cruz 44: 233–­238. Riley, J., Self, J.T. (1980): On the systematics and life-cycle of the pentastomid genus Kiricephalus Sambon, 1922 with description of three new species. Systematic Parasitology 1: 127–­140. Self, J.T. (1969): Biological relationships of the Pentastomida; a bibliography on the Pentastomida. Experimental Parasitology 24: 63–­119. Smith, H.M. (1941): A review of the subspecies of the indigo snake (Drymarchon corais). Journal of the Washington Academy of Sciences 31: 466–­481. Stevenson, D.J., Dyer, K.J., Willis-Stevenson, B.A. (2003): Survey and monitoring of the eastern indigo snake in Georgia. Southeastern Naturalist 16: 393–­408. Uetz, P., Freed, P., Hošek, J. (2019): The Reptile Database, available at www.reptiledatabase.org. Accessed 25 April 2020. Wüster, W., Yrausquin, J.L., Mijares-Urrutia, A. (2001): A new species of indigo snake from north-western Venezuela (Serpentes: Colubridae: Drymarchon). The Herpetological Journal 11: 157–­165. Zweifel, R.G., Norris, K.S. (1955): Contribution to the herpetology of Sonora, Mexico: descriptions of new subspecies of snakes (Micruroides euryxanthus and Lampropeltis getulus) and miscellaneous collecting notes. The American Midland Naturalist 54: 230–­249. Accepted by Andrew Durso.
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