Porocephalus crotali (Pentastomida) Parasitizing the Yucatan Neotropical Rattlesnake (Crotalus tzabcan) in the Yucatan Peninsula, Mexico

Author(s): David Gonzlez-Sols and Sergio A. Tern-Jurez Source: The Southwestern Naturalist, 58(2):251-253. 2013. Published By: Southwestern Association of Naturalists DOI: http://dx.doi.org/10.1894/0038-4909-58.2.251 URL: http://www.bioone.org/doi/full/10.1894/0038-4909-58.2.251

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THE SOUTHWESTERN NATURALIST 58(2): 251253

POROCEPHALUS CROTALI (PENTASTOMIDA) PARASITIZING THE YUCATAN NEOTROPICAL RATTLESNAKE (CROTALUS TZABCAN) IN THE YUCATAN PENINSULA, MEXICO
DAVID GONZALEZ -SOL IS* AND -JUAREZ SERGIO A. TERAN

Laboratorio de Necton, El Colegio de la Frontera Sur, Unidad Chetumal, Avenida Centenario Km. 5.5, C.P. 77900, Chetumal, Quintana Roo, Mexico (DGS) Instituto Tecnol ogico de Chetumal. Insurgentes No. 330, Colonia David Gustavo Guti errez, A.P. 267, C.P. 77013, Chetumal, Quintana Roo, Mexico (SATJ) *Correspondent: dgonzale@ecosur.mx

ABSTRACTWe report the rst record of the parasitic pentastomid Porocephalus crotali in the Yucatan neotropical rattlesnake, Crotalus tzabcan, from the Yucatan Peninsula. The species of parasite was described from three males and ve females collected from the lungs of a female rattlesnake killed on Km 260.5 Escarcega-Chetumal highway in January 2007. The parasites harbored similar morphometric values, a mouth as a keyhole situated in the inner hook line, simple internal hooks, and double external hooks, which are consistent with features reported in the original description of P. crotali. The occurrence of P. crotali in the Yucatan neotropical rattlesnake represents new geographical and host records for this species. Porocephalus crotali is one of six species of the genus described from the Americas and is apparently the most widely distributed pentastomid infecting snakes. Moreover, this is the fth record of a porocephalid pentastomid in Mexican snakes. We discussed the zoonotic implications of pentastomes. RESUMENReportamos el primer registro del par asito pentastomido Porocephalus crotali en la serpiente de cascabel de Yucat an, Crotalus tzabcan, en la Pen nsula de Yucat an. La especie de par asito fue descrita a partir de tres machos y cinco hembras colectadas de los pulmones de una hembra muerta por atropellamiento en el km. 260.5 de la carretera Esc arcega-Chetumal, en enero de 2007. Los par asitos presentaron medidas morfom etricas similares, una boca en forma de cerradura situada en la l nea interna de los ganchos, ganchos internos simples, y ganchos externos dobles consistentes con las caracter sticas reportadas en la descripcio n original de P. crotali. La presencia de P. crotali en la serpiente de cascabel de Yucat an representa un nuevo registro geogr a co y de hospedero para esta especie. Porocephalus crotali es una de las seis especies del g enero descritas en Am erica, y aparentemente es el pentast omido m as ampliamente distribuido entre las serpientes. Adem as, representa el quinto registro de un pentast omido porocef alido en serpientes mexicanas. Discutimos las implicaciones zoonoticas de los pentast omidos. Pentastomida is a group of broadly distributed endoparasites that feed on the blood and other tissues of hosts and seriously affect the respiratory tract of reptiles (venomous and constricting snakes, lizards, crocodilians, piscivorous chelonians) in tropical and subtropical regions (Almeida and Christoffersen, 1999; Par e, 2008). Currently, about 131 species have been described, and most of them (70%) use snakes as denitive hosts (Storch, 1993; Almeida and Christoffersen, 1999). The most recent phylogenetic systematization showed that the Class Pentastomida is divided into four orders (Cephalobaenida, Raillietiellida, Reighardiida, and Porocephalida), the latter with two superfamilies (Linguatuloidea and Porocephaloidea) and four families (Linguatulidae, Subtriquetridae, Sebekidae, and Porocephalidae; see Almeida and Christoffersen, 1999). The family Porocephalidae is formed by seven genera, including Porocephalus. This genus is represented by eight species that parasitize snakes, six in the Americas (P. basiliscus, P. clavatus, P. crotali, P. dominicana, P. stilesi, and P. tortuguensis) and two in Africa (P. benoiti and P. subulifer). Recently, a new species from China, P. taiwana, was described based on the morphology of nymphs (Qiu et al., 2005). Porocephalus crotali was originally described from a Venezuelan rattlesnake, Crotalus durissus terricus, by Von Humboldt (1808). Since then, it has been recorded as adults from various North American rattlesnakes (genus Crotalus), cottonmouths, and water moccasins (genus Agkistrodon ), with rodents acting as

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intermediate hosts (Riley and Self, 1979; Par e, 2008). The nymphal stages have been found in a wide variety of mammals (Layne, 1967). Its geographical distribution is related to the home range of its crotalid hosts, which could be from southern Canada to northern Argentina (Riley and Self, 1979), although sanitation of water and food also plays an important role in the spread of this parasite (Drabick, 1987). A total of eight large pentastomids (three males, ve females) was collected from the lungs of a female Yucatan neotropical rattlesnake, Crotalus tzabcan, found dead on a road. The snake was 1,360 mm in total length and 1,200 g in weight and was collected at Km 260.5 EscarcegaChetumal highway in January 2007. The crotalid specimen (skin) was deposited in the Museum of Zoology, El Colegio de la Frontera Sur-Chetumal, Quintana Roo, Mexico (Catalog No. 2730). This species of crotalid is endemic to the southern region of the Yucatan Peninsula, northern Belize, and Guatemala, and its taxonomy was recently partially claried by Wuster et al. (2005). This terrestrial, diurnal, crepuscular or nocturnal species feeds mostly on rodents, lizards, and ground-nesting birds (Klauber, 1956; Campbell, 1998). In recent times, this species has become very rare in several places because people kill them. To date, there are no reports on parasites in this snake. Our survey deals with the occurrence of P. crotali in the Yucatan neotropical rattlesnake in Quintana Roo, Mexico. Two male and two female pentastomids were measured to corroborate the specic identity of the specimens. Males were an average total length of 31.2 0.3 mm with the following dimensions of hooks (sensu Riley, 1981; Buckle et al., 1997): overall length of hook = 332.2 0.2 lm; length of hook from the point at which the blade meets the shank to the tip of the anterior apodeme = 240.3 0.5 lm. Females were 55.5 0.5 mm in average total length; overall length of hook = 501.1 0.2 lm, and length of hook from shank to tip = 317.4 0.1 lm. The measurements of overall length of hook, the presence a mouth as a keyhole situated in the inner hook line, and simple internal hooks and double external hooks are consistent with the description of P. crotali. The specimens were deposited in the collection of the Laboratorio de Zoologia/Universidade Regional do Cariri (LZ URCA; Catalog No. LZ URCA 111, 112, 113, 114, 115, 116, 117, and 118). The occurrence of P. crotali in the Yucatan neotropical rattlesnake represents new geographical (Yucatan Peninsula) and host (C. tzabcan) records for this species. It was previously reported from an undetermined species of rattlesnake from the Gulf of California (Sambon, 1922; Teague-Self and McMurry, 1948) and from Crotalus catalinensis in Baja California Sur (Goldberg et al., 2003). Taking this into account, this is the fth record of a porocephalid pentastomid in Mexican snakes. The following pentastomids and their crotalid host were

already reported: P. tortuguensis in C. tortuguensis from the Gulf of California, P. basiliscus in C. basiliscus in Colima (Riley and Self, 1979); and P. crotali from an unidentied snake and C. catalinensis in Baja California (Sambon, 1922; Goldberg et al., 2003). Of the six species of Porocephalus described from the Americas, P. crotali is apparently the most widely distributed pentastomid infecting snakes. Other species seem to be more specic to their host; e.g., P. basiliscus, P. dominicana, P. tortuguensis, P. clavatus, and P. stilesi are found only in one or very few hosts (Goldberg et al., 2003). Riley (1986) argued that pentastomids show a high degree of host specicity; however, Almeida et al. (2008) mentioned that evidence indicates that American porocephalids are mostly generalists because they parasitize several species and families of ophidians (boids, colubrids, elpids, and viperines). The life cycle of most species of Porocephalus involves the discharge of eggs through nasal secretions or feces, which remain viable in water or on the ground for several months. Rats (Rodentia), cats (Felidae), monkeys (Primates), goats (Bovidae), chickens (Galliformes), and rarely some snakes act as intermediate hosts, while snakes (boids, elapids, viperids, and crotalids) serve as the nal hosts (Reid and Jones, 1963; Par e, 2008). As did other Porocephalus, this species probably uses mammals (muskrats, Cricetidae; mice, Rodentia; opossums, Didelphimorphia; skunks, Mephitidae) as intermediate hosts, because snakes prey mainly on warm-blooded vertebrates (Riley and Walters, 1980). Probably, the house mouse, Mus musculus, is one of the most common preys consumed by C. tzabcan, as previously reported (Luja et al., 2005). The zoonotic implications of pentastomes are related with the ingestion of water or food contaminated with secretions of the respiratory tract of snakes or the direct ingestion of undercooked meat of snakes (Reid and Jones, 1963). To date, about 10 pentastomid species have been involved in zoonotic infections. Linguatula serrata and Armillifer armillatus were associated with 99% of the reported cases of human pentastomiasis (Drabick, 1987; Par e, 2008). However, only species of the genera Armillifer and Porocephalus have been clearly demonstrated to show zoonotic potential (Par e, 2008). At present, there is no report of pentastomid infections in humans in Mexico. Even though the rattlesnake examined during this survey did not appear to be seriously affected by the presence of pentastomids, these parasites might cause serious or lethal infections to their hosts by producing lesions in lungs and obstruction of trachea, which result in interstitial subacute pneumonia with congestion (Grego et al., 2004). Although most infections in wild snakes are subclinical, they could cause anemia in heavily infected hosts, morbidity due to larval or nymphal molting or migration, or mechanical damage to the pulmonary lining by the hooks and mouth of adults (Par e, 2008). Probably, these clinical disorders are more

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253 and captive pit vipers (Bothrops jararaca). Veterinary Record 154:559562. KLAUBER, L. M. 1956. Rattlesnake: their habits, life histories, and inuence of mankind. Volume 2. Berkeley-University of California Press, Berkley. LAYNE, J. N. 1967. Incidence of Porocephalus crotali (Pentastomida) in Florida mammals. Bulletin of the Wildlife Disease Association 3:105109. PEZ. 2005. LUJA, V. H., A. RAM IREZ-BAUTISTA, AND M. SANVICENTE-LO Crotalus simus tzabkan (Tropical rattlesnake) diet. Herpetological Review 36:192193. , J. A. 2008. An overview on pentastomiasis in reptiles and PARE other vertebrates. Journal of Exotic Pet Medicine 17:285294. QIU, M. H., K. C. MA, P. C. FAN, AND S. S. LU. 2005. Discovery of a new species of the pentastomid genus Porocephalus from Taiwan, China and its pathogenic features. Chinese Journal of Parasitology and Parasitic Diseases 23:6972. REID, A. M., AND D. W. E. JONES. 1963. Porocephalus armillatus larvae presenting in the eye. British Journal of Ophthalmology 47:169. RILEY, J. 1981. Some observations on the development of Porocephalus crotali (Pentastomida: Porocephalidae) in the western diamondback rattlesnake (Crotalus atrox). International Journal for Parasitology 11:127131. RILEY, J. 1986. The biology of pentastomids. Advances in Parasitology 25:45128. RILEY, J., AND J. T. SELF. 1979. On the systematics of the pentastomid genus Porocephalus (Humboldt, 1811) with descriptions of two new species. Systematic Parasitology 1:2542. RILEY, J., AND L. S. WALTERS. 1980. Porocephalus dominicana n. sp. from the Dominican boa (Constrictor constrictor nebulosus). Systematic Parasitology 1:123126. SAMBON, L. W. 1922. A synopsis of the family Linguatulidae. Journal of Tropical Medicine and Hygiene 25:188206, 391 428. STORCH, V. 1993. Pentastomida. Pages 115142 in Microscopic anatomy of vertebrates: Onychophora, Chilopoda, and lesser Protostomata (F. W. Harrison and M. E. Rice, editors). Volume 12. Wiley-Liss, New York. TEAGUE-SELF, J., AND R. E. KUNTZ. 1967. Host parasite relations in some Pentastomida. Journal of Parasitology 53:202206. TEAGUE-SELF, T., AND F. B. MCMURRY. 1948. Porocephalus crotali Humboldt (Pentastomida) in Oklahoma. Journal of Parasitology 34:2123. VON HUMBOLDT, A. 1808. Ansichten de Natur mit Wissenschaftlichen Erl auterungen. Volume I, Tubingen. STER, W., J. E. FERGUSON, J. A. QUIJADA-MASCARENAS, C. E. POOK, WU O, AND R. S. THORPE. 2005. Tracing an invasion: M. G. SALOMA landbridges, refugia, and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Molecular Ecology 14:1,0951,108. Submitted 24 September 2010. Accepted 23 March 2013. Associate Editor was Felipe de Jesus Rodriguez Romero.

frequent and evident in captive animals because of stress (Par e, 2008). To elucidate the degree of damage caused by the parasites, it is necessary to conduct histopathological studies. Unfortunately, the viscera of the sole specimen examined were in bad condition. Several examples provided by Teague-Self and Kuntz (1967) showed that the high degree of adaptation and hostparasite co-evolution of pentastomes and their reptilian hosts have resulted in a poorly exacerbated tissue and physiological reaction to the infection. Pentastomes can be present in large numbers in their native host without apparent harm or being subclinical (Drabick, 1987; Par e, 2008). Perhaps, the pentastomid plays an important role as a mortality factor when environmental conditions are severe or when the immunological response of the host is compromised. Because only one organism was dissected in our study, we cannot elucidate on this. Translocation, importation, or exportation of infected rattlesnakes may lead to the spreading of their parasites and cross-infection to other congeners or non-congener organisms (Par e, 2008). This might produce severe pathologies, because hosts are not adapted to this parasite.
We thank P. Ramos for collecting and providing the snake, and W. de Oliveira Almeida for his invaluable support in identication of parasites. This work was partly supported by Consejo Nacional de Ciencia y Tecnologia, Mexico, and the Institute of Parasitology (projects Nos. Z60220518 and LC 522). LITERATURE CITED ALMEIDA, W. O., AND L. CHRISTOFFERSEN. 1999. A cladistic approach to relationship in Pentastomida. Journal of Parasitology 85:695704. ALMEIDA, W. O., F. SILVA-FERREIRA, M. CAMARGO-GUARNIERI, AND S. VIEIRA-BRITO. 2008. Porocephalus species (Pentastomida) infecting Boa constrictor (Boidae) and Lachesis muta (Viperidae) in northeastern Brazil. Biotemas 21:165168. BUCKLE, A. C., J. RILEY, AND G. F. HILL. 1997. The in vitro development of the pentastomid Porocephalus crotali from the infective instar to the adult stage. Parasitology 115:503512. CAMPBELL, J. A. 1998. Amphibians and reptiles of northern Guatemala, the Yucatan and Belize. University of Oklahoma Press, Norman. DRABICK, J. J. 1987. Pentastomiasis. Reviews of Infectious Diseases 9:1,0871,094. GOLDBERG, S. R., C. R. BURSEY, AND K. R. BEAMAN. 2003. First reported occurrence of Porocephalus crotali (Pentastomida, Porocephalidae) in the Santa Catalina Island rattleless rattlesnake. California Fish and Game 89:5153. O-DIAS. 2004. GREGO, K. F., C. H. GARDINER, AND J. L. CATA Comparative pathology of parasitic infections in free-ranging