We examined two species of xantusiid lizards, Lepidophyma flavimaculatum Duméril, 1851 and L. reticulatum Taylor, 1955 from Costa Rica for the presence of helminths

Bursey, Charles R.

Goldberg, Stephen R.

Phyllomedusa Journal of Herpetology

English

Cadernos Espinosanos (E-Journal)

85Phyllomedusa - 10(1), July 2011Phyllomedusa 10(1):85–88, 2011© 2011 Departamento de Ciências Biológicas - ESALQ - USP ISSN 1519-1397Received 18 October 2010.Accepted 20 March 2011.Distributed July 2011.Short CommuniCationHelminths of two lizard species, Lepidophyma flavimaculatum and L. reticulatum (Squamata: Xantusiidae), from Costa RicaStephen R. Goldberg1 and Charles R. Bursey21 Department of Biology, Whittier College, Whittier, California 90608, USA. E-mail: sgoldberg@whittier.edu.2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, USA, E-mail: cxb13@psu.edu.Keywords: Squamata, Xantusiidae, Lepidophyma, helminths, Costa Rica.Palabras claves: Squamata, Xantusiidae, Lepidophyma, helmintos, Costa Rica.Palavras-chave: Squamata, Xantusiidae, Lepidophyma, helmintos, Costa Rica.The helminth biodiversity of Neotropical vertebrates is poorly known (Salgado-Maldonado et al. 2000) and merits investigation in view of the loss of habitat (Sasa et al. 2010) and extinction of species (Collins and Crump 2009). Also, invasive species may transport helminths native to their site of emigration (Goldberg and Bursey 2000). Because the invasion rate already is substantial (Kraus 2009), it is critical to document the native helminth fauna before it is contaminated with exotic helminth species. We examined two species of xantusiid lizards, Lepidophyma flavimaculatum Duméril, 1851 and L. reticulatum Taylor, 1955 from Costa Rica. Species of Lepidophyma especially merit investi-gation because of their secretive habits and propensity to live under debris or in fallen logs in relatively undisturbed forests (Savage 2002). As the habitat used by species of Lepidophyma becomes cleared for agriculture or human habitation, the long-term survival of these taxa is questionable. Lepidophyma currently contains 19 species, only two of which occur in Costa Rica—L. flavimaculatum and L. reticulatum (Savage 2002). Herein we establish an initial list of helminths for L. reticulatum and add to the list for L. flavimaculatum. Bursey et al. (2006) described the nematode Aplectana herediaensis Goldberg, Bursey, and Telford, 2006 and also reported the digenean Mesocoelium monas (Rudolphi, 1819) from L. flavimaculatum collected in Costa Rica. Lepidophyma flavimaculatum occurs from Oaxaca and Veracruz, Mexico, to central Panama; L. reticulatum occurs in southwestern Costa Rica and probably adjacent southwestern Panama (Savage 2002). Samples of 13 Lepidophyma flavimaculatum (mean snout–vent length [SVL] = 85.7 mm ± 7.6 SD; range = 68–95 mm from Limón Province, Costa Rica, collected in 1979 and two L. reticulatum from Puntarenas Province, Costa Rica, collected in 1973 (mean SVL = 69.0 mm; range = 65–73 mm) from the herpetology collection of the Natural History Museum of Los Angeles County (LACM) were examined: 86Phyllomedusa - 10(1), July 2011Goldberg and BurseyL. flavimaculatum, LACM 131086, 131092, 131098–99, 131001–02, 131004–07, 131009–11; L. reticulatum, LACM 159130, 159133. The digestive tract was removed from the body cavity. We opened the esophagus, stomach, and small and large intestines and searched for helminths, using a dissecting microscope. Digeneans were regressively stained in hema toxylin, mounted in Canada balsam, studied under a compound microscope, and identified. Nematodes were cleared in a drop of glycerol on a microscope slide, cover-slipped, studied under a compound microscope, and identified. In L. flavimaculatum, we found one species of Digenea, Mesocoelium monas, in the small intestines, and three species of Nematoda—Africana telfordi Bursey and Goldberg, 2002, in the small intestines; Raillietnema brachyspiculatum Bursey, Goldberg, Salgado-Maldonadó and Mendez-de la Cruz, 1998, in small and large intestines; and larvae of Contracaecum sp. in cysts in the stomach wall. In L. reticulatum, we found two species of Nematoda—A. herediaensis Bursey, Goldberg and Telford, 2006 and Africana telfordi, both in the large intestines. Parasite terminology follows that of Bush et al. (1997). Voucher helminths are deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland, as: L. flavimaculatum: A. telfordi (USNPC 103903); R. brachyspiculatum (USNPC 103904); and Contracaecum sp. (103905). Lepidophyma reticulatum: Africana telfordi (USNPC 104035) and Aplectana here diaensis (USNPC 104036).Number of helminths, prevalence, mean intensity ± 1 SD, and range for both host species are given in Table 1. The digenean Mesocoelium monas is cosmopolitan in distribution, utilizes a single molluscan host, and infection occurs with the ingestion of an infected snail or vegetation supporting cysts (Thomas 1965). Hosts are listed in Goldberg et al. (2009). Africana tel-fordi was described from the iguanid lizard, Enyalioides heterolepis (Bocourt, 1874) from Panama by Bursey and Goldberg (2002). It also has been reported in Gonatodes albogularis (Duméril and Bibron, 1836) from Panama (Bursey et al. 2007), Corytophanes cristatus (Merrem, 1820), and Anolis lionotus Cope, 1861 from Costa Rica (Bursey and Brooks 2010). Africana is a taxon of Heterakidae; infection occurs when the host ingests an egg (Anderson 2000). Aplectana herediaensis was described from L. flavima culatum from Costa Rica by Bursey et al. (2006). Aplectana is a taxon of the Cosmocercidae, which infect directly, either by ingestion or skin penetration (Anderson 2000). Railletnema bra chyspiculatum was described from Lepidophyma tuxtlae Werler and Shannon, 1957 from Mexico by Bursey et al. (1998) and recently, was reported from Morunasaurus annularis (O’Shaughnessy, 1881) from Ecuador by McAllister et al. (2010). Raillietnema also is a member of Cosmocercidae. Adult species of Contracaceum are found in piscivorous birds and aquatic mammals; a great variety of invertebrates serve as paratenic (= transport) hosts (Anderson 2000). Lizards likely become infected by eating infected invertebrates and, in turn, may serve as a paratenic host; development to the adult nematode does not occur until the definitive host is reached.Africana telfordi, Raillentnema  brachyspicu-latum, and Contracaecum sp. (larvae) represent new helminth records for L. flavimaculatum and are added to the helminth list that also includes M. monas, Aplectana herediaensis, Parapharyn-go don colonensis Bursey, Goldberg and Telford, 2007, and Strongyluris panamensis Bursey, Goldberg and Telford, 2003. The helminth list for L. reticulatum currently consists of two species of nematodes, Africana telfordi and Aplectana herediaensis. These findings support the observation of Bursey and Brooks (2010) that lizards from Central and South America harbor generalist helminths that, under suitable conditions, can infect a variety of host species.Acknowledgments.—We thank C. Thacker (LACM) for permission to examine Lepidophyma, and Cecilia Nava and Daisy Salguero (Whittier College) for assistance with dissections. 87Phyllomedusa - 10(1), July 2011Helminths of two xantusiid lizards from Costa RicaTable 1. Number of helminths, prevalence (%), mean intensity ± 1 SD, and range for 13 Lepidophyma flavimaculatum and two L. reticulatum from Costa Rica; * = new host record.Taxon N Prevalence (%) Mean intensity RangeL. flavimaculatumDigeneaMesocoelium monas 7 23.0 2.3 ± 2.3 1–5NematodaAfricana telfordi* 4 7.6 4.0 —Raillietnema brachyspiculatum* 1242 92.3 103.5 ± 78.0 1–248Contracaecum sp. (larvae)* 4 7.6 4.0 —L. reticulatumAfricana telfordi* 3 50.0 3.0 —Aplectana herediaensis* 44 50.0 44.0 —Lepidophyma reticulatum belong to the CRE (Costa Rica Expeditions) collection donated to LACM by J. M. Savage in 1998.ReferencesAnderson, R. C. 2000. Nematode Parasites of Vertebrates. Their Development and Transmission. CABI Publishing, Oxon, UK. 650 pp.Bursey, C. R. and D. R. Brooks. 2010. Nematode parasites of 16 lizard species from the Area de Conservación Guanacaste, Costa Rica. Comparative Parasitology 77: 232–235.Bursey, C. R. and S. R. Goldberg. 2002. Africana telfordi n. sp. (Nematoda: Heterakidae) from the lizard, Enyalioides heterolepis (Sauria; Iguanidae) from Panama. Journal of Parasitology 88: 926–928.Bursey, C. R., S. R. Goldberg, G. Salgado-Maldonado, and F. R. Méndez-de La Cruz. 1998. Raillietnema brachyspiculatum sp. n. (Nematoda: Cosmocercidae) from Lepidophyma tuxtlae (Sauria: Xantusiidae) from México. Journal of the Helminthological Society of Washington 65: 164–168.Bursey, C. R., S. R. Goldberg, and S. R. Telford, Jr. 2006. New species of Aplectana (Nematoda: Cosmocercidae) and Mesocoelium monas (Digenea: Brachycoeliidae) in Lepidophyma flavimaculatum (Squamata: Xantusiidae) from Costa Rica. Caribbean Journal of Science 42: 164–170.Bursey, C. R., S. R. Goldberg, and S. R. Telford, Jr. 2007. Gastrointestinal helminths of 14 species of lizards from Panama with descriptions of five new species. Com-parative Parasitology 74: 108–140.Bush, A. O., K.D. Lafferty, J. M. Lotz, and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583.Collins, J. P. and M. L. Crump. 2009. Extinction in Our Times. Global Amphibian Decline. Oxford, UK. Oxford University Press. 273 pp.Goldberg, S. R. and C. R. Bursey. 2000. Transport of helminths to Hawaii via the brown anole, Anolis sagrei (Polychrotidae). Journal of Parasitology 86: 750–755.Goldberg, S. R., C. R. Bursey, and F. Kraus. 2009. Endo-parasites in 12 species of Sphenomorphus (Squamata: Scincidae) from Papua New Guinea. Comparative Parasitology 76: 58–83.88Phyllomedusa - 10(1), July 2011Goldberg and BurseyKraus, F. 2009. Alien Reptiles and Amphibians. A Scientific Compendium and Analysis. Dordrecht, Netherlands. Springer Science and Business Media B. V. 563 pp.McAllister, C. T., C. R. Bursey, and P. S. Freed. 2010. Helminth parasites of selected amphibians and reptiles from the Republic of Ecuador. Comparative Parasitology 77: 52–66.Salgado-Maldonado, G., A. N. García Aldrete, and V. M. Vidal-Martínez (eds.). 2000. Metazoan Parasites in the Neotropics: A Systematic and Ecological Perspective. I México, D.F. Instituto de Biología, Universidad Nacional Autónoma de México. 310 pp.Sasa, M., G. Chaves, and L.W. Porras. 2010. The Costa Rican herpetofauna: conservation status and future perspectives. Pp. 511–603 in L.D. Wilson, J. H. Townsend and J. D. Johnson (eds.), Conservation of Mesoamerican Amphi-bians and Reptiles. Eagle Mountain, Utah. Eagle Mountain Publishing, LC. 812 pp.Savage, J. M. 2002. The Amphibians and Reptiles of Costa Rica. A Herpetofauna Between Two Continents, Between Two Seas. Chicago. The University of Chicago Press. 934 pp. Thomas, J. D. 1965. The anatomy, life history and size allometry of Mesocoelium monodi Dolfuss, 1929. Journal of Zoology 146: 413–446.

Helminths of two lizard species, Lepidophyma flavimaculatum and L. reticulatum (Squamata: Xantusiidae), from Costa Rica

Stephen R. Goldberg

Charles R. Bursey

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Helminths of two lizard species, Lepidophyma flavimaculatum and L. reticulatum (Squamata: Xantusiidae), from Costa Rica

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