First record of Urotrema scabridum (Platyhelminthes), and new records of helminths of Tadarida brasiliensis from Mexican Plateau

Elizabeth A. Martínez-Salazar, Andrea J. Medina-Rodríguez, Rogelio Rosas-Valdez, Melina Del Real-Monroy, Jorge Falcón-Ordaz

Resumen


The Mexican free-tailed bat (Tadarida brasiliensis) is an abundant, widely distributed species in Mexico, except for most of the Yucatán peninsula.  We studied the helminth fauna of T. b. mexicana at seven localities in the State of Zacatecas in order to advance the knowledge of helminth parasites of wild vertebrates in northern-central Mexico.  Eighty-four bat specimens were examined for the presence of helminth parasites following standard procedures; helminths found were identified and infections were characterized.  Of the specimens examined, 65.47 % were parasitized.  The helminth fauna comprises five taxa: three digeneans (Dicrocoelium rileyi, Ochoterenatrema labda, and Urotrema scabridum); one cestode (Vampirolepis sp.); and one nematode (Tadaridanema delicatus).  We present a brief morphological description of Urotrema scabridum.  D. rileyi was the most prevalent and abundant helminth species.  The intestine was the habitat most parasitized, with four species.  Indirect life cycles predominate, and are related to the insectivorous habits of this host.  Further studies on this host-parasite system are necessary to contribute to population monitoring and conservation; biogeographic patterns of helminth parasites of bats should also be studied to explore their origins and evolution in the region. U. scabridum is reported for the first time from Zacatecas.  All species are new locality records.


Palabras clave


Cestoda; Helminth parasites; Mexican free-tailed bat; Mexican Plateau; Nematoda; Trematoda.

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Referencias


ANDERSON, C. 2000. Nematode parasites of vertebrates. Their development and transmission. Centre for Agricultural Bioscience International. Wallingford, U.K.

ALTRINGHAM, J. D. 2011. Bats: from evolution to conservation. Oxford University Press. Oxford, U.S.A.

ÁLVAREZ-CASTAÑEDA, S. T., T. ÁLVAREZ, AND N. GONZÁLEZ-RUIZ. 2015. Guía para la identificación de los mamíferos de México en campo y laboratorio/keys for identifying Mexican Mammals in the field and in the laboratory. Centro de Investigaciones Biológicas del Noroeste, S. C. y Asociación Mexicana de Mastozoología, A. C. Ciudad de México, México.

ARMSTRONG, K. 2008. Brazilian free-tailed bat (Tadarida brasiliensis). Mammalian Species 4:1-6.

BRAY, R. A., D. GIBSON, AND Z. JIANYING. 1999. Urotrematidae Poche, 1926 (Platyhelminthes: Digenea) in Chinese freshwater fishes. Systematic Parasitology 91:193-200.

BRAY, R. A., D. I. GIBSON, AND A. JONES. 2008. Keys to the Trematoda, Volume III. Centre for Agricultural Bioscience International and Natural History Museum. Wallingford, U.K.

BUSH, A. O., J. C. FERNANDEZ, G. ESCH, AND J. R. SEED (EDS). 2001. Parasitism: The diversity and ecology of animal parasites. Cambridge University Press. Cambridge, U.K.

BUSH, O. A., D. K. LAFFERTY, M. J. LOTZ, AND W. A. SHOSTAK. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575–583.

CABALLERO Y CABALLERO, E. 1940. Algunos tremátodos intestinales de los murciélagos de México. Anales del Instituto de Biología 11:215–223.

CABALLERO Y CABALLERO, E. 1942. Descripción de Parallintoshius tadaridae n. sp. (Nematoda: Trichostrongylidae) de los murciélagos de México. Anales del Instituto de Biología 13:105–109.

CABALLERO Y CABALLERO, E. 1943. Tremátodos de los murciélagos de México IV. Descripción de un nuevo género de la subfamilia Lecithodendriidae Looss, 1902, y una nueva especie de Prosthodendrium Dollfus, 1931. Anales del Instituto de Biología 14:173–192.

CABALLERO Y CABALLERO, E. 1964. Helmintos de la República de Panamá, XXIV. Descripción de tres especies de tremátodos Lecithodendriidae que parasitan al murciélago Myotis nigricans nigricans (Schinz). Anales de la Escuela Nacional de Ciencias Biológicas 13:73–81.

CABALLERO Y CABALLERO, E., AND M. BRAVO. 1950. Tremátodos de los murciélagos de México VI. Descripción de una nueva especies de Limatulum (Trematoda: Lecithodendriidea). Anales del Instituto de Biología 21:345–350.

CABALLERO Y CABALLERO, E., AND G. CABALLERO-RODRÍGUEZ. 1969. Tremátodos de los murciélagos de México IX. Descripción de una nueva especie de Platynostomum Looss, 1907 y continuación el primer suplemento del Catálogo taxonómico de los tremátodos que parasitan a los murciélagos. Revista de la Sociedad Mexicana de Historia Natural 30:263–290.

CABALLERO Y CABALLERO, E., AND R. G. GROCCOTT. 1960. Helmintos de la República de Panamá. 23. Estudios de los trematodos de murciélagos, con descripción de una nueva especie. Ciencia 19:244–248.

CAIN, G. D. 1966. Helminth parasites of bats from Carlsbad Caverns, New Mexico. Journal of Parasitology 52:351–357.

CAIN, G. D., AND E. H. STUDIER. 1974. Parasite helminths of bats from southwestern United States and Mexico. Proceedings of the Helminthological Society of Washington 41:113–114.

CASPETA-MANDUJANO, J. M., J. L. PERALTA-RODRÍGUEZ, S. B. RAMÍREZ-CHÁVEZ, S. E. RAMÍREZ-DÍAZ, M. DEL C. P. OJEDA, V. JUÁREZ-GONZÁLEZ, M. TAPIA-OSORIO, M. G. JUÁREZ-URBINA, J. A. GUERRERO E., M. G. GALINDO-GARCÍA, AND G. MARTÍNEZ-RODRÍGUEZ. 2017. Helmintos parásitos de murciélagos en México. Universidad Autónoma del Estado de Morelos. Praxis digital 13. Morelos, México.

CHEUICHE, P. T., S. NUNES G., A. M. RUI, AND G. MÜLLER. 2015. Helminths in Tadarida brasiliensis (Chiroptera: Molossidae) from Southern Brazil. Neotropical Helminthology 9:3–20.

CLARKE-CRESPO, E., G. PÉREZ-PONCE DE LEÓN, S. MONTIEL-ORTEGA, AND M. RUBIO-GODOY. 2017. Helminth fauna associated with three Neotropical bat species (Chiroptera: Mormoopidae) in Veracruz, México. Journal of Parasitology 103:338–342.

FABIÁN, M. E., HARTZ, S. M., AND T. H. A. ARIGONY. 1990. Alimentação de Tadarida brasiliensis brasiliensis (Geoffroy, 1824) na região urbana de Porto Alegre, RS, Brasil (Chiroptera, Molossidae). Brazilian Journal of Biology 50:387-392.

FALCÓN-ORDAZ, J., C. GUZMÁN-CORNEJO, L. GARCÍA-PRIETO, AND S. L. GARDNER. 2006. Tadaridanema delicatus (Schwartz, 1927) n. gen., n. comb. (Trichostrongylina: Molineidae) parasite of Molossidae bats. Journal of Parasitology 92:1035-1042.

FALCÓN-ORDAZ, J., P. OCTAVIO-AGUILAR, AND S. I. ESTRELLA-CRUZ. 2019. Morphological and morphometric variations of Dicrocoelium rileyi (Digenea: Dicrocoelidae) parasitizing Tadarida brasiliensis (Chiroptera: Molosiidae) in Mexico. Anais da Academia Brasileira de Ciências 91:e20180436.

FONT, W. F., AND J. M. LOTZ. 2008. Family Urotrematidae Poche, 1926. Pp. 441–445 in Keys to the Trematoda, Volume 3 (Bray, R. A., D. I. Gibson, and A. Jones, eds.). Centre for Agricultural Bioscience International. Wallingford, U.K.

GARCÍA-PRIETO, L., J. FALCÓN-ORDAZ, AND C. GUZMÁN-CORNEJO. 2012. Helmith parasites of wild Mexican mammals: list of species, hosts and geographical distribution. Zootaxa 3290:1-92.

GOLDBERG, S. R., C. R. BURSEY, AND H. CHEAM. 1996. Gastrointestinal helminths of six anole species, Anolis armouri, A. barahonae, A. bahorucoensis, A. brevirostris, A. chlorocyanus and A. coelestinus (Polychrotidae) from Hispaniola. Caribbean Journal of Science 32:112-115.

GOLDBERG, S. R., C. R. BURSEY, AND H. CHEAM. 1998. Helminths of six species of Anolis lizards (Polychrotidae) from Hispaniola, West Indies. Journal of Parasitology 84:1291-1295.

GOLDBERG, S. R., C. R. BURSEY, AND R. TAWIL. 1994. Helminth parasites of the bark anole, Anolis distichus and the brown anole, Anolis sagrei (Polychridae) from Florida and the Bahamas. Caribbean Journal of Science 30:275-277.

GUZMÁN-CORNEJO, M. C., L. GARCÍA-PRIETO, G. PÉREZ-PONCE DE LEÓN, AND J. MORALES-MALACARA. 2003. Parasites of Tadarida brasiliensis mexicana (Chiroptera: Molossidae) from Arid Regions of México. Comparative Parasitology 70:11-25.

HILTON, C. D., AND T. L. BEST. 2000. Gastrointestinal helminth parasites of bats in Alabama. Occasional Papers of the North Carolina Museum of Natural Sciences and the North Carolina Biological Survey 12:57–66.

HUTSON, A. M., S. P. MICKLEBURGH, AND P. RACEY (COMP.). 2001. Microchiropteran bats: global status survey and conservation action plan. IUCN/SSC Chiroptera Specialist Group. International Union for Conservation of Nature, Gland, Switzerland and Cambridge, U.K.

JIMÉNEZ, F. A., J. M. CASPETA-MANDUJANO, S. B. RAMÍREZ-CHÁVEZ, S. E. RAMÍREZ-DÍAZ, M. G. JUÁREZ-URBINA, J. L. PERALTA-RODRÍGUEZ, AND J. A. GUERRERO. 2017. Checklist of Helminths of Bats from Mexico and Central America. MANTER: Journal of Parasite Biodiversity 7:1–28.

KHALIL, L. F., A. JONES, AND R. A. BRAY. 1994. Keys to the Cestode Parasite of Vertebrates. Centre for Agricultural Bioscience International. Albans, U.K.

KERTH, G. 2008. Causes and consequences of sociality in bats. BioScience 8:737–746.

KUNZ, T. H., J. O. JR. WHITAKER, AND M. D. WADANOLI. 1995. Dietary energetics of the insectivorous Mexican free-tailed bat (Tadarida brasiliensis) during pregnancy and lactation. Oecologia 101:407–415.

LAMOTHE-ARGUMEDO, A. R. 1997. Manual de técnicas para preparar y estudiar los parásitos de animales silvestres. AGT. Editor, S.A. Ciudad de México, México.

LORD, J. S., S. PARKER, F. PARKER, AND D. R. BROOKS. 2012. Gastrointestinal helminths of pipistrelle bats (Pipistrellus pipistrellus/Pipistrellus pygmaeus) (Chiroptera: Vespertilionidae) of England. Parasitology 139:366–374.

LUNASCHI, L. 2002. Redescripción y comentarios taxonómicos sobre Ochoterenatrema labda (Digenea: Lecithodendriidae), parásito de quirópteros en México. Anales del Instituto de Biología 73:11–18.

LUNASCHI, L., AND J. NOTARNICOLA. 2010. New host records for Anenterotrematidae, Lecithodendriidae and Urotrematidae trematodes in bats from Argentina, with redescription of Anenterotrema liliputianum. Revista Mexicana de Biodiversidad 81:281–287.

LUVIANO-HERNÁNDEZ, L., D. TAFOLLA-VENEGAS, E. MELÉNDEZ-HERRERA, AND A. L. FUENTES-FARÍAS. 2018. Helmintos del murciélago Macrotus waterhousii (Chiroptera: Phyllostomidae) en dos refugios de selva baja caducifolia en el municipio de Huetamo, Michoacán, México. Revista Mexicana de Biodiversidad 89:1315–1321.

MACY, R. W. 1931. New bat trematodes of genera Plagiorchis, Limatulum and Dicrocoelium. Journal of Parasitology 18:28–33.

MCCRACKEN, G. F., M. K. MCCRACKEN, AND A. T., VAWTER. 1994. Genetic structure in migratory population of the bat Tadarida brasiliensis Mexicana. Journal of Mammalogy 75:500–514.

MCWILLIAMS, L. A. 2005. Variation in diet of the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Journal of Mammalogy 86:599–605.

NARANJO-GARCÍA, E. 2014. Biodiversidad de moluscos terrestres en México. Revista Mexicana de Biodiversidad 85:S431–S440.

OLSEN, O. W. 1986. Animal Parasites. Their Life Cycles and Ecology. Dover Publications, Inc. New York, U.S.A.

POJMAŃSKA, T. 2008. Family Dicrocoeliide Looss, 1899. Pp. 233–260 in Keys to the Trematoda, Volume 3 (Bray, R. A., D. I. Gibson, and A. Jones, eds.). Centre for Agricultural Bioscience International. Wallingford, U.K.

ROBERTS, L. S., AND J. JANOVY, JR. 2009. Foundations of Parasitology. Eighth edition. McGraw-Hill. New York, U.S.A.

RUSSELL, A. L., R. A. MEDELLÍN, AND G. F. MCCRACKEN. 2005. Genetic variation and migration in the Mexican free-tailed bat (Tadarida brasiliensis mexicana). Molecular Ecology 14:2207–2222.

RYDELL, P. 2006. Bats and their insect prey at streetlights. Pp. 43–60 in Ecological consequences of artificial night lighting. (Rich, C. and T. Longcore, eds). Island Press. U.S.A.

SALINAS-RAMOS, V. B., L. G. HERRERA, D. I. HERNÁNDEZ-MENA, D. OSORIO-SARABIA, AND V. LEÓN-RÈGAGNON. 2017. Seasonal variation of gastro-intestinal helminths of three bat species in the dry forest of western Mexico. Revista Mexicana de Biodiversidad 88:646–653.

SÁNCHEZ-CORDERO, V., F. BOTELLO, J. J. FLORES-MARTÍNEZ, R. A. GÓMEZ-RODRÍGUEZ, L. GUEVARA, G. GUTIÉRREZ-GRANADOS, AND A. RODRÍGUEZ-MORENO. 2014. Biodiversidad de Chordata (Mammalia) en México. Revista Mexicana de Biodiversidad 85:S496–S504.

SCHMIDLY, D. J. 1991. The bats of Texas. Texas A&M University Press, College Station. College Station, U.S.A.

SCHMIDT, G. 1986. CRC handbook of tapeworm identification. CRC Press. Boca Raton, U.S.A.

SCALES, J.A., AND K. T., WILKINS. 2007. Seasonality and fidelity in roost use of the Mexican free-tailed bat, Tadarida brasiliensis, in an urban setting. Western North American Naturalist 67:402–408.

SELLERS, L. G., AND G. GRAHAM. 1987. Trematodes of Cuban brown anoles, Anolis sagrei sagrei from Florida. Journal of the Helminthological Society of Washington 54:266–267.

SIKES, R. S., AND ANIMAL CARE AND USE COMMITTEE OF THE AMERICAN SOCIETY OF MAMMALOGISTS. 2016. Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97:663–688.

SIMMONS, N. B. 2005. Order Chiroptera. Pp. 312–529 in Mammal species of the world: a taxonomic and geographic reference. Third Edition, Volume 1 (Wilson D. E., and D. M. Reeder, eds.). Johns Hopkins University Press. Baltimore, U.S.A.

THOMPSON, F. G. 2011. An annotated checklist and bibliography of the land and freshwater snails of Mexico and Central America. Bulletin of the Florida Museum of Natural History 50:1–299

TKACH, V. V., S. E. GREIMAN, E. E. PULIS, D. R. BROOKS, AND C. CARRION. 2019. Phylogenetic relationships and systematic position of the enigmatic Urotrema Braun, 1900 (Platyhelminthes: Digenea). Parasitology International 70:118–122.

TKACH, V. V., V. D. TIMOTHY, J. LITTLEWOOD, P. D. OLSON, J. M. KINSELLA, AND Z. SWIDERSS. 2003. Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56:1–15.

TRAVASSOS, L. 1944. Revisao da Familia Dicrocoeliidae Odhner, 1910. Monografías do Instituto Oswaldo Cruz. Impresa Nacional Rio de Janeiro-Brasil. Rio de Janeiro, Brazil.

TUTTLE, M. D. 1994. The lives of Mexican Free-tailed Bats. Bats 3:6–14.

VÁSQUEZ-BOLAÑOS, M. 2011. Lista de especies de hormigas (Hymenoptera: Formicidae) para México. Dugesiana 18:95–133.

WILKINS, K. T. 1989. Tadarida brasiliensis. Mammalian Species 331:1–10.

WITHAKER, J. O., J. R. NEEFUS, AND T. H. KUNZ. 1996. Dietary variation in the Mexican free tailed bat (Tadarida brasiliensis mexicana). Journal of Mammalogy 77:716-724.

YAMAGUTI, S. 1958. Systema Helminthum. Vol. I. Digenetic Trematodes. Interscience. New York, U.S.A.

YAMAGUTI, S. 1971. Synopsis of digenetic trematodes of vertebrates. Vols 1. Keigaku Publishing Company. Tokyo. Japan.

YAMAGUTI, S. 1975. A synoptical review of the life histories of digenetic trematodes of vertebrates: with special reference to the morphology of their larval forms. Keigaku Publishing Company. Tokyo, Japan.

ZAMPARO, D., D. R. BROOKS, AND V. TKACH. 2005. Urotrema shirleyae n. sp. (Trematoda: Digenea: Urotrematidae) in Norops oxylophus and N. cupreus (Squamata: Iguania: Polychrotidae) from the Area de Conservación Guanacaste, Guanacaste, Costa Rica. Journal of Parasitology 91:648–652.


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