Ectoparasites (Polyctenidae, Streblidae, Nycteribiidae) of bats (Mammalia: Chiroptera) from the Caribbean region of Colombia
Keywords:
Caribbean region, Colombia, Cordoba, ectoparasitism, extensive livestock, Phyllostomidae, silvopastoral system, tropical dry forest.Abstract
Bats are hosts of a high taxonomic diversity of ectoparasites. Six hundred eighty seven insect species have been reported as bat ectoparasites, belonging to orders Dermaptera, Lepidoptera, Diptera and Siphonaptera (Marshall 1982). This study lists an inventory of bat ectoparasites found in fragments of Tropical Dry Forest on the Caribbean coast of Colombia. The study was conducted in the Department of Cordoba in four farms with fragments of Tropical Dry Forest. Bats were captured using mist nets and were collected and stored in plastic bags for subsequent examination in the laboratory. Ectoparasites were stored in alcohol and identified using a stereo microscope and taxonomic keys. Two hundred fifty one bats belonging to 21 species were captured. The most abundant family was Phyllostomidae, followed by Emballonuridae, Noctilionidae, Vespertilionidae and Molossidae. Twelve genera of ectoparasites were found, belonging to families Streblidae, Nycteribiidae and Polyctenidae. Streblidae was the most abundant family and included the largest number of species. Thirty five percent of bats examined were hosts to at least one ectoparasite species. In this study, carried out in fragments of tropical dry forest in Cordoba, Colombia, we recorded dipterans in 17 out of 21 bat species. Hemypteran ectoparasites of the family Polyctenidae were found in Molossus molossus only. Eighty seven individual dipterans were found among 51 Carollia perspicillata specimens, which is consistent with the high parasitism levels previously reported. The bat species C. brevicauda, P. discolor, U. bilobatum and C. perspicillata carried the highest number of ectoparasite species.References
Aguiar, L., and Y. Antonini. 2011. Descriptive ecology of bat flies (Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the Cerrado of central Brazil. Memórias do Instituto Oswaldo Cruz 106:170-176.
Aguiar, L., W. Camargo, and A. Portella. 2006. Occurrence of white-winged vampire bat, Diaemus youngi (Mammalia, Chiroptera), in the Cerrado of Distrito Federal, Brazil. Revista Brasileira de Zoologia 23:893–896.
Altringham, J. D. 1996. Bats: Biology and behavior. Oxford University Press. New York, U. S. A.
Anderson, R., and H. Filho. 2006. Dípteros ectoparasitas (Diptera, Streblidae) de filostomídeos (Chiroptera, Mammalia) do parque municipal no cinturão verde de cianorte, Paraná, Brasil e sua incidênciaao longo das estações do ano. Chiroptera Neotropical 12:238–243.
Azevedo, A., and P. Linardi. 2002. Streblidae (Diptera) of phyllostomid bats from Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz 97:421-422.
Ballesteros, J., C. Fernández, and R. Dueñas. 2006. Introducción a la diversidad faunística del Departamento de Córdoba. Informe técnico. Universidad de Córdoba, Facultad de Ciencias Básicas e Ingenierías. Montería, Colombia.
Ballesteros-Correa, J. 2015. Efecto del manejo silvopastoril y convencional de ganadería extensiva sobre el ensamblaje de murciélagos asociados a fragmentos de bosque seco tropical en Córdoba, Colombia. Tesis doctoral. Doctorado en Ciencias Biológicas. Facultad de Ciencias. Pontificia Universidad Javeriana. Bogotá, Colombia.
Bergallo, H., C. Esbérard, M. Ribeiro, V. Lins, R. Mangolin, G. Melo, and M. Baptista. 2003. Bat species richness in Atlantic Forest: What is the minimum sampling effort? Biotropica 35:278-288.
Berlota, P., C. Aires, S. Favorito, G. Graciolli, M. Amaku, and R. Pinto-Da-Rocha, R. 2005. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz 100:25-32.
Boshell, J., and J. Kerr. 1942. Veinticinco especies nuevas de Trombidiideos de Colombia. Revista Academia Colombiana de Ciencias 5:110-127.
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.
Calonge-Camargo, B. 2012. Ectoparásitos de murciélagos presentes en fragmentos de bosque seco tropical en manejos de ganadería convencional y silvopastoril (Córdoba – Colombia). Tesis de Maestría. Maestría en Ciencias Biológicas. Facultad de Ciencias. Pontificia Universidad Javeriana. Bogotá, Colombia.
Camilotti, V. L., G. Graciolli, M. M. Weber, J. Arruda, and N. Cáceres. 2010. Bat flies from the deciduous Atlantic Forest in southern Brazil: Host-parasite relationships and parasitism rates. Acta Parasitologica 55:194–200.
Christe, P., M. Giorgi, P. Vogel, and R. Arlettaz. 2003. Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialization? Journal of Animal Ecology 72:866–872.
Clark, G. M. 1967. New Speleognathinae from Central and South American mammals (Acarina, Trombidiformes). The Helminthological Society of Washington 32:240-243.
Cloutier, D., and D. Thomas. 1992. Carollia perspicillata. Mammalian Species 417:1-9.
Dick, C. W., M. R. Gannon, W. E. Little, and M. J. Patrick. 2003. Ectoparasite associations of bats from central Pennsylvania. Journal of Medical Entomology 40:813–819.
Dick, C. W., and D. Gettinger. 2005. A faunal survey of streblid flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology 91:1015-1024.
Dick, C. W., Graciolli, G., and R. Guerrero. 2016. Family Streblidae. Zootaxa 4122:784-802.
Durán, A., Álvarez-Garcia, D., and G. Graciolli. 2017. Ectoparasitic flies (Diptera, Streblidae) on bats (Mammalia, Chiroptera) in a dry tropical forest in the northern Colombia. Papéis Avulsos de Zoologia 57:105-111.
Emerson, J., and A. Roark. 2007. Composition of guano produced by frugivorous, sanguinovorous, and insectivorous bats. Acta chiropterologica 9:261-267.
Emmons, L., and F. Feer. 1997. Neotropical rainforest mammals: a field guide. University of Chicago Press. Illinois, EE.UU.
Esberard, C. E. L., A. C. Jesus, A. Motta, H. Bergallo, and D. Gettinger. 2005. Hesperoctenes fumarius (Hemiptera: Polyctenidae) Infesting Molossus rufus (Chiroptera: Molossidae) in Southeastern Brazil. The Journal of Parasitology 91:465-467.
Fernández, A., R. Guerrero, R. Lord, J. Ochoa, and G. Ulloa. 1988. Mamíferos de Venezuela: Lista y claves para su identificación. 1ra. Edición. ASOVEM. Caracas, Venezuela.
Fritz, G. 1983. Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology 20:1-10.
Gardner, A. L. 2007. Order Chiroptera. Pp. 187-188 in Mammals of South America: Volume 1 Marsupials, Xenarthrans, Shrews, and Bats (Gardner, A. L., ed.). Chicago: University of Chicago Press. Chicago, U. S. A.
Graciolli, G., and C. J. B. Carvalho. 2001. Moscas ectoparasitas (Diptera, Hippoboscoidea) de morcegos (Mammalia, Chiroptera) do Estado do Paraná. 11. Streblidae. Chave pictórica para gêneros e espécies. Revista Brasileira de Zoologia 18:907-960.
Graciolli, G., F. Passos, W. Pedro, and B. Lim. 2006. Moscas ectoparasitas (Diptera, Streblidae) de morcegos filostomideos (Mammalia, Chiroptera) na Estação Ecológica dos Caetetus, São Paulo, Brasil. Revista Brasileira de Zoologia 23:298-299.
Guerrero, R. 1993. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. I. Clave para los géneros y Nycterophiliinae. Acta Biológica Venezuelica 14:61-75.
Guerrero, R. 1997. Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos del nuevo mundo. VII. Lista de Especies, hospedadores y países. Acta Biológica Venezuelica 17:9-24.
Hart, B. L. 1990. Behavioral adaptations to pathogens and parasites. Neuroscience and Biobehavioral Reviews 14:273-294.
Herrera-Sepúlveda, M.T. 2013. Comparación de la carga de ectoparásitos entre harenes y grupos mixtos de la población de Carollia perspicillata en la cueva Macaregua (Santander, Colombia). Tesis de Pregrado. Biología. Facultad de Ciencias. Pontificia Universidad Javeriana. Bogotá, Colombia.
Kerth, G. 2008. Causes and consequences of sociality in bats. BioScience. 58:737-746.
Komeno, C., and A. Linhares. 1999. Batflies parasitic on some phyllostomid bats in southeastern Brazil: Parasitism rates and host-parasite relationships. Memórias do Instituto Oswaldo Cruz 94:151-156.
Kunz, T. H. 1976. Observations on the winter ecology of the bat fly Trichobius corynorhini. Journal of Medical Entomology 12:631-636.
Laval, R.K., and B. Rodríguez-H. 2002. Murciélagos de Costa Rica, Bats. 1 ed. Instituto Nacional de Biodiversidad, INBio, Santo Domingo de Heredia, Costa Rica.
Linares, O. 1998. Mamíferos de Venezuela. Primera edición. Sociedad Conservacionista Audubon de Venezuela. Caracas, Venezuela.
Machado-Allison, C., and R. Antequera. 1969. Algunos datos sobre la distribución y huéspedes de los Spinturnicidae de Colombia (Acarina, Mesostigmata, Spinturnicidae). Caldasia 10:371-376.
Marinkelle, J. 1967. Cimex hemipterus from bats in Colombia, South America. Proceedings of the Entomological Society of Washington 69:179–180.
Marinkelle, J., and E. Grose. 1981. A list of ectoparasites of colombian bats. Revista de Biología Tropical 29:11–20.
Marshall, A. G. 1991. The ecology of ectoparasitic insects. Academic Press. New York, U. S. A.
Marshall, A. 1982. Ecology of insects ectoparasitic on bats. Pp: 369–401, in Kunz, T. Ecology of bats. Plenum Press. New York. U. S. A.
McCracken, G., and G. Wilkinson. 2000. Bat mating systems. Reproductive biology of bats. Academic Press. New York, U. S. A.
Moore, S. L., and K. Wilson. 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015– 2018.
Mooring, M., D. Reisig, J. Niemeyer, and E. Osborne. 2002. Sexually and developmentally dimorphic grooming: A comparative survey of the Ungulata. Ethology 108:911—934.
Morand, S., J. Gouy de Bellocq, M. Stanko, y D. Miklisová. 2004. Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of central Europe? Parasitology 129:505–510.
Ochoa, J. 1985. El murciélago carnívoro Chrotopterus auritus (Peters). Natura 77:30–32.
Patterson, B. D., C. W. Dick, and K. Dittmar. 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera:Streblidae). Journal of Tropical Ecology 23:177–189.
Presley, S. J., and M. R. Willig. 2008. Intraspeciï¬c patterns of ectoparasite abundances on Paraguayan bats: effects of host sexa nd body size. Journal of Tropical Ecology 24:75–83.
Racero-Casarrubia, J., J. Ballesteros-Correa, and J. Pérez-Torres. 2015. Mamíferos del departamento de Córdoba-Colombia: Historia y estado de conservación. Biota Colombiana 16:128-148.
Racero-Casarrubia, J., J. Pinedo-Hernandez, J. Ballesteros-Correa, and J. Marrugo-Negrete. 2017. Metales pesados en especies de murciélagos (Quiróptera) asociados a una finca bajo manejo silvopastoril en el departamento de Córdoba, Colombia. Acta Zoológica Mexicana (n. s.) 33:45-54.
Rui, A. M., and G. Graciolli. 2005: Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasitas e taxas de infestação. Revista Brasileira de Zoologia 22:438–445.
Ryckman, R. E., and M. A. Casdin. 1977. The Polyctenidae of the world, A checklist with Bibliography. Vector Views 24:25-31.
Santos, M. F., L. Aguirre, B. Vázquez, and J. Ortega. 2004. Phyllostomus hastatus. Mammalian Species 722:1–6.
Santos, C. L. C., A. C. N. Pereira, V. J. C. Bastos, G. Graciolli, and J. M. M. Rebêlo. 2013. Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica 58:207–214.
Schuh, R. T., and J. A. Slater. 1995. The true bugs of the world (Hemiptera: Heteroptera). Classification and Natural History Cornell University Press, Ithaca. New York, U. S. A.
Sikes, R. 2016. 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97(3):663–688.
Tarquino-Carbonell, A., K. Gutiérrez-Díaz, E. Galindo-Espinosa, G. Reinoso-Flórez, S. Solari, S. and R. Guerrero. 2015. Ectoparasites associated with bats in northeastern Tolima, Colombia. Mastozoología Neotropical 22:349-358.
Tasmitt, J. R., and I. Fox. 1970. Records of bat ectoparasites from the Caribbean region (Siphonaptera, Acarina, Diptera). Canadian Journal of Zoology 48:1093-1097.
ter Hofstede, H., and M. B. Fenton. 2005. Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. Journal of Zoology 266:333–340.
ter Hofstede H.M., M.B. Fenton, and J.O. Whitaker Jr. 2004. Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology 82:616-626.
Theodor, O. 1967. An illustrated catalogue of the Rothschild collection of Nycteribiidae (Diptera) in the British Museum (Natural History). British Museum of Natural History. London, England.
Timm, R.M., and R.K. Laval. 1998. A field key to the bats of Costa Rica. Ocassional publication series, University of Kansas, Center of Latin American Studies 22:1-30.
Tuttle, M. D. 1970. Distribution and zoogeography of Peruvian bats, with comments on natural history. University of Kansas. Science Bulletin 49:45–86.
Ueshima, N. 1972. New World Polyctenidae (Hemiptera), with special reference to Venezuelan species. Brigham Young University Science Bulletin 17:13-21.
Wenzel, R.L. 1976. The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin 20:177.
Wenzel, R., J. Tipton, and A. Kiewlicz. 1966. The streblid batflies of Panama (Diptera: Streblidae). Pp: 405-675 in: Wenzel, L. y Tipton, V. (eds). Ectoparasites of Panama. Field Museum of Natural History. Chicago.
Whitaker, J., C. Ritzi, and C. Dick. 2009. Collecting and preserving bats ectoparasites. Pp: 806 – 827 in: Ecological and Behavioral Methods for the Study of Bats. Kunz, T. y Parson, S. eds. Second edition.
Zhang, L., S. Parsons, P. Daszak, L. Wei, G. Zhu, and S. Zhang. 2010. Variation in the abundance of ectoparasitic mites of flat-headed bats. Journal of Mammalogy 91:136–143.
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