Parasitism of bat flies (Nycteribiidae and Streblidae) on bats in urban environments: lower prevalence, infracommunities, and specificity

• Autorzy: Urbieta G.L. , Torres J.M. , Carvalho Dos Anjos E.A. , Espinola Carvalho C.M. , Graciolli G.
• Języki publikacji: EN

Abstrakty

EN

Studies involving parasitism between ectoparasitic flies and bats are scarce for urban environments, which makes it difficult to find association patterns in these altered environments. Herein, we describe the bat flies community, and estimate the prevalence, mean intensity of infestation, infracommunities, and specificity of bat fliesassociations in urban remnants of Cerrado. We collected 371 bat flies of 14 species and 944 bats of 17 species. The most abundant species of bats were Artibeus planirostris (n = 312), Artibeus lituratus (n = 197), Carollia perspicillata (n = 124) and Platyrrhinus lineatus (n = 110). Regarding bat flies, Megistopoda aranea (n = 148) and Trichobius joblingi (n = 118) were the most abundant. The prevalence of bat flies ranged from 0.3 to 43.5% and the mean infestation intensity from 1 to 12 (mean general of 2.04). We found 16 bat flies infracommunities on the most representative hosts (n > 30). Concerning specificity, 71% of bat flies were associated with a single host species (monoxenic). Our results indicate that bats were most parasitized by a single bat flies species, and prevalence and specificity between bat flies and bats were lower in these urban environments.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2018
• Tom: 20
• Numer: 2
• Opis fizyczny: p.511-518,fig.,ref.

Twórcy

autor

Urbieta G.L.

• Programa de Pos-Graduacao em Biologia Animal, Laboratorio de Sistematica, Ecologia e Evolucao (LSEE), Instituto de Biociencias (INBIO), Universidade Federal de Mato Grosso do Sul (UFMS), 79090-900, Campo Grande, MS, Brazil

autor

Torres J.M.

• Programa de Pos-Graduacao em Biotecnologia, Universidade Catolica Dom Bosco (UCDB), Campo Grande, MS, Brazil

autor

Carvalho Dos Anjos E.A.

• Bolsista CAPES - Proc. Number 1218-13-1, University of Manitoba,Biological Sciences Building, Winnipeg, MB R3T 2N2, Canada

autor

Espinola Carvalho C.M.

• Programa de Pos-Graduacao em Biotecnologia, Universidade Catolica Dom Bosco (UCDB), Campo Grande, MS, Brazil

autor

Graciolli G.

• Programa de Pos-Graduacao em Biologia Animal, Laboratorio de Sistematica, Ecologia e Evolucao (LSEE), Instituto de Biociencias (INBIO), Universidade Federal de Mato Grosso do Sul (UFMS), 79090-900, Campo Grande, MS, Brazil

Bibliografia

• 1. Aguiar, L. M. S., and Y. Antonini. 2016. Prevalence and intensity of Streblidae in bats from a Neotropical savanna region in Brazil. Folia Parasitologica, 63: 1–8. Google Scholar
• 2. Aguirre, L. F., A. Vargas, and S. Solari. 2009. Clave de campo para la identificacion de los murcielagos de Bolivia. Centro de Estudios en Biologia Teorica y Aplicada, Etreus, Cochabamba, 38 pp. Google Scholar
• 3. Barbier, E., and G. Graciolli. 2016. Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts, aggregation, prevalence, infestation intensity, and infracommunities. Studies on Neotropical Fauna and Environment, 51: 176–187. Google Scholar
• 4. Barbier, E., and E. Bernard. 2017. From the Atlantic Forest to the borders of Amazonia: species richness, distribution, and host association of ectoparasitic flies (Diptera: Nycteribiidae and Streblidae) in northeastern Brazil. Parasitology Research, 116: 3043–3055. Google Scholar
• 5. Barbier, E., F. Hintze, C. Jardelino, and E. Bernard. 2018. First record of the bat ectoparasitic fly Strebla proxima Wenzel, 1976 (Diptera: Streblidae) from Brazil. Entomological News, 127: 369–374. Google Scholar
• 6. Barquez, R. M., and M. M. Diaz. 2009. Los murcielagos de Argentina: clave de identificacion [Key to the bats of Argen tina]. Publicacion Especial PCMA (Programa de Conserva cion de los Murcielagos de Argentina), Tucuman, 80 pp. Google Scholar
• 7. Bertola, P. B., C. C. Aires, S. E. Favorito, G. Graciolli, M. Amaku, and R. Pinto-Da-Rocha. 2005. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, Sao Paulo, Brazil: parasitismo rates and host-parasite associations. Me morias do Instituto Oswaldo Cruz, 100: 25–32. Google Scholar
• 8. Bolivar-Cime, B., A. Cuzim-Koyoc, E. Reyes-Novelo, J. B. Morales-Malacara, J. Laborde, and R. Flores-Peredo. 2018. Habitat fragmentation and the prevalence of parasites (Diptera, Streblidae) on three phyllostomid bat species. Biotropica, 50: 90–97. Google Scholar
• 9. Bordes, F., S. Morand, and R. Guerrero. 2008. Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia, 158: 109–116. Google Scholar
• 10. Buczkowski, G., and D. S. Richmond. 2012. The effect of ur banization on ant abundance and diversity: a temporal examination of factors affecting biodiversity. PLoS One, 7: e41729. Google Scholar
• 11. Bush, A. O., J. M. Lafferty, J. M. LOTZ, and A. W. Sho Stak. 1997. Parasitology meets ecology in its own terms: Margolis et al. revisited. Journal of Parasitology, 83: 575–583. Google Scholar
• 12. Combes, C. 1991. Evolution of parasite life cycles. Pp. 62–82, in Parasite-host associations: coexistence or conflict? ( C. A. Toft and L. Boris, eds.). Oxford University Press, Oxford, 384 pp. Google Scholar
• 13. Dar, P. A., and Z. A. Reshi. 2014. Components, processes and consequences of biotic homogenization: a review. Contemporary Problems of Ecology, 7: 123–136. Google Scholar
• 14. Dick, C. W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology, 32: 446–450. Google Scholar
• 15. Dick, C. W., and D. Gettinger. 2005. A faunal survey of streblid bat flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology, 91: 1015–1024. Google Scholar
• 16. Dick, C. W., and B. D. Patterson. 2007. Against all odds: explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology, 37: 871–876. Google Scholar
• 17. Dick, C. W., C. E. L. Esberard, G. Graciolli, H. G. Bergallo, and D. Gettinger. 2009. Assessing host specificity of obligate ectoparasites in the absence of dispersal barriers. Parasitology Research, 105: 1345–1349. Google Scholar
• 18. Dittmar, K., S. F. Morse, C. W. Dick, and B. D. Patterson. 2015. Bat fly evolution form the Eocene to the present (Hippoboscoidea: Streblidae and Nycteribiidae. Pp. 246–264, in Parasite diversity and diversification: evolutionary ecology meets phylogenetics ( S. Morand, B. R. Krasnov, and D. T. J. Littlewood, eds.). Cambridge University Press, Cambridge, 488 pp. Google Scholar
• 19. Dornelles, G. D. P., and G. Graciolli. 2017. Streblidae bat flies on phyllostomid bats from an island off the coast of Sao Paulo, Brazil. Papeis Avulsos de Zoologia, 57: 31–36. Google Scholar
• 20. Dornelles, G. D. P., G. Graciolli, O. Anderson, and M. O. Bordignon. 2017. Infracommunities of Streblidae and Nycte ribiidae (Diptera) on bats in an ecotone area between Cerrado and Atlantic Forest in the state of Mato Grosso do Sul. Iheringia. Serie Zoologia, 107: e2017044. Google Scholar
• 21. Eriksson, A., G. Graciolli, and E. Fischer. 2011. Bat flies on phyllostomid hosts in the Cerrado region: component community, prevalence and intensity of parasitism. Memorias do Instituto Oswaldo Cruz, 106: 274–278. Google Scholar
• 22. Feijo, A., P. A. Rocha, and S. L. Althoff. 2015. New species of Histiotus (Chiroptera: Vespertilionidae) from northeastern Brazil. Zootaxa, 4048: 412–427. Google Scholar
• 23. Frank, H. K., C. D. Mendenhall, S. D. Judson, G. C. Daily, and E. A. Hadly. 2016. Anthropogenic impacts on Costa Rican bat parasitism are sex specific. Ecology and Evolution, 6: 4898–4909. Google Scholar
• 24. Fritz, G. N. 1983. Biology and ecology of bat flies (Diptera: Streblidae) on bats of the genus Carollia. Journal of Medicine Entomology, 20: 1–10. Google Scholar
• 25. Gardner, A. L. 2008. Mammals of South America. University of Chicago Press, Chicago, 669 pp. Google Scholar
• 26. Graciolli, G. 2004. Nycteribiidae (Diptera, Hippoboscoidea) no sul do Brasil. Revista Brasileira de Zoologia, 21: 971–985. Google Scholar
• 27. Graciolli, G. 2017. Streblidae in Catalogo Taxonomico da Fauna do Brasil. Brazil, PNUD. Available at http://fauna.jbrj.gov.br/fauna/faunadobrasil/2624. Google Scholar
• 28. Graciolli, G., and C. J. B. Carvalho. 2001. Moscas ectoparasitas (Diptera, Hippoboscoidea, Nycteribiidae) de morcegos (Mammalia, Chiroptera) do estado do Parana, Brasil. II. Streb lidae. Chave pictorica para generos e especies. Revista Brasileira Zoologia, 18: 907–960. Google Scholar
• 29. Graciolli, G., A. G. Autino, and G. L. Claps. 2007. Catalogue of American Nycteribiidae (Diptera, Hippoboscoidea). Revista Brasileira de Entomologia, 51: 142–159. Google Scholar
• 30. Graciolli, G., A. A. Azevedo, M. Arzua, D. M. Barrosbattesi, and P. M. Linardi. 2008. Artropodos ectoparasitos de morcegos no Brasil. Pp. 123–138, in Morcegos no Brasil: biologia, sistematica, ecologia e conservacao, 1st edition ( G. S. Pacheco, R. V. Marques, and C. E. L. Esberard, eds.). Armazem Digital, Porto Alegre, 568 pp. Google Scholar
• 31. Gregorin, R., and V. A. Taddei. 2002. Chave artificial para a identificacao de molossideos brasileiros (Mammalia: Chiroptera). Mastozoologia Neotropical, 9: 13–32. Google Scholar
• 32. Gregorin, R., L. M. Moras, L. H. Acosta, L. K. Vasconcelos, J. L. poma, F. R. Santos, and R. C. Paca. 2016. A new spe cies of Eumops (Chiroptera: Molossidae) from southeastern Brazil and Bolivia. Mammalian Biology, 81: 235–246. Google Scholar
• 33. Guerrero, R. 1994a. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. II. Los grupos: pallidus, caecus, major, uniformis y longipes del genero Trichobius Gervais, 1844. Acta Biologica Venezuelica, 15: 1–18. Google Scholar
• 34. Guerrero, R. 1994b. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. IV. Trichobiinae con alas desarrolladas. Boletin de Entomologia Venezolana, 9: 161–192. Google Scholar
• 35. Guerrero, R. 1995. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. V. Trichobiinae con alas reducidas o ausentes y miscelaneos. Boletin de Entomologia Venezolana, 10: 135–160. Google Scholar
• 36. Guerrero, R. 1996. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia, Chiroptera) del Nuevo Mundo. VI. Streblinae. Acta Biologica Venezu elica, 16: 1–26. Google Scholar
• 37. Guerrero, R. 1997. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. VII. Lista de especies, hospedadores y paises. Acta Biologica Venezuelica, 17: 9–24. Google Scholar
• 38. Hansen, A. J., R. L. Knigth, J. M. Marzluff, S. Powell, K. Brown, P. H. Gude, and K. Jones. 2005. Effects of exurban development on biodiversity: patterns, mechanisms, and research needs. Ecological Applications, 15: 1893–1905. Google Scholar
• 39. Hofstede, H. M., and M. B. Fenton. 2005. Relationships between roost preferences, ectoparasite density and grooming behaviour of neotropical bats. Journal of Zoology (London), 266: 333–340. Google Scholar
• 40. Ingram, T., and J. B. Shurin. 2009. Trait-based assembly and phylogenetic structure in northeast Pacific rockfish assemblages. Ecology, 90: 2444–2453. Google Scholar
• 41. Jung, K., and E. K. V. Kalko. 2011. Adaptability and vulnerability of high flying Neotropical aerial insectivorous bats to urbanization. Diversity and Distributions, 17: 262–274. Google Scholar
• 42. Krasnov, B. R., S. Pilosof, M. Stanko, S. Morand, N. P. Korallo-Vinarskaya, M. V. Vinarski, and R. Poulin. 2014. Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: limiting similarity versus environmental filtering. Oikos, 123: 63–70. Google Scholar
• 43. Komeno, C. A., and A. X. Linhares. 1999. Bat flies parasitic on some Phyllostomidae bats in southeastern Brazil: Parasitism rates and host-parasite relationships. Memorias do Instituto Oswaldo Cruz, 94: 151–156. Google Scholar
• 44. Lourenco, E. C., P. M. P. Patricio, M. C. Pinheiro, R. M. Dias, and K. M. Famadas. 2014. Streblidae (Diptera) on bats (Chiroptera) in an area of Atlantic Forest, state of Rio de Ja neiro. Brazilian Journal of Veterinary Parasitology, 23: 164–170. Google Scholar
• 45. Marshall, A. G. (ed.). 1981. The ecology of Ectoparasites Insects. Academic Press, London, 459 pp. Google Scholar
• 46. Marshall, A. G. 1982. Ecology of insects ectoparasitic on bats. Pp. 369–401, in Ecology of bats ( T. H. Kunz, ed.). Plenum Publishing, New York, 450 pp. Google Scholar
• 47. Mbora, D. N. M., and M. Mcpeek. 2009. Host density and human activities mediate increased parasite prevalence and richness in primates threatened by habitat loss and fragmentation. Journal of Animal Ecology, 78: 210–218. Google Scholar
• 48. MacGregor-Fors, I. 2011. Misconceptions or misunderstandings? On the standardization of basic terms of urban ecology. Landscape and Urban Planning, 100: 347–349. Google Scholar
• 49. McKinney, M. L. 2002. Urbanization, biodiversity, and conservation. Bioscience, 52: 883–890. Google Scholar
• 50. Morand, S., and R. Poulin. 1998. Density, body mass and parasite species richness of terrestrial mammals. Evolutionary Ecology, 12: 717–727. Google Scholar
• 51. Moratelli, R., and D. Dias. 2015. A new species of nectarfeed ing bat, genus Lonchophylla, from the Caatinga of Brazil (Chiroptera, Phyllostomidae). ZooKeys, 514: 73–91. Google Scholar
• 52. Nogueira, M. R., I. P. Lima, R. Moratelli, V. C. Tavares, R. Gregorin, and A. L. Peracchi. 2014. Checklist of Brazilian bats, with comments on original records. Check List, 10: 808–821. Google Scholar
• 53. Ortega-Alvarez, R., and I. MacGregor-Fors. 2009. Living in the big city: effects of urban land-use on bird community structure, diversity, and composition. Landscape and Urban Planning, 90: 189–195. Google Scholar
• 54. Patterson, B. D., K. 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. Google Scholar
• 55. Pavan, C. A., E. D. Bobrowiec, and A. R. Percequillo. 2018. Geographic variation in a South American clade of mormoopid bats, Pteronotus (Phyllodia), with description of a new species. Journal of Mammalogy, 99: 624–645. Google Scholar
• 56. Peel, M. C., B. L. Finlayson, T. A. MacMahon. 2007. Updated world map of the Koppen-Geiger climate classification. Hydrology and Earth System Science, 11: 1633–1644. Google Scholar
• 57. Pilosof, S., C. W. Dick, C. Korine, B. D. Patterson, and B. R. Krasnov. 2012. Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism. PLoS ONE, 7: e41487. Google Scholar
• 58. Poulin, R., and D. Mouillot. 2005. Combining phylogenetic and ecological information into a new index of host specificity. Journal Parasitology, 91: 511–514. Google Scholar
• 59. Planurb [Instituto Municipal De Planejamento Urbano].2016. Perfil socio-economico de Campo Grande Estado do Mato Grosso do Sul. Available at http://www.portal.capital.ms.gov.br. Google Scholar
• 60. Presley, S. J. 2011. Interspecific aggregation of ectoparasites on bats: importance of hosts as habitats supersedes interspecific interactions. Oikos, 120: 832–841. Google Scholar
• 61. Reis, N. R., A. L. Peracchi, W. A. Pedro, and I. P. Lima (eds.). 2007. Morcegos do Brasil. Universidade Estadual de Londrina, Londrina, 253 pp. Google Scholar
• 62. Riley, S., E. Boydston, K. Crooks, and L. Lyren. 2010. Bobcats (Lynx rufus). Pp. 121–138, in Urban carnivores: ecology, conflict, and conservation ( S. D. Gehrt, S. P. D. Riley, and B. L. Cypher, eds.). Johns Hopkins University Press, Baltimore, 285 pp. Google Scholar
• 63. Rocha, P. A., M. V. Brandao, G. S. T. Garbino, I. N. Cunha, and C. C. Aires. 2016. First record of Salvin's big-eyed bat Chiroderma salvini Dobson, 1878 for Brazil. Mammalia, 80: 573–578. Google Scholar
• 64. Rozsa, L., J. Reiczigel, and G. Majoros. 2000. Quantifying parasites in samples of hosts. Journal of Parasitology, 86: 228–232. Google Scholar
• 65. Salkeld, D. J., K. A. Padgett, and K. A. A. Jones. 2013. A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecology Letters, 16: 679–686. Google Scholar
• 66. Santos, C. L. C., P. A. Dias, F. S. Rodrigues, and K. S. Lobato. 2009. Moscas ectoparasitas (Diptera: Streblidae) de morcegos (Mammalia: Chiroptera) do municipio de Sao Luis, MA: taxas de infestacao e associacoes parasito-hospedeiro. Neotropical Entomology, 38: 595–601. Google Scholar
• 67. Santos, C. L. C., A. C. N. Pereira, V. J. C. Bastos, G. Graciolli, and J. M. M. Rebelo. 2013. Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica, 58: 207–214. Google Scholar
• 68. Straube, F. C., and G. V. Bianconi. 2002. Sobre a grandeza e a unidade utilizada para estimar o esforco de captura com utilizacao de redes-de-neblina. Chiroptera Neotropical, 8: 150–152. Google Scholar
• 69. Urbieta, G. L., J. M. Torres, L. B. M. Almeida, A. Shinohara, and E. C. Anjos. 2014. Infestacao de morcegos (Mammalia, Chiroptera) por moscas do genero Megistopo da (Diptera, Streblidae) em um fragmento urbano de Cerrado de Campo Grande, Mato Grosso do Sul. Boletim da Socie dade Brasileira de Mastozoologia, 69: 10–13. Google Scholar
• 70. Vasconcelos, P. F., L. A. D. Falcao, G. Graciolli, and M. A. S. Borgens. 2016. Parasite-host interactions of bat flies (Diptera: Hippoboscoidea) in Brazilian tropical dry forests. Parasitology Research, 115: 367–377. Google Scholar
• 71. Wenzel, R. L., V. J. Tipton, and A. Kiewlicz. 1966. The streblid bat flies of Panama (Diptera: Calyptera: Streblidae). Pp. 405–675, in Ectoparasites of Panama ( R. L.Wenzel and V. J. Tipton, eds.). Field Museum of Natural History, Chicago, Illinois, 882 pp. Google Scholar

Identyfikatory

DOI

10.3161/15081109ACC2018.20.2.021