Parasitism by bat flies on an urban population of Cynopterus brachyotis in Singapore

• Autorzy: Lee V.N. , Mendenhall I.H. , Lee B.P.Y.-H. , Posa M.R.C.
• Języki publikacji: EN

Abstrakty

EN

This study characterizes the patterns of bat fly parasitism on Cynopterus brachyotis, the most common fruit bat in the tropical urban environment of Singapore. Mist netting was conducted over a period of five months in two secondary forest sites, where 211 unique individuals were captured and examined for ectoparasites. The relative density, prevalence and mean intensity of parasitism by the wingless nycteriibid Leptocyclopodia ferrarii ferrarii were compared with respect to sex, age and reproductive status of captured bats. The overall prevalence of parasitism was 40.3% and analyses revealed no significant differences in the three parameters when comparisons were made between demographic subgroups. However, adults, females and pregnant females had a higher prevalence of infestation, while juveniles, males and non-pregnant females had higher mean intensity of bat flies. Roosting behavior is likely to be the driving factor for parasite transmission, as bat flies are more likely to encounter females because of C. brachyotis' harembased social structure. No correlation was found between bat body condition and parasite load, even when the relationship was examined for juveniles and adults separately. The observation of a re-infestation within 46 days suggests that there is high intraindividual and intra-roost parasite transmission. Research into roost group size, distribution, site fidelity, and connectivity is needed to better understand the patterns and dynamics of parasitism on bats living in the urban environment.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2018
• Tom: 20
• Numer: 1
• Opis fizyczny: p.177-185,fig.,ref.

Twórcy

autor

Lee V.N.

• Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 129793, Singapore

autor

Mendenhall I.H.

• Program in Emerging Infectious Diseases, Duke-NUS Medical School, 8 College Road, Singapore 169857, Singapore

autor

Lee B.P.Y.-H.

• Centre for Urban Greenery and Ecology, National Parks Board, 1 Cluny Road, Singapore 259569, Singapore

autor

Posa M.R.C.

• Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 129793, Singapore

Bibliografia

• 1. Advani, R., and T. G. Vazirani. 1981. Studies on ectoparasites of bats of Rajasthan and Gujarat (India). Records of the Zoological Survey of India: Occasional Paper, 22: 1–155. Google Scholar
• 2. Alvarez, J. D. V., I. L. Lit, Jr. , and P. A. Alviola. 2015. Bat flies (Diptera: Nycteribiidae) from Mount Makiling, Luzon island: new host and distribution records, with a checklist of species found in the Philippines. Check List, 11: 1509. Google Scholar
• 3. Alvarez, J. D. V., I. L. Lit, Jr. , P. A. Alviola, E. A. Cosico, and E. G. Eres. 2016. A contribution to the ectoparasite fauna of bats in Mindoro Island, Philippines: I. Blood sucking Diptera (Nycteribiidae, Streblidae) and Siphonaptera (Ischnopsyllidae). International Journal of Tropical Insect Science, 36: 188–194. Google Scholar
• 4. Amarga, A. K. S., P. A. Alviola, I. L. Lit, Jr. , and S. A. Yap. 2017. Checklist of ectoparasitic arthropods among cavedwelling bats from Marinduque Island, Philippines. Checklist, 13: 2029. Google Scholar
• 5. Aroon, S., J. G. Hill III , T. Artchawakom, S. PinmongKhol Gul, S. Kupittayanant, and N. Thanee. 2015. Ectopara sites associated with bats in tropical forest of northeastern Thailand. Journal of Agricultural Technology, 11: 1781–1792. Google Scholar
• 6. Azhar, I., F. A. A. Khan, N. Ismail, and M. T. Abdullah. 2015. Checklist of bat flies (Diptera: Nycteribiidae and Streblidae) and their associated bat hosts in Malaysia. Checklist, 11: 1777. 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, São Paulo, Brazil: parasitism rates and host-parasite associations. Memórias do Instituto Oswaldo Cruz, 100: 25–32. Google Scholar
• 8. Bonaccorso, F. J., and N. Smythe. 1972. Punch-marking bats: an alternative to banding. Journal of Mammalogy, 53: 389–390. Google Scholar
• 9. Brunet-Rossinni, A. K., and G. S. Wilkinson. 2009. Methods for age estimation and the study of senescence in bats. Pp. 315–325, in Ecological and behavioral methods for the study of bats ( T. H. Kunz and S. Parsons, eds.). Johns Hopkins University Press, Baltimore, 920 pp. Google Scholar
• 10. Bumrungsri, S., W. Leelapaibul, and P. A. racey. 2007. Resource partitioning in sympatric Cynopterus bats in lowland tropical rain forest, Thailand. Biotropica, 39: 241–248. Google Scholar
• 11. Calabrese, J. M., J. L. Brunner, and R. S. Ostfeld. 2011. Partitioning the aggregation of parasites on hosts into intrinsic and extrinsic components via an extended Poissongamma mixture model. PLoS ONE, 6: e29215. Google Scholar
• 12. Campbell, C. 2008. The relationship between roosting ecology and degree of polygyny in harem-forming bats: perspectives from Cynopterus. Journal of Mammalogy, 89: 1351–1360. Google Scholar
• 13. Campbell, C., A. Zubaid, A. M. Adnan, and T. H. Kunz. 2006. Resource distribution in harem-forming Old World fruit bats: variations on a polygynous theme. Animal Behaviour, 72: 687–698. Google Scholar
• 14. Campbell, P., C. J. Scheider, A. M. Adnan, A. Zubaid, and T. H. Kunz. 2004. Phylogeny and phylogeography of Old World fruit bats in the Cynopterus brachyotis complex. Molecular Phylogenetics and Evolution, 33: 764–781. Google Scholar
• 15. Campbell, P., C. J. Scheider, A. M. Adnan, A. Zubaid, and T. H. Kunz. 2004. Phylogeny and phylogeography of Old World fruit bats in the Cynopterus brachyotis complex. Molecular Phylogenetics and Evolution, 33: 764–781. Google Scholar
• 16. Campbell, P., N. M. Reid, A. Zubaid, A. M. Adnan, and T. H. Kunz. 2006. Comparative roosting ecology of Cynopterus (Chiroptera: Pteropodidae) fruit bats in Peninsular Malaysia. Biotropica, 38: 725–734. Google Scholar
• 17. Christie, P., R. Arlettaz, and P. Vogel. 2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecology Letters, 3: 207–212. Google Scholar
• 18. Christie, P., M. S. 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. Google Scholar
• 19. Christie, P., O. Glaizot, G. Evanno, N. Bruyndonckx, G. Devevey, G. Yannic, P. Patthey, A. Maeder, P. Vogel, and R. Arlettaz. 2007. Host sex and ectoparasites choice: preference for, and higher survival on female hosts. Journal of Animal Ecology, 76: 703–710. Google Scholar
• 20. Dick, C. W., and B. D. Patterson. 2006. Bat flies: obligate ectoparasites of bats. Pp. 179–194, in Micromammals and macroparasites: from evolutionary ecology to management ( S. Morand, B. R. Krasnov, and R. Poulin, eds.). Springer Japan, Tokyo, 397 pp. Google Scholar
• 21. Francis, C. M. 2008. A field guide to the mammals of South-East Asia. New Holland Publishers, London, 392 pp. Google Scholar
• 22. Funakoshi, K., and A. Zubaid. 1997. Behavioural and reproductive ecology of the dog-faced fruit bats, Cynopterus brachyotis and C. horsfieldi, in a Malaysian rainforest. Mammal Study, 22: 95–108. Google Scholar
• 23. Gay, N., K. J. Olival, S. Bumrungsri, B. Siriaroonat, M. Bourgarel, and S. Morand. 2014. Parasite and viral species richness of Southeast Asian bats: fragmentation of area distribution matters. International Journal for Parasitology: Parasites and Wildlife, 3: 161–170. Google Scholar
• 24. Goldberg, T. L., A. J. Bennett, R. Kityo, J. H. Kuhn, and C. A. Chapman. 2017. Kanyawara virus: a novel rhabdovirus infecting newly discovered nycteribiid bat flies infesting previously unknown pteropodid bats in Uganda. Scientific Reports, 7: 5287. Google Scholar
• 25. Hart, B. L. 1992. Behavioral adaptations to parasites: an ethological approach. Journal of Parasitology, 78: 256–265. Google Scholar
• 26. Kingston, T. 2010. Research priorities for bat conservation in Southeast Asia: a consensus approach. Biodiversity and Conservation, 19: 471–484. Google Scholar
• 27. Lane, D. J. W., T. Kingston, and B. P. Y.-H. Lee. 2006. Dramatic decline bat species richness in Singapore, with implications for Southeast Asia. Biological Conservation, 131: 584–593. Google Scholar
• 28. Lehmann, T. 1993. Ectoparasites: direct impacts on host fitness. Parasitology Today, 9: 8–13. Google Scholar
• 29. Linhares, A. X., and C.A. Komeno. 2000. Trichobius joblingi, Aspidoptera falcata, and Megistopoda proxima (Diptera: Streblidae) parasitic on Carollia perspicillata and Sturnira lillium (Chiroptera: Phyllostomidae) in southeastern Brazil: sex ratios, seasonality, host site preference, and effect of parasitism on the host. Journal of Parasitology, 86: 167–170. Google Scholar
• 30. Maa, T. C. 1975. On new Diptera: Pupipara from the Oriental Region. Pacific Insects, 16: 465–486. Google Scholar
• 31. Marshall, A. G. 1982. Ecology of insects ectoparasitic on bats. Pp. 369 – 401, in Ecology of bats ( T. H. Kunz, ed.). Plenum Press, New York, 425 pp. Google Scholar
• 32. Mickleburgh, S. P., A. M. Huston, and P. A. Racey (comp.). 1992. Old World fruit bats: an action plan for their conservation. IUCN, Gland, Switzerland, 252 pp. Google Scholar
• 33. Mohd-Azlan, J., A. A. Tuen, and M. R. A. Rahman. 2010. Preliminary assessment of activity pattern and diet of the lesser dog-faced fruit bat, Cynopterus brachyotis in a dipterocarp forest, Sarawak, Borneo. Tropical Ecology, 51: 175–180. Google Scholar
• 34. Nunes, H., F. L. Rocha, and P. Cordeiro-Estrela. 2017. Bats in urban areas of Brazil: roosts, food resources and parasites in disturbed environments. Urban Ecosystems, 20: 953–969. Google Scholar
• 35. Olival, K. J., C. W. Dick, N. B. Simmons, J. C. Morales, D. J. Melnick, K. Dittmar, S. L. Perkins, P. Daszak, and R. De Salle. 2013. Lack of population genetic structure and host specificity in the bat fly, Cyclopodia horsfieldi, across species of Pteropus bats in Southeast Asia. Parasites and Vectors, 6: 231. Google Scholar
• 36. Pape, T., and F. C. Thompson (eds.). 2013. Systema Dipterorum, Version 1.5. Available at http://www.diptera.org/. Accessed on 22 August 2017. Google Scholar
• 37. Patterson, B. D., C. W. Dick, and K. Dittmar. 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera: Stre blidae). Journal of Tropical Ecology, 23: 177–189. Google Scholar
• 38. Patterson, B. D., C. W. Dick, and K. Dittmar. 2008. Sex biases in parasitism of neotropical bats by bat flies (Diptera: Streblidae). Journal of Tropical Ecology, 24: 387–396. Google Scholar
• 39. Pearce, R. D., and T. J. O'shea. 2007. Ectoparasites in an urban population of big brown bats (Eptesicus fuscus) in Colorado. Journal of Parasitology, 93: 518–530. Google Scholar
• 40. Pearce, R. D., T. J. O'shea, and B. A. Wunder. 2008. Evaluation of morphological indices and total body electrical conductivity to assess body composition in big brown bats. Acta Chiropterologica, 10: 153–159. Google Scholar
• 41. Phua, P. B., and R. T. Corlett. 1989. Seed dispersal by the lesser short-nosed fruit bat (Cynopterus brachyotis, Pteropodidae, Megachiroptera). Malayan Nature Journal, 42: 251–256. Google Scholar
• 42. Pierce, M. W., and M. Keith. 2011. Healing rates of wing membranes in two species of vespertilionid bats. African Bat Conservation News, 25: 3–5. Google Scholar
• 43. Pilosof, S., C. W. Dick, C. Korine, B. D. Patterson, and B. R. Krasnov. 2012. Effects of anthropogenic disturbance and climate change on patterns of bat fly parasitism. PLoS ONE, 7: e41487. Google Scholar
• 44. Postawa, T., and Z. Nagy. 2016. Variation of parasitism patterns in bats during hibernation: the effect of host species, resources, health status, and hibernation period. Parasitological Research, 115: 3767–3778. Google Scholar
• 45. R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at www.r-project.org. Google Scholar
• 46. Rajemison, F. I., O. S. N. Lalaivoniaina, A. Andrianarimisa, and S. M. Goodman. 2017a. Host-parasite relationships between a Malagasy fruit bat (Pteropodidae) and associated bat fly (Diptera: Nycteribiidae): seasonal variation of host body condition and the possible impact of parasite abundance. Acta Chiropterologica, 19: 229–238. Google Scholar
• 47. Rajemison, F. I., O. S. N. Lalaivoniaina, and S. M. Goodman. 2017b. Parasitism by Nycteribiidae and Streblidae flies (Diptera) of a Malagasy fruit bat (Pteropodidae): effects of body size and throat gland development on parasite abundance. Journal of Medical Entomology, 54: 805–811. Google Scholar
• 48. Russo, D., and L. Ancillotto. 2015. Sensitivity of bats to urbanization: a review. Mammalian Biology, 80: 205–212. Google Scholar
• 49. Sim, J. W. S., H. T. W. Tan, and I. M. Turner. 1992. Adinandra belukar: an anthropogenic heath forest in Singapore. Vegetatio, 102: 125–137. Google Scholar
• 50. Teo, R. C. H., and S. Rajathurai. 1997. Mammals, reptiles and amphibians in the nature reserves of Singapore — diversity, abundance and distribution. Gardens' Bulletin Singapore, 49: 353–425. Google Scholar
• 51. Ter 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
• 52. Theodor, O. 1967. An illustrated catalogue of the Rothschild collection of Nycteriibidae (Diptera) in the British Museum (Natural History). British Museum, London, 506 pp. Google Scholar
• 53. Van Vuren, P. J., M. Wiley, G. Palacios, N. Storm, S. McCulloch, W. Markotter, M. Birkhead, A. Kemp, and J. T. Paweska. 2016. Isolation of a novel fusogenic ortheovirus from Eucampsipoda africana bat flies in South Africa. Viruses, 8: 65. Google Scholar
• 54. Weaver, K. N., S. E. Alfano, A. R. Kronquist, and D. M. Reeder. 2009. Healing rates of wing punch wounds in freeranging little brown myotis (Myotis lucifugus). Acta Chiropterologica, 11: 220–223. Google Scholar
• 55. Yee, A. T. K., R. T. Corlett, S. C. Liew, and H. T. W. Tan. 2011. The vegetation of Singapore — an updated map. Garden's Bulletin Singapore, 63: 205–212. Google Scholar
• 56. Zahn, A., and D. Rupp. 2004. Ectoparasite load in European ves pertilionid bats. Journal of Zoology (London), 262: 383–391. Google Scholar

Identyfikatory

DOI

10.3161/15081109ACC2018.20.1.013