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Sex biases in parasitism of neotropical bats by bat flies (Diptera: Streblidae)

Published online by Cambridge University Press:  01 July 2008

Bruce D. Patterson ,
Carl W. Dick  and
Katharina Dittmar
Bruce D. Patterson*
Affiliation:
Department of Zoology, 1400 S. Lake Shore Dr., Field Museum of Natural History, Chicago, IL 60605-2496, USA
Carl W. Dick
Affiliation:
Department of Zoology, 1400 S. Lake Shore Dr., Field Museum of Natural History, Chicago, IL 60605-2496, USA
Katharina Dittmar
Affiliation:
Department of Zoology, 1400 S. Lake Shore Dr., Field Museum of Natural History, Chicago, IL 60605-2496, USA Department of Biological Sciences, State University of New York at Buffalo, 109 Cooke Hall, Buffalo, NY 14260, USA
*
1Corresponding author. Email: bpatterson@fieldmuseum.org
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Abstract

We describe levels of parasitism of ectoparasitic bat flies (Hippoboscoidea: Streblidae) on male and female bats from an extensive Neotropical survey. The collection resulted from coordinated vertebrate-parasite surveys undertaken by the Smithsonian Venezuelan Project (SVP) from 1965–1968, which sexed 24 978 bats of 130 species. Streblid parasites were recovered from 6935 individuals of 87 bat species, but only 47 species were captured frequently enough (≥ 20 infested individuals) to permit reliable estimates of streblid parasitism on males and females. Well-sampled species included 39 phyllostomids, four mormoopids, two noctilionids, one natalid and one molossid. Prevalence of streblid parasitism (proportion of individuals infested) of male and female bats was generally not significantly different, and averaged 0.34 across infested species. In species-level analyses assessed against captures, significant sex differences in infestation levels were noted in six species; all had mean prevalence below 0.5 and females were parasitized disproportionately in each. Sex differences in total numbers of flies were noted in 21 species, and in 16 of these, females carried disproportionately heavy loads. Sex differences were also found for eight species of bat in the number of fly species infesting an individual; seven of eight showed heavier female parasitism. In analyses weighted by infestation levels, sex differences in total number of flies were found in only 12 species, with seven showing excessive parasitism of females, and no species showed sex differences in the number of fly species infesting them. These significant biases were not associated with sexual size dimorphism among the bat species. Generally higher levels of parasitism among female bats accords with theory, given their generally higher survivorship and enhanced probabilities of lateral and vertical transmission of host-specific parasites, but contrasts with patterns shown by many other parasitic arthropods. Future analyses should target social groupings of bats, not passively sampled foragers, to better address the mechanisms responsible for this pattern.

Keywords

ChiropteraectoparasitesNeotropicsparasitismsex ratiosVenezuela
Type
Research Article
Information
Journal of Tropical Ecology , Volume 24 , Issue 4 , July 2008 , pp. 387 - 396
Copyright
Copyright © Cambridge University Press 2008

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References

LITERATURE CITED

BERGER, J., STACEY, P. B., BELLIS, L. & JOHNSON, M. P. 2001. A mammalian predator-prey imbalance: grizzly bear and wolf extinction affect avian neotropical migrants. Ecological Applications 11:947–960.Google Scholar
BERTOLA, P. B., AIRES, C. C., FAVORITO, S. E., GRACIOLLI, G., AMAKU, M., PINTO, D. A. & ROCHA, R. 2005. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, Sao Paulo, Brazil: parasitism rates and host-parasite associations. Memorias do Instituto Oswaldo Cruz 100:25–32.Google Scholar
BIZE, P., JEANNERET, C., KLOPFENSTEIN, A. & ROULIN, A. 2008. What makes a host profitable? Parasites balance host nutritive resources against immunity. American Naturalist 171:107–118.CrossRefGoogle ScholarPubMed
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575–583.CrossRefGoogle Scholar
CHRISTE, P., ARLETTAZ, R. & VOGEL, P. 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.CrossRefGoogle Scholar
CHRISTE, P., GLAIZOT, O., EVANNO, G., BRUYNDONCKX, N., DEVEVEY, G., YANNIC, G., PATTHEY, P., MAEDER, A., VOGEL, P. & ARLETTAZ, R. 2007. Host sex and ectoparasites choice: preference for, and higher survival on female hosts. Journal of Animal Ecology 76:703–710.Google Scholar
COGGINS, J. R. 1988. Methods for the ecological study of bat endoparasites. Pp. 475–489 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, DC.Google Scholar
DICK, C. W. 2005. Ecology and host specificity of bat flies (Diptera: Streblidae) and their chiropteran hosts. Ph.D. Dissertation thesis, Texas Tech University.Google Scholar
DICK, C. W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology 32:446–450.CrossRefGoogle Scholar
DICK, C. W. & DICK, S. C. 2006. Effects of prior infestation on host choice of bat flies (Diptera: Streblidae). Journal of Medical Entomology 43:433–436.Google Scholar
DICK, C. W. & GETTINGER, D. 2005. A faunal survey of streblid flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology 91:1015–1024.Google Scholar
DICK, C. W. & PATTERSON, B. D. 2006. Bat flies – obligate ectoparasites of bats. Pp. 179–194 in Morand, S., Krasnov, B. & Poulin, R. (eds.). Micromammals and macroparasites: from evolutionary ecology to management. Springer-Verlag, Tokyo.Google Scholar
DICK, C. W. & PATTERSON, B. D. 2007. Against all odds: explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology 37:871– 876.Google Scholar
DICK, C. W., GANNON, M. R., LITTLE, W. E. & PATRICK, M. J. 2003. Ectoparasite associations of bats from central Pennsylvania. Journal of Medical Entomology 40:813–819.Google Scholar
DITTMAR, K., PORTER, M. L., MURRAY, S. & WHITING, M. F. 2006. Molecular phylogenetic analysis of nycteribiid and streblid bat flies (Diptera: Brachycera, Calyptratae): implications for host associations and phylogeographic origins. Molecular Phylogenetics and Evolution 38:155–170.Google Scholar
FOLSTAD, I. & KARTER, A. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist 139:603–622.Google Scholar
FRITZ, G. N. 1983. Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology 20:1–10.Google Scholar
GIORGI, M. S., ARLETTAZ, R., CHRISTE, P. & VOGEL, P. 2001. The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proceedings of the Royal Society of London, Series B 268:2071–2075.CrossRefGoogle ScholarPubMed
HANDLEY, C. O. 1976. Mammals of the Smithsonian Venezuela Project. Brigham Young University Science Bulletin. Biological Series 20:1–89.CrossRefGoogle Scholar
HEITHAUS, E. R. 1982. Coevolution between bats and plants. Pp. 327–367 in Kunz, T. H. (ed.). Ecology of bats. Plenum Press, New York.Google Scholar
HUTCHINSON, G. E. 1959. Homage to Santa Rosalia or why are there so many kinds of animals? American Naturalist 93:145–159.CrossRefGoogle Scholar
KALKO, E. K. V. 1997. Diversity in tropical bats. Pp. 13–43 in Ulrich, H. (ed.). Tropical biodiversity and systematics. Proceedings of the International Symposium on Biodiversity and Systematics in Tropical Ecosystems, 1994. Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn.Google Scholar
KOMENO, C. A. & LINHARES, A. X. 1999. Batflies parasitic on some phyllostomid bats in southeastern Brazil: parasitism rates and host-parasite relationships. Memorias do Instituto Oswaldo Cruz 94:151–156.Google Scholar
KRASNOV, B., SHENBROT, G. & KHOKHLOVA, I. 2002. The effect of host density on ectoparasite distribution: an example of a rodent parasitized by fleas. Ecology 83:164–175.Google Scholar
KRASNOV, B. R., MOUILLOT, D., SHENBROT, G. I., KHOKHLOVA, I. S. & POULIN, R. 2005. Abundance patterns and coexistence processes in communities of fleas parasitic on small mammals. Ecography 28:453–464.CrossRefGoogle Scholar
KUNZ, T. H. 1982. Roosting ecology. Pp. 1–55 in Kunz, T. H. (ed.). Ecology of bats. Plenum Press, New York.CrossRefGoogle Scholar
LEWIS, S. E. 1995. Roost fidelity of bats: a review. Journal of Mammalogy 76:481–496.Google Scholar
LIM, B. K. & ENGSTROM, M. D. 2004. Mammals of Iwokrama Forest. Proceedings, Academy of Natural Sciences, Philadelphia 154:71–108.Google Scholar
LINARES, O. J. 1998. Mamíferos de Venezuela. Sociedad Conservacionista Audubon de Venezuela, Caracas. 691 pp.Google Scholar
LÓPEZ-GONZÁLEZ, C. 2004. Ecological zoogeography of the bats of Paraguay. Journal of Biogeography 31:33–45.CrossRefGoogle Scholar
MACARTHUR, R. H. 1972. Geographical ecology: patterns in the distribution of species. Harper and Row, New York. 269 pp.Google Scholar
MARSHALL, A. G. 1981. The ecology of ectoparasitic insects. Academic Press, London. 459 pp.Google Scholar
MARSHALL, A. G. 1982. Ecology of insects ectoparasitic on bats. Pp. 369–401 in Kunz, T. H. (ed.). Ecology of bats. Plenum Press, New York.CrossRefGoogle Scholar
MCCRACKEN, G. F. 1984. Communal nursing in Mexican free-tailed bat maternity colonies. Science 223:1090–1091.Google Scholar
MEAD-BRIGGS, A. R. & RUDGE, A. J. B. 1960. Breeding of the rabbit flea, Spilopsyllus cuniculi (Dale): requirement of a ‘factor’ from a pregnant rabbit for ovarian maturation. Nature 187:1136.Google Scholar
MORAN, M. D. 2003. Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405.Google Scholar
MORAND, S., KRASNOV, B. R. & POULIN, R. 2006. Micromammals and macroparasites: from evolutionary ecology to management. Springer, Tokyo. 647 pp.CrossRefGoogle Scholar
MOURA, M. O., BORDIGNON, M. O. & GRACIOLLI, G. 2003. Host characteristics do not affect community structure of ectoparasites on the fishing bat Noctilio leporinus (L., 1758) (Mammalia: Chiroptera). Memorias do Instituto Oswaldo Cruz 98:811–815.CrossRefGoogle Scholar
MUÑOZ-ROMO, M. 2006. Ethogram and diurnal activities of a colony of Artibeus lituratus (Phyllostomidae: Stenodermatinae). Acta Chiropterologica 8:231–238.Google Scholar
MYERS, N. 1992. The primary source: tropical forests and our future. Norton, New York. 448 pp.Google Scholar
OVERAL, W. L. 1980. Host-relations of the batfly Megistopoda aranea (Diptera: Streblidae) in Panama. University of Kansas Science Bulletin 52:1–20.Google Scholar
PACKER, C., HOLT, R. D., HUDSON, P. J., LAFFERTY, K. D. & DOBSON, A. P. 2003. Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecology Letters 6:797–802.Google Scholar
PATTERSON, B. D., WILLIG, M. R. & STEVENS, R. D. 2003. Trophic strategies, niche partitioning, and patterns of ecological organization. Pp. 536–579 in Kunz, T. H. & Fenton, M. B. (eds.). Bat ecology. University of Chicago Press, Chicago.Google Scholar
PATTERSON, B. D., DICK, C. W. & DITTMAR, K. 2007. Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23:177–189.Google Scholar
POULIN, R. 1996. Sexual inequalities in helminth infections: a cost of being a male? American Naturalist 147:287–295.Google Scholar
POULIN, R. 1998. Evolutionary ecology of parasites: from individuals to communities. Chapman and Hall, London. 212 pp.Google Scholar
POULIN, R. 2007. Evolutionary ecology of parasites. (Second edition). Princeton University Press, Princeton. 332 pp.Google Scholar
PRESLEY, S. J. 2007. Streblid bat fly assemblage structure on Paraguayan Noctilio leporinus (Chiroptera: Noctilionidae): nestedness and species co-occurrence. Journal of Tropical Ecology 23:409–417.Google Scholar
PRESLEY, S. J. & WILLIG, M. R. 2008. Intraspecific patterns of ectoparasite abundances on Paraguayan bats: effects of host sex and body size. Journal of Tropical Ecology 24:75–83.Google Scholar
RALLS, K. 1976. Mammals in which females are larger than males. Quarterly Review of Biology 51:245–276.CrossRefGoogle ScholarPubMed
RECKARDT, K. & KERTH, G. 2006. The reproductive success of the parasitic bat fly Basilia nana (Diptera: Nycteribiidae) is affected by the low roost fidelity of its host, the Bechstein's bat (Myotis bechsteinii). Parasitology Research 98:237–243.CrossRefGoogle ScholarPubMed
ROBERTS, L. & JANOVY, J. 2000. Foundations of parasitology. (Sixth edition). McGraw-Hill Companies, Dubuque. 688 pp.Google Scholar
ROTHSCHILD, M. & FORD, B. 1964. Breeding of the rabbit flea (Spilopsyllus cuniculi (Dale)) controlled by the reproductive hormones of the host. Nature 201:103–104.Google Scholar
SCHALK, G. & FORBES, M. R. 1997. Male biases in parasitism of mammals: effects of study type, host age and parasite taxon. Oikos 78:67–74.Google Scholar
SIMMONS, N. B. 2005. Chiroptera. Pp. 312–529 in Wilson, D. E. & Reeder, D. A. M. (eds.). Mammal species of the world: a taxonomic and geographic reference, vol. 1. (Third edition). Johns Hopkins University Press, Baltimore.Google Scholar
SOLARI, S., PACHECO, V., LUNA, L., VELAZCO, P. M. & PATTERSON, B. D. 2006. Mammals of the Manu Biosphere Reserve. Pp. 13–22 in Patterson, B. D., Stotz, D. F. & Solari, S. (eds.). Mammals and birds of the Manu Biosphere Reserve, Peru. Fieldiana: Zoology, new series 110. Field Museum of Natural History, Chicago.Google Scholar
TELLO, J. S., STEVENS, R. D. & DICK, C. W. 2008. Patterns of species co-occurrence and density compensation: a test for interspecific competition in bat ectoparasite communities. Oikos 117:693–702.Google Scholar
TER HOFSTEDE, H. M., FENTON, M. B. & WHITAKER, J. O. 2004. Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology 82:616–626.CrossRefGoogle Scholar
TERBORGH, J. 1988. The big things that run the world – a sequel to E. O. Wilson. Conservation Biology 2:402–403.CrossRefGoogle Scholar
THOMPSON, J. N. 1999. The evolution of species interactions. Science 284:2116–2118.Google Scholar
TIMM, R. M. 1987. Tent construction by bats of the genera Artibeus and Uroderma. Pp. 187–212 in Patterson, B. D. & Timm, R. M. (eds.). Studies in Neotropical Mammalogy. Essays in honor of Philip Hershkovitz. Fieldiana: Zoology, new series 39. Field Museum of Natural History, Chicago.Google Scholar
TUTTLE, M. D. 1983. Can rain forests survive without bats? Bats 1:1–2.Google Scholar
WENZEL, R. L. 1976. The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin. Biological Series 20:1–177.Google Scholar
WENZEL, R. L., TIPTON, V. J. & KIEWLICZ, A. 1966. The streblid batflies of Panama (Diptera Calypterae: Streblidae). Pp. 405–675 in Wenzel, R. L. & Tipton, V. J. (eds.). Ectoparasites of Panama. Field Museum of Natural History, Chicago.CrossRefGoogle Scholar
WHITAKER, J. O. 1988. Collecting and preserving ectoparasites for ecological study. Pp. 459–474 in Kunz, T. H. (ed.). Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, DC.Google Scholar
WHITAKER, J. O., WALTERS, B. L., CASTOR, L. K., RITZI, C. M. & WILSON, N. 2007. Host and distribution lists of mites (Acari), parasitic and phoretic, in the hair or on the skin of North American wild mammals north of Mexico: records since 1974. Faculty Publications from the Harold W. Manter Laboratory of Parasitology, University of Nebraska, Lincoln. 173 pp.Google Scholar
WHITEMAN, N. K. & PARKER, P. G. 2004. Effects of host sociality on ectoparasite population biology. Journal of Parasitology 90:939–947.CrossRefGoogle ScholarPubMed
WILKINSON, G. S. 2003. Social and vocal complexity in bats. Pp. 322–341 in Waal, F. B. M. d. & Tyack, P. L. (eds.). Animal social complexity: intelligence, culture and individualized societies. Harvard University Press, Cambridge.CrossRefGoogle Scholar
WOHLAND, P. 2000. Grooming behavior and parasite loads in the greater horseshoe bat (Rhinolophus femurequinum). Diploma thesis, University of Konstanz.Google Scholar
ZAHN, A. & RUPP, D. 2004. Ectoparasite load in European vespertilionid bats. Journal of Zoology 262:383–391.Google Scholar