Oecologia

, Volume 158, Issue 1, pp 109–116

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain

  • Frédéric Bordes
  • Serge Morand
  • Guerrero Ricardo
Community Ecology - Original Paper

Abstract

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness.

Key words

Parasite species richness Tropical bats Roosting ecology Group size Body size 

Supplementary material

442_2008_1115_MOESM1_ESM.xls (38 kb)
Supplementary material (XLS 39 kb)

References

  1. Agnew P, Koella JC, Michalakis Y (2000) Host life history responses to parasitism. Microbes Infect 2:891–896PubMedCrossRefGoogle Scholar
  2. Altizer S, Nunn C, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Syst 34:517–547CrossRefGoogle Scholar
  3. Arneberg P (2002) Host population density and body mass as determinants of species richness in parasites communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25:88–94CrossRefGoogle Scholar
  4. Alzaga V, Vicente J, Villanua D, Acevedo P, Casas F, Gortazar C (2008) Body condition and parasite intensity correlates with escape capacity in Iberian hares. Behav Ecol Sociobiol 62:769–775CrossRefGoogle Scholar
  5. Bartonicka T, Gaisler J (2007) Seasonnal dynamics in the numbers of parasitic bugs (Heteroptera, Cimicidae): a possible cause of roost switching in bats (Chiroptera, Vespertilionidae). Parasitol Res 100:1323–1330PubMedCrossRefGoogle Scholar
  6. Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Lett 3:692–694PubMedCrossRefGoogle Scholar
  7. Clayton DH, Walther BA (2001) Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94:455–467CrossRefGoogle Scholar
  8. 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). Ecol Lett 3:207–212CrossRefGoogle Scholar
  9. Dick CW, Gannon MR, Little WE, Patrick M (2003) Ectoparasites associations of bats from Central Pennsylvania. J Med Entomol 40:813–819PubMedCrossRefGoogle Scholar
  10. Dick CW, Gettinger D (2005) A faunal survey of streblid flies (Diptera: Streblidae) associated with bats in Paraguay. J Parasitol 91:1015–1024PubMedCrossRefGoogle Scholar
  11. Dick CW, Graciolli G. (2006) Checklist of world Steblidae (Diptera:Hippoboscidae) found at http://www.fieldmuseum.org/aa/files/cdick/streblidae_checklist_eoct.06.pdf
  12. Dick CW, Patterson BD (2006) Bat flies: obligate ectoparasites of bats. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and macroparasites, from evolutionary ecology to management. Springer, Tokyo, pp 179–191CrossRefGoogle Scholar
  13. Dunbar RIM (1995) Neocortex size and group size in primates: a test of the hypothesis. J Hum Evol 28:282–287CrossRefGoogle Scholar
  14. Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6:178–190CrossRefGoogle Scholar
  15. Ezenwa V, Price SA, Altizer S, Vitone ND, Cook C (2006) Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos 115:526–537CrossRefGoogle Scholar
  16. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  17. Fitze PS, Tschirren B, Richner H (2004) Life history and fitness consequences of ectoparasites. J Anim Ecol 73:216–226CrossRefGoogle Scholar
  18. Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturix myoti) upon its bat host (Myotis myotis). Proc R Soc Lond B 268:2071–2075CrossRefGoogle Scholar
  19. Guégan JF, Morand S, Poulin R (2004) Are there general laws in parasite community ecology? The emergence of spatial parasitology and epidemiology. In: Thomas F, Guégan JF, Renaud F (eds) Parasitism and ecosystems. Oxford University Press, Oxford, pp 22–42Google Scholar
  20. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc Lond B 271:925–930CrossRefGoogle Scholar
  21. Holmstad PR, Hudson PJ, Skorping A (2005) The influence of a parasite community of a host population: a longitudinal study on willow ptarmigan and their parasites. Oikos 111:377–391CrossRefGoogle Scholar
  22. Irvine JT, Corbishley H, Pilkington JG, Albon SD (2006) Low levels of parasitic worms burdens may reduce body condition in free ranging red deer (Cervus elaphus). Parasitology 133:465–475PubMedCrossRefGoogle Scholar
  23. Jacobs LC (1996) The economy of winter: phenotypic plasticity in behavior and brain structure. Biol Bull 191:92–100PubMedCrossRefGoogle Scholar
  24. Jones KE, Purvis A, MacLarnon A, Bininda-Emonds ORP, Simmons NB (2002) A phylogenic supertree of the bats (Mammalia: Chiroptera). Biol Rev 77:223–259PubMedCrossRefGoogle Scholar
  25. Jones KE, Mac Larnon AM (2004) Affording large brains: testing hypotheses of mammalian brain evolution in bats. Am Nat 164:20–31CrossRefGoogle Scholar
  26. Kohkhlova IS, Krasnov BR, Kam M, Burdelova NI, Degen AA (2002) Energy costs of parasitism by the flea Xenopsylla ramenis on the desert gerbil Gerbillus dasyurus. J Zool 256:349–354CrossRefGoogle Scholar
  27. Krasnov B, Shenbrot GI, Khokhlova I, Degen AA (2004) Flea species richness and parameters of host body, host geography and host “milieu”. J Anim Ecol 73:1121–1128CrossRefGoogle Scholar
  28. Krasnov B, Shenbrot GI, Medvedev SG, Vatschenok VS, Khokhlova I (1997) Host-habitat relation as an important determinant of spatial distribution of fleas assemblages (Siphonaptera) on rodents in the Negev desert. Parasitology 114:159–173PubMedCrossRefGoogle Scholar
  29. Kunz TH (1982) Roosting ecology. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 1–55Google Scholar
  30. Kunz TH, Lumsden LF (2003) Ecology of cavity and foliage roosting bats. In: Kunz TH, Fenton MB (eds) Bat ecology. The University of Chicago Press, Chicago London, pp 3–89Google Scholar
  31. Kuris AM, Blaustein AR, Alio JJ (1980) Hosts as islands. Am Nat 116:570–586CrossRefGoogle Scholar
  32. Lim BK, Engstrom MD, Lee TEJ, Patton JC, Bickam JW (2004) Molecular differentiation of large species of fruit eating bats (Artibeus) and phylogenic relationships based on the cytochrome b gene. Acta Chiropterol 6:1–12Google Scholar
  33. Linares OJ (1998) Mamiferos de Venezuela. Sociedad de Conservationista Audubon de Venezuela, Caracas, p 691Google Scholar
  34. Lindenfors PL, Nunn CL, Jones KE, Cunningham AA, Sechrest W, Gittleman JL (2007) Parasites species richness in carnivores: effects of host body mass, latitude geographical range and population density. Global Ecol Biogr 1:1–14Google Scholar
  35. Møller AP (1997) Parasites and the evolution of life history. In: Clayton D, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 105–127Google Scholar
  36. Møller AP, Erritzoe J, Garamszegi Z (2005) Covariation between brain size and immunity in birds: implications for brain size evolution. J Evol Biol 18:223–237PubMedCrossRefGoogle Scholar
  37. Morand S, Poulin R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol Ecol 12:717–727CrossRefGoogle Scholar
  38. Morand S (2000) Wormy world: comparative tests of theoritical hypotheses on parasite species richness. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of hosts–parasite relationships: theory meets reality. Elsiever, Amsterdam, pp 63–79Google Scholar
  39. Morand S, Harvey P (2000) Mammalian metabolism, longevity and parasites species richness. Proc R Soc Lond B 267:1999–2003CrossRefGoogle Scholar
  40. Neuhaus P (2003) Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus). Proc R Soc Lond B 270:213–215CrossRefGoogle Scholar
  41. Nunn CL, Altizer S, Jones KE, Sechrest W (2003) Comparative tests of parasites species richness in primates. Am Nat 162:597–614PubMedCrossRefGoogle Scholar
  42. Pagel MD, Harvey PH (1998) The taxon-level problem in the evolution of mammalian brain size: facts and artefacts. Am Nat 132:344–359CrossRefGoogle Scholar
  43. Patterson BD, Dick CW, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23:177–189CrossRefGoogle Scholar
  44. Pitnick S, Jones KE, Wilkinson G (2006) Mating systems and brain size in bats. Proc R Soc Lond B 273:719–724CrossRefGoogle Scholar
  45. Poulin R, Morand R (2004) The parasite biodiversity. Smithsonian Institution Press, WashingtonGoogle Scholar
  46. Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. C A Bios 11:247–251Google Scholar
  47. Reader S, Laland KN (2002) Social intelligence, innovation and enhanced brain size in primates. Proc Natl Acad Sci 99:4436–4441PubMedCrossRefGoogle Scholar
  48. 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). Parasite Res 98:237–243Google Scholar
  49. Richner H, Tripet F (1999) Ectoparasitism and the trade off between current and future reproduction. Oikos 86:535–538CrossRefGoogle Scholar
  50. Speakman JR (2005) Correlations between physiology and lifespan: two widely ignored problems with comparative studies. Aging Cells 4:167–175CrossRefGoogle Scholar
  51. Shimalov VV, Demyanchik MG, Demyanchik VT (2002) A study of the helminh fauna of the bats (Mammalia, Chiroptera: Vespertillionidae) in Belarus. Parasite Res 88:1011CrossRefGoogle Scholar
  52. Shultz S, Dunbar RIM (2006) Both social and ecological factors predict ungulate brain size. Proc R Soc Lond B 273:207–215CrossRefGoogle Scholar
  53. Šimková A, Ottová E, Morand S (2006) MHC variability, life traits and parasite diversity of European cyprinid fish. Evol Ecol 20:465–467Google Scholar
  54. Simmons NB (2005) Chiroptera.In: Wilson DE, Reeder DAM (eds) Mammal species of the World: a taxonomic and geographic reference, vol 1. Smithsonian Institution Press, Washington DC, pp 312–529Google Scholar
  55. Stanko M, Miklisova D, Goüy de Bellocq J, Morand S (2002) Mammal density and patterns of ectoparasites species richness and abundance. Oecologia 131:289–295CrossRefGoogle Scholar
  56. Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584PubMedCrossRefGoogle Scholar
  57. ter Hofstede HN, Fenton MB (2005) Relationships between roosts prefernce, ectoparasites density ang grooming behaviour of Neotropical bats. J Zool 266:333–340CrossRefGoogle Scholar
  58. Wilkinson GS, South J (2002) Life history, ecology and longevity in bats. Aging Cells 1:124–131CrossRefGoogle Scholar
  59. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex in the wild. J Evol Biol 16:224–232PubMedCrossRefGoogle Scholar
  60. Wenzel RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin. Biol Ser 20:1–177Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Frédéric Bordes
    • 1
  • Serge Morand
    • 1
  • Guerrero Ricardo
    • 2
  1. 1.Institut des Sciences de l’EvolutionCNRS-UM2, CC065, Université Montpellier 2Montpellier Cedex 05France
  2. 2.Laboratoria Ecologia y Sistematica de Parasitos, Inst. Zoologia Tropical, Fac. de CienciasUniversidad Central de VenezuelaCaracasVenezuela

Personalised recommendations