Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T04:22:20.477Z Has data issue: false hasContentIssue false
  • English
  • Français

Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae)

Published online by Cambridge University Press:  22 March 2018

Thomas Hiller ,
Benjamin Honner ,
Rachel A. Page  and
Marco Tschapka
Thomas Hiller*
Affiliation:
Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein-Allee 11, Ulm 89081, Germany Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Panamá
Benjamin Honner
Affiliation:
Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein-Allee 11, Ulm 89081, Germany
Rachel A. Page
Affiliation:
Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Panamá
Marco Tschapka
Affiliation:
Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein-Allee 11, Ulm 89081, Germany Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Panamá
*
Author for correspondence: Thomas Hiller, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Bat flies (Streblidae) are diverse, obligate blood-feeding insects and probably the most conspicuous ectoparasites of bats. They show preferences for specific body regions on their host bat, which are reflected in behavioural characteristics. In this study, we corroborate the categorization of bat flies into three ecomorphological groups, focusing only on differences in hind leg morphology. As no detailed phylogeny of bat flies is available, it remains uncertain whether these morphological differences reflect the evolutionary history of bat flies or show convergent adaptations for the host habitat type. We show that the division of the host bat into three distinct habitats contributes to the avoidance of interspecific competition of bat fly species. Finally, we found evidence for density-dependent competition between species belonging to the same ecomorphological group.

Keywords

Bat fliesco-occurrenceecomorphologyparasite interactionsphyllostomidae
Type
Research Article
Information
Parasitology , Volume 145 , Issue 11 , September 2018 , pp. 1475 - 1482
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beuttell, K and Losos, JB (1999) Ecological morphology of Caribbean anoles. Herpetological Monographs 13, 1–28.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cirranello, A, Simmons, NB, Solari, S and Baker, RJ (2016) Morphological diagnoses of higher-level phyllostomid taxa (Chiroptera: Phyllostomidae). Acta Chiropterologica 18, 39–71.Google Scholar
Dick, C (2005) Ecology and host specificity of Neotropical bat flies (Diptera: Streblidae) and their chiropteran hosts. Lubbock, Texas, USA: Texas Tech University, p. 265.Google Scholar
Dick, CW and Dick, SC (2006) Effects of prior infestation on host choice of bat flies (Diptera: Streblidae). Journal of Medical Entomology 43, 433–436.Google Scholar
Dick, CW and 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, CW and Miller, J (2010) Streblidae. In Brown, B, Borkent, A, Cumming, J, Wood, D, Woodley, N and Zumbado, M (eds)). Manual of Central American Diptera. Costa Rica: Los Angeles County Museum of Natural History and Instituto Nacional de Biodiversidad, vol. 2, pp. 1249–1260.Google Scholar
Dick, CW and Patterson, BD (2006) Bat flies: obligate ectoparasites of bats. In Morand, S, Krasnov, BR and Poulin, R (eds)). Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo: Springer, pp. 179–191.Google Scholar
Dick, CW and Patterson, BD (2007) Against all odds: explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology 37, 871–876.Google Scholar
Dittmar, K, Porter, ML, Murray, S and Whiting, MF (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
Dittmar, K, Dick, CW, Patterson, BD, Whiting, MF and Gruwell, ME (2009) Pupal deposition and ecology of bat flies (Diptera: Streblidae): Trichobius sp. (Caecus group) in a Mexican cave habitat. Journal of Parasitology 95, 308–314.Google Scholar
Dittmar, K, Morse, SF, Dick, CW and Patterson, BD (2015) Bat fly evolution from the Eocene to the present (Hippoboscoidea, Streblidae and Nycteribiidae). In Morand, S, Krasnov, BR and Littlewood, DTJ (eds). Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics. Cambridge: Cambridge University Press, pp. 246–264.Google Scholar
Fritz, GN (1983) Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology 20, 1–10.Google Scholar
Full, RJ and Tu, MS (1991) Mechanics of a rapid running insect: two-, four- and six-legged locomotion. Journal of Experimental Biology 156, 215–231.Google Scholar
Giraudoux, P (2016) pgirmess: Data analysis in ecology. R package version 1.6.5. Available at https://CRAN.R-project.org/package=pgirmess.Google Scholar
Gotelli, NJ and Rohde, K (2002) Co-occurrence of ectoparasites of marine fishes: a null model analysis. Ecology Letters 5, 86–94.Google Scholar
Graciolli, G (2010) Nycteribiidae. In Brown, B, Borkent, A, Cumming, J, Wood, D, Woodley, N and Zumbado, M (eds). Manual of Central American Diptera. Costa Rica: Los Angeles County Museum of Natural History and Instituto Nacional de Biodiversidad, vol. 2, pp. 1261–1266.Google Scholar
Graham, D (1985) Pattern and control of walking in insects. Advances in Insect Physiology 18, 31–140.Google Scholar
Guerrero, R (1993) Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo I. Clave para los géneros y Nycterophiliinae. Acta Biologica Venezuelica 14, 61–75.Google Scholar
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 género Trichobius (Gervais, 1844). Acta Biologica Venezuelica 15, 1–18.Google Scholar
Guerrero, R (1994b) Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo IV. Trichobiinae con alas desarrolladas. Boletín Entomologica Venezolana 9, 161–192.Google Scholar
Guerrero, R (1995a) Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo III. Los grupos: dugesii, dunni y phyllostomae del género Trichobius (Gervais, 1844). Acta Biologica Venezuelica 15, 1–27.Google Scholar
Guerrero, R (1995b) 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
Guerrero, R (1996) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo VI. Streblinae. Acta Biologica Venezuelica 16, 1–26.Google Scholar
Guerrero, R (1997) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo VII. Lista de especies, hospedadores y países. Acta Biologica Venezuelica 17, 9–24.Google Scholar
Guerrero, R (1998) Notes on Neotropical batflies (Diptera, Streblidae). I. The genus Trichobius, with description of two new species and one new subspecies from Venezuela. Acta Parasitologica 43, 86–93.Google Scholar
Handley, COW and Gardner, AL (1991) Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panamá. Smithsonian Contributions to Zoology 155, 1–173.Google Scholar
Hsu, M-H, Hsu, T-C and Wu, W-J (2002) Distribution of cat fleas (Siphonaptera: Pulicidae) on the cat. Journal of Medical Entomology 39, 685–688.Google Scholar
Iturralde-Vinent, MA and MacPhee, R (1996) Age and paleogeographical origin of Dominican amber. Science 273, 1850.Google Scholar
Lapinski, W, Walther, P and Tschapka, M (2015) Morphology reflects microhabitat preferences in an assemblage of neotropical wandering spiders. Zoomorphology 134, 219–236.Google Scholar
Linhares, AX and Komeno, CA (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
Losos, JB and Sinervo, B (1989) The effects of morphology and perch diameter on sprint performance of Anolis lizards. Journal of Experimental Biology 145, 23–30.Google Scholar
Marshall, AG (1981) The Ecology of Ectoparasitic Insects. Academic Press Inc Ltd, London, UK, p. 446.Google Scholar
Morand, S, Krasnov, BR and Poulin, R (2006) Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo: Springer, p. 640.Google Scholar
Mouillot, D, George-Nascimento, M and Poulin, R (2003) How parasites divide resources: a test of the niche apportionment hypothesis. Journal of Animal Ecology 72, 757–764.Google Scholar
Oksanen, J, Blanchet, F, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, R, Simpson, G, Solymos, P, Stevens, M, Szoecs, E and Wagner, H (2016). vegan: Community ecology package. R package version 2.4–1. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Overal, WL (1980) Host-relations of the bat fly Megistopoda aranea (Diptera: Streblidae) in Panama. University of Kansas Science Bulletin 52, 1–20.Google Scholar
Patterson, BD, Dick, CW and Dittmar, K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23, 177–189.Google Scholar
Patterson, BD, Dick, CW and Dittmar, K (2009) Nested distributions of bat flies (Diptera: Streblidae) on Neotropical bats: artifact and specificity in host-parasite studies. Ecography 32, 481–487.Google Scholar
Poinar, G and Brown, A (2012) The first fossil streblid bat fly, Enischnomyia stegosoma n. gen., n. sp.(Diptera: Hippoboscoidea: Streblidae). Systematic Parasitology 81, 79–86.Google Scholar
Poulin, R and Morand, S (2000) The diversity of parasites. Quarterly Review of Biology 75, 277–293.Google Scholar
Presley, SJ (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, SJ (2010) Interspecific aggregation of ectoparasites on bats: importance of hosts as habitats supersedes interspecific interactions. Oikos 120, 832–841.Google Scholar
R Development Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rasband, W (1997–2016). ImageJ. Bethesda, Maryland, USA: US National Institutes of Health. Available at http://imagej.nih.gov/ij/.Google Scholar
Rojas, D, Warsi, OM and Dávalos, LM (2016) Bats (Chiroptera: Noctilionoidea) challenge a recent origin of extant neotropical diversity. Systematic Biology 65, 432–448.Google Scholar
Ross, A (1961) Biological studies on bat ectoparasites of the genus Trichobius (Diptera: Streblidae) in North America, north of Mexico. Wasmann Journal of Biology 19, 229–246.Google Scholar
Schlee, D (1990) Das Bernstein-Kabinett. Stuttgarter Beitraege zur Naturkunde, Serie C 28, 1–100.Google Scholar
Schoener, TW (1974) Resource partitioning in ecological communities. Science 185, 27–39.Google Scholar
Spielberg, S (1997) The Lost World: Jurassic Park. USA: Universal Pictures.Google Scholar
Tello, SJ, Stevens, RD and Dick, CW (2008) Patterns of species co-occurrence and density compensation: a test for interspecific competition in bat ectoparasite infracommunities. Oikos 117, 693–702.Google Scholar
ter Hofstede, HM and Fenton, MB (2005) Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. Journal of Zoology 266, 333–340.Google Scholar
ter Hofstede, HM, Fenton, MB and Whitaker, JO 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.Google Scholar
Wenzel, RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin 20, 1–177.Google Scholar
Wenzel, RL, Tipton, VJ and Kiewlicz, A (1966). The streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In Wenzel, RL and Tipton, VJ (eds). Ectoparasites of Panama, Vol. Fieldiana. Zoology. Special Publications. Chicago: Field Museum of Natural History, pp. 405–676.Google Scholar
Windsor, DA (1998) Controversies in parasitology, most of the species on earth are parasites. International Journal for Parasitology 28, 1939–1941.Google Scholar
Supplementary material: File

Hiller et al. supplementary material

Hiller et al. supplementary material 1

Download Hiller et al. supplementary material(File)
File 41.7 KB