Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-23T16:46:45.843Z Has data issue: false hasContentIssue false
  • English
  • Français

How do ectoparasitic nycteribiids locate their bat hosts?

Published online by Cambridge University Press:  29 July 2008

S. I. LOURENÇO  and
J. M. PALMEIRIM
S. I. LOURENÇO*
Affiliation:
Centro de Biologia Ambiental, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, 1749-016 Lisboa, Portugal
J. M. PALMEIRIM
Affiliation:
Centro de Biologia Ambiental, Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, 1749-016 Lisboa, Portugal
*
*Corresponding author: Tel: 00351 217500000. E-mail: silourenco@fc.ul.pt
Get access Rights & Permissions [Opens in a new window]

Summary

Nycteribiids (Diptera: Nycteribiidae) are specific haematophagous ectoparasites of bats, which spend nearly all their adult lives on hosts. However, females have to leave bats to deposit their larva on the walls of the roosts, where they later emerge as adult flies. Nycteribiids had thus to evolve efficient sensorial mechanisms to locate hosts from a distance. We studied the sensory cues involved in this process, experimentally testing the role of specific host odours, and general cues such as carbon dioxide, body heat, and vibrations. As models we used two nycteribiids (Penicillidia conspicua and Penicillidia dufourii) and their primary bat hosts (Miniopterus schreibersii and Myotis myotis, respectively). Carbon dioxide was the most effective cue activating and orientating the responses of nycteribiids, followed by body heat and body odours. They also responded to vibration, but did not orientate to its source. In addition, sensory cues combined (carbon dioxide and body heat) were more effective in orientating nycteribiids than either cue delivered alone. Results suggest that nycteribids have some capacity to distinguish specific hosts from a distance, probably through their specific body odours. However, the strong reliance of nycteribiids on cues combined indicates that they follow these to orientate to nearby multispecies bat clusters, where the chances of finding their primary hosts are high. The combination of sensory cues seems therefore an effective strategy used by nycteribiids to locate bat hosts at a distance.

Keywords

ectoparasitismbat fliesNycteribiidaehost locationsensory cuesChiroptera
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 10 , September 2008 , pp. 1205 - 1213
Copyright
Copyright © 2008 Cambridge University Press

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

REFERENCES

Bandilla, M., Hakalahti-Sirén, T. and Valtonen, E. T. (2007). Experimental evidence for a hierarchy of mate- and host-induced cues in a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura). International Journal for Parasitology 37, 1343–1349. doi:10.1016/j.ijpara.2007.04.004.CrossRefGoogle Scholar
Barrozo, R. B. and Lazzari, C. R. (2004). Orientation behaviour of the blood-sucking bug Triatoma infestans to short-chain fatty acids: synergistic effect of L-lactic acid and carbon dioxide. Chemical Senses 29, 833–841. doi:10.1093/chemse/bjh249.CrossRefGoogle ScholarPubMed
Ching, L. M. and Marshall, A. G. (1968). The breeding biology of the bat-fly Eucampispoda sundaicum Theodor, 1955 (Diptera: Nycteribiidae). Malayan Nature Journal 21, 171–180.Google Scholar
Costantini, C., Birkett, M. A., Gibson, G., Ziesmann, J., Sagnon, N. F., Mohammed, H. A., Coluzzi, M. and Pickett, J. A. (2001). Electroantennogram and behavioural responses of the malaria vector Anopheles gambiae to human-specific sweat components. Medical and Veterinary Entomology 15, 259–266. doi:10.1046/j.0269-283x.2001.00297.x.CrossRefGoogle ScholarPubMed
Dick, C. W. and Patterson, B. D. (2006). Bat flies: obligate ectoparasites of bats. In Micromammals and Macroparasites: From Evolutionary Ecology to Management (ed. Morand, S., Krasnov, B. and Poulin, R.), pp. 179–194. Springer-Verlag Publishing, Tokyo.CrossRefGoogle Scholar
Estrada-Peña, A., Balcells, E. and Serra-Cobo, J. (1991). Los artropodos ectoparasitos de murciélagos en España: In Los Murciélagos de España y Portugal (ed. Benzal, J. and De Paz, O.), pp. 253–279. Colección Técnica. ICONA.Google Scholar
Gillies, M. T. (1980). The role of carbon dioxide in host-finding by mosquitoes (Diptera: Culicidae): a review. Bulletin of Entomological Research 70, 525–532.CrossRefGoogle Scholar
Guerenstein, P. G. and Hildebrand, J. G. (2008). Roles and effects of environmental carbon dioxide in insect life. Annual Review of Entomology 53, 161–178. doi:10.1146/annurev.ento.53.103106.093402.CrossRefGoogle ScholarPubMed
Humphries, D. A. (1968). The host-finding behaviour of the hen flea, Ceratophyllus gallinae (Schrank) (Siphonaptera). Parasitology 58, 403–414.CrossRefGoogle Scholar
Imaz, E., Aihartza, J. R. and Totorika, M. J. (1999). Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (N. Iberian peninsula). Miscelanea Zoológica 22, 21–30.Google Scholar
Jackson, R. R., Clark, R. J. and Harland, D. P. (2002). Behavioural and cognitive influences of kairomones on an araneophagic jumping spider. Behaviour 139, 749–775.CrossRefGoogle Scholar
Kilpinen, O. and Mullens, B. A. (2004). Effect of food deprivation on response of the mite, Dermanyssus gallinae, to heat. Medical and Veterinary Entomology 18, 368–371.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Oguzoglu, I. and Burdelova, N. I. (2002). Host discrimination by two desert fleas using an odour cue. Animal Behaviour 64, 33–40. doi:10.1006/anbe.2002.3030.CrossRefGoogle Scholar
Lawrence, P. O. (1981). Host vibration – a cue to host location by the parasite, Biosteres longicaudatus. Oecologia 48, 1432–1939.CrossRefGoogle ScholarPubMed
Lehane, M. J. (2005). The Biology of Blood-Sucking Insects. 2nd Edn.Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Lourenço, S. I. and Palmeirim, J. M. (2007). Can mite parasitism affect the condition of bat hosts? Implications for the social structure of colonial bats. Journal of Zoology 273, 161–168. doi:10.1111/j.1469-7998.2007.00322.x.CrossRefGoogle Scholar
Marshall, A. G. (1970). The life cycle of Basilia hispida Theodor 1957 (Diptera:Nycteribiidae) in Malaysia. Parasitology 61, 1–18.CrossRefGoogle Scholar
Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Academic Press, London, UK.Google Scholar
Meyrowitsch, D., Christensen, N. O. and Hindsbo, O. (1991). Effects of temperature and host density on the snail-finding capacity of cercariae of Echinostoma caproni (Digenea: Echinostomatidae). Parasitology 102, 391–395.CrossRefGoogle ScholarPubMed
Mikheev, V. N., Valtonen, E. T. and Rintamaki-kinnunen, P. (1998). Host searching in Argulus foliaceus L. (Crustacea: Branchiura): the role of vision and selectivity. Parasitology 116, 425–430.CrossRefGoogle ScholarPubMed
Newcombe, R. G. (1998). Two-sided confidence intervals for the single proportion: comparison of seven methods. Statistics in Medicine 17, 857–872.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Osterkamp, J., Wahl, U., Schmalfuss, G. and Haas, W. (1999). Host-odour recognition in two tick species is coded in a blend of vertebrate volatiles. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology 18, 59–67.CrossRefGoogle Scholar
Overal, W. L. (1980). Host-relations of the bat fly Megistopoda aranea (Diptera: Streblidae) in Panamá. The University of Kansas Science Bulletin 52, 1–20.Google Scholar
Palmeirim, J. M. (1990). Bats of Portugal: zoogeography and systematics. The University of Kansas, Museum of Natural History 82, 1–53.Google Scholar
Palmeirim, J. M., Rodrigues, L., Rainho, A. and Ramos, M. J. (1999). Chiroptera. In Mamíferos Terrestres de Portugal Continental, Açores e Madeira (ed. Mathias, M. L., Santos-Reis, M., Palmeirim, J. M. and Ramalhinho, M. G.), pp. 41–95. Instituto da Conservação da Natureza e Centro de Biologia Ambiental, Lisboa.Google Scholar
Poulin, R., Curtis, M. A. and Rau, M. E. (1990). Responses of the fish ectoparasite Salmincola edwardsii (Copepoda) to stimulation, and their implication for host-finding. Parasitology 100, 417–421.CrossRefGoogle ScholarPubMed
Rodrigues, L., Zahn, A., Rainho, A. and Palmeirim, J. M. (2003). Contrasting the roosting behaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67, 321–335.CrossRefGoogle Scholar
Ryberg, O. (1947). Studies on Bats and Bat Parasites. Bokförlaget Svensk Natur, Stockholm.Google Scholar
Smallegange, R. C., Qiu, Y. T., van Loon, J. J. and Takken, W. (2005). Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chemichal Senses 30, 145–152. doi:10.1093/chemse/bji010.CrossRefGoogle ScholarPubMed
Sokal, R. R. and Rohlf, F. J. (1995). Biometry: the Principles and Practice of Statistics in Biological Research, 3rd Edn, W. H. Freeman and Company, New York, USA.Google Scholar
Takken, W. and Knols, B. G. J. (1999). Odor-mediated behavior of Afrotropical malaria mosquitoes. Annual Review of Entomology 44, 131–157.CrossRefGoogle ScholarPubMed
ter Hofstede, H. M., Fenton, M. B. and Whitaker, J. O. 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. doi:10.1139/z04-030.CrossRefGoogle Scholar
Vaughan, J. A. and Mead-Briggs, A. R. (1970). Host-finding behaviour of the rabbit flea, Spilopsyllus cuniculi with special reference to the significance of urine as an attractant. Parasitology 61, 397–409.CrossRefGoogle Scholar
Wigglesworth, V. B. (1941). The sensory physiology of the human louse Pediculus humanus corporis de Geer (Anoplura). Parasitology 33, 67–109.CrossRefGoogle Scholar