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The effect of infection with Lyme disease spirochetes (Borrelia burgdorferi) on the phototaxis, activity, and questing height of the tick vector Ixodes scapularis

Published online by Cambridge University Press:  06 April 2009

H. Lefcort*
Affiliation:
Department of Biology, Georgia Southern University, Landrum Box 8042, Statesboro, Georgia, 30460-8042, USA
L. A. Durden
Affiliation:
Institute of Arthropodology and Parasitology, Georgia Southern University, Landrum Box 8056, Statesboro, Georgia 30460-8056, USA
*
*Corresponding author. Biology Department, Gonzaga University, Spokane, Washington, 99258-0001USA. Tel: 509-328-4220 ext 3306. Fax: 509-324-5718. E-mail: [email protected].

Summary

Little is known about the effects of infection with Borrelia burgdorferi, the bacterium that causes Lyme disease, on its tick vectors. The purpose of this study was to determine the behavioural and ecological effects of infection by the bacterium in nymphal and adult black-legged (Ixodes scapularis) ticks. We found that the effects of infection were more pronounced in adults than in nymphs. Compared to uninfected adults, infected adults were less able to overcome physical obstacles, avoided vertical surfaces, were less active and quested at lower heights. Infected nymphs showed increased phototaxis and attraction to vertical surfaces. Infected nymphs also showed trends toward increased questing height and a greater tendency to overcome physical obstacles although these trends were not statistically significant. These altered behaviours in an infected tick may affect survival or pathogen transmission and may reflect kin selection in the bacterial pathogen.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Anez, N. & East, J. S. (1984). Studies on Trypanosoma rangeli Tejera, 1920. II. Its effect on feeding behaviour of triatome bugs. Acta Tropica 41, 9395.Google Scholar
Baer, G. M. (1973). The Natural History of Rabies, Vol. I and II. Academic Press, New York.Google Scholar
Beach, R., Kiilu, G. & Leeuwenberg, J. (1985). Modification of sandfly biting behavior by Leishmania leads to increased parasite transmission. American Journal of Tropical Medicine and Hygiene 34, 278282.CrossRefGoogle ScholarPubMed
Burgdorfer, W., Hayes, S. F. & Corwin, D. (1989). Pathophysiology of the Lyme disease spirochete, Borrelia burgdoferi, in ixodid ticks. Reviews of Infectious Diseases 11, S1442–S1450.CrossRefGoogle Scholar
Daniels, T. J., Fish, D. & Falco, R. C. (1989). Seasonal activity and survival of adult Ixodes dammini (Acari: Ixodidae) in southern New York state. Journal of Medical Entomology 26, 610614.CrossRefGoogle ScholarPubMed
Endris, R. G. & Hess, W. R. (1994). Attempted transovarial and venereal transmission of African swine fever virus by the Iberian soft tick Ornithodoros (Pavilovskyella) marocanus (Acari: Ixodidea: Argasidae). Journal of Medical Entomology 31, 373381.CrossRefGoogle Scholar
Ginsburg, H. S. & Ewing, C. P. (1989). Habitat distribution of Ixodes dammini (Acari: Ixodidae) and Lyme Disease Spirochetes On Fire Island, New York. Journal of Medical Entomology 26, 183189.CrossRefGoogle Scholar
Goddard, J. (1993). Ecological studies of Ixodes scapularis (Acari: Ixodidae) in central Mississippi: lateral movement of adult ticks. Journal of Medical Entomology 30, 824826.CrossRefGoogle ScholarPubMed
Grimstad, P. R., Ross, Q. E. & Craig, G. B. Jr. (1980). Aedes triseriatus (Diptera: Culicidae) and La Crosse virus II. Modification of mosquito feeding behavior by virus infection. Journal of Medical Entomology 17, 117.CrossRefGoogle ScholarPubMed
Hamilton, W. D. (1964). The genetical evolution of social behaviour, I, II. Journal of Theoretical Biology 7, 151.CrossRefGoogle Scholar
Hechtel, L. J., Johnson, C. L. & Juliano, S. A. (1993). Modification of antipredator behavior of Caecidotea intermedius by its parasite Acanthocephalus dirus. Ecology 74, 710713.CrossRefGoogle Scholar
Holmes, J. C. & Bethel, W. M. (1972). Modifications of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. & Wright, C. A.) pp. 123149. Academic Press, London.Google Scholar
James, A. M. & Oliver, J. H. Jr. (1990). Feeding and host preference of immature Ixodes dammini, I. scapularis and I. pacificus (Acari: Ixodidae). Journal of Medical Entomology 27, 324330.CrossRefGoogle ScholarPubMed
Jenni, L., Molyneux, D. H., Livesey, J. L. & Galun, R. (1980). Feeding behaviour of tsetse flies infected with salivarian trypanosomes. Nature, London 283, 383–85.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. (1995). Decreased predator avoidance in parasitized mice: neuromodulatory correlates. Parasitology 111, 257263.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (1992). Foraging on prey that are modified by parasites. American Naturalist 140, 854867.CrossRefGoogle Scholar
Lane, R. S. (1992). Effect of transovarially and transtadially-passed Lyme disease spirochetes on the developmental and reproductive biology of Ixodes pacificus (Acari: Ixodidae) In Proceedings and Abstracts of the First International Conference on Tick- Borne Pathogens at the Host—Vector Interface: An Agenda for Research (ed. Munderloh, U. G. & Kurtti, T. J.) pp. 282289. St Paul: University of Minnesota.Google Scholar
Lane, R. S., Piesman, J. & Burgdorfer, W. (1991). Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annual Review of Entomology 36, 587609.CrossRefGoogle Scholar
Lefcort, H. & Bayne, C. J. (1991). Temperature distributions of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to Schistosoma mansoni. Parasitology 103, 357362.CrossRefGoogle Scholar
Lefcort, H. & Blaustein, A. R. (1995). Disease, predator avoidance, and vulnerability to predation in tadpoles. Oikos 74, 469474.CrossRefGoogle Scholar
Lefcort, H. & Eiger, S. M. (1993). Antipredatory behaviour of feverish tadpoles: implications for pathogen transmission. Behaviour 126, 1327.CrossRefGoogle Scholar
Lester, R. J. G. (1971). The influence of Schistocephalus plerocercoids on the respiration of Gasterosteus and a possible resulting effect on the behaviour of fish. Canadian Journal of Zoology 49, 361366.CrossRefGoogle Scholar
Lewengrub, S., Rudzinska, M. A., Piesman, J., Spielman, A. & Zung, J. (1989). The influence of heat on the development of Babesia microti in unfed nymphs of Ixodes dammini. Canadian Journal of Zoology 67, 15101515.CrossRefGoogle Scholar
Loye, J. E. & Lane, R. S. (1988). Questing behavior of Ixodes pacificus (Acari: Ixodidae) in relation to meteorological and seasonal factors. Journal of Medical Entomology 25, 391398.CrossRefGoogle ScholarPubMed
Mather, T. N., Duffy, D. C. & Campbell, S. R. (1993). An unexpected result from burning vegetation to reduce Lyme disease transmission risks. Journal of Medical Entomology 30, 642645.CrossRefGoogle ScholarPubMed
Mather, T. N., Piesman, J. & Spielman, A. (1987). Absence of spirochetes (Borrelia burgdoferi) and piroplasms (Babesia microti) in deer ticks (Ixodes dammini) parasitized by chalcid wasps (Hunterellus hookeri). Medical and Veterinary Entomology 1, 38.CrossRefGoogle Scholar
Mather, T. N. & Spielman, A. (1986). Diurnal detachment of immature deer ticks (Ixodes dammini) from nocturnal hosts. American Journal of Tropical Medicine and Hygiene 35, 182186.CrossRefGoogle ScholarPubMed
Michalakis, Y. & Hochberg, M. E. (1994). Parasitic effects on host life-history traits: A review of recent studies. Parasite 1, 291294.CrossRefGoogle ScholarPubMed
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205216.CrossRefGoogle Scholar
Molyneux, D. H. & Jefferies, D. (1986). Feeding behavior of pathogen-infected vectors. Parasitology 92, 721736.CrossRefGoogle ScholarPubMed
Moore, J. (1993). Parasites and the behavior of biting flies. Journal of Parasitology 79, 116.CrossRefGoogle ScholarPubMed
Oliver, J. H. Jr., Chandler, F. W., Luttrell, M. P., James, A. M., Stallknecht, D. E., McGuire, B. S., Hutcheson, H. J., Cummins, G. A. & Lane, R. S. (1993). Isolation and transmission of the Lyme disease spirochete from the southeastern United States. Proceedings of the National Academy of Sciences, USA 90, 73717375.CrossRefGoogle ScholarPubMed
Poulin, R. (1994). The Evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.CrossRefGoogle ScholarPubMed
Renz, A. & Wenk, P. (1981). Intracellular development of the cotton rat filaria Litomosoides carinii in the vector mite Ornithonyssus bacoti. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 166168.CrossRefGoogle ScholarPubMed
Rossignol, P. A. (1988). Parasite modification of mosquito probing behavior. Miscellaneous Publications of the Entomological Society of America 68, 2528.Google Scholar
Rossignol, P. A., Ribeiro, J. M. C. & Spielman, A. (1984). Increased intradermal probing time in sporozoite-infected mosquitoes. American Journal of Tropical Medicine and Hygiene 33, 1720.CrossRefGoogle ScholarPubMed
Schoeler, G. B. & Lane, R. S. (1993). Efficiency of transovarial transmission of the Lyme disease spirochete, Borrelia burgdorferi, in the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Journal of Medical Entomology 30, 8086.CrossRefGoogle ScholarPubMed
Steere, A. C., Malawista, S. E., Snydman, D. R., Shope, R. E., Andiman, W. A., Ross, M. R. & Steele, F. M. (1977). Lyme arthritis: an epidemic of oligoarticular arthritis in children and adults in three Connecticut communities. Arthritis and Rheumatism 20, 717.CrossRefGoogle ScholarPubMed
Telford, S. R. III., Urioste, S. S. & Spielman, A. (1992). Clustering of host-seeking nymphal deer ticks (Ixodes dammini) infected by Lyme disease spirochetes (Borrelia burgdoferi). American Journal of Tropical Medicine and Hygiene 47, 5560.CrossRefGoogle Scholar
Vasil'eva, I. S., Byzova, Y. B. & Ershova, A. s. (1990). Effect of the causative agent of relapsing fever on the respiration of the vector Ornithodoros papillipes Birula, 1985 (Ixodoidea, Argasidae). Izvestiya Akademii Nauk SSSR, Leningrad Series Biological 5, 717727 (in Russian).Google Scholar
Werder, J. & Gothe, R. (1993). Hyalomma truncatum and Rhipicephalus evertsi (Ixodoidea, Ixodidae): reactions of adult ticks to vertically incident narrow – and wideband optical radiation with and without the influence of a CO2 gradient. Experimental and Applied Acarology 17, 489501.CrossRefGoogle Scholar
Winston, P. W. & Bates, D. H. (1960). Saturated solutions for the control of humidity in biological research. Ecology 41, 232237.CrossRefGoogle Scholar