Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T10:57:08.390Z Has data issue: false hasContentIssue false

Biotic and abiotic predictors of tick (Dermacentor variabilis) abundance and engorgement on free-ranging raccoons (Procyon lotor)

Published online by Cambridge University Press:  23 August 2007

R. J. MONELLO*
Affiliation:
Department of Fisheries and Wildlife Sciences, 302 Anheuser-Busch Natural Resources Building, University of Missouri, Columbia, MO 65211, USA
M. E. GOMPPER
Affiliation:
Department of Fisheries and Wildlife Sciences, 302 Anheuser-Busch Natural Resources Building, University of Missouri, Columbia, MO 65211, USA
*
*Corresponding author: Tel: +011 573 882 8099. Fax: +011 573 884 5070. E-mail: [email protected]

Summary

We examined the relative importance of abiotic and biotic factors on the ability of adult Dermacentor variabilis ticks to attach and engorge with blood across 10 populations of free-ranging raccoons (Procyon lotor). We developed a priori models that represented explicit hypotheses based on the literature and tested the ability of these models to explain non-replete and replete (fully engorged with blood) tick infestation using generalized linear models and Akaike's Information Criterion. Abiotic models that included month and site of collection clearly provided a better fit for non-replete tick abundance data, while biotic models with host age and sex covariates best fit the replete tick data. Abiotic models of non-replete abundance were superior to biotic models because of large seasonal and site fluctuations in non-replete abundance that masked differences due to host characteristics. Conversely, best-fitting models of replete tick abundance included only age and sex and suggest that once a tick has reached a host, host-parasite interactions are the primary determinant of engorgement by female ticks. Host population structure may have a large influence on potential cohort size of ticks by reducing or increasing the total number and proportion that can become engorged and moult or lay eggs.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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

Allan, S. A. (2001). Ticks. In Parasitic Diseases of Wild Mammals (ed. Samuel, W. M., Pybus, M. J. and Kocan, A. A.), pp. 72106. Iowa State Press, Ames, USA.CrossRefGoogle Scholar
Atwood, E. L. and Sonenshine, D. E. (1967). Activity of the American dog tick, Dermacentor variabilis (Acarina: Ixodidae), in relation to solar energy changes. Annals of the Entomological Society of America 60, 354362.CrossRefGoogle ScholarPubMed
Bliss, C. I. and Fisher, R. A. (1953). Fitting the negative binomial distribution to biological data. Biometrics 9, 176199.CrossRefGoogle Scholar
Burg, J. G. (2001). Seasonal activity and spatial distribution of host seeking adults of the tick Dermacentor variabilis. Medical and Veterinary Entomology 15, 413421.CrossRefGoogle ScholarPubMed
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach. Springer-Verlag, New York.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Campbell, A. (1979). Ecology of the American dog tick, Dermacentor variabilis, in southwestern Nova Scotia. In Recent Advances in Acarology (ed. Rodriguez, J. G.), pp. 135143. Academic Press, New York.CrossRefGoogle Scholar
Campbell, A. and MacKay, P. R. (1979). Distribution of the American dog tick, Dermacentor variabilis (Say), and its small-mammal hosts in relation to vegetation types in a study area of Nova Scotia. Canadian Journal of Zoology 57, 19501959.CrossRefGoogle Scholar
Carroll, J. F. and Nichols, J. D. (1986). Parasitization of meadow voles, Microtus pennsylvanicus (Ord), by American dog ticks, Dermacentor variabilis (Say), and adult tick movement during high host density. Journal of Entomological Science 21, 102113.CrossRefGoogle Scholar
Castagnolli, K. C., de Figueiredo, L. B., Santana, D. A., De Castro, M. B., Romano, M. A. and Szabó, M. P. J. (2003). Acquired resistance of horses to Amblyomma cajennense (Fabricius, 1787) ticks. Veterinary Parasitology 117, 271283.CrossRefGoogle ScholarPubMed
Cox, R. M. and John-Alder, H. B. (2007). Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Functional Ecology 21, 327334.CrossRefGoogle Scholar
Craig, L. E., Norris, D. E., Sanders, M. L., Glass, G. E. and Schwartz, B. S. (1996). Acquired resistance and antibody response of raccoons (Procyon lotor) to sequential feedings of Ixodes scapularis (Acari: Ixodidae). Veterinary Parasitology 63, 291301.CrossRefGoogle ScholarPubMed
Daniel, M. (1978). Microclimate as a determining element in the distribution of ticks and their developmental cycles. Folia Parasitologica 25, 9194.Google Scholar
denHollander, N. and Allen, J. R. (1985). Dermacentor variabilis: acquired resistance to ticks in BALB/c mice. Experimental Parasitology 59, 118129.CrossRefGoogle ScholarPubMed
Dobson, A. and Meagher, M. (1996). The population dynamics of Brucellosis in the Yellowstone National Park. Ecology 77, 10261036.CrossRefGoogle Scholar
Evans, R. H. (2002). Raccoons and relatives (Carnivora, Procyonidae). Zoological Restraint and Anesthesia (ed. Heard, D.). International Veterinary Information Service, Ithaca. doi: http://www.ivis.org/special_books/Heard/evans/chapter_frm.asp?LA=1.Google Scholar
Festa-Bianchet, M. (1989). Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). Journal of Animal Ecology 58, 785795.CrossRefGoogle Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603622.CrossRefGoogle Scholar
Gallivan, G. J., Culverwell, J., Girdwood, R. and Surgeoner, G. A. (1995). Ixodid ticks of impala (Aepyceros melampus) in Swaziland: effects of age class, sex, body condition and management. South African Journal of Zoology 30, 178186.CrossRefGoogle Scholar
Goethert, H. K. and Telford, S. R. III. (2005). A new Francisella (Beggiatiales: Francisellaceae) inquiline within Dermacentor variabilis Say (Acari: Ixodidae). Journal of Medical Entomology 42, 502505.CrossRefGoogle ScholarPubMed
Gompper, M. E. (2004). Correlations of coati (Nasua narica) social structure with parasitism by ticks and chiggers. In Contribuciones Mastozoológicas en Homenaje a Bernardo Villa (ed. Sánchez-Cordero, V. and Meddellín, R. A.), pp. 527534. National Autonomous University of Mexico, Mexico City.Google Scholar
Grau, G. A., Sanderson, G. C. and Rogers, J. P. (1970). Age determination in raccoons. Journal of Wildlife Management 34, 364372.CrossRefGoogle Scholar
Gregory, R. D., Montgomery, S. S. J. and Montgomery, W. I. (1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749757.CrossRefGoogle Scholar
Halvorsen, O. (1986). Epidemiology of reindeer parasites. Parasitology Today 2, 334339.CrossRefGoogle ScholarPubMed
Hawlena, H., Abramsky, Z. and Krasnov, B. R. (2006). Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148, 3039.CrossRefGoogle Scholar
Hudson, P. J. (1992). Grouse in Space and Time. Game Conservancy Ltd, Fordingbridge, UK.Google Scholar
Hudson, P. J. and Dobson, A. P. (1995). Macroparasites: observed patterns. In Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. and Dobson, A. P.), pp. 144176. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
Hughes, V. L. and Randolph, S. E. (2001). Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. Journal of Parasitology 87, 4954.CrossRefGoogle ScholarPubMed
Johnson, J. B. and Omland, K. S. (2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101108.CrossRefGoogle ScholarPubMed
Kollars, T. M. Jr. and Kengluecha, A. (2001). Spotted fever group Rickettsia in Dermacentor variabilis (Acari: Ixodidae) infesting raccoons (Carnivora: Procyonidae) and opossums (Marsupialia: Didelphimorphidae) in Tennessee. Journal of Medical Entomology 38, 601602.CrossRefGoogle Scholar
Kollars, T. M. Jr., Oliver, J. H. Jr., Masters, E. J., Kollars, P. G. and Durden, L. A. (2000). Host utilization and seasonal occurrence of Dermacentor species (Acari: Ixodidae) in Missouri, USA. Experimental and Applied Acarology 24, 631643.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Burdelova, N. V., Khokhlova, I. S., Shenbrot, G. I. and Degen, A. (2005). Larval interspecific competition in two flea species parasitic on the same rodent host. Ecological Entomology 30, 146155.CrossRefGoogle Scholar
Larson, J. S. and Taber, R. D. (1980). Criteria of sex and age. In Wildlife Management Techniques Manual (ed. Schemnitz, S. D.), pp. 143202. Wildlife Society, Washington DC.Google Scholar
Lindström, A. and Jaenson, T. G. T. (2003). Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. Journal of Medical Entomology 40, 375378.CrossRefGoogle ScholarPubMed
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A. and Keesing, F. (2003). The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proceedings of the National Academy of Sciences, USA 100, 567571.CrossRefGoogle ScholarPubMed
Lotze, J. H. and Anderson, S. (1979). Procyon lotor. Mammalian Species 119, 18.CrossRefGoogle Scholar
Macaluso, K. R., Sonenshine, D. E., Ceraul, S. M. and Azad, A. F. (2002). Rickettsial infection in Dermacentor variabilis (Acari: Ixodidae) inhibits transovarial transmission of a second Rickettsia. Journal of Medical Entomology 398, 809813.CrossRefGoogle Scholar
McEnroe, W. D. (1971). The effect of automobile traffic on American dog tick distribution (Dermacentor variabilis, Say: Acarina: Ixodidae). Environmental Pollution 2, 135143.Google Scholar
McEnroe, W. D. (1974). The regulation of adult American dog tick, Dermacentor variabilis Say, seasonal activity and breeding potential (Ixodidae: Acarina). Acarologia 16, 651663.Google Scholar
McEnroe, W. D. (1979). Dermacentor variabilis (Say) in eastern Massachusetts. In Recent Advances in Acarology (ed. Rodriguez, J. G.), pp. 145153. Academic Press, New York.CrossRefGoogle Scholar
McEnroe, W. D. and Specht, H. B. (1987). Age effect analysis of Dermacentor variabilis (Say) adult populations during seasonal activity (Acari: Ixodidae). Canadian Journal of Zoology 65, 455457.CrossRefGoogle Scholar
Moore, S. L. and Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 20152018.CrossRefGoogle ScholarPubMed
Mooring, M. S., McKenzie, A. A. and Hart, B. L. (1996). Role of sex and breeding status in grooming and total tick load of impala. Behavioral Ecology and Sociobiology 39, 259266.CrossRefGoogle Scholar
Morales-Montor, J., Chavarria, A., De León, M. A., Del Castillo, L. I., Escobedo, E. G., Sánchez, E. N., Vargas, J. A., Hernández-Flores, M., Romo-González, T. and Larralde, C. (2004). Host gender in parasitic infections of mammals: an evaluation of the female host supremacy paradigm. Journal of Parasitology 90, 531554.CrossRefGoogle ScholarPubMed
Newhouse, V. F. (1983). Variations in population density, movement, and rickettsial infection rates in a local population of Dermacentor variabilis (Acarina: Ixodidae) ticks in the Piedmont of Georgia. Environmental Entomology 12, 17371746.CrossRefGoogle Scholar
Parola, P., Paddock, C. D. and Raoult, D. (2005). Tick borne rickettsioses around the world: emerging diseases challenging old concepts. Clinical Microbiology Reviews 18, 719756.CrossRefGoogle ScholarPubMed
Piesman, J., Mather, T. N., Sinsky, R. J. and Spielman, A. (1987). Duration of tick attachment and Borrelia burgdorferi transmission. Journal of Clinical Microbiology 25, 557558.CrossRefGoogle ScholarPubMed
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being male? American Naturalist 147, 287295.CrossRefGoogle Scholar
Quinnell, R. J. (1992). The population dynamics of Heligmosomoides polygyrus in an enclosed population of wood mice. Journal of Animal Ecology 61, 669679.CrossRefGoogle Scholar
Randolph, S. E. (1994). Population dynamics and density-dependent seasonal mortality indices of the tick Rhipicephalus appendiculatus in eastern and southern Africa. Medical and Veterinary Entomology 8, 351368.CrossRefGoogle ScholarPubMed
Rozsa, L., Reiczigel, J. and Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.CrossRefGoogle ScholarPubMed
Schalk, G. and Forbes, M. R. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 6774.CrossRefGoogle Scholar
Sonenshine, D. E. (1979). Zoogeography of the American dog tick, Dermacentor variabilis. In Recent Advances in Acarology (ed. Rodriguez, J. G.), pp. 123134. Academic Press, New York.CrossRefGoogle Scholar
Sonenshine, D. E. (1991). Biology of Ticks. Oxford University Press, New York.Google Scholar
Sonenshine, D. E. and Stout, J. J. (1971). Ticks infesting medium-sized wild mammals in two forest localities in Virginia. Journal of Medical Entomology 8, 217227.CrossRefGoogle ScholarPubMed
Strickland, R. K., Gerrish, R. R., Hourrigan, J. L. and Schubert, G. O. (1976). Ticks of Veterinary Importance. Washington D.C. APHIS, USDA Handbook 485.Google Scholar
Trager, W. (1939). Acquired immunity to ticks. Journal of Parasitology 25, 5781.CrossRefGoogle Scholar
Tripet, F. and Richner, H. (1999). Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology 80, 12671277.CrossRefGoogle Scholar
Whitaker, J. O. Jr. (1982). Ectoparasites of Mammals of Indiana. The Indiana Academy of Science, Indianapolis, USA.Google Scholar
Wikel, S. K. (1996). The Immunology of Host-Ectoparasitic Arthropod Relationships. CAB International, Wallingford, UK.Google Scholar
Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2003). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (ed. Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp. 644. Oxford University Press, New York.Google Scholar
Wilson, M. L., Litwin, T. S., Gavin, T. A., Capkanis, M. C., MaClean, D. C. and Spielman, A. (1990). Host-dependent differences in feeding and reproduction of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology 27, 945954.CrossRefGoogle ScholarPubMed
Wright, A. N. and Gompper, M. G. (2005). Altered parasite assemblages in raccoons in response to manipulated resource availability. Oecologia 144, 148156.CrossRefGoogle ScholarPubMed
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 10091023.CrossRefGoogle ScholarPubMed