Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T22:37:57.876Z Has data issue: false hasContentIssue false
  • English
  • Français

Trypanosomes, fleas and field voles: ecological dynamics of a host-vector–parasite interaction

Published online by Cambridge University Press:  06 May 2005

A. SMITH ,
S. TELFER ,
S. BURTHE ,
M. BENNETT  and
M. BEGON
A. SMITH
Affiliation:
Population Biology Research Group, School of Biological Sciences, Biosciences Building, University of Liverpool, Liverpool L69 7ZB, UK
S. TELFER
Affiliation:
Population Biology Research Group, School of Biological Sciences, Biosciences Building, University of Liverpool, Liverpool L69 7ZB, UK Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
S. BURTHE
Affiliation:
Population Biology Research Group, School of Biological Sciences, Biosciences Building, University of Liverpool, Liverpool L69 7ZB, UK
M. BENNETT
Affiliation:
Department of Veterinary Pathology, University of Liverpool, Leahurst, Neston CH64 7TE, UK
M. BEGON
Affiliation:
Population Biology Research Group, School of Biological Sciences, Biosciences Building, University of Liverpool, Liverpool L69 7ZB, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

To investigate the prevalence of a flea-borne protozoan (Trypanosoma (Herpetosoma) microti) in its field vole (Microtus agrestis) host, we monitored over a 2-year period a range of intrinsic and extrinsic parameters pertaining to host demographics, infection status and vector (flea) prevalence. Generalized Linear Mixed Modelling was used to analyse patterns of both flea and trypanosome occurrence. Overall, males of all sizes and ages were more likely to be infested with fleas than their female counterparts. Flea prevalence also showed direct density dependence during the winter, but patterns of density dependence varied amongst body mass (age) classes during the summer. Trypanosome prevalence did not vary between the sexes but was positively related to past flea prevalence with a lag of 3 months, with the highest levels occurring during the autumn season. A convex age-prevalence distribution was observed, suggesting that individuals develop a degree of immunity to trypanosome infection with age and exposure. An interaction between age and whether the individual was new or recaptured suggested that infected animals are less likely to become territory holders than their uninfected counterparts.

Keywords

Trypanosoma microtiMicrotus agrestisfield volevector borneSiphonapteraacquired immunitynatural populationsex-biasKielder Forest
Type
Research Article
Information
Parasitology , Volume 131 , Issue 3 , September 2005 , pp. 355 - 365
Copyright
© 2005 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

Agrell, J., Erlinge, S., Nelson, J. and Sandell, M. ( 1996). Shifting spacing behaviour of male field voles (Microtus agrestis) over the reproductive season. Annales Zoologici Fennici 33, 243–248.Google Scholar
Albright, J. W. and Albright, J. F. ( 1991). Rodent trypanosomes: Their conflict with the immune system of the host. Parasitology Today 7, 137–140.CrossRefGoogle Scholar
Bajer, A., Pawelczyk, A., Behnke, J. M., Gilbert, F. S. and Sinski, E. ( 2001). Factors affecting the component community structure of haemoparasites in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 122, 43–54.CrossRefGoogle Scholar
Barrett, M. P., Burchmore, R. J. S., Stich, A., Lazzari, J. O., Frasch, A. C., Cazzulo, J. J. and Krishna, S. ( 2003). The trypanosomiases. Lancet 362, 1469–1480.CrossRefGoogle Scholar
Borowski, Z. ( 2003). Habitat selection and home range size of field voles Microtus agrestis in Slowinski National Park, Poland. Acta Theriologica 48, 325–333.CrossRefGoogle Scholar
Bown, K. J., Begon, M., Bennett, M., Woldehiwet, Z. and Ogden, N. H. ( 2003). Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases 9, 63–70.CrossRefGoogle Scholar
Brambell, F. W. R. ( 1958). The passive immunity of the young mammal. Biological Reviews of the Cambridge Philosophical Society 33, 488–531.CrossRefGoogle Scholar
Brown, M. J. F., Loosli, R. and Schmid-Hempel, P. ( 2000). Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427.CrossRefGoogle Scholar
Brown, M. J. F., Schmid-Hempel, R. and Schmid-Hempel, P. ( 2003). Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology 72 994–1002.CrossRefGoogle Scholar
Burnham, K. P. and Anderson, D. R. ( 2002). Model Selection and Multi-model Inference: A Practical Information-Theoretic Approach, Springer Verlag, Berlin.
Burnham, K. P., White, G. C. and Anderson, D. R. ( 1995). Model selection strategy in the analysis of capture-recapture data. Biometrics 51, 888–898.CrossRefGoogle Scholar
Bursten, S. N., Kimsey, R. B. and Owings, D. H. ( 1997). Ranging of male Oropsylla montana fleas via male California ground squirrel (Spermophilus beecheyi) juveniles. Journal of Parasitology 83, 804–809.CrossRefGoogle Scholar
Cavanagh, R. D. ( 2001). Interactions between population dynamics, body condition and infectious diseases (Cowpox virus and Mycobacterium microti of wild rodents). Ph.D. thesis, University of Liverpool.
Cavanagh, R. D., Lambin, X, Ergon, T., Bennett, M., Graham, I. M., Van Soolingen, D. and Begon, M. ( 2004). Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proceedings of the Royal Society of London, B 271, 859–867.CrossRefGoogle Scholar
Daszak, P., Cunningham, A. and Hyatt, A. D. ( 2000). Wildlife ecology – emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle Scholar
De almeida, P., Ndao, M., Goossens, B. and Osaer, S. ( 1998). PCR primer evaluation for the detection of trypanosome DNA in naturally infected goats. Veterinary Parasitology 80, 111–116.CrossRefGoogle Scholar
Deerenberg, C., Arpanius, V., Daan, S. and Bos, N. ( 1997). Reproductive effort decreases antibody responsiveness. Proceedings of the Royal Society of London, B 264, 1021–1029.CrossRefGoogle Scholar
Desquesnes, M. and Davila, A. M. R. ( 2002). Applications of PCR-based tools for detection and identification of animal trypanosomes: a review and perspectives. Veterinary Parasitology 109, 213–231.CrossRefGoogle Scholar
Healing, T. D. ( 1981). Infections with blood parasites in the small British rodents Apodemus sylvaticus, Clethrionomys glareolus and Microtus agrestis. Parasitology 83, 179–189.CrossRefGoogle Scholar
Hoare, C. A. ( 1972). The Trypanosomes of Mammals: a Zoological Monograph. Blackwell Scientific Publications, Oxford.
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. 114–176. Cambridge University Press, Cambridge.CrossRef
Johnson, J. B. and Omland, K. S. ( 2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108.CrossRefGoogle Scholar
Khansari, D. N., Murgo, A. J. and Faith, R. E. ( 1990). Effects of stress on the immune system. Immunology Today 11, 170–175.CrossRefGoogle Scholar
Klein, S. L. and Nelson, R. J. ( 1999). Influence of social factors on immune function and reproduction. Reviews of Reproduction 4, 168–178.CrossRefGoogle Scholar
Krasnov, B., Khokhlova, I. and Shenbrot, G. ( 2002). The effect of host density on ectoparasite distribution: An example of a rodent parasitized by fleas. Ecology 83, 164–175.CrossRefGoogle Scholar
Krebs, C. J. ( 1966). Demographic changes in fluctuating populations of Microtus californicus. Ecological Monographs 36, 240–273.CrossRefGoogle Scholar
Lambin, X., Petty, S. J. and MacKinnon, J. L. ( 2000). Cyclic dynamics in field vole populations and generalist predation. Journal of Animal Ecology 69, 106–118.CrossRefGoogle Scholar
Lang, J. D. ( 1996). Factors effecting the seasonal abundance of ground squirrel and wood rat fleas (Siphonaptera) in San Diego County, California. Journal of Medical Entomology 33, 790–804.CrossRefGoogle Scholar
Lehmann, T. ( 1992). Reproductive activity of Synosternus cleopatrae (Siphonaptera, Pulicidae) in relation to host factors. Journal of Medical Entomology 29, 946–952.CrossRefGoogle Scholar
Littell, R. C., Milliken, G. A., Srtoup, W. W. and Wolfinger, R. D. ( 1996). SAS System for Mixed Models. SAS Institute InC., Cary, NC.
Lundqvist, L. ( 1988). Reproductive strategies of ectoparasites on small mammals. Canadian Journal of Zoology-Revue Canadienne De Zoologie 66, 774–781.CrossRefGoogle Scholar
Masiga, D. K., Smyth, A. J., Hayes, P., Bromidge, T. J. and Gibson, W. C. ( 1992). Sensitive detection of trypanosomes in tsetse flies by DNA amplification. International Journal for Parasitology 22, 909–918.CrossRefGoogle Scholar
Molyneux, D. H. ( 1968). Trypanosomes of Microtus agrestis and Clethrionomys glareolus. Parasitology 58, 6.Google Scholar
Molyneux, D. H. ( 1969). Morphology and life history of Trypanosoma (Herpetosoma) microti of field vole, Microtus agrestis. Annals of Tropical Medicine and Parasitology 63, 229–244.CrossRefGoogle Scholar
Morales-Montor, J., Chavarria, A., De Leon, M. A., Del Castillo, L. I., Escobedo, E. G., Sanchez, E. N., Vargas, J. A., Hernandez-Flores, M., Romo-Gonzalez, T. and Larralde, C. ( 2004). Host gender in parasitic infections of mammals: An evaluation of the female host supremacy paradigm. Journal of Parasitology 90, 531–546.CrossRefGoogle Scholar
Morner, T. D., Obendorf, L., Artois, M. and Woodford, M. H. ( 2002). Surveillance and monitoring of wildlife diseases. Revue Scientifique et Technique de L' Office International des Epizooties 21, 67–76.CrossRefGoogle Scholar
Myllymaki, A. ( 1977). Intraspecific competition and home range dynamics in field vole Microtus agrestis. Oikos 29, 553–569.CrossRefGoogle Scholar
Noyes, H. A., Ambrose, P., Barker, F., Begon, M., Bennet, M., Bown, K. J. and Kemp, S. J. ( 2002). Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology 124, 185–190.Google Scholar
Noyes, H. A., Stevens, J. R., Teixeira, M., Phelan, J. and Holz, P. ( 1999). A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 29, 331–339.CrossRefGoogle Scholar
Noyes, H. A., Stevens, J. R., Teixeira, M., Phelan, J. and Holz, P. ( 2000). A nested PCR for the ssrRNA gene detects Trypanosoma binneyi in the platypus and Trypanosoma sp. in wombats and kangaroos in Australia. International Journal for Parasitology 30, 228–228.CrossRefGoogle Scholar
Otis, D. L., Burnham, K. P., White, G. C. and Anderson, D. R. ( 1978). Statistical inference from capture data on closed animal populations. Wildlife Monographs 62, 7–135.Google Scholar
Paterson, S. and Lello, J. ( 2003). Mixed models: getting the best use of parasitological data. Trends in Parasitology 19, 370–375.CrossRefGoogle Scholar
Pawelczyk, A., Bajer, A., Behnke, J. M., Gilbert, F. S. and Sinski, E. ( 2004). Factors affecting the component community structure of haemoparasites in common voles (Microtus arvalis) from the Mazury Lake District region of Poland. Parasitology Research 92, 270–284.CrossRefGoogle Scholar
Perkins, S. E., Cattadori, I. M., Tagliapietra, V., Rizzoli, A. P. and Hudson, P. J. ( 2003). Empirical evidence for key hosts in persistence of a tick-borne disease. International Journal for Parasitology 33, 909–917.CrossRefGoogle Scholar
Pollock, K. H. ( 1982). A capture-recapture design robust to unequal probability of capture. Journal of Wildlife Management 46, 752–757.CrossRefGoogle Scholar
Poulin, R. ( 1996). Sexual inequalities in helminth infections: A cost of being a male? American Naturalist 147, 287–295.Google Scholar
Pusenius, J. and Viitala, J. ( 1993). Varying spacing behaviour of field voles, Microtus agrestis. Annales Zoologici Fennici 30, 143–152.Google Scholar
Reich, L. M., Wood, K. M., Rothstein, B. E. and Tamarin, R. H. ( 1982). Aggressive behaviour of male Microtus breweri and its demographic implications. Animal Behaviour 30, 117–122.CrossRefGoogle Scholar
Robbins, R. G. and Faulkenberry, G. D. ( 1982). A population model for fleas of the grey tailed vole, Microtus canicaudus Miller. Entomological News 93, 70–74.Google Scholar
Saino, N., Canova, L., Fasola, M. and Martinelli, R. ( 2000). Reproduction and population density affect humoral immunity in bank voles under field experimental conditions. Oecologia 124, 358–366.CrossRefGoogle Scholar
SAS/STAT ( 1992). SAS/STAT Users Guide. Version 6, Fourth Edition. SAS Institute, Cary, North Carolina, USA.
Sato, H., Ishita, K., Osanai, A., Yagisawa, M., Kamiya, H. and Ito, M. ( 2004). T cell dependent elimination of dividing Trypanosoma grosi from the bloodstream Mongolian jirds. Parasitology 128, 295–304.CrossRefGoogle Scholar
Shaw, D. J. and Dobson, A. P. ( 1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111 (Suppl.) S111–S133.CrossRefGoogle Scholar
Solano, P., Michel, J. F., Lefrancois, T., De la Rocque, S., Sidibe, I., Zoungrana, A. and Cuisance, D. ( 1999). Polymerase chain reaction as a diagnosis tool for detecting trypanosomes in naturally infected cattle in Burkina Faso. Veterinary Parasitology 86, 95–103.CrossRefGoogle Scholar
Stanko, M., Miklisova, D., De Bellocq, J. G. and Morand, S. ( 2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295.CrossRefGoogle Scholar
Stark, H. E. ( 2002). Population dynamics of adult fleas (Siphonaptera) on hosts and in nests of the California vole. Journal of Medical Entomology 39, 818–824.CrossRefGoogle Scholar
Taylor, G. T., Haller, J., Rupich, R. and Weiss, J. ( 1984). Testicular hormones and intermale aggressive behaviour in the presence of a female rat. Journal of Endocrinology 100, 315–321.CrossRefGoogle Scholar
Tschirren, B., Fitze, P. S. and Richner, H. ( 2003). Sexual dimorphism in susceptibility to parasites and cell- mediated immunity in great tit nestlings. Journal of Animal Ecology 72, 839–845.CrossRefGoogle Scholar
Turchin, P. ( 2003). Complex Population Dynamics: A Theoretical Synthesis. Princeton University Press, Princeton, New Jersey.
Turner, C. M. R. ( 1986). Seasonal and age distributions of Babesia, Hepatozoon, Trypanosoma and Grahamella species in Clethrionomys glareolus and Apodemus sylvaticus populations. Parasitology 93, 279–289.CrossRefGoogle Scholar
Wiger, R. ( 1977). Some pathological effects of endoparasites on rodents with special reference to population ecology of microtines. Oikos 29, 598–606.CrossRefGoogle Scholar
Williams, E. S., Yuill, T., Artois, M., Fischer, J. and Haigh, S. A. ( 2002). Emerging infectious diseases in wildlife. Revue Scientifique et Technique de L' Office International des Epizooties 21, 139–157.CrossRefGoogle Scholar
Wita, I., Karbowiak, G. and Czaplinska, U. ( 2003). Trypanosoma (Herpetosoma) microti Laveran et Pettit, 1909 in the social vole, Microtus socialis (Pallas, 1771) from Ukraine. Acta Parasitologica 48, 155–162.Google Scholar
Woolhouse, M. E. J., Dye, C., Etard, J. F., Smith, T., Charlwood, J. D., Garnett, G. P., Hagan, P., Hii, J. L. K., Ndhlovu, P. D., Quinnell, R. J., Watts, C. H., Chandiwana, S. K. and Anderson, R. M. ( 1997). Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences, USA 94, 338–342.CrossRefGoogle Scholar
Zuk, M. and McKean, K. A. ( 1996). Sex differences in parasite infections: Patterns and processes. International Journal for Parasitology 26, 1009–1023.CrossRefGoogle Scholar