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Disruption of a host-parasite system following the introduction of an exotic host species

Published online by Cambridge University Press:  15 February 2005

S. TELFER ,
K. J. BOWN ,
R. SEKULES ,
M. BEGON ,
T. HAYDEN  and
R. BIRTLES
S. TELFER
Affiliation:
School of Biological Sciences, The University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, The University of Liverpool, Leahurst, Neston CH64 7TE, UK
K. J. BOWN
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, The University of Liverpool, Leahurst, Neston CH64 7TE, UK
R. SEKULES
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, The University of Liverpool, Leahurst, Neston CH64 7TE, UK
M. BEGON
Affiliation:
School of Biological Sciences, The University of Liverpool, Biosciences Building, Liverpool L69 7LB, UK
T. HAYDEN
Affiliation:
Department of Zoology, University College Dublin, National University of Ireland Dublin, Belfield, Dublin 4, Ireland
R. BIRTLES
Affiliation:
Centre for Comparative Infectious Diseases, Department of Veterinary Pathology, The University of Liverpool, Leahurst, Neston CH64 7TE, UK
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Abstract

The potential of biological invasions to threaten native ecosystems is well recognized. Here we describe how an introduced species impacts on native host-parasite dynamics by acting as an alternative host. By sampling sites across an invasion front in Ireland, we quantified the influence of the introduced bank vole (Clethrionomys glareolus) on the epidemiology of infections caused by flea-transmitted haemoparasites of the genus Bartonella in native wood mice (Apodemus sylvaticus). Bartonella infections were detected on either side of the front but occurred exclusively in wood mice, despite being highly prevalent in both rodent species elsewhere in Europe. Bank vole introduction has, however, affected the wood mouse-Bartonella interaction, with the infection prevalence of both Bartonella birtlesii and Bartonella taylorii declining significantly with increasing bank vole density. Whilst flea prevalence in wood mice increases with wood mouse density in areas without bank voles, no such relationship is detected in invaded areas. The results are consistent with the dilution effect hypothesis. This predicts that for vector-transmitted parasites, the presence of less competent host species may reduce infection prevalence in the principal host. In addition we found a negative relationship between B. birtlesii and B. taylorii prevalences, indicating that these two microparasites may compete within hosts.

Keywords

introduced speciesreservoir competencedensity-dependent transmissionhost specificitySiphonapteravectordilution effect
Type
Research Article
Information
Parasitology , Volume 130 , Issue 6 , June 2005 , pp. 661 - 668
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

BAJER, A., PAWELCZYK, A., BEHNKE, J. M., GILBERT, F. S. & 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
BIRTLES, R. J., HARRISON, T. G. & MOLYNEUX, D. H. ( 1994). Grahamella in small woodland mammals in the UK – isolation, prevalence and host-specificity. Annals of Tropical Medicine and Parasitology 88, 317–327.CrossRefGoogle Scholar
BIRTLES, R. J., HAZEL, S. M., BENNETT, M., BOWN, K., RAOULT, D. & BEGON, M. ( 2001). Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126, 323–329.CrossRefGoogle Scholar
BOULOUIS, H. J., BARRAT, F., BERMOND, D., BERNEX, F., THIBAULT, D., HELLER, R., FONTAINE, J. J., PIEMONT, Y. & CHOMEL, B. B. ( 2001). Kinetics of Bartonella birtlesii infection in experimentally infected mice and pathogenic effect on reproductive functions. Infection and Immunity 69, 5313–5317.CrossRefGoogle Scholar
BOWN, K. J., BEGON, M., BENNETT, M., WOLDEHIWIT, Z. & 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
BURNHAM, K. P. & ANDERSON, D. R. ( 1992). Data-based selection of an appropriate biological model: the key to modern data analysis. In Wildlife 2001: Populations (ed. McCullough, D. R. & Barrett, R. H.), pp. 16–30. Elsevier Science Publishers, London.CrossRef
CHOMEL, B. B., KASTEN, R. W., SYKES, J. E., BOULOUIS, H. J. & BREITSCHWERDT, E. B. ( 2003). Clinical impact of persistent Bartonella bacteremia in humans and animals. Annals of the New York Academy of Science 990, 267–278.CrossRefGoogle Scholar
COX, F. E. G. ( 2001). Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.CrossRefGoogle Scholar
DOBSON, A. & FOUFOPOULOS, J. ( 2001). Emerging infectious pathogens of wildlife. Philosophical Transactions of the Royal Society of London Series B 356, 1001–1012.CrossRefGoogle Scholar
HOLMBERG, M., MILLS, J. N., MCGILL, S., BENJAMIN, G. & ELLIS, B. A. ( 2003). Bartonella infection in sylvatic small mammals of central Sweden. Epidemiology and Infection 130, 149–157.CrossRefGoogle Scholar
HOLT, R. D., DOBSON, A. P., BEGON, M., BOWERS, R. G. & SCHAUBER, E. M. ( 2003). Parasite establishment in host communities. Ecology Letters 6, 837–842.CrossRefGoogle Scholar
HOLT, R. D. & LAWTON, J. H. ( 1993). Apparent competition and enemy-free space in insect host- parasitoid communities. American Naturalist 142, 623–645.CrossRefGoogle Scholar
HUDSON, P. J., DOBSON, A. P. & NEWBORN, D. ( 1998). Prevention of population cycles by parasite removal. Science 282, 2256–2258.CrossRefGoogle Scholar
JOHNSON, J. B. & OMLAND, K. S. ( 2004). Model selection in ecology and evolution. Trends in Ecology and Evolution 19, 101–108.CrossRefGoogle Scholar
KHOKHLOVA, I. S., KRASNOV, B. R., KAM, M., BURDELOVA, N. I. & DEGEN, A. A. ( 2002). Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus. Journal of Zoology 258, 349–354.CrossRefGoogle Scholar
KOSOY, M. Y., REGNERY, R. L., TZIANABOS, T., MARSTON, E. L., JONES, D. C., GREEN, D., MAUPIN, G. O., OLSON, J. G. & CHILDS, J. E. ( 1997). Distribution, diversity, and host specificity of Bartonella in rodents from the southeastern United States. American Journal of Tropical Medicine and Hygiene 57, 578–588.CrossRefGoogle Scholar
KOSOY, M. Y., SAITO, E. K., GREEN, D., MARSTON, E. L., JONES, D. C. & CHILDS, J. E. ( 2000). Experimental evidence of host specificity of Bartonella infection in rodents. Comparative Immunology, Microbiology and Infectious Diseases 23, 221–238.CrossRefGoogle Scholar
KRAMPITZ, H. E. ( 1962). Weitere Untersuchungen an Grahamella Brumpt 1911. Zeitschrift für Tropenmedizin und Parasitologie 13, 34–53.Google Scholar
KRAMPITZ, H. E. & KLEINSCHMIDT, A. ( 1960). Grahamella Brumpt 1911. Biologische und morphologische Untersuchungen. Zeitschrift für Tropenmedizin und Parasitologie 11, 336–352.Google Scholar
LAURENSON, M. K., NORMAN, R. A., GILBERT, L., REID, H. W. & HUDSON, P. J. ( 2003). Identifying disease reservoirs in complex systems: mountain hares as reservoirs of ticks and louping-ill virus, pathogens of red grouse. Journal of Animal Ecology 72, 177–185.CrossRefGoogle Scholar
LELLO, J., BOAG, B., FENTON, A., STEVENSON, I. R. & HUDSON, P. J. ( 2004). Competition and mutalism among the gut helminths of a mammalian host. Nature, London 428, 840–844.CrossRefGoogle Scholar
LOGIUDICE, K., OSTFELD, R. S., SCHMIDT, K. A. & 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, 567–571.CrossRefGoogle Scholar
MACK, R. N., SIMBERLOFF, D., LONSDALE, W. M., EVANS, H., CLOUT, M. & BAZZAZ, F. A. ( 2000). Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689–710.CrossRefGoogle Scholar
MITCHELL, C. E. & POWER, A. G. ( 2003). Release of invasive plants from fungal and viral pathogens. Nature, London 421, 625–627.CrossRefGoogle Scholar
NEUHAUS, P. ( 2003). Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus). Proceedings of the Royal Society of London, B (Suppl.) 270, S213–S215.CrossRefGoogle Scholar
NORMAN, R., BOWERS, R. G., BEGON, M. & HUDSON, P. J. ( 1999). Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite mediated competition. Journal of Theoretical Biology 200, 111–118.CrossRefGoogle Scholar
OSTFELD, R. & KEESING, F. ( 2000 a). The function of biodiversity in the ecology of vector-borne zoonotic diseases. Canadian Journal of Zoology 78, 2061–2078.Google Scholar
OSTFELD, R. S. & KEESING, F. ( 2000 b). Biodiversity and disease risk: The case of lyme disease. Conservation Biology 14, 722–728.Google Scholar
ROUX, V. & RAOULT, D. ( 1995). Inter- and Intra- species identification of Bartonella (Rochalimaea) species. Journal of Clinical Microbiology 33, 1573–1579.Google Scholar
SMAL, C. M. & FAIRLEY, J. S. ( 1984). The spread of the bank vole Clethrionomys glareolus in Ireland. Mammal Review 14, 71–78.CrossRefGoogle Scholar
SMIT, F. G. A. M. ( 1957). Siphonaptera. Royal Entomological Society of London, London.
TELFER, S., BENNETT, M., BOWN, K., CAVANAGH, R., CRESPIN, L., HAZEL, S., JONES, T. & BEGON, M. ( 2002). The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology 71, 558–568.CrossRefGoogle Scholar
TOMPKINS, D. M., DOBSON, A. P., ARNEBERG, P., BEGON, M. E., CATTADORI, I. M., GREENMAN, J. V., HEESTERBEEK, J. A. P., HUDSON, P. J., NEWBORN, D., PUGLIESE, A., RIZZOLI, A. P., ROSA, R., ROSSO, F. & WILSON, K. ( 2002). Parasites and host population dynamics. In The Ecology of Wildlife Diseases (ed. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. & Dobson, A. P.), pp. 45–62. Oxford University Press, Oxford.
TORCHIN, M. E., LAFFERTY, K. D., DOBSON, A. P., MCKENZIE, V. J. & KURIS, A. M. ( 2003). Introduced species and their missing parasites. Nature, London 421, 628–630.CrossRefGoogle Scholar
WALKER, P., LEATHER, S. R. & CRAWLEY, M. J. ( 2002). Differential rates of invasion in three related alien oak gall wasps (Cynipidae: Hymenoptera). Diversity and Distributions 8, 335–346.CrossRefGoogle Scholar
WIGER, R. ( 1979). Seasonal and annual variations in the prevalence of blood parasites in cyclic species of small rodents in Norway with special reference to Clethrionomys glareolus. Holarctic Ecology 2, 169–175.CrossRefGoogle Scholar