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The effect of Babesia microti on feeding and survival in its tick vector, Ixodes trianguliceps

Published online by Cambridge University Press:  06 April 2009

S. E. Randolph
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS

Summary

Evidence is presented that Babesia microti may promote its transmission amongst rodents by enhancing the feeding success and survival of its tick vector, Ixodes trianguliceps. Both the mean engorged weight of larval ticks and the percentage moult of larvae to nymphs increased as larvae fed on naive hosts later in the parasitaemic cycle up to a point a few days beyond the loss of a patent infection. This increased feeding success and survival was not dependent on the level of infection by B. microti. Two possible, host-mediated mechanisms for the observed parasite–vector interactions are suggested, the anti-haemostatic effects induced by babesiosis and the interaction of the immunosuppressive effects of Babesia and the development of immunity to ixodid ticks by their vertebrate hosts.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

Allen, P. C., Frierichs, W. M. & Holbrook, A. A. (1975). Experimental acute Babesia caballi infections. II. Response of platelets and fibrinogen. Experimental Parasitology 37, 373–9.CrossRefGoogle ScholarPubMed
Aron, J. L. & May, R. M. (1982). The population dynamics of malaria. In Population Dynamics of Infectious Diseases (ed. Anderson, R. M.), pp. 139–79. London: Chapman & Hall.CrossRefGoogle Scholar
Barnett, S. F. & Croft, R. A. (1978). The epidemiology of Babesia microti in the bank vole Clethrionomys glareolus. In Tick-borne Diseases and their Vectors (ed. Wilde, J. K. H.), pp. 137–43. Edinburgh: Centre for Tropical Veterinary Medicine.Google Scholar
Bowessidjaou, J., Brossard, M. & Aeschlimann, A. (1977). Effects and duration of resistance acquired by rabbits on feeding and egg laying in Ixodes ricinus L. Experientia 33, 528–30.CrossRefGoogle ScholarPubMed
Brossard, M. (1977). Rabbits infested with the adults of Ixodes ricinus L.: passive transfer of resistance with immune serum. Bulletin de la Société de Pathologie Exotique 70, 289–94.Google ScholarPubMed
Brossard, M. & Fivaz, V. (1982). Ixodes ricinus L.: mast cells, basophils and eosinophils in the sequence of cellular events in the skin of infested or re-infested rabbits. Parasitology 85, 583–92,CrossRefGoogle ScholarPubMed
Brossard, M., Monneron, J. P. & Papatheodorou, V. (1982). Progressive sensitization of circulating basophils Ixodes ricinus L. antigens during repeated infestations on rabbits. Parasite Immunology 4, 355–61.CrossRefGoogle Scholar
Callow, L. L. & Stewart, N. P. (1978). Immunosuppression by Babesia bovis against its tick vector, Boophilus microplus. Nature, London 272, 818–19.CrossRefGoogle ScholarPubMed
Clarke, F. C., Els, D. A., Heller-Haupt, A., Rechav, Y. & Varma, M. G. R. (1989). Expression of acquired immunity to immature stages of the tick Rhipicephalus evertsi evertsi by rabbits and guinea-pigs. Medical and Veterinary Entomology 3, 35–9.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (1976). Increased virulence of trypanosome infections in mice with malaria or piroplasmosis: immunological considerations. In Second International Symposium on the Biochemistry of Parasites and Host–Parasite Relationships (ed. Van der Bossche, H.), pp. 129–34. Amsterdam: Elsevier.Google Scholar
Davey, R. B. (1981). Effects of Babesia bovis on the ovipositional success of the southern cattle tick, Boophilus microplus. Annals of the Entomological Society of America 74, 331–3.CrossRefGoogle Scholar
De VOS, A. J., Stewart, N. P. & Dalgliesh, R. J. (1989). Effect of different methods of maintenance on the pathogenicity and infectivity of Babesia bigemina for the vector Boophilus microplus. Research in Veterinary Science 46, 139–42.CrossRefGoogle ScholarPubMed
Gray, J. S. (1982). The effects of the piroplasm Babesia bigemina on survival and reproduction of the blue tick, Boophilus decoloratus. Journal of Invertebrate Pathology 39, 413–15.CrossRefGoogle ScholarPubMed
Gray, G. D. & Phillips, R. S. (1983). Suppression of primary and secondary antibody responses and inhibition of antigen priming during Babesia microti infections in mice. Parasite Immunology 5, 123–34.CrossRefGoogle ScholarPubMed
Hussein, H. S. (1981). Studies on the haematology of Babesia hylomysci and Babesia microti infections in mice. I. Haematological parameters during the infections. Sudan Journal of Veterinary Science and Animal Husbandry 22, 4254.Google Scholar
Molyneux, D. H. & Jefferies, D. (1986). Feeding behaviour of pathogen-infected vectors. Parasitology 92, 721–36.CrossRefGoogle ScholarPubMed
Njau, B. C. & Nyindo, M. (1987). Humoral response of rabbits to Rhipicephalus appendiculatus infestation. Research in Veterinary Science 43, 271–2CrossRefGoogle ScholarPubMed
Phillips, R. S. & Wakelin, D. (1976). Trichuris muris: effect of concurrent infections with rodent piroplasms on immune expulsion from mice. Experimental Parasitology 39, 95100.CrossRefGoogle ScholarPubMed
Purvis, A. C. (1977). Immunodepression in Babesia microti infections. Parasitology 75, 197205.CrossRefGoogle ScholarPubMed
Randolph, S. E. (1979). Population regulation in ticks: the role of acquired resistance in natural and unnatural hosts. Parasitology 79, 141–56.CrossRefGoogle ScholarPubMed
Rechav, Y. & Dauth, J. (1987). Development of resistance in rabbits to immature stages of the Ixodid tick Rhipicephalus appendiculatus. Medical and Veterinary Entomology 1, 177–83.CrossRefGoogle ScholarPubMed
Rechav, Y., Dauth, J., Varma, M. G. R., Clarke, F. C., Els, D. A., Heller-HAUPT, A. & Dreyer, M. J. (1989). Changes in the concentration of globulins in naive guinea pigs during feeding by the immature stages of Rhipicephalus evertsi evertsi (Acari: Ixodidae). Journal of Medical Entomology 26, 247–51.CrossRefGoogle ScholarPubMed
Rogers, D. J. (1988). A general model for the African trypanosomiases. Parasitology 97, 193212.CrossRefGoogle ScholarPubMed
Rossingnol, P. A., Ribeiro, J. M. C., Jungery, M., Turell, M. J., Spielman, A. & Bailey, C. L. (1985). Enhanced mosquito blood-finding success on parasitaemic hosts: Evidence for vector-parasite mutualism. Proceedings of the National Academy of Sciences, USA 82, 7725–7.CrossRefGoogle Scholar
Turner, C. M. R. & Cox, F. E. G. (1985). The stability of Babesia microti infections after prolonged passage, a comparison with a recently isolated strain. Annals of Tropical Medicine and Parasitology 79, 659–61.CrossRefGoogle Scholar
Turell, M. J., Gargan, T. P. & Bailey, C. L. (1985). Culex pipiens (Diptera: Culicidae) morbidity and mortality associated with Rift Valley Fever virus infection. Journal of Medical Entomology 3, 332–7.CrossRefGoogle Scholar
Walker, A. R. & Fletcher, J. D. (1987). Histology of digestion in nymphs of Rhipicephalus appendiculatus fed on rabbits and cattle naive and resistant to the ticks. International Journal for Parasitology 17, 13931411.CrossRefGoogle Scholar
Wikel, S. K. (1982). Immune responses to arthropods and their products. Annual Review of Entomology 27, 2148.CrossRefGoogle ScholarPubMed
Wikel, S. K. & Allen, J. R. (1982). Immunological basis of host resistance to ticks. In Physiology of Ticks (ed. Obenchain, F. D. & Galun, R.) pp. 169–96. Oxford: Pergamon.CrossRefGoogle Scholar
Willadsen, P. (1980). Immunity to ticks. Advances in Parasitology 18, 293313.CrossRefGoogle ScholarPubMed
Young, A. S. (1970). Investigations on the epidemiology of blood parasites of small mammals with special reference to piroplasms. Ph.D. thesis, University of London.Google Scholar