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Differential virulence in two congeneric ticks infesting songbird nestlings

Published online by Cambridge University Press:  09 June 2011

DIETER J. A. HEYLEN  and
ERIK MATTHYSEN
DIETER J. A. HEYLEN*
Affiliation:
Evolutionary Ecology Group, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerpen, Belgium
ERIK MATTHYSEN
Affiliation:
Evolutionary Ecology Group, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerpen, Belgium
*
*Corresponding author: Groenenborgerlaan 171, B-2020 Antwerpen, Belgium. Tel: +32 3 265 34 70. Fax: +32 3 265 34 74. E-mail: [email protected]
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Summary

Virulence is part of the proximate base to the understanding of host–parasite interactions, and therefore it is crucial to interpret parasite-induced damage as an outcome of co-evolution between parasite and host. We experimentally investigated the impact of 2 congeneric ticks with contrasting transmission modes and host specificity, on the health of songbird nestlings (Parus major). The nidicolous Ixodes arboricola lives in tree holes where it obtains blood from adult birds and their nestlings, hence is prone to vertical transmission. All developmental stages of the field-dwelling Ixodes ricinus feed on different host taxa, hence are prone to horizontal transmission. Within each nest we infested 3 nestlings with varying loads of I. ricinus and 3 with Ixodes arboricola. Ixodes arboricola had no negative effects on nestling health (haematocrit, inflammation, body size, body condition). Body size was positively associated with the number of feeding I. arboricola adults. In contrast, I. ricinus infestations by nymphs and adult ticks led to haematocrit reductions. Furthermore, I. arboricola was a more prudent feeder, with longer feeding durations for smaller bloodmeals. Although the negative effects on nestling health were limited, our results are in line with current theories, stating that virulence increases with horizontal transmission, reduced dependence on individual hosts and reduced relatedness among co-exploiting ticks.

Keywords

virulencetransmissionkin selectionIxodesgreat tit
Type
Research Article
Information
Parasitology , Volume 138 , Issue 8 , July 2011 , pp. 1011 - 1021
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411–426.CrossRefGoogle ScholarPubMed
Apanius, V. (1998). Ontogeny of immune function. In Avian Growth and Development: Evolution Within the Altricial-Precocial Spectrum (ed. Starck, J. M. and Ricklefs, R. E.), pp. 203–222. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Baerg, W. J. (1944). Ticks and other parasites attacking northern cliff swallows. Auk 61, 413–414.CrossRefGoogle Scholar
Balashov, Y. S. (1972). Bloodsucking ticks (Ixodidea) – vectors of diseases of man and animals. Miscellaneous Publications of the Entomological Society of America 8, 159–376.Google Scholar
Bergström, S., Haemig, P. D. and Olsen, B. (1999). Increased mortality of black-browed albatross chicks at a colony heavily-infested with the tick Ixodes uriae. International Journal for Parasitology 29, 1359–1361.CrossRefGoogle Scholar
Bouslama, Z., Chabi, Y. and Lambrechts, M. M. (2001). Chicks resist high parasite intensities in an Algerian population of blue tits. Ecoscience 8, 320–324.CrossRefGoogle Scholar
Buckling, A. and Brockhurst, M. A. (2008). Kin selection and the evolution of virulence. Heredity 100, 484–488.CrossRefGoogle ScholarPubMed
Campbell, T. W. (1994). Cytology. In Avian Medicine: Principles and Applications (ed. Harrison, G. J. and Harrison, L. R.), pp. 199–221. Winger's Publishing, Lake Worth, FL, USA.Google Scholar
Chapman, B. R. and George, J. E. (1991). The effects of ectoparasites on cliff swallow growth and survival. In Bird-Parasite Interactions: Ecology, Evolution and Behaviour (ed. Loye, J. E. and Zuk, M.), pp. 69–92. Oxford University Press, Oxford, UK.Google Scholar
Christe, P., Richner, H. and Oppliger, A. (1996). Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behavioral Ecology 7, 127–131.CrossRefGoogle Scholar
Clayton, D. H. and Moore, J. (1997). Host-Parasite Evolution: General Principles and Avian Models, Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Clayton, D. H. and Tompkins, D. M. (1994). Ectoparasite virulence is linked to mode of transmission. Proceedings of the Royal Society of London, B 256, 211–217.Google ScholarPubMed
Combes, C. (1997). Fitness of parasites: pathology and selection. International Journal for Parasitology 27, 1–10.CrossRefGoogle ScholarPubMed
Comstedt, P., Bergstrom, S., Olsen, B., Garpmo, U., Marjavaara, L., Mejlon, H., Barbour, A. G. and Bunikis, J. (2006). Migratory passerine birds as reservoirs of lyme borreliosis in Europe. Emerging Infectious Diseases 12, 1087–1095.CrossRefGoogle ScholarPubMed
Cox, D. R. and Oakes, D. (1984). Analysis of Survival Data, 1st Edn. Chapman and Hall, London, UK.Google Scholar
Dein, J. (1986). Hematology. In Clinical Avian Medicine, Harrison, G. J. and Harrison, L. R. pp. 174–191. Saunders, London, UK.Google Scholar
Doby, J. M. (1998). Contribution à la connaissance de la biologie de Ixodes (Trichotoixodes) pari Leach (=I. frontalis (Panzer)) (Acari: Ixodidae), Tique spécifique des oiseaux. Acarologia 19, 315–325.Google Scholar
Donohue, K. V., Khalil, S. M. S., Ross, E., Mitchell, R. D., Roe, R. M. and Sonenshine, D. E. (2009). Male engorgement factor: Role in stimulating engorgement to repletion in the ixodid tick, Dermacentor variabilis. Journal of Insect Physiology 55, 909–918.CrossRefGoogle ScholarPubMed
Dubiec, A. and Cichon, M. (2001). Seasonal decline in health status of Great Tit (Parus major) nestlings. Canadian Journal of Zoology-Revue Canadienne De Zoologie 79, 1829–1833.CrossRefGoogle Scholar
Duffy, D. C. (1983). The ecology of tick parasitism on densely nesting peruvian seabirds. Ecology 64, 110–119.CrossRefGoogle Scholar
Dusek, R. J., Spalding, M. G., Forrester, D. J. and Greiner, E. C. (2004). Haemoproteus balearicae and other blood parasites of free-ranging Florida sandhill crane chicks. Journal of Wildlife Diseases 40, 682–687.CrossRefGoogle ScholarPubMed
Eggert, L. M. and Jodice, P. G. R. (2008). Growth of Brown Pelican nestlings exposed to sublethal levels of soft tick infestation. Condor 110, 134–142.CrossRefGoogle Scholar
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 14, 465–485.CrossRefGoogle Scholar
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 37–78.CrossRefGoogle ScholarPubMed
Gallizzi, K., Bischoff, L. L., Gern, L. and Richner, H. (2008). An experimental study on the influence of tick infestations on nestling performance in Great tits (Parus Major). Auk 125, 915–922.CrossRefGoogle Scholar
Garamszegi, L. Z. (2006). The evolution of virulence and host specialization in malaria parasites of primates. Ecology Letters 9, 933–940.CrossRefGoogle ScholarPubMed
Gauthier-Clerc, M., Mangin, S., Le Bohec, C. and Gendner, J. P. (2003). Comparison of behaviour, body mass, haematocrit level, site fidelity and survival between infested and non-infested king penguin Aptenodytes patagonicus by ticks Ixodes uriae. Polar Biology 26, 379–382.CrossRefGoogle Scholar
Glines, M. V. and Samuel, W. M. (1989). Effect of Dermacentor albipictus (Acari, Ixodidae) on blood composition, weight-gain and hair coat of Moose, Alces alces. Experimental & Applied Acarology 6, 197–213.CrossRefGoogle ScholarPubMed
Gosler, A. (1993). The Great Tit, Hamlyn, London, UK.Google Scholar
Gray, J. S. (1991). The development and seasonal activity of the tick Ixodes ricinus: a vector of Lyme borreliosis. Review of Medical and Veterinary Entomology 79, 323–333.Google Scholar
Gray, J. S. (1998). The ecology of ticks transmitting lyme borreliosis. Experimental and Applied Acarology 22, 249–258.CrossRefGoogle Scholar
Grégoire, A., Faivre, B., Heeb, P. and Cezilly, F. (2002). A comparison of infestation patterns by Ixodes ticks in urban and rural populations of the Common Blackbird Turdus merula. Ibis 144, 640–645.CrossRefGoogle Scholar
Griffiths, R., Daan, S. and Dijkstra, C. (1996). Sex identification in birds using two CHD genes. Proceedings of the Royal Society of Londo, B 263, 1251–1256.Google ScholarPubMed
Harvey, P. H. and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology, Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Hesse, G. H. (1985). Brutverluste von Uferschwalben (Riparia riparia) durch massive parasitierung nestbewohnender Flohe und Zecken. Ornithologische Mitteilungen, Göttingen 37, 31–32.Google Scholar
Heylen, D., Adriaensen, F., Dauwe, T., Eens, M. and Matthysen, E. (2009). Offspring quality and tick infestation load in brood rearing great tits Parus major. Oikos 118, 1499–1506.CrossRefGoogle Scholar
Heylen, D. J. A. and Matthysen, E. (2008). Effect of tick parasitism on the health status of a passerine bird. Functional Ecology 22, 1099–1107.CrossRefGoogle Scholar
Heylen, D. J. A. and Matthysen, E. (2010). Contrasting detachment strategies in two congeneric ticks (Ixodidae) parasitizing the same songbird. Parasitology 137, 661–667.CrossRefGoogle ScholarPubMed
Heylen, D. J. A. and Matthysen, E. (2011). Experimental evidence for host preference in a tick parasitizing songbird nestlings. Oikos (in the Press).CrossRefGoogle Scholar
Hillyard, P. D. (1996). Ticks of North-West Europe, Backhuys Publishers, London, UK.Google Scholar
Hoodless, A. N., Kurtenbach, K., Nuttall, P. A. and Randolph, S. E. (2002). The impact of ticks on pheasant territoriality. Oikos 96, 245–250.CrossRefGoogle Scholar
Hudde, H. and Walter, G. (1988). Verbreitung und Wirtswahl der Vogelzecke Ixodes arboricola (Ixodoidea, Ixodidae) in der Bundesrepublik Deutschland. Vogelwarte 34, 201–207.Google Scholar
Humair, P. F., Turrian, N., Aeschlimann, A. and Gern, L. (1993). Ixodes ricinus immatures on birds in a focus of Lyme Borreliosis. Folia Parasitologica 40, 237–242.Google Scholar
Jongejan, F. and Uilenberg, G. (2004). The global importance of ticks. Parasitology 129, S3–S14.CrossRefGoogle ScholarPubMed
Jonsson, N. N., Mayer, D. G., Matschoss, A. L., Green, P. E. and Ansell, J. (1998). Production effects of cattle tick (Boophilus microplus) infestation of high yielding dairy cows. Veterinary Parasitology 78, 65–77.CrossRefGoogle ScholarPubMed
Kahl, O. and Knülle, W. (1988). Water vapour uptake from subsaturated atmosphere by engorged immature ixodid ticks. Experimental and Applied Acarology 4, 73–83.CrossRefGoogle ScholarPubMed
Kaiser, A., Seitz, A. and Strub, O. (2002). Prevalence of Borrelia burgdorferi sensu lato in the Nightingale (Luscinia megarhynchos) and other passerine birds. International Journal of Medical Microbiology 291, 75–79.CrossRefGoogle ScholarPubMed
Kaufman, J. (1996). Parasitic Infections of Domestic Animals: a Diagnostic Manual, Birkhäuser Verlag, Basel, Switzerland.CrossRefGoogle Scholar
King, K. A., Keith, J. O., Mitchell, C. A. and Keirans, J. E. (1977). Ticks as a factor in nest desertions of California brown pelicans. Condor 79, 507–509.CrossRefGoogle Scholar
Kirby, A. D., Smith, A. A., Benton, T. G. and Hudson, P. J. (2004). Rising burden of immature sheep ticks (Ixodes ricinus) on red grouse (Lagopus lagopus scoticus) chicks in the Scottish uplands. Medical and Veterinary Entomology 18, 67–70.CrossRefGoogle ScholarPubMed
Klompen, J. S. H., Black, W. C., Keirans, J. E. and Oliver, J. H. (1996). Evolution of ticks. Annual Review of Entomology 41, 141–161.CrossRefGoogle ScholarPubMed
Knülle, W. and Rudolph, D. (1982). Humidity relationships and water balance of ticks. In Physiology of Ticks, Vol. 1 (ed. Obenchain, F. D. and Galun, R.), pp. 43–70. Pergamon Press Ltd, Oxford, UK.CrossRefGoogle Scholar
Latshaw, J. D. (1991). Nutrition – mechanisms of immunosuppression. Veterinary Immunology and Immunopathology 30, 111–120.CrossRefGoogle ScholarPubMed
Lee, E. W., Wei, L. J. and Amato, D. A. (1992). Cox-type regression analysis for large numbers of small groups of correlated failure time observations. In Survival Analysis: State of the Art (ed. Klein, J. P. and Goel, P. K.), pp. 237–247. Kluwer, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Lees, A. D. (1948). The sensory physiology of the sheep tick, Ixodes ricinus L. Journal of Experimental Biology 25, 145–207.CrossRefGoogle Scholar
Lehmann, T. (1993). Ectoparasites: direct impact on host fitness. Parasitology Today 9, 8–13.CrossRefGoogle ScholarPubMed
Lichard, M. and Kozuch, O. (1967). Persistence of tick-borne encephalitis virus in nymphs and adults of Ixodes arboricola and its transmission to White Mice. Acta Virologica 11, 480.Google ScholarPubMed
Luttrell, M. P., Creekmore, L. H. and Mertins, J. W. (1996). Avian tick paralysis caused by Ixodes brunneus in the southeastern United States. Journal of Wildlife Diseases 32, 133–136.CrossRefGoogle ScholarPubMed
Maley, G. J. M. and Desser, S. S. (1977). Anemia in Leucocytozoon simondi infections .1. Quantification of anemia, gametocytemia, and osmotic fragility of erythrocytes in naturally infected pekin ducklings. Canadian Journal of Zoology-Revue Canadienne De Zoologie 55, 355–358.CrossRefGoogle Scholar
Mangin, S., Gauthier-Clerc, M., Frenot, Y., Gendner, J. P. and Le Maho, Y. (2003). Ticks Ixodes uriae and the breeding performance of a colonial seabird, king penguin Aptenodytes patagonicus. Journal of Avian Biology 34, 30–34.CrossRefGoogle Scholar
Matthysen, E., Adriaensen, F. and Dhondt, A. A. (2001). Local recruitment of great and blue tits (Parus major, P. caeruleus) in relation to study plot size and degree of isolation. Ecography 24, 33–42.CrossRefGoogle Scholar
McKilligan, N. G. (1996). Field experiments on the effect of ticks on breeding success and chick health of cattle egrets. Australian Journal of Ecology 21, 442–449.CrossRefGoogle Scholar
Mejlon, H. A. and Jaenson, T. G. T. (1997). Questing behaviour of Ixodes ricinus (Acari: Ixodidae). Experimental and applied acarology 21, 247–255.CrossRefGoogle Scholar
Merino, S. and Potti, J. (1998). Growth, nutrition, and blow fly parasitism in nestling Pied Flycatchers. Canadian Journal of Zoology-Revue Canadienne De Zoologie 76, 936–941.CrossRefGoogle Scholar
Møller, A. P., Arriero, E., Lobato, E. and Merino, S. (2009). A meta-analysis of parasite virulence in nestling birds. Biological Reviews 84, 567–588.CrossRefGoogle ScholarPubMed
Monks, D., Fisher, M. and Forbes, N. A. (2006). Ixodes frontalis and avian tick-related syndrome in the United Kingdom. Journal of Small Animal Practice 47, 451–455.CrossRefGoogle ScholarPubMed
O'Kelly, J. C. and Seifert, G. W. (1970). Effects of tick (Boophilus microplus) infestations on blood composition of shorthorn by Hereford cattle on high and low planes of nutrition. Australian Journal of Biological Sciences 23, 681–690.CrossRefGoogle Scholar
Olsen, B., Gylfe, A. and Bergstrom, S. (1996). Canary finches (Serinus canaria) as an avian infection model for Lyme borreliosis. Microbial Pathogenesis 20, 319–324.CrossRefGoogle ScholarPubMed
Olsen, B., Jaenson, T. G. T. and Bergström, S. (1995). Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Applied and Environmental Microbiology 61, 3082–3087.CrossRefGoogle ScholarPubMed
Ots, I., Murumagi, A. and Hõrak, P. (1998). Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation. Functional Ecology 12, 700–707.CrossRefGoogle Scholar
Pappas, P. J. and Oliver, J. H. (1972). Reproduction in Ticks (Acari-Ixodoidea) .2. Analysis of stimulus for rapid and complete feeding of female Dermacentor variabilis (Say). Journal of Medical Entomology 9, 47–50.CrossRefGoogle ScholarPubMed
Pfäffle, M., Petney, T., Elgas, M., Skuballa, J. and Taraschewski, H. (2009). Tick-induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus). Parasitology 136, 443–452.CrossRefGoogle ScholarPubMed
Piersma, T., Koolhaas, A., Dekinga, A. and Gwinner, E. (2000). Red blood cell and white blood cell counts in sandpipers (Philomachus pugnax, Calidris canutus): effects of captivity, season, nutritional status, and frequent bleedings. Canadian Journal of Zoology-Revue Canadienne De Zoologie 78, 1349–1355.CrossRefGoogle Scholar
Potti, J., Moreno, J., Merino, S., Frias, O. and Rodriguez, R. (1999). Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120, 1–8.CrossRefGoogle ScholarPubMed
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Rechav, Y., Goldberg, M. and Fielden, L. J. (1997). Evidence for attachment pheromones in the Cayenne tick (Acari: Ixodidae). Journal of Medical Entomology 34, 234–237.CrossRefGoogle ScholarPubMed
Regoes, R. R., Nowak, M. A. and Bonhoeffer, S. (2000). Evolution of virulence in a heterogeneous host population. Evolution 54, 64–71.Google Scholar
Richner, H., Oppliger, A. and Christe, P. (1993). Effect of an ectoparasite on reproduction in Great Tits. Journal of Animal Ecology 62, 703–710.CrossRefGoogle Scholar
Saino, N., Calza, S. and Möller, A. P. (1998). Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81, 217–228.CrossRefGoogle Scholar
Seebeck, R. M., Springel, P. H. and O'Kelly, J. C. (1971). Alterations in host metabolism by specific and anorectic effects of cattle tick (Boophilus microplus) .1. Food Intake and body weight growth. Australian Journal of Biological Sciences 24, 373–380.CrossRefGoogle Scholar
Sonenshine, D. E. (1991). Biology of Ticks. Oxford University Press, New York, USA.Google Scholar
Sonenshine, D. E. (2004). Pheromones and other semiochemicals of ticks and their use in tick control. Parasitology 129, S405–S425.CrossRefGoogle ScholarPubMed
Szép, T. and Møller, A. P. (1999). Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-offspring conflict? Oecologia 119, 9–15.Google Scholar
Szép, T. and Møller, A. P. (2000). Exposure to ectoparasites increases within-brood variability in size and body mass in the sand martin. Oecologia 125, 201–207.CrossRefGoogle ScholarPubMed
Thorud, C. (1999). Experimentelle Infektion der Vogelzecke Ixodes (Pholeoixodes) arboricola mit Borrelia burgdorferi sensu lato. Institute for Parasitology, Hannover, Germany.Google Scholar
Toivanen, P. and Toivanen, A. (1987). Avian Immunology, CRC Press, Boca Raton, FL, USA.Google Scholar
Tompkins, D. M., Jones, T. and Clayton, D. H. (1996). Effect of vertically transmitted ectoparasites on the reproductive success of Swifts (Apus apus). Functional Ecology 10, 733–740.CrossRefGoogle Scholar
Toutoungi, L. N., Gern, L. and Aeschlimann, A. (1993). Biology of Ixodes (Pholeoixodes) hexagonus under laboratory conditions. 1. Immature stages. Experimental and Applied Acarology 17, 655–662.CrossRefGoogle Scholar
Toutoungi, L. N., Gern, L. and Aeschlimann, A. (1995). Biology of Ixodes (Pholeoixodes) hexagonus under laboratory conditions. 2. Effect of mating on feeding and fecundity of females. Experimental and Applied Acarology 19, 233–245.CrossRefGoogle ScholarPubMed
Tripet, F. and Richner, H. (1997). Host responses to ectoparasites: food compensation by parent blue tits. Oikos 78, 557–561.CrossRefGoogle Scholar
Verbeke, G. and Molenberghs, G. (2001). Linear Mixed Models for Longitudinal Data. Springer-Verlag, Berlin-Heidelberg-New York, USA.Google Scholar
Wanless, S., Barton, T. R. and Harris, M. P. (1997). Blood hematocrit measurements of 4 species of North Atlantic seabirds in relation to levels of infestation by the tick Ixodes uriae. Colonial Waterbirds 20, 540–544.CrossRefGoogle Scholar
Weiss, B. L. and Kaufman, W. R. (2004). Two feeding-induced proteins from the male gonad trigger engorgement of the female tick Amblyomma hebraeum. Proceedings of the National Academy of Sciences, USA 101, 5874–5879.CrossRefGoogle ScholarPubMed