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Blood parasitaemia in a high latitude flexible breeder, the white-winged crossbill, Loxia leucoptera: contribution of seasonal relapse versus new inoculations

Published online by Cambridge University Press:  23 October 2009

P. DEVICHE ,
H. B. FOKIDIS ,
B. LERBOUR  and
E. GREINER
P. DEVICHE*
Affiliation:
School of Life Sciences, Arizona State University, Tempe, AZ 87287-4501, USA
H. B. FOKIDIS
Affiliation:
School of Life Sciences, Arizona State University, Tempe, AZ 87287-4501, USA
B. LERBOUR
Affiliation:
Université de Poitiers, U.F.R. Sciences Fondamentales et Appliquées, 86022Poitiers Cedex, France
E. GREINER
Affiliation:
Department of Infectious Diseases and Pathology, College of Veterinary Medicine, University of Florida, Gainesville, FL 32611, USA
*
*Corresponding author: School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA. Tel: +480 965 0726. Fax: +480 965 6899. E-mail: deviche@asu.edu
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Summary

We measured seasonal changes in the prevalence of haematozoa (Leucocytozoon fringillinarum, Haemoproteus fringillae, and Trypanosoma avium) in free-ranging White-winged Crossbills, Loxia leucoptera, over 1·5 year in Fairbanks, Alaska, USA. This prevalence was low during early winter. L. fringillinarum prevalence increased in late winter/early spring, in the absence of vectors, suggesting relapse of latent infection. By contrast, the prevalence of T. avium and H. fringillae did not increase until mid-spring, coincident with the emergence of putative vectors and suggestive of new inoculations. The winter breeding period was not associated with lower body condition or elevated blood heterophil/lymphocyte ratios than the summer post-breeding period. Thus, birds unlikely perceived their breeding effort as particularly stressful. Adult males in May and June had low plasma testosterone and their blood prevalence of L. fringillinarum, but not other haemoparasites, was higher than in adult females. This difference may have resulted from sex differences in behaviour and/or plumage colouration – bright red in males, dull green/yellow in females. Species in which reproduction and vector abundance are seasonally dissociated may constitute important models for investigating the respective contribution of reproductive hormones, breeding effort, and vector abundance to patent and latent hemoparasitic infections and to new inoculations.

Keywords

LeucocytozoonTrypanosomaHaemoproteustestosteronereproductionsex differencesexual dimorphism
Type
Research Article
Information
Parasitology , Volume 137 , Issue 2 , February 2010 , pp. 261 - 273
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Ahmed, F. E. and Mohammed, A. H. (1978). Haemoproteus columbae: course of infection, relapse and immunity to reinfection in the pigeon. Zeitschrift für Parasitenkunde 57, 229–236.CrossRefGoogle ScholarPubMed
Al-Mohammed, H. I. (2006). Parasitological and immunological studies on rats experimentally infected with Saudi Arabian strain of Trypanosoma evansi. Journal of the Egyptian Society of Parasitology 36, 363–371.Google ScholarPubMed
Allander, K. (1997). Reproductive investment and parasite susceptibility in the Great Tit. Functional Ecology 11, 358–364.Google Scholar
Arriero, E., Moreno, J., Merino, S. and Martinez, J. (2008). Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism. Physiological and Biochemical Zoology 81, 195–203.CrossRefGoogle ScholarPubMed
Benkman, C. W. (1992). White-winged Crossbill. In The Birds of North America (ed. Poole, A. and Gill, F.),No. 27, pp. 1–18. Academy of Natural Sciences, Philadelphia and American Ornithologists' Union, Washington, DC, USA.Google Scholar
Bennett, G. F. (1970). Simple technique for making avian blood smears. Canadian Journal of Zoology 48, 585–586.CrossRefGoogle Scholar
Bennett, G. F., Thommes, F., Blancou, J. and Artois, M. (1982). Blood parasites of some birds from the Lorraine region, France. Journal of Wildlife Diseases 18, 81–88.CrossRefGoogle ScholarPubMed
Bensch, S., Waldenstrom, J., Jonzen, N., Westerdahl, H., Hansson, B., Sejberg, D. and Hasselquist, D. (2007). Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 76, 112–122.CrossRefGoogle Scholar
Bent, A. C. (1968). Life histories of North American birds. Smithsonian Institution United States National Museum Bulletin 237 (Part 1): 527–544. United States Government Printing Office.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, 575–583.Google Scholar
Cernetich, A., Garver, L. S., Jedlicka, A. E., Klein, P. W., Kumar, N., Scott, A. L. and Klein, S. L. (2006). Involvement of gonadal steroids and gamma interferon in sex differences in response to blood-stage malaria infection. Infection and Immunity 74, 3190–3203.CrossRefGoogle ScholarPubMed
Conover, W. J. and Iman, R. L. (1981). Rank-transformations as a bridge between parametric and nonparametric statistics. American Statistician 35, 124–129.CrossRefGoogle Scholar
Cosgrove, C. L., Wood, M. J., Day, K. P. and Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology 77, 540–548.CrossRefGoogle Scholar
Costantini, D., Casagrande, S. and Dell'omo, G. (2007). MF magnitude does not affect body condition, pro-oxidants and anti-oxidants in Eurasian kestrel (Falco tinnunculus) nestlings. Environmental Research 104, 361–366.CrossRefGoogle Scholar
Day, L. B., McBroom, J. T. and Schlinger, B. A. (2006). Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus). Hormones and Behavior 49, 223–232.CrossRefGoogle Scholar
de Souza, E. M., Rivera, M. T., raujo-Jorge, T. C. and de Castro, S. L. (2001). Modulation induced by estradiol in the acute phase of Trypanosoma cruzi infection in mice. Parasitology Research 87, 513–520.Google Scholar
Deviche, P. (2000). Timing, pattern, and extent of first prebasic molt of White-winged Crossbills in Alaska. Journal of Field Ornithology 71, 217–226.CrossRefGoogle Scholar
Deviche, P. and Cortez, L. (2005). Androgen control of immunocompetence in the male house finch, Carpodacus mexicanus Muller. Journal of Experimental Biology 208, 1287–1295.CrossRefGoogle ScholarPubMed
Deviche, P., Greiner, E. C. and Manteca, X. (2001). Seasonal and age-related changes in blood parasite prevalence in Dark-eyed Juncos (Junco hyemalis, Aves, Passeriformes). Journal of Experimental Zoology 289, 456–466.CrossRefGoogle ScholarPubMed
Deviche, P. and Gulledge, C. C. (2000). Vocal control region sizes of an adult female songbird change seasonally in the absence of detectable circulating testosterone concentrations. Journal of Neurobiology 42, 202–211.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Deviche, P., McGraw, K. and Greiner, E. C. (2005). Interspecific differences in hematozoan infection in Sonoran desert Aimophila sparrows. Journal of Wildlife Diseases 41, 532–541.CrossRefGoogle ScholarPubMed
Deviche, P., Parris, J. and Greiner, E. C. (2006). Testosterone treatment to free-living Dark-eyed Juncos, Junco hyemalis, exacerbates hemoparasitic infection. Auk 123, 548–562.CrossRefGoogle Scholar
Deviche, P. and Sharp, P. J. (2001). Reproductive endocrinology of a free-living, opportunistically breeding passerine (white-winged crossbill, Loxia leucoptera). General and Comparative Endocrinology 123, 268–279.Google Scholar
Dick, J. W. (1978). Leucocytozoon smithi: persistence of gametocytes in peripheral turkey blood. Avian Diseases 22, 82–85.Google Scholar
Do Prado, J. C. Jr., Leal, M. P., Anselmo-Franci, J. A., de Andrade, H. F. and Kloetzel, J. K. (1998). Influence of female gonadal hormones on the parasitemia of female Calomys callosus infected with the “Y” strain of Trypanosoma cruzi. Parasitology Research 84, 100–105.CrossRefGoogle Scholar
Do Prado, P. J. Jr., Levy, A. M., Leal, M. P., Bernard, E. and Kloetzel, J. K. (1999). Influence of male gonadal hormones on the parasitemia and humoral response of male Calomys callosus infected with the Y strain of Trypanosoma cruzi. Parasitology Research 85, 826–829.CrossRefGoogle Scholar
Earle, R. A., Horak, I. G., Huchzermeyer, F. W., Bennett, G. F., Braack, L. E. and Penzhorn, B. L. (1991). The prevalence of blood parasites in helmeted guineafowls, Numida meleagris, in the Kruger National Park. Onderstepoort. Journal of Veterinary Research 58, 145–147.Google Scholar
Fallis, A. M., Desser, S. S. and Khan, R. A. (1974). On species of Leucocytozoon. Advances in Parasitology 12, 1–67.CrossRefGoogle ScholarPubMed
Fokidis, B. H., Greiner, E. C and Deviche, P. (2008). Interspecific variation in avian blood parasites and haematology associated with urbanization in a desert habitat. Journal of Avian Biology 39, 300–310.CrossRefGoogle Scholar
Garvin, M. and Remsen, J. V. Jr. (1997). An alternative hypothesis for heavier parasite loads of brightly colored birds: Exposure at the nest. Auk 114, 179–191.Google Scholar
Garvin, M. C. and Greiner, E. C. (2003). Epizootiology of Haemoproteus danilewskyi (Haemosporina: Haemoproteidae) in blue jays (Cyanocitta cristata) in southcentral Florida. Journal of Wildlife Diseases 39, 1–9.Google Scholar
Garvin, M. C. and Schoech, S. J. (2006). Hormone levels and infection of Haemoproteus danilewskyi in free-ranging blue jays (Cyanocitta cristata). Journal of Parasitology 92, 659–662.CrossRefGoogle ScholarPubMed
Godfrey, R. D., Pence, D. B. and Fedynich, A. M. (1990). Effects of host and spatial factors on a haemoproteid community in Mourning Doves from Western Texas. Journal of Wildlife Diseases 26, 435–441.CrossRefGoogle ScholarPubMed
Greiner, E. C., Bennett, G. F., White, E. M. and Coombs, R. F. (1975). Distribution of the avian haematozoa of North America. Canadian Journal of Zoology 53, 1762–1787.CrossRefGoogle Scholar
Gross, W. B. (1988). Effect of environmental stress on the responses of ascorbic-acid-treated chickens to Escherichia coli challenge infection. Avian Diseases 32, 432–436.CrossRefGoogle ScholarPubMed
Gross, W. B. and Siegel, H. S. (1983). Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Diseases 27, 972–979.Google Scholar
Gustafsson, L., Nordling, D., Andersson, M. S., Sheldon, B. C. and Qvarnström, A. (1994). Infectious diseases, reproductive effort and the cost of reproduction in birds. Philosophical Transactions of the Royal Society of London, B 346, 323–331.Google Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Harder, A., Wunderlich, F. and Marinovski, P. (1992). Effects of testosterone on Heterakis spumosa infections in mice. Parasitology 105, 335–342.CrossRefGoogle ScholarPubMed
Hartup, B. K., Oberc, A., Stott-Messick, B., Davis, A. K. and Swarthout, E. C. (2008). Blood parasites of House Finches (Carpodacus mexicanus) from Georgia and New York. Journal of Wildlife Diseases 44, 469–474.Google Scholar
Hellgren, O., Bensch, S. and Malmqvist, B. (2008). Bird hosts, blood parasites and their vectors–associations uncovered by molecular analyses of blackfly blood meals. Molecular Ecology 17, 1605–1613.Google Scholar
Ilmonen, P., Hasselquist, D., Langefors, A. and Wiehn, J. (2003). Stress, immunocompetence and leucocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136, 148–154.Google Scholar
Ketterson, E. D., Nolan, V. Jr. and Sandell, M. (2005). Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both? American Naturalist 166, (Suppl. 4), S85–S98.CrossRefGoogle ScholarPubMed
Kiyota, M., Korenaga, M., Nawa, Y. and Kotani, M. (1984). Effect of androgen on the expression of the sex difference in susceptibility to infection with Strongyloides ratti in C57BL/6 mice. Australian Journal of Experimental Biology and Medicine 62, 607–618.CrossRefGoogle ScholarPubMed
Klei, T. R. and DeGiusti, D. L. (1975). Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. Journal of Wildlife Diseases 11, 130–135.Google Scholar
Kocan, R. M. and Clark, D. T. (1966). Prepatent period and parasitemia in Leucocytozoon simondi infections resulting from short exposures to sporozoites. Journal of Parasitology 52, 962–966.CrossRefGoogle Scholar
Levine, N. D. (1985). Vertebrate Protozoology. Iowa State University, Ames, IA, USA.Google Scholar
Merilä, J., Bjorkund, M. and Bennett, G. F. (1995). Geographic and individual variation in hematozoan infections in the greenfinch, Carduelis chloris. Canadian Journal of Zoology 73, 1798–1804.CrossRefGoogle Scholar
Mullens, B. A., Cardona, C. J., McClellan, L., Szijj, C. E. and Owen, J. P. (2006). Culicoides bottimeri as a vector of Haemoproteus lophortyx to quail in California, USA. Veterinary Parasitology 140, 35–43.Google Scholar
Murata, K., Tamada, A., Ichikawa, Y., Hagihara, M., Sato, Y., Nakamura, H., Nakamura, M., Sakanakura, T. and Asakawa, M. (2007). Geographical distribution and seasonality of the prevalence of Leucocytozoon lovati in Japanese rock ptarmigans (Lagopus mutus japonicus) found in the alpine regions of Japan. Journal of Veterinary Medicine Science 69, 171–176.Google Scholar
Newton, I. (1972). Finches. Collins, London, UK.Google Scholar
Noblet, R., Adkins, T. R. and Kissam, J. B. (1972). Simulium congareenarum (Diptera: Simuliidae), a new vector of Leucocytozoon smithi (Sporozoa: Leucocytozoidae) in domestic turkeys. Journal of Medical Entomology 9, 580.CrossRefGoogle Scholar
Norris, K., Anwar, M. and Read, A. F. (1994). Reproductive effort influences the prevalence of haematozoan parasites in great tits. Journal of Animal Ecology 63, 601–610.Google Scholar
Ochs, C. L. and Dawson, R. D. (2008). Patterns of variation in leucocyte counts of female tree swallows, Tachycineta bicolor: repeatability over time and relationships with condition and costs of reproduction. Comparative Biochemistry and Physiology. A. Molecular and Integrative Physiology 150, 326–331.Google Scholar
Ots, I. and Hõrak, P. (1996). Great Tits Parus major trade health for reproduction. Proceedings of the Royal Society of London, B 263, 1443–1447.Google Scholar
Pawelczyk, A., Gryczynska, A. and Mazgajski, T. D. (2003). Parasites of chaffinch (Fringilla coelebs) population. Part II. Blood parasites. Wiad Parazytologia 49, 31–38.Google Scholar
Peirce, M. A. and Baker, J. R. (1976). Biology of the trypanosomes of birds. In Biology of the Kinetoplastida (ed. Lumsden, W. H. R. and Evans, D. A.), Vol. 3, pp. 131–174. Academic Press, London, UK.Google Scholar
Pyle, P. (1997). Identification Guide to North American Birds. Part I. Columbidae to Ploceidae. Slate Creek Press, Bolinas, CA, USA.Google Scholar
Rintamaki, P. T., Huhta, E., Jokimaki, J. and Squires-Parsons, D. (1999). Leucocytozoonosis and trypanosomiasis in redstarts in Finland. Journal of Wildlife Diseases 35, 603–607.Google Scholar
Scheuerlein, A. and Ricklefs, R. E. (2004). Prevalence of blood parasites in European passeriform birds. Proceedings of the Royal Society of London, B 271, 1363–1370.Google Scholar
Schrader, M. S., Walters, E. L., James, F. C. and Greiner, E. (2003). Seasonal prevalence of a haematozoan parasite of Red-bellied Woodpeckers (Melanerpes carolinus) and its association with host condition and overwinter survival. Auk 120, 130–137.Google Scholar
Schuster, J. P. and Schaub, G. A. (2001). Experimental Chagas disease: the influence of sex and psychoneuroimmunological factors. Parasitology Research 87, 994–1000.Google Scholar
Seutin, G. (1994). Plumage redness in redpoll finches does not reflect hemoparasitic infection. Oikos 70, 280–286.Google Scholar
Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York, USA.Google Scholar
Spinney, L. H., Bentley, G. E. and Hau, M. (2006). Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis). Hormones and Behavior 50, 762–771.Google Scholar
Steele, E. J. and Noblet, G. P. (2001). Gametogenesis, fertilization and ookinete differentiation of Leucocytozoon smithi. Journal of Eukaryotic Microbiology 48, 118–125.Google Scholar
Strand, C. R., Ross, M. S., Weiss, S. L. and Deviche, P. (2008). Testosterone and social context affect singing behavior but not song control region volumes in adult male songbirds in the fall. Behavioural Processes 78, 29–37.CrossRefGoogle Scholar
Super, P. E. and van Riper, C. III (1995). A comparison of avian hematozoan epizootiology in two California coastal scrub communities. Journal of Wildlife Diseases 31, 447–461.Google Scholar
Valkiunas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiunas, G. and Iezhova, T. A. (2004). Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 194–196.CrossRefGoogle ScholarPubMed
Valkiunas, G., Bairlein, F., Iezhova, T. A. and Dolnik, O. V. (2004). Factors affecting the relapse of Haemoproteus belopolskyi infections and the parasitaemia of Trypanosoma spp. in a naturally infected European songbird, the blackcap, Sylvia atricapilla. Parasitology Research 93, 218–222.CrossRefGoogle Scholar
Van Duyse, E., Pinxten, R. and Eens, M. (2002). Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major. Hormones and Behavior 41, 178–186.Google Scholar
Votypka, J. and Svobodova, M. (2004). Trypanosoma avium: experimental transmission from black flies to canaries. Parasitology Research 92, 147–151.Google Scholar
Weatherhead, P. J. and Bennett, G. F. (1991). Ecology of Red-winged Blackbird parasitism by haematozoa. Canadian Journal of Zoology 69, 2352–2359.CrossRefGoogle Scholar
Weatherhead, P. J. and Bennett, G. F. (1992). Ecology of parasitism of Brown-headed Cowbirds by haematozoa. Canadian Journal of Zoology 70, 1–7.Google Scholar
Werner, S. (1992). Life Cycle of Mosquitoes in Alaska. Fairbanks Daily News-Miner, Fairbanks, Alaska, D-4, USA.Google Scholar
Wood, M. J., Cosgrove, C. L., Wilkin, T. A., Knowles, S. C., Day, K. P. and Sheldon, B. C. (2007). Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology 16, 3263–3273.Google Scholar
Yu, C. Y., Wang, J. S. and Yeh, C. C. (2000). Culicoides arakawae (Diptera: Ceratopogonidae) population succession in relation to leucocytozoonosis prevalence on a chicken farm in Taiwan. Veterinary Parasitology 93, 113–120.Google Scholar
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1023.Google Scholar