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Haemoproteus infected birds have increased lifetime reproductive success

Published online by Cambridge University Press:  24 March 2015

M. ZYLBERBERG ,
E. P. DERRYBERRY ,
C. W. BREUNER ,
E. A. MACDOUGALL-SHACKLETON ,
J. M. CORNELIUS  and
T. P. HAHN
M. ZYLBERBERG*
Affiliation:
University of California, San Francisco, 1700 4th St, San Francisco, California 94158, USA University of California, Davis, One Shields Avenue, Davis, California 95616, USA
E. P. DERRYBERRY
Affiliation:
Tulane University, 6823 St Charles Ave, New Orleans, Louisiana 70118, USA
C. W. BREUNER
Affiliation:
University of Montana, 32 Campus Dr, Missoula, Montana 59812, USA
E. A. MACDOUGALL-SHACKLETON
Affiliation:
University of Western Ontario, 1151 Richmond St, London, ON N6A 3K7, Canada
J. M. CORNELIUS
Affiliation:
University of California, Davis, One Shields Avenue, Davis, California 95616, USA Eastern Michigan University, 900 Oakwood St, Ypsilanti, Michigan 48198, USA
T. P. HAHN
Affiliation:
University of California, Davis, One Shields Avenue, Davis, California 95616, USA
*
*Corresponding author. University of California, San Francisco, Byers Hall, MC2542, 1700 4th St., Room 403, San Francisco, California 94158, USA. E-mail: MaxineZylberberg@gmail.com
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Summary

The impact of haematozoan infection on host fitness has received substantial attention since Hamilton and Zuk posited that parasites are important drivers of sexual selection. However, short-term studies testing the assumption that these parasites consistently reduce host fitness in the wild have produced contradictory results. To address this complex issue, we conducted a long-term study examining the relationship between naturally occurring infection with Haemoproteus and Plasmodium, and lifetime reproductive success and survival of Mountain White-crowned Sparrows. Specifically, we tested the hypothesis that birds infected with haematozoan parasites have reduced survival (as determined by overwinter return rates) and reproductive success. Contrary to expectation, there was no relationship between Haemoproteus and Plasmodium infection and reproduction or survival in males, nor was there a relationship between Plasmodium infection and reproduction in females. Interestingly, Haemoproteus-infected females had significantly higher overwinter return rates and these females fledged more than twice as many chicks during their lifetimes as did uninfected females. We discuss the impact of parasitic infections on host fitness in light of these findings and suggest that, in the case of less virulent pathogens, investment in excessive immune defence may decrease lifetime reproduction.

Keywords

HaemoproteusPlasmodiumhaematozoaavian malariahost fitnessMountain White-crowned SparrowZonotrichia leucophrys orianthahost-parasite interactionsparasite tolerance
Type
Research Article
Information
Parasitology , Volume 142 , Issue 8 , July 2015 , pp. 1033 - 1043
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Copyright
Copyright © Cambridge University Press 2015 

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References

REFERENCES

Allander, K. and Bennett, G. F. (1995). Retardation of breeding onset in great tits (Parus major) by blood parasites. Functional Ecology 9, 677–682.CrossRefGoogle Scholar
Anderson, R. M. and May, R. M. (1982). Coevolution of hosts and parasites. Parasitology 85, 411–426.CrossRefGoogle ScholarPubMed
Apanius, V. (1993). Blood parasitism, immunity and reproduction in American Kestrels (Falco sparverius). In Biology and Conservation of Small Falcons: Proceedings of the Hawk and Owl Trust Conference (ed. Nicholls, M. K. and Clarke, R.), pp. 117–125. Hawk and Owl Trust, London.Google Scholar
Apanius, V., Deerenberg, C., Visser, H. and Daan, S. (1994). Reproductive effort and parasite resistance: evidence for an energetically based trade-off. Journal für Ornithologie 135, 404–404.Google Scholar
Ashford, R. W. (1971). Blood parasites and migratory fat at Lake Chad. Ibis 113, 100–101.CrossRefGoogle Scholar
Atkinson, C. T. and van Riper, C. III (1991). Pathogenicity and epizootiology of avian hematozoa: Plasmodium, Leucocytozoon and Haemoproteus. In Bird–Parasite Interactions: Ecology, Evolution, and Behavior (ed. Loye, J. and Zuk, M.), pp. 19–48. Oxford University Press, New York.CrossRefGoogle Scholar
Ayres, J. S. and Schneider, D. S. (2012). Tolerance of infections. Annual Review of Immunology 30, 271–294.CrossRefGoogle ScholarPubMed
Behnke, J. M., Barnard, C. J. and Wakelin, D. (1992). Understanding chronic nematode infections: Evolutionary considerations, current hypotheses, and the way forward. International Journal of Parasitology 22, 861–907.CrossRefGoogle ScholarPubMed
Bennett, G., Caines, J. and Bishop, M. (1988). Influence of blood parasites on the body mass of passeriform birds. Journal of Wildlife Diseases 24, 339–343.CrossRefGoogle ScholarPubMed
Bennett, G. F., Peirce, M. A. and Ashford, R. W. (1993). Avian Haematozoa: mortality and pathogenicity. Journal of Natural History 27, 993–1001.CrossRefGoogle Scholar
Campbell, T. W. (1995). Avian Hematology and Cytology, 2nd Edn. Iowa State University Press, Ames.Google Scholar
Chastel, O., Weimerskirch, H. and Jouventin, P. (1995). Influence of body condition on reproductive decision and reproductive success in the blue petrel. The Auk 112, 964–972.CrossRefGoogle Scholar
Cornelius, J., Zylberberg, M., Breuner, C., Gleiss, A. C. and Hahn, T. (2014). Assessing the role of reproduction and stress in the spring emergence of Haematozoan parasites in birds. The Journal of Experimental Biology 217, 841–849.Google ScholarPubMed
Davidar, P. and Morton, E. S. (1993). Living with parasites: prevalence of a blood parasite and its effect on survivorship in the purple martin. The Auk 110, 109–116.Google Scholar
Dawson, R. D. and Bortolotti, G. R. (2000). Effects of hematozoan parasites on condition and return rates of American Kestrels. The Auk 117, 373–380.CrossRefGoogle Scholar
Fargallo, J. A. and Merino, S. (2004). Clutch size and haemoparasite species richness in adult and nestling blue tits. Ecoscience 11, 168–174.CrossRefGoogle Scholar
Festa-Bianchet, M. (1989). Individual differences, parasites, and the costs of reproduction for Bighorn Ewes (Ovis canadensis). Journal of Animal Ecology 58, 785–795.CrossRefGoogle Scholar
Forrester, D. J. and Spalding, M. G. (2003). Parasites and Diseases of Wild Birds in Florida, University Press of Florida, Gainesville, Florida.Google Scholar
Garvin, M. C., Szell, C. C. and Moore, F. R. (2006). Blood parasites of Nearctic–Neotropical migrant passerine birds during spring trans-gulf migration: impact on host body condition. Journal of Parasitology 92, 990–996.CrossRefGoogle ScholarPubMed
Grenfell, B. T. and Dobson, A. (eds.) (1995). Ecology of Infectious Diseases in Natural Populations, Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Groote, L. W. d. and Rodewald, P. G. (2010). Blood parasites in migrating wood-warblers (Parulidae): effects on refueling, energetic condition, and migration timing. Journal of Avian Biology 41, 147–153.Google Scholar
Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282–290.CrossRefGoogle Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science, 218, 384–387.CrossRefGoogle Scholar
Hurd, H. (2001). Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363–368.CrossRefGoogle ScholarPubMed
Johnson, L. L. and Boyce, M. S. (1991). Female choice of males with low parasite loads in sage grouse. In Bird–Parasite Interactions: Ecology, Evolution, and Behaviour (ed. Loye, J. E. and Zuk, M.), pp. 377–388. Oxford University Press, Oxford.CrossRefGoogle Scholar
Kilpatrick, A. M., LaPointe, D. A., Atkinson, C. T., Woodworth, B. L., Lease, J. K., Reiter, M. E. and Gross, K. (2006). Effects of chronic avian malaria (Plasmodium relictum) infection on reproductive success of Hawaii Amakihi (Hemignathus virens). The Auk 123, 764–774.CrossRefGoogle Scholar
Klasing, K. C. (1998). Nutritional modulation of resistance to infectious diseases. Poultry Science 77, 1119–1125.CrossRefGoogle ScholarPubMed
Knowles, S. C. L., Palinauskas, V. and Sheldon, B. C. (2010a). Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. Journal of Evolutionary Biology 23, 557–569.CrossRefGoogle ScholarPubMed
Korpimaki, E., Hakkarainen, H. and Bennett, G. F. (1993). Blood parasites and reproductive success of Tengmalm's owls: detrimental effects on females but not on males? Functional Ecology 7, 420–426.CrossRefGoogle Scholar
Korpimaki, E., Tolonen, P. and Bennet, G. F. (1995). Blood parasites, sexual selection and reproductive success in European kestrels. Ecoscience 2, 335–343.CrossRefGoogle Scholar
Lee, K. P., Cory, J. S., Wilson, K., Raubenheimer, D. and Simpson, S. J. (2006). Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proceedings of the Royal Society B: Biological Sciences 273, 823–829.CrossRefGoogle Scholar
Li, L., Victoria, J. G., Wang, C., Jones, M., Fellers, G. M., Kunz, T. H. and Delwart, E. (2010). Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. Journal of Virology 84, 6955–6965.CrossRefGoogle ScholarPubMed
Love, O. P., Chin, E. H., Wynne-Edwards, K. E. and Williams, T. D. (2005). Stress hormones: a link between maternal condition and sex-biased reproductive investment. American Naturalist 166, 751–766.CrossRefGoogle ScholarPubMed
MacDougall-Shackleton, E. A., Derryberry, E. P. and Hahn, T. P. (2002). Nonlocal male mountain white-crowned sparrows have lower paternity and higher parasite loads than males singing local dialect. Behavioral Ecology 13, 682–689.CrossRefGoogle Scholar
Martin, L. B., Scheuerlein, A. and Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proceedings of the Royal Society Biological Sciences Series, B 270, 153–158.CrossRefGoogle ScholarPubMed
Marzal, A., Lope, F. d., Navarro, C. and Møller, A. P. (2005). Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia Aquatica 142, 541–545.CrossRefGoogle Scholar
Marzal, A., Bensch, S., Reviriego, M., Balbontin, J. and De Lope, F. (2008). Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology 21, 979–987.CrossRefGoogle Scholar
McCurdy, D. G., Shutler, D., Mullie, A. and Forbes, M. R. (1998). Sex-biased parasitism of Avian hosts: relations to blood parasite taxon and mating system. Oikos 82, 303–312.CrossRefGoogle Scholar
Medzhitov, R., Schneider, D. S. and Soares, M. P. (2012). Disease tolerance as a defense strategy. Science 335, 936–941.CrossRefGoogle ScholarPubMed
Merino, S., Moreno, J., Sanz, J. J. and Arriero, E. (2000). Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proceedings of the Royal Society of London, Series B: Biological Sciences 267, 2507–2510.CrossRefGoogle Scholar
Morton, M. L. (1992). Effects of sex and birth date on premigration biology, migration schedules, return rates and natal dispersal in the mountain white-crowned sparrow. The Condor 94, 117–133.CrossRefGoogle Scholar
Norte, A. C., AraÚJo, P. M., Sampaio, H. L., Sousa, J. P. and Ramos, J. A. (2009). Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis 151, 677–688.CrossRefGoogle Scholar
Owen-Ashley, N. and Wingfield, J. (2007). Acute phase responses of passerine birds: characterization and seasonal variation. Journal of Ornithology 148, 583–591.CrossRefGoogle Scholar
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2008). Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology 120, 372–380.CrossRefGoogle ScholarPubMed
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2011). Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology 127, 527–533.CrossRefGoogle ScholarPubMed
Palinauskas, V., Iezhova, T. A., Križanauskienė, A., Markovets, M. Y., Bensch, S., Valkiūnas, G. (2013). Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitology International 62, 358–363.CrossRefGoogle ScholarPubMed
Podmokła, E., Dubiec, A., Drobniak, S. M., Arct, A., Gustafsson, L. and Cichoń, M. (2014). Avian malaria is associated with increased reproductive investment in the blue tit. Journal of Avian Biology 45, 219–224.CrossRefGoogle Scholar
Poulin, R. (1996). Sexual inequalities in Helminth infections: a cost of being a male. The American Naturalist 147, 287–295.CrossRefGoogle Scholar
Poulin, R., Marshall, L. J. and Spencer, H. G. (2000). Genetic variation and prevalence of blood parasites do not correlate among bird species. Journal of Zoology 252, 381–388.CrossRefGoogle Scholar
Pruett-Jones, S. G., Pruett-Jones, M. A. and Jones, H. I. (1990). Parasites and sexual selection in birds of paradise. American Zoologist 30, 287–298.CrossRefGoogle Scholar
Rätti, O., Dufva, R. and Alatalo, R. (1993). Blood parasites and male fitness in the pied flycatcher. Oecologia 96, 410–414.CrossRefGoogle ScholarPubMed
Richner, H., Christe, P. and Oppliger, A. (1995). Paternal investment affects prevalence of malaria. Proceedings of the National Academy of Sciences 92, 1192–1194.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., Fallon, S. M., Latta, S. C., Swanson, B. L. and Birmingham, E. (2005). Migrants and their parasites: a bridge between two worlds. In Birds of Two Worlds: the Ecology and Evolution of Migration (ed. Greenberg, R. and Marra, P. P.), pp. 210–221. Johns Hopkins University Press, Baltimore, Maryland.Google Scholar
Sanz, J. J., Arriero, E. and Moreno, J. (2001). Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers. Oecologia 126, 339–344.CrossRefGoogle ScholarPubMed
Schalk, G. and Forbes, M. R. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67–74.CrossRefGoogle Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Sheridan, L. A. D., Poulin, R., Ward, D. F. and Zuk, M. (2000). Sex differences in parasitic infections among arthropod hosts: is there a male bias? Oikos 88, 327–334.CrossRefGoogle Scholar
Shurulinkov, P., Chakarov, N. and Daskalova, G. (2012). Blood parasites, body condition, and wing length in two subspecies of yellow wagtail (Motacilla flava) during migration. Parasitology Research 110, 2043–2051.CrossRefGoogle ScholarPubMed
Siikamaki, P., Ratti, O., Hovi, M. and Bennett, G. F. (1997). Association between haematozoan infections and reproduction in the Pied Flycatcher. Functional Ecology 11, 176–183.CrossRefGoogle Scholar
Smith, V. W. and Cox, F. E. G. (1972). Blood parasites and the weights of palaearctic migrants in central Nigeria. Ibis 114, 105–106.CrossRefGoogle Scholar
Sorci, G. (2013). Immunity, resistance and tolerance in bird–parasite interactions. Parasite Immunology 35, 350–361.CrossRefGoogle ScholarPubMed
Tieleman, B. I., Dijkstra, T. H., Klasing, K. C., Visser, G. H. and Williams, J. B. (2008). Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behavioral Ecology 19, 949–959.CrossRefGoogle Scholar
Tuomi, J., Hakala, T. and Haukioja, E. (1983). Alternative concepts of reproductive effort, costs of reproduction, and selection in life-history evolution. American Zoologist 23, 25–34.CrossRefGoogle Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and Other HAEMOSPORIDIA, CRC Press, Boca Raton, Florida.Google Scholar
Valkiūnas, G., Bensch, S., Iezhova, T. A., Križanauskienė, A., Hellgren, O. and Bolshakov, C. V. (2006). Nested Cytochrome B polymerase chain reaction diagnostics underestimate mixed infections of avian blood Haemosporidian parasites: microscopy is still essential. Journal of Parasitology 92, 418–422.CrossRefGoogle ScholarPubMed
Van Riper, C. III , Van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian USA land birds. Ecological Monographs 56, 327–344.CrossRefGoogle Scholar
Waldenström, J., Bensch, S., Kiboi, S., Hasselquist, D. and Ottosson, U. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 1545–1554.CrossRefGoogle ScholarPubMed
Wang, D., Coscoy, L., Zylberberg, M., Avila, P. C., Boushey, H. A., Ganem, D. and DeRisi, J. L. (2002). Microarray-based detection and genotyping of viral pathogens. Proceedings of the National Academy of Sciences 99, 15687–15692.CrossRefGoogle ScholarPubMed
Wiehn, J., Korpimáki, E., Bildstein, K. L. and Sorjonen, J. (1997). Mate choice and reproductive success in the American Kestrel: a role for blood parasites? Ethology 103, 304–317.CrossRefGoogle Scholar
Williams, G. C. (1966). Adaptation and Natural Selection, Princeton University Press, Princeton, NJ.Google Scholar
Zylberberg, M. (2014). Galapagos ground finches balance investment in behavioural and immunological pathogen defences. Ibis 156, 615–626.CrossRefGoogle Scholar
Zylberberg, M., Klasing, K. C. and Hahn, T. P. (2013a). House finches (Carpodacus mexicanus) balance investment in behavioural and immunological defences against pathogens. Biology Letters 9, 20120856.CrossRefGoogle ScholarPubMed
Zylberberg, M., Lee, K. A., Klasing, K. C., Wikelski, M. (2013b). Variation with land use of immune function and prevalence of Avian Pox in Galapagos finches. Conservation Biology 27, 103–112.CrossRefGoogle ScholarPubMed
Zylberberg, M., Klasing, K. C. and Hahn, T. P. (2014). In house finches, Haemorhous mexicanus, risk takers invest more in innate immune function. Animal Behaviour 89, 115–122.CrossRefGoogle Scholar