Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds (original) (raw)

Abstract

An important pattern in host-parasite assemblages is a higher intensity of parasites in juveniles than in adults, but the reasons for these differences remain obscure. Three non-mutually exclusive hypotheses have been proposed: (1) heavily parasitized juveniles die before being recruited into the adult population ('selection' hypothesis); (2) the development of an acquired immunity by the host in front of the parasite reduces the intensity of the parasite in adult hosts ('immunity' hypothesis); and (3) differences in behavior makes adults less exposed to the parasite than juveniles ('vector exposure' hypothesis). Having rejected the 'vector exposure' hypothesis in a previous study, here we tested the 'selection' and 'immunity' hypotheses in feral pigeons (Columba livia) infected by the blood parasite Haemoproteus columbae. In agreement with the 'selection' hypothesis, young (but not adult) pigeons that were highly parasitized had a lower probability of surviving until adulthood, independent of their body condition. However, selection was not strong enough to account for the observed differences in parasite intensity between age-classes, and after selection parasite intensity of survivors still remained 85% higher in juveniles than in adults. In contrast, the 'immunity' hypothesis offered a greater explanatory power. The intensity of blood parasites in young pigeons, but not in adults, decreased over time so dramatically that by the time they had become adults their intensities were indistinguishable from that typically seen in adults. Therefore, while selection against highly parasitized juveniles can contribute to some extent to a reduction in parasitism seen in the adult population, age-specific blood parasitism in feral pigeons is best explained as a transitory phase just before the host develops an effective immune response.

Access this article

Log in via an institution

Subscribe and save

• Starting from 10 chapters or articles per month
• Access and download chapters and articles from more than 300k books and 2,500 journals
• Cancel anytime View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

• Allander K, Bennett GF (1994) Prevalence and intensity of haematozoan infections in a population of great tits Parus major from Gotland, Sweden. J Avian Biol 25:69–74
  Google Scholar
• Atkinson CT (1999) Hemosporidiosis. In: Friend M, Franson JC (eds) Field manual of wildlife diseases: general field procedures and diseases of birds. Biological Resources Division Information and Technology Report 1999–001. Government Printing Office, Washington, D.C., pp 193–199
  Google Scholar
• Atkinson CT, van Riper III C (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In: Loye JE, Zuk M (eds) Bird-parasite interactions. Oxford University Press, Oxford, pp 19–48
• Bennett GF, Peirce MA (1990) The haemoproteid parasites of the pigeons and doves (Family Columbidae). J Nat Hist 24:311–325
  Google Scholar
• Bennett GF, Caines JR, Bishop MA (1988) Influence of blood parasites on the body mass of passeriform birds. J Wildl Dis 24:339–343
  CAS PubMed Google Scholar
• Bennett GF, Squires-Parsons D, Siikamäki P, Huhta E, Allander K, Hillström L (1995) A comparison of the blood parasites of three Fenno-Scandian populations of the Pied Flycatcher Ficedula hypoleuca. J Avian Biol 26:33–38
  Google Scholar
• Davidar P, Morton ES (1993) Living with parasites: prevalence of a blood parasite and its effects on survivorship in the Purple Martin. Auk 110:109–116
  Google Scholar
• Dawson RD, Bortolotti, GR (1999) Prevalence and intensity of hematozoan infections in a population of American kestrels. Can J Zool 77:162–170
  Article Google Scholar
• Dawson RD, Bortolotti, GR (2000) Effects of hematozoan parasites on condition and return rates of American kestrels. Auk 117:373–380
  Google Scholar
• Endler JA (1986) Natural selection in the wild. : Princeton University Press, Princeton, N.J.
• Garcia-Berthou E (2001) On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. J Anim Ecol 70:708–711
  Article Google Scholar
• Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, Brabin BJ, Gibson FD, Bradley DJ, Alpers MP (1988) Measurements of malarial infectivity of human populations to mosquitoes in the Madang area, Papua New Guinea. Parasitology 96:251–263
  PubMed Google Scholar
• Gregory RD, Montgomery SSJ, Montgomery WI (1992) Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. J Anim Ecol 61:749–757
  Google Scholar
• Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
  CAS PubMed Google Scholar
• Hudson PJ, Dobson AP (1997) Host-parasite processes and demographic consequences. In: Clayton DH, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 128–154
  Google Scholar
• Kautz JE, Seamans TW (1986) Estimating age of nestling and juvenile feral rock doves. J Wildl Manage 50:544–547
  Google Scholar
• Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
  Google Scholar
• Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? Proc Natl Acad Sci USA 98:2071–2076
  Article CAS PubMed Google Scholar
• Merino S, Moreno J, Sanz JJ, Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B 267:1–4
  Article PubMed Google Scholar
• Poulin R, Marshall LJ, Spencer HG (2000) Genetic variation and prevalence of blood parasites do not correlate among bird species. J Zool 252:381–388
  Article Google Scholar
• Schluter D (1988) Estimating the form of natural selection on a quantitative trait. Evolution 42:849–861
  Google Scholar
• Siikamäki P, Rätti O, Hovi M, Bennett GF (1997) Association between haematozoan infections and reproduction in the pied flycatcher. Funct Ecol 11:176–183
  Google Scholar
• Sol D (2000) Introduced species: an important component of the global environmental change. PhD thesis, Universitat de Barcelona
  Google Scholar
• Sol D, Senar JC (1995) Urban pigeon populations: stability, home range, and the effect of removal of individuals. Can J Zool 73:1154–1160
  Google Scholar
• Sol D, Santos DM, Garcia J, Cuadrado M (1998) Competition for food in urban pigeons: the cost of being juvenile. Condor 100:298–304
  Google Scholar
• Sol D, Jovani R, Torres J (2000) Geographical variation in blood parasites in the feral pigeon: the role of vectors. Ecography 23:307–314
  Google Scholar
• Valkiünas G (1997) Bird haemosporida. Acta Zool Lituanica, vol 3–5. Institute of Ecology, Vilnius, Lithuania
• Wunderle JM (1991) Age-specific foraging proficiency in birds. Curr Ornithol 3:273–324
  Google Scholar

Download references

Acknowledgements

We thank D.M. Santos, M. Bosch, J. Garcia and D. Ventura for their assistance in the field. The paper was significantly improved with the valuable comments of D. Ryan, D. Reale, J.L. Tella, S.M. Reader and an anonymous referee. We specially thank J.D. Rodríguez-Teijeiro for his support and logistic assistance during the study, J. Champeny, L.l. Colom and F. Costa for the facilities given to work within the installations of the "Zoològic de Barcelona" and C. Pujol, J.D. Rodríguez-Teijeiro and L. Lefebvre for their constant support. This work was partially supported by a Québec Ministry of Education Postdoctoral Fellowship to D.S.

Author information

Authors and Affiliations

1. Department of Biology, McGill University, 1205 avenue Docteur Penfield, Montreal, Quebec, H3A 1B1, Canada
   Daniel Sol
2. Department of Applied Biology, Estación Biológica de Doñana, C.S.I.C., Avda. Mª Luisa s/n, 41013, Sevilla, Spain
   Roger Jovani
3. Departament de Microbiologia I Parasitologia Sanitàries, Universitat de Barcelona, Av. Diagonal 643, 08028, Barcelona, Catalonia, Spain
   Jordi Torres

Authors

1. Daniel Sol
2. Roger Jovani
3. Jordi Torres

Corresponding author

Correspondence toDaniel Sol.

Rights and permissions

About this article

Cite this article

Sol, D., Jovani, R. & Torres, J. Parasite mediated mortality and host immune response explain age-related differences in blood parasitism in birds.Oecologia 135, 542–547 (2003). https://doi.org/10.1007/s00442-003-1223-6

Download citation

• Received: 17 June 2002
• Accepted: 12 February 2003
• Published: 28 March 2003
• Issue date: May 2003
• DOI: https://doi.org/10.1007/s00442-003-1223-6

Keywords