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Oecologia

, Volume 145, Issue 2, pp 326–333 | Cite as

Cross-fostering reveals an effect of spleen size and nest temperatures on immune responses in nestling European starlings

  • Daniel R. Ardia
Behavioral ecology

Abstract

Immunocompetence may be a good measure of offspring quality, however, factors affecting variation in immune responses are not clear. Research suggests that immune function can vary due to differences in genetics, development conditions and individual quality. Here, I examined factors affecting variation in immune response among nestling European starlings through a split-nest cross-fostering brood manipulation that included two important covariates: spleen size and nest temperatures. Immunocompetence was assessed via a cell-mediated immune response to phytohaemagglutinin (PHA). This paper provides the first direct evidence that individuals with large spleens also mount strong immune responses. Exposure to PHA did not cause splenomegaly, as there was no difference in spleen size between control birds and those injected with PHA. Offspring immune function was affected by common origin and by rearing environment, though rearing environment appeared to exert its influence only through nest temperatures. A comparison of the immune performance of siblings reared in their home nest versus those reared in other nests revealed a strong effect of maternal quality. As the difference in natal clutch size increased, the magnitude of the difference in immune performance between home-reared nestlings versus out-reared nestlings increased. Overall, nestling immune function appears to be determined by the combination of genetic, maternal and environmental effects.

Keywords

Cell-mediated immune function Cross-fostering Offspring quality Rearing environment Sturnus vulgaris 

Notes

Acknowledgements

I am grateful to John and Meg Flux for letting me work at the Belmont field site and for their generosity of time and advice, and Nathaniel Taylor for assistance under difficult field conditions. Elizabeth Atkinson and Fabio provided additional support. This manuscript was improved through discussions with Andre Dhondt, David Winkler, Wesley Hochachka, Karel Schat, Matt Wasson, Dana Hawley, Becca Safran and Mark Hauber. Victor Apanius, Charles Brown and Carol Vleck made comments that substantively improved this manuscript. The U.S. Environmental Protection Agency provided financial support. This work was carried out under an Animal Care Protocol approved by the Cornell Center for Research Animal Resources.

References

  1. Adriaensen F, Dhondt AA, Van Dongen S, Lens S, Matthysen E (1998) Stabilizing selection on blue tit fledgling mass in the presence of sparrowhawks. Proc R Soc Lond B Biol Sci 265:1011–1016CrossRefGoogle Scholar
  2. Apanius V (1998) Ontogeny of immune function. In: Starck JM, Ricklefs RE (eds) Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 203–222Google Scholar
  3. Blanco G, de la Puente J, Corroto M, Baz A, Cola J (2001) Condition-dependent immune defence in the Magpie: how important is ectoparasitism? Biol J Linnean Soc 72:279–286Google Scholar
  4. Blount JD, Houston DC, Møller AP, Wright J (2003) Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds. Oikos 102:340–350CrossRefGoogle Scholar
  5. Brinkhof MWG, Heeb P, Kölliker M, Richner H (1999) Immunocompetence of nestling great tits in relation to rearing environment and parentage. Proc R Soc Lond B Biol Sci 266: 2315–2322CrossRefGoogle Scholar
  6. Brown CR, Brown MB (2002) Spleen volume varies with colony size and parasite load in a colonial bird. Proc R Soc Lond B 269:1367–1373CrossRefGoogle Scholar
  7. Brown CR, Sherman LC (1989) Variation in the appearance of swallow eggs and the detection of intraspecific brood parasitism. Condor 91:620–627CrossRefGoogle Scholar
  8. Cheng S, Lamont SJ (1988) Genetic analysis of immunocompetence measures in a white leghorn chicken line. Poul Sci 67:989–995PubMedGoogle Scholar
  9. Christe P, Møller AP, de Lope F (1998) Immunocompetence and nestling survival in the house martin: the tasty chick hypothesis. Oikos 83:175–179CrossRefGoogle Scholar
  10. Christians JK, Evanson M, Aiken JJ (2001) Seasonal decline in clutch size in European starlings: A novel randomization test to distinguish between the timing and quality hypotheses. J Anim Ecol 70:1080–1087CrossRefGoogle Scholar
  11. Darlington RB, Smulders TV (2001) Problems with residual analysis. Anim Behav 62:599–602CrossRefGoogle Scholar
  12. Dhondt AA (1971) The regulation of numbers in Belgian populations of great tits. In: den Boer PJ, Gradwell JR (eds) Dynamics of populations. Advanced Study Institute, Wageningen, pp 532–547Google Scholar
  13. Dietert RR, Golemboski KA, Austic RE (1994) Environment-immune interactions. Poult Sci 73:1062–1076PubMedGoogle Scholar
  14. Donker RA, Nieuwland MGB, Vanderzijpp AJ (1990) Heat-stress influences on antibody-production in chicken lines selected for high and low immune responsiveness. Poult Sci 69:599–607PubMedGoogle Scholar
  15. Flux JEC, Flux MM (1981) Artificial selection and gene flow in wild starlings, Sturnus vulgaris. Naturwissenschaften 69: 96–97CrossRefGoogle Scholar
  16. Hõrak P, Tegelmann L, Ots I, Møller AP (1999) Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121:316–322CrossRefGoogle Scholar
  17. Henken AM, Schaarsberg AMJG, Nieuwland MGB (1983) The effect of environmental-temperature on immune-response and metabolism of the young chicken 3: Effect of environmental-temperature on the humoral immune-response following injection of sheep red-blood-cells. Poult Sci 62:51–58PubMedGoogle Scholar
  18. Hochachka W, Smith JNM (1991) Determinants and consequences of nestling condition in song sparrows. J Anim Ecol 60:995–1008CrossRefGoogle Scholar
  19. Hoi-Leitner M, Romero-Pujante M, Hoi H, Pavlova A (2001) Food availability and immune capacity in serin nestlings. Behav Ecol Sociobiol 49:333–339CrossRefGoogle Scholar
  20. John JL (1994) The avian spleen: a neglected organ. Q Rev Biol 69:327–351PubMedCrossRefGoogle Scholar
  21. John JL (1995) Parasites and the avian spleen: Helminths. Biol J Linnean Soc 54:87–106CrossRefGoogle Scholar
  22. Kirkley JS, Gessaman JA (1990) Ontogeny of thermoregulation in red-tailed hawks and Swainson’s hawks. Wilson Bull 102:71–83Google Scholar
  23. Klasing KC (1998) Nutritional modulation of resistance to infectious disease. Poult Sci 77:1119–1125PubMedGoogle Scholar
  24. Liker A, Màrkus M, Vozár A, Zemankovics E, Rózsa L (2001) Distribution of Carnus hemapterus in a starling colony. Can J Zool 79:574–580CrossRefGoogle Scholar
  25. Linden M, Gustafsson L, Part T (1992) Selection on fledging mass in the collared flycatcher and the great tit. Ecology 73:336–343CrossRefGoogle Scholar
  26. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, CaryGoogle Scholar
  27. Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510Google Scholar
  28. Miller L, Qureshi MA (1992) Induction of heat-shock proteins and phagocytic function of chicken macrophages following in vitro heat exposure. Vet Immunol Immunopathol 30:179–192PubMedCrossRefGoogle Scholar
  29. Møller AP, Erritzøe J (2000) Predation against birds with low immmunocompetence. Oecologia 122:500–504CrossRefGoogle Scholar
  30. Møller AP, Sorci G, Erritzøe J (1998a) Host immune function and sexual selection in birds. J Evol Biol 11:703–719CrossRefGoogle Scholar
  31. Møller AP, Sorci G, Erritzøe J, Mavarez J (1998b) Condition, disease, and immune defence. Oikos 83:301–306CrossRefGoogle Scholar
  32. Perrins CM (1964) Survival of young swifts in relation to brood size. Nature 201:1147CrossRefGoogle Scholar
  33. Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66: 827–836CrossRefGoogle Scholar
  34. Smith HG (2004) Selection for synchronous breeding in the European starling. Oikos 105:301–311CrossRefGoogle Scholar
  35. Smith KG, Hunt JL (2004) On the use of the avian spleen as a measure of avian immune strength. Oecologia 138:28–31PubMedCrossRefGoogle Scholar
  36. Smits JE, Williams TD (1999) Validation of ecotoxicology techniques in passerine chicks exposed to oil sands tailings water. Ecotoxicol Environ Saf 44:105–112PubMedCrossRefGoogle Scholar
  37. Taylor RLJ, Cotter PF, Wing TL, Briles WE (1987) Major histocompatibility B complex and sex effects on the phytohaemagglutinin wattle response. Anim Genet 18:343–350PubMedGoogle Scholar
  38. Tella JL, Bortolotti GR, Dawson RD, Forero MG (2000) The T-cell-mediated immune response of fledgling American kestrels are positively correlated with parental clutch size. Proc R Soc Lond B 267:891–895CrossRefGoogle Scholar
  39. Thompson CF, Flux JEC (1988) Body mass and lipid content at nest-leaving of European starlings in New Zealand. Ornis Scandinavica 19:1–6CrossRefGoogle Scholar
  40. Thompson CF, Flux JEC, Tetzlaff VT (1993) The heaviest nestlings are not necessarily the fattest nestlings. J Field Ornithol 64:426–432Google Scholar
  41. Visser GH (1998) Development of temperature regulation. In: Starck JM, Ricklefs RE (eds) Avian growth and development: Evolution within the altricial-precocial spectrum. Oxford Ornithology Series, Oxford University Press, Oxford, pp 117–156Google Scholar
  42. Warner CM, Meeker DL, Rothschild MF (1987) Genetic control of immune responsiveness: a review of its use as a tool for selection for disease resistance. J Anim Sci 64:394–406PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA
  2. 2.Program in Organismic and Evolutionary Biology, Morrill Science CenterUniversity of MassachusettsAmherstUSA

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