, 159:697 | Cite as

Rearing environment effects on immune defence in blue tit Cyanistes caeruleus nestlings

  • Elena ArrieroEmail author
Physiological Ecology - Original Paper


Rearing conditions may influence ontogeny and functioning of the immune system. Activation of different mechanisms involved in host disease resistance and their internal regulation can be affected by intrinsic and extrinsic factors influencing development. I investigated how rearing environment can influence associations between humoral and cellular constituents of immune defence in nestling blue tits (Cyanistes caeruleus). The ability to mount a cell-mediated immune response was estimated as a hypersensitivity reaction to phytohaemagglutinin, and the ontogeny of humoral immunity was determined by assessing circulating levels of total IgG in 15-day-old nestlings. Heterogeneity in rearing conditions was evoked by placing nest-boxes in areas differing in habitat structural characteristics, and examining natural variation in nest ectoparasite infestations, hatching date, brood size and brood sex-ratio. Habitat characteristics, parasitism and hatching date may shape associations between different components of the immune system in developing birds. I discuss the effects of rearing conditions on the interaction between different arms of the immune system and the implications for understanding negative correlations within the immune system at the individual and brood level.


Circulating immunoglobulins Ectoparasites Forest structure Immune function Phytohaemagglutinin 



I thank J. Moreno, A.P. Møller and two anonymous reviewers for valuable comments on the manuscript. The study was supported financially by projects 07M/0137/2000 (Comunidad de Madrid) to L.M. Carrascal and CGL2004-00787/BOS to J. Moreno (Ministerio de Ciencia y Tecnología). E.A. was supported by a fellowship from El Ventorrillo-CSIC during field and laboratory work. During final analyses and writing, support to E.A. was provided by Laboratoire de Parasitologie Evolutive UPMC UMR 7103, France. J.A. Fargallo, J.J. Sanz, S. Merino and A. Martin were of great help in the field and in different phases of the project. I thank J. Martinez, J.A. Davila and A. Machordon for advice in laboratory techniques. Museo Nacional de Ciencias Naturales (CSIC) and El-Ventorrillo field station provided infrastructure and logistical support during field and laboratory work. Capture of birds and fieldwork in the study area was conducted under authorization from Comunidad de Madrid and Ministerio de Medio Ambiente, Spain.


  1. Adamo SA (2004) How should behavioural ecologists interpret measurements of immunity? Anim Behav 68:1443–1449CrossRefGoogle Scholar
  2. Apanius V (1998) The immune system. In: Starck JM, Ricklefs RE (eds) Avian growth and development. Oxford University Press, New York, pp 203–222Google Scholar
  3. Ardia DR (2007) The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow. Ecography 30:23–30Google Scholar
  4. Arriero E, Sanz JJ, Romero-Pujante M (2006) Habitat structure in Mediterranean deciduous forests in relation to reproductive success in the blue tit Parus caeruleus: effects operate during laying and incubation. Bird Study 53:12–19CrossRefGoogle Scholar
  5. Arriero E, Moreno J, Merino S, Martinez J (2008) Habitat effects on physiological stress response in nestling blue tits are mediated through parasitism. Physiol Biochem Zool 81:195–203PubMedCrossRefGoogle Scholar
  6. Blondel J, Dias PC, Maistre M, Perret P (1993) Habitat heterogeneity and life-history variation in Mediterranean blue tits (Parus caeruleus). Auk 110:511–520Google Scholar
  7. Bonneaud C, Mazuc J, González G, Haussy C, Chastel O, Faivre B, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161:367–379PubMedCrossRefGoogle Scholar
  8. Brokaw NVL, Lent RA (1999) Vertical structure. In: Hunter ML (ed) Maintaining biodiversity in forest ecosystems. Cambridge University Press, Cambridge, pp 373–399Google Scholar
  9. Brommer JE (2004) Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proc Biol Sci 271(Suppl 3):S110–S113PubMedCrossRefGoogle Scholar
  10. Buchanan KL, Evans MR, Goldsmith AR (2003) Testosterone dominance signaling and immunosuppression in the house sparrow, Passer domesticus. Behav Ecol Sociobiol 55:50–59CrossRefGoogle Scholar
  11. Buechler K, Fitze PS, Gottstein B, Jacot A, Richner H (2002) Parasite-induced maternal response in a natural bird population. J Anim Ecol 71:247–252CrossRefGoogle Scholar
  12. Cotter SC, Kruuk LEB, Wilson K (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17:421–429PubMedCrossRefGoogle Scholar
  13. Demas GE (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45:173–180PubMedCrossRefGoogle Scholar
  14. Dubiec A, Cichón M, Deptuch K (2006) Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings. Proc Biol Sci 273:1759–1764PubMedCrossRefGoogle Scholar
  15. Faivre B, Préault M, Salvadori F, Théry M, Gaillard M, Cézilly F (2003) Bill colour and immunocompetence in the European blackbird. Anim Behav 65:1125–1131CrossRefGoogle Scholar
  16. Forsman AM, Vogel LA, Sakaluk SK, Grindstaff JL, Thompson CF (2008) Immune-challenged house wren broods differ in the relative strengths of their responses among different axes of the immune system. J Evol Biol 21:873–878PubMedCrossRefGoogle Scholar
  17. Garvin MC, Remsen JV (1997) An alternative hypothesis for heavier parasite loads of brightly colored birds: exposure at the nest. Auk 114:179–191Google Scholar
  18. Gasparini J, McCoy KD, Tveraa T, Boulinier T (2002) Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol Lett 5:519–524CrossRefGoogle Scholar
  19. Gasparini J, Roulin A, Gill VA, Hatch SA, Boulinier T (2006) In kittiwakes food availability partially explains the seasonal decline in humoral immunocompetence. Funct Ecol 20:457–463CrossRefGoogle Scholar
  20. Gershwin ME, Beach RS, Hurley LS (1985) Nutrition and immunity. Academic, OrlandoGoogle Scholar
  21. Gonzalez G, Sorci G, Møller AP, Ninni P, Haussy C, de Lope F (1999) Immunocompetence and condition-dependent sexual advertisement in male house sparrows (Passer domesticus). J Anim Ecol 68:1225–1234CrossRefGoogle Scholar
  22. Graham AL (2002) When T-helper cells don’t help: immunopathology during concomitant infection. Q Rev Biol 77:409–434PubMedCrossRefGoogle Scholar
  23. Griffiths R, Double MC, Orr K, Dawson JG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  24. Grindstaff JL, Hasselquist D, Nilsson J-Å, Sandell M, Smith HG, Stjernman M (2006) Trangenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc Biol Sci 273:2551–2557PubMedCrossRefGoogle Scholar
  25. Heeb P, Werner I, Mateman AC, Kölliker M, Brinkhof MWG, Lessells CM, Richner H (1999) Ectoparasite infestation and sex-biased local recruitment of hosts. Nature 400:63–65PubMedCrossRefGoogle Scholar
  26. Hoi-Leitner M, Romero-Pujante M, Hou H, Pavlova A (2001) Food availability and immune capacity in serin (Serinus serinus) nestlings. Behav Ecol Sociobiol 49:333–339CrossRefGoogle Scholar
  27. Keil D, Luebke RW, Pruett SB (2001) Quantifying the relationship between multiple immunological parameters and host resistance: probing the limits of reductionism. J Immunol 167:4543–4552PubMedGoogle Scholar
  28. Martin LBII, Weil ZM, Kuhlman JR, Nelson RJ (2006a) Trade-offs within the immune systems of female White-footed Mice, Peromyscus leucopus. Funct Ecol 20:630–636CrossRefGoogle Scholar
  29. Martin LBII, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006b) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299CrossRefGoogle Scholar
  30. Martínez J, Tomás G, Merino S, Arriero E, Moreno J (2003) Detection of serum immunoglobulins in wild birds by direct ELISA: a methodological study to validate the technique in different species using antichicken antibodies. Funct Ecol 17:700–706CrossRefGoogle Scholar
  31. Matson KD, Cohen AA, Klasing KC, Ricklefs RE, Scheuerlein A (2006) No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl. Proc Biol Sci 273:815–822PubMedCrossRefGoogle Scholar
  32. Merilä J, Björklund M, Bennett GF (1995) Geographic and individual variation in haematozoan infections in the greenfinch, Carduelis chloris. Can J Zool 73:1798–1804CrossRefGoogle Scholar
  33. Merino S, Potti J (1995) Mites and blowflies decrease growth and survival in nestling pied flycatchers. Oikos 73:95–103CrossRefGoogle Scholar
  34. Merino S, Møller AP, de Lope F (2000) Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: a parasite-mediated effect? Oikos 90:327–332CrossRefGoogle Scholar
  35. Morales J, Moreno J, Merino S, Tomas G, Martinez J, Garamszegi L (2004) Associations between immune parameters, parasitism, and stress in breeding pied flycatcher (Ficedula hypoleuca) females. Can J Zool 82:1484–1492CrossRefGoogle Scholar
  36. Moreno J, Lobato E, Morales J, Merino S, Martínez-De La Puente J, Tomás G (2008) Pre-laying nutrition mediates maternal effects on offspring immune capacity and growth in the pied flycatcher. Oecologia 156:727–735PubMedCrossRefGoogle Scholar
  37. Møller AP, Saino N (2004) Immune response and survival. Oikos 104:299–304CrossRefGoogle Scholar
  38. Møller AP, Christe P, Garamszegi L (2005) Coevolutionary arms races: increased host immune defense promotes specialization by avian fleas. J Evol Biol 18:46–59PubMedCrossRefGoogle Scholar
  39. Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defence and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145PubMedCrossRefGoogle Scholar
  40. Prendergast BJ, Hotchkiss AK, Bilbo SD, Nelson RJ (2004) Peripubertal immune challenges attenuate reproductive development in male Siberian hamsters (Phodopus sungorus). Biol Reprod 70:813–820PubMedCrossRefGoogle Scholar
  41. Råberg L, Nilsson JA, Ilmonen P, Stjerman M, Hasselquist D (2000) The cost of an immune response: vaccination reduces parental effort. Ecol Lett 3:382–386CrossRefGoogle Scholar
  42. Reid JM, Arcese P, Keller LF, Hasselquist D (2006) Long-term maternal effect on offspring immune response in song sparrows Melospiza melodia. Biol Lett 2:573–576PubMedCrossRefGoogle Scholar
  43. Richner H, Oppliger A, Christe P (1993) Effect of an ectoparasite on reproduction in great tits. J Anim Ecol 62:703–710CrossRefGoogle Scholar
  44. Ricklefs RE (1992) Embryonic development period and the prevalence of avian blood parasites. Proc Natl Acad Sci USA 89:4722–4725PubMedCrossRefGoogle Scholar
  45. Roit IM, Brostoff J, Male DK (1998) Immunology. Mosby, LondonGoogle Scholar
  46. Rosenthal R (1994) Parametric measures of effect size. In: Cooper H, Hedges LV (eds) The handbook of research synthesis. Russell Sage Foundation, New York, pp 231–244Google Scholar
  47. Roulin A, Christe P, Dijkstra C, Ducrest AL, Jungi TW (2007) Origin-related, environmental, sex, and age determinants of immunocompetence, susceptibility to ectoparasites, and disease symptoms in the barn owl. Biol J Linn Soc 90:703–718CrossRefGoogle Scholar
  48. 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
  49. Scheuerlein A, Ricklefs RE (2004) Prevalence of blood parasites in European passeriform birds. Proc Biol Sci 271:1363–1370PubMedCrossRefGoogle Scholar
  50. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefGoogle Scholar
  51. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  52. Soler JJ, de Neve L, Perez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc Biol Sci 270:241–248PubMedCrossRefGoogle Scholar
  53. Sorci G, Soler JJ, Møller AP (1997) Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica). Proc R Soc Lond B 264:1593–1598CrossRefGoogle Scholar
  54. Tremblay I, Thomas DW, Lambrechts MM, Blondel J, Perret P (2003) Variation in blue tit breeding performance across gradients in habitat richness. Ecology 84:3033–3043CrossRefGoogle Scholar
  55. Wakelin D (1996) Immunity to parasites. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Laboratoire de Parasitologie EvolutiveUPMC Univ Paris 06, CNRS UMR 7103ParisFrance
  2. 2.Centre d’Ecologie Fonctionnelle et Evolutive, CNRS UMR 5175Montpellier cedex 5France

Personalised recommendations