Skip to main content
SpringerLink
Log in

Age and environment affect constitutive immune function in Red Knots (Calidris canutus)

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

We studied subspecies, age and environmental effects on constitutive immune function (natural antibody and complement titres, haptoglobin activity and leukocyte concentrations) in Red Knots (Calidris canutus). We compared C. c. islandica and C. c. canutus in the Wadden Sea and found no difference in immune function between subspecies. However, C. c. canutus on their wintering grounds in Banc d’Arguin had higher natural antibody and lower complement levels than C. c. canutus or C. c. islandica in the Wadden Sea. This suggests that immune function is determined more by the surrounding environment than by subspecies. We also compared age classes in the Wadden Sea and found that first year birds had significantly lower natural antibody levels than adults, but that second year birds no longer differed from adults. Finally, we examined the interaction of age and environment in Banc d’Arguin. We found that first year birds (but not adults) in a low quality habitat had higher leukocyte concentrations than first year birds or adults in a high quality habitat. Differences in available resources and defence needs between environments, and differences among individuals differentially distributed between sites, are likely important contributors to the variation in immune function we report. Future studies, which examine these factors on wild birds, will be important for our understanding of how animals function in their natural environment. (220).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baker AJ, Piersma T, Greenslade AD (1999) Molecular vs. phenotypic sexing in red knots. Condor 101:887–893

    Article  Google Scholar 

  • Baumgarth N, Tung JW, Herzenberg LA (2005) Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Semin Immunopathol 26:347–362

    Article  CAS  Google Scholar 

  • Buehler DM, Baker AJ (2005) Population divergence times and historical demography in red knots and dunlins. Condor 107:497–513

    Article  Google Scholar 

  • Buehler DM, Piersma T (2008) Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants. Philos Trans R Soc Lond B 363:247–266

    Article  Google Scholar 

  • Buehler DM, Bhola N, Barjaktarov D, Goymann W, Schwabl I, Tieleman BI, Piersma T (2008a) Constitutive immune function responds more slowly to handling stress than corticosterone in a shorebird. Physiol Biochem Zool 81:673–681

    Article  Google Scholar 

  • Buehler DM, Piersma T, Matson K, Tieleman BI (2008b) Seasonal redistribution of immune function in a shorebird: annual cycle effects override adjustments to thermal regime. Am Nat 172:783–796

    Article  Google Scholar 

  • Campbell TW (1995) Avian hematology and cytology, 2nd edn. Iowa State University Press, Ames Iowa

    Google Scholar 

  • Davidson NC, Wilson JR (1992) The migration system of European-wintering knots Calidris canutus islandica. Wader Study Group Bull 64(Supplement):39–51

    Google Scholar 

  • Delers F, Strecker G, Engler R (1988) Glycosylation of chicken haptoglobin: isolation and characterization of three molecular variants and studies of their distribution in hen plasma before and after turpentine-induced inflammation. Biochem Cell Biol 66:208–217

    Article  CAS  Google Scholar 

  • Janeway CA, Travers P, Walport M, Shlomchik M (2004) Immunobiology: the immune system in health and disease, 6th edn. Garland, New York

    Google Scholar 

  • Leyrer J, Spaans B, Camara M, Piersma T (2006a) Small home ranges and high site fidelity in red knots (Calidris c. canutus) wintering on the Banc d’Arguin, Mauritania. J Ornithol 147:376–384

    Article  Google Scholar 

  • Leyrer J, Spaans B, Piersma T (2006b) Sex, age and survival differences between adjacent functional units of tropical wintering habitat in a flocking long-distance migrant shorebird. J Ornithol 147 (Supplement 1 Abstracts of the 24th International Ornithological Congress, Hamburg, Germany):202

  • Matson KD (2006) Are there differences in immune function between continental and insular birds? Proc R Soc Lond B 273:2267–2274

    CAS  Google Scholar 

  • Matson KD, Ricklefs RE, Klasing KC (2005) A hemolysis-hemagglutination assay for characterizing constitutive innate humoral immunity in wild and domestic birds. Dev Comp Immunol 29:275–286

    Article  CAS  Google Scholar 

  • Mauck RA, Matson KD, Philipsborn J, Ricklefs RE (2005) Increase in the constitutive innate humoral immune system in Leach’s storm-petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate. Funct Ecol 19:1001–1007

    Article  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045

    Article  Google Scholar 

  • Nebel S, Piersma T, van Gils JA, Dekinga A, Spaans B (2000) Length of stopover, fuel storage and a sex-bias in the occurrence of red knots Calidris canutus canutus and C.c. islandica in the Wadden Sea during southward migration. Ardea 88:165–176

    Google Scholar 

  • Ochsenbein AF, Zinkernagel RM (2000) Natural antibodies and complement link innate and acquired immunity. Immunol Today 21:624–630

    Article  CAS  Google Scholar 

  • Ochsenbein AF, Fehr T, Lutz C, Suter M, Brombacher F, Hengartner H, Zinkernagel RM (1999) Control of early viral and bacterial distribution and disease by natural antibodies. Science 286:2156–2159

    Article  CAS  Google Scholar 

  • Piersma T (2006) Understanding the numbers and distributions of waders and other animals in a changing world: habitat choice as the lock and the key. Stilt 50:3–14

    Google Scholar 

  • Piersma T (2007) Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J Ornithol 148(Suppl 1):S45–S59

    Article  Google Scholar 

  • Piersma T, Davidson NC (1992) The migrations and annual cycles of five subspecies of knots in perspective. Wader Study Group Bull 64(Suppl):187–197

    Google Scholar 

  • Piersma T, Prokosch P, Bredin D (1992) The migration system of Afro-Siberian knots Calidris canutus canutus. Wader Study Group Bull 64(Suppl):52–63

    Google Scholar 

  • Piersma T, de Goeij TP, Tulp I (1993) An evaluation of intertidal feeding habitats from a shorebird perspective: towards relevant comparisons between temperate and tropical mudflats. Netherlands J Sea Res 31:503–512

    Article  Google Scholar 

  • Piersma T, Rogers DI, González PM, Zwarts L, Niles LJ, de Lima Serrano do Nascimento I, Minton CDT, Baker AJ (2005) Fuel storage rates before northward flights in red knots worldwide: facing the severest constraint in tropical intertidal environments? In: Greenberg R, Marra PP (eds) Birds of two worlds: the ecology and evolution of migration. Johns Hopkins University Press, Baltimore, pp 262–273

    Google Scholar 

  • Prater AJ, Marchant JH, Vuorinen J (1977) Guide to the identification and aging of Holarctic waders. BTO Guide, Tring, UK

  • Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32

    Article  Google Scholar 

  • Seto F, Henderson WG (1968) Natural and immune hemagglutinin forming capacity of immature chickens. J Exp Zool 169:501–511

    Article  CAS  Google Scholar 

  • van Gils JA, Battley PF, Piersma T, Drent R (2005) Reinterpretation of gizzard sizes of red knots world-wide, emphasizes overriding importance of prey quality at migratory stopover sites. Proc R Soc Lond B 272:2609–2618

    Google Scholar 

  • Wiersma P, Piersma T (1994) Effects of microhabitat, flocking, climate and migratory goal on energy expenditure in the annual cycle of knots. Condor 96:257–279

    Article  Google Scholar 

  • Wolff WJ, Smit CJ (1990) The Banc d’Arguin, Mauritania, as an environment for coastal birds. Ardea 78:17–38

    Google Scholar 

  • Zwarts L, Blomert A-M, Ens BJ, Hupkes R, van Spanje TM (1990) Why do waders reach high feeding densities on the intertidal flats of the Banc d’Arguin, Mauritania? Ardea 78:39–52

    Google Scholar 

Download references

Acknowledgments

We thank Alberto Castillo for help in the field and laboratory; Nina Bhola, Daliborka Barjaktarov, François Vézina, Magali Petit, Anne Dekinga, Bernard Spaans and the crew of the H. M. Navicula for support in the Wadden Sea; Bernard Spaans, Jutta Leyrer, Jeroen Reneerkens, Edward Koomson, H. ould M. El Hacen and M. Camara for support in Mauritania; Bernard Spaans and Jutta Leyrer for help identifying C. c. islandica and C. c. canutus from resight/recapture data; Anneke Bol for help with molecular sexing and Dick Visser for finalising the figures. Funding was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC) PGSB-267701-2003, a University of Groningen Ubbo Emmius Scholarship, a Netherlands Organization for Scientific Research (NWO) travel grant, and Schure-Beijerinck-Popping Fonds to D.M.B., N.W.O. and the University of Groningen to B.I.T. and T.P., operational grants from the Royal Netherlands Institute for Sea Research (NIOZ) to T.P. and a MAVA grant to T.P. and J. Leyrer.

Author information

Authors and Affiliations

  1. Animal Ecology Group, Centre for Ecological and Evolutionary Studies, University of Groningen, PO Box 14, 9750 AA, Haren, The Netherlands

    Deborah M. Buehler, B. Irene Tieleman & Theunis Piersma

  2. Department of Marine Ecology and Evolution, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, 1790 AB, Den Burg, Texel, The Netherlands

    Theunis Piersma

Authors
  1. Deborah M. Buehler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Irene Tieleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Theunis Piersma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deborah M. Buehler.

Additional information

Communicated by C. G. Guglielmo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buehler, D.M., Irene Tieleman, B. & Piersma, T. Age and environment affect constitutive immune function in Red Knots (Calidris canutus). J Ornithol 150, 815–825 (2009). https://doi.org/10.1007/s10336-009-0402-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-009-0402-6

Keywords

Search

Navigation