Skip to main content

Advertisement

SpringerLink
Log in

Swainson’s thrushes in migratory disposition exhibit reduced immune function

  • Article
  • Published:
Journal of Ethology Aims and scope Submit manuscript

Abstract

Evidence indicates that the immune system, which protects an organism from parasitic and pathogenic infections, is frequently suppressed when animals are engaged in activities involving strenuous exercise. We tested the hypothesis that birds reduce immune function during the migratory period in preparation for the anticipated heightened energetic demands of long flights. Swainson’s thrushes (Catharus ustulatus), captured in fall, were held in an indoor aviary until January, when migratory disposition was induced in half of the birds with an artificially prolonged daylength. Experimental birds became hyperphagic and deposited fat stores, and then displayed nocturnal activity (Zugunruhe) characteristic of the spring migratory period. Cell-mediated immunity was measured by intradermal injection of phytohemagglutinin in the wing patagium of both control and experimental birds. Birds exhibiting migratory restlessness had a reduced cell-mediated immune response compared to control birds. Our results suggest that birds are immunosuppressed during the migratory period. The suppression may be a nonadaptive response due to unrelated physiological processes, or it may be an adaptive response to the physiological demands associated with migration, such as high energetic demands and the negative consequences of a hyperactive immune system.

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

Similar content being viewed by others

References

  • Bairlein F (1985) Body weights and fat deposition of Palaearctic passerine migrants in the central Sahara. Oecologia 66:141–146

    Article  Google Scholar 

  • Bentley GE, Demas GE, Nelson RJ, Ball GF (1998) Melatonin, immunity and cost of reproductive state in male European starlings. Proc R Soc Lond B Biol Sci 265:1191–1195

    Article  CAS  Google Scholar 

  • Berthold P (ed) (1975) Migration: control and metabolic physiology. Academic Press, New York

  • Berthold P (1990) Bird migration: a general survey. Oxford University Press, Oxford

    Google Scholar 

  • Blem CR (1990) Avian energy storage. Curr Ornithol 7:59–113

    Google Scholar 

  • Boyum A, Wiik P, Gustavsson E, Veiby OP, Reseland J, Haugen AH, Opstad PK (1996) The effect of strenuous exercise, calorie deficiency and sleep deprivation on white blood cells, plasm immunoglobulins and cytokines. Scand J Immunol 43:228–235

    Article  PubMed  CAS  Google Scholar 

  • Deerenberg C, Apanius V, Daan S, Bos N (1997) Reproductive effort decreases antibody responsiveness. Proc R Soc Lond B Biol Sci 264:1021–1029

    Article  Google Scholar 

  • Deerenberg C, Biebach H, Bauchinger U (2003) Spleen size variation during long-distance migration in the garden warbler Sylvia borin. Avian Sci 2:217–226

    Google Scholar 

  • Evans MD, Yong W (2000) Swainson’s Thrush (Catharus ustulatus). In: Poole A, Gill F (eds) The Birds of North America, no. 540. The Birds of North America Inc., Philadelphia, PA

  • Fänge R, Silverin B (1985) Variation of lymphoid activity in the spleen of a migratory bird, the Pied Flycatcher (Ficedula hypoleuca; Aves, Passeriformes). J Morphol 184:33–40

    Article  Google Scholar 

  • Glick B (2000) Immunophysiology. In: Whittow GC (ed) Sturkie’s avian physiology. Academic Press, San Diego, CA

  • Goto N, Kodama H, Okada K, Fujimoto Y (1978) Suppression of phytohemagglutinin skin response in thymectimized chickens. Poult Sci 52:246–250

    Google Scholar 

  • Guglielmo CG, Piersma T, Williams TD (2001) A sport-physiological perspective on bird migration: evidence for flight-induced muscle damage. J Exp Biol 204:2683–2690

    PubMed  CAS  Google Scholar 

  • Gylfe A, Bergstrom S, Lundstrom J, Olsen B (2000) Reactivation of Borrelia infection in birds. Nature 403:724–725

    Article  PubMed  CAS  Google Scholar 

  • Haldar C, Singh SS (2001) Melatonin and immunological functions/ expression by the bursa of Fabricius in Indian jungle bush quail Perdicula asiatica. In: Dawson A, Chaturvedi CM (eds) Avian endocrinology. Narosa, New Delhi

  • Hasselquist D, Marsh JA, Sherman PW, Wingfield JC (1999) Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45:167–175

    Article  Google Scholar 

  • Hasselquist D, Lindstrom A, Jenni-Eiermann S, Koolhaas A, Piersma T (2007) Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment. J Exp Biol 210:1123–1131

    Article  PubMed  Google Scholar 

  • Hoffman-Goetz L, Pedersen BK (1994) Exercise and the immune system: a model of the stress response. Immunol Today 15:382–387

    Article  PubMed  CAS  Google Scholar 

  • Holberton RL (1999) Changes in patterns of corticosterone secretion concurrent with migratory fattening in a Neotropical migratory bird. Gen Comp Endocrinol 116:49–58

    Article  PubMed  CAS  Google Scholar 

  • Ilmonen P, Hasselquist D, Langefors Å, Wiehn J (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136:148–154

    Article  PubMed  Google Scholar 

  • Jehl J (1997) Cyclical changes in body composition in the annual cycle and migration of the Eared Grebe Podiceps nigricollis. J Avian Biol 28:132–142

    Google Scholar 

  • John JL (1994) The avian spleen: a neglected organ. Q Rev Biol 69:327–351

    Article  PubMed  CAS  Google Scholar 

  • Klasing KC, Leshchinsky TV (1998) Functions, costs, and benefits of the immune system during development and growth. Proc Int Ornithol Congr 22:2817–2835

    Google Scholar 

  • Landys-Ciannelli MM, Piersma T, Jukema J (2003) Strategic size changes of internal organs and muscle tissue in the Bar-tailed Godwit during fat storage on a spring stopover site. Funct Ecol 17:151–159

    Article  Google Scholar 

  • Lifjeld JT, Dunn PO, Whittingham LA (2002) Short-term fluctuations in cellular immunity of tree swallows feeding nestlings. Oecologia 130:185–190

    Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299

    Article  Google Scholar 

  • Martin LB, Scheuerlein A, Wikelski M (2003) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc Lond B Biol Sci 270:153–158

    Article  Google Scholar 

  • McCorkle F, Olah I, Glick B (1980) The morphology of the phytohemagglutinin-induced cell response in the chicken’s wattle. Poult Sci 59:616–623

    Google Scholar 

  • Møller AP, Erritzoe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953

    Article  Google Scholar 

  • Møller AP, Saino N (2004) Immune response and survival. Oikos 104:299–304

    Article  Google Scholar 

  • Moore CB, Siopes TD (2000) Effects of lighting conditions and melatonin supplementation on the cellular and humoral immune responses in Japanese Quail (Coturnix coturnix japonica). Gen Comp Endocrinol 119:95–104

    Google Scholar 

  • Moore FR, Kerlinger P (1987) Stopover and fat deposition by North American wood-warblers (Parulinae) following spring migration over the Gulf of Mexico. Oecologia 74:47–54

    Article  Google Scholar 

  • Muñoz FJ, De La Fuente M (2003) Lymphoid distribution in the migratory gull Larus ridibundus. Comp Biochem Physiol A 136:749–756

    Article  Google Scholar 

  • Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548

    Article  PubMed  CAS  Google Scholar 

  • Nieman DC, Buckley KS, Henson DA, Warren BJ, Suttles J, Ahle JC, Simandle S, Fagoaga OR, Nehlsen-Cannarella SL (1995) Immune function in marathon runners versus sedentary controls. Med Sci Sports Exerc 27:986–992

    Article  PubMed  CAS  Google Scholar 

  • Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR, Henson DA, Shannon M, Hjertman JM, Schmitt RL, Bolton MR, Austin MD, Schilling BK, Thorpe R (2000) Immune function in female elite rowers and non-athletes. Br J Sports Med 34:181–187

    Article  PubMed  CAS  Google Scholar 

  • Niess AM, Dickhuth HH, Northoff H, Fehrenbach E (1999) Free radicals and oxidative stress in exercise–immunological aspects. Exerc Immunol Rev 5:22–56

    PubMed  CAS  Google Scholar 

  • Nilsson JÅ, Granborn M, Råberg L (2007) Does the strength of an immune response reflect its energetic cost? J Avian Biol 38:488–494

    Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Ots I, Hõrak P (1996) Great tits Parus major trade health for reproduction. Proc R Soc Lond B Biol Sci 263:1443–1447

    Google Scholar 

  • Ots I, Kerimov AB, Ivankina EV, Ilyina TA, Hõrak P (2001) Immune challenge affects basal metabolic activity in wintering great tits. Proc R Soc Lond B Biol Sci 268:1175–1181

    Article  CAS  Google Scholar 

  • Owen JC, Moore FR (2006) Seasonal differences in immunological condition of three species of thrushes. Condor 108:390–399

    Article  Google Scholar 

  • Pedersen BK, Bruunsgaard H, Klokker M, Kappel M, Maclean DA, Nielsen HB, Rohde T, Ullum H, Zacho M (1997) Exercise-induced immunomodulation–possible roles of neuroendocrine and metabolic factors. Int J Sports Med 18(Suppl 1):S2–7

    Article  PubMed  CAS  Google Scholar 

  • Peijie C, Hongwu L, Fengpeng X, Jie R, Jie Z (2003) Heavy load exercise induced dysfunction of immunity and neuroendocrine responses in rats. Life Sci 72:2255–2262

    Article  PubMed  Google Scholar 

  • Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415

    Article  PubMed  CAS  Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B Biol Sci 265:1637–1641

    Article  Google Scholar 

  • Råberg L, Nilsson J, Ilmonen P, Stjernman M, Hasselquist D (2000) The cost of an immune response: vaccination reduces parental effort. Ecol Lett 3:382–386

    Article  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    Article  PubMed  CAS  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  Google Scholar 

  • Silverin B, Fänge R, Viebke P, Westin J (1999) Seasonal changes in mass and histology of the spleen in Willow Tits Parus montanus. J Avian Biol 30:255–262

    Google Scholar 

  • Smith KG, Hunt JL (2004) On the use of spleen mass as a measure of avian immune system strength. Oecologia 138:28–31

    Article  PubMed  Google Scholar 

  • Svensson E, Raberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919

    Article  Google Scholar 

  • SPSS (2004) SPSS user’s guide. SPSS Inc., Chicago, IL

  • Stadecker M, Lukic M, Dvorak A, Leaskowitz S (1977) The cutaneous basophil response to phytohemagglutinin in chickens. J Immunol 118:1564–1568

    PubMed  CAS  Google Scholar 

  • Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol 288:345–353

    Google Scholar 

  • Viney ME, Riley EM, Buchanan KL (2005) Optimal immune responses immunocompetence revisited. Trends Ecol Evol 20:665–669

    Article  PubMed  Google Scholar 

  • Ward P, D’Cruz D (1968) Seasonal changes in the thymus gland of a tropical bird. Ibis 110:203–205

    Google Scholar 

  • Yong W, Moore FR (1997) Spring stopover of intercontinental migratory thrushes along the northern coast of the Gulf of Mexico. Auk 114:236–278

    Google Scholar 

Download references

Acknowledgments

We thank the USM Animal Research Facility staff, Juliann Rich, Rachel Bru, and Sarah Middleton, for their assistance with the care of the birds. Jeff Farrington assisted with the capture of the birds at the Fort Morgan banding station. The research was supported by funding awarded to Owen by Sigma Xi and the American Ornithologist’s Union.

Author information

Author notes

  1. Jennifer C. Owen

    Present address: Department of Fisheries and Wildlife, Michigan State University, 13 Natural Resources, East Lansing, MI, 48824, USA

Authors and Affiliations

  1. Department of Biological Sciences, University of Southern Mississippi, 118 College Avenue, Box 5018, Hattiesburg, MS, 39406, USA

    Jennifer C. Owen & Frank R. Moore

Authors
  1. Jennifer C. Owen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frank R. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer C. Owen.

About this article

Cite this article

Owen, J.C., Moore, F.R. Swainson’s thrushes in migratory disposition exhibit reduced immune function . J Ethol 26, 383–388 (2008). https://doi.org/10.1007/s10164-008-0092-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10164-008-0092-1

Keywords

Search

Navigation