Skip to main content
SpringerLink
Log in

Serum immunoglobulin G levels are positively related to reproductive performance in a long-lived seabird, the common tern (Sterna hirundo)

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The evolution of longevity requires a low risk of mortality from extrinsic factors, relative to intrinsic factors, so that individuals that differentially invest in physiological self-maintenance and minimize their annual reproductive costs will maximize lifetime fitness through a prolonged reproductive lifespan. The trade-off between reproductive effort and self-maintenance, as measured by immune function, has been well documented in short-lived birds, but is difficult to demonstrate in long-lived birds. To assess self-maintenance in a long-lived seabird, we measured serum protein levels, including immunoglobulin G (IgG = IgY), in 30 breeding pairs of common terns (Sterna hirundo) and their first-hatched (A) chicks. Most parents were of known age from banding as hatchlings; our sample was selected to contrast young breeders (6–9 years) with very old birds (17–23 years). Body-mass of the parents declined by 5% during the chick-rearing period, while serum protein levels were stable. Serum IgG levels were higher in parents of offspring with faster growth rates, while IgG levels were lower in parents whose broods were reduced by starvation. A-chicks in broods of two had higher IgG levels than singleton chicks. Albumin levels were not related to reproductive performance. Thus, despite adequate statistical power, we could find no evidence for a trade-off between reproduction and self-maintenance in common terns, even in old age. The results are consistent with life-history predictions for long-lived vertebrates, in which selection favors sustained self-maintenance across the reproductive lifespan. The positive relationships between IgG levels and reproductive performance indicate that IgG can be used as an index of parental “quality.”

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

  • Apanius V, Temple SA, Bale M (1983) Serum proteins of wild turkey vultures (Cathartes aura). Comp Biochem Physiol 76B:907–913

    CAS  Google Scholar 

  • Apanius V (1998) Ontogeny of immune function. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial–precocial spectrum. Oxford University Press, Oxford, pp 203–222

    Google Scholar 

  • Apanius V, Nisbet ICT (2003) Serum immunoglobulin G levels in very old common terns Sterna hirundo. Exp Gerontol 38:761–764

    Article  PubMed  CAS  Google Scholar 

  • Arnold JM, Hatch JJ, Nisbet ICT (2004) Seasonal declines in reproductive success of the common tern: timing or parental quality? J Avian Biol 35:33–45

    Article  Google Scholar 

  • Barnard C, Behnke J, Sewell J (1994) Social behaviour and susceptibility to infection in house mice (Mus musculus): effects of group size, aggressive behaviour and status-related hormonal responses prior to infection on resistance to Babesia microti. Parasitology 108:487–496

    PubMed  CAS  Google Scholar 

  • Benner R, van Oudenaren A, Björklund M, Ivars F, Holmberg D (1982) ‘Background’ immunoglobulin production: measurement, biological significance and regulation. Immunol Today 3:243–249

    Article  Google Scholar 

  • Bollinger PB (1994) Relative effects of hatching order, egg-size variation, and parental quality on chick survival in common terns. Auk 111:263–273

    Google Scholar 

  • Bond C, Gilbert P (1958) Comparative study of blood volume in representative aquatic and non-aquatic birds. Am J Physiol 194:519–521

    PubMed  CAS  Google Scholar 

  • Bridge E, Nisbet ICT (2004) Wing molt and assortative mating in common terns: a test of the molt-signaling hypothesis. Condor 106:336–343

    Article  Google Scholar 

  • Cam E, Link WA, Cooch EG, Monnat JY, Danchin E (2002) Individual covariation in life-history traits: seeing the trees despite the forest. Am Nat 159:96–105

    Article  PubMed  Google Scholar 

  • Cam E, Monnat JY (2000) Stratification based on reproductive state reveals contrasting patterns of age-related variation in demographic parameters in the kittiwake. Oikos 90:560–574

    Article  Google Scholar 

  • Cichon M, Sendecka J, Gustafsson L (2003) Age-related decline in humoral immune function in collared flycatchers. J Evol Biol 16:1205–1210

    Article  PubMed  CAS  Google Scholar 

  • Christe P, Møller AP, Saino N, de Lope F (2000) Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird (Delichon urbica) (the house martin). Heredity 85:75–83

    Article  PubMed  Google Scholar 

  • Christe P, de Lope F, Gonzalez G, Saino N, Møller AP (2001) The influence of environmental conditions on immune responses, morphology and recapture probability of nestling house martins (Delichon urbica). Oecologia 126:333–338

    Article  Google Scholar 

  • Coulson JC, Thomas CS (1985) Differences in the breeding performance of individual kittiwake gulls (Rissa tridactyla). In: Sibly RM, Smith RH (eds) Behavioural ecology. Blackwell Scientific Publications, Oxford, pp 489–503

    Google Scholar 

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

    Article  Google Scholar 

  • de Lope F, Møller AP, de la Cruz C (1998) Parasitism, immune response and reproductive success in the house martin Delichon urbica. Oecologia 114:188–193

    Article  Google Scholar 

  • DeVries AC, et al (1997) Stress affects corticosteroid and immunoglobulin concentrations in male house mice (Mus musculus) and prairie voles (Microtus ochrogaster). Comp Biochem Physiol A 118:655–663

    Article  CAS  Google Scholar 

  • Doumas B, Watson W, Biggs H (1971) Albumin standards and the measurement of serum albumin with bromcresol green. Clin Chim Acta 1:87–96

    Article  Google Scholar 

  • Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    PubMed  Google Scholar 

  • Eising CM, Groothuis TGG (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66:1027–1034

    Article  Google Scholar 

  • Fudge AM (2000) Avian blood sampling and artifact considerations. In: Fudge AM (ed) Laboratory medicine: avian and exotic pets. WB Saunders, Philadelphia, pp 1–8

    Google Scholar 

  • Gustafsson L, Pärt T (1990) Acceleration of senescence in the collared flycatcher Ficedula albicollis by reproductive costs. Nature 347:279–281

    Article  Google Scholar 

  • Hamer KC, Schreiber E, Burger J (2002) Breeding biology, life histories and life history-environment interactions in seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, FL, pp 217–261

    Google Scholar 

  • 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 

  • Holmes DJ, Ottinger MA (2003) Birds as long-lived animal models for the study of aging. Exp Gerontol 38:1365–1375

    Article  PubMed  CAS  Google Scholar 

  • Hõrak P, Jenni ES, Ots I, Tegelmann L (1998) Health and reproduction: the sex-specific clinical profile of great tits (Parus major) in relation to breeding. Can J Zool 76:2235–2244

    Article  Google Scholar 

  • Kaneko J (1997) Serum proteins and the dysproteinemias. In: Kaneko J, Harvey J, Bruss M (eds) Clinical biochemistry of domestic animals, 5th edn. Academic Press, New York, pp 117–138

    Google Scholar 

  • Kitaysky AS, Piatt JF, Wingfield JC (1999) The adrenocortical stress-response of black-legged kittiwakes chicks in relation to dietary restrictions. J Comp Physiol B 169:303–310

    Article  CAS  Google Scholar 

  • Kitaysky AS, Wingfield JC, Piatt JF (2001) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav Ecol 12:619–625

    Article  Google Scholar 

  • Klasing K (1998) Comparative avian nutrition. CAB International, New York

    Google Scholar 

  • Kowalczyk K, Daiss J, Halpern J, Roth TF (1985) Quantitation of maternal-fetal IgG transport in the chicken. Immunology 54:755–762

    PubMed  CAS  Google Scholar 

  • Kuhlmann-Rabens I, Wanke R, Storandt F, Altmann B, Losch U, Merkenschlager M (1987) Attempts to localize the defect in dysgammaglobulinemia of UM-B19 chickens by studying the effect of immunomodulating substances on immunoglobulin and antibody production. Vet Immunol Immunopathol 14:123–143

    Article  PubMed  CAS  Google Scholar 

  • Lee K, Klasing K (2004) A role for immunology in invasion biology. Trends Ecol Evol 19:523–529

    Article  PubMed  Google Scholar 

  • Lemke H, Coutinho A, Lange H (2004) Lamarckian inheritance of somatically acquired maternal IgG phenotypes. Trends Immunol 25:180–186

    Article  PubMed  CAS  Google Scholar 

  • Leslie G, Clem L (1970) Chicken immunoglobulins: biological half-lives and normal adult serum concentrations of IgM and IgY. Proc Soc Exp Biol Med 134:195–198

    PubMed  CAS  Google Scholar 

  • Leveille G, Sauberlich H (1961) Influence of dietary protein level on serum protein components and cholesterol in the growing chick. J Nutr 74:500–504

    CAS  Google Scholar 

  • Littell RC, Pendergast J, Natarajan R (2000) Modelling covariance structure in the analysis of repeated measures data. Stat Med 2000:1793–1819

    Article  Google Scholar 

  • Lung N, Thompson J, Kollias G, Olsen J, Zdziarski J, Klein P (1996) Maternal immunoglobulin G antibody transfer and development of immunoglobulin G antibody responses in blue and gold Macaw (Ara ararauna) chicks. Am J Vet Res 57:1162–1167

    PubMed  CAS  Google Scholar 

  • Mills JA (1989) Red-billed gull. In: Newton I (ed) Lifetime reproductive success. Academic Press, London, pp 387–404

    Google Scholar 

  • Møller AP, de Lope F (1999) Senescence in a short-lived migratory bird: age-dependent morphology, migration, reproduction and parasitism. J Anim Ecol 68:163–171

    Article  Google Scholar 

  • Moreno J (2003) Lifetime reproductive success in seabirds: interindividual differences and implications for conservation. Sci Mar 67(Suppl. 2):7–12

    Google Scholar 

  • Nisbet ICT (2001) Detecting and measuring senescence in wild birds: experience with long-lived seabirds. Exp Gerontol 36:833–843

    Article  PubMed  CAS  Google Scholar 

  • Nisbet ICT (2002) Common tern (Sterna hirundo). In: Poole A, Gill F (eds) The birds of North America, No. 618. The Birds of North America Inc., Philadelphia

    Google Scholar 

  • Nisbet ICT, Cam E (2002) Test for age-specificity in survival of the common tern. J Appl Stat 29:65–83

    Article  MathSciNet  Google Scholar 

  • Nisbet ICT, Apanius V, Friar MS (2002a) Breeding performance of very old common terns. J Field Ornithol 73:117–124

    Google Scholar 

  • Nisbet ICT, Finch CE, Thompson N, Russek-Cohen E, Proudman JA, Ottinger MA (1999) Endocrine patterns during aging in the common tern (Sterna hirundo). Gen Comp Endocrinol 114:279–286

    Article  PubMed  CAS  Google Scholar 

  • Nisbet ICT, Montoya JP, Burger J, Hatch JJ (2002b) Use of stable isotopes to investigate individual differences in diets and mercury exposures among common terns Sterna hirundo in breeding and wintering grounds. Mar Ecol Prog Ser 242:267–274

    Article  CAS  Google Scholar 

  • Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc Lond B 265:1291–1298

    Article  Google Scholar 

  • Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262

    Article  PubMed  CAS  Google Scholar 

  • Nur N (1984a) The consequences of brood size for breeding blue tits I Adult survival, weight change and the cost of reproduction. J Anim Ecol 53:479–496

    Article  Google Scholar 

  • Nur N (1984b) The consequences of brood size for breeding blue tits II Nestling weight, offspring survival and optimal brood size. J Anim Ecol 53:497–517

    Article  Google Scholar 

  • O’Brien P, Aitken R (2002) Antibody phage display: methods and protocols. Humana Press, Totowa

    Google Scholar 

  • Rees MJ, Nordskog AW (1981) Genetic control of serum immunoglobulin G levels in the chicken. J Immunogenet 8:425–431

    Article  PubMed  CAS  Google Scholar 

  • Rehder NB, Bird DM, Lague PC (1982) Variations in blood packed cell volume of captive American kestrels. Comp Biochem Physiol 72A:105–109

    Article  Google Scholar 

  • Ricklefs RE (1992) The roles of parent and chick in determining feeding rates in Leach’s storm-petrel. Anim Behav 43:895–906

    Article  Google Scholar 

  • Ricklefs RE (2000) Intrinsic aging-related mortality in birds. J Avian Biol 31:103–111

    Article  Google Scholar 

  • Ros AFH, Groothuis TGG, Apanius V (1997) The relationship between gonadal steroids, immunocompetence, body mass, and behavior in young black-headed gulls (Larus ridibundus). Am Nat 150:201–219

    Article  PubMed  CAS  Google Scholar 

  • Roskaft E (1985) The effect of enlarged brood size on the future reproductive potential of the rook. J Anim Ecol 54:255–260

    Article  Google Scholar 

  • Rowe D, McGregor I, Smith SJ (1968) Plasma immunoglobulin concentrations in a West African (Gambian) community and in a group of healthy British adults. Clin Exp Immunol 3:63–79

    PubMed  CAS  Google Scholar 

  • Sabbele N, van Oudenaren A, Benner R (1983) The effect of corticosteroids upon the number and organ distribution of ‘background’ immunoglobulin-secreting cells in mice. Cell Immunol 77:308–317

    Article  PubMed  CAS  Google Scholar 

  • Sabiston B, Ste Rose J (1976) Effect of cold exposure on the metabolism of immunoglobulins in rabbits. J Immunol 116:106–111

    PubMed  CAS  Google Scholar 

  • Sæther BE, Andersen R, Pedersen HC (1993) Regulation of parental effort in a long-lived seabird—an experimental manipulation of the cost of reproduction in the Antarctic petrel, Thalassoica antarctica. Behav Ecol Sociobiol 33:147–150

    Article  Google Scholar 

  • Saino N, Bolzern AM, Møller AP (1997) Immunocompetence, ornamentation, and viability of male barn swallows (Hirundo rustica). Proc Nat Acad Sci U S A 94:549–552

    Article  CAS  Google Scholar 

  • Saino N, Martinelli R, Møller AP (2001a) Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica). J Evol Biol 14:95–109

    Article  CAS  Google Scholar 

  • Saino N, Incagli M, Martinelli R, Ambrosini R, Møller AP (2001b) Immunity, growth and begging behaviour of nestling barn swallows Hirundo rustica in relation to hatching order. J Avian Biol 32:263–270

    Article  Google Scholar 

  • Saino N, Ambrosini R, Martinelli R, Møller AP (2002) Mate fidelity, senescence in breeding performance and reproductive trade-offs in the barn swallow. J Anim Ecol 71:309–319

    Article  Google Scholar 

  • Saino N, Ferrari RP, Romano M, Rubolini D, Møller AP (2003) Humoral immune response in relation to senescence, sex and sexual ornamentation in the barn swallow (Hirundo rustica). J Evol Biol 16:1127–1134

    Article  PubMed  CAS  Google Scholar 

  • Sanz JJ, Moreno J (2000) Delayed senescence in a southern population of the pied flycatcher (Ficedula hypoleuca). Ecoscience 7:25–31

    Google Scholar 

  • Sarker N, Tsudzuki M, Nishibori M, Yamamoto Y (1999) Direct and correlated response to divergent selection for serum immunoglobulin M and G levels in birds. Poult Sci 78:1–7

    PubMed  CAS  Google Scholar 

  • Sarker N, Tsudzuki M, Nishibori M, Yasue H, Yamamoto Y (2000) Cell-mediated and humoral immunity and phagocytic ability in chicken lines divergently selected for serum immunoglobulin M and G levels. Poult Sci 79:1705–1709

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Solomon JB (1970) Unification of foetal and neonatal immunology. Nature 227:895–897

    Article  PubMed  CAS  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Szep T, Møller AP (1999) Cost of parasitism and host immune defence in the sand martin (Riparia riparia): a role for parent-offspring conflict? Oecologia 119:9–15

    Article  Google Scholar 

  • Tims J, Nisbet ICT, Friar MS, Mostello C, Hatch JJ (2004) Characteristics and performance of common terns in old and newly-established colonies. Waterbirds 27:321–332

    Article  Google Scholar 

  • Waldmann T, Blaese R, Strober W (1970) Physiological factors controlling immunoglobulin metabolism. In: Rothschild M, Waldmann T (eds) Plasma protein metabolism: regulation of synthesis, distribution, and degradation. Academic Press, New York, pp 269–286

    Google Scholar 

  • Warr GW, Magor KE, Higgins DA (1995) IgY: clues to the origins of modern antibodies. Immunol Today 16:392–398

    Article  PubMed  CAS  Google Scholar 

  • Wendeln H, Becker PH (1996) Body mass change in breeding common terns Sterna hirundo. Bird Study 43:85–95

    Article  Google Scholar 

  • Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

    Google Scholar 

Download references

Acknowledgments

We thank Suzanne Conlon, Margaret Friar, Tim Meehan, and Jeremy Hatch for help in the field in 1999, many other colleagues and assistants for banding chicks since 1976, and the Town of Marion for permission to work at Bird Island. Laboratory analyses were assisted by P. Scipio, Y. Sanchez, D. Rodriguez, and Y. Tran and supported by NIH-MBRS (GM61347). This research was approved by institutional, state, and federal agencies for compliance with animal welfare and migratory bird regulations.

Author information

Authors and Affiliations

  1. Department of Biology, Wake Forest University, PO Box 7325, Winston Salem, NC, 27109, USA

    Victor Apanius

  2. I.C.T. Nisbet & Company, 150 Alder Lane, North Falmouth, MA, 02556, USA

    Ian C.T. Nisbet

Authors
  1. Victor Apanius
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ian C.T. Nisbet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor Apanius.

Additional information

Communicated by Carol Vleck

Rights and permissions

Reprints and permissions

About this article

Cite this article

Apanius, V., Nisbet, I.C. Serum immunoglobulin G levels are positively related to reproductive performance in a long-lived seabird, the common tern (Sterna hirundo). Oecologia 147, 12–23 (2006). https://doi.org/10.1007/s00442-005-0238-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-005-0238-6

Keywords

Search

Navigation