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Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ridibundus) depend on the hatching order

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Abstract

Hatching asynchrony in avian species leads to age and size differences between nestlings within a brood, handicapping last-hatched chicks in the sibling rivalry. Starvation due to this competitive disadvantage has been regarded as the primary cause of an increase in mortality with hatching order. However, for gulls it has also been suggested that disease is the cause of mortality for last-hatched chicks, possibly through reduced immunocompetence and thereby an enhanced susceptibility to infection. In addition, the male-biased mortality reported for several gull species may be related to a higher vulnerability to diseases in males compared to females. To determine the potential influence of the immune system on these mortality patterns, we investigated the T-cell-mediated immunity (CMI) of black-headed gull chicks in relation to hatching order and sex. We found a significant decrease in the CMI with hatching order. This result may be causally related to systematic changes in maternal yolk steroids and carotenoids within the laying sequence. For second-laid eggs, male CMI was significantly lower than female CMI. This is possibly linked to higher plasma levels of testosterone in male embryos which might have an immunosuppressive effect. If so, this effect is masked in eggs of either high (first egg) or low (last egg) quality. Chicks with low CMI showed enhanced mortality rates. Thus the differences in immune response are likely to contribute to the observed mortality patterns. However, hatching order significantly affected mortality independently of CMI, suggesting that competitive disadvantage due to hatching asynchrony is also important.

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References

  • Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on avian T-cell mediated immune response. Can J Zool 79:101–105

    Article  Google Scholar 

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

  • Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy M (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36

    Article  CAS  PubMed  Google Scholar 

  • Blount, JD, Metcalfe, NB, Birkhead, TR, Surai, PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127

    Article  CAS  PubMed  Google Scholar 

  • Bolton M (1991) Determinants of chick survival in the lesser black-backed gull: relative contributions of egg size and parental quality. J Anim Ecol 61:949–960

    Google Scholar 

  • Bowry TR (1984) Immunology. Oxford University Press, Oxford

  • Clark AB, Wilson DS (1981) Avian breeding adaptations: hatching asynchrony, brood reduction and nest failure. Q Rev Biol 56:253–277

    Google Scholar 

  • Cramp S, Simmons KEL (eds.) (1983) The birds of the western Palearctic, vol 3. Oxford University Press, Oxford

  • Christe P, Møller AP, de Lope F (1998) Immunocompetence and nestling survival in the house martin: the tasty chick hypothesis. Oikos 83:175–179

    CAS  Google Scholar 

  • Dijkstra C, Daan S, Pen I (1998) Fledgling sex ratios in relation to brood size in size-dimorphic altricial birds. Behav Ecol 9: 287–296

    Google Scholar 

  • Duffy DL, Bentley GE, Drazen DL, Ball GF (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 11:654–662

    Article  Google Scholar 

  • Eising CM, Eikenaar C, Schwabl H, TGG Groothuis (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268:839–846

    Article  CAS  PubMed  Google Scholar 

  • Fargallo AJ, Laaksonen T, Pöyri V, Korpimäki E (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecology Lett 5: 95–101

    Article  Google Scholar 

  • Folstad I, Carter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Glutz von Blotzheim UN, Bauer KM (1982) Handbuch der Vögel Mitteleuropas, band 8. Akademische Verlagsgesellschaft, Wiesbaden

  • Goldstein H (1995) Multilevel statistical approach. Arnold, London

  • Griffiths R (1992) Sex-biased mortality in the lesser black-backed gull Larus fuscus during the nestling stage. Ibis 134:237–244

    Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    CAS  PubMed  Google Scholar 

  • Groothuis TGG, Schwabl H (2002) The influence of laying sequence and habitat characteristics on maternal yolk hormone levels. Funct Ecol 16:281–289

    Article  Google Scholar 

  • Hario M, Rudbäck E (1996) Effects of supplementary feeding on the C-egg constituents in the nominate lesser black-backed gull Larus f. fuscus. Ornis Fenn 74:167–177

    Google Scholar 

  • Hario M, Rudbäck E (1999) Dying in the midst of plenty – the third chick fate in nominate lesser black-backed gulls Larus f. fuscus. Ornis Fenn 76:71–77

    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 

  • Hõrak P, Tegelmann L, Ots I, Møller AP (1999) Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121:316–322

    Article  Google Scholar 

  • Ketterson ED, Nolan V (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154:4-25

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Google Scholar 

  • Lipar JL, ED Ketterson (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Aegelius phoeniceus. Proc R Soc Lond B 267: 2005–2010

    Article  CAS  PubMed  Google Scholar 

  • Magrath RD (1989) Hatching asynchrony and reproductive success in the blackbird. Nature 339:536–538

    Article  Google Scholar 

  • Martin, LB, Scheuerlein, A, Wikelski, M. (2002) Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs. Proc R Soc Lond B 270:153–158

    Article  Google Scholar 

  • Martinez J, Potti J, Davila JA, Blanco G (2001) Sex, immune response and hatching asynchrony in Mediterranean kestrels (Falco tinnunculus). Abstr 4th Eurasian Congr Raptors, Seville 2001

  • 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 90:327–332

    Google Scholar 

  • Müller W, Eising C, Dijkstra C, Groothuis TGG (2002) Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc R Soc Lond B 269:2249–2256

    Article  PubMed  Google Scholar 

  • Nager RG, Monaghan P, Houston DC, Genovart M (2000a) Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behav Ecol Sociobiol 48:452–457

    Article  Google Scholar 

  • Nager RG, Monaghan P, Houston DC (2000b) Within-clutch trade-offs between the number and quality of eggs; experimental manipulations in gulls. Ecology 81: 1339–1350

    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 

  • Parsons J (1975a) Asynchronous hatching and chick mortality in the herring gull Larus argentatus. Ibis 117:517–520

    Google Scholar 

  • Parsons, J (1975b) Relationship between egg size and post-hatching chick mortality in the herring gull (Larus argentatus). Nature 228:1221–1222

    Google Scholar 

  • Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001) Sex differences in avian yolk hormone levels. Nature 412:498

    Google Scholar 

  • Rasbash J, Browne W, Healy M, Cameron B, Charlton C (2000) Multilevel models project. University of London, London

  • Reid, WV (1987) Constraints on clutch size in the glaucous-winged gull. Stud Avian Biol 10:8-25

    Google Scholar 

  • Royle NJ (2000) Overproduction in the lesser black-backed gull: can marginal chicks overcome the initial handicap of hatching asynchrony? J Avian Biol 31:335–344

    Google Scholar 

  • Royle NJ, Surai PF, McCartney RJ, Speake BK (1999) Parental investment and egg yolk lipid composition in gulls. Funct Ecol 13:298–306

    Article  Google Scholar 

  • Royle NJ, Surai PF, Hartley IR (2001) Maternal derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12:381–385

    Article  Google Scholar 

  • Schantz T von, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B: 266:1-12

    Google Scholar 

  • Sayce JR, Hunt GL (1987) Sex ratios of prefledging western gulls. Auk 104:33–37

    Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450

    CAS  PubMed  Google Scholar 

  • Schwabl H (1996) Maternal testosterone in the egg enhances postnatal growth. Comp Biochem Physiol114:271–276

    Article  Google Scholar 

  • Slagsvold T (1986) Hatching asynchrony: interspecific comparisons of altricial birds. Am Nat 128:120–125

    Article  Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Article  Google Scholar 

  • Stockland JN, Amundsen, T (1988) Initial size hierarchy in broods of the shag: relative significance of egg size and hatching asynchrony. Auk 107:359–366

    Google Scholar 

  • Surai PF (1999) Vitamin E in avian reproduction. Poult Avian Biol Rev 10:1-60

    Google Scholar 

  • Tella JL, Bortolotti GR, Forero MG, Dawson RD (2000) Environmental and genetic variation in T-cell-mediated immune response of fledging American kestrels. Oecologia 123:453–459

    Article  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Williams JD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–69

    Google Scholar 

  • Woods JE, Simpson RM, Moore PL (1975) Plasma testosterone levels in the chick embryo. Gen Comp Endocrinol 27:543–547

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Jenny de Vries and Durk Venema for their help in the field. We would also like to thank Akzo Nobel Delfzijl (particularly Harry Rodenhuis) and It Fryske Gea for granting us permission to work on their properties. We also thank the referees, Corine Eising, Serge Daan and Tim Fawcett for valuable comments on the manuscript. This project was approved by the animal experimentation committee of the University of Groningen (licences DEC 2687 and DEC 2843).

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  1. Wendt Müller

    Present address: , Kerklaan 30, P.O. Box 14, 9750 AA Haren, The Netherlands

Authors and Affiliations

  1. Department of Animal Behavior, University of Groningen, Groningen, The Netherlands

    Wendt Müller, Cor Dijkstra & Ton G. G. Groothuis

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  1. Wendt Müller
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  2. Cor Dijkstra
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  3. Ton G. G. Groothuis
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Correspondence to Wendt Müller.

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Communicated by M. Webster

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Müller, W., Dijkstra, C. & Groothuis, T.G.G. Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ridibundus) depend on the hatching order. Behav Ecol Sociobiol 55, 80–86 (2003). https://doi.org/10.1007/s00265-003-0681-5

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  • DOI: https://doi.org/10.1007/s00265-003-0681-5

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