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Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation

  • Behavioural Ecology
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Abstract

The two main trade-offs considered determining reproductive patterns in iteroparous organisms are the one between current and future reproduction, and the one between the number and quality of offspring. Recently, it has been suggested that these trade-offs may be mediated by stress-induced reduction in immunocompetence. To test the hypothesis that stress reduces immune function, we investigated the effects of brood size manipulation on stress hormone levels, leukocyte profiles and immune responses against challenge with novel antigens in nestling and parent male pied flycatchers (Ficedula hypoleuca). In male parents, heterophil (H) and lymphocyte (L) numbers, as well as H/L ratio increased with experimentally enlarged brood size, and corticosterone levels tended to do so, indicating that high parental work load altered their stress level and physiological state. Despite this, we found no effects on humoral immune responsiveness, measured as antibody production against diphtheria-tetanus vaccine. In nestlings, heterophil numbers and H/L ratio increased in enlarged broods, whereas T-cell-mediated immune responsiveness, measured against phytohemagglutinin (PHA), decreased in enlarged broods. The results support the view that growth-stress-induced immunosuppression may be an important physiological pathway mediating the trade-off between the number and viability of offspring. The difference in the observed immune-related responses between nestlings and males may be because we measured different aspects of the immune system (cellular vs humoral). However, it may also be a result of males lowering their own costs by feeding less, (and their mate possibly compensate by feeding more), whereas nestlings cannot escape the costs of increased intra-brood competition.

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References

  • Apanius V (1998) Stress and immune defence. In: Møller AP, Millinski M, Slater PJB (eds) Stress and behavior: advances in the study of behavior, vol 27. Academic Press, pp 133–153

    Google Scholar 

  • Besedovsky HO, del Rey A (1996) Immune-neuro-endocrine interactions: facts and hypotheses. Endocr Rev 17:64–97

    CAS  PubMed  Google Scholar 

  • Chandra RK, Newberne PM (1977) Nutrition, immunity and infection. Plenum Press, New York

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

    Article  Google Scholar 

  • Cichoń M, Dubiec A, Chadzińska M (2001) The effect of elevated reproductive effort on humoral immune function in collared flycatcher females. Acta Oecol 22:71–76

    Article  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 

  • Gaines SD, Rice WR (1990) Analyses of biological data when there are ordered expectations. Am Nat 135:310–317

    Article  Google Scholar 

  • Gross WB, Siegel HS (1973) Effects of social stress and steroids on antibody production. Avian Dis 17:807–815

    CAS  PubMed  Google Scholar 

  • Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis 27:972–979

    CAS  PubMed  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 

  • Hawkey C, Samour HJ, Henderson GM, Hart MG (1985) Haematological findings in captive gentoo penguins (Pygoscelis papua) with bumblefoot. Avian Pathol 14:251–256

    Google Scholar 

  • Hegner RE, Wingfield JC (1987) Effects of brood size manipulations on parental investment, breeding success, and reproductive endocrinology of house sparrows. Auk 104:470–480

    Google Scholar 

  • Hemborg C (1999) Annual variation in the timing of breeding and moulting in male and female pied flycachers Ficedula hypoleuca. Ibis 141:226–232

    Google Scholar 

  • Hoffmann-Goetz L, Pedersen BK (1994) Exercise and the immune system: a model of the stress response? Immunol Today 14:382–387

    Article  Google Scholar 

  • Hõrak P, Ots I, Murumägi A (1998) Haematological health state indices of reproducing great tits: a response to brood size manipulation. Oecologia 116:441–448

    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 

  • Ilmonen P, Hakkarainen H, Koivunen V, Korpimäki E, Mullie A, Shutler D (1999) Parental effort and blood parasitism in Tengmalm's owl: effects of natural and experimental variation in food abundance. Oikos 86:79–86

    Google Scholar 

  • Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B 267:665–670

    Article  CAS  PubMed  Google Scholar 

  • Klasing KC (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77:1119–1125

    CAS  PubMed  Google Scholar 

  • Kölliker M, Brinkhof MWG, Heeb P, Fitze PS, Richner H (2000) The quantitative genetic basis of offspring solicitation and parental response in a passerine bird with biparental care. Proc R Soc Lond B 267:2127–2132

    PubMed  Google Scholar 

  • Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510

    Google Scholar 

  • Maier SF, Watkins LR, Fleshner M (1994) Psychoneuroimmunology: the interface between behavior, brain, and immunity. Am Psychol 49:1004–1017

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Moreno J, Cowie RJ, Sanz JJ, Williams RSR (1995) Differential response by males and females to brood manipulations in the pied flycatcher: energy expenditure and nestling diet. J Anim Ecol 64:721–732

    Google Scholar 

  • Moreno J, Sanz JJ, Arriero H (1999) Reproductive effort and T-lymphocyte cell-mediated immunocompetence in female pied flycatchers Ficedula hypoleuca. Proc R Soc Lond B 266:1105–1109

    Article  Google Scholar 

  • Moreno J, Sanz JJ, Merino S, Arriero H (2001) Daily energy expenditure and cell-mediated immunity in pied flycatchers: interaction with moult. Oecologia 129:492–497

    Google Scholar 

  • Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168

    PubMed  Google Scholar 

  • Nieman DC, Pedersen BK (1999) Exercise and immune function: recent developments. Sports Med 27:73–80

    CAS  PubMed  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 

  • Norris K, Anwar M, Read AF (1994) Reproductive effort influences the prevalence of haematozoan parasites in great tits. J Anim Ecol 63:601–610

    Google Scholar 

  • Oppliger A, Christe P, Richner H (1996) Clutch size and malaria resistance. Nature 381:565

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Ots I, Murumägi A, Hõrak P (1998) Haematological health state indices of reproducing Great tits: methodology and sources of natural variation. Funct Ecol 12:700–707

    Article  Google Scholar 

  • Reznick D (1992) Measuring the cost of reproduction. Trends Ecol Evol 7:42–45

    Google Scholar 

  • Richner H, Christe P, Oppliger A (1995) Paternal effort affects malaria outbreak in great tits. Proc Natl Acad Sci USA 92:1192–1194

    CAS  PubMed  Google Scholar 

  • Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New York

    Google Scholar 

  • Rose EM, Hesketh P, Ogilvie BM (1979) Peripheral blood leukocyte response to coccidial infection: a comparison of the response in rats and chickens and its correlation with resistance to reinfection. Immunology 36:71–79

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66:827–836

    Google Scholar 

  • Saino N, Calza S, Møller AP (1999) Parental care and offspring immunity. In: Adams NJ, Slotow RH (eds) Proc 22 Int Ornithol Congr, Durban. BirdLife South Africa, Johannesburg, pp 2163–2172

  • Saino N, Icagli M, Martinelli R, Møller AP (2002) Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels and sexual ornamentation. Behav Ecol 13:169–174

    Article  Google Scholar 

  • Sapolsky RM (1992) Neuroendrocrinology of the stress response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural endrocrinology. MIT Press, Cambridge, Mass., pp 287–324

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

    PubMed  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 (1982) Endocrine correlates of brood size in adult pied flycatchers Ficedula hypoleuca. Gen Comp Endrocrinol 47:18–23

    CAS  Google Scholar 

  • Sinervo B, Svensson E (1998) Mechanistic and selective causes of life-history trade-offs and plasticity. Oikos 83:432–442

    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 

  • 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 264:1593–1598

    Article  Google Scholar 

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

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

    Article  Google Scholar 

  • Verboven N, Visser ME (1998) Seasonal variation in local recruitment of great tits: the importance of being early. Oikos 81:511–524

    Google Scholar 

  • Wiehn J, Korpimäki E (1997) Food limitation on brood size: experimental evidence in the Eurasian kestrel. Ecology 78:2043-2050

    Google Scholar 

  • Wiehn J, Korpimäki E (1998) Resource levels, reproduction and resistance to haematozoan infections. Proc R Soc Lond B 265:1197–1201

    Article  Google Scholar 

  • Wiehn J, Korpimäki E, Pen I (1999) Haematozoan infections in the Eurasian kestrel: effects of fluctuating food supply and experimental manipulation of parental effort. Oikos 84:87–98

    Google Scholar 

  • Williams GC (1966) Natural selection, the cost of reproduction and refinement of Lack's principle. Am Nat 100:687–690

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Tapio Eeva, Matti Halonen, Esa Lehikoinen, Mikko Nikinmaa, Saila Sillanpää, Milla Suvanto, Lea Tegelmann, Olli Vainio, and Ismo Yli-Tuomi for help and support throughout this study. Harri Hakkarainen, Janne Henriksson, Peeter Hõrak, Erkki Korpimäki, and Olli Vainio provided constructive comments on previous drafts of this manuscript. Financial support was provided by the Academy of Finland (to Erkki Korpimäki, J.W., and P.I.), the Jenny and Antti Wihuri Foundation, and the Kone Foundation to P.I., Formas/SJFR, Carl Tryggers Stiftelse, and Crafoordska Stiftelsen to D.H. The study was conducted with the permission of the South West Finland Regional Environment Center (0299L0299-254).

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  1. Petteri Ilmonen

    Present address: Department of Biology, University of Utah, 257 S. 1400 E., Salt Lake City, UT 84132, USA

Authors and Affiliations

  1. Section of Ecology, Department of Biology, University of Turku, 20014 , Turku, Finland

    Petteri Ilmonen & Jürgen Wiehn

  2. Department of Animal Ecology, Ecology Building, 223 62, Lund, Sweden

    Dennis Hasselquist & Åsa Langefors

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  1. Petteri Ilmonen
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Correspondence to Petteri Ilmonen.

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Ilmonen, P., Hasselquist, D., Langefors, Å. et al. Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136, 148–154 (2003). https://doi.org/10.1007/s00442-003-1243-2

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