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Physiological pace of life: the link between constitutive immunity, developmental period, and metabolic rate in European birds

  • Physiological ecology - Original research
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Abstract

Constitutive innate immunity is the first lined of defence against infections, but the causes determining its variability among species are poorly understood. The pace of life hypothesis predicts that species with a fast speed of life, characterized by high energy turnover and short developmental time, invest relatively little in defence in favour of growth and early reproduction, whereas ‘slow-living’ species are predicted to invest more resources into costly defence. We conducted phylogenetic comparative analysis on 105 European bird species and determined that the number of leukocytes, and the levels of natural antibodies (NAbs) and complement, measured on adult birds, increased or tended to positively correlate with the length of incubation period. However, we found that the length of incubation and fledging periods have opposite effects on immune defence (i.e. immune parameters show a negative association with the length of fledging period). Our results suggest that the contrasting effects of the incubation and fledging periods are related to the timing of the development of immune cells and of NAbs and complement, which largely mature during the embryonic phase of development. In support of this hypothesis, we found that species with a long relative incubation period [i.e. whose total pre-fledging developmental time (incubation plus fledging) consists largely of the incubation period] invested more in constitutive innate immunity. Finally, in support of the pace of life hypothesis, for a subsample of 63 species, we found that the basal metabolic rate significantly or tended to negatively correlate with immune measures.

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Acknowledgments

During fieldwork, we enjoyed the faithful help accorded by Z. Benkő, T. Rácz, A. Fülöp, S. Daróczi, A. Stermin, A. Marton, L. Bărbos, K. Sándor, I. Kovács, T. Miholcsa, E. Szöllősi, A. Fenesi and E. Ruprecht. We thank the administration of the Botanical Garden of Cluj Napoca for permission to capture birds. We are grateful to J. Tökölyi and L. Z. Garamszegi who kindly helped us with the statistical analyses and data collection, and to A. Liker, T. Székely and G. Sorci for their constructive comments on an earlier version of the manuscript. L. Eberhart-Phillips kindly helped us with correcting the English. The comments given by three reviewers on a previous version of the manuscript greatly improved the quality of this study. This work was carried out with permission from the Romanian Academy of Sciences and adhered to recommended practices for the ringing, measuring and sampling of wild birds for research purposes. The research of P. L. P. was supported by TÁMOP-4.2.4.A/2-11/1-2012-0001 National Excellence Program, and C. I. V. was supported by TÁMOP-4.2.2/B-10/1-2010-0024. These projects were sponsored by the European Union and the State of Hungary, and co-financed by the European Social Fund. The research infrastructure was supported by a research grant (PN II. RU TE 291/2010) of the Romanian Ministry of Education and Research. C. I. V. is financed by a post-doctoral grant (GTC 34062/2013) of the Babeş-Bolyai University. G. Á. C. was supported by the Leibniz Institute for Zoo and Wildlife Research Berlin.

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Authors and Affiliations

  1. MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology and Human Biology, University of Debrecen, Egyetem tér 1, 4032, Debrecen, Hungary

    Péter László Pap, Csongor István Vágási & Orsolya Vincze

  2. Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeş-Bolyai University, Clinicilor Street 5-7, 400006, Cluj Napoca, Romania

    Péter László Pap, Csongor István Vágási, Orsolya Vincze, Gergely Osváth & Judit Veres-Szászka

  3. Museum of Zoology, Babeş-Bolyai University, Clinicilor Street 5-7, 400006, Cluj Napoca, Romania

    Gergely Osváth

  4. Department of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

    Gábor Árpád Czirják

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  1. Péter László Pap
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  2. Csongor István Vágási
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  3. Orsolya Vincze
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  5. Judit Veres-Szászka
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  6. Gábor Árpád Czirják
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Correspondence to Péter László Pap.

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Communicated by Pawel Koteja.

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Pap, P.L., Vágási, C.I., Vincze, O. et al. Physiological pace of life: the link between constitutive immunity, developmental period, and metabolic rate in European birds. Oecologia 177, 147–158 (2015). https://doi.org/10.1007/s00442-014-3108-2

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