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The stress of growing old: sex- and season-specific effects of age on allostatic load in wild grey mouse lemurs

  • Physiological ecology - Original research
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Abstract

Chronic stress [i.e. long-term elevation of glucocorticoid (GC) levels] and aging have similar, negative effects on the functioning of an organism. Aged individuals’ declining ability to regulate GC levels may therefore impair their ability to cope with stress, as found in humans. The coping of aged animals with long-term natural stressors is virtually unstudied, even though the ability to respond appropriately to stressors is likely integral to the reproduction and survival of wild animals. To assess the effect of age on coping with naturally fluctuating energetic demands, we measured stress hormone output via GC metabolites in faecal samples (fGCM) of wild grey mouse lemurs (Microcebus murinus) in different ecological seasons. Aged individuals were expected to exhibit elevated fGCM levels under energetically demanding conditions. In line with this prediction, we found a positive age effect in the dry season, when food and water availability are low and mating takes place, suggesting impaired coping of aged wild animals. The age effect was significantly stronger in females, the longer-lived sex. Body mass of males but not females correlated positively with fGCM in the dry season. Age or body mass did not influence fGCM significantly in the rainy season. The sex- and season-specific predictors of fGCM may reflect the differential investment of males and females into reproduction and longevity. A review of prior research indicates contradictory aging patterns in GC regulation across and even within species. The context of sampling may influence the likelihood of detecting senescent declines in GC functioning.

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Acknowledgments

We thank Bruno Tsiverimana, Léonard Razafimanantsoa and the rest of the Kirindy research station staff, as well as Melanie Dammhahn, Eva Pechouskova, Josue Rakotoniaina and Zo Samuel Ella Fenosoa for their help in collecting data, Andrea Heistermann for conducting the hormone analyses, Peter Kappeler and Rodin Rasoloarison for their administrative and logistic support and Hanta Razafindraibe and the Département de Biologie Animale of the University of Antananarivo for their continued collaboration. Constructive comments by Pawel Koteja and two anonymous reviewers helped improve an earlier version of the manuscript. Ministère de l’Environment et des Eaux et Fôrets, MINEEF Direction des Eaux et Forêts of Madagascar and CNFEREF Morondava permitted research in Kirindy and all research was approved by the appropriate Animal Use and Care committees of Germany (Bundesministerium für Naturschutz, BfN) and complies with the applicable national laws of Madagascar. Funding was provided by the Deutsche Forschungsgemeinschaft (awarded to C.K., KR3834/1-1).

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The authors declare that they have no conflict of interest.

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All applicable institutional and/or national guidelines for the care and use of animals were followed.

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Author notes

  1. Anni Hämäläinen

    Present address: Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada

Authors and Affiliations

  1. Department of Sociobiology/Anthropology, University of Göttingen, Kellnerweg 6, 37077, Göttingen, Germany

    Anni Hämäläinen & Cornelia Kraus

  2. Behavioral Ecology and Sociobiology Unit, German Primate Center, Kellnerweg 4, 37077, Göttingen, Germany

    Anni Hämäläinen & Cornelia Kraus

  3. Endocrinology Laboratory, German Primate Center, Kellnerweg 4, 37077, Göttingen, Germany

    Michael Heistermann

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Correspondence to Anni Hämäläinen.

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Communicated by Pawel Koteja.

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Hämäläinen, A., Heistermann, M. & Kraus, C. The stress of growing old: sex- and season-specific effects of age on allostatic load in wild grey mouse lemurs. Oecologia 178, 1063–1075 (2015). https://doi.org/10.1007/s00442-015-3297-3

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  • DOI: https://doi.org/10.1007/s00442-015-3297-3

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