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The neutrophil to lymphocyte ratio indexes individual variation in the behavioural stress response of wild roe deer across fluctuating environmental conditions

  • Jeffrey CarbilletEmail author
  • Benjamin Rey
  • Typhaine Lavabre
  • Yannick Chaval
  • Joël Merlet
  • François Débias
  • Corinne Régis
  • Sylvia Pardonnet
  • Jeanne Duhayer
  • Jean-Michel Gaillard
  • A. J. M. Hewison
  • Jean-François Lemaître
  • Maryline Pellerin
  • Benoit Rannou
  • Hélène Verheyden
  • Emmanuelle Gilot-Fromont
Original Article

Abstract

Understanding how wild animals adapt to perturbations and their consequences for life history traits and population dynamics is a current focus of attention in ecology and conservation biology. Here, we analysed variation in the neutrophil to lymphocyte ratio (N:L ratio), a proxy of stress level, in wild roe deer Capreolus capreolus from three populations experiencing markedly different environmental conditions. We first assessed whether among-individual differences in the N:L ratio were consistent over time and across environmental contexts. We then investigated how both individual characteristics (behaviour at capture, age, sex, body mass), and environmental context (habitat and year quality) were linked to this indicator of stress level. We found moderate, but consistent, repeatability of the N:L ratio in all three populations, indicating stable among-individual differences in the way individuals cope physiologically with varying environmental conditions. In addition, we found a weak, but consistent, association between the N:L ratio and behaviour at capture in two of the three populations. Finally, the N:L ratio also varied in relation to temporal changes in environmental conditions. In particular, individuals had, on average, higher levels of stress in poor-quality years in two of the three populations. We discuss our results in relation to the coping styles framework.

Significance statement

Due to global change, natural populations are increasingly faced with unpredictable fluctuations of their environment. The stress response, via the release of glucocorticoids, is a key mechanism that enables individuals to cope with these variations. However, all individuals do not necessarily cope with life threatening and/or stressful situations in the same way, but as yet, the major drivers underlying variation in stress level remain unclear. We showed that the N:L ratio, reflecting baseline stress level, was repeatable and influenced by both individual and environmental factors. In particular, variation in the N:L ratio was linked to the quality of the year in terms of resource availability and, to a lesser extent, to the individual’s behaviour at capture. Our study demonstrates that both environmental context and individual characteristics drive variation in the N:L ratio in a wild vertebrate population.

Keywords

Stress Capreolus capreolus N:L ratio Environmental conditions Behaviour 

Notes

Acknowledgments

We thank all the CEFS, ONCFS staff and all the field volunteers for the organisation and their assistance during the roe deer captures. We thank the local hunting associations and the Fédération Départementale des Chasseurs de la Haute Garonne. We also thank the CEFS team, and particularly Laura Gervais, Delphine Ducros and Nicolas Morellet for constructive discussions and comments that helped to improve this manuscript. We also thank the two anonymous referees and the associate editor for their insightful comments on the manuscript.

Funding Information

The study was funded by INRA, VetAgro Sup and ONCFS, and was performed in the framework of the LABEX ECOFECT (ANR-11-LABX-0048) of Université de Lyon, within the program “Investissements d’Avenir” (ANR-11-IDEX-0007).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. For Trois-Fontaines and Chizé populations, the protocol of capture and blood sampling of roe deer under the authority of the Office National de la Chasse et de la Faune Sauvage (ONCFS) was approved by the Director of Food, Agriculture and Forest (Prefectoral order 2009-14 from Paris). All procedures were approved by the Ethical Committee of Lyon 1 University (project DR2014-09, June 5, 2014). For the Aurignac population, the study was permitted by the land manager (hunting groups and farmers) and the prefecture of the Haute Garonne. All procedures were approved by the Ethical Committee 115 of Toulouse and were authorised by the French government (APAFIS#7880-2016120209523619_v5).

Supplementary material

265_2019_2755_MOESM1_ESM.docx (15 kb)
ESM 1 (DOCX 14 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Jeffrey Carbillet
    • 1
    • 2
    Email author
  • Benjamin Rey
    • 3
  • Typhaine Lavabre
    • 4
  • Yannick Chaval
    • 1
  • Joël Merlet
    • 1
  • François Débias
    • 3
  • Corinne Régis
    • 3
  • Sylvia Pardonnet
    • 3
  • Jeanne Duhayer
    • 3
  • Jean-Michel Gaillard
    • 3
  • A. J. M. Hewison
    • 1
  • Jean-François Lemaître
    • 3
  • Maryline Pellerin
    • 5
  • Benoit Rannou
    • 2
  • Hélène Verheyden
    • 1
  • Emmanuelle Gilot-Fromont
    • 2
    • 3
  1. 1.CEFSUniversité de Toulouse, INRACastanet TolosanFrance
  2. 2.Université de Lyon, VetAgro SupMarcy-l’EtoileFrance
  3. 3.Université de Lyon, Université Lyon 1, UMR CNRS 5558Villeurbanne CedexFrance
  4. 4.Equipe de Biologie médicale-Histologie, CREFRE, Inserm-UPS-ENVTToulouseFrance
  5. 5.Office National de la Chasse et de la Faune Sauvage, Direction de la Recherche et de l’Expertise, Unité Ongulés SauvagesGièresFrance

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