Abstract
Oxidative stress occurs when reactive oxygen species (ROS) exceed antioxidant defences, which can have deleterious effects on cell function, health and survival. Therefore, organisms are expected to finely regulate pro-oxidant and antioxidant processes. ROS are mainly produced through aerobic metabolism and vary in response to changes in energetic requirements, whereas antioxidants may be enhanced, depleted or show no changes in response to changes in ROS levels. We investigated the repeatability, within-individual variation and correlation across different conditions of two plasmatic markers of the oxidative balance in 1108 samples from 635 free-living adult collared flycatchers (Ficedula albicollis). We sought to manipulate energy constraints by increasing wing load in 2012 and 2013 and by providing additional food in 2014. We then tested the relative importance of within- and between-individual variation on reactive oxygen metabolites (ROMs), a marker of lipid and protein peroxidation, and on non-enzymatic antioxidant defences (OXY test). We also investigated whether the experimental treatments modified the correlation between markers. Antioxidant defences were repeatable (range of repeatability estimates = 0.128–0.581), whereas ROMs were not (0–0.061). Antioxidants varied neither between incubation and nestling feeding nor between sexes. ROMs increased from incubation to nestling feeding in females and were higher in females than males. Antioxidant defences and ROM concentration were globally positively correlated, but the correlation varied between experimental conditions and between years. Hence, the management of oxidative balance in wild animals appears flexible under variable environmental conditions, an observation which should be confirmed over a wider range of markers.
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Data availability
The datasets, the R script and the results of the MCMC sampling generated during the current study are available in the figshare repository (Récapet et al. 2019; https://doi.org/10.6084/m9.figshare.7813457.v1).
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Acknowledgements
Many thanks to the landowners of Gotland for access to the study sites; to Lars Gustafsson for logistics on the field; to fifteen students and field assistants for their contribution to fieldwork; to François Criscuolo for his help designing the study and his comments on this manuscript; to Holger Schielzeth and Pierre de Villemereuil for their advice on adjusting repeatability and correlation estimates for measurement error and to Alan A. Cohen, David Costantini and anonymous reviewers for their comments on previous versions of this manuscript. This work was supported by the French National Center for Scientific Research (PICS France–Switzerland to B.D.); the French Ministry of Research (PhD fellowship to C.R.); the University of Aberdeen (stipend to C.R.); the L’Oréal Foundation-UNESCO “For Women in Science” program (fellowship to C.R.); the Région Rhône-Alpes (Explora’doc mobility Grant to C.R.); the Fédération de Recherche 41 BioEnvironnement et Santé (training Grant to CR); the Rectors’ Conference of the Swiss Universities (joint doctoral program Grant to C.R.) and the Fondation pour l’Université de Lausanne (exchange Grant to C.R.); and the Journal of Experimental Biology (travel Grant to CR).
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CR, BD and PB designed the study. CR carried out the fieldwork. CR and MA performed the laboratory analyses and analysed the data. CR, BD and PB drafted the manuscript and MA reviewed it for substantial content. All authors gave final approval for publication.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Permission for catching and ringing adult and young birds was granted by the Ringing Centre from the Museum of Natural History in Stockholm (license number 471:M009 to C.R.). Permission for blood taking and experimental procedures was granted by the Ethical Committee for Experiments on Animals in Sweden (license number C 108/7).
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Appendix
Appendix
Correlation between markers of oxidative balance and nutritional state in the plasma
In 2014, the concentrations of triglycerides, glucose and lactate were measured in whole blood immediately after blood taking using a portable test strip reader designed for point-of-care measures in humans (Accutrend, Roche Diagnostics), whereas antioxidant capacity and ROM concentrations were measured through the OXY and d-ROMs tests, following the protocol described in the main text. Individuals were only measured once. The quantity of blood deposited on the test strip was 10 µL for triglycerides and glucose and 15 µL for lactate. ROM concentrations were not significantly correlated with triglycerides (Spearman’s rank correlation test: ρ = − 0.01, N = 76, S = 74,136, P = 0.91), lactate (ρ = 0.18, N = 19, S = 937, P = 0.47), or glucose concentration (ρ = − 0.37, N = 20, S = 1817, P = 0.11). There was no correlation between the total antioxidant capacity of the plasma and triglycerides (ρ = − 0.16, N = 93, S = 155,677, P = 0.12), lactate (ρ = 0.30, N = 21, S = 1072, P = 0.18) or glucose concentrations (ρ = − 0.09, N = 24, S = 2510, P = 0.67) either.
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Récapet, C., Arrivé, M., Doligez, B. et al. Antioxidant capacity is repeatable across years but does not consistently correlate with a marker of peroxidation in a free-living passerine bird. J Comp Physiol B 189, 283–298 (2019). https://doi.org/10.1007/s00360-019-01211-1
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DOI: https://doi.org/10.1007/s00360-019-01211-1