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Food supplementation, but not predation risk, alters female antioxidant status during breeding

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Abstract

Predator presence and shortage of food resources can alter behavior and cause chronic physiological stress, with long-term detrimental effects on the prey. Recently, it has been hypothesized that cellular damage via oxidative stress could be associated with such effects. Variation in food availability and predation risk could modify the oxidative/antioxidant status of prey. However, data from wild populations is scarce and, importantly, the interactive effects of these major ecological factors on oxidative/antioxidant status are poorly understood. We present the first study in a wild vertebrate, addressing the combined effects of experimental food supplementation and increased predation risk (cues of Mustela erminea) on antioxidant status of female pied flycatchers (Ficedula hypoleuca). We tested the effects during breeding, assuming that such variation could modify the antioxidant cost of reproduction. Supplementary food increased female body mass, independently of predator treatment. However, timing of breeding and reproductive investment remained unaffected by the treatments. Principal component 1 (PC 1) of antioxidant levels [reflecting superoxidase dismutase (SOD), glutathione peroxidase (GPx), and glutathione (tGSH)] showed lower values in the food-supplemented than non-food-supplemented group. Neither PC 2 [reflecting catalase (CAT) and GSH/GSSG ratio] nor PC 1 was affected by predation risk, and further, predation risk did not alter the effect of supplementary food on either PC. These results suggest that food resources may have a stronger impact than predation risk on female antioxidant status during breeding. This is the first fully experimental study focusing on the interactive effects of key environmental variables on antioxidant status in wild vertebrates; more studies are however needed to understand the role of these factors in shaping the cost of reproduction.

Significance statement

Predator presence and shortage of food resources may modify animal behavior and cause chronic physiological stress response with long-term detrimental effects on the prey. Recently, it has been hypothesized that cellular damage via oxidative stress (i.e., imbalance between pro-oxidants and antioxidant defenses) could be associated with such effects, but evidence from wild populations is scarce. Importantly, the interactive effects of food and predation are not well understood. For the first time in a vertebrate, we experimentally studied the combined effects of food availability and (simulated) predation risk on antioxidant status, using wild breeding passerines. Higher food availability, but not increased perceived predation risk, lowered the antioxidant defenses. Predation risk did not alter the effect of supplementary food. The role of such interactions in shaping the cost of reproduction (via antioxidant/oxidative status) should be further studied.

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Acknowledgments

We thank Mirella Kanerva, Miia Rainio, and Janina Stauffer for instructions on the antioxidant assays and Alexandre Villers, Ryan Miller, Stefan Siivonen, and Elina Ode for extensive help in the fieldwork. We are grateful to the Ähtäri zoo for providing the material necessary for the predator treatment. We thank the associate editor and anonymous reviewers for their constructive feedback, which significantly improved the manuscript.

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Authors and Affiliations

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

    Suvi Ruuskanen, Chiara Morosinotto, Robert L. Thomson, Chaminda Pradeep Ratnayake & Erkki Korpimäki

  2. FitzPatrick Institute of African Ornithology, DST-NRF Centre of Excellence, Department of Biological Sciences, University of Cape Town, Cape Town, South Africa

    Robert L. Thomson

  3. Division of Ecology & Evolution, Research School of Biology, Australian National University, Canberra, Australia

    Chaminda Pradeep Ratnayake

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  1. Suvi Ruuskanen
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  2. Chiara Morosinotto
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  5. Erkki Korpimäki
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Correspondence to Suvi Ruuskanen.

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Ethical approval

Applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Experiments and sample collection were conducted under licenses of the Animal Experiment Committee of the State Provincial Office of Southern Finland and the Environmental Centre of Southwest Finland (license number EPOELY/456/07.01/2012).

Conflict of interest

The authors declare that they have no conflict of interest.

Data accessibility

The data will be deposited in Dryad upon acceptance.

Funding

This study was financially supported by the Academy of Finland (grant nos. 123379, 136717, and 250709 to EK, 258419 to SR), South Ostrobothnia Regional Fund of the Finnish Cultural Foundation (to CM), and Erasmus Mundus EXPERT Asia program (to CPR).

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Communicated by B. Voelkl

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Ruuskanen, S., Morosinotto, C., Thomson, R.L. et al. Food supplementation, but not predation risk, alters female antioxidant status during breeding. Behav Ecol Sociobiol 71, 69 (2017). https://doi.org/10.1007/s00265-017-2299-z

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  • DOI: https://doi.org/10.1007/s00265-017-2299-z

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