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Fasting affects amino acid nitrogen isotope values: a new tool for identifying nitrogen balance of free-ranging mammals

  • Physiological ecology – original research
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Abstract

Changes in the nutritional status of free-ranging animals have a strong influence on individual fitness, yet it remains challenging to monitor longitudinally. Nitrogen (δ15N) and carbon (δ13C) isotope values measured chronologically along the length of metabolically inert keratinous tissues can be used as a nutritional biomarker to retrospectively reconstruct the foraging ecology and eco-physiology of consumers. We quantitatively describe the physiological effects of fasting on amino acid metabolism using sequentially measured bulk tissue and amino acid δ15N values along the length of whiskers sampled from free-ranging juvenile, subadults, adult female, and male southern elephant seals (SES; Mirounga leonina) on Marion Island in the Southern Ocean. For both juveniles and adult females, whisker segments representing fasting had significantly higher bulk tissue δ15N values of 0.6 ± 0.5‰ and 1.3–1.8‰, respectively, in comparison to segments unaffected by fasting. We also found a large increase (2–6‰) in δ15N values for most glucogenic amino acids and a simultaneous depletion (2–3‰) of alanine in segments reflecting fasting, which enabled us to accurately predict (74%) the nutritional status of our model species. We hypothesize that the glucose-alanine cycle is the mechanism driving the observed depletion of alanine δ15N values during fasting. We demonstrated that keratinaceous tissues can be used as a longitudinal nutritional biomarker to detect changes in the nitrogen balance of an individual. Moreover, it is evident that physiological factors have an important influence on tissue δ15N values and can lead to erroneous bulk tissue or amino acid isotope-based reconstructions of foraging habits.

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Acknowledgements

The Animal Use and Care Committee (AUCC) of the Faculty of Veterinary Science, University of Pretoria, provided ethical clearance for the research under AUCC 040827-022, AUCC 040827-023, EC030602-016, and EC077-15. We thank Prof Dan Costa (University of California, Santa Cruz, USA) for his vital role with the sample handling [National Marine Fisheries Service (NMFS), National Oceanic and Atmospheric Administration (NOAA) Permit number 19439]. The National Research Foundation (NRF) (Grant no. SFH14070373490) funded the research and supported N. Lübcker through an Innovation Scholarship. The ‘Society for Marine Mammalogy (SMM) Small Grant in Aid of Research’ provided additional support for the sample analyses. The conclusions drawn are attributed to the authors and not necessarily to the NRF and SMM. Logistical support was provided by the Department of Environmental Affairs under the South African National Antarctic Program (SANAP). We express our sincerest gratitude towards the staff and colleagues at the University of New Mexico Center for Stable Isotopes (Albuquerque, NM, USA) for their support, with a special mention for Dr. Viorel Atudorei and Emma Elliot Smith, as well as to Dr. Grant Hall, Nicolas Prinsloo, Michael Mole, and André van Tonder and field personne from the University of Pretoria, South Africa. Lastly, we thank the reviewers for their time and valuable contributions.

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Authors and Affiliations

  1. Department of Zoology and Entomology, Mammal Research Institute, University of Pretoria, Private Bag X20, Hatfield, 0028, South Africa

    Nico Lübcker & P. J. Nico de Bruyn

  2. Department of Biological Sciences, Old Dominion University, Norfolk, VA, 23529, USA

    John P. Whiteman

  3. Centre for Neuroendocrinology and Department of Immunology, Faculty of Health Sciences, University of Pretoria, Pretoria, 0001, South Africa

    Robert P. Millar

  4. Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA

    John P. Whiteman & Seth D. Newsome

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  1. Nico Lübcker
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  4. P. J. Nico de Bruyn
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Contributions

NL, SDN, RPM, JPW, and PJNdB conceived and designed the experiments. PJNdB, JPW, SDN, and RPM enabled sample collection and sample analyses. NL and JW analysed the data. NL wrote the manuscript; other authors provided editorial advice.

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Correspondence to Nico Lübcker.

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All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Communicated by Helene Marsh.

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Lübcker, N., Whiteman, J.P., Millar, R.P. et al. Fasting affects amino acid nitrogen isotope values: a new tool for identifying nitrogen balance of free-ranging mammals. Oecologia 193, 53–65 (2020). https://doi.org/10.1007/s00442-020-04645-5

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