Assessing seasonal changes in animal diets with stable-isotope analysis of amino acids: a migratory boreal songbird switches diet over its annual cycle
Tools to study seasonal changes in animal diets are needed to address a wide range of ecological questions. This is especially true of migratory animals that experience distinct environments where diets may be substantially different. However, tracking diets of individuals that move vast distances has proven difficult. Compound-specific isotope analysis has emerged as a valuable tool to study diets but has been little used to study dietary changes of migratory animals. Using this technique, we quantify seasonal variation in the annual diet of a migratory songbird (gray-cheeked thrush, Catharus minimus) and test the hypothesis that migrants change their diet in response to the energetic requirements of different periods of the annual cycle. By measuring δ13C and δ15N values of amino acids from feathers grown on the breeding grounds, blood formed during migration and claw grown on the wintering grounds, we found that migration is associated with greater consumption of fruit, compared to the breeding or wintering periods. This was confirmed by the lower trophic position of blood compared to feather and claw, by a decrease in the δ15N value of the source amino acid phenylalanine in blood as a function of days of stopover, and by the positive correlation between δ15N and δ13C values of phenylalanine in blood, and not in feather or claw. This study illustrates how isotopic analysis of amino acids can contribute to understand food webs, seasonal dietary changes and metabolic routing of nutrients in migratory animals.
KeywordsAmino acids Compound specific δ13C and δ15N Dietary routing Food web Gray-cheeked thrush Migration Trophic position
We thank Natalie Wallsgrove for her training and help in the lab, and Nick Bayly, Jeyson Sanabria, Laura Céspedes and Paulo Pulgarín for their support in the field. We also thank Nathan Cooper, Seth Newsome and two anonymous reviewers for their comments, which helped us improve previous versions of this manuscript. All applicable institutional and/or national guidelines for the care and use of animals were followed. This is SOEST Contribution number 10332.
Author contribution statement
CG, BP, KAH and CDC designed the study and CG collected the samples. CG, TL and KH ran laboratory analyses. CG analyzed the data, led the writing of the manuscript and all authors contributed critically to the drafts and gave approval for publication.
This study was funded by a ‘research in residence’ award from the University of Utah (NSF award #1137336 for inter-university training in continental-scale ecology), by Colciencias (‘Ciencias Básicas’ Grant no. 658), by the Universidad de Los Andes (Proyecto Semilla) and by a Memorial fund Grant from the Eastern Bird Banding Association. TL was supported by the DFG funded Cluster of Excellence 80 “The Future Ocean”.
- BirdLife International (2017) Species factsheet: Catharus minimus. Downloaded from http://www.birdlife.org on 31/01/2017. http://datazone.birdlife.org/species/factsheet/grey-cheeked-thrush-catharus-minimus/distribution. Accessed 31 Jan 2017
- Chikaraishi Y, Ogawa N, Ohkouchi N (2010) Further evaluation of the trophic level estimation based on nitrogen isotopic composition of amino acids. In: Ohkouchi N, Tayasu I, Koba K (eds) Earth, life, isotopes. Kyoto University Press, Kyoto, pp 37–51Google Scholar
- Fernandes R, Millard AR, Brabec M et al (2014) Food reconstruction using isotopic transferred signals (FRUITS): a Bayesian model for diet reconstruction. PLoS ONE 9:1–9Google Scholar
- Hobson KA (2005) Flying Fingerprints. In: Greenberg R, Marra PP (eds) Birds of two worlds. The ecology and evolution of migration. Johns Hopkins University Press, Baltimore, pp 235–247Google Scholar
- Hutto RL (1990) Studies of foraging behavior: central to understanding the ecological consequences of variation in food abundance. Stud Avian Biol 13:389–390Google Scholar
- Lowther PE, Rimmer CC, Kessel B et al (2001) Gray-cheeked thrush (Catharus minimus). In: Birds of North America. https://birdsna.org/Species-Account/bna/species/gycthr. Accessed 8 Feb 2013
- Nisbet ICT, Drury WH, Baird J (1963) Weight loss during migration part I: deposition and consumption of fat by the Blackpoll Warbler. Bird XXXIV:107–138Google Scholar
- Popp BN, Graham BS, Olson RJ et al (2007) Insight into the trophic ecology of yellowfin tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. In: Dawson TE, Siegwolf RTW (eds) Isotopes as indicators of ecological change. Elsevier Inc., Amsterdam, pp 173–190Google Scholar
- Powell RL, Still CJ (2009) Biogeography of C3 and C4 vegetation in South America. An. XIV Simp. Bras. Sensoramento Remoto, pp 2935–2942Google Scholar
- R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. ISBN: 3-900051-07-0
- Rosenberg KV (1990) Dead-leaf foraging specialization in tropical forest birds: measuring resource availability and use. Stud Avian Biol 13:360–368Google Scholar
- Rosenberg KV, Cooper RJ (1990) Approaches to avian diet analysis. Stud Avian Biol 13:80–90Google Scholar