Advertisement

Marine Biology

, Volume 161, Issue 1, pp 229–237 | Cite as

Differences in δ13C and δ15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations

  • Yves CherelEmail author
  • Sébastien Jaquemet
  • Alessio Maglio
  • Audrey Jaeger
Method

Abstract

Blood and feathers are the most targeted tissues for isotopic investigations in avian ecology, primarily because they can be easily and non-destructively sampled on live individuals. Comparing blood and feather isotopic ratios can provide valuable information on dietary shifts, trophic specialization and migration patterns, but it requires a good knowledge of the isotopic differences between the two tissues. Here, δ13C and δ15N values of whole blood (in blood cells of a few species) and simultaneously grown body feathers were measured in seabird chicks to quantify the tissue-related isotopic differences. Seabirds include 27 populations of 22 wild species that were sampled in 2000–2008, and a review of the literature added 8 groups (including adult birds) to the analysis. The use of a large data set that overall encompasses wide δ13C and δ15N ranges allowed us to depict for the first time accurate relationships between blood and feather isotopic ratios across avian taxa. Blood was impoverished in 13C and generally in 15N compared with feathers. Both mean δ13C and δ15N values of feathers and blood were highly positively and linearly related [feather δ13C = 0.972 (±0.020) blood δ13C + 0.962 (±0.414), and feather δ15N = 1.014 (±0.056) blood + 0.447 (±0.665), respectively; both P < 0.0001]. The regressions should be applied to mathematically correct feather or whole blood δ13C and δ15N values when comparing isotopic ratios within and between ecological studies on birds.

Keywords

Dietary Shift Discrimination Factor Isotopic Difference Giant Petrel Body Feather 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors thank the numerous fieldworkers and students for their help in the field, F. Capoulun, M. Connan and T. Cook for preparing samples, and G. Guillou, P. Richard and J. Lanham for stable isotope analysis. The present work was supported financially and logistically by the Institut Polaire Français Paul Emile Victor (Programme No. 109, H. Weimerskirch) and the Terres Australes et Antarctiques Françaises.

References

  1. Bearhop S, Teece MA, Waldron S, Furness RW (2000) Influence of lipid and uric acid on δ13C and δ15N values of avian blood: implications for trophic studies. Auk 117:504–507Google Scholar
  2. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458CrossRefGoogle Scholar
  3. Bost CA, Jouventin P (1991) The breeding biology of the gentoo penguin Pygoscelis papua on the Crozet Islands. Ibis 133:14–25CrossRefGoogle Scholar
  4. Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Commun Mass Spectrom 22:2457–2462CrossRefGoogle Scholar
  5. Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453CrossRefGoogle Scholar
  6. Cherel Y (2008) Isotopic niches of emperor and Adélie penguins in Adélie Land, Antarctica. Mar Biol 154:813–821CrossRefGoogle Scholar
  7. Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888CrossRefGoogle Scholar
  8. Cherel Y, Hobson KA, Hassani S (2005b) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115CrossRefGoogle Scholar
  9. Cherel Y, Hobson KA, Weimerskirch H (2005c) Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia 145:533–540CrossRefGoogle Scholar
  10. Cherel Y, Le Corre M, Jaquemet S, Ménard F, Richard P, Weimerskirch H (2008) Resource partitioning within a tropical seabird community: new information from stable isotopes. Mar Ecol Prog Ser 366:281–291CrossRefGoogle Scholar
  11. Cruz LL, McGill RAR, Goodman SJ, Hamer KC (2012) Stable isotope ratios of a tropical marine predator: confounding effects of nutritional status during growth. Mar Biol 159:873–880CrossRefGoogle Scholar
  12. Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144:647–658CrossRefGoogle Scholar
  13. Evans Ogden LJ, Hobson KA, Lank DB (2004) Blood isotopic (δ13C and δ15N) turnover and diet-tissue fractionation factors in captive dunlin (Calidris alpina pacifica). Auk 121:170–177CrossRefGoogle Scholar
  14. Federer RN, Hollmen TE, Esler D, Wooller MJ, Wang SW (2010) Stable carbon and nitrogen isotope discrimination factors from diet to blood plasma, cellular blood, feathers, and adipose tissue fatty acids in spectacled eiders (Somateria fischeri). Can J Zool 88:866–874CrossRefGoogle Scholar
  15. Fort J, Cherel Y, Harding AMA, Welcker J, Jakubas D, Steen H, Karnovsky NJ, Grémillet D (2010) Geographic and seasonal variability in the isotopic niche of little auks. Mar Ecol Prog Ser 414:293–302CrossRefGoogle Scholar
  16. Hahn S, Hoye BJ, Korthals H, Klaassen M (2012) From food to offspring down: tissue-specific discrimination and turn-over of stable isotopes in herbivorous waterbirds and other avian foraging guilds. PLoS One 7:e30242CrossRefGoogle Scholar
  17. Haramis GM, Jorde DG, Macko SA, Walker JL (2001) Stable-isotope analysis of canvasback winter diet in upper Chesapeake Bay. Auk 118:1008–1017Google Scholar
  18. Hedd A, Fifield DA, Burke CM, Montevecchi WA, McFarlane Tranquilla L, Regular PM, Buren AD, Robertson GJ (2010) Seasonal shift in the foraging niche of Atlantic puffins Fratercula arctica revealed by stable isotope (δ15N and δ13C) analyses. Aquat Biol 9:13–22CrossRefGoogle Scholar
  19. Hobson KA (2011) Isotopic ornithology. J Ornithol 152(Suppl. 1):S49–S66CrossRefGoogle Scholar
  20. Hobson KA, Bairlein F (2003) Isotopic fractionation and turnover in captive garden warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Can J Zool 81:1630–1635CrossRefGoogle Scholar
  21. Hobson KA, Bond AL (2012) Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses. Mar Ecol Prog Ser 461:233–243CrossRefGoogle Scholar
  22. Hobson KA, Clark RG (1992a) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188CrossRefGoogle Scholar
  23. Hobson KA, Clark RG (1992b) Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197CrossRefGoogle Scholar
  24. Hobson KA, Clark RG (1993) Turnover of 13C in cellular and plasma fractions of blood: implications for nondestructive sampling in avian dietary studies. Auk 110:638–641CrossRefGoogle Scholar
  25. Hobson KA, Gibbs HL, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Can J Zool 75:1720–1723CrossRefGoogle Scholar
  26. Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461CrossRefGoogle Scholar
  27. Jaeger A, Connan M, Richard P, Cherel Y (2010) Use of stable isotopes to quantify seasonal changes of trophic niche and levels of population and individual specialisation in seabirds. Mar Ecol Prog Ser 401:269–277CrossRefGoogle Scholar
  28. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27CrossRefGoogle Scholar
  29. Kempster B, Zanette L, Longstaffe FJ, MacDougall-Shackleton SA, Wingfield JC, Clinchy M (2007) Do stable isotopes reflect nutritional stress? Results from a laboratory experiment on song sparrows. Oecologia 151:365–371CrossRefGoogle Scholar
  30. Kohler SA, Connan M, Hill JM, Mablouké C, Bonnevie B, Ludynia K, Kemper J, Huisamen J, Underhill LG, Cherel Y, McQuaid CD, Jaquemet S (2011) Geographic variation in the trophic ecology of an avian rocky shore predator, the African black oystercatcher, along the southern African coastline. Mar Ecol Prog Ser 435:235–249CrossRefGoogle Scholar
  31. Lorrain A, Graham B, Ménard F, Popp B, Bouillon S, van Breugel P, Cherel Y (2009) Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar Ecol Prog Ser 391:293–306CrossRefGoogle Scholar
  32. Martinez del Rio C, Sabat P, Anderson-Sprecher R, Gonzalez SP (2009) Dietary and isotopic specialization: the isotopic niche of three Cinclodes ovenbirds. Oecologia 161:149–159CrossRefGoogle Scholar
  33. Murphy ME, King JR (1991) Nutritional aspects of avian molt. In: Beff BD, Cossee RO, Flux JEC, Heather BD, Hitchmough RA, Robertson CJR, Williams MJ (eds) Acta XX Congressus Internationalis Ornithologici. Christchurch, pp 2186–2193Google Scholar
  34. Murphy ME, King JR, Taruscio TG, Geupel GR (1990) Amino acid composition of feather barbs and rachises in three species of pygoscelid penguins: nutritional implications. Condor 92:913–921CrossRefGoogle Scholar
  35. Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436Google Scholar
  36. Pearson SF, Levey DJ, Greenberg CH, Martinez del Rio C (2003) Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135:516–523Google Scholar
  37. Phillips RA, Hamer KC (2000) Postnatal development of northern fulmar chicks, Fulmarus glacialis. Physiol Biochem Zool 73:597–604CrossRefGoogle Scholar
  38. Post DM, Layman CA, Albrey Arrington D, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189CrossRefGoogle Scholar
  39. Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598CrossRefGoogle Scholar
  40. Sanpera C, Moreno R, Ruiz X, Jover L (2007) Audouin’s gull chicks as bioindicators of mercury pollution at different breeding locations in the western Mediterranean. Mar Pollut Bull 54:691–696CrossRefGoogle Scholar
  41. Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48CrossRefGoogle Scholar
  42. Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182CrossRefGoogle Scholar
  43. Wolf N, Carleton SA, Martinez del Rio C (2009) Ten years of experimental animal isotopic ecology. Funct Ecol 23:17–26CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Yves Cherel
    • 1
    Email author
  • Sébastien Jaquemet
    • 2
  • Alessio Maglio
    • 1
  • Audrey Jaeger
    • 1
    • 2
  1. 1.Centre d’Etudes Biologiques de Chizé (CEBC)UPR 1934 du CNRSVilliers-en-BoisFrance
  2. 2.Laboratoire ECOMARUniversité de La RéunionSaint-Denis CedexFrance

Personalised recommendations