Skip to main content
SpringerLink
Log in

Testing the usefulness of hydrogen and compound-specific stable isotope analyses in seabird feathers: a case study in two sympatric Antarctic storm-petrels

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Nitrogen and carbon stable isotopes provide tools to investigate ecological segregation, prey choice and spatial distribution in seabirds. However, the interpretation of stable isotopes is frequently hampered by a lack of isotopic baseline data. In this study, two techniques proposed to overcome such shortages were tested: compound-specific isotope analyses of amino acids (AA-CSIA) and the analysis of hydrogen stable isotope ratios (HSIA). Feathers of two sympatric storm-petrels were compared. The two species, Black-bellied storm-petrels Fregetta tropica and Wilson’s storm-petrels Oceanites oceanicus, moult in oceanic waters and differ in diet composition. For HSIA, a range of species with broad diet and non-breeding distribution was also investigated. Differences in carbon isotope values suggested differences in the spatial distribution and thus, in isotopic baseline values, during moult. Bulk nitrogen analyses of adult feathers did not detect species differences in trophic level. However, AA-CSIA detected clear differences in trophic levels in line with expectations: Black-bellied storm-petrels fed at a higher trophic level than Wilson‘s storm-petrels. Hydrogen values also differed between the species, but contrary to expectations were highly enriched in Black-bellied storm-petrels, but much less enriched in Wilson’s storm-petrels. Hydrogen data of seven petrel species challenge the suggestion that depleted δD values indicate a higher percentage of isosmotic fish. The present results suggest that the difference in hydrogen ratios may be explained by these petrels moulting in different ocean zones. Amino acid-specific stable isotope analyses were useful for estimating isotopic baselines and thus true trophic levels, whereas hydrogen isotopes were not.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Cherel Y, Quillfeldt P, Delord K, Weimerskirch H (2016) Combination of at-sea activity, geolocation and feather stable isotopes documents where and when seabirds molt. Front Ecol Evol 4:3

    Article  Google Scholar 

  • Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y, Suga H, Tomitani A, Miyashita H, Kitazato H, Ohkouchi N (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr Method 7:740–750

    Article  CAS  Google Scholar 

  • del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (Eds) (2016) Handbook of the birds of the world alive. Lynx Edicions, Barcelona. URL http://www.hbw.com. Accessed 7 Oct 2016

  • Elliott KH, Elliott JE (2016) Origin of sulfur in diet drives spatial and temporal mercury trends in seabird eggs from Pacific Canada 1968–2015. Environ Sci Technol 50:13380–13386

    Article  CAS  Google Scholar 

  • González-Solís J, Croxall JP, Oro D, Ruiz X (2007) Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird. Front Ecol Environ 5:297–301

    Article  Google Scholar 

  • Grecian JW, Taylor GA, Loh G, McGill RAR, Miskelly CM, Phillips RA, Thompson DR, Furness RW (2016) Contrasting migratory responses of two closely related seabirds to long-term climate change. Mar Ecol Progr Ser 559:231–242

    Article  Google Scholar 

  • Hahn S (1998) The food and chick feeding of black-bellied storm-petrel (Fregetta tropica) at King George Island, South Shetlands. Polar Biol 19:354–357

    Article  Google Scholar 

  • Hahn S, Peter H-U, Quillfeldt P, Reinhardt K (1998) The birds of the Potter Peninsula, King George Island, South Shetland Islands, Antarctica, 1965–1998. Mar Ornithol 26:1–6

    Google Scholar 

  • Hannides CCS, Popp BN, Landry MR, Graham BS (2009) Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes. Limnol Oceanogr 54:50–61

    Article  CAS  Google Scholar 

  • Hebert CE, Popp BN, Fernie KJ, Ka’apu-Lyons C, Rattner BA, Wallsgrove N (2016) Amino acid specific stable nitrogen isotope values in avian tissues: insights from captive American Kestrels and wild Herring Gulls. Environ Sci Technol 50:12928–12937

    Article  CAS  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • 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 391:293–306

    Article  CAS  Google Scholar 

  • McClelland JW, Montoya JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83:2173–2180

    Article  Google Scholar 

  • McMahon KW, McCarthy MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere. doi:10.1002/ecs2.1511

    Google Scholar 

  • McMahon KW, Thorrold SR, Elsdon TS, McCarthy MD (2015a) Trophic discrimination of nitrogen stable isotopes in amino acids varies with diet quality in a marine fish. Limnol Oceanogr 60:1076–1087

    Article  CAS  Google Scholar 

  • McMahon KW, Polito MJ, Abel S, McCarthy MD, Thorrold SR (2015b) Carbon and nitrogen isotope fractionation of amino acids in an avian marine predator, the gentoo penguin (Pygoscelis papua). Ecol Evol 5:1278–1290

    Article  Google Scholar 

  • Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajthaand K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, Oxford, pp 138–157

    Google Scholar 

  • Mizutani H, Fukuda M, Kabaya Y (1992) δ13C and δ15N enrichment factors of feathers of 11 species of adult birds. Ecology 73:1391–1395

    Article  Google Scholar 

  • Ostrom PH, Wiley AE, Rossman S, Stricker CA, James HF (2014) Unexpected hydrogen isotope variation in oceanic pelagic seabirds. Oecologia 175:1227–1235

    Article  Google Scholar 

  • Pakhomov EA, McClelland JW, Bernard K, Kaehler S, Montoya JP (2004) Spatial and temporal shifts in stable isotope values of the bottom-dwelling shrimp Nauticaris marionis at the sub-Antarctic archipelago. Mar Biol 144:317–325

    Article  Google Scholar 

  • Popp BN, Graham BS, Olson RJ, Hannides CCS, Lott M, López-Ibarra G, Galván-Magaña F (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) Stable isotopes as indicators of ecological change. Academic Press, Cambridge, pp 173–190

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models. Methods and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Quillfeldt P (2002) Seasonal and annual variation in the diet of breeding and non-breeding Wilson’s storm-petrels on King George Island, South Shetland Islands. Polar Biol 25:216–221

    Google Scholar 

  • Quillfeldt P, Masello JF, Navarro J, Phillips RA (2013) Year-round distribution suggests spatial segregation of two small petrel species in the South Atlantic. J Biogeogr 40:430–441

    Article  Google Scholar 

  • Quillfeldt P, Cherel Y, Delord K, Weimerkirch H (2015a) Cool, cold or colder? Spatial segregation of prions and blue petrels is explained by differences in preferred sea surface temperatures. Biol Lett 11:20141090

    Article  Google Scholar 

  • Quillfeldt P, Ekschmitt K, Brickle P, McGill RA, Wolters V, Dehnhard N, Masello JF (2015b) Variability of higher trophic level stable isotope data in space and time—a case study in a marine ecosystem. Rapid Commun Mass Spectrom 29:667–674

    Article  CAS  Google Scholar 

  • R Development Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, URL: http://www.R-project.org. Accessed 7 Oct 2016

  • Ramos R, Sanz V, Militao T, Bried J, Neves VC, Biscoito M, Phillips RA, Zino F, Gonzales-Solis J (2015) Leapfrog migration and habitat preferences of a small oceanic seabird, Bulwer’s Petrel (Bulweria bulwerii). J Biogeogr 42:1651–1664

    Article  Google Scholar 

  • Schmidt K, Atkinson A, Petzke K-J, Voss M, Pomd DW (2006) Protozoans as a food source for Antarctic krill, Euphausia superba: complementary insights from stomach content, fatty acids, and stable isotopes. Limnol Oceanogr 51:2409–2427

    Article  CAS  Google Scholar 

  • Stille P, Chaudhuri S, Kharaka YK, Clauer N (1992) Neodymium, strontium, oxygen and hydrogen isotope compositions of waters in present and past oceans: a review. In: Chaudhuri S, Clauer N (eds) Isotopic signatures and sedimentary records. Lecture notes in earth sciences. Springer, Berlin

    Google Scholar 

  • Walsh R, He S, Yarnes CT (2014) Rapid compound-specific stable isotope analysis of amino acids by GC-C-IRMS of methyl chloroformate derivatives. Rapid Commun Mass Spectrom 28:96–108

    Article  CAS  Google Scholar 

  • Wassenaar LI, Hobson KA (2003) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Health Stud 39:211–217

    Article  CAS  Google Scholar 

  • Weiss F, Furness RW, McGill RAR, Strange IJ, Masello JF, Quillfeldt P (2009) Trophic segregation of Falkland Islands seabirds—insights from stable isotope analysis. Polar Biol 32:1753–1763

    Article  Google Scholar 

  • Xu X, Werner M, Butzin M, Lohmann G (2012) Water isotope variations in the global ocean model MPI-OM. Geosci Model Dev 5:809–818

    Article  CAS  Google Scholar 

  • Yarnes CT, Herszage J (2017) The relative influence of derivatization and normalization procedures on the compound-specific stable isotope analysis of nitrogen in amino acids. Rapid Comm Mass Spectrom 31:693–704

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Vitor Paiva and two anonymous reviewers for helpful comments on the manuscript, and Joy Matthews and Chris Yarnes for running the analyses at UC Davis and discussing methodological details. We are grateful for logistic support by the Alfred Wegener Institute (Dirk Mengedoht), the Instituto Antarctico Argentino (Buenos Aires) and Department of Conservation (New Zealand).

Author information

Author notes

  1. Simon Thorn

    Present address: Field Station Fabrikschleichach, Department of Animal Ecology and Tropical Biology, Biocenter University of Würzburg, Glashüttenstraße 5, 96181, Rauhenebrach, Germany

Authors and Affiliations

  1. Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Heinrich-Buff-Ring, 35392, Giessen, Germany

    Petra Quillfeldt, Simon Thorn, Benjamin Richter & Juan F. Masello

  2. Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, Alte. Brown 3700, Puerto Madryn, Chubut, Argentina

    Marcela Nabte

  3. Departamento de Ciencias de la Vida, Instituto Antártico Argentino, Cerrito 1248, C1010AAZ, Buenos Aires, Argentina

    Nestor Coria & Marcela Libertelli

  4. School of Environmental Sciences, Institute for Land, Water and Society, Charles Sturt University, Albury, NSW, 2640, Australia

    Melanie Massaro

  5. Department of Oceanography and Fisheries (DOP), MARE (Marine and Environmental Sciences Centre), IMAR (Institute of Marine Research) and LARSyS Associated Laboratory, University of the Azores, Rua Prof Dr Frederico Machado 4, PT-9901-862, Horta, Azores, Portugal

    Verónica C. Neves

Authors
  1. Petra Quillfeldt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simon Thorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Benjamin Richter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcela Nabte
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nestor Coria
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juan F. Masello
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Melanie Massaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Verónica C. Neves
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marcela Libertelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Petra Quillfeldt.

Ethics declarations

Conflict of interest

We declare that we have no conflict of interest.

Funding

This study was funded by the Deutsche Forschungsgemeinschaft (DFG) in the framework of the priority programme SPP1154 “Antarctic Research with comparative investigations in Arctic ice areas” by a grant to PQ (Qu148/16). VN is funded by FCT, Portugal—SFRH/BPD/88914/2012.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: V. Paiva.

Reviewed by K. H. Elliott and an undisclosed expert.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quillfeldt, P., Thorn, S., Richter, B. et al. Testing the usefulness of hydrogen and compound-specific stable isotope analyses in seabird feathers: a case study in two sympatric Antarctic storm-petrels. Mar Biol 164, 192 (2017). https://doi.org/10.1007/s00227-017-3224-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3224-8

Search

Navigation