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Polar Biology

, Volume 40, Issue 11, pp 2225–2238 | Cite as

Reconstructing variability in West Greenland ocean biogeochemistry and bowhead whale (Balaena mysticetus) food web structure using amino acid isotope ratios

  • Corinne PomerleauEmail author
  • Mads Peter Heide-Jørgensen
  • Steven H. Ferguson
  • Harry L. Stern
  • Jacob L. Høyer
  • Gary A. Stern
Original Paper

Abstract

Climate change is causing physical and biological changes in the polar marine environment, which may impact higher trophic level predators such as the bowhead whale (Balaena mysticetus) and the structure of their food webs. We used bulk stable isotope analysis and compound-specific isotope analysis (CSIA) of individual amino acids (AA) to examine bowhead whale trophic position and the biogeochemistry of one of their feeding grounds, Disko Bay, West Greenland, over a period of 7 years (2007–2013). We also examined whether environmental conditions such as sea ice concentration and sea surface temperature were causing any interannual variation in isotope data. Bulk δ 15N values were consistent across the 7 years of sampling and were similar between sex classes. Bulk δ 13C and essential-AAs δ 13C values displayed an overall temporal decline of 1.0 and 1.4‰, respectively. A significant positive linear relationship was found between δ 13C of bulk skin and essential-AAs suggesting that some of the observed isotopic variation in bowhead whales between years reflect changes in the carbon at the base of the food web. There were no correlations between the δ 13C and δ 15N values of isotopic tracers with sea ice concentrations or sea surface temperatures. The trophic level of bowhead whales remained stable over time despite large interannual variability in ice and temperature regimes. Our results indicate that the recent environmental changes in West Greenland resulted in no trophic perturbation being transferred to bowhead whales during that time period. Our study shows that the novel approach of CSIA-AA can be used effectively to study the combined temporal variation of bowhead whale food web structure and ecosystem isotopic baseline values and detect changes at the species and ecosystem levels.

Keywords

Amino acids Bowhead whale Carbon Compound-specific isotope analysis Nitrogen Stable isotope analysis 

Notes

Acknowledgements

This study was funded by Fisheries and Oceans Canada and the Greenland Institute of Natural Resources. We are grateful to local hunters in Qeqertarsuaq for collection of the skin biopsies. CITES permits have been provided by Greenlandic and Norwegian authorities. We thank Chris Yarnes and Joy Matthews from the University of California Davis and Anna Hussey and Aaron Fisk from the University of Windsor for sample analysis. Ecosystem data were provided by DiskoBasis/Arctic Station, University of Copenhagen. C. Pomerleau was supported by a W. Garfield Weston Postdoctoral fellowship. We would like to thank three anonymous reviewers for their insightful comments.

References

  1. Albouy C, Velez L, Coll M, Colloca F, Loch FL, Mouillot D, Gravel D (2014) From projected species distribution to foodweb structure under climate change. Glob Chang Biol 20:730–741CrossRefPubMedGoogle Scholar
  2. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefPubMedGoogle Scholar
  3. Bowes RE, Thorp JH (2015) Consequences of employing amino acid vs. bulk-tissue, stable isotope analysis: a laboratory trophic position experiment. Ecosphere 6:1–12CrossRefGoogle Scholar
  4. Bradley CJ, Madigan DJ, Block BA, Popp BN (2014) Amino acid isotope incorporation and enrichment factors in Pacific bluefin tuna, Thunnus orientalis. PLoS ONE 9:e85818CrossRefPubMedCentralPubMedGoogle Scholar
  5. Browning NE, Dold C, Fan J, Worthy GAJ (2014) Isotope turnover rates and diet–tissue discrimination in skin of ex situ bottlenose dolphins. J Exp Biol 217:214–221CrossRefPubMedGoogle Scholar
  6. Burkhardt S, Riebesell U, Zondervan I (1999) Effects of growth rate, CO2 concentration, and cell size on the stable carbon isotope fractions in marine phytoplankton. Geochim Cosmochim Acta 63:3729–3741CrossRefGoogle Scholar
  7. Caut S, Laran S, Garcia-Hartmann E, Das K (2011) Stable isotopes of captive cetaceans. J Exp Biol 214:538–545CrossRefPubMedGoogle Scholar
  8. Cavalieri DJ, Parkinson CL, Gloersen P, Zwally HJ (1996) Sea ice concentrations from Nimbus-7 SMMR and DMSP SSM/I-SSMIS passive microwave data. NASA National Snow and Ice Data Center Distributed Active Archive Center, BoulderGoogle Scholar
  9. Chikaraishi Y, Kashiyama Y, Ogawa NO, Kitazato H, Ohkouchi J (2007) Biosynthetic and metabolic controls of nitrogen isotopic composition of amino acids in marine macroalgae and gastropods: implications for aquatic food web studies. Mar Ecol Prog Ser 342:85–90CrossRefGoogle Scholar
  10. Chikaraishi Y, Ogawa NO, Kashiyama Y, Takano Y et al (2009) Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr 7:740–750CrossRefGoogle Scholar
  11. Choy CA, Davison PC, Drazen JC, Flynn A et al (2012) Global trophic position comparison of two dominant mesopelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analyses. PLoS ONE 7:e50133CrossRefPubMedCentralPubMedGoogle Scholar
  12. Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  13. Dale JJ, Wallsgrove NJ, Popp BN, Holland KN (2011) Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar Ecol Prog Ser 433:221–236CrossRefGoogle Scholar
  14. Décima M, Landry MR, Popp BN (2013) Environmental perturbation effects on baseline nitrogen values and zooplankton trophic flexibility in the Southern California Current Ecosystem. Limnol Oceanogr 58:624–634CrossRefGoogle Scholar
  15. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  16. Docherty G, Evershed RP (2001) Practical and theoretical considerations in the gas chromatography/combustion/isotope ratio mass spectrometry δ13C analysis of small polyfunctional compounds. Rapid Commun Mass Spectrom 15:730–738CrossRefPubMedGoogle Scholar
  17. Dunton KH, Weingartner T, Carmack E (2006) The nearshore western Beaufort Sea ecosystem: circulation and importance of terrestrial carbon in arctic coastal food webs. Prog Oceanogr 71:362–378CrossRefGoogle Scholar
  18. Ferguson SH, Stirling I, McLoughlin P (2005) Climate change and ringed seal (Phoca hispida) recruitment in western Hudson Bay. Mar Mamm Sci 21:121–135CrossRefGoogle Scholar
  19. Ferguson SH, Dueck L, Loseto LL, Luque SP (2010) Bowhead whale (Balaena mysticetus) seasonal selection of sea ice. Mar Ecol Prog Ser 41:285–297CrossRefGoogle Scholar
  20. Gannes LZ, O’Brien DM, del Rio CM (1997) Stable isotopes in animal ecology: assumptions, caveats and a call for more laboratory experiments. Ecology 78:1271–1276CrossRefGoogle Scholar
  21. Germain LR, Koch PL, Harvey J, McCarthy MD (2013) Nitrogen isotope fractionation in amino acids from harbor seals: implications for compound-specific trophic position calculations. Mar Ecol Prog Ser 482:265–277CrossRefGoogle Scholar
  22. Gladish CV, Holland DM, Lee CM (2015) Oceanic boundary conditions for Jakobshavn Glacier. Part II: provenance and sources of variability of Disko Bay and Ilulissat icefjord waters, 1990–2011. J Phys Oceanogr 45:33–63CrossRefGoogle Scholar
  23. Goericke R, Montoya JP, Fry B (1994) Physiology of isotopic fractionation in algae and cyanobacteria. In: Lajhta K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, Cambridge, pp 187–221Google Scholar
  24. Hanna E, Jones JM, Cappelen J, Mernild SH, Wood L, Steffen K, Huybrechts P (2012) The influence of North Atlantic atmospheric and oceanic forcing effects on 1900-2010 Greenland summer climate and ice melt/runoff. Int J Climatol 33:862–880CrossRefGoogle Scholar
  25. Hawkings JR, Wadham JL, Tranter M et al (2015) The effect of warming climate on nutrient and solute export from the Greenland Ice Sheet. Geochem Persp Let 1:94–104CrossRefGoogle Scholar
  26. Heide-Jørgensen MP, Laidre KL, Wiig J, Dueck L et al (2003) From Greenland to Canada in two weeks: movements of bowhead whales in Baffin Bay. Arctic 56:21–31CrossRefGoogle Scholar
  27. Heide-Jørgensen MP, Laidre KL, Jensen MV, Dueck L, Postma LD (2006) Dissolving stock discreteness with satellite tracking: bowhead whales in Baffin Bay. Mar Mamm Sci 22:34–45CrossRefGoogle Scholar
  28. Heide-Jørgensen MP, Laidre KL, Borchers D, Stern H (2007) Increasing abundance of bowhead whales in West Greenland. Biol Lett 3:577–580CrossRefPubMedCentralPubMedGoogle Scholar
  29. Heide-Jørgensen MP, Garde E, Nielsen NH, Andersen ON (2012) Biological data from the hunt of bowhead whales in West Greenland 2009 and 2010. J Cetac Res Manag 12:329–333Google Scholar
  30. Heide-Jørgensen MP, Laidre KL, Nielsen NH, Hansen RG, Røstad S (2013) Winter and spring feeding behavior of bowhead whales. Anim Biotelem 1:1–15. doi: 10.1186/2050-3385-1-15 CrossRefGoogle Scholar
  31. Hirons AC, Schell DM, Finney BP (2001) Temporal record of δ13C and δ15N in North Pacific pinnipeds: inferences regarding environmental change and diet. Oecologia 129:591–601CrossRefPubMedGoogle Scholar
  32. Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefPubMedGoogle Scholar
  33. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528–533CrossRefGoogle Scholar
  34. Hobson KA, Fisk A, Karnovsky N, Holst M, Gagnon JM, Fortier M (2002) A stable isotope model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants. Deep Sea Res II 49:5131–5150CrossRefGoogle Scholar
  35. Hoen DK, Kim SL, Hussey NE, Wallsgrove NJ, Drazen JC, Popp BN (2014) Amino acid δ15N trophic enrichment factors of four large carnivorous fishes. J Exp Mar Biol Ecol 453:76–83CrossRefGoogle Scholar
  36. Hofmann D, Gehre M, Jung K (2003) Sample preparation techniques for the determination of natural 15 N/14 N variations in amino acids by gas chromatography-combustion-isotope ratio mass spectrometry (GC-C-IRMS). Isot Environ Health Stud 39:233–244CrossRefGoogle Scholar
  37. Holland D, Thomas R, Young BD, Ribergaard M, Lyberth B (2008) Acceleration of Jakobshavn Isbræ triggered by warm subsurface ocean waters. Nat Geosci 1:659–664CrossRefGoogle Scholar
  38. Iken K, Bluhm B, Dunton K (2010) Benthic food-web structure under differing water mass properties in the southern Chukchi Sea. Deep Sea Res II 57:71–85CrossRefGoogle Scholar
  39. Jochmann M, Schmidt T (2012) Compound-specific stable isotope analysis. Royal Society of Chemistry, Cambridge, p 376Google Scholar
  40. Kortsch S, Primicerio R, Beuchel F, Renaud PE, Rodrigues J, Lønne OJ, Gulliksen B (2012) Climate-driven regime shifts in Arctic marine benthos. Proc Natl Acad Sci 109:14052–14057CrossRefPubMedCentralPubMedGoogle Scholar
  41. Koski WR, Heide-Jørgensen MP, Laidre KL (2006) Winter abundance of bowhead whales, Balaena mysticetus, in Hudson Strait, March 1981. J Cetac Res Manag 8:139–144Google Scholar
  42. Kuzyk ZZA, Macdonald RW, Tremblay JÉ, Stern GA (2010) Elemental and stable isotopic constraints on river influence and patterns of nitrogen cycling and biological productivity in Hudson Bay. Cont Shelf Res 30:163–176CrossRefGoogle Scholar
  43. Laidre KL, Heide-Jørgensen MP (2012) Spring partitioning of Disko Bay, West Greenland, by Arctic and Subarctic baleen whales. ICES J Mar Sci 69:226–1233CrossRefGoogle Scholar
  44. Laidre K, Heide-Jørgensen MP, Nielsen TG (2007) Role of the bowhead whale as a predator in West Greenland. Mar Ecol Prog Ser 346:285–297CrossRefGoogle Scholar
  45. Laidre KL, Stern H, Kovacs KM et al (2015) Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century. Conserv Biol 29:724–737CrossRefPubMedCentralPubMedGoogle Scholar
  46. Larsen T, Taylor DL, Leigh M, O’Brien DM (2009) Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 12:3526–3535CrossRefGoogle Scholar
  47. Larsen T, Wooller MJ, Fogel ML, O’Brien DM (2012) Can amino acid carbon isotope ratios distinguish primary producers in a mangrove ecosystem? Rapid Comm Mass Spectrom 26:541–548CrossRefGoogle Scholar
  48. Larsen T, Ventura M, Andersen N, O’Brien DM, Piatkowski U, McCarthy MD (2013) Tracing carbon sources through aquatic and terrestrial food webs using amino acid stable isotope fingerprinting. PLoS ONE 8:e73441CrossRefPubMedCentralPubMedGoogle Scholar
  49. Laws EA, Popp BN, Bidigare RR, Kennicutt MC, Macko SA (1995) Dependence of phytoplankton carbon isotopic composition on growth rate and (CO2)aq: theoretical considerations and experimental results. Geochim Cosmochim Acta 5:1131–1138CrossRefGoogle Scholar
  50. Lesage V, Morin Y, Rioux E, Pomerleau C, Ferguson SH, Pelletier E (2010) Stable isotopes and trace metals as indicators of diet and habitat use in cetaceans: predicting errors related to preservation, lipid extraction and normalization. Mar Ecol Prog Ser 419:249–265CrossRefGoogle Scholar
  51. Linneberg J, Hobson KA, Fort J, Nielsen T, Møller P, Wieland K, Riget F, Mosbech A (2016) Deciphering the structure of the West Greenland marine food web using stable isotopes (δ13C, δ15N). Mar Biol 163:230CrossRefGoogle Scholar
  52. Lorrain A, Graham B, Menard F, Popp BN, Bouillon S et al (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
  53. Lowry LF, Sheffield G, George JG (2004) Bowhead whale feeding in the Alaskan Beaufort Sea, based on stomach contents analysis. J Cetac Res Manag 6:215–223Google Scholar
  54. Matthews C, Ferguson SH (2014) Spatial segregation and similar trophic-level diet among eastern Canadian Arctic/northwest Atlantic killer whales inferred from bulk and compound specific isotopic analysis. J Mar Biol Assoc UK 94:1343–1355CrossRefGoogle Scholar
  55. McClelland JW, Montoya JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83:2173–2180CrossRefGoogle Scholar
  56. McMahon KW, Fogel ML, Elsdon TS, Thorrold SR (2010) Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. J Anim Ecol 79:1132–1141CrossRefPubMedGoogle Scholar
  57. McMahon KW, Fogel ML, Johnson BJ, Houghton LA, Thorrold SR (2011) A new method to reconstruct fish diet and movement patterns from 13C values in otolith amino acids. Can J Fish Aquat Sci 68:1330–1340CrossRefGoogle Scholar
  58. McMahon KW, Elsdon T, Thorrold SR, McCarthy M (2015) Trophic discrimination of nitrogen stable isotopes in amino acids varies with diet quality in a marine fish. Limnol Oceanogr 60:1076–1087CrossRefGoogle Scholar
  59. McMeans BC, Olins JA, Benz GW (2009) Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. J Fish Biol 75:2464–2474CrossRefPubMedGoogle Scholar
  60. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidences and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140CrossRefGoogle Scholar
  61. Newsome SD, Etnier MA, Kurle CM, Waldebauer JR, Chamberlain CP, Koch PL (2007) Historic decline in primary productivity in western Gulf of Alaska and eastern Bering Sea: isotopic analysis of northern fur seal teeth. Mar Ecol Prog Ser 332:211–224CrossRefGoogle Scholar
  62. Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26:509–572Google Scholar
  63. Newsome SD, Fogel ML, Kelly L, Martinez del Rio C (2011) Contributions of direct incorporation from diet and microbial amino acids to protein synthesis in Nile tilapia (Oreochromis niloticus). Funct Ecol 25:1051–1062CrossRefGoogle Scholar
  64. Newsome SD, Wolf N, Peters J, Fogel ML (2014) Amino acid δ13C analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore. Int Comp Biol 54:890–902CrossRefGoogle Scholar
  65. Nielsen NH, Laidre KL, Larsen RS, Heide-Jørgensen MP (2015a) Identification of potential foraging areas for bowhead whales in Baffin Bay and adjacent waters. Arctic 68:169–179CrossRefGoogle Scholar
  66. Nielsen JM, Popp BN, Winder M (2015b) Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178:631–642CrossRefPubMedGoogle Scholar
  67. Palsbøll PJ, Larsen F, Hansen ES (1991) Sampling of skin biopsies from free-ranging large cetaceans in West Greenland: development of new biopsy tips and bolt designs. Rep Int Whal Comm 13:71–79Google Scholar
  68. Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481CrossRefGoogle Scholar
  69. Pineault S, Tremblay JÉ, Gosselin M, Thomas H, Shadwick E (2013) The isotopic signature of particulate organic C and N in bottom ice: key influencing factors and applications for tracing the fate of ice-algae in the Arctic Ocean. J Geophys Res Oceans 118:1–14CrossRefGoogle Scholar
  70. Pomerleau C, Patterson TA, Luque S, Lesage V, Heide-Jørgensen MP, Dueck L, Ferguson SH (2011a) Bowhead whale diving and movement patterns in the Eastern Canadian Arctic: implications for foraging ecology. Endanger Species Res 15:167–177CrossRefGoogle Scholar
  71. Pomerleau C, Ferguson SH, Walkusz W (2011b) Stomach contents of bowhead whales (Balaena mysticeus) from four locations in the Canadian Arctic. Polar Biol 34:615–620CrossRefGoogle Scholar
  72. Pomerleau C, Lesage V, Ferguson SH, Winkler G, Petersen S, Higdon J (2012) Prey assemblage isotopic variability as a tool for assessing diet and the spatial distribution of bowhead whale foraging in the Canadian eastern Arctic. Mar Ecol Prog Ser 469:161–174CrossRefGoogle Scholar
  73. Pomerleau C, Lesage V, Winkler G, Rosenberg B, Ferguson SH (2014) Contemporary diet of bowhead whales (Balaena mysticetus) from the Eastern Canadian Arctic inferred from fatty acid biomarkers. Arctic 67:84–92CrossRefGoogle Scholar
  74. Popp BN, Graham BS, Olson RJ, Hannides CCS 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 TD, Siegwolf RTW (eds) Stable isotopes as indicators of ecological change. Elsevier, New York, pp 173–190Google Scholar
  75. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  76. Post DM, Arrington DA, Layman CA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189CrossRefPubMedGoogle Scholar
  77. Rau GH, Takahashi T, Marais DJD (1989) Latitudinal variations in plankton δ13C: implications for CO2 and productivity in past oceans. Nature 341:516–518CrossRefPubMedGoogle Scholar
  78. Reinneke S, Juchelka D, Steinbeiss S, Meyer A, Hilkert A, Elsner M (2012) Gas chromatography/isotope ratio mass spectrometry of recalcitrant target compounds: performance of different combustion reactors and strategies for standardization. Rapid Commun Mass Spectrom 26:1053–1060CrossRefGoogle Scholar
  79. Rekdal SL, Hansen RG, Borchers D, Bachmann L, Laidre KL, Wiig Ø, Nielsen NH, Fossette S, Tervo O, Heide-Jørgensen MP (2015) Trends in bowhead whales in West Greenland; Aerial surveys vs. genetic capture-recapture. Mar Mamm Sci 3:133–154CrossRefGoogle Scholar
  80. Rignot E, Velicogna I, VandenBroeke MR, Monaghan A, Lenaerts J (2011) Acceleration of the contribution of the Greenland and Antarctic ice sheets to sea level rise. Geophys Res Lett 38:L05503CrossRefGoogle Scholar
  81. Ruiz-Cooley RI, Koch PL, Fiedler PC, McCarthy MD (2014) Carbon and nitrogen isotopes from top predator amino acids reveal rapidly shifting ocean biochemistry in the outer California Current. PLoS ONE 9:e110355CrossRefPubMedCentralPubMedGoogle Scholar
  82. Sacks GL, Brenna JT (2005) 15N/14N position-specific isotopic analyses of polynitrogenous amino acids. Anal Chem 77:1013–1019CrossRefPubMedGoogle Scholar
  83. Schell DM (2000) Declining carrying capacity in the Bering Sea: isotopic evidence from whale baleen. Limnol Oceanogr 45:459–462CrossRefGoogle Scholar
  84. Schiff JT, Batista FC, Sherwood OA, Guilderson TP, Hill TM, Ravelon AC, McMahon KW, McCarthy MD (2014) Compound specific amino acid δ13C patterns in a deep-sea proteinaceous coral: implications for reconstructing detailed δ13C records of exported primary production. Mar Chem 166:82–91CrossRefGoogle Scholar
  85. Seminoff JA, Benson SR, Arthur KE, Eguchi T, Dunton PH, Tapilatu RF, Popp BN (2012) Stable isotope tracking of endangered sea turtles: validation with satellite telemetry and δ15N analysis of amino acids. PLoS ONE 12:e37403CrossRefGoogle Scholar
  86. Sherwood OA, Lehmann MF, Schubert CJ, Scott DB, McCarthy MD (2011) Nutrient regime shift in the western North Atlantic indicated by compound-specific δ15N of deep-sea gorgonian corals. Proc Natl Acad Sci 108:1011–1015CrossRefPubMedCentralPubMedGoogle Scholar
  87. Sonnerup RE, Quay PD, McNichol AP, Bullister JA, Westby TA, Anderson HL (1999) Reconstructing the oceanic δ13C Suess effect. Glob Biogeochem Cycles 13:857–872CrossRefGoogle Scholar
  88. St-Aubin DJ, Smith TG, Geraci JR (1990) Seasonal epidermal moult in beluga whales, Delphinapterus leucas. Can J Zool 68:359–367CrossRefGoogle Scholar
  89. Swalethorp R, Kjellerup S, Dünweber M, Nielsen TG, Møller EF, Rysgaard S, Hansen BW (2011) Production of Calanus finmarchicus, C. glacialis and C. hyperboreus in Disko Bay, Western Greenland, with emphasis on life strategy. Mar Ecol Prog Ser 429:125–144CrossRefGoogle Scholar
  90. Tanaka T, Watanabe Y, Watanabe S, Noriki S, Tsurushima N, Nojiri Y (2003) Oceanic Suess effect of δ13C in subpolar region. Geophys Res Lett 30:2159. doi: 10.1029/2003GL018503 Google Scholar
  91. Tremblay JE, Gratton Y, Fauchot J, Price NM (2002) Climatic and oceanic forcing of new, net and diatom production in the North Water Polynya. Deep-Sea Res II 49:4927–4946CrossRefGoogle Scholar
  92. Vokhshoori NL, McCarthy MD (2014) Compound-specific δ15N amino acid measurements in littoral mussels in the California Upwelling ecosystem: a new approach to generating baseline δ15N isoscapes for coastal ecosystems. PLoS ONE 9:e98087CrossRefPubMedCentralPubMedGoogle Scholar
  93. Vokhshoori NL, Larsen TM, McCarthy MD (2014) Reconstructing δ13C isoscapes of phytoplankton production in a coastal upwelling system with amino acid isotope values of littoral mussels. Mar Ecol Prog Ser 504:59–72CrossRefGoogle Scholar
  94. Wadham JL, Hawkings J, Telling J, Chandler D et al (2016) Sources, cycling and export of nitrogen on the Greenland Ice Sheet. Biogeosci Discuss 13:6339–6352CrossRefGoogle Scholar
  95. Walsh R, He S, Yarnes CT (2014) Rapid compound-specific stable isotope analysis of amino acids by GC-C-IRMS of methylchloroformate derivatives. Rapid Comm Mass Spec 28:96–108CrossRefGoogle Scholar
  96. Wiig Ø, Heide-Jørgensen MP, Lindqvist C, Laidre KL (2011) Recaptures of genotyped bowhead whales in Eastern Canada and West Greenland. Endanger Species Res 14:235–242CrossRefGoogle Scholar
  97. Woodby DA, Botkins DB (1993) Stock sizes prior to commercial whaling. In: Burns JJ, Montague JJ, Cowles CJ (eds) The bowhead whale. The Society of Marine Mammalogy. Special Publication, pp 387–407Google Scholar
  98. 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 Commun Mass Spectrom 31:693–704CrossRefPubMedGoogle Scholar
  99. Zhang J, Spitz YH, Steele M, Ashjian C, Campbell R, Berline L, Matrai P (2010) Modeling the impact of declining sea ice on the Arctic marine planktonic ecosystem. J Geophys Res 115:C10015CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Centre for Earth and Observation ScienceUniversity of ManitobaWinnipegCanada
  2. 2.Birds and MammalsGreenland Institute of Natural ResourcesNuukGreenland
  3. 3.Natural History Museum of DenmarkUniversity of CopenhagenCopenhagenDenmark
  4. 4.Freshwater Institute, Fisheries and Oceans CanadaWinnipegCanada
  5. 5.Applied Physics LaboratoryUniversity of WashingtonSeattleUSA
  6. 6.Danish Meteorological InstituteClimate and Arctic ResearchCopenhagenDenmark

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