Advertisement

Oecologia

, Volume 157, Issue 1, pp 117–129 | Cite as

Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis

  • S. M. BudgeEmail author
  • M. J. Wooller
  • A. M. Springer
  • S. J. Iverson
  • C. P. McRoy
  • G. J. Divoky
Ecosystem Ecology - Original Paper

Abstract

Global warming and the loss of sea ice threaten to alter patterns of productivity in arctic marine ecosystems because of a likely decline in primary productivity by sea ice algae. Estimates of the contribution of ice algae to total primary production range widely, from just 3 to >50%, and the importance of ice algae to higher trophic levels remains unknown. To help answer this question, we investigated a novel approach to food web studies by combining the two established methods of stable isotope analysis and fatty acid (FA) analysis—we determined the C isotopic composition of individual diatom FA and traced these biomarkers in consumers. Samples were collected near Barrow, Alaska and included ice algae, pelagic phytoplankton, zooplankton, fish, seabirds, pinnipeds and cetaceans. Ice algae and pelagic phytoplankton had distinctive overall FA signatures and clear differences in δ13C for two specific diatom FA biomarkers: 16:4n-1 (−24.0 ± 2.4 and −30.7 ± 0.8‰, respectively) and 20:5n-3 (−18.3 ± 2.0 and −26.9 ± 0.7‰, respectively). Nearly all δ13C values of these two FA in consumers fell between the two stable isotopic end members. A mass balance equation indicated that FA material derived from ice algae, compared to pelagic diatoms, averaged 71% (44–107%) in consumers based on δ13C values of 16:4n-1, but only 24% (0–61%) based on 20:5n-3. Our estimates derived from 16:4n-1, which is produced only by diatoms, probably best represented the contribution of ice algae relative to pelagic diatoms. However, many types of algae produce 20:5n-3, so the lower value derived from it likely represented a more realistic estimate of the proportion of ice algae material relative to all other types of phytoplankton. These preliminary results demonstrate the potential value of compound-specific isotope analysis of marine lipids to trace C flow through marine food webs and provide a foundation for future work.

Keywords

Pelagic phytoplankton Diatoms Trophic linkages Compound specific Lipid 

Notes

Acknowledgements

We thank the whaling captains of Barrow and Kaktovik and the Alaska Eskimo Whaling Commission for providing samples from the whales, C. Hanns and C. George of the North Slope Borough Department of Wildlife Management for organizing and conducting bowhead sample collection, G. Sheehan of the Barrow Arctic Science Consortium for logistical assistance, fishermen at Barrow for providing arctic cod, R. Elsner at the University of Alaska Fairbanks for providing blubber samples from seals, and N. Haubenstock and T. Howe at the Alaska Stable Isotope Facility and J. Gopaul, C. Sumi and A. Timmins at Dalhousie University for technical assistance. D. Phillips and an anonymous reviewer provided comments that greatly improved the manuscript. Whale samples were collected under authorization of National Marine Fisheries Service scientific research permit 481-1464 and 782-1694. Seal specimen collections were authorized by National Marine Fisheries Service scientific research permit 782-1399. This study was funded by the Cooperative Institute for Arctic Research, the Natural Sciences and Engineering Research Council of Canada, and start up funds awarded to M. J. W. from the University of Alaska Fairbanks. Additional support was provided by Friends of Cooper Island. We declare that the study described here complies with the current laws of both the USA and Canada.

References:

  1. Albers CS, Kattner G, Hagen W (1996) The composition of wax esters, triacylglycerols and phospholipids in Arctic and Antarctic copepods: evidence of energetic adaptations. Mar Chem 55:347–358CrossRefGoogle Scholar
  2. Auel H, Harjes M, de Rocha R, Stübing D, Hagen W (2002) Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biol 25:374–383Google Scholar
  3. Booth BC, Horner RA (1997) Microalgae on the Arctic Ocean Section, 1994: species abundance and biomass. Deep Sea Res II 44:1607–1622CrossRefGoogle Scholar
  4. Bradstreet MSW (1980) Thick-billed murres and black guillemots in the Barrow Strait area, N·W.T., during spring: diets and food availability along ice edges. Can J Zool 58:2120–2140CrossRefGoogle Scholar
  5. Bradstreet MSW, Cross WE (1982) Trophic relationships at high Arctic ice edges. Arctic 35:1–12Google Scholar
  6. Budge SM, Parrish CC (1999) Lipid class and fatty acid composition of Pseudo-nitzschia multiseries and Pseudo-nitzschia pungens and effects of lipolytic enzyme deactivation. Phytochemistry 52:561–566CrossRefGoogle Scholar
  7. Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mam Sci 22:759–801CrossRefGoogle Scholar
  8. Budge SM, Springer AM, Iverson SJ, Sheffield G (2007) Fatty acid biomarkers reveal niche separation in an arctic benthic food web. Mar Ecol Prog Ser 336:305–309CrossRefGoogle Scholar
  9. Clarke KR, Green RH (1988) Statistical design and analysis for a ‘biological effects’ study. Mar Ecol Prog Ser 46:213–226CrossRefGoogle Scholar
  10. Conte MH, Volkman JK, Eglinton G (1994) Lipid biomarkers of the Haptophyta. In: Green JC, Leadbeater BSC (eds) The haptophyte algae. Systematics association special volume no. 51. Clarendon Press, Oxford, pp 351–377Google Scholar
  11. Cooper MH (2004) Fatty acid metabolism in marine carnivores: implications for quantitative estimation of predator diets. Ph.D. thesis, Dalhousie University, Halifax, CanadaGoogle Scholar
  12. Cooper MH, Iverson SJ, Heras H (2005) Dynamics of blood chylomicron fatty acids in a marine carnivore: implications for lipid metabolism and quantitative estimation of predator diets. J Comp Physiol B 175:133–145CrossRefPubMedGoogle Scholar
  13. Craig PC, Griffiths WB, Haldorson L, McElderry H (1982) Ecological studies of Arctic cod (Boreogadus saida) in Beaufort Sea coastal waters, Alaska. Can J Fish Aquat Sci 39:395–406CrossRefGoogle Scholar
  14. Dunstan GA, Volkman JK, Barrett SM, Leroi J-M, Jeffrey SW (1994) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155–161CrossRefGoogle Scholar
  15. Falk-Petersen S, Sargent JR, Henderson J, Hegseth EN, Hop H, Okolodkov YB (1998) Lipids and fatty acids in ice algae and phytoplankton from the Marginal Ice Zone in the Barents Sea. Polar Biol 20:41–47CrossRefGoogle Scholar
  16. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509PubMedGoogle Scholar
  17. Gannes LZ, O’Brien DM, Martinez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats and a call for more laboratory experiments. Ecology 78:1271–1276CrossRefGoogle Scholar
  18. Gosselin M, LeVasseur M, Wheeler PA, Horner RA, Booth BC (1997) New measurements of phytoplankton and ice algal production in the Arctic Ocean. Deep Sea Res 44:1623–1644CrossRefGoogle Scholar
  19. Gradinger R (1999) Integrated abundance and biomass of sympagic meiofauna in Arctic and Antarctic pack ice. Polar Biol 22:169–177CrossRefGoogle Scholar
  20. Graeve M, Kattner G, Wiencke C, Karsten U (2002) Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogenetic and trophic relationships. Mar Ecol Prog Ser 231:67–74CrossRefGoogle Scholar
  21. Graeve M, Albers C, Kattner G (2005) Assimilation and biosynthesis of lipids in Arctic Calanus species based on feeding experiments with a 13C labelled diatom. J Exp Mar Biol Ecol 317:109–125CrossRefGoogle Scholar
  22. Harrison PJ, Thompson PA, Calderwood GS (1990) Effects of nutrients and light limitation on the biochemical composition of phytoplankton. J Appl Phycol 2:45–56CrossRefGoogle Scholar
  23. Hill V, Cota G, Stockwell D (2005) Spring and summer phytoplankton communities in the Chukchi and Eastern Beaufort Seas. Deep Sea Res II 52:3369–3385CrossRefGoogle Scholar
  24. Hobson KA (1993) Trophic relationships among high Arctic seabirds: insights from tissue-dependent stable-isotope models. Mar Ecol Prog Ser 95:7–18CrossRefGoogle Scholar
  25. Hobson KA, Fisk A, Karnovsky N, Holst M, Gagnon J-M, Fortier M (2002) A stable isotope (δ13C, δ15 N) 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
  26. Hoekstra PF, Dehn LA, George JC, Solomon KR, Muir DCG, O’Hara TM (2002) Trophic ecology of bowhead whales (Balaena mysticetus) compared with that of other arctic marine biota as interpreted from carbon-, nitrogen-, and sulphur-isotope signatures. Can J Zool 80:223–231CrossRefGoogle Scholar
  27. Iverson SJ (2002) Blubber. In: Perrin WF, Wursig B, Thewissen HGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 107–112Google Scholar
  28. Iverson SJ, Frost KJ, Lang SLC (2002) Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Mar Ecol Prog Ser 241:161–181CrossRefGoogle Scholar
  29. Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diet. Ecol Monogr 74:11–235CrossRefGoogle Scholar
  30. Iverson SJ, Stirling I, Lang SLC (2006) Spatial and temporal variation in the diets of polar bears across the Canadian Arctic: links with and indicators of changes in prey populations. In: Boyd IL, Wanless S, Camphuysen CJ (eds) Top predators in marine ecosystems: their role in monitoring and management. Cambridge University Press, Cambridge, pp 98–117CrossRefGoogle Scholar
  31. Johannessen O, Bengtsson L, Miles MW, Kuzmina SI, Semenov VA, Alekseev GV, Nagurnyi AP, Zakharov VF, Bobylev LP, Pettersson LH, Hasselmann K, Cattle HP (2004) Arctic climate change: observed and modeled temperature and sea-ice variability. Tellus 56:328–341CrossRefGoogle Scholar
  32. Jones EP, Swift JH, Anderson LG, Lipizer M, Civitarse G, Falkner KK, Kattner G, McLaughlin F (2003) Tracing Pacific water in the North Atlantic Ocean. J Geophys Res 108, C4, 3116CrossRefGoogle Scholar
  33. Kirsch PE, Iverson SJ, Bowen WD, Kerr SR, Ackman RG (1998) Dietary effects on the fatty acid signature of whole Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 55:1378–1386CrossRefGoogle Scholar
  34. Kukert H, Riebesell U (1998) Phytoplankton carbon isotope fractionation during a diatom spring bloom in a Norwegian fjord. Mar Ecol Prog Ser 173:127–137CrossRefGoogle Scholar
  35. Lee SH, Schell DM, McDonald TL, Richardson WJ (2005) Regional and seasonal feeding by bowhead whales Balaena mysticetus as indicated by stable isotope ratios. Mar Ecol Prog Ser 285:271–287CrossRefGoogle Scholar
  36. Lowry LF, Frost KJ, Burns JJ (1980a) Feeding of bearded seals in the Bering and Chukchi seas and trophic interactions with Pacific walruses. Arctic 33:330–342CrossRefGoogle Scholar
  37. Lowry LF, Frost KJ, Burns JJ (1980b) Variability in the diet of ringed seals, Phoca hispida, in Alaska. Can J Fish Aquat Sci 37:2254–2261CrossRefGoogle Scholar
  38. Lowry LF, Sheffield G, George JC (2004) Bowhead whale feeding in the Alaskan Beaufort Sea, based on stomach contents analyses. J Cetacean Res Manage 6:215–223Google Scholar
  39. McMahon KW, Ambrose WG, Johnson BJ, Sun M, Lopez GR, Clough LM, Carroll ML (2006) Benthic community response to ice algae and phytoplankton in Ny Alesund, Svalbard. Mar Ecol Prog Ser 310:1–14CrossRefGoogle Scholar
  40. McRoy CP, Goering JJ (1976) Annual budget of primary production in the Bering Sea. Mar Sci Comm 2:255–267Google Scholar
  41. Meier-Augenstein W (2002) Stable isotope analysis of fatty acids by gas chromatography-isotope ratio mass spectrometry. Anal Chim Acta 465:63–79CrossRefGoogle Scholar
  42. Michel C, Legnedre L, Ingram RG, Gosselin M, Lavasseur M (1996) Carbon budget of sea-ice algae in spring: evidence of a significant transfer to zooplankton grazers. J Geophys Res 101:18345–18360CrossRefGoogle Scholar
  43. Monson KD, Hayes JM (1982) Biosynthetic control of the natural abundance of carbon 13 at specific positions within fatty acids in Saccharomyces cerevisiae: isotopic fractionations in lipid synthesis as evidence for peroxisomal regulations. J Biol Chem 257:5568–5575PubMedGoogle Scholar
  44. Moore SE, Reeves RR (1993) Distribution and movement. In: Burns JJ, Montague JJ, Cowles CJ (eds) The bowhead whale. Special publication no. 2. Society for Marine Mammalogy. Allen Press, Lawrence, pp 313–368Google Scholar
  45. Moreno VJ, De Moreno JEA, Brenner RR (1978) Fatty acid metabolism in the calanoid copepod Paracalanus parvus. 1. Polyunsaturated fatty acids. Lipids 14:313–317CrossRefGoogle Scholar
  46. Nanton DA, Castell JD (1999) The effects of temperature and dietary fatty acids on the fatty acid composition of harpacticoid copepods, for use as a live food for marine fish larvae. Aquaculture 175:167–181CrossRefGoogle Scholar
  47. Norsker N-H, Støttrup JG (1994) The importance of dietary HUFAs for fecundity and HUFA content in the harpacticoid, Tisbe holothuriae Humes. Aquaculture 125:155–166CrossRefGoogle Scholar
  48. Parrish DM (1987) Annual primary production in the Alaskan Arctic Ocean. MS thesis. University of Alaska, FairbanksGoogle Scholar
  49. Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT, Wainman BC (eds) Lipids in freshwater ecosystems. Springer, New York, pp 4–20CrossRefGoogle Scholar
  50. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269CrossRefPubMedGoogle Scholar
  51. Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527CrossRefPubMedGoogle Scholar
  52. Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718CrossRefGoogle Scholar
  53. Rieley G (1994) Derivatization of organic compounds prior to gas chromatographic-combustion–isotope ratio mass spectrometric analyses: identification of isotope fractionation processes. Analyst 119:915–919CrossRefGoogle Scholar
  54. Sargent JR, Henderson RJ (1986) Lipids. In: Corner EDS, O’Hara SCM (eds) The biological chemistry of marine copepods. Clarendon, Oxford, pp 59–108Google Scholar
  55. Sargent JR, Falk-Petersen S (1988) The lipid biochemistry of calanoid copepods. Hydrobiologia 167(168):101–114CrossRefGoogle Scholar
  56. Sherr EB, Sherr BF, Wheeler PA, Thompson K (2003) Temporal and spatial variation in stocks of autotrophic and heterotrophic microbes in the upper water column of the central Arctic Ocean. Deep Sea Res I 50:557–571CrossRefGoogle Scholar
  57. Søreide JE, Hop H, Carroll ML, Falk-Petersen S, Hegseth EN (2006) Seasonal food web structures and sympagic–pelagic coupling in the European Arctic revealed by stable isotopes and a two-source food web model. Prog Oceanogr 71:59–87CrossRefGoogle Scholar
  58. Sprecher H (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim Biophys Acta 1486:219–231CrossRefPubMedGoogle Scholar
  59. Springer AM, McRoy CP (1993) The paradox of pelagic food webs in the northern Bering Sea. III. Patterns of primary production. Cont Shelf Res 13:575–599CrossRefGoogle Scholar
  60. Springer AM, McRoy CP, Turco KR (1989) The paradox of pelagic food webs in the northern Bering Sea. II. Zooplankton communities. Cont Shelf Res 9:359–386CrossRefGoogle Scholar
  61. St. John MA, Lund T (1996) Lipid biomarkers: linking the utilization of frontal plankton biomass to enhanced condition of juvenile North Sea cod. Mar Ecol Prog Ser 131:75–85CrossRefGoogle Scholar
  62. Tang KW, Jakobsen HH, Visser AW (2001) Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: feeding, growth, and trophic interactions among grazers. Limnol Oceanogr 46:1860–1870CrossRefGoogle Scholar
  63. Thompson PA, Gou M, Harrison PJ, Whyte JNC (1992) Effects of variation in temperature II. On the fatty acid composition of eight species of marine phytoplankton. J Phycol 28:488–497CrossRefGoogle Scholar
  64. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184CrossRefGoogle Scholar
  65. Viso A, Marty J (1993) Fatty acids from 28 marine microalgae. Prog Lipid Res 32:1521–1533Google Scholar
  66. Walton MJ, Henderson RJ, Pomeroy PP (2000) Use of blubber fatty acid profiles to distinguish dietary differences between grey seals Halichoerus grypus from two UK breeding colonies. Mar Ecol Prog Ser 193:210–208CrossRefGoogle Scholar
  67. Werner I (1997) Grazing of Arctic under-ice amphipods on sea-ice algae. Mar Ecol Prog Ser 160:93–99CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • S. M. Budge
    • 1
    Email author
  • M. J. Wooller
    • 2
    • 3
  • A. M. Springer
    • 3
  • S. J. Iverson
    • 4
  • C. P. McRoy
    • 3
  • G. J. Divoky
    • 5
  1. 1.Department of Process Engineering and Applied ScienceDalhousie UniversityHalifaxCanada
  2. 2.Alaska Stable Isotope Facility, Water and Environmental Research CenterUniversity of Alaska FairbanksFairbanksUSA
  3. 3.Institute of Marine Science, School of Fisheries and Ocean SciencesUniversity of Alaska FairbanksFairbanksUSA
  4. 4.Department of BiologyDalhousie UniversityHalifaxCanada
  5. 5.Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA

Personalised recommendations