Marine Biology

, Volume 160, Issue 6, pp 1311–1323 | Cite as

Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica

  • Michael J. Polito
  • Christian S. Reiss
  • Wayne Z. Trivelpiece
  • William P. Patterson
  • Steven D. Emslie
Original Paper

Abstract

Antarctic krill (Euphausia superba) occupy a key position in the Southern Ocean linking primary production to secondary consumers. While krill is a dominant grazer of phytoplankton, it also consumes heterotrophic prey and the relative importance of these two resources may differ with ontogeny. We used stable isotope analyses to evaluate body size-dependent trophic and habitat shifts in krill during the austral summer around the South Shetland Islands, Antarctica. We found evidence for an asymmetric, ontogenetic niche expansion with adults of both sexes having higher and more variable δ15N values but consistent δ13C values in comparison with juveniles. This result suggests that while phytoplankton likely remains an important life-long resource, krill in our study area expand their dietary niche to include higher trophic food sources as body size increases. The broader dietary niches observed in adults may help buffer them from recent climate-driven shifts in phytoplankton communities that negatively affect larval or juvenile krill that rely predominately on autotrophic resources.

Notes

Acknowledgments

This research was funded by U.S. National Science Foundation (NSF) Office of Polar Programs (OPP) grant ANT-0739575 and the US AMLR program. We thank A. Cossio, K. Dietrich, R. Driscoll, M. Goebel, C. Hewes, V. Loeb, A. VanCise, J. Walsh and the AMLR physical and biological oceanography and zooplankton teams for assistance with the collection of oceanographic data and krill samples. J. Seminoff, K. Durenberger, D. Besic, and J. Blum assisted with lipid extractions, stable isotope, and statistical analyses. J. Hinke, M. Goebel and two anonymous reviewers provided helpful comments on an earlier version of this manuscript.

References

  1. Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Proceedings of the Second International Symposium on Information Theory. Akademiai Kiado, Budapest, pp 267–281Google Scholar
  2. Anderson ORJ, Phillips RA, McDonald RA, Shore RF, McGill RAR, Bearhop S (2009) Influence of trophic position and foraging range on mercury levels within a seabird community. Mar Ecol Prog Ser 375:277–288CrossRefGoogle Scholar
  3. Atkinson A, Snÿder R (1997) Krill–copepod interactions at South Georgia, Antarctica, I. Omnivory by Euphausia superba. Mar Ecol Prog Ser 160:67–76CrossRefGoogle Scholar
  4. Atkinson A, Meyer B, Stübing D, Hagen W, Schmidt K, Bathmann UV (2002) Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter. II. Juveniles and adults. Limnol Oceanogr 47:953–966CrossRefGoogle Scholar
  5. Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103CrossRefGoogle Scholar
  6. Barkley E (1940) Nahrung und Filterapparat des Walkrebschens Euphausia superba Dana. Z Fisch 1:65–156Google Scholar
  7. Cherel Y (2008) Isotopic niches of emperor and Adélie penguins in Adélie Land Antarctica. Mar Biol 54(5):813–821CrossRefGoogle Scholar
  8. Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287CrossRefGoogle Scholar
  9. Cripps GC, Atkinson A (2000) Fatty acid composition as an indicator of carnivory in Antarctic krill, Euphausia superba. Can J Fish Aquat Sci 57(S3):31–37Google Scholar
  10. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  11. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351CrossRefGoogle Scholar
  12. Dunton KH (2001) Delta N-15 and delta C-13 measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41:99–112CrossRefGoogle Scholar
  13. Everson I (2000) Role of krill in marine food webs: the Southern Ocean. In: Everson I (ed) Krill: biology, ecology and fisheries. Blackwell Science, Oxford, pp 194–201Google Scholar
  14. Fach BA, Meyer B, Wolf-Gladrow D, Bathmann U (2008) Biochemically based modeling study of Antarctic krill Euphausia superba growth and development. Mar Ecol Prog Ser 360:147–161CrossRefGoogle Scholar
  15. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  16. Frazer TK, Ross RM, Quetin LB, Montoya JP (1997) Turnover of carbon and nitrogen during growth of larval krill, Euphausia superba Dana: a stable isotope approach. J Exp Mar Biol Ecol 212:259–275CrossRefGoogle Scholar
  17. Freeman KH, Hayes JM (1992) Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO2 levels. Global Biogeochem Cy 6:185–198CrossRefGoogle Scholar
  18. Gille ST (2002) Warming of the Southern Ocean since the 1950s. Science 295(5558):1275–1277CrossRefGoogle Scholar
  19. Gómez I, Wulff A, Roleda MY, Huovinen P, Karsten U, Quartino ML, Dunton K, Wiencke C (2009) Light and temperature demands of marine benthic microalgae and seaweeds in polar regions. Bot Mar 52:593–608Google Scholar
  20. Gorokhova E, Hansson S (1999) An experimental study on variations in stable carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Can J Fish Aquat Sci 56:2203–2210CrossRefGoogle Scholar
  21. Graham BS, Grubbs D, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar Biol 150(4):647–658CrossRefGoogle Scholar
  22. Granéli E, Granéli W, Rabbani MM, Daugbjerg N, Fransz G, Cuzin-Roudy J, Alder VA (1993) The influence of copepod and krill grazing on the species composition of phytoplankton communities from the Scotia-Weddell Sea. Polar Biol 13:201–213CrossRefGoogle Scholar
  23. Haberman KL, Ross RM, Quetin LB (2003) Diet of the Antarctic krill (Euphausia superba Dana): II. Selective grazing in mixed phytoplankton assemblages. J Exp Mar Biol Ecol 283:97–113CrossRefGoogle Scholar
  24. Hammerschlag-Peyer CM, Yeager LA, Araújo MS, Layman CA (2011) A hypothesis-testing framework for studies investigating ontogenetic niche shifts using stable isotope ratios. PLoS ONE 6(11):e27104CrossRefGoogle Scholar
  25. Hamner WM (1988) Biomechanics of filter feeding in the Antarctic krill Euphausia superba: review of past work and new observations. J Crustac Biol 8:149–163CrossRefGoogle Scholar
  26. Hamner WM, Hamner PP (2000) Behavior of Antarctic krill (Euphausia superba): schooling, foraging, and antipredatory behavior. Can J Fish Aquat Sci 57:192–202CrossRefGoogle Scholar
  27. Hernández-León S, Almeida C, Portillo-Hahnefeld A, Bé-cognée P, Moreno I (2001) Diel feeding behaviour of krill in the Gerlache Strait, Antarctica. Mar Ecol Prog Ser 223:235–242CrossRefGoogle Scholar
  28. Hewes CD, Reiss CS, Holm-Hansen O (2009) A quantitative analysis of sources for summertime phytoplankton variability over 18 years in the South Shetland Islands (Antarctica) region. Deep-Sea Res I 56:1230–1241CrossRefGoogle Scholar
  29. Hill JM, McQuaid CD (2011) Stable isotope methods: the effect of gut contents on isotopic ratios of zooplankton. Estuar Coast Shelf Sci 92(3):480–485CrossRefGoogle Scholar
  30. Hilton GM, Thompson DR, Sagar PM, Cuthbert RJ, Cherel Y, Bury SJ (2006) A stable isotopic investigation into the causes of decline in a sub-Antarctic predator, the rockhopper penguin Eudyptes chrysocome. Global Change Biol 12:611–625CrossRefGoogle Scholar
  31. Hinga KR, Arthur MA, Pilson MEO, Whitaker D (1994) Carbon isotope fractionation by marine phytoplankton in culture: the effects of CO2 concentration, pH, temperature, and species. Global Biogeochem Cy 8:91–102CrossRefGoogle Scholar
  32. Hirons AC, Schell DM, Finney BP (2001) Temporal records of δ13C and δ15N in North Pacific pinnipeds: inferences regarding environmental change and diet. Oecologia 129:591–601Google Scholar
  33. Hodum PJ, Hobson KA (2000) Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable isotope (δ15N and δ13C) analyses. Mar Ecol Prog Ser 198:273–281CrossRefGoogle Scholar
  34. Holm-Hansen O, Riemann B (1978) Chlorophyll a determination: improvements in methodology. Oikos 30:438–447CrossRefGoogle Scholar
  35. Hutchinson GE (1957) Concluding remarks, cold spring harbor symposium. Quant Biol 22:415–427CrossRefGoogle Scholar
  36. Hutchinson GE (1959) Homage to Santa Rosalia, or why are there so many kinds of animals? Am Nat 93:145–159CrossRefGoogle Scholar
  37. Jaeger A, Cherel Y (2011) Isotopic investigation of contemporary and historic changes in penguin trophic niches and carrying capacity of the Southern Indian Ocean. PLoS ONE 6(2):e16484CrossRefGoogle Scholar
  38. Ju SJ, Harvey HR (2004) Lipids as markers of nutritional condition and diet in the Antarctic krill Euphausia superba and Euphausia crystallorophias during austral winter. Deep-Sea Res II 51:2199–2214CrossRefGoogle Scholar
  39. Lara RJ, Alder V, Franzosi CA, Kattner G (2010) Characteristics of suspended particulate organic matter in the southwestern Atlantic: influence of temperature, nutrient and phytoplankton features on the stable isotope signature. J Marine Syst 79(1–2):199–209CrossRefGoogle Scholar
  40. Laws RM (1985) The ecology of the Southern Ocean. Am Sci 73:26–40Google Scholar
  41. 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 59:1131–1138CrossRefGoogle Scholar
  42. Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide quantitative measures of trophic diversity within food webs? Ecology 88:42–48CrossRefGoogle Scholar
  43. Maciejewska K (1993) Feeding of Antarctic krill Euphausia superba. Pol Polar Res 14:43–54Google Scholar
  44. Martínez del Rio C, Wolf BO (2005) Mass balance models for animal isotopic ecology. In: Starck MA, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, Enfield, pp 141–174Google Scholar
  45. Meyer B, Auerswald L, Siegel V, SpahiT S, Pape C, Fach B, Teschke M, Lopata A, Fuentes V (2010) Seasonal variation in body composition, metabolic activity, feeding, and growth of adult krill Euphausia superba in the Lazarev Sea. Mar Ecol Prog Ser 398:1–18CrossRefGoogle Scholar
  46. Miller TE, Rudolf VH (2011) Thinking inside the box: community-level consequences of stage-structured populations. Trends Ecol Evol 26(9):457–466CrossRefGoogle Scholar
  47. Miller AK, Trivelpiece WZ (2007) Cycles of Euphausia superba recruitment evident in the diet of Pygoscelid penguins and net trawls in the South Shetland Islands, Antarctica. Polar Biol 30:1615–1623CrossRefGoogle Scholar
  48. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140CrossRefGoogle Scholar
  49. Moline MA, Claustere H, Frazer TK, Schofield O, Vernet M (2004) Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Glob Change Biol 10:1973–1980CrossRefGoogle Scholar
  50. Montes-Hugo M, Doney SC, Ducklow HW, Fraser W, Martinson D, Stammerjohn SE, Schofield O (2009) Recent changes in phytoplankton communities associated with rapid regional climate change along the western Antarctic Peninsula. Science 323:1470–1473CrossRefGoogle Scholar
  51. Newsome SD, Martínez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436Google Scholar
  52. Opaliński KW, Maciejewska K, Georgieva LV (1997) Notes on food selection in the Antarctic krill Euphausia superba. Polar Biol 17:350–357CrossRefGoogle Scholar
  53. Pakhomov EA, Perissinotto R, Froneman PW, Miller DGM (1997) Energetics and feeding of Euphausia superba in the South Georgia region during the summer of 1994. J Plankton Res 19:399–423CrossRefGoogle Scholar
  54. Park JI, Kang CK, Suh HL (2011) Ontogenetic diet shift in the euphausiid Euphausia pacifica quantified using stable isotope analysis. Mar Ecol Prog Ser 429:103–109CrossRefGoogle Scholar
  55. Perissinotto R, Gurney L, Pakhomov EA (2000) Contribution of heterotrophic material to diet and energy budget of Antarctic krill, Euphausia superba. Mar Biol 136:129–135CrossRefGoogle Scholar
  56. Polito MJ, Goebel ME (2010) Investigating the use of stable isotope analysis of milk to infer seasonal trends in the diets and foraging habitats of female Antarctic fur seals. J Exp Mar Biol Ecol 39:1–9CrossRefGoogle Scholar
  57. Polito MJ, Fisher S, Tobias CR, Emslie SD (2009) Tissue- specific isotopic discrimination factors in gentoo penguin (Pygoscelis papua) egg components: implications for dietary reconstructions using stable isotopes. J Exp Mar Biol Ecol 372:106–112CrossRefGoogle Scholar
  58. Polito MJ, Lynch HJ, Naveen R, Emslie SD (2011a) Stable isotopes reveal regional heterogeneity in the pre-breeding distribution and diets of sympatrically breeding Pygoscelis spp. penguins. Mar Ecol Prog Ser 421:265–277CrossRefGoogle Scholar
  59. Polito MJ, Trivelpiece WZ, Karnovsky NJ, Ng E, Patterson WP, Emslie SD (2011b) Integrating stomach content and stable isotope analyses to quantify the diets of pygoscelid penguins. PLoS ONE 6:e26642CrossRefGoogle Scholar
  60. Rau GH, Takahashi T, Des Marais DJ, Sullivan CW (1991) Particulate organic matter δ13C variations across the Drake Passage. J Geophys Res 96:15131–15135CrossRefGoogle Scholar
  61. Reich KJ, Bjorndal KA, Martínez del Rio C (2008) Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155:651–663CrossRefGoogle Scholar
  62. Reid K, Murphy EJ, Loeb V, Hewitt RP (2002) Krill population dynamics in the Scotia Sea: variability in growth and mortality within a single population. J Mar Syst 36:1–10CrossRefGoogle Scholar
  63. Reiss CS, Cossio AM, Loeb V, Demer DA (2008) Variations in the biomass of Antarctic krill (Euphausia superba) around the South Shetland Islands, 1996–2006. ICES J Mar Sci 65(4):497–508CrossRefGoogle Scholar
  64. Rudolf VHW, Lafferty KD (2011) Stage structure alters how complexity affects stability of ecological networks. Ecol Lett 14(1):75–79CrossRefGoogle Scholar
  65. Scharf FS, Juanes F, Rountree RA (2000) Predator size-prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248CrossRefGoogle Scholar
  66. Schell DM (2000) Declining carrying capacity in the Bering Sea: isotopic evidence from whale baleen. Limnol Oceanogr 45:459–462CrossRefGoogle Scholar
  67. Schell DM, Barnett BA, Vinette KA (1998) Carbon and nitrogen isotope ratios in zooplankton of the Bering, Chukchi and Beaufort seas. Mar Ecol Prog Ser 162:11–23CrossRefGoogle Scholar
  68. Schmidt K, Atkinson A, Stübing D, McClelland JW, Montoya JP, Voss M (2003) Trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnol Oceanogr 48(1):277–289CrossRefGoogle Scholar
  69. Schmidt K, McClelland JW, Mente E, Montoya JP, Atkinson A, Voss M (2004) Trophic-level interpretation based on δ15N values: implications of tissue-specific fractionation and amino acid composition. Mar Ecol Prog Ser 266:43–58CrossRefGoogle Scholar
  70. Schmidt K, Atkinson A, Petzke KJ, Voss M, Pond DW (2006) Protozoans as a food source for Antarctic krill, Euphausia superba: complementary insights from stomach content, fatty acids, and stable isotopes. Limnol Oceanogr 51:2409–2427CrossRefGoogle Scholar
  71. Schmidt K, Atkinson A, Steigenberger S, Fielding S, Lindsay MCM, Pond DW, Tarling GA, Klevjer TA, Allen CS, Nicol S, Achterberg EP (2011) Seabed foraging by Antarctic krill: implications for stock assessment, bentho-pelagic coupling and the vertical transfer of iron. Limnol Oceanogr 56:1411–1428CrossRefGoogle Scholar
  72. Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional stress on seabird stable isotope ratios. Oecologia 159:41–48CrossRefGoogle Scholar
  73. Seminoff JA, Bjorndal KA, Bolten AB (2007) Stable carbon and nitrogen isotope discrimination and turnover in pond sliders Trachemys scripta: insights for trophic study of freshwater turtles. Copeia 2007(3):534–542Google Scholar
  74. Siegel V, Loeb V (1994) Length and age at maturity of Antarctic krill. Antarct Sci 6:479–482CrossRefGoogle Scholar
  75. Siegel V, Nicol S (2000) Population parameters. In: Everson I (ed) Krill biology, ecology and fisheries. Blackwell Science, London, pp 103–149Google Scholar
  76. Siegel V, Kawaguchi S, Ward P, Litvinov F, Sushin V, Loeb V, Watkins J (2004) Krill demography and large-scale distribution in the southwest Atlantic during January/February 2000. Deep Sea Res II 51:1253–1273Google Scholar
  77. Stammerjohn SE, Martinson DG, Smith RC, Iannuzzi RA (2008) Sea ice in the western Antarctic Peninsula region: spatio-temporal variability from ecological and climate change perspectives. Deep-Sea Res II 55:2041–2058CrossRefGoogle Scholar
  78. Stowasser G, Atkinson A, McGill RAR, Phillips RA, Collins MA, Pond DW (2012) Food web dynamics in the Scotia Sea in summer: a stable isotope study. Deep-Sea Res II 59–60:208–221CrossRefGoogle Scholar
  79. Tierney M, Southwell C, Emmerson LM, Hindell MA (2008) Evaluating and using stable-isotope analysis to infer diet composition and foraging ecology of Adélie penguins Pygoscelis adeliae. Mar Ecol Prog Ser 355:297–307CrossRefGoogle Scholar
  80. Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci USA 108:7625–7628CrossRefGoogle Scholar
  81. Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet isotope spacing in rapidly growing animal. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Sp 29:3239–3247CrossRefGoogle Scholar
  82. Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233CrossRefGoogle Scholar
  83. Van Cise AM (2009) AMLR 2008/2009 field season report: objectives, accomplishments and tentative conclusions. U.S. Department of Commerce, NOAA Technical Memorandum NMFS, NOAA-TM-NMFS-SWFSC-445, 83 pGoogle Scholar
  84. Vaughan DG, Marshall GJ, Connolley WM, Parkinson CL, Mulvaney R, Hodgson DA, King JC, Pudsey CJ, Turner J (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Clim Change 60:243–274CrossRefGoogle Scholar
  85. Wada E, Terazaki M, Kabaya Y, Nemoto T (1987) 15 N and 13C abundances in the Antarctic ocean with emphasis on the biogeochemical structure of the food web. Deep-Sea Res I 34:829–841CrossRefGoogle Scholar
  86. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–394CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Michael J. Polito
    • 1
    • 2
  • Christian S. Reiss
    • 3
  • Wayne Z. Trivelpiece
    • 3
  • William P. Patterson
    • 4
  • Steven D. Emslie
    • 2
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA
  2. 2.Department of Biology and Marine BiologyUniversity of North Carolina WilmingtonWilmingtonUSA
  3. 3.Antarctic Ecosystem Research DivisionNational Marine Fisheries Service, Southwest Fisheries Science CenterLa JollaUSA
  4. 4.Department of Geological Sciences, Saskatchewan, Isotope LaboratoryUniversity of SaskatchewanSaskatoonCanada

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