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.
Similar content being viewed by others
References
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 267–281
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 375:277–288
Atkinson A, Snÿder R (1997) Krill–copepod interactions at South Georgia, Antarctica, I. Omnivory by Euphausia superba. Mar Ecol Prog Ser 160:67–76
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 47:953–966
Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103
Barkley E (1940) Nahrung und Filterapparat des Walkrebschens Euphausia superba Dana. Z Fisch 1:65–156
Cherel Y (2008) Isotopic niches of emperor and Adélie penguins in Adélie Land Antarctica. Mar Biol 54(5):813–821
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 329:281–287
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):31–37
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Dunton KH (2001) Delta N-15 and delta C-13 measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41:99–112
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 194–201
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 360:147–161
France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312
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 212:259–275
Freeman KH, Hayes JM (1992) Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO2 levels. Global Biogeochem Cy 6:185–198
Gille ST (2002) Warming of the Southern Ocean since the 1950s. Science 295(5558):1275–1277
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 52:593–608
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 56:2203–2210
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):647–658
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 13:201–213
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 283:97–113
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):e27104
Hamner WM (1988) Biomechanics of filter feeding in the Antarctic krill Euphausia superba: review of past work and new observations. J Crustac Biol 8:149–163
Hamner WM, Hamner PP (2000) Behavior of Antarctic krill (Euphausia superba): schooling, foraging, and antipredatory behavior. Can J Fish Aquat Sci 57:192–202
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 223:235–242
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 56:1230–1241
Hill JM, McQuaid CD (2011) Stable isotope methods: the effect of gut contents on isotopic ratios of zooplankton. Estuar Coast Shelf Sci 92(3):480–485
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 12:611–625
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 8:91–102
Hirons AC, Schell DM, Finney BP (2001) Temporal records of δ13C and δ15N in North Pacific pinnipeds: inferences regarding environmental change and diet. Oecologia 129:591–601
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 198:273–281
Holm-Hansen O, Riemann B (1978) Chlorophyll a determination: improvements in methodology. Oikos 30:438–447
Hutchinson GE (1957) Concluding remarks, cold spring harbor symposium. Quant Biol 22:415–427
Hutchinson GE (1959) Homage to Santa Rosalia, or why are there so many kinds of animals? Am Nat 93:145–159
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):e16484
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 51:2199–2214
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):199–209
Laws RM (1985) The ecology of the Southern Ocean. Am Sci 73:26–40
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 59:1131–1138
Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide quantitative measures of trophic diversity within food webs? Ecology 88:42–48
Maciejewska K (1993) Feeding of Antarctic krill Euphausia superba. Pol Polar Res 14:43–54
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 141–174
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 398:1–18
Miller TE, Rudolf VH (2011) Thinking inside the box: community-level consequences of stage-structured populations. Trends Ecol Evol 26(9):457–466
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 30:1615–1623
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 48:1135–1140
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 10:1973–1980
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 323:1470–1473
Newsome SD, Martínez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436
Opaliński KW, Maciejewska K, Georgieva LV (1997) Notes on food selection in the Antarctic krill Euphausia superba. Polar Biol 17:350–357
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 19:399–423
Park JI, Kang CK, Suh HL (2011) Ontogenetic diet shift in the euphausiid Euphausia pacifica quantified using stable isotope analysis. Mar Ecol Prog Ser 429:103–109
Perissinotto R, Gurney L, Pakhomov EA (2000) Contribution of heterotrophic material to diet and energy budget of Antarctic krill, Euphausia superba. Mar Biol 136:129–135
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 39:1–9
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 372:106–112
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 421:265–277
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:e26642
Rau GH, Takahashi T, Des Marais DJ, Sullivan CW (1991) Particulate organic matter δ13C variations across the Drake Passage. J Geophys Res 96:15131–15135
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 155:651–663
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 36:1–10
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):497–508
Rudolf VHW, Lafferty KD (2011) Stage structure alters how complexity affects stability of ecological networks. Ecol Lett 14(1):75–79
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 208:229–248
Schell DM (2000) Declining carrying capacity in the Bering Sea: isotopic evidence from whale baleen. Limnol Oceanogr 45:459–462
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 162:11–23
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):277–289
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 266:43–58
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 51:2409–2427
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 56:1411–1428
Sears J, Hatch SA, O’Brien DM (2009) Disentangling effects of growth and nutritional stress on seabird stable isotope ratios. Oecologia 159:41–48
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):534–542
Siegel V, Loeb V (1994) Length and age at maturity of Antarctic krill. Antarct Sci 6:479–482
Siegel V, Nicol S (2000) Population parameters. In: Everson I (ed) Krill biology, ecology and fisheries. Blackwell Science, London, pp 103–149
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 51:1253–1273
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 55:2041–2058
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 59–60:208–221
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 355:297–307
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 108:7625–7628
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 29:3239–3247
Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233
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 p
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 60:243–274
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 34:829–841
Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–394
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Atkinson.
Rights and permissions
About this article
Cite this article
Polito, M.J., Reiss, C.S., Trivelpiece, W.Z. et al. Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica. Mar Biol 160, 1311–1323 (2013). https://doi.org/10.1007/s00227-013-2182-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-013-2182-z