Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis

ZHANG Ye; LI Chaolun; YANG Guang; WANG Yanqing; TAO Zhencheng; ZHANG Yongshan; WANG Aijun

doi:10.1007/s13131-017-1049-4

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Article Navigation > Acta Oceanologica Sinica > 2017 > 36(12): 67-78

ZHANG Ye, LI Chaolun, YANG Guang, WANG Yanqing, TAO Zhencheng, ZHANG Yongshan, WANG Aijun. Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis[J]. Acta Oceanologica Sinica, 2017, 36(12): 67-78. doi: 10.1007/s13131-017-1049-4

Citation:

ZHANG Ye, LI Chaolun, YANG Guang, WANG Yanqing, TAO Zhencheng, ZHANG Yongshan, WANG Aijun. Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis[J]. Acta Oceanologica Sinica, 2017, 36(12): 67-78. doi: 10.1007/s13131-017-1049-4

Citation:

ZHANG Ye, LI Chaolun, YANG Guang, WANG Yanqing, TAO Zhencheng, ZHANG Yongshan, WANG Aijun. Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis[J]. Acta Oceanologica Sinica, 2017, 36(12): 67-78. doi: 10.1007/s13131-017-1049-4

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Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis

doi: 10.1007/s13131-017-1049-4

1.
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;University of Chinese Academy of Sciences, Beijing 100049, China;Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
2.
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
3.
Third Institute of Oceanography, State Oceanic Administration, Xiamen 361005, China

Received Date: 2016-01-20

Abstract

Abstract

As one of the most common and dominant species in the Southern Ocean, Antarctic krill (Euphausia superba) play a significant role in food web structure and the process of energy flow. The diet of Antarctic krill in the Prydz Bay during austral summer of 2012/2013 was investigated and the ontogenetic shift in krill diet was evaluated using the stable isotope method. The nitrogen stable isotope values (δ¹⁵N) of adults ((2.78±0.58)‰) were much higher than those of juveniles ((1.69±0.70)‰), whereas the carbon stable isotope values (δ¹³C) of adults (-(28.26±1.08)‰) were slightly lower than those of juveniles (-(27.48±1.35)‰). Particulate organic matter (POM) from 0, 25, and 50 m depth combined (0/25/50 m) represented phytoplankton food items. The results showed that phytoplankton food items in surface water and mesozooplankton were two essential food items for Antarctic krill in the Prydz Bay during summer. POM (0/25/50 m) contributes 56%-69% and 26%-34% to the diet of juvenile and adult krill, respectively, whereas mesozooplankton composes 13%-34% and 58%-71% of the diet of juvenile and adult krill, respectively. Thus, an ontogenetic diet shift from POM (0/25/50 m), which consists mainly of phytoplankton, to a higher trophic level diet containing mesozooplankton, was detected. The capacity for adults to consume more zooplankton food items may minimize their food competition with juveniles, which rely mostly on phytoplankton food items. This suggests “diet shift with ontogeny” which may somehow help krill keep their dietary energy budget balanced and well adapted to the Antarctic marine ecosystem as a dominant species.
- Antarctic krill,
- Prydz Bay,
- diet shift,
- stable isotope,
- IsoSource

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References(73)

References

Alexander S A, Hobson K A, Gratto-Trevor C L. 1996. Conventional and isotopic determinations of shorebird diets at an inland stopover: the importance of invertebrates and Potamogeton pectinatus tubers. Canadian Journal of Zoology, 74(6): 1057-1068

Atkinson A, Meyer B, Stubing D. 2002. Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter: Ⅱ. Juveniles and adults. Limnology and Oceanography, 47(4): 953-966

Atkinson A, Siegel V, Pakhomov E. 2004. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature, 432(7013): 100-103

Atkinson A, Snÿder R. 1997. Krill-copepod interactions at South Georgia, Antarctica: I. omnivory by Euphausia superba. Marine Ecology Progress Series, 160: 63-76

Atkinson A, Ward P, Hill A. 1999. Krill-copepod interactions at South Georgia, Antarctica: Ⅱ. Euphausia superba as a major control on copepod abundance. Marine Ecology Progress Series, 176: 63-79

Båmstedt U, Gifford D J, Irigoien X, et al. 2000. Feeding. In: Harris R, Wiebe P, Lenz J, et al., eds. ICES Zooplankton Methodology Manual. London: Academic Press

Benstead J P, March J G, Fry B. 2006. Testing IsoSource: stable isotope analysis of a tropical fishery with diverse organic matter sources. Ecology, 87(2): 326-333

Boyd C M, Heyraud M, Boyd C N. 1984. Feeding of the Antarctic krill Euphausia superba. Journal of Crustacean Biology, 4(S1): 123-141

Brodie C R, Casford J S L, Lloyd J M. 2011. Evidence for bias in C/N, δ¹³C and δ¹⁵N values of bulk organic matter, and on environmental interpretation, from a lake sedimentary sequence by pre-analysis acid treatment methods. Quaternary Science Reviews, 30(21-22): 3076-3087

Cabana G, Rasmussen J B. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences of the United States of America, 93(20): 10844-10847

Cherel Y, Ducatez S, Fontaine C. 2008. Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Marine Ecology Progress Series, 370: 239-247

Daly K, Macaulay M C. 1991. Influence of physical and biological mesoscale dynamics on the seasonal distribution and behavior of Euphausia superba in the Antarctic marginal ice zone. Marine Ecology Progress Series, 79(1): 37-66

Daly K L. 1990. Overwintering development, growth, and feeding of larval Euphausia superba in the Antarctic marginal ice zone. Limnology and Oceanography, 35(7): 1564-1576

Daly K L. 2004. Overwintering growth and development of larval Euphausia superba: an interannual comparison under varying environmental conditions west of the Antarctic Peninsula. Deep Sea Research Part Ⅱ: Topical Studies in Oceanography, 51(17-19): 2139-2168

DeNiro M J, Epstein S. 1977. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science, 197(4300): 261-263

Everson I. 2000. Krill: Biology, Ecology and Fisheries. Oxford Malden, MA: Blackwell Science, 1-372

Fischer G. 1991. Stable carbon isotope ratios of plankton carbon and sinking organic matter from the Atlantic sector of the Southern Ocean. Marine Chemistry, 35(1-4): 581-596

Gurney L J, Froneman P W, Pakhomov E A. 2001. Trophic positions of three euphausiid species from the Prince Edward Islands (Southern Ocean): implications for the pelagic food web structure. Marine Ecology Progress Series, 217: 167-174

Haberman K L, Quetin L B, Ross R M. 2003a. Diet of the Antarctic krill (Euphausia superba Dana): I. Comparisons of grazing on Phaeocystis antarctica (Karsten) and Thalassiosira antarctica (Comber). Journal of Experimental Marine Biology and Ecology, 283(1-2): 79-95

Haberman K L, Ross R M, Quetin L B. 2003b. Diet of the Antarctic krill (Euphausia superba Dana): Ⅱ. Selective grazing in mixed phytoplankton assemblages. Journal of Experimental Marine Biology and Ecology, 283(1-2): 97-113

Hansson L A, Tranvik L J. 2003. Food webs in sub-Antarctic lakes: a stable isotope approach. Polar Biology, 26(12): 783-788

Hellmann C, Wissel B, Winkelmann C. 2013. Omnivores as seasonally important predators in a stream food web. Freshwater Science, 32(2): 548-562

Hodum P J, Hobson K A. 2000. Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable-isotope (δ¹⁵N and δ¹³C) analyses. Marine Ecology Progress Series, 198: 273-281

Hopkins T L, Torres J J. 1989. Midwater food web in the vicinity of a marginal ice zone in the western Weddell Sea. Deep Sea Research Part I. Oceanographic Research Papers, 36(4): 543-560

Hosie G W. 1991. Distribution and abundance of euphausiid larvae in the Prydz Bay region, Antarctica. Antarctic Science, 3(2): 167-180

Hosie G W, Cochran T G. 1994. Mesoscale distribution patterns of macrozooplankton communities in Prydz Bay, Antarctica-January to February 1991. Marine Ecology Progress Series, 106(1-2): 21-39

Hosie G W, Ikeda T, Stolp M. 1988. Distribution, abundance and population structure of the Antarctic krill (Euphausia superba Dana) in the Prydz Bay region, Antarctica. Polar Biology, 8(3): 213-224

Kiljunen M, Grey J, Sinisalo T. 2006. A revised model for lipid-normalizing delta δ¹³C values from aquatic organisms, with implications for isotope mixing models. Journal of Applied Ecology, 43(6): 1213-1222

Kopczyńska E E, Goeyens L, Semeneh M. 1995. Phytoplankton composition and cell carbon distribution in Prydz Bay, Antarctica: relation to organic particulate matter and its δ¹³C values. Journal of Plankton Research, 17(4): 685-707

Legendre L, Ackley S F, Dieckmann G S. 1992. Ecology of sea ice biota. Polar Biology, 12(3-4): 429-444

Lesage V, Hammill M O, Kovacs K M. 2001. Marine mammals and the community structure of the Estuary and Gulf of St Lawrence, Canada: evidence from stable isotope analysis. Marine Ecology Progress Series, 210: 203-221

Maciejewska K. 1993. Feeding of antarctic krill Euphausia superba in Weddell sea. Polish Polar Research, 14(1): 43-54

McClatchie S, Boyd C M. 1983. Morphological study of sieve efficiencies and mandibular surfaces in the Antarctic krill, Euphausia superba. Canadian Journal of Fisheries and Aquatic Sciences, 40(7): 955-967

McConnaughey T, McRoy C P. 1979. Food-web structure and the fractionation of carbon isotopes in the bering sea. Marine Biology, 53(3): 257-262

Meyer B, Atkinson A, Stöbing D. 2002. Feeding and energy budgets of Antarctic krill Euphausia superba at the onset of winter: I. Furcilia Ⅲ larvae. Limnology and Oceanography, 47(4): 943-952

Minagawa M, Wada E. 1984. Stepwise enrichment of ¹⁵N along food chains: further evidence and the relation between δ¹⁵N and animal age. Geochimica et Cosmochimica Acta, 48(5): 1135-1140

Miquel J C. 1991. Distribution and abundance of post-larval krill (Euphausia superba Dana) near Prydz Bay in summer with reference to environmental conditions. Antarctic Science, 3(3): 279-292

Neill C, Cornwell J C. 1992. Stable carbon, nitrogen, and sulfur isotopes in a prairie marsh food web. Wetlands, 12(3): 217-224

Nicol S. 2006. Krill, currents, and sea ice: Euphausia superba and its changing environment. BioScience, 56(2): 111-120

Nordhausen W. 1994. Winter abundance and distritubion of Euphausia superba, E. crystallorophias, and Thysanoessa macrura in Gerlache Strait amd Crystal Sound, Antarctica. Marine Ecology Progress Series, 109(2-3): 131-142

Norkko A, Thrush S T, Cummings V J. 2007. Trophic structure of coastal Antarctic food webs associated with changes in sea ice and food supply. Ecology, 88(11): 2810-2820

Ogle K, Tucker C, Cable J M. 2014. Beyond simple linear mixing models: process-based isotope partitioning of ecological processes. Ecological Applications, 24(1): 181-195

Park J I, Kang C K, Suh H L. 2011. Ontogenetic diet shift in the euphausiid Euphausia pacifica quantified using stable isotope analysis. Marine Ecology Progress Series, 429: 103-109

Perissinotto R, Gurney L, Pakhomov E A. 2000. Contribution of heterotrophic material to diet and energy budget of Antarctic krill, Euphausia superba. Marine Biology, 136(1): 129-135

Phillips D L, Gregg J W. 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia, 136(2): 261-269

Phillips D L, Newsome S D, Gregg J W. 2005. Combining sources in stable isotope mixing models: alternative methods. Oecologia, 144(4): 520-527

Polito M J, Reiss C S, Trivelpiece W Z. 2013. Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica. Marine Biology, 160(6): 1311-1323

Ponomareva L A. 1954. Euphausiids of the Sea of Japan feeding on copepods. Dokl Akad Nauk SSSR, 98: 153-154

Post D M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83(3): 703-718

Price H J, Boyd K R, Boyd C M. 1988. Omnivorous feeding behavior of the Antarctic krill Euphausia superba. Marine Biology, 97(1): 67-77

Pu Shuzhen, Dong Zhaoqian. 2003. Progress in physical oceanographic studies of Prydz Bay and its adjacent oceanic area. Chinese Journal of Polar Research (in Chinese), 15(1): 53-64

Quetin L B, Ross R M. 1991. Behavioral and physiological characteristics of the Antarctic krill, Euphausia superba. American Zoologist, 31(1): 49-63

Quetin L B, Ross R M. 2009. Life under Antarctic pack ice: a krill perspective. In: Krupnik I, Lang M A, Miller S E, eds. Smithsonian at the Poles: Contributions to International Polar Year Science. Washington, DC: Smithsonian Institution Scholarly Press, doi: 10.5479/si.097884601X.21

Rau G H, Hopkins T L, Torres J J. 1991a. ¹⁵N/¹⁴N and ¹³C/¹²C in Weddell Sea invertebrates: implications for feeding diversity. Marine Ecology Progress Series, 77(1): 1-6

Rau G H, Sullivan C W, Gordon L I. 1991b. δ¹³C and δ¹⁵N variations in Weddell Sea particulate organic matter. Marine Chemistry, 35(1-4): 355-369

Rau G H, Takahashi T, Des Marais D J. 1991c. Particulate organic matter δ¹³C variations across the Drake Passage. Journal of Geophysical Research, 96(C8): 15131-15135

Ross R M, Quetin L B, Newberger T. 2004. Growth and behavior of larval krill (Euphausia superba) under the ice in late winter 2001 west of the Antarctic Peninsula. Deep Sea Research Part Ⅱ: Topical Studies in Oceanography, 51(17-19): 2169-2184

Schmidt K, Atkinson A, Petzke K J. 2006. Protozoans as a food source for Antarctic krill, Euphausia superba: complementary insights from stomach content, fatty acids, and stable isotopes. Limnology and Oceanography, 51(5): 2409-2427

Schmidt K, Atkinson A, Pond D W. 2014. Feeding and overwintering of Antarctic krill across its major habitats: the role of sea ice cover, water depth, and phytoplankton abundance. Limnology and Oceanography, 59(1): 17-36

Schmidt K, Atkinson A, Steigenberger S. 2011. Seabed foraging by Antarctic krill: implications for stock assessment, bentho-pelagic coupling, and the vertical transfer of iron. Limnology and Oceanography, 56(4): 1411-1428

Schmidt K, Atkinson A, Stübing D. 2003. Trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnology and Oceanography, 48(1): 277-289

Siegel V, Bergström B, Strömberg J O. 1990. Distribution, size frequencies and maturity stages of krill, Euphausia superba, in relation to sea-ice in the northern Weddell Sea. Polar Biology, 10(7): 549-557

Smith N R, Dong Zhaoqian, Kerry K R. 1984. Water masses and circulation in the region of Prydz Bay, Antarctica. Deep Sea Research Part I. Oceanographic Research Papers, 31(9): 1121-1147

Søreide J E, Hop H, Carroll M L. 2006. Seasonal food web structures and sympagic-pelagic coupling in the European Arctic revealed by stable isotopes and a two-source food web model. Progress in Oceanography, 71(1): 59-87

Stowasser G, Atkinson A, McGill R A R. 2012. Food web dynamics in the Scotia Sea in summer: a stable isotope study. Deep Sea Research Part Ⅱ: Topical Studies in Oceanography, 59-60: 208-221

Suh H L, Choi S D. 1998. Comparative morphology of the feeding basket of five species of Euphausia (Crustacea, Euphausiacea) in the western North Pacific, with some ecological considerations. Hydrobiologia, 385(1-3): 107-112

Suh H L, Nemoto T. 1987. Comparative morphology of filtering structure of five species of Euphausia (Euphausiacea, Crustacea) from the Antarctic Ocean. Proceedings of the NIPR Symposium on Polar Biology, 1: 72-83

Taki K, Yabuki T, Noiri Y. 2008. Horizontal and vertical distribution and demography of euphausiids in the Ross Sea and its adjacent waters in 2004/2005. Polar Biology, 31(11): 1343-1356

Thomas P G, Green K. 1988. Distribution of Euphausia crystallorophias within Prydz Bay and its importance to the inshore marine ecosystem. Polar Biology, 8(5): 327-331

Tierney M, Southwe C, Emmerson L M. 2008. Evaluating and using stable-isotope analysis to infer diet composition and foraging ecology of Adélie penguins Pygoscelis adeliae. Marine Ecology Progress Series, 355: 297-307

Vander Zanden M J, Rasmussen J B. 1999. Primary consumer δ¹³C and δ¹⁵N and the trophic position of aquatic consumers. Ecology, 80(4): 1395-1404

Wada E, Terazaki M, Kabaya Y. 1987. ¹⁵N and ¹³C abundances in the Antarctic ocean with emphasis on biogeochemical structure of the food web. Deep Sea Research Part I. Oceanographic Research Papers, 34(5-6): 829-841

Yin Xijie, Li Yunhai, Qiao Lei. 2014. Distribution of particulate organic carbon (POC) and δ¹³C_poc in surface waters in summer in Prydz Bay, Antarctica. Chinese Journal of Polar Research (in Chinese), 26(1): 159-166

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