Major, trace, and rare-earth elements in the zooplankton of the Laptev Sea in relation to community composition

  • Nikolay V. LobusEmail author
  • Elena G. Arashkevich
  • Ekaterina A. Flerova
Research Article


We investigated the concentrations of major, trace, and rare-earth elements in zooplankton in relation to species community composition from the eastern part of the Lena Delta to the continental slope of the Laptev Sea in September 2015. The elemental composition of zooplankton inhabiting different areas demonstrated similarities. Cross-shelf changes were found for only 4 (Li, Zn, As, and U) of the 56 elements analyzed. Zinc was the only element concentration of which successively reduced across coastal–open ocean gradient. Considering own and literary data, we can assume that the cross-shelf decrease of zinc accumulation in zooplankton is a universal pattern, manifested in different climatic and biogeochemical environmental conditions and with different species compositions of the zooplankton community. Cross-shelf changes were also established for Li, As, and U. However, the concentrations of these elements increased along the gradient. We assume that increased As concentration in zooplankton across the shelf–continental slope gradient of the Laptev Sea is associated with a change in the feeding behavior of the species of the zooplankton community. However, a sharp increase in the concentrations of Li and U in zooplankton was associated with the appearance of Calanus copepods in the community. The average total concentration of rare-earth elements and yttrium in zooplankton of the Laptev Sea was 752.8 ng g−1 of dry weight. We found record high levels of rare-earth elements for zooplankton of the inner shelf, near the eastern part of the Lena Delta. From the inner shelf to the continental slope of the Laptev Sea, La, Ce, and Nd were the dominant rare-earth elements. The elemental composition of zooplankton in the Arctic Seas is characterized by a much lower content of major and trace elements in comparison with the zooplankton and total plankton of the ocean.


Arctic Chemical composition of zooplankton Bioaccumulation Emerging pollutants 



The sea expeditionary research was performed under a state assignment by the Shirshov Institute of Oceanology. The authors are grateful to the supervisor M. V. Flint, the scientific parties, and the crew of R/V Akademik Mstislav Keldysh, cruise 63, for their professional support on the investigation of the Russian Arctic seas. The authors are also grateful to Dr. E. A. Romankevich for his insightful comments on the manuscript. English was checked by professional editor service ( with native English.

Funding information

This research was funded by the Russian Science Foundation, research project no. 18-77-00064 (collecting and processing of data of the major, trace, and rare-earth element composition of zooplankton), research project no. 14-50-00095 (collecting and processing of data of the biomass and species composition of zooplankton), and the state assignment of IO RAS, theme 0149-2019-0006 (analytical processing of data of the OC and ash content).


  1. Abramova E, Tuschling K (2005) A 12-year study of the seasonal and interannual dynamics of mesozooplankton in the Laptev Sea: significance of salinity regime and life cycle patterns. Glob Planet Chang 48:141–164. CrossRefGoogle Scholar
  2. Anikeev VV, Dudarev OV, Kasatkina AP (1996) The influence of terrigenous and biogenic factors on the formation of element particle fluxes offshore the sea of Japan. Geochem Int 34:53–65Google Scholar
  3. Antia AN, Burkill PH, Balzer W, de Baar HJW, Mantoura RFC, Simó R, Wallace D (2003) Coupled biogeochemical cycling and controlling factors. In: Wefer G, Lamy F, Mantoura F (eds) Marine science Frontiers for Europe. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 147–162. CrossRefGoogle Scholar
  4. Arashkevich EG, Drits AV, Pasternak AF, Flint MV, Demidov AB, Amelina AB, Kravchishina MD, Sukhanova IN, Shchuka SA (2018) Distribution and feeding of herbivorous zooplankton in the Laptev Sea. Oceanology 58:381–395. CrossRefGoogle Scholar
  5. Baar de HJW, La Roche J (2003) Trace metals in the oceans: evolution, biology and global change. In: Marine science frontiers for Europe. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 79–105. CrossRefGoogle Scholar
  6. Baines SB, Chen XI, Twining BS, Fisher NS, Landry MR (2016) Factors affecting Fe and Zn contents of mesozooplankton from the Costa Rica Dome. J Plankton Res 38:331–347. CrossRefGoogle Scholar
  7. Bamstedt U (1986) Chemical composition and energy content. In: Corner EDS, O’Hara SCM (eds.) The biological chemistry of marine copepods. Oxford University Press, New York, p 1–58Google Scholar
  8. Battuello M, Brizio P, Sartor RM, Nurra N, Pessani D, Abete MC, Squadrone S (2016) Zooplankton from a North Western Mediterranean area as a model of metal transfer in a marine environment. Ecol Indic 66:440–451. CrossRefGoogle Scholar
  9. Battuello M, Sartor RM, Brizio P, Nurra N, Pessani D, Abete MC, Squadrone S (2017) The influence of feeding strategies on trace element bioaccumulation in copepods (Calanoida). Ecol Indic 74:311–320. CrossRefGoogle Scholar
  10. Baturin GN, Emel’yanov EM, Stryuk VL (1993) Geochemistry of plankton and suspended matter in the Baltic Sea. Okeanologiya 33:126–132Google Scholar
  11. Benedetti F, Gasparini S, Ayata S-D (2016) Identifying copepod functional groups from species functional traits. J Plankton Res 38:159–166. CrossRefGoogle Scholar
  12. Black FJ, Bokhutlo T, Somoxa A, Maethamako M, Modisaemang O, Kemosedile T, Cobb-Adams C, Mosepele K, Chimbari M (2011) The tropical African mercury anomaly: lower than expected mercury concentrations in fish and human hair. Sci Total Environ 409:1967–1975. CrossRefGoogle Scholar
  13. Brodskiy KA (1967) Calanoida of the Far Eastern seas and Polar Basin of the USSR. [Translated from the Russian. Originally published 1950]. Jerusalem: Israel Program for Scientific TranslationsGoogle Scholar
  14. Brodsky K, Vyshkvartzeva N, Kos M, Markhaseva E (1983) Copepod crustaceans (Copepoda Calanoida) of the USSR seas and adjacent water. Opredeliteli po faune SSSRGoogle Scholar
  15. Bruland KW, Middag R, Lohan MC (2014) Controls of trace metals in seawater. In: Holland HD, Turekian KK (eds) Treatise on geochemistry. Elsevier, Philadelphia, pp 19–51. CrossRefGoogle Scholar
  16. Campbell LM, Norstrom RJ, Hobson KA, Muir DCG, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351–352:247–263. CrossRefGoogle Scholar
  17. Carmack EC, Yamamoto-Kawai M, Haine TWN, Bacon S, Bluhm BA, Lique C, Melling H, Polyakov IV, Straneo F, Timmermans M-L, Williams WJ (2016) Freshwater and its role in the Arctic Marine System: sources, disposition, storage, export, and physical and biogeochemical consequences in the Arctic and global oceans. J Geophys Res Biogeosci 121:675–717. CrossRefGoogle Scholar
  18. Conover RJ, Huntley M (1991) Copepods in ice-covered seas—distribution, adaptations to seasonally limited food, metabolism, growth patterns and life cycle strategies in polar seas. J Mar Syst 2:1–41. CrossRefGoogle Scholar
  19. DeForest DK, Brix KV, Adams WJ (2007) Assessing metal bioaccumulation in aquatic environments: the inverse relationship between bioaccumulation factors, trophic transfer factors and exposure concentration. Aquat Toxicol 84:236–246. CrossRefGoogle Scholar
  20. Dittmar T, Kattner G (2003) The biogeochemistry of the river and shelf ecosystem of the Arctic Ocean: a review. Mar Chem 83:103–120. CrossRefGoogle Scholar
  21. Dubinina EO, Kossova SA, Miroshnikov AY, Kokryatskaya NM (2017) Isotope (δD, δ18О) systematics in waters of the Russian Arctic seas. Geochem Int 55:1022–1032. CrossRefGoogle Scholar
  22. Dubinina EO, Miroshnikov AY, Kossova SA, Shchuka SA (2019) Modification of the Laptev Sea freshened shelf waters based on isotope and salinity relations. Geochem Int 57:1–19. CrossRefGoogle Scholar
  23. Duncan EG, Maher WA, Foster SD, Krikowa F (2013) The influence of arsenate and phosphate exposure on arsenic uptake, metabolism and species formation in the marine phytoplankton Dunaliella tertiolecta. Mar Chem 157:78–85. CrossRefGoogle Scholar
  24. Edwards M (2017) Plankton and global change. In: Castellani C, Edwards M (eds) Marine plankton: a practical guide to ecology, methodology, and taxonomy. Oxford University Press, Oxford, pp 67–80. Google Scholar
  25. Falk-Petersen S, Mayzaud P, Kattner G, Sargent JR (2009) Lipids and life strategy of Arctic Calanus. Mar Biol Res 5:18–39. CrossRefGoogle Scholar
  26. Fedorova I, Chetverova A, Bolshiyanov D, Makarov A, Boike J, Heim B, Morgenstern A, Overduin PP, Wegner C, Kashina V, Eulenburg A, Dobrotina E, Sidorina I (2015) Lena Delta hydrology and geochemistry: long-term hydrological data and recent field observations. Biogeosciences 12:345–363. CrossRefGoogle Scholar
  27. Fisher T, Peele E, Ammerman J, Harding L (1992) Nutrient limitation of phytoplankton in Chesapeake Bay. Mar Ecol Prog Ser 82:51–63. CrossRefGoogle Scholar
  28. Fisher N, Stupakoff I, Sañudo-Wilhelmy S, Wang W, Teyssié J, Fowler S, Crusius J (2000) Trace metals in marine copepods: a field test of a bioaccumulation model coupled to laboratory uptake kinetics data. Mar Ecol Prog Ser 194:211–218. CrossRefGoogle Scholar
  29. Flerova E, Bogdanova A (2014) The features of biochemical indices of strain chlorella vulgaris IGF no. С-111, grown in closed system. J Microbiol Biotechnol Food Sci 3:311–313Google Scholar
  30. Flint MV, Semenova TN, Arashkevich EG, Sukhanova IN, Gagarin VI, Kremenetskiy VV, Pivovarov MA, Soloviev KA (2010) Structure of the zooplankton communities in the region of the Ob River’s estuarine frontal zone. Oceanology 50:766–779. CrossRefGoogle Scholar
  31. Flint MV, Poyarkov SG, Rimsky-Korsakov NA (2016) Ecosystems of the Russian Arctic-2015 (63rd cruise of the research vessel Akademik Mstislav Keldysh). Oceanology 56:459–461. CrossRefGoogle Scholar
  32. Fowler SW, Knauer GA (1986) Role of large particles in the transport of elements and organic compounds through the oceanic water column. Prog Oceanogr 16:147–194. CrossRefGoogle Scholar
  33. Freese D, Niehoff B, Søreide JE, Sartoris FJ (2015) Seasonal patterns in extracellular ion concentrations and pH of the Arctic copepod Calanus glacialis. Limnol Oceanogr 60:2121–2129. CrossRefGoogle Scholar
  34. Gaillardet J, Viers J, Dupré B (2014) Trace elements in river waters. In: Treatise on geochemistry. Elsevier, pp 195–235.
  35. Gobas FA, Morrison HA (2000) Bioconcentration and biomagnification in the aquatic environment. In: Mackay D, Boethling RS (eds) Handbook of property estimation methods for chemicals. CRC Press, pp 211–254.
  36. Gonzalez-Davila M, Santana-Casiano JM, Millero FJ (1990) The adsorption of Cd(II) and Pb(II) to chitin in seawater. J Colloid Interface Sci 137:102–110. CrossRefGoogle Scholar
  37. Gordeev VV, Lisitzin AP (2014) Geochemical interaction between the freshwater and marine hydrospheres. Russ Geol Geophys 55:562–581. CrossRefGoogle Scholar
  38. Gordeev VV, Beeskow B, Meeresforschung P-UND (2007) Geochemistry of the Ob and Yenisey estuaries: a comparative study, Reports on Polar and Marine ResearchGoogle Scholar
  39. Guieu C, Huang WW, Martin J-M, Yong YY (1996) Outflow of trace metals into the Laptev Sea by the Lena River. Mar Chem 53:255–267. CrossRefGoogle Scholar
  40. Gwenzi W, Mangori L, Danha C, Chaukura N, Dunjana N, Sanganyado E (2018) Sources, behaviour, and environmental and human health risks of high-technology rare earth elements as emerging contaminants. Sci Total Environ 636:299–313. CrossRefGoogle Scholar
  41. Hecky RE, Kilham P (1988) Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment1. Limnol Oceanogr 33:796–822. Google Scholar
  42. Ho T-Y, Wen L-S, You C-F, Lee D-C (2007) The trace metal composition of size-fractionated plankton in the South China Sea: biotic versus abiotic sources. Limnol Oceanogr 52:1776–1788. CrossRefGoogle Scholar
  43. Holemann J, Schirmacher M, Prance A (2005) Seasonal variability of trace metals in the Lena River and the southeastern Laptev Sea: impact of the spring freshet. Glob Planet Chang 48:112–125. CrossRefGoogle Scholar
  44. Hsiao S-HH, Hwang J-SS, Fang T-HH (2011) Copepod species and their trace metal contents in coastal northern Taiwan. J Mar Syst 88:232–238. CrossRefGoogle Scholar
  45. Hutchins D, Bruland K (1994) Grazer-mediated regeneration and assimilation of Fe, Zn and Mn from planktonic prey. Mar Ecol Prog Ser 110:259–269. CrossRefGoogle Scholar
  46. Hutchins DA, Wang W-X, Fisher NS (1995) Copepod grazing and the biogeochemical fate of diatom iron. Limnol Oceanogr 40:989–994. CrossRefGoogle Scholar
  47. Kahle J, Zauke G-P (2003) Trace metals in Antarctic copepods from the Weddell Sea (Antarctica). Chemosphere 51:409–417. CrossRefGoogle Scholar
  48. Karandashev VK, Turanov AN, Orlova TA, Lezhnev AE, Nosenko SV, Zolotareva NI, Moskvitina IR (2008) Use of the inductively coupled plasma mass spectrometry for element analysis of environmental objects. Inorg Mater 44:1491–1500. CrossRefGoogle Scholar
  49. Karnovsky N, Kwasniewski S, Weslawski J, Walkusz W, Beszczynska-Möller A (2003) Foraging behavior of little auks in a heterogeneous environment. Mar Ecol Prog Ser 253:289–303. CrossRefGoogle Scholar
  50. Karpov YA, Orlova VA (2008) Modern methods of autoclave sample preparation in chemical analysis of substances and materials. Inorg Mater 44:1501–1508. CrossRefGoogle Scholar
  51. Kassens H, Lisitzin AP, Thiede J, Polyakova YI, Timokhov LA, Frolov IE (eds) (2009) System of rhe Laptev Sea and adjacent Arctic seas. Moscow University Press, MoscowGoogle Scholar
  52. Kosobokova KN, Hanssen H, Hirche H-J, Knickmeier K (1997) Composition and distribution of zooplankton in the Laptev Sea and adjacent Nansen Basin during summer, 1993. Polar Biol 19:63–76. CrossRefGoogle Scholar
  53. Lee BG, Fisher N (1992) Decomposition and release of elements from zooplankton debris. Mar Ecol Prog Ser 88:117–128. CrossRefGoogle Scholar
  54. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306. CrossRefGoogle Scholar
  55. Leonova GA, Bobrov VA, Bogush AA, Bychinskii VA (2013) Concentration of chemical elements by zooplankton of the White Sea. Oceanology 53:54–70. CrossRefGoogle Scholar
  56. Li Y-H (1991) Distribution patterns of the elements in the ocean: a synthesis. Geochim Cosmochim Acta 55:3223–3240. CrossRefGoogle Scholar
  57. Lobus NV (2016) Elemental composition of zooplankton in the Kara Sea and the bays on the eastern side of Novaya Zemlya. Oceanology 56:809–818. CrossRefGoogle Scholar
  58. Lobus NV, Drits AV, Flint MV (2018) Accumulation of chemical elements in the dominant species of copepods in the Ob estuary and the adjacent shelf of the Kara Sea. Oceanology 58:405–415. CrossRefGoogle Scholar
  59. MacMillan GA, Chételat J, Heath JP, Mickpegak R, Amyot M (2017) Rare earth elements in freshwater, marine, and terrestrial ecosystems in the eastern Canadian Arctic. Environ Sci Process Impacts 19:1336–1345. CrossRefGoogle Scholar
  60. Maher WA (1985) Distribution of arsenic in marine animals: relationship to diet. Comp Biochem Physiol Part C Comp 82:433–434. CrossRefGoogle Scholar
  61. Maher W, Butler E (1988) Arsenic in the marine environment. Appl Organomet Chem 2:191–214. CrossRefGoogle Scholar
  62. Martin JH (1970) The possible transport of trace metals via moulted copepod exoskeletons. Limnol Oceanogr 15:756–761. CrossRefGoogle Scholar
  63. Martin JH, Knauer GA (1973) The elemental composition of plankton. Geochim Cosmochim Acta 37:1639–1653. CrossRefGoogle Scholar
  64. Navarro J, Zhao F (2014) Life-cycle assessment of the production of rare-earth elements for energy applications: a review. Front Energy Res 2:45. CrossRefGoogle Scholar
  65. Navratilova J, Raber G, Fisher SJ, Francesconi KA (2011) Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic. Environ Chem 8:44–51. CrossRefGoogle Scholar
  66. Neff JM (1997) Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 16:917–927. Google Scholar
  67. Neruchev SG (2007) Uranium and life in the history of the earth, 2nd ed. All-Russia Petroleum Research Exploration Institute, St. PetersswburgGoogle Scholar
  68. Nummelin A, Ilicak M, Li C, Smedsrud LH (2016) Consequences of future increased Arctic runoff on Arctic Ocean stratification, circulation, and sea ice cover. J Geophys Res Ocean 121:617–637. CrossRefGoogle Scholar
  69. Omori M (1969) Weight and chemical composition of some important oceanic zooplankton in the North Pacific Ocean. Mar Biol 3:4–10. CrossRefGoogle Scholar
  70. Oremland RS, Stolz JF (2003) The ecology of arsenic. Science (80- ) 300:939–944. CrossRefGoogle Scholar
  71. Orlova VA (2003) Analytical autoclaves: autoclave preparation of samples in chemical analysis. Central Scientific Research Institute of Agrochemical Service of Agriculture Moscow, MoscowGoogle Scholar
  72. PAME (1996) Working Group on the Protection of the Arctic Marine Environment. Report to the Third Ministerial Conference on the protection of the Arctic environment, Norwegian Ministry of Environment. OsloGoogle Scholar
  73. Pasternak AF, Drits AV, Abyzova GA, Semenova TN, Sergeeva VM, Flint MV (2015) Feeding and distribution of zooplankton in the desalinated “lens” in the Kara Sea: impact of the vertical salinity gradient. Oceanology 55:863–870. CrossRefGoogle Scholar
  74. Pavlov VK, Timokhov LA, Baskakov GA, Kulakov MY, Kurazhov VK, Pavlov PV, Pivovarov SV, Stanovoy VV (1996) Hydrometeorological regime of the Kara, Laptev, and East-Siberian Seas. Technical Memorandum APL-UW TM1-96, University of Washington, 179 p.Google Scholar
  75. Peters J, Tuschling K, Brandt A (2004) Zooplankton in the arctic Laptev Sea - feeding ecology as indicated by fatty acid composition. J Plankton Res 26:227–234. CrossRefGoogle Scholar
  76. Pohl C (1992) Correlations between trace metal concentrations (Cd, Cu, Pb, Zn) in seawater and zooplankton organisms (Copepoda) of the Arctic and Atlantic Ocean. Ber Polarforsch 101:198Google Scholar
  77. Polyakov I, Walsh D, Dmitrenko I, Colony RL, Timokhov LA (2003) Arctic Ocean variability derived from historical observations. Geophys Res Lett 30.
  78. Polyakov IV, Alexeev VA, Belchansky GI, Dmitrenko IA, Ivanov VV, Kirillov SA, Korablev AA, Steele M, Timokhov LA, Yashayaev I (2008) Arctic Ocean freshwater changes over the past 100 years and their causes. J Clim 21:364–384. CrossRefGoogle Scholar
  79. Price A, Maher W, Kirby J, Krikowa F, Duncan E, Taylor A, Potts J (2012) Distribution of arsenic species in an open seagrass ecosystem: relationship to trophic groups, habitats and feeding zones. Environ Chem 9:77–88. CrossRefGoogle Scholar
  80. Purkerson DG, Doblin MA, Bollens SM, Luoma SN, Cutter GA (2003) Selenium in San Francisco Bay zooplankton: potential effects of hydrodynamics and food web interactions. Estuar Coasts 26:956–969. CrossRefGoogle Scholar
  81. Rahman AM, Hasegawa H, Peter Lim R (2012) Bioaccumulation, biotransformation and trophic transfer of arsenic in the aquatic food chain. Environ Res. Academic Press.
  82. Rainbow PS (1997a) Trace metal accumulation in marine invertebrates: marine biology or marine chemistry? J Mar Biol Assoc United Kingdom 77:195–210. CrossRefGoogle Scholar
  83. Rainbow PS (1997b) Ecophysiology of trace metal uptake in crustaceans. Estuar Coast Shelf Sci 44:169–176. CrossRefGoogle Scholar
  84. Rainbow PS (1998) Phylogeny of trace metal accumulation in crustaceans. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environments. Springer US, Boston, MA, pp 285–319. CrossRefGoogle Scholar
  85. Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507. CrossRefGoogle Scholar
  86. Rauschenberg S, Twining BS (2015) Evaluation of approaches to estimate biogenic particulate trace metals in the ocean. Mar Chem 171:67–77. CrossRefGoogle Scholar
  87. Reinfelder JR, Fisher NS (2009) The assimilation of elements ingested by marine copepods. Science 251:794–796. CrossRefGoogle Scholar
  88. Reinfelder JR, Fisher NS, Fowler SW, Teyssié J-L (1993) Release rates of trace elements and protein from decomposing planktonic debris. 2. Copepod carcasses and sediment trap particulate matter. J Mar Res 51:423–442. CrossRefGoogle Scholar
  89. Reinfelder JR, Fisher NS, Luoma SN, Nichols JW, Wang WX (1998) Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach. Sci Total Environ 219:117–135. CrossRefGoogle Scholar
  90. Rejomon G, Kumar PKD, Nair M, Muraleedharan KR (2010) Trace metal dynamics in zooplankton from the Bay of Bengal during summer monsoon. Environ Toxicol 25:622–633. CrossRefGoogle Scholar
  91. Ritterhoff J, Zauke G-P (1997) Trace metals in field samples of zooplankton from the Fram Strait and the Greenland Sea. Sci Total Environ 199:255–270. CrossRefGoogle Scholar
  92. Robinson KA, Baird DJ, Wrona FJ (2003) Surface metal adsorption on zooplankton carapaces: implications for exposure and effects in consumer organisms. Environ Pollut 122:159–167. CrossRefGoogle Scholar
  93. Sanders JG (1980) Arsenic cycling in marine systems. Mar Environ Res 3:257–266. CrossRefGoogle Scholar
  94. Savenko VS (1989) Elementary chemical composition of ocean plankton. Geokhimiya 8:1084–1089Google Scholar
  95. Srichandan S, Panigrahy RC, Baliarsingh SK, Rao BS, Pati P, Sahu BK, Sahu KC (2016) Distribution of trace metals in surface seawater and zooplankton of the Bay of Bengal, off Rushikulya estuary, East Coast of India. MPB.
  96. Stegen KS (2015) Heavy rare earths, permanent magnets, and renewable energies: an imminent crisis. Energy Policy 79:1–8. CrossRefGoogle Scholar
  97. Stein R, Fahl K, Fütterer DK, Galimov EM, Stepanets OV (eds) (2003) Siberian river run-off in the Kara Sea: characterisation, quantification, variability, and environmental significance, 1st edn. Elsevier Science, AmsterdamGoogle Scholar
  98. Steinberg DK, Landry MR (2017) Zooplankton and the ocean carbon cycle. Annu Rev Mar Sci 9:413–444. CrossRefGoogle Scholar
  99. Stepanova SV, Polukhin AA, Kostyleva AV (2017) Hydrochemical structure of the waters in the eastern part of the Laptev Sea in autumn 2015. Oceanology 57:58–64. CrossRefGoogle Scholar
  100. Sukhanova IN, Flint MV, Georgieva EJ, Lange EK, Kravchishina MD, Demidov AB, Nedospasov AA, Polukhin AA (2017) The structure of phytoplankton communities in the eastern part of the Laptev Sea. Oceanology 57:75–90. CrossRefGoogle Scholar
  101. Tang KW, Elliott DT (2014) Copepod carcasses: occurrence, fate and ecological importance. In: Seuront L (ed) Copepods: diversity, habitat and behaviour. Nova Science, Incorporated, pp 255–278Google Scholar
  102. Tao Y, Yuan Z, Xiaona H, Wei M (2012) Distribution and bioaccumulation of heavy metals in aquatic organisms of different trophic levels and potential health risk assessment from Taihu Lake, China. Ecotoxicol Environ Saf 81:55–64. CrossRefGoogle Scholar
  103. Timokhov LA (1994) Regional characteristics of the Laptev and the East Siberian seas: climate, topography, ice phases, thermohaline regime, circulation. In: Kassens H, Hubberten HW, Pryamiko VM, Stein R (eds) Russian-German cooperation in the Siberian shelf seas: geosystem Laptev Sea. Rep Polar Res, pp 15–31Google Scholar
  104. Turner JT (2015) Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceanogr 130:205–248. CrossRefGoogle Scholar
  105. Wang WX, Fisher NS (1998) Accumulation of trace-elements in a marine copepod. Limnol Oceanogr 43:273–283CrossRefGoogle Scholar
  106. Warren GJ (1985) Predaceous feeding habits of Limnocalanus macrurus. J Plankton Res 7:537–552. CrossRefGoogle Scholar
  107. White SL, Rainbow PS (1985) On the metabolic requirements for copper and zinc in molluscs and crustaceans. Mar Environ Res 16:215–229. CrossRefGoogle Scholar
  108. Wolfe-Simon F, Switzer Blum J, Kulp TR, Gordon GW, Hoeft SE, Pett-Ridge J, Stolz JF, Webb SM, Weber PK, Davies PCW, Anbar AD, Oremland RS (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332:1163–1166. CrossRefGoogle Scholar
  109. Xu L-Q, Liu X-D, Sun L, Chen Q-Q, Yan H, Liu Y, Luo Y-H, Huang J (2011) A 700-year record of mercury in avian eggshells of Guangjin Island, South China Sea. Environ Pollut 159:889–896. CrossRefGoogle Scholar
  110. Zauke G-P, Schmalenbach I (2006) Heavy metals in zooplankton and decapod crustaceans from the Barents Sea. Sci Total Environ 359:283–294. CrossRefGoogle Scholar
  111. Zauke G-P, Krause M, Weber A (1996) Trace metals in Mesozooplankton of the North Sea: concentrations in different taxa and preliminary results on bioaccumulation in copepod collectives (Calanus finmarchicus/C. helgolandicus). Int Rev der gesamten Hydrobiol und Hydrogr 81:141–160. CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Shirshov Institute of OceanologyRussian Academy of SciencesMoscowRussia
  2. 2.Yaroslavl Scientific Research Institute of Livestock Breeding and Forage ProductionRussian Academy of SciencesYaroslavlRussia

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