Polar Biology

, Volume 41, Issue 1, pp 175–191 | Cite as

Trace elements in invertebrates and fish from Kerguelen waters, southern Indian Ocean

  • Caio V. Z. Cipro
  • Y. Cherel
  • P. Bocher
  • F. Caurant
  • P. Miramand
  • P. Bustamante
Original Paper


Given the lack of background data on essential and non-essential trace elements in invertebrates and fish known to be the predominant prey of marine mammals and seabirds breeding at the Kerguelen Islands, this study intends to provide these results of great influence for predators in higher trophic levels. To this end, plankton organisms (9 species/4 phyla), mollusks (2 bivalves and 2 squid species) and fishes (8 benthic and 10 pelagic species) from Kerguelen waters were analysed for cadmium (Cd), copper (Cu), mercury (Hg) and zinc (Zn). Individual concentrations of non-essential elements (particularly Cd) showed larger variation in comparison with essential ones likely due to their homeostasis. Thus Cd ranged over 4 orders of magnitude; however, Hg ranged only 1, without significant correlation to trophic level. Instead, ecological parameters (benthic/mesopelagic habitat and feeding ecology) showed a more important influence on the results. Concerning seashore organisms, bivalves collected inside the Gulf of Morbihan had higher Cd concentrations compared to those from the Kerguelen shelf, suggesting a local source of Cd, such as runoff water from bird colonies. Comparison with the literature showed metal concentrations in invertebrates and fishes from Kerguelen Islands somewhat lower than those in the Antarctic area, with Hg prevailing in benthic species and Cd in pelagic ones. In contrast to Hg, Cd values of squids, jellyfish and the amphipod Themisto gaudichaudii were significantly higher than all other species. Finally, top predators foraging in this area that can be subject to potentially high Hg and Cd exposure through their diet at Kerguelen are reviewed.


Plankton Myctophid Food web Metals Trace elements Kerguelen 



We thank G. Duhamel and the crew of the RV ‘La Curieuse’ for their help in the collection of the fish specimens. This work was financially supported by the Agence Nationale de la Recherche (Program POLARTOP, O. Chastel), the Institut Paul Emile Victor(IPEV, Programme No. 109, H. Weimerskirch), the Terres Australes et Antarctiques Françaises (TAAF) and the CPER (Contrat de Projet Etat-Région) for funding the AMA of the Plateforme Analyses Elémentaires of LIENSs. C.V.Z. Cipro was supported financially through a post-doctoral grant from the University of La Rochelle and the CNRS (French acronym for National Council of Scientific Research), and also scholarships from CAPES (Coordination for the Improvement of Higher Education Personnel via the Science without Borders programme, Brazil) and FAPESP (São Paulo Research Foundation, Brazil) during the course of this work and its publication. The IUF (Institut Universitaire de France) is acknowledged for its support to Paco Bustamante.

Supplementary material

300_2017_2180_MOESM1_ESM.xlsx (16 kb)
Supplementary material 1 (XLSX 16 kb)


  1. Aguilar A, Borrell A, Pastor T (1999) Biological factors affecting variability of persistent pollutant levels in cetaceans. J Cetacean Res Manag 1:83–116Google Scholar
  2. Ahn I-Y, Lee SH, Kim KT, Shim JH, Kim D-Y (1996) Baseline heavy metal concentrations in the Antarctic clam, Laternula elliptica in Maxwell Bay, King George Island, Antarctica. Mar Pollut Bull 32:592–598. doi: 10.1016/0025-326X(95)00247-K CrossRefGoogle Scholar
  3. Amiard J-C, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202. doi: 10.1016/j.aquatox.2005.08.015 PubMedCrossRefGoogle Scholar
  4. 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. doi: 10.3354/meps07784 CrossRefGoogle Scholar
  5. Anderson ORJ, Phillips RA, Shore RF, McGill RAR, McDonald RA, Bearhop S (2010) Element patterns in albatrosses and petrels: influence of trophic position, foraging range, and prey type. Environ Pollut 158:98–107. doi: 10.1016/j.envpol.2009.07.040 PubMedCrossRefGoogle Scholar
  6. Andersson I, Parkman H, Jernelöv A (1990) The role of sediments as sink or source for environmental contaminants—a case study of mercury and chlorinated organic compounds. Limnol Jena 20:347–359Google Scholar
  7. Bargagli R (2001) Trace metals in Antarctic organisms and the development of circumpolar biomonitoring networks. Rev Env Contam Toxicol 171:53–110CrossRefGoogle Scholar
  8. Bargagli R (2008) Environmental contamination in Antarctic ecosystems. Sci Total Environ 400:212–226. doi: 10.1016/j.scitotenv.2008.06.062 PubMedCrossRefGoogle Scholar
  9. Bargagli R, Nelli L, Ancora S, Focardi S (1996) Elevated cadmium accumulation in marine organisms from Terra Nova Bay (Antarctica). Polar Biol 16:513–520. doi: 10.1007/BF02329071 CrossRefGoogle Scholar
  10. Beltcheva M, Metcheva R, Peneva V, Marinova M, Yankov Y, Chikova V (2011) Heavy metals in Antarctic notothenioid fish from South Bay, Livingston Island, South Shetlands (Antarctica). Biol Trace Elem Res 141:150–158. doi: 10.1007/s12011-010-8739-5 PubMedCrossRefGoogle Scholar
  11. Blévin P, Carravieri A, Jaeger A, Chastel O, Bustamante P, Cherel Y (2013) Wide Range of Mercury Contamination in Chicks of Southern Ocean Seabirds. PLoS ONE 8:e54508. doi: 10.1371/journal.pone.0054508 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bocher P, Cherel Y, Labat J, Mayzaud P, Razouls S, Jouventin P (2001) Amphipod-based food web: Themisto gaudichaudii caught in nets and by seabirds in Kerguelen waters, southern Indian Ocean. Mar Ecol Prog Ser 223:261–276. doi: 10.3354/meps223261 CrossRefGoogle Scholar
  13. Bocher P, Cherel Y, Alonzo F, Razouls S, Labat JP, Mayzaud P, Jouventin P (2002) Importance of the large copepod Paraeuchaeta antarctica (Giesbrecht, 1902) in coastal waters and the diet of seabirds at Kerguelen, Southern Ocean. J Plankton Res 24:1317–1333. doi: 10.1093/plankt/24.12.1317 CrossRefGoogle Scholar
  14. Bocher P, Caurant F, Miramand P, Cherel Y, Bustamante P (2003) Influence of the diet on the bioaccumulation of heavy metals in zooplankton-eating petrels at Kerguelen archipelago, Southern Indian Ocean. Polar Biol 26:759–767. doi: 10.1007/s00300-003-0552-6 CrossRefGoogle Scholar
  15. Borsa P (1997) Seasonal trends in the occurrence of marine mammals in the golfe du Morbihan, Kerguelen Islands. Mar Mammal Sci 13:314–316. doi: 10.1111/j.1748-7692.1997.tb00635.x CrossRefGoogle Scholar
  16. Brasso R, Lang J, Jones C, Polito M (2014) Ontogenetic niche expansion influences mercury exposure in the Antarctic silverfish Pleuragramma antarcticum. Mar Ecol Prog Ser 504:253–263. doi: 10.3354/meps10738 CrossRefGoogle Scholar
  17. Bustamante P, Caurant F, Fowler SW, Miramand P (1998a) Cephalopods as a vector for the transfer of cadmium to top marine predators in the north-east Atlantic Ocean. Sci Total Environ 220:71–80PubMedCrossRefGoogle Scholar
  18. Bustamante P, Cherel Y, Caurant F, Miramand P (1998b) Cadmium, copper and zinc in octopuses from Kerguelen Islands, Southern Indian Ocean. Polar Biol 19:264–271. doi: 10.1007/s003000050244 CrossRefGoogle Scholar
  19. Bustamante P, Cosson RP, Gallien I, Caurant F, Miramand P (2002) Cadmium detoxification processes in the digestive gland of cephalopods in relation to accumulated cadmium concentrations. Mar Environ Res 53:227–241PubMedCrossRefGoogle Scholar
  20. Bustamante P, Bocher P, Cherel Y, Miramand P, Caurant F (2003) Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands. Sci Total Environ 313:25–39. doi: 10.1016/S0048-9697(03)00265-1 PubMedCrossRefGoogle Scholar
  21. Bustamante P, Lahaye V, Durnez C, Churlaud C, Caurant F (2006) Total and organic Hg concentrations in cephalopods from the North Eastern Atlantic waters: influence of geographical origin and feeding ecology. Sci Total Environ 368:585–596. doi: 10.1016/j.scitotenv.2006.01.038 PubMedCrossRefGoogle Scholar
  22. Bustamante P, Carravieri A, Goutte A, Barbraud C, Delord K, Chastel O, Weimerskirch H, Cherel Y (2016) High feather mercury concentrations in the wandering albatross are related to sex, breeding status and trophic ecology with no demographic consequences. Environ Res 144:1–10. doi: 10.1016/j.envres.2015.10.024 PubMedCrossRefGoogle Scholar
  23. 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. doi: 10.1016/j.scitotenv.2005.02.043 PubMedCrossRefGoogle Scholar
  24. Carravieri A, Bustamante P, Tartu S, Meillère A, Labadie P, Budzinski H, Peluhet L, Barbraud C, Weimerskirch H, Chastel O, Cherel Y (2014a) Wandering albatrosses document latitudinal variations in the transfer of persistent organic pollutants and mercury to southern ocean predators. Environ Sci Technol 48:14746–14755. doi: 10.1021/es504601m PubMedCrossRefGoogle Scholar
  25. Carravieri A, Cherel Y, Blévin P, Brault-Fravrou M, Chastel O, Bustamante P (2014b) Mercury exposure in a large subantarctic avian community. Environ Pollut 190C:51–57. doi: 10.1016/j.envpol.2014.03.017 CrossRefGoogle Scholar
  26. Caurant F, Bustamante P, Bordes M, Miramand P (1999) Bioaccumulation of cadmium, copper and zinc in some tissues of three species of marine turtles stranded along the French Atlantic Coasts. Mar Pollut Bull 38:1085–1091. doi: 10.1016/S0025-326X(99)00109-5 CrossRefGoogle Scholar
  27. Cherel Y, Hobson KA (2005) Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc Biol Sci 272:1601–1607. doi: 10.1098/rspb.2005.3115 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cherel Y, Weimerskirch H, Trouvé C (2000) Food and feeding ecology of the neritic-slope forager black-browed albatross and its relationships with commercial fisheries in Kerguelen waters. Mar Ecol Prog Ser 207:183–199. doi: 10.3354/meps207183 CrossRefGoogle Scholar
  29. Cherel Y, Duhamel G, Gasco N (2004) Cephalopod fauna of subantarctic islands: new information from predators. Mar Ecol Prog Ser 266:143–156. doi: 10.3354/meps266143 CrossRefGoogle Scholar
  30. Cherel Y, Ducatez S, Fontaine C, Richard P, Guinet C (2008) Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands. Mar Ecol Prog Ser 370:239–247. doi: 10.3354/meps07673 CrossRefGoogle Scholar
  31. Cherel Y, Fontaine C, Richard P, Labat J-P (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr 55:324–332. doi: 10.4319/lo.2010.55.1.0324 CrossRefGoogle Scholar
  32. Chouvelon T, Spitz J, Cherel Y, Caurant F, Sirmel R, Mèndez-Fernandez P, Bustamante P (2011) Inter-specific and ontogenic differences in δ13C and δ15N values and Hg and Cd concentrations in cephalopods. Mar Ecol Prog Ser 433:107–120. doi: 10.3354/meps09159 CrossRefGoogle Scholar
  33. Chouvelon T, Spitz J, Caurant F, Mèndez-Fernandez P, Autier J, Lassus-Débat A, Chappuis A, Bustamante P (2012) Enhanced bioaccumulation of mercury in deep-sea fauna from the Bay of Biscay (north-east Atlantic) in relation to trophic positions identified by analysis of carbon and nitrogen stable isotopes. Deep Sea Res I 65:113–124. doi: 10.1016/j.dsr.2012.02.010 CrossRefGoogle Scholar
  34. Choy ES, Gauthier M, Mallory ML, Smol JP, Douglas MSV, Lean D, Blais JM (2010) An isotopic investigation of mercury accumulation in terrestrial food webs adjacent to an Arctic seabird colony. Sci Total Environ 408:1858–1867. doi: 10.1016/j.scitotenv.2010.01.014 PubMedCrossRefGoogle Scholar
  35. Cipro CVZ, Yogui GT, Bustamante P, Taniguchi S, Sericano JL, Montone RC (2011) Organic pollutants and their correlation with stable isotopes in vegetation from King George Island, Antarctica. Chemosphere 85:393–398. doi: 10.1016/j.chemosphere.2011.07.047 PubMedCrossRefGoogle Scholar
  36. Cipro CVZ, Cherel Y, Caurant F, Miramand P, Méndez-Fernandez P, Bustamante P (2014) Trace elements in tissues of white-chinned petrels (Procellaria aequinoctialis) from Kerguelen waters, Southern Indian Ocean. Polar Biol 37:763–771. doi: 10.1007/s00300-014-1476-z CrossRefGoogle Scholar
  37. Coale KH (1991) Effects of iron, manganese, copper, and zinc enrichments on productivity and biomass in the subarctic Pacific. Limnol Oceanogr 36:1851–1864. doi: 10.4319/lo.1991.36.8.1851 CrossRefGoogle Scholar
  38. Dehn L-A, Follmann EH, Thomas DL, Sheffield GG, Rosa C, Duffy LK, O’Hara TM (2006) Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci Total Environ 362:103–123. doi: 10.1016/j.scitotenv.2005.11.012 PubMedCrossRefGoogle Scholar
  39. Delord K, Cotté C, Péron C, MarteauC Pruvost P, Gasco N, Duhamel G, Cherel Y, Weimerskirch H (2010) At-sea distribution and diet of an endangered top predator: relationship between white-chinned petrels and commercial longline fisheries. Endanger Species Res 13:1–16. doi: 10.3354/esr00309 CrossRefGoogle Scholar
  40. Dorneles PR, Lailson-Brito J, Dos Santos RA, da Costa PAS, Malm O, Azevedo AF, Torres JPM (2007) Cephalopods and cetaceans as indicators of offshore bioavailability of cadmium off Central South Brazil Bight. Environ Pollut 148:352–359. doi: 10.1016/j.envpol.2006.09.022 PubMedCrossRefGoogle Scholar
  41. dos Santos IR, Silva-Filho EV, Schaefer C, Sella SM, Silva CA, Gomes V, Passos MJACR, Ngan PV (2006) Baseline mercury and zinc concentrations in terrestrial and coastal organisms of Admiralty Bay, Antarctica. Environ Pollut 140:304–311. doi: 10.1016/j.envpol.2005.07.007 PubMedCrossRefGoogle Scholar
  42. Dubé J (1982) Étude de la distribution de quelques metaux dans le zooplancton de deux ecosystèmes du Saint-Laurent. Université du Québec, QuebecGoogle Scholar
  43. Espejo W, Celis JE, González-Acuña D, Jara S, Barra R (2014) Concentration of trace metals in excrements of two species of penguins from different locations of the Antarctic Peninsula. Polar Biol 37:675–683. doi: 10.1007/s00300-014-1468-z CrossRefGoogle Scholar
  44. Gallien I, Caurant F, Bordes M, Bustamante P, Miramand P, Fernandez B, Quellard N, Babin P (2001) Cadmium-containing granules in kidney tissue of the Atlantic white-sided dolphin (Lagenorhyncusacutus) off the Faroe Islands. Comput Biochem Physiol C 130:389–395Google Scholar
  45. Giraldo C, Cherel Y, Vallet C, Mayzaud P, Tavernier E, Moteki M, Hosie G, Koubbi P (2011) Ontogenic changes in the feeding ecology of the early life stages of the Antarctic silverfish (Pleuragramma antarcticum) documented by stable isotopes and diet analysis in the Dumont d’Urville Sea (East Antarctica). Polar Sci 5:252–263. doi: 10.1016/j.polar.2011.04.004 CrossRefGoogle Scholar
  46. Goutte A, Bustamante P, Barbraud C, Delord K, Weimerskirch H, Chastel O (2014) Demographic responses to mercury exposure in two closely related Antarctic top predators. Ecology 95:1075–1086. doi: 10.1890/13-1229.1 PubMedCrossRefGoogle Scholar
  47. Goutte A, Cherel Y, Churlaud C, Ponthus J-P, Massé G, Bustamante P (2015) Trace elements in Antarctic fish species and the influence of foraging habitats and dietary habits on mercury levels. Sci Total Environ 538:743–749. doi: 10.1016/j.scitotenv.2015.08.103 PubMedCrossRefGoogle Scholar
  48. Guinet C, Cherel Y, Ridoux V, Jouventin P (1996) Consumption of marine resources by seabirds and seals in Crozet and Kerguelen waters: changes in relation to consumer biomass 1962–85. Antarct Sci 8:23–30CrossRefGoogle Scholar
  49. Guynn KD, Peterson MS (2008) Mercury concentrations in the Patagonian toothfish, Dissostichus eleginoides Smitt 1898, among three distinct stocks. Polar Biol 31:269–274. doi: 10.1007/s00300-007-0354-3 CrossRefGoogle Scholar
  50. Hamanaka T, Tsujita T (1981) Cadmium and zinc concentrations in zooplankton in the subarctic region of the North Pacific. J Oceanogr Soc Jpn 37:160–172. doi: 10.1007/BF02309053 CrossRefGoogle Scholar
  51. Hanchet SM, Tracey D, Dunn A, Horn P, Smith N (2012) Mercury concentrations of two toothfish and three of its prey species from the Pacific sector of the Antarctic. Antarct Sci 24:34–42. doi: 10.1017/S0954102011000654 CrossRefGoogle Scholar
  52. Headley AD (1996) Heavy metal concentrations in peat profiles from the high Arctic. Sci Total Environ 177:105–111. doi: 10.1016/0048-9697(95)04867-7 CrossRefGoogle Scholar
  53. Hennig H, Eagle G, McQuaid C, Rickett L (1985) Metal Concentrations in Antarctic Zooplankton Species. In: Siefried W, Condy P, Laws R (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 656–661CrossRefGoogle Scholar
  54. Kahle J, Zauke GP (2003) Trace metals in Antarctic copepods from the Weddell Sea (Antarctica). Chemosphere 51:409–417. doi: 10.1016/S0045-6535(02)00855-X PubMedCrossRefGoogle Scholar
  55. Kannan K, Smith RG Jr, Lee RF, Windom HL, Heitmuller PT, Macauley JM, Summers JK (1998) Distribution of total mercury and methyl mercury in water, sediment, and fish from South Florida Estuaries. Arch Environ Contam Toxicol 34:109–118. doi: 10.1007/s002449900294 PubMedCrossRefGoogle Scholar
  56. Klaassen CD, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmacol Toxicol 39:267–294. doi: 10.1146/annurev.pharmtox.39.1.267 PubMedCrossRefGoogle Scholar
  57. Kock K-H (2005a) Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part II. Polar Biol 28:897–909. doi: 10.1007/s00300-005-0020-6 CrossRefGoogle Scholar
  58. Kock K-H (2005b) Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I. Polar Biol 28:862–895. doi: 10.1007/s00300-005-0019-z CrossRefGoogle Scholar
  59. Kock KH, Wilhelms S, Everson I, Groger J (1994) Variations in the diet composition and feeding intensity of mackerel icefish Champsocephalus gunnari at South Georgia (Antarctic). Mar Ecol Prog Ser 108:43–58. doi: 10.3354/meps108043 CrossRefGoogle Scholar
  60. Kojadinovic J, Potier M, Le Corre M, Cosson RP, Bustamante P (2007) Bioaccumulation of trace elements in pelagic fish from the Western Indian Ocean. Environ Pollut. doi: 10.1016/j.envpol.2006.07.015 PubMedGoogle Scholar
  61. Kojadinovic J, Jackson CH, Cherel Y, Jackson GD, Bustamante P (2011) Multi-elemental concentrations in the tissues of the oceanic squid Todarodes filippovae from Tasmania and the southern Indian Ocean. Ecotoxicol Environ Saf 74:1238–1249. doi: 10.1016/j.ecoenv.2011.03.015 PubMedCrossRefGoogle Scholar
  62. Lahaye V, Bustamante P, Spitz J, Dabin W, Das K, Pierce GJ, Caurant F (2005) Long-term dietary segregation of common dolphins Delphinus delphis in the Bay of Biscay, determined using cadmium as an ecological tracer. Mar Ecol Prog Ser 305:275–285. doi: 10.3354/meps305275 CrossRefGoogle Scholar
  63. Lane TW, Morel FM (2000) A biological function for cadmium in marine diatoms. Proc Natl Acad Sci USA 97:4627–4631. doi: 10.1073/pnas.090091397 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Lane TW, Saito MA, George GN, Pickering IJ, Prince RC, Morel FMM (2005) A cadmium enzyme from a marine diatom. Nature 434:42. doi: 10.1038/434455a CrossRefGoogle Scholar
  65. Lescroël A, Bost CA (2005) Foraging under contrasting oceanographic conditions: the gentoo penguin at Kerguelen Archipelago. Mar Ecol Prog Ser 302:245–261. doi: 10.3354/meps302245 CrossRefGoogle Scholar
  66. Lescroël A, Ridoux V, Bost CA (2004) Spatial and temporal variation in the diet of the gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol 27:206–216. doi: 10.1007/s00300-003-0571-3 CrossRefGoogle Scholar
  67. Locarnini S, Presley B (1995) Trace element concentrations in Antarctic krill, Euphausia superba. Polar Biol 15:283–288Google Scholar
  68. Macdonald C, Sprague J (1988) Cadmium in marine invertebrates and arctic cod in the Canadian Arctic. Distribution and ecological implications. Mar Ecol Prog Ser 47:17–30. doi: 10.3354/meps047017 CrossRefGoogle Scholar
  69. Mackay EA, Overnell J, Dunbar B, Davidson I, Hunziker PE, Kägi JH, Fothergill JE (1993) Complete amino acid sequences of five dimeric and four monomeric forms of metallothionein from the edible mussel Mytilus edulis. Eur J Biochem 218:183–194PubMedCrossRefGoogle Scholar
  70. Martin JH, Flegal AR (1975) High copper concentrations in squid livers in association with elevated levels of silver, cadmium, and zinc. Mar Biol 30:51–55. doi: 10.1007/BF00393752 CrossRefGoogle Scholar
  71. McArthur T, Butler ECV, Jackson GD (2003) Mercury in the marine food chain in the Southern Ocean at Macquarie Island: an analysis of a top predator, Patagonian toothfish (Dissostichus eleginoides) and a mid-trophic species, the warty squid (Moroteuthis ingens). Polar Biol 27:1–5. doi: 10.1007/s00300-003-0560-6 CrossRefGoogle Scholar
  72. McIntyre JK, Beauchamp DA (2007) Age and trophic position dominate bioaccumulation of mercury and organochlorines in the food web of Lake Washington. Sci Total Environ 372:571–584. doi: 10.1016/j.scitotenv.2006.10.035 PubMedCrossRefGoogle Scholar
  73. Miramand P, Bentley D (1992) Concentration and distribution of heavy metals in tissues of two cephalopods, Eledone cirrhosa and Sepia officinalis, from the French coast of the English Channel. Mar Biol 114:407–414CrossRefGoogle Scholar
  74. Miramand P, Guary JC (1980) High concentrations of some heavy metals in tissues of the mediterranean Octopus. Bull Environ Contam Toxicol 24:738–788CrossRefGoogle Scholar
  75. Miramand P, Fichet D, Bentley D (1998) Concentrations en métaux lourds (Cd, Cu, Pb, Zn) observées le long du gradient de salinité dans le réseau trophique pélagique de l’estuaire de la Seine. Comptes Rendus l’Académie des Sci Sci la terre des planètes 327:259–264Google Scholar
  76. Miramand P, Pigeot J, Guyot T, Fichet D (1999) Ecotoxicologie intégrée de l’espèce à l’écosystème. Océanis 25:581–608Google Scholar
  77. Miramand P, Guyot T, Rybarczyk H, Elkaim B, Mouny P, Dauvin JC, Bessineton C (2001) Contamination of the biological compartment in the Seine estuary by Cd, Cu, Pb, and Zn. Estuaries 24:1056–1065CrossRefGoogle Scholar
  78. Monteiro LR, Costa V, Furness RW, Santos RS (1996) Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Mar Ecol Prog Ser 141:21–25CrossRefGoogle Scholar
  79. Mougeot F, Genevois F, Bretagnolle V (1998) Predation on burrowing petrels by the brown skua (Catharacta skua lönnbergi) at Mayes Island, Kerguelen. J Zool Lond 244:429–438. doi: 10.1017/S0952836998003136 Google Scholar
  80. Muirhead SJ, Furness RW (1988) Heavy metal concentrations in the tissues of seabirds from Gough Island, South Atlantic Ocean. Mar Pollut Bull 19:278–283. doi: 10.1016/0025-326X(88)90599-1 CrossRefGoogle Scholar
  81. Øverjordet IB, Kongsrud MB, Gabrielsen GW, Berg T, Ruus A, Evenset A, Borgå K, Christensen G, Jenssen BM (2015) Toxic and essential elements changed in black-legged kittiwakes (Rissa tridactyla) during their stay in an Arctic breeding area. Sci Total Environ 502:548–556. doi: 10.1016/j.scitotenv.2014.09.058 PubMedCrossRefGoogle Scholar
  82. Pakhomov EA, Perissinotto R (1996) Trophodynamics of the hyperiid amphipod Themisto gaudichaudi in the South Georgia region during late austral summer. Mar Ecol Prog Ser 134:91–100. doi: 10.3354/meps134091 CrossRefGoogle Scholar
  83. Penicaud V, Lacoue-Labarthe T, Bustamante P (2017) Metal bioaccumulation and detoxification processes in cephalopods: a review. Environ Res 155:123–133. doi: 10.1016/j.envres.2017.02.003 PubMedCrossRefGoogle Scholar
  84. Petri G, Zauke G-P (1993) Trace metal in the crustaceans in the Antarctic Ocean. Ambio 1(22):529–536Google Scholar
  85. Pierce GJ, Stowasser G, Hastie LC, Bustamante P (2008) Geographic, seasonal and ontogenetic variation in cadmium and mercury concentrations in squid (Cephalopoda: Teuthoidea) from UK waters. Ecotoxicol Environ Saf 70:422–432. doi: 10.1016/j.ecoenv.2007.07.007 PubMedCrossRefGoogle Scholar
  86. Pigeot J, Miramand P, Guyot T, Sauriau P-G, Fichet D, Le Moine O, Huet V (2006) Cadmium pathways in an exploited intertidal ecosystem with chronic cadmium inputs (Marennes-Oléron, Atlantic coast, France). Mar Ecol Prog Ser 307:101–114CrossRefGoogle Scholar
  87. Pinkerton MH, Forman J, Bury SJ, Brown J, Horn P, O’Driscoll RL (2013) Diet and trophic niche of Antarctic silverfish Pleuragramma antarcticum in the Ross Sea, Antarctica. J Fish Biol 82:141–164. doi: 10.1111/j.1095-8649.2012.03476.x PubMedCrossRefGoogle Scholar
  88. Rainbow P (1989) Copper, cadmium and zinc concentrations in oceanic amphipod and euphausiid crustaceans, as a source of heavy metals to pelagic seabirds. Mar Biol 103:513–518CrossRefGoogle 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 219:117–135PubMedCrossRefGoogle Scholar
  90. Ritterhoff J, Zauke G-P (1997) Influence of body length, life-history status and sex on trace metal concentrations in selected zooplankton collectives from the Greenland Sea. Mar Pollut Bull 34:614–621. doi: 10.1016/S0025-326X(96)00181-6 CrossRefGoogle Scholar
  91. Romeo M, Gnassia-Barelli M, Carre C (1987) Trace metals: Cd, Cu, Pb and Zn in gelatinous macroplankton from the Northwestern Mediterranean. Water Res 21:1287–1292CrossRefGoogle Scholar
  92. Romeo M, Gnassia-Barelli M, Carre C (1992) Importance of gelatinous plankton organisms in the storage and transfer of trace metals in the north-western Mediterranean. Mar Ecol Prog Ser 82:267–274CrossRefGoogle Scholar
  93. Sanchez-Hernandez JC (2000) Trace element contamination in Antarctic ecosystems. Rev Env Contam Toxicol 166:83–127Google Scholar
  94. Saunders RA, Collins MA, Ward P, Stowasser G, ShreeveR Tarling GA (2015) Distribution, population structure and trophodynamics of Southern Ocean Gymnoscopelus (Myctophidae) in the Scotia Sea. Polar Biol 38:287–308. doi: 10.1007/s00300-014-1584-9 CrossRefGoogle Scholar
  95. Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295PubMedCrossRefGoogle Scholar
  96. Stewart F, Phillips R, Bartle J (1999) Influence of phylogeny, diet, moult schedule and sex on heavy metal concentrations in New Zealand Procellariiformes. Mar Ecol Prog Ser 178:295–305CrossRefGoogle Scholar
  97. Stoeppler M, Nürnberg HW (1979) Comparative studies on trace metal levels in marine biota. Ecotoxicol Environ Saf 3:335–351. doi: 10.1016/0147-6513(79)90023-X PubMedCrossRefGoogle Scholar
  98. Tan SW, Meiller JC, Mahaffey KR (2009) The endocrine effects of mercury in humans and wildlife. Crit Rev Toxicol 39:228–269. doi: 10.1080/10408440802233259 PubMedCrossRefGoogle Scholar
  99. Tartu S, Goutte A, Bustamante P, Angelier F, Moe B, Clément-Chastel C, Bech C, Gabrielsen GW, Bustnes JO, Chastel O (2013) To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird. Biol Lett 9:1–4. doi: 10.1098/rsbl.2013.0317 CrossRefGoogle Scholar
  100. Tavares S, Xavier JC, Phillips RA, Pereira ME, Pardal MA (2013) Influence of age, sex and breeding status on mercury accumulation patterns in the wandering albatross Diomedea exulans. Environ Pollut 181:315–320. doi: 10.1016/j.envpol.2013.06.032 PubMedCrossRefGoogle Scholar
  101. Tsui MTK, Wang WX (2004) Uptake and Elimination Routes of Inorganic Mercury and Methylmercury in Daphnia magna. Environ Sci Technol 38:808–816. doi: 10.1021/es034638x PubMedCrossRefGoogle Scholar
  102. von Waldow H, Macleod M, Scheringer M, Hungerbühler K (2010) Quantifying remoteness from emission sources of persistent organic pollutants on a global scale. Environ Sci Technol 44:2791–2796. doi: 10.1021/es9030694 CrossRefGoogle Scholar
  103. Wang W (2002) Interactions of trace metals and different marine food chains. Mar Ecol Prog Ser 243:295–309. doi: 10.3354/meps243295 CrossRefGoogle Scholar
  104. Wang W, Fisher NS (1998) Accumulation of trace elements in a marine copepod. Limnol Oceanogr 43:273–283. doi: 10.4319/lo.1998.43.2.0273 CrossRefGoogle Scholar
  105. Wang W-X, Reinfelder JR, Lee B-G, Fisher NS (1996) Assimilation and regeneration of trace elements by marine copepods. Limnol Oceanogr 41:70–81. doi: 10.4319/lo.1996.41.1.0070 CrossRefGoogle Scholar
  106. Weimerskirch H, Zotier R, Jouventin P (1989) The avifauna of the Kerguelen Islands. EMU 89:15–29CrossRefGoogle Scholar
  107. Wintle NJP, Sleadd IM, Gundersen DT, Kohl K, Buckley BA (2015) Total mercury in six Antarctic Notothenioid fishes. Bull Environ Contam Toxicol 95:557–560. doi: 10.1007/s00128-015-1594-5 PubMedCrossRefGoogle Scholar
  108. Wöhrmann APA, Hagen W, Kunzmann A (1997) Adaptations of the Antarctic silverfish Pleuragramma antarcticum (Pisces: Nototheniidae) to pelagic life in high-Antarctic waters. Mar Ecol Prog Ser 151:205–218CrossRefGoogle Scholar
  109. Xu Y, Feng L, Jeffrey PD, Shi Y, Morel FMM (2008) Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452:56–61. doi: 10.1038/nature06636 PubMedCrossRefGoogle Scholar
  110. Zauke G-P, Clason B, Savinov VM, Savinova T (2003) Heavy metals of inshore benthic invertebrates from the Barents Sea. Sci Total Environ 306:99–110. doi: 10.1016/S0048-9697(02)00487-4 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Littoral Environnement et Sociétés (LIENSs), UMR 7266CNRS-Université de La RochelleLa Rochelle Cedex 01France
  2. 2.Laboratório de Química Orgânica MarinhaInstituto Oceanográfico, Universidade de São PauloSão PauloBrazil
  3. 3.Centre d’Etudes Biologiques de Chizé, UMR 7372CNRS-Université de La RochelleVilliers-en-BoisFrance

Personalised recommendations