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Influence of the diet on the bioaccumulation of heavy metals in zooplankton-eating petrels at Kerguelen archipelago, Southern Indian Ocean

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Abstract

Concentrations of cadmium, mercury, copper and zinc were measured in muscle, kidney and liver tissues and in the main prey of five species of zooplankton-eating petrels: blue petrel (Halobaena caerulea), thin-billed (Pachyptila belcheri) and Antarctic (P. desolata) prions, and South Georgian (Pelecanoides georgicus) and common (Pelecanoides urinatrix) diving petrels. Since some of these species are closely related species with respect to body size, timing of moult and life span, their diet has been examined to evaluate its influence on heavy-metal bioaccumulation. Inter-specific differences were significant for Hg concentrations in the liver and for Zn concentrations in both liver and kidney tissues. Blue petrels exhibited the highest Hg concentrations in the liver (3.9±2.02 µg.g−1 wet weight). No significant differences were found in Cd concentrations between species. Exposure to heavy metals through the most important prey species in the diet during the breeding period was evaluated. The most evident result was the influence of fish prey on Hg levels. Although crustacean species exhibit different cadmium concentrations, the diet composition does not appear to be discriminant for Cd bioaccumulation within the small petrel community at Kerguelen.

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References

  • Barrett RT, Krasnov YV (1996) Recent responses to changes in stock of prey species by seabirds breeding in the southern Barents Sea. ICES J Mar Sci 53:713–722

    Article  Google Scholar 

  • Bocher P, Cherel Y, Hobson KA (2000) Complete trophic segregation between South Georgian and common diving petrels during breeding at Iles Kerguelen. Mar Ecol Prog Ser 208:249–264

    Google Scholar 

  • Bocher P, Cherel Y, Labat JP, 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

    Google Scholar 

  • Bried J, Jouventin P (2002) Site and mate choice in seabirds: an evolutionary approach. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC, Boca Raton, Fla, pp 263–305

  • Burger AE (1993) Estimating the mortality of seabirds following oil spills: effects of spill volume. Mar Pollut Bull 26:40–143

    Article  Google Scholar 

  • Bustamante P, Caurant F, Fowler SW, Miramand P (1998) Cephalopods as a vector for the transfer of Cd to top marine predators in the north-east Atlantic Ocean. Sci Total Environ 220:71–80

    Article  CAS  PubMed  Google Scholar 

  • Cairns DK (1987) Seabirds as indicators of marine food supplies. Biol Ocean 5:261–271

    Google Scholar 

  • Camphuysen CJ, Van Franeker JA (1992) The value of beached bird surveys in monitoring marine oil pollution. Techn Rap Vogelbescherming 10. Nederlandse Vereniging tot Bescherming van Vogels, Zeist

  • Caurant F, Amiard-Triquet C (1995) Cadmium contamination in pilot whales Globicephala melas: source and potential hazard to the species. Mar Pollut Bull 30:207–210

    Article  CAS  Google Scholar 

  • Caurant F, Navarro M, Amiard JC (1996) Mercury in pilot whales: possible limits to the detoxification process. Sci Total Environ 186:95–104

    Article  CAS  PubMed  Google Scholar 

  • Chastel O (1995) Effort de reproduction chez les oiseaux longévifs: fréquence de reproduction et condition physique chez les pétrels. Thesis, Université François Rabelais, Tours

  • Cherel Y, Weimerskirch H (1995) Seabirds as indicators of marine resources: black-browed albatrosses feeding on ommastrephid squids in Kerguelen waters. Mar Ecol Prog Ser 129:295–300

    Google Scholar 

  • Cherel Y, Bocher P, De Broyer C, Hobson KA (2002a) Food and feeding ecology of the sympatric thin-billed Pachyptila belcheri and Antarctic P. desolata prions at Iles Kerguelen, Southern Indian Ocean. Mar Ecol Prog Ser 228:263–281

    Google Scholar 

  • Cherel Y, Bocher P, Trouvé C, Weimerskirch H (2002b) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, southern Indian Ocean. Mar Ecol Prog Ser 228:283–299

    Google Scholar 

  • Coquery M, Azemard S, Mora SJ de (2001) The analytical performance study for the Medpol region: determination of trace elements and methylmercury in estuarine sediment sample IAEA-405. IAEA Rep

    Google Scholar 

  • Cuvin-Aralar ML, Furness RW (1991) Mercury and selenium interaction: a review. Ecotox Environ Saf 21:348–364

    CAS  Google Scholar 

  • Dietz R, Riget F, Johansen P (1996) Lead, cadmium, mercury and selenium in Greenland marine animals. Sci Total Environ 18:67–93

    Article  Google Scholar 

  • Dietz R, Norgaard J, Hansen JC (1998) Have arctic marine mammals adapted to high cadmium levels? Mar Pollut Bull 36:490–492

    Article  CAS  Google Scholar 

  • Elliot JE, Scheuhammer AM (1997) Heavy metal and metallothionein concentrations in seabirds from the Pacific coast of Canada. Mar Pollut Bull 34:794–801

    Article  Google Scholar 

  • Elliot JE, Scheuhammer AM, Leighton FA, Pearce PA (1992) Heavy metal and metallothionein concentrations in Atlantic Canadian seabirds. Arch Environ Contam Toxicol 22:63–73

    PubMed  Google Scholar 

  • Friberg L, Piscator M, Nordberg GF, Kjellstrom T (1974) Cadmium in the environment, 2ndedn. CRC, Cleveland, Ohio

  • Furness RW (1993) Birds as monitors of pollutants. In: Furnesss RW, Greenwood JJD (eds) Birds as monitors of environmental change. Chapman and Hall, London, pp 86–143

  • Furness RW, Camphuysen CJ (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci 54:726–737

    Article  Google Scholar 

  • Furness RW, Muirhead SJ, Woodburn M (1986) Using bird feathers to measure mercury in the environment : relationships between mercury content and moult. Mar Pollut Bull 17:27–30

    Article  CAS  Google Scholar 

  • Furness RW, Greenwood JJD, Jarvis PJ (1993) Can birds be used to monitor the environment? In: Furness RW, Greenwood JJD (eds) Birds as monitors of environmental change. Chapman and Hall, London, pp 86–143

  • Hindell MA, Brother N, Gales R (1999) Mercury and cadmium concentrations in the tissues of three species of southern albatrosses. Polar Biol 22:102–108

    Article  Google Scholar 

  • Honda K, Tatsukawa R, Itano K, Miyazaki N, Fujiyama T (1983) Heavy metal concentrations in muscle, liver and kidney tissue of striped dolphin, Stenella coeruleoalba, and their variations with body length, weight, age and sex. Agric Biol Chem 47:1219–1228

    CAS  Google Scholar 

  • Hopkins TL (1985) Food web of an Antarctic midwater ecosystem. Mar Biol 89:197–212

    Google Scholar 

  • Kim EY, Goto R, Tanabe S, Tatsukawa R (1998) Distribution of 14 elements in tissues and organs of oceanic seabirds. Arch Environ Contam Toxicol 35:638–645

    Article  CAS  PubMed  Google Scholar 

  • Koeman JH, Van De Ven WSM, De Goeij JJM, Tjoe PS, Van Haaften JL (1975) Mercury and selenium in marine mammals and birds. Sci Total Environ 3:279–287

    Article  CAS  PubMed  Google Scholar 

  • Marchant S, Higgins PJ (1990) Handbook of Australian, New Zealand and Antarctic Birds, vol 1. Oxford University Press, Melbourne

  • Martoja R, Berry JP (1980) Identification of tiemannite as a probable product of demethylation of mercury by selenium in cetaceans. A complement to the scheme of the biological cycle of mercury. Vie Milieu 30:7–10

    Google Scholar 

  • Monteiro LR, Furness RW (1995) Seabirds as monitors of mercury in the environment. Water Air Soil Pollut 80:851–870

    CAS  Google Scholar 

  • Monteiro LR, Granadeiro JP, Furness RW (1998) Relationship between mercury levels and diet in Azores seabirds. Mar Ecol Prog Ser 166:259–265

    CAS  Google Scholar 

  • Montevecchi WA (1993) Seabird indication of squid stock conditions. J Cephal Biol 2:57–63

    Google Scholar 

  • Montevecchi WA, Myers RA (1997) Centurial and decadal oceanographic influences on changes in northern gannet populations and diets in the north-west Atlantic: implications for climate change. ICES J Mar Sci 54:608–614

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Omori M, Ikeda T (1984) Methods in marine zooplankton ecology. Wiley, New York

  • Palmisano F, Cardellichio N, Zambonin PG (1995) Speciation of mercury in dolphin liver: a two stage mechanism for the demethylation accumulation process and role of selenium. Mar Environ Res 40:109–121

    Article  CAS  Google Scholar 

  • Petri G, Zauke GP (1993) Trace metals in crustaceans in the Antarctic Ocean. Ambio 22:529–536

    Google Scholar 

  • Regehr HM, Montevecchi WA (1997) Interactive effects of food shortage and predation on breeding failure of black-legged kittiwakes: indirect effects of fisheries activities and implications for indicator species. Mar Ecol Prog Ser 155:249–260

    Google Scholar 

  • Sanchez-Hernandez JC (2000) Trace element contamination in Antarctic ecosystems. Rev Environ Contam Toxicol 166:83–127

    CAS  PubMed  Google Scholar 

  • Schreiber EA, Burger J (2002) Biology of marine birds. CRC, Boca Raton

  • Stewart FM, Furness RW (1998) The influence of age on cadmium concentrations in seabirds. Environ Monit Assess 50:159–171

    Article  CAS  Google Scholar 

  • Stewart FM, Phillips RA, Catry P, Furness RW (1997) Influence of species, age and diet on mercury concentrations in Shetland seabirds. Mar Ecol Prog Ser 151:237–244

    CAS  Google Scholar 

  • Stewart FM, Furness RW, Monteiro LR (1998) Relationships between heavy metal and metallothionein concentrations in lesser black-backed gulls, Larus fuscus, and Cory’s shearwater, Calonectris diomedea. Arch Environ Contam Toxicol 30:299–305

    Google Scholar 

  • Stewart FM, Pillips RA, Bartle A, Craig J, Shooter D (1999) Influence of phylogeny, diet, moult schedule and sex on heavy metal concentrations in New Zealand procellariiformes. Mar Ecol Prog Ser 178:295–305

    CAS  Google Scholar 

  • Szefer P, Czarnowski W, Pempkowiak J, Holm E (1993a) Mercury and major essential elements in seals, penguins, and other representative fauna of the Antarctic. Arch Environ Contam Toxicol 25:422–427

    CAS  PubMed  Google Scholar 

  • Szefer P, Pempkowiak J, Skwarzec B, Bojanowski R, Holm E (1993b) Concentration of selected metals in penguins and other representative fauna of the Antarctica. Sci Total Environ 138:281–288

    Article  CAS  PubMed  Google Scholar 

  • Thompson DR (1990) Metal concentrations in marine vertebrates. In: Furness RW, Rainbow PS (eds) Heavy metals in the marine environment. CRC, Boca Raton, pp 143–183

  • Thompson DR, Furness RW (1989) The chemical form of mercury stored in South Atlantic seabirds. Environ Pollut 60:305–317

    Article  CAS  Google Scholar 

  • Thompson DR, Furness RW, Monteiro LR (1998) Seabirds as monitors of mercury inputs to epipelagic and mesopelagic marine food chains. Sci Total Environ 213:299–305

    Article  CAS  Google Scholar 

  • Underwood EJ (1977) Trace elements in human and animal nutrition. Academic, New York

  • Wagemann R, Stewart REA, Beland P, Desjardins C (1990) Heavy metals and selenium in tissues of beluga whales, Delphinapterus leucas, from the Canadian Arctic and the St Laurent Estuary. In: Smith TG, St Aubin DJ, Geraci JR (eds) Advances in research on the beluga whale, Delphinapterus leucas. Can Bull Fish Aquat Sci 224:191–206

    Google Scholar 

  • Walsh PM (1990) The use of seabirds as monitors of heavy metals in the marine environment. In: Furness RW, Rainbow PS (eds) Heavy metals in the marine environment. CRC, New York, pp 183–204

  • Webb M (1987) Toxicological significance of metallothionein. In: Kägi JHR, Kojima Y (eds) Metallothionein II. Birkhaüser, Basel, pp 109–134

  • Weimerskirch H, Zotier R, Jouventin P (1989) The avifauna of the Kerguelen Islands. Emu 89:15–29

    Google Scholar 

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We are very grateful to Damian Lidgard for reviewing the English of the manuscript.

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Correspondence to F. Caurant.

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Bocher, P., Caurant, F., Miramand, P. et al. 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 (2003). https://doi.org/10.1007/s00300-003-0552-6

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