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Trace elements in tissues of white-chinned petrels (Procellaria aequinoctialis) from Kerguelen waters, Southern Indian Ocean

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Abstract

The use of seabirds to assess marine contamination by trace elements in areas remote from pollutant emission points has already been done at various latitudes. Nevertheless, little information is available concerning the Southern Indian Ocean. Determining the contaminants levels, there appears necessary not only due to several deleterious effects reported in literature, but also as previous studies have highlighted elevated concentrations of cadmium (Cd) and mercury (Hg) in mollusks, crustaceans and fish. Within this context, the white-chinned petrel appears as a key species due to its lifespan, diet and trophic position. Thirty-three accidentally killed (collision with lights/bycatch in longline vessels) individuals collected in Kerguelen waters were analysed for Cd, copper (Cu), Hg, selenium (Se) and zinc (Zn) in liver, kidney, pectoral muscle, feathers and for mature males, testis. Elevated Hg concentrations (average 58.4 μg g−1 dw in liver) are likely due to the presence of mesopelagic prey in the diet of Procellaria aequinoctialis. Cd concentrations (average of 65.7 μg g−1 dw in kidney) can be attributed to a high level of fisheries offal consumption, as well as crustacean and squid ingestion. Correlation of Hg with Se indicates its detoxification by co-precipitation, and correlation of Cd with Zn suggests its displacement by Cd on metallothioneins binding sites. This work also indirectly confirms ecological data (range and diet composition) from the wintering period of the species, which is rather scarce. Seasonal diet change and moulting accounted more for the obtained results than sex of the birds.

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References

  • Abdulla M, Chmielnicka J (1990) New aspects on the distribution and metabolism of essential trace elements after dietary exposure to toxic metals. Biol Trace Elem Res 23:25–53

    Article  CAS  Google Scholar 

  • Agusa T, Matsumoto T, Ikemoto T, Anan Y, Kubota R, Yasunaga G, Kunito T, Tanabe S, Ogi H, Shibata Y (2005) Body distribution of trace elements in black-tailed gulls from Rishiri Island, Japan: age-dependent accumulation and transfer to feather and eggs. Environ Toxicol Chem 24:2107–2120

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Barbraud C, Marteau C, Ridoux V, Delord K, Weimerskirch H (2008) Demographic response of a population of white-chinned petrels Procellaria aequinoctialis to climate and longline fishery bycatch. J Appl Ecol 45:1460–1467

    Article  Google Scholar 

  • Barbraud C, Delord K, Marteau C, Weimerskirch H (2009) Estimates of population size of white-chinned petrels and grey petrels at Kerguelen Islands and sensitivity to fisheries. Anim Conserv 12:258–265

    Article  Google Scholar 

  • Berrow SD, Croxall JP, Grant SD (2000) Status of white-chinned petrels Procellaria aequinoctialis Linnaeus 1758, at Bird Island, South Georgia. Antarct Sci 12:399–405

  • Birdlife International (2013) White-chinned Petrel Procellaria aequinoctialis. http://www.birdlife.org/datazone/speciesfactsheet.php?id=3922. Accessed 2 July 2013

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Borgå K, Campbell L, Gabrielsen GW, Norstrom RJ, Muir DCG, Fisk AT (2006) Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds. Environ Toxicol Chem 25:2927–2936

    Article  PubMed  Google Scholar 

  • Bugoni L, Furness R (2009) Age composition and sexual size dimorphism of albatrosses and petrels off Brazil. Mar Ornithol 260:253–260

    Google Scholar 

  • 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 220:71–80

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bustamante P, Bertrand M, Boucaud-Camou E, Miramand P (2006a) Subcellular distribution of Ag, Cd Co, Cu, Fe, Mn, Pb, and Zn in the digestive gland of the common cuttlefish Sepia officinalis. J Shellfish Res 25:987–993

    Google Scholar 

  • Bustamante P, Lahaye V, Durnez C, Churlaud C, Caurant F (2006b) 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

    Article  CAS  PubMed  Google Scholar 

  • Carravieri A, Bustamante P, Churlaud C, Cherel Y (2013) Penguins as bioindicators of mercury contamination in the Southern Ocean: birds from the Kerguelen Islands as a case study. Sci Total Environ 454(455):141–148

    Article  PubMed  Google Scholar 

  • Catard A, Weimerskirch H, Cherel Y (2000) Exploitation of distant Antarctic waters and close shelf-break waters by white-chinned petrels rearing chicks. Mar Ecol Prog Ser 194:249–261

    Article  Google Scholar 

  • Cherel Y, Attaix D, Rosolowska-Huszcz D, Belkhou R, Robin JR, Arnal M, Le Maho Y (1991) Whole-body and tissue protein synthesis during brief and prolonged fasting in the rat. Clin Sci 81:611–619

    CAS  PubMed  Google Scholar 

  • 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 Part I 65:113–124

    Article  CAS  Google Scholar 

  • Connan M, Cherel Y, Mabille G, Mayzaud P (2007) Trophic relationships of white-chinned petrels from Crozet Islands: combined stomach oil and conventional dietary analyses. Mar Biol 152:95–107

    Article  CAS  Google Scholar 

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

  • Delord K, Cotté C, Péron C, Marteau C, 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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fitzgerald W, Engstrom D (1998) The case for atmospheric mercury contamination in remote areas. Environ Sci Technol 32:1–7

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gilbertson M, Elliott JE, Peakall DB (1987) Seabirds as indicators of marine pollution. In: Diamond AW, Filion F (eds) The value of birds. International Council for Bird Preservation, Cambridge, pp 231–248

    Google Scholar 

  • Goutte A, Bustamante P, Barbraud C, Delord K, Weimeskirch H, Chastel O (2014) Demographic responses to mercury exposure in two closely-related Antarctic top predators. ESA Ecol. doi:10.1890/13-1229.1

    Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188

    Article  Google Scholar 

  • Honda K, Marcovecchio JE, Kan S, Tatsukawa R, Ogi H (1990) Metal concentrations in pelagic seabirds from the North Pacific Ocean. Arch Environ Contam Toxicol 19:704–711

    Article  CAS  PubMed  Google Scholar 

  • Ikemoto T, Kunito T, Tanaka H, Baba N, Miyazaki N, Tanabe S (2004) Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver. Arch Environ Contam Toxicol 47:402–413

    CAS  PubMed  Google Scholar 

  • Jackson S (1988) Diets of the white-chinned petrel and sooty shearwater in the southern Benguela region, South Africa. Condor 90:20–28

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Klaassen CD, Liu J, Choudhuri S (1999) Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmacol Toxicol 39:267–294

    Article  CAS  PubMed  Google Scholar 

  • Kojadinovic J, Le Corre M, Cosson RP, Bustamante P (2007) Trace elements in three marine birds breeding on Reunion Island (Western Indian ocean): part 1-factors influencing their bioaccumulation. Arch Environ Contam Toxicol 52:418–430

    Article  CAS  PubMed  Google Scholar 

  • Levengood JM, Skowron LM (2007) Coaccumulation of cadmium and zinc in tissues of sentinel mallards (Anas platyrhynchos) using a former dredge-disposal impoundment. Arch Environ Contam Toxicol 53:281–286

    Article  CAS  PubMed  Google Scholar 

  • Mailman RB (1980) Heavy metals. In: Perry JJ (ed) Introduction to environmental toxicology. Elsevier, New York, pp 34–43

    Google Scholar 

  • Malinga M, Szefer P, Gabrielsen GW (2010) Age, sex and spatial dependent variations in heavy metals levels in the Glaucous Gulls (Larus hyperboreus) from the Bjørnøya and Jan Mayen, Arctic. Environ Monit Assess 169:407–416

    Article  CAS  PubMed  Google Scholar 

  • Metian M, Warnau M, Chouvelon T, Pedraza F, Rodriguez Y, Baena AM, Bustamante P (2013) Trace element bioaccumulation in reef fish from New Caledonia: influence of trophic groups and risk assessment for consumers. Mar Environ Res 87(88):26–36

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Monteiro LR, Costa V, Furness RW, Santos RS (1996) Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environments. Mar Ecol Prog Ser 141:21–25

    Article  CAS  Google Scholar 

  • Muirhead S, 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 

  • Nigro M, Leonzio C (1996) Intracellular storage of mercury and selenium in different marine vertebrates. Mar Ecol Prog Ser 135:137–143

    Article  CAS  Google Scholar 

  • Ninomiya R, Koizumi N, Murata K (2004) Metal concentrations in the liver and kidney of aquatic mammals and penguins. Biol Trace Elem Res 97:135–148

    Article  CAS  PubMed  Google Scholar 

  • Norheim G (1987) Levels and interactions of heavy metals in sea birds from Svalbard and the Antarctic. Environ Pollut 47:83–94

    Article  CAS  PubMed  Google Scholar 

  • Ochoa-acuña H, Sepúlveda MS, Gross TS (2002) Mercury in feathers from Chilean birds: influence of location, feeding strategy, and taxonomic affiliation. Mar Pollut Bull 44:340–345

    Article  PubMed  Google Scholar 

  • Péron C, Delord K, Phillips RA, Charbonnier Y, Marteau C, Louzao M, Weimerskirch H (2010) Seasonal variation in oceanographic habitat and behaviour of white-chinned petrels Procellaria aequinoctialis from Kerguelen Island. Mar Ecol Prog Ser 416:267–284

    Article  Google Scholar 

  • Ridoux V (1994) The diets and dietary segregation of seabirds at the subantarctic Crozet Islands (part 1). Mar Ornithol 22:1–64

    Google Scholar 

  • Ritterhoff J, Zauke GP (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

    Article  CAS  Google Scholar 

  • Scheuhammer AM (1987) The chronic toxicity of aluminium, cadmium, mercury, and lead in birds: a review. Environ poll 46:263–295

    Article  CAS  Google Scholar 

  • Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–18

    Article  CAS  PubMed  Google Scholar 

  • Selin NE (2009) Global biogeochemical cycling of mercury: a review. Annu Rev Environ Resour 34:43–63

    Article  Google Scholar 

  • 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 178:295–305

    Article  CAS  Google Scholar 

  • Tan SW, Meiller JC, Mahaffey KR (2009) The endocrine effects of mercury in humans and wildlife. Crit Rev Toxicol 39:228–269

    Article  CAS  PubMed  Google Scholar 

  • Tartu S, Goutte A, Bustamante P, Angelier F, Moe B, Clément-Chastel C, Bech C, Gabrielsen GW, Bustness JO, Chastel O (2013) To breed or not to breed: endocrine response to mercury contamination by an arctic seabird. Biol Lett 9:20130317

    Article  PubMed  Google Scholar 

  • Thompson DR, Furness RW, Monteiro LR (1998) Seabirds as biomonitors 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 ed, New York

  • 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

    Google Scholar 

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Acknowledgments

The authors thank the fieldworkers who helped with collecting the petrels. The present work was supported financially and logistically by the Agence Nationale de la Recherche (programme POLARTOP, O. Chastel), the Institut Polaire Français Paul Emile Victor (IPEV, programme no. 109, H. Weimerskirch) and the Terres Australes et Antarctiques Françaises (TAAF). 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).

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  1. Littoral Environnement et Sociétés (LIENSs), UMR 7266, CNRS-Université de La Rochelle, 2 rue Olympe de Gouges, 17042, La Rochelle Cedex 01, France

    Caio V. Z. Cipro, Florence Caurant, Pierre Miramand, Paula Méndez-Fernandez & Paco Bustamante

  2. Centre d’Etudes Biologiques de Chizé, UPR 1934 du Centre National de la Recherche Scientifique, BP 14, 79360, Villiers-en-Bois, France

    Caio V. Z. Cipro & Yves Cherel

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  1. Caio V. Z. Cipro
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  2. Yves Cherel
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  3. Florence Caurant
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Correspondence to Caio V. Z. Cipro.

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Cipro, C.V.Z., Cherel, Y., Caurant, F. et al. Trace elements in tissues of white-chinned petrels (Procellaria aequinoctialis) from Kerguelen waters, Southern Indian Ocean. Polar Biol 37, 763–771 (2014). https://doi.org/10.1007/s00300-014-1476-z

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  • DOI: https://doi.org/10.1007/s00300-014-1476-z

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