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Trace Elements in Three Marine Birds Breeding on Reunion Island (Western Indian Ocean): Part 1—Factors Influencing Their Bioaccumulation

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Abstract

This work aimed to use seabirds as bioindicators of trace element levels in the tropical waters and food webs of the Western Indian Ocean. The accumulation patterns of selected toxic (Cd and Hg) and essential (Cu, Fe, Mn, Se, and Zn) elements were determined in liver, kidney, and pectoral muscle of 162 marine birds belonging to 3 species collected in Reunion Island between 2002 and 2004. These pelagic seabirds belong to the following species: Barau’s Petrel (Pterodroma baraui), Audubon’s Shearwater (Puffinus lherminieri bailloni), and White-Tailed Tropicbird (Phaethon lepturus). Hg levels were also measured in breast feathers. Highest mean kidney Cd and liver Hg levels (respectively, 27.79 ± 13.78 μg.g −1 dry weight (dw) and 24.31 ± 14.13 μg.g −1 dw) were found in the squid-eating Barau’s Petrel. Barau’s Petrel feather Hg levels fell in the range of 0.6 to 2.7 μg.g−1 dw previously reported for other petrels and shearwaters. The values of the other elements were also in the same range as those previously reported in the published literature concerning related seabirds, although Se and Zn burdens in the Reunion birds were among the highest values. Levels of Zn, Fe, and, to a lesser extent, Cu appeared to be regulated in seabird tissues. Uptake and pathways of metabolism and storage seemed to be similar for the five essential elements. The reproductive status of the bird did not seem to affect element levels, which, moreover, were not significantly different between male and female birds. However, trace elements in sampled birds varied according to the tissue considered, the age of the animal, and its species. Diet was seemingly a major influencing factor. Health status also appeared to have an impact on element levels.

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References

  • Ancora S, Volpi V, Olmastroni S, Focardi S, Leonzio C (2002) Assumption and elimination of trace elements in adélie penguins from antartica: A preliminary study, Mar Environ Res 54:341–344

    Article  CAS  Google Scholar 

  • Bailey RS (1967) The pelagic distribution of sea-birds in the Western Indian Ocean. Ibis 110:492–493

    Google Scholar 

  • Barré N, Barau A, Jouanin C (1996) Oiseaux de la Réunion. Paris, France, Les Editions du Pacifique

    Google Scholar 

  • Bearhop S, Waldreon S, Thompson D, Furness R (2000) Bioamplification of mercury in Great Skua and Catharacta Skua chicks: The influence of trophic status as determined by stable isotope signatures of blood and feathers. Mar Poll Bull 40:181–185

    Article  CAS  Google Scholar 

  • Bloom NS (1992) A survey of size-specific mercury concentrations ingame fish from Maryland fresh and estuarine waters. Arch Environ Contam Toxicol 39:53–59

    Google Scholar 

  • Bocher P, Caurant F, Cherel Y, Miramand P, Bustamarite 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 

  • Bolton M, Monaghan P, Houston DC (1991) An improved technique for estimating pectoral muscle protein condition from body measurements of live gulls. Ibis 133:264–270

    Google Scholar 

  • Bretagnolle V, Attié C (1991) Status of Barau’s Petrel Pterodroma baraui: Colony sites, breeding population and taxonomic affinities. Colonial Waterbirds 14:25–33

    Article  Google Scholar 

  • Burger J (1993) Metals in feathers of brown noddy (Anous stolidus): Evidence for bioaccumulation or exposure levels? Environ Monit Asses 24:181–187

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (1997) Risk, mercury levels, and birds: Relating adverse laboratory effects to field biomonitoring. Environ Res 75:160–172

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (2000) Metal levels in feathers of 12 species of seabirds from Midway Atoll in the northern Pacific Ocean. Sci Total Environ 257:37–52

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bustamante P, Cherel Y, Caurant F, Miramand P (1998b) Cadmium, copper and zinc in octopuses from the Kerguelen islands, Southern Indian Ocean. Polar Biol 19:264–271

    Article  Google Scholar 

  • Bustamante R, Lahaye V, Durnez C, Churlaud C, Caurant F (2006) Total and organic Hg concentrations in cephalopods from the north east atlantic waters: Influence of geographical origin and feeding ecology. Science of the Total Environment 368(2–3):585–596

    Article  Google Scholar 

  • Clarke (1986) A handbook for the identification of cephalopod beaks. Oxford, UK, Sierra Club Books

  • Debacker V, Jauniaux T, Coignoul F, Bouquegneau J-M (2001a) Heavy metal contamination arid body condition of wintering Guillemots (Uria aatge) at the Belgian coast from 1993 to 1998. Environ Res 84:310–317

    Article  Google Scholar 

  • Debacker V, Schiettecatte L-S, Jauniaux T, Bouquegneau J-M (2001b) Influence of age, sex and body condition on zinc, copper, cadmium and metallothioneins in Common Guillemots (Uria aalqe) stranded at the Belgian coast. Mar Environ Res 52:427–444

    Article  CAS  Google Scholar 

  • Eisler R (1985) Cadmium hazards to fish, wildlife, and invertebrates: A synoptic review. Technical Report 1.2, Fish and Wildlife Service United States

  • Eisler R (1987) Cadmium hazards to fish, wildlife, and invertebrates: A synoptic review. Technical Report 1.10, Fish and Wildlife Service

  • Elliott JE, Scheuhammer A, Leighton FA, Pearce PA (1992), Heavy metal and metal lothionein concentrations in Atlantic Canadian seabirds. Arch Environ Toxical 22:63–73

    Article  CAS  Google Scholar 

  • Fiona FM, Phillips 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

    Google Scholar 

  • Furness RW (1996) Cadmium in birds. In: Beyer WN, Heinz GH, Redmon- AW (eds) Environmental contaminants in wildlife: Interpreting tissues concentrations. Boca Raton, FL, Lewis, pp. 389–404

    Google Scholar 

  • Furness RW, Greenwood JJD, Jarvis PJ, Lehr Brisbin I, Ormerod SJ, Tyler SJ, et al. (1993) Birds as monitors of environmental changes, Cornwall, UK, Chapman and Hall

    Google Scholar 

  • Furness RW, Rainbow PS (1990) Heavy metals in the marine environment. Boca Raton, FLO, CRC Press

    Google Scholar 

  • Gonzalez-Solis J, Sanpera C, Ruiz X (2002) Metals and selenium as bioindicators of geographic and trophic segregation in Giant Petrels Macronectes. Mar Ecol Prog Sen 244:257–264

    CAS  Google Scholar 

  • Gray J (2002) Biomagnification in marine systems: The perspective of an ecologist. Mar Pollut Bull 45:46–52

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jaquemet S Le Corre M, Weimerskirch H (2004) Seabird community structure in a coastal tropical environment: importance of natural factors and fish aggregating devices (fads). Mar Ecol Prog Ser 268:281–292

    Google Scholar 

  • Jouanin C (1963) Un pétrel nouveau de La Réunion Bulweria baraui. Bull Muséum National d’Histoire Naturelle 35:593–597

    Google Scholar 

  • Kim EY, Goto R, Tanaka S, Tatsukawa R (1998) Distribution of 14 elements in tissues and organs of oceanic seabirds. Arch Environ Contam Toxicol 33:638–645

    Article  Google Scholar 

  • Kim EY Saeki K, Tanabe S, Tanaka S, Tatsukawa R (1996) Specific accumulation of mercury and selenium in seabirds. Environ Pollut 95:261–265

    Article  Google Scholar 

  • Le Corre M (2000) Taxonomic affinities of Audubon’s shearwater from Europa Island. Condor 102:187–190

    Article  Google Scholar 

  • Le Corre M, Ollivier A, Ribes S Jouventin P (2001) Light-induced mortality of petrels: A 4-year study from Reunion Island (Indian Ocean). Biol Consen 105:93–102

    Article  Google Scholar 

  • Le Corre M, Safford R (2000) Réunion et iles éparses. In: Fishpool, Evans (eds) Important bird areas in Africa and associated islands: Priority sites for conservation. BirdLife Conservation series no.11. Pisces Publication, Cambridge, UK, pp 693–702

  • Monteiro LR, Costa V, Furness RW, Santos RS (1996) Mercury concentrations in prey fish indicate enhanced bioaccumulation in mesopelagic environment Mar Ecol Prog Ser 14l:21–25

    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 

  • 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 

  • Nesis (1987) Cephalopods of the world. T F H. Publications

  • Ochoa-Acuna H, Sepulveda MS, Gross TS (2002) Mercury in feathers from Chilean birds: Influence of location, feeding strategy and taxonomic effiliation. Mar Pollut Bull 44:340–349

    Article  CAS  Google Scholar 

  • R Development Core Team (2005) R: A language and environment for statistical computing. Vienna, Austria, Boca Raton, FL, R Foundation for Statistical Computing

    Google Scholar 

  • Schreiber EA, Burger J, (2001) Biology of marine birds. Boca Raton, FL, CRC Press

    Google Scholar 

  • Smith JD, Plues L, Heyraud M, Cherry RD (1984) Concentrations of the elements Ag, Al, Ca, Cd, Cu, Fe, Mg, Pb and Zn, and the radionuclides 210po in the digestive gland of the squid Nototodarus gouldi. Mar Environ Res 68:13–55

    Google Scholar 

  • Stahl J, Bartle JA (1991) Distribution, abundance and aspects of the pelagic ecology of Barau’s Petrel (Pterodroma baraui) in the south-west Indian Ocean. Notornis 38:211–225

    Google Scholar 

  • Stewart FM, Monteiro LR, Furness RW (1997) Heavy metal concentrations in Cory’s sheawater, Calonectris diomedea, fledglings from the Azores, Portugal. Bull Environ Contam Toxicol 58:115–122

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Stewart FM, Thompson DR, Furness RW, Harrison N (1994) Seasonal variation in heavy metals in tissues of Common Guillemots, Uria aalqe from northwest Scotland. Arch Environ Contam Toxicol 27:168–175

    Article  CAS  Google Scholar 

  • Szefer P, Pempkowiak J, Skwarzec B, Bojaniowski R, Holm E (1993) Concentration of selected metals in penguins and other representative fauna of the antartic. Sci Total Environ 138:28l–288

    Article  Google Scholar 

  • Thompson DR, Furness RW, Heinz GH (1996) Environmental contaminants in wildlife. Interpreting tissue concentrations. New York, NY, Beyer, Heinz and Redmon-Norwood

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Walsh PM (1990) The use of seabirds as monitors of heavy metals in the marine environment. In: Furness R, Rainbow P (eds) Heavy metals in the marine environment. Boca Raton, FL, CRC Press, pp. 183–205

    Google Scholar 

  • Weimerskirch H (2001) Seabird demography and its relationship with the marine environment. In: Schreiber EA, Burger J (eds) Biology of Mar birds. Boca Raton, FL, CRC Press pp. 115–135

    Google Scholar 

  • Wenzel C, Adelung D (1996) The suitability of oiled Guillemots (Uria aalge) as monitoring organisms for geographical comparisons of trace element contaminants. Arch Environ Contam Toxicol 31:368–377

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Conseil Général de La Réunion. J. K. also benefited from support of the Conseil Régional de La Réunion and the European Social Fund through a doctoral grant. The authors would like to thank E. Robert, M. Rouquette, P. Grondin, and N. Ghanem in La Réunion for their help with tissue preparation and C. Churlaud, Centre Commun d’ Analyse (La Rochelle), for her assistance with the analyses on the ICP-AES. We would also like to thank the numerous volunteers who participate in the SEOR Petrel rescue program. We are also grateful toward the referees for helpful comments on the manuscript.

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Authors and Affiliations

  1. Université de La Réunion, ECOMAR, 15 Avenue René Cassin, Saint Denis de La Réunion, F-97715, France

    J. Kojadinovic & M. Le Corre

  2. Université de Nantes, EMI, EA 2663, BP 92208, Nantes Cedex 3, F-44322, France

    J. Kojadinovic & R. P. Cosson

  3. CRELA, UMR 6217, CNRS-IFREMER–Université de La Rochelle, 22 Avenue Michel Crépeau, La Rochelle, F-17042, France

    J. Kojadinovic & P. Bustamante

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  1. J. Kojadinovic
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Correspondence to J. Kojadinovic.

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Kojadinovic, J., Corre, M.L., Cosson, R.P. et al. 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 (2007). https://doi.org/10.1007/s00244-005-0225-2

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