Maternal transfer of trace elements in leatherback turtles (Dermochelys coriacea) of French Guiana

[en] In sea turtles, parental investment is limited to the nutrients and energy invested in eggs that will support embryonic development. Leatherback females have the largest clutches with the biggest eggs of the sea turtles and the highest reproductive output in reptiles. The migration between foraging sites and nesting beaches also represents high energy expenditure. The toxicokinetic of pollutants in the tissues is thus expected to vary during those periods but there is a lack of information in reptiles. Concentrations of essential (Copper, Zinc, Selenium) and non-essentials elements (Cadmium, Lead, Mercury) were determined in blood (n = 78) and eggs (n = 76) of 46 free-ranging leatherback females collected in French Guiana. Maternal transfer to eggs and relationships between blood and eggs concentrations during the nesting seasonwere investigated. All trace elementswere detectable in both tissues. Levels of toxic metals were lower than essential elements likely due to the high pelagic nature of leatherbacks that seems to limit exposure to toxic elements. Significant relationships between blood and egg concentrations were observed for Se and Cd. Se could have an important role in embryonic development of leatherback turtles and Cd transfer could be linked to similar carrier proteins as Se. Finally, as multiple clutcheswere sampled from each female, trends in trace elements were investigated along the nesting season. No change was observed in eggs but changeswere recorded in blood concentrations of Cu. Cu level decreased while blood Pb levels increased through the nesting season. The high demand on the body during the breeding season seems to affect blood Cu concentrations. Calcium requirement for egg production with concomitant Pb mobilization could explain the increase in blood Pb concentrations along the nesting season.

Research Center/Unit :

MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège

Disciplines :

Aquatic sciences & oceanology
Chemistry
Zoology
Environmental sciences & ecology

Author, co-author :

Guirlet, Elodie ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie

Das, Krishna ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie

Girondot, Marc; Université de Paris Sud > Laboratoire d’Ecologie, Systématique et Evolution

Language :

English

Title :

Maternal transfer of trace elements in leatherback turtles (Dermochelys coriacea) of French Guiana

Publication date :

2008

Journal title :

Aquatic Toxicology

ISSN :

0166-445X

eISSN :

1879-1514

Publisher :

Elsevier Science, Amsterdam, Netherlands

Volume :

Pages :

267-276

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 27 November 2008

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111

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Bibliography

Anan Y., Kunito T., Watanabe I., Sakai H., and Tanabe S. Trace element accumulation in hawksbill turtles (Eretmochelys imbricata) and green turtles (Chelonia mydas) from Yaeyama Islands, Japan. Environ. Toxicol. Chem. 20 (2001) 2802-2814
Andreani G., Santoro M., Cottignoli S., Fabbri M., Carpenè E., and Isani G. Metal distribution and metallothionein in loggerhead (Caretta caretta) and grenn (Chelonia mydas) sea turtles. Sci. Total Environ. 390 (2008) 287-294
Bell B.A., Spotila J.R., Paladino F.V., and Reina R.D. Low reproductive success of leatherback turtles, Dermochelys coriacea, is due to high embryonic mortality. Biol. Conserv. 115 (2003) 131-138
Bergeron C.M., Husak J.F., Unrine J.M., Romanek C.S., and Hopkins W.A. Influence of feeding ecology on blood mercury concentrations in four species of turtles. Environ. Toxicol. Chem. 26 (2007) 1733-1741
Bilinski J.J., Reina R.D., Spotila J.R., and Paladino F.V. The effects of nest environment on calcium mobilization by leatherback turtle embryos (Dermochelys coriacea) during development. Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 130 (2001) 151-162
Blanvillain G., Schwenter J.A., Day R.D., Point D., Christopher S.J., Roumillat W.A., and Owens D.W. Diamondback terrapins, Malaclemys terrapin, as a sentinel species for monitoring mercury pollution of estuarine systems in South Carolina and Georgia, USA. Environ. Toxicol. Chem. 26 (2007) 1441-1450
Brasfield S.M., Bradham K., Wells J.B., Talent L.G., Lanno R.P., and Janz D.M. Development of a terrestrial vertebrate model for assessing bioavailability of cadmium in the fence lizard (Sceloporus undulatus) and in ovo effects on hatchling size and thyroid function. Chemosphere 54 (2004) 1643-1651
Burger J., and Gochfeld M. Cadmium and lead in common terns (Aves Sterna-Hirundo)-relationship between levels in parents and eggs. Environ. Monit. Assess. 16 (1991) 253-258
Burger J., Carruth-Hinchey C., Ondroff E., McMahon M., Gibbons J.W., and Gochfeld M. Effects of lead on behavior, growth, and survival of hatchling slider turtles. J. Toxicol. Environ. Health Part A 55 (1998) 495-502
Burger J., and Gibbons J.W. Trace elements in egg contents and egg shells of slider turtles (Trachemys scripta) from the savannah river site. Arch. Environ. Contam. Toxicol. 34 (1998) 382-386
Canas J.E., and Anderson T.A. Organochlorine contaminants in eggs: the influence of contaminated nest material. Chemosphere 47 (2002) 585-589
Caurant F., Bustamante P., Bordes M., and Miramand P. 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 (1999) 1085-1091
Caut S., Guirlet E., Jouquet P., and Girondot M. Influence of nest location and yolkless eggs on the hatching success of leatherback turtle clutches in French Guiana. Can. J. Zool. 84 (2006) 908-915
Caut, S., Guirlet, E., Angulo, E., Das, K., Girondot, M., 2008. Isotope analysis reveals foraging area dichotomy for Atlantic leatherback turtles. PLoS One 3(3), e1845, doi:10.1371/journal.pone.0001845.
Clarkson T.W., Vyas J.B., and Ballatorl N. Mechanisms of mercury disposition in the body. Am. J. Ind. Med. 50 (2007) 757-764
Creocean, 2006. Déclaration d'ouverture de travaux de recherche de mines d'hydrocarbures liquides ou gazeux. In: Hardman Petroleum France (Ed.), Pièce n°3: Notice d'impact, Tome 3: Etude biosédimentaire, pp. 1-112.
Damstra T., Barlow S., Bergman A., Kavlock R., and Van der Kraak G. Global Assessment of the State-of-the-Science of Endocrine Disruptors, WHO Publication No. WHO/PCS/EDC/02.2 (2002), World Health Organization, Geneva, Switzerland
Das K., Debacker V., Pillet S., and Bouquegneau J.M. Heavy metals in marine mammals. In: Vos J.G., Bossart G., Fournier M., and O'Shea T. (Eds). Toxicology of Marine Mammals (2003), Taylor and Francis Publishers, Washington D.C. 135-167
Davenport J. Sustaining endothermy on a diet of cold jelly: energetics of the leatherback turtle Dermochelys coriacea. Herpet. Bull. 62 (1998) 4-8
Day R.D., Christopher S.J., Becker P.R., and Whitaker D.W. Monitoring mercury in the loggerhead sea turtle, Caretta caretta. Environ. Sci. Technol. 39 (2005) 437-446
Debier C., Pomeroy P.P., Dupont C., Joiris C., Comblin V., Le Boulenge E., Larondelle Y., and Thome J.P. Dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus: differences in PCB profile between compartments of transfer and changes during the lactation period. Mar. Ecol. -Prog. Ser. 247 (2003) 249-256
Debier C., Pomeroy P.P., Dupont C., Joiris C., Comblin V., Le Boulenge E., Larondelle Y., and Thome J.P. Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar. Ecol. -Prog. Ser. 247 (2003) 237-248
Debier C., Chalon C., Le Boeuf B.J., de Tillesse T., Larondelle Y., and Thome J.P. Mobilization of PCBs from blubber to blood in northern elephant seals (Mirounga angustirostris) during the post-weaning fast. Aquat. Toxicol. 80 (2006) 149-157
Devkota B., and Schmidt G.H. Effects of heavy metals (Hg2+, Cd2+, Pb2+) during the embryonic development of acridid grasshoppers (Insecta Caelifera). Arch. Environ. Contam. Toxicol. 36 (1999) 405-414
Doyle T.K., Houghton J.D.R., O'Suilleabhain P.F., Hobson V.J., Marnell F., Davenport J., and Hays G.C. Leatherback turtles satellite-tagged in European Waters. Endangered Species Res. (2007) 3
Eisler, R., 1985. Cadmium hazards to fish, wildlife, and invertebrates: A synoptic review. US Fish and Wildlife Service. Biological Report 85 (1.2).
Eisler R, 1988, Lead hazards to fish, wildlife, and invertebrates: A synoptic review. US Fish and Wildlife Service. Biological Report 85 (1.14).
Eisler, R., 1998. Copper hazards to fish, wildlife and invertebrates: A synoptic review. US Fish and Wildlife Service. Biological Science Report USGS/BRD/BSR 1997-0002.
Falchuk K.H., and Montorzi M. Zinc physiology and biochemistry in oocytes and embryos. Biometals 14 (2001) 385-395
Ferraroli S., Georges J.Y., Gaspar P., and Le Maho Y. Endangered species-Where leatherback turtles meet fisheries. Nature 429 (2004) 521-522
Fossette S., Ferraroli S., Tanaka H., Ropert-Coudert Y., Arai N., Sato K., Naito Y., Le Maho Y., and Georges J.Y. Dispersal and dive patterns in gravid leatherback turtles during the nesting season in French Guiana. Mar. Ecol. -Prog. Ser. 338 (2007) 233-247
Fretey J., Billes A., and Tiwari M. Leatherback, Dermochelys coriacea, nesting along the Atlantic coast of Africa. Chelon. Conserv. Biol. 6 (2007) 126-129
Ghosh P., and Thomas P. Binding of metals to Red Drum Vitellogenin and incorporation into oocytes. Mar. Environ. Res. 39 (1995) 165-168
Girondot M., and Fretey J. Leatherback turtles, Dermochelys coriacea, nesting in French Guiana 1978-1995. Chelon. Conserv. Biol. 2 (1996) 204-208
Godley B.J., Thompson D.R., and Furness R.W. Do heavy metal concentrations pose a threat to marine turtles from the Mediterranean Sea?. Mar. Pollut. Bull. 38 (1999) 497-502
Greig D.J., Ylitalo G.M., Hall A.J., Fauquier D.A., and Gulland F.M.D. Transplacental transfer of organochlorines in California sea lions (Zalophus californianus). Environ. Toxicol. Chem. 26 (2007) 37-44
Hamer D.H. Metallothionein. Annu. Rev. Biochem. 55 (1986) 913-951
Hammerschmidt C.R., Wiener J.G., Frazier B.E., and Rada R.G. Methylmercury content of eggs in yellow perch related to maternal exposure in four Wisconsin lakes. Environ. Sci. Technol. 33 (1999) 999-1003
Hays G.C., Houghton J.D.R., and Myers A.E. Endanqered species-Pan-Atlantic leatherback turtle movements. Nature 429 (2004) 522-1522
Hewavisenthi S., and Parmenter C.J. Influence of incubation environment on the development of the flatback turtle (Natator depressus). Copeia (2001) 668-682
Hewavisenthi S., and Parmenter C.J. Egg components and utilization of yolk lipids during development of the flatback turtle Natator depressus. J. Herpetol. 36 (2002) 43-50
Hopkins W.A., Rowe C.L., and Congdon J.D. Elevated trace element concentrations and standard metabolic rate in banded water snakes (Nerodia fasciata) exposed to coal combustion wastes. Environ. Toxicol. Chem. 18 (1999) 1258-1263
Hopkins W.A., Staub B.P., Baionno J.A., Jackson B.P., Roe J.H., and Ford N.B. Trophic and maternal transfer of selenium in brown house snakes (Lamprophis fuliginosus). Ecotoxicol. Environ. Saf. 58 (2004) 285-293
Hopkins W.A., DuRant S.E., Staub B.P., Rowe C.L., and Jackson B.P. Reproduction, embryonic development, and maternal transfer of contaminants in the amphibian Gastrophryne carolinensis. Environ. Health Perspect. 114 (2006) 661-666
James M.C., Ottensmeyer C.A., and Myers R.A. Identification of high-use habitat and threats to leatherback sea turtles in northern waters: new directions for conservation. Ecol. Lett. 8 (2005) 195-201
Kaplan I.C. A risk assessment for Pacific leatherback turtles (Dermochelys coriacea). Can. J. Fish. Aquat. Sci. 62 (2005) 1710-1719
Kaska Y., and Furness R.W. Heavy metals in marine turtle eggs and hatchlings in the Mediterranean. Zool. Middle East 24 (2001) 127-132
Keen C.L., Taubeneck M.W., Zidenberg-Cherr S., Daston G.P., and Rogers J.M. Toxicant exposure and trace element metabolism in pregnancy. Environ. Toxicol. Pharmacol. 4 (1997) 301-308
Kelleher S.L., and Lonnerdal B. Molecular regulation of milk trace mineral homeostasis. Mol. Aspects Med. 26 (2005) 328-339
Kenyon L.O., Landry A.M., and Gill G.A. Trace metal concentrations in blood of the Kemp's Ridley Sea Turlte (Lepidochelys kempii). Chelon. Conserv. Biol. 4 (2001) 128-135
Kitana N., and Callard I.P. Effect of cadmium on gonadal development in freshwater turtle (Trachemys scripta Chrysemys picta) embryos. J. Environ. Sci. Health Part A-Toxic/Hazard. Subst. Environ. Eng. 43 (2008) 262-271
Klaassen C.D., Liu J., and Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 267-294
Kobayashi N., and Okamura H. Effects of heavy metals on sea urchin embryo development. 1. Tracing the cause by the effects. Chemosphere 55 (2004) 1403-1412
Kubota R., Kunito T., Tanabe S., Ogi H., and Shibata Y. Maternal transfer of arsenic to eggs of black-tailed gull (Larus crassirostris) from Rishiri Island, Japan. Appl. Organomet. Chem. 16 (2002) 463-468
Lam J.C.W., Tanabe S., Chan S.K.F., Lam M.H.W., Martin M., and Lam P.K.S. Levels of trace elements in green turtle eggs collected from Hong Kong: evidence of risks due to selenium and nickel. Environ. Pollut. 144 (2006) 790-801
Maffucci F., Caurant F., Bustamante P., and Bentivegna F. Trace element (Cd, Cu, Hg, Se Zn) accumulation and tissue distribution in loggerhead turtles (Caretta caretta) from the Western Mediterranean Sea (southern Italy). Chemosphere 58 (2005) 535-542
Marchand C., Lallier-Verges E., Baltzer F., Alberic P., Cossa D., and Baillif P. Heavy metals distribution in mangrove sediments along the mobile coastline of French Guiana. Mar. Chem. 98 (2006) 1-17
Marco A., Lopez-Vicente M., and Perez-Mellado V. Arsenic uptake by reptile flexible-shelled eggs from contaminated nest substrates and toxic effect on embryos. Bull. Environ. Contam. Toxicol. 72 (2004) 983-990
Martinez L.S., Barragan A.R., Munoz D.G., Garcia N., Huerta P., and Vargas F. Conservation and biology of the leatherback turtle in the Mexican Pacific. Chelon. Conserv. Biol. 6 (2007) 70-78
McNabb F.M.A., and Wilson C.M. Thyroid hormone deposition in avian eggs and effects on embryonic development. Am. Zool. 37 (1997) 553-560
Miller J.D. Embryology of marine turtles. In: Gans C., Billet F., and Maderson P.F.A. (Eds). Biology of the Reptilia (1985), John Wiley and Sons, New York 269-328
Miller J.D. Reproduction in sea turtles. In: Lutz P.L., and Musick J.A. (Eds). The Biology of Sea Turtles (1997), CRC Press 51-82
Miller J.D., Limpus C.J., and Godfrey M.H. Nest Site selection, oviposition, eggs, development, hatching, and emergence of loggerhead turtles. In: Bolten A.B., and Witherington B.E. (Eds). Loggerhead Sea Turtles (2003), Smithsonian Institution Press 125-143
Mol J.H., Ramlal J.S., Lietar C., and Verloo M. Mercury contamination in freshwater, estuarine, and marine fishes in relation to small-scale gold mining in Suriname, South America. Environ. Res. 86 (2001) 183-197
Nagle R.D., Rowe C.L., and Congdon J.D. Accumulation and selective maternal transfer of contaminants in the turtle Trachemys scripta associated with coal ash deposition. Arch. Environ. Contam. Toxicol. 40 (2001) 531-536
Nendza M., Herbst T., Kussatz C., and Gies A. Potential for secondary poisoning and biomagnification in marine organisms. Chemosphere 35 (1997) 1875-1885
Nicoletto P.F., and Hendricks A.C. Sexual differences in accumulation of mercury in 4 species of centrarchid fishes. Can. J. Zool. 66 (1988) 944-949
Noonan C.W., Sarasua S.M., Campagna D., Kathman S.J., Lybarger J.A., and Mueller P.W. Effects of exposure to low levels of environmental cadmium on renal biomarkers. Environ. Health Perspect. 110 (2002) 151-155
Ozdilek H.G., and Ozdilek S.Y. Impact of corrosive trace elements on sea turtle eggs during embryonic growth. Asian J. Chem. 19 (2007) 807-809
Palmer B.D., Demarco V.G., and Guillette L.J. Oviductal morphology and eggshell formation in the lizard sceloporus woodi. J. Morphol. 217 (1993) 205-217
Palmiter R.D. The elusive function of metallothioneins. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 8428-8430
Pappas A.C., Karadas F., Surai P.F., Wood N.A.R., Cassey P., Bortolotti G.R., and Speake B.K. Interspecies variation in yolk selenium concentrations among eggs of free-living birds: the effect of phylogeny. J. Trace Elem. Med. Biol. 20 (2006) 155-160
Pattee O.H., and Pain D.J. Lead in the environment. In: Hoffman D.R., Rattner B.A., Burton Jr. G.A., and Cairns Jr. J. (Eds). Handbook of Ecotoxicology (2003), CRC Press Inc., Boca Raton, FL 373-408
Richard S., Arnoux A., Cerdan P., Reynouard C., and Horeau V. Mercury levels of soils, sediments and fish in French Guiana, South America. Water Air Soil Pollut. 124 (2000) 221-244
Riggio M., Lee J., Scudiero R., Parisi E., Thiele D.J., and Filosa S. High affinity copper transport protein in the lizard Podarcis sicula: molecular cloning, functional characterization and expression in somatic tissues, follicular oocytes and eggs. Biochim. Biophys. Acta-Gene Struct. Expr. 1576 (2002) 127-135
Riggio M., Trinchella F., Filosa S., Parisi E., and Scudiero R. Accumulation of zinc, copper, and metallothionein mRNA in lizard ovary proceeds without a concomitant increase in metallothionein content. Mol. Reprod. Dev. 66 (2003) 374-382
Rivalan P., Prevot-Julliard A.C., Choquet R., Pradel R., Jacquemin B., and Girondot M. Trade-off between current reproductive effort and delay to next reproduction in the leatherback sea turtle. Oecologia 145 (2005) 564-574
Roe J.H., Hopkins W.A., Baionno J.A., Staub B.P., Rowe C.L., and Jackson B.P. Maternal transfer of selenium in Alligator mississippiensis nesting downstream from a coal-burning power plant. Environ. Toxicol. Chem. 23 (2004) 1969-1972
Rostal D.C., Paladino F.V., Patterson R.M., and Spotila J.R. Reproductive physiology of nesting leatherback turtles (Dermochelys coriacea) at Las Baulas de Guanacaste National Park, Costa Rica. Chelon. Conserv. Biol. 2 (1996) 27-35
Rostal D.C., Grumbles J.S., Palmer K.S., Lance V.A., Spotila J.R., and Paladino F.V. Changes in gonadal and adrenal steroid levels in the leatherback sea turtle (Dermochelys coriacea) during the nesting cycle. Gen. Comp. Endocrinol. 122 (2001) 139-147
Russell R.W., Gobas F., and Haffner G.D. Maternal transfer and in ovo exposure of organochlorines in oviparous organisms: a model and field verification. Environ. Sci. Technol. 33 (1999) 416-420
Sakai H., Ichihashi H., Suganuma H., and Tatsukawa R. Heavy-metal monitoring in sea-turtles using eggs. Mar. Pollut. Bull. 30 (1995) 347-353
Sakai H., Saeki K., Ichihashi H., Kamezaki N., Tanabe S., and Tatsukawa R. Growth-related changes in heavy metal accumulation in green turtle (Chelonia mydas) from Yaeyama Islands, Okinawa, Japan. Arch. Environ. Contam. Toxicol. 39 (2000) 378-385
SAS Institute Inc. SAS, 9.1.3, Help and Documentation (2004), SAS Institute Inc., Cary, NC, USA
Sasakura C., and Suzuki K.T. Biological interaction between transition metals (Ag, Cd and Hg), selenide/sulfide and selenoprotein P. J. Inorg. Biochem. 71 (1998) 159-162
Shepherdley C.A., Daniels C.B., Orgeig S., Richardson S.J., Evans B.K., and Darras V.M. Glucocorticoids, thyroid hormones, and iodothyronine deiodinases in embryonic saltwater crocodiles. Am. J. Physiol. -Regul. Integr. Comp. Physiol. 283 (2002) R1155-R1163
Shepherdley C.A., Richardson S.J., Evans B.K., Kuhn E.R., and Darras V.M. Thyroid hormone deiodinases during embryonic development of the saltwater crocodile (Crocodylus porosus). Gen. Comp. Endocrinol. 126 (2002) 153-164
Silbergeld E.K. Lead in bone-implications for toxicology during pregnancy and lactation. Environ. Health Perspect. 91 (1991) 63-70
Southwood A.L., Andrews R.D., Paladino F.V., and Jones D.R. Effects of diving and swimming behavior on body temperatures of Pacific leatherback turtles in tropical seas. Physiol. Biochem. Zool. 78 (2005) 285-297
Spotila J.R., Dunham A.E., Leslie A.J., Steyermark A.C., Plotkin P.T., and Paladino F.V. Worldwide population decline of Dermochelys coriacea: are leatherback turlte going to extinct?. Chelon. Conserv. Biol. 2 (1996) 209-222
StatSoft Inc., 2001. Data Analysis Software System, version 6, http://www.statsoft.com.
Sutija M., and Joss J.M.P. Thyroid hormone deiodinases revisited: insights from lungfish: a review. J. Comp. Physiol. B-Biochem. Syst. Environ. Physiol. 176 (2006) 87-92
Unrine J.M., Jackson B.P., Hopkins W.A., and Romanek C. Isolation and partial characterization of proteins involved in maternal transfer of selenium in the western fence lizard (Sceloporus occidentalis). Environ. Toxicol. Chem. 25 (2006) 1864-1867
Van de Vijver K.I., Hoff P.T., Das K., Van Dongen W., Esmans E.L., Siebert U., Bouquegneau J.M., Blust R., and De Coen W.M. Baseline study of perfluorochemicals in harbour porpoises (Phocoena phocoena) from Northern Europe. Mar. Pollut. Bull. 48 (2004) 992-997
Wallace B.P., Williams C.L., Paladino F.V., Morreale S.J., Lindstrom R.T., and Spotila J.R. Bioenergetics and diving activity of internesting leatherback turtles Dermochelys coriacea at Parque Nacional Marino las Baulas, Costa Rica. J. Exp. Biol. 208 (2005) 3873-3884
Wallace B.P., Sotherland P.R., Tomillo P.S., Bouchard S.S., Reina R.D., Spotila J.R., and Paladino F.V. Egg components, egg size, and hatchling size in leatherback turtles. Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 145 (2006) 524-532
Wallace B.P., Sotherland P.R., Tomillo P.S., Reina R.D., Spotila J.R., and Paladino F.V. Maternal investment in reproduction and its consequences in leatherback turtles. Oecologia 152 (2007) 37-47
Wilson C.M., and McNabb F.M.A. Maternal thyroid hormones in Japanese quail eggs and their influence on embryonic development. Gen. Comp. Endocrinol. 107 (1997) 153-165
Wolfe M.F., Schwarzbach S., and Sulaiman R.A. Effects of mercury on wildlife: a comprehensive review. Environ. Toxicol. Chem. 17 (1998) 146-160