[en] Northern elephant seal (Mirounga angustirostris) pups undergo a substantial intertissue reorganization of protein, minerals, and other cellular components during their postweaning development, which might entail the mobilization of associated contaminants. The authors investigated the changes in concentrations of 11 elements (Ca, Cd, Cr, Cu, Fe, Hg, Ni, Pb, Se, V, and Zn) in a longitudinal study on 22 northern elephant seal pups during the postweaning fast. Slight changes in most element concentrations were observed in blood throughout the fast. Circulating levels of Hg, Se, and Cu appeared less altered during the postweaning fast than during suckling (previously measured). Despite the considerable fat utilization, element concentrations in blubber remained stable throughout the fast (except Fe), which suggests that elements are mobilized from blubber as efficiently as lipids. As indicators of the placental transfer, concentrations in lanugo hair revealed the existence of maternal transfer and accumulation of all assayed trace elements during fetal development. In addition, the new pelage, rapidly produced after weaning, appeared to be an important elimination route for toxic metals like Hg, Cd, and Pb. The high mineral content detected in pup hair suggests that this species would be more exposed to trace elements than other phocids (except Cd and Pb). This statement needs nevertheless further monitoring and toxicological studies to determine better the exposition to trace elements and its potential impact on the northern elephant seal’s health.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Habran, Sarah ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie
Crocker, D
Debier, C
Das, Krishna ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanologie
Language :
English
Title :
How are trace elements mobilized during the post-weaning fast in northern elephant seals?
Le Boeuf BJ, Laws RM. 1994. Elephant seals: An introduction to the genus. In Le Boeuf BJ, Laws RM, eds, Elephant Seals: Population Ecology, Behavior, and Physiology. University of California Press, Berkeley, CA, USA, pp 1-26.
Crocker DE, Williams JD, Costa DP, Le Boeuf BJ. 2001. Maternal traits and reproductive effort in northern elephant seals. Ecology 82:3541-3555.
Kirby VL, Ortiz CL. 1994. Hormones and fuel regulation in fasting elephant seals. In Le Boeuf BJ, Laws RM, eds, Elephant Seals: Population Ecology, Behavior, and Physiology. University of California press, Berkeley, CA, USA, pp 374-386.
Noren DP, Crocker DE, Williams TM, Costa DP. 2003. Energy reserve utilization in northern elephant seal (Mirounga angustirostris) pups during the postweaning fast: Size does matter. J Comp Physiol B Biochem Syst Environ Physiol 173:443-454.
Reiter J, Stinson NL, Le Boeuf BJ. 1978. Northern elephant seal development: The transition from weaning to nutritional independence. Behav Ecol Sociobiol 3:337-367.
Worthy GAJ, Lavigne DM. 1987. Mass loss, metabolic rate, and energy utilization by harp and gray seal pups during the postweaning fast. Physiol Zool 60:352-364.
Rea LD, Costa DP. 1992. Changes in standard metabolism during long-term fasting in northern elephant seal pups (Mirounga angustirostris). Physiol Zool 65:97-111.
Debier C, Pomeroy PP, Dupont C, Joiris C, Comblin V, Le Boulenge E, Larondelle Y, Thome JP. 2003. Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar Ecol Prog Ser 247:237-248.
Debier C, Chalon C, Le Boeuf BJ, de Tillesse T, Larondelle Y, Thome JP. 2006. Mobilization of PCBs from blubber to blood in northern elephant seals (Mirounga angustirostris) during the post-weaning fast. Aquat Toxicol (Amst) 80:149-157.
Vanden Berghe M, Mat A, Arriola A, Polain S, Stekke V, Thomé J-P, Gaspart F, Pomeroy P, Larondelle Y, Debier C. 2010. Relationships between vitamin A and PCBs in grey seal mothers and pups during lactation. Environ Pollut 158:1570-1575.
Das K, Debacker V, Pillet S, Bouquegneau JM. 2003. Heavy metals in marine mammals. In Vos JG, Bossart GD, Fournier M, O'Shea TJ, eds, Toxicology of Marine Mammals. New Perspectives: Toxicology and the Environment. Taylor & Francis, London, UK, pp 135-167.
Das K, Siebert U, Gillet A, Dupont A, Di-Poï C, Fonfara S, Mazzucchelli G, De Pauw E, De Pauw-Gillet M-C. 2008. Mercury immune toxicity in harbour seals: Links to in vitro toxicity. Environ Health 7:1-17.
Habran S, Debier C, Crocker DE, Houser DS, Das K. 2011. Blood dynamics of mercury and selenium in northern elephant seals during the lactation period. Environ Pollut 159:2523-2529.
Miranda-Filho KC, Metcalfe TL, Metcalfe CD, Robaldo RB, Muelbert MMC, Colares EP, Martinez PE, Bianchini A. 2007. Residues of persistent organochlorine contaminants in southern elephant seals (Mirounga leonina) from Elephant Island, Antarctica. Environ Sci Technol 41:3829-3835.
Miranda-Filho KC, Metcalfe CD, Metcalfe TL, Muelbert MMC, Robaldo RB, Martinez PE, Colares EP, Bianchini A. 2009. Lactational transfer of PCBs and chlorinated pesticides in pups of southern elephant seals (Mirounga leonina) from Antarctica. Chemosphere 75:610-616.
OSPAR. 2010. Quality Status Report 2010. OSPAR Commission, London, UK.
Bryan CE, Christopher SJ, Balmer BC, Wells RS. 2007. Establishing baseline levels of trace elements in blood and skin of bottlenose dolphins in Sarasota Bay, Florida: Implications for non-invasive monitoring. Sci Total Environ 388:325-342.
Muyssen BTA, Brix KV, DeForest DK, Janssen CR. 2004. Nickel essentiality and homeostasis in aquatic organisms. Environ Rev 12:113-131.
Saeki K, Nakajima M, Noda K, Loughlin TR, Baba N, Kiyota M, Tatsukawa R, Calkins DG. 1999. Vanadium accumulation in pinnipeds. Arch Environ Contam Toxicol 36:81-86.
Pechova A, Pavlata L. 2007. Chromium as an essential nutrient: A review. Vet Med 52:1-18.
Wolfe MF, Schwarzbach S, Sulaiman RA. 1998. Effects of mercury on wildlife: A comprehensive review. Environ Toxicol Chem 17:146-160.
Arctic Monitoring and Assessment Programme. 2005. AMAP Assessment 2002: Heavy Metals in the Arctic. Oslo, Norway.
Godwin HA. 2001. The biological chemistry of lead. Curr Opin Chem Biol 5:223-227.
Chatt A, Katz SA. 1988. The biological basis for trace metals in hair. In Katz SA, Chatt A, eds, Hair Analysis: Applications in the Biomedical and Environmental Sciences. Wiley-VCH, New York, NY, USA.
Griesel S, Kakuschke A, Siebert U, Prange A. 2008. Trace element concentrations in blood of harbor seals (Phoca vitulina) from the Wadden Sea. Sci Total Environ 392:313-323.
Baraj B, Bianchini A, Niencheski LFH, Campos CCR, Martinez PE, Robaldo RB, Muelbert MMC, Colares EP, Zarzur S. 2001. The performance of Zeiss GFAAS-5 instrument on the determination of trace metals in whole blood samples of southern elephant seals (Mirounga leonina) from Antarctica. Fresenius Environ Bull 10:859-862.
Habran S, Pomeroy PP, Debier C, Das K. 2012. Changes in trace elements during lactation in a marine top predator, the grey seal. Aquat Toxicol (Amst), DOI: 10.1016/j.aquatox.2012.08.011.
Brookens TJ, Harvey JT, O'Hara TM. 2007. Trace element concentrations in the Pacific harbor seal (Phoca vitulina richardii) in central and northern California. Sci Total Environ 372:676-692.
Ancora S, Rossi R, Di Simplicio P, Lusini L, Leonzio C. 2002. In vitro study of methylmercury in blood of bottlenose dolphin (Tursiops truncatus). Arch Environ Contam Toxicol 42:348-353.
Berglund M, Lind B, Björnberg KA, Palm B, Einarsson Ö, Vahter M. 2005. Inter-individual variations of human mercury exposure biomarkers: A cross-sectional assessment. Environ Health 4:1-20.
Gurzau ES, Neagu C, Gurzau AE. 2003. Essential metals-Case study on iron. Ecotoxicol Environ Saf 56:190-200.
Lewis M, Campagna C, Uhart M, Ortiz CL. 2001. Ontogenetic and seasonal variation in blood parameters in southern elephant seals. Mar Mamm Sci 17:862-872.
Noren SR, Iverson SJ, Boness DJ. 2005. Development of the blood and muscle oxygen stores in gray seals (Halichoerus grypus): Implications for juvenile diving capacity and the necessity of a terrestrial postweaning fast. Physiol Biochem Zool 78:482-490.
Thorson PH, Le Boeuf BJ. 1994. Developmental aspects of diving in northern elephant seal pups. In Le Boeuf BJ, Laws RM, eds, Elephant Seals: Population Ecology, Behavior, and Physiology. University of California Press, Berkeley, CA, USA, pp 271-289.
Strandberg U, Kakela A, Lydersen C, Kovacs KM, Grahl-Nielsen O, Hyvarinen H, Kakela R. 2008. Stratification, composition, and function of marine mammal blubber: The ecology of fatty acids in marine mammals. Physiol Biochem Zool 81:473-485.
Dunkin RC, McLellan WA, Blum JE, Pabst DA. 2005. The ontogenetic changes in the thermal properties of blubber from Atlantic bottlenose dolphin Tursiops truncatus. J Exp Biol 208:1469-1480.
Henderson RJ, Kalogeropoulos N, Alexis MN. 1994. The lipid composition of selected tissues from a Mediterranean monk seal, Monachus monachus. Lipids 29:577-582.
Mellish JAE, Iverson SJ, Bowen WD. 1999. Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol Biochem Zool 72:677-690.
Agusa T, Yasugi S, Iida A, Ikemoto T, Anan Y, Kuiken T, Osterhaus ADME, Tanabe S, Iwata H. 2011. Accumulation features of trace elements in mass-stranded harbor seals (Phoca vitulina) in the North Sea coast in 2002: The body distribution and association with growth and nutrition status. Mar Pollut Bull 62:963-975.
Yamamoto Y, Honda K, Hidaka H, Tatsukawa R. 1987. Tissue distribution of heavy metals in Weddell seals (Leptonychotes weddellii). Mar Pollut Bull 18:164-169.
Medvedev N, Panichev N, Hyvärinen H. 1997. Levels of heavy metals in seals of Lake Ladoga and the White Sea. Sci Total Environ 206:95-105.
Wenzel C, Adelung D, Kruse H, Wassermann O. 1993. Trace metal accumulation in hair and skin of the harbour seal, Phoca vitulina. Mar Pollut Bull 26:152-155.
Ikemoto T, Kunito T, Watanabe I, Yasunaga G, Baba N, Miyazaki N, Petrov EA, Tanabe S. 2004. Comparison of trace element accumulation in Baikal seals (Pusa sibirica), Caspian seals (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ Pollut 127:83-97.
Gray R, Canfield P, Rogers T. 2008. Trace element analysis in the serum and hair of Antarctic leopard seal, Hydrurga leptonyx, and Weddell seal, Leptonychotes weddellii. Sci Total Environ 399:202-215.
Aubail A, Teilmann J, Dietz R, Riget F, Harkonen T, Karlsson O, Rosing-Asvid A, Caurant F. 2011. Investigation of mercury concentrations in fur of phocid seals using stable isotopes as tracers of trophic levels and geographical regions. Polar Biol 34:1411-1420.
Watanabe I, Tanabe S, Amano M, Miyazaki N, Petrov EA, Tatsukawa R. 1998. Age-dependent accumulation of heavy metals in Baikal seal (Phoca sibirica) from the Lake Baikal. Arch Environ Contam Toxicol 35:518-526.
Ling JK. 1984. Epidermal cycles and moulting in marine mammals. Acta Zool Fenn 171:23-26.
Eads EA, Lambdin CE. 1973. A survey of trace metals in human hair. Environ Res 6:247-252.
Wagemann R, Stewart REA, Lockhart WL, Stewart BE, Povoledo M. 1988. Trace metals and methyl mercury: Associations and transfer in harp seal (Phoca groenlandica) mothers and their pups. Mar Mamm Sci 4:339-355.
Ask K, Akesson A, Berglund M, Vahter M. 2002. Inorganic mercury and methylmercury in placentas of Swedish women. Environ Health Perspect 110:523-526.
National Research Council. 2000. Toxicological Effects of Methylmercury. National Academy, Washington, DC, USA.
Andrade S, Carlini AR, Vodopivez C, Poljak S. 2007. Heavy metals in molted fur of the southern elephant seal Mirounga leonina. Mar Pollut Bull 54:602-605.
Le Boeuf BJ, Crocker DE, Costa DP, Blackwell SB, Webb PM, Houser DS. 2000. Foraging ecology of northern elephant seals. Ecol Monogr 70:353-382.
Simmons SE, Crocker DE, Kudela RM, Costa DP. 2007. Linking foraging behaviour of the northern elephant seal with oceanography and bathymetry at mesoscales. Mar Ecol Prog Ser 346:265-275.
Hyvärinen H, Sipilä T. 1984. Heavy metals and high pup mortality in the Saimaa ringed seal population in eastern Finland. Mar Pollut Bull 15:335-337.
Yediler A, Panou A, Schramel P. 1993. Heavy metals in hair samples of the Mediterranean monk seal (Monachus monachus). Mar Pollut Bull 26:156-159.
Agusa T, Nomura K, Kunito T, Anan A, Iwata H, Tanabe S. 2011. Accumulation of trace elements in harp seals (Phoca groenlandica) from Pangnirtung in the Baffin Island, Canada. Mar Pollut Bull 63:489-499.