Abstract
This study compared the concentration of essential (Co, Cr, Cu, Fe, Mn, Ni, Se, Zn) and nonessential (Ag, As, Cd, Hg, Pb) trace elements in the muscle tissue of a pregnant common thresher shark (Alopias vulpinus) to the concentration in the three embryos. With the exception of Ag, Cd, Cr, and Ni which were below the detection limit, all other elements accumulated in the embryo muscle tissue. The Se:Hg molar ratios in the embryos averaged 9.8, indicating that Se may have a protective role against Hg toxicity during this early life stage. Maternal transfer as a source of trace elements in sharks should not be overlooked and future studies need to focus on how reproductive strategy influences this process.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams DH, McMichael RH (1999) Mercury levels in four species of sharks from the Atlantic coast of Florida. Fish Bull 97:372–379
Bakker AK, Dutton J, Sclafani M, Santangelo N (2017) Maternal transfer of trace elements in the Atlantic horseshoe crab (Limulus polyphemus). Ecotoxicology 26:46–57. https://doi.org/10.1007/s10646-016-1739-2
Branco V, Vale C, Canário J, dos Santos MN (2007) Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environ Poll 150:373–380. https://doi.org/10.1016/j.envpol.2007.01.040
Castro JI (2011) The sharks of North America. Oxford University Press, New York
Cazan AM, Klerks PL (2014) Evidence of maternal copper and cadmium transfer in two live-bearing fish species. Ecotoxicology 23:1774–1783. https://doi.org/10.1007/s10646-014-1342-3
Clarkson TW (1993) Molecular and ionic mimicry of toxic metals. Annu Rev Pharmacol Toxicol 32:545–571
Dutton J, Fisher NS (2011) Bioaccumulation of As, Cd, Cr, Hg(II), and MeHg in killifish (Fundulus heteroclitus) from amphipod and worm prey. Sci Total Environ 409:3438–3447. https://doi.org/10.1016/j.scitotenv.2011.05.022
Dutton J, Fisher NS (2014) Modeling metal bioaccumulation and tissue distribution in killifish (Fundulus heteroclitus) in three contaminated estuaries. Environ Toxicol Chem 33(1):89–101. https://doi.org/10.1002/etc.2392.
Endo T, Kimura O, Ohta C, Koga N, Kato Y, Fujii Y, Haraguchi K (2016) Metal concentrations in the liver and stable isotope ratios of carbon and nitrogen in the muscle of silvertip shark (Carcharhinus albimarginatus) culled off Ishigaki Island, Japan: changes with growth. PLoS ONE 11(2):e0147797. https://doi.org/10.1371/journal.pone.0147797
Frías-Espericueta MG, Cardenas-Nava NG, Márquez-Farías JF, Osuna-López JI, Muy-Rangel MD, Rubio-Carrasco W, Voltolina D (2014) Cadmium, copper, lead and zinc concentrations in female and embryonic Pacific sharpnose shark (Rhizoprionodon longurio) tissues. Bull Environ Contam Toxicol 93:532–535. https://doi.org/10.1007/s00128-014-1360-0
Frías-Espericueta MG, Zamora-Sarabia FKG, Márquez-Farías JF, Osuna-López JI, Ruelas-Inzunza J, Voltolina D (2015) Total mercury in female Pacific sharpnose sharks Rhizoprionodon longurio and their embryos. Lat Am J Aquat Res 43(3):534–538
Gervelis BJ, Natanson LJ (2013) Age and growth of the common thresher shark in the western North Atlantic Ocean. Trans Am Fish Soc 142:1535–1545. https://doi.org/10.1080/00028487.2013.815658
Guirlet E, Das K, Girondot M (2008) Maternal transfer of trace elements in leatherback turtles (Dermochelys coriacea) of French Guiana. Aquat Toxicol 88:267–276. https://doi.org/10.1016/j.aquatox.2008.05.004
Kaneko JJ, Ralston NVC (2007) Selenium and mercury in pelagic fish in the central North Pacific near Hawaii. Biol Trace Elem Res 119:242–254. https://doi.org/10.1007/s12011-007-8004-8
Kleiven M, Rosseland BO, Teien HC, Joner EJ, Oughton DH (2018) Route of exposure has a major impact on uptake of silver nanoparticles in Atlantic salmon (Salmo salar). Environ Tox Chem 37(11):2895–2903. https://doi.org/10.1002/etc.4251
Lahaye V, Bustamante P, Dabin W, Churland C, Caurant F (2007) Trace elements levels in foetus-mother pairs of short-beaked common dolphins (Delphinus delphis) stranded along the French coasts. Environ Int 33:1021–1028. https://doi.org/10.1016/j.envint.2007.05.008
Lyons K, Adams DH (2015) Maternal offloading of organochlorine contaminants in the yolk-sac placental scalloped hammerhead shark (Sphyrna lewini). Ecotoxicology 24:553–562. https://doi.org/10.1007/s10646-014-1403-7
Lyons K, Lowe CG (2013) Mechanisms of maternal transfer of organochlorine contaminants and mercury in the common thresher shark (Alopias vulpinus). Can J Fish Aquat Sci 70:1667–1672. https://doi.org/10.1139/cjfas-2013-0222
Lyons K, Carlisle A, Preti A, Mull C, Blasius M, O’Sullivan J, Winkler C, Lowe CG (2013) Effects of trophic ecology and habitat use on maternal transfer of contaminants in four species of young of the year lamniform sharks. Mar Environ Res 90:27–38. https://doi.org/10.1016/j.marenvres.2013.05.009
Mull CG, Lyons K, Blasius ME, Winkler C, O’Sullivan JB, Lowe CG (2013) Evidence of maternal offloading of organic contaminants in white sharks (Carcharodon carcharias). PLoS ONE 8(4):e62886. https://doi.org/10.1371/journal.pone.0062886
Natanson LJ, Gervelis BJ (2013) The reproductive biology of the common thresher shark in the western North Atlantic Ocean. Trans Am Fish Soc 142:1546–1562. https://doi.org/10.1080/00028487.2013.811099
Olin JA, Beaudry M, Fisk AT, Paterson G (2014) Age-related polychlorinated biphenyl dynamics in immature bull sharks (Carcharhinus leucas). Environ Toxicol Chem 33(1):35–43. https://doi.org/10.1002/etc.2402
Palaniappan PLRM, Karthikeyan S (2009) Bioaccumulation and depuration of chromium in the selected organs and whole body tissues of freshwater fish Cirrhinus mrigala individually and in binary solutions with nickel. J Environ Sci 21:229–236. https://doi.org/10.1016/S1001-0742(08)62256-1
Pane EF, Bucking C, Patel M, Wood CM (2005) Renal function in the freshwater rainbow trout (Oncorhynchus mykiss) following acute and prolonged exposure to waterborne nickel. Aquat Toxicol 72:119–133. https://doi.org/10.1016/j.aquatox.2004.11.020
Ralston NVC, Raymond LJ (2010) Dietary selenium’s protective effects against methylmercury toxicity. Toxicology 278:112–123. https://doi.org/10.1016/j.tox.2010.06.004
Rossouw GJ (1987) Function of the liver and hepatic lipids of the lesser sand shark, Rhinobatos annulatus (Műller and Henle). Comp Biochem Physiol B 86(4):785–790. https://doi.org/10.1016/0305-0491(87)90225-2
Ruelas-Inzunza J, Šlejkovec Z, Mazej D, Fajon V, Horvat M, Ramos-Osuna M (2018) Bioaccumulation of As, Hg, and Se in tunas Thunnus albacares and Katsuwonus pelamis from the eastern Pacific: tissue distribution and As speciation. Environ Sci Poll Res 25:19499–19509. https://doi.org/10.1007/s11356-018-2166-0
Terrazas-López R, Arreola-Mendoza L, Galván-Magaña F, Anguiano-Zamora M, Sujitha SB, Jonathan MP (2016) Cadmium concentration in liver and muscle of silky shark (Carcharhinus falciformis) in the tip of Baja California Sur. México. Mar Poll Bull 107(1):389–392. https://doi.org/10.1016/j.marpolbul.2016.03.035
van Hees KE, Ebert DA (2017) An evaluation of mercury offloading in two Central California elasmobranchs. Sci Total Environ 590–591:154–162. https://doi.org/10.1016/j.scitotenv.2017.02.191
Weijs L, Briels N, Adams DH, Lepoint G, Das K, Blust R (2015) Maternal transfer of organohalogenated compounds in sharks and stingrays. Mar Poll Bull 92:59–68. https://doi.org/10.1016/j.marpolbul.2014.12.056
Wood CM, Farrell AP, Brauner CJ (2012a) Fish physiology: homeostatis and toxicology of essential metals, vol 31A. Academic Press, New York
Wood CM, Farrell AP, Brauner CJ (2012b) Fish physiology: homeostatis and toxicology of non-essential metals, vol 31B. Academic Press, New York
Acknowledgements
We thank B. Jackson for the ICP-MS analysis and two anonymous reviewers whose thoughtful comments improved this manuscript. This study was funded by the Adelphi University Frederick Bettelheim Research Award to J. Dutton.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dutton, J., Venuti, V.M. Comparison of Maternal and Embryonic Trace Element Concentrations in Common Thresher Shark (Alopias vulpinus) Muscle Tissue. Bull Environ Contam Toxicol 103, 380–384 (2019). https://doi.org/10.1007/s00128-019-02667-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-019-02667-1