Ecotoxicology

, Volume 26, Issue 1, pp 46–57 | Cite as

Maternal transfer of trace elements in the Atlantic horseshoe crab (Limulus polyphemus)

  • Aaron K. Bakker
  • Jessica Dutton
  • Matthew Sclafani
  • Nicholas Santangelo
Article

Abstract

The maternal transfer of trace elements is a process by which offspring may accumulate trace elements from their maternal parent. Although maternal transfer has been assessed in many vertebrates, there is little understanding of this process in invertebrate species. This study investigated the maternal transfer of 13 trace elements (Ag, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, and Zn) in Atlantic horseshoe crab (Limulus polyphemus) eggs and compared concentrations to those in adult leg and gill tissue. For the majority of individuals, all trace elements were transferred, with the exception of Cr, from the female to the eggs. The greatest concentrations on average transferred to egg tissue were Zn (140 µg/g), Cu (47.8 µg/g), and Fe (38.6 µg/g) for essential elements and As (10.9 µg/g) and Ag (1.23 µg/g) for nonessential elements. For elements that were maternally transferred, correlation analyses were run to assess if the concentration in the eggs were similar to that of adult tissue that is completely internalized (leg) or a boundary to the external environment (gill). Positive correlations between egg and leg tissue were found for As, Hg, Se, Mn, Pb, and Ni. Mercury, Mn, Ni, and Se were the only elements correlated between egg and gill tissue. Although, many trace elements were in low concentration in the eggs, we speculate that the higher transfer of essential elements is related to their potential benefit during early development versus nonessential trace elements, which are known to be toxic. We conclude that maternal transfer as a source of trace elements to horseshoe crabs should not be overlooked and warrants further investigation.

Keywords

Maternal transfer Atlantic horseshoe crab Limulus polyphemus Trace elements Tissue distribution 

References

  1. 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 feathers and eggs. Environ Toxicol Chem 24:2107–2120. doi:10.1897/04-617R.1 CrossRefGoogle Scholar
  2. Atlantic States Marine Fisheries Commission (ASMFC) (1998) Interstate fishery management plan for horseshoe crab. Atlantic States Marine Fisheries Commission, Washington, DC, Fishery Management Report No. 32Google Scholar
  3. Atlantic States Marine Fisheries Commission (ASMFC) (2013) 2013 Horseshoe Crab Stock Assessment Update. ASMFC, Washington, DCGoogle Scholar
  4. Bang A, Grønkjær P, Lorenzen B (2008) The relation between concentrations of ovarian trace elements and the body size of Atlantic cod Gadus morhua. ICES J Mar Sci 65:1191–1197. doi:10.1093/icesjms/fsn094 CrossRefGoogle Scholar
  5. Beene LC, Halluer J, Yoshinaga M, Hamdi M, Liu Z (2011) Pentavalent arsenate transport by zebrafish phosphate transporter NaPi-IIb1. Zebrafish 8:125–131. doi:10.1089/zeb.2011.0701 CrossRefGoogle Scholar
  6. Bergeron CM, Bodinof CM, Unrine JM, Hopkins WA (2010) Bioaccumulation and maternal transfer of mercury and selenium in amphibians. Environ Toxicol Chem 29:989–997. doi:10.1002/etc.125 CrossRefGoogle Scholar
  7. Berkson J, Shuster Jr CN (1999) The horseshoe crab: the battle for a true multiple-use resource. Fisheries 24:6–10. doi:10.1577/1548-8446(1999)024<0006:THCTBF>2.0.CO;2CrossRefGoogle Scholar
  8. Botton ML, Johnson K, Helleby L (1998) Effects of copper and zinc on embryos and larvae of the horseshoe crab, Limulus polyphemus. Arch Environ Contam Toxicol 64:25–32. doi:10.1007/s002449900344 Google Scholar
  9. Botton ML (2000) Toxicity of cadmium and mercury to horseshoe crab (Limulus polyphemus), embryos and larvae. Bull Environ Contam Toxicol 64:137–143. doi:10.1007/s001289910021 CrossRefGoogle Scholar
  10. Bryan Jr AL, Hopkins WA, Baionno JA, Jackson BP (2003) Maternal transfer of contaminants to eggs in common grackles (Quiscalus quiscala) nesting on coal fly ash basins. Arch Environ Contam Toxicol 45:273–277. doi:10.1007/s00244-002-0212-9 CrossRefGoogle Scholar
  11. Burger J, Gochfeld M (1991) Cadmium and lead in common terns (Aves: Sterna hirundo): relationship between levels in parents and eggs. Environ Monit Assess 16:253–258. doi:10.1016/0016-2361(95)93464-O CrossRefGoogle Scholar
  12. Burger J (1997) Heavy metals in the eggs and muscle of horseshoe crabs (Limulus polyphemus) from Delaware Bay. Environ Monit Assess 46:279–287. doi:10.1023/A:1005718419708 CrossRefGoogle Scholar
  13. Burger J, Dixon C, Shukla T, Tsipoura N, Gochfeld M (2002) Metal levels in horseshoe crabs (Limulus polyphemus) from Maine to Florida. Environ Res 90:227–236. doi:10.1016/S0013-9351(02)00027-0 CrossRefGoogle Scholar
  14. Burger J, Gochfeld M (2013) Selenium and mercury molar ratios in commercial fish from New Jersey and Illinois: variation within species and relevance to risk communication. Food Chem Toxicol 57:235–245. doi:10.1016/j.fct.2013.03.021 CrossRefGoogle Scholar
  15. Burger J, Tsipoura N (2014) Metals in horseshoe crab eggs from Delaware Bay, USA: temporal patterns from 1993 to 2012. Environ Monit Assess 186:6947–6958. doi:10.1007/s10661-014-3901-8 CrossRefGoogle Scholar
  16. Chowdhury MJ, Bucking C, Wood CM (2008) Pre-exposure to waterborne nickel downregulates gastrointestinal nickel uptake in rainbow trout: indirect evidence for nickel essentiality. Environ Sci Technol 42:1359–1364. doi:10.1021/es071889n CrossRefGoogle Scholar
  17. Cochran JK, Hirschberg DJ, Wang J, Dere C (1998) Atmospheric deposition of metals to coastal waters (Long Island Sound, New York U.S.A.): evidence from Saltmarsh deposits. Estuarine Coastal Shelf Sci 46:503–522. doi:10.1006/ecss.1997.0299 CrossRefGoogle Scholar
  18. Conley JM, Funk DH, Buchwalter DB (2009) Selenium bioaccumulation and maternal transfer in the mayfly Centroptilum triangulifer in a life-cycle, periphyton-biofilm trophic assay. Environ Sci Technol 43:7952–7957. doi:10.1021/es9016377 CrossRefGoogle Scholar
  19. Drown DB, Oberg SG, Sharma RP (1986) Pulmonary clearance of soluble and insoluble forms of manganese. J Toxicol Environ Health 17:201–212. doi:10.1080/15287398609530816 CrossRefGoogle Scholar
  20. Duruibe JO, Ogwuegbu MOC, Egwurugwu JNE (2007) Heavy metal pollution and human biotoxic effects. Int J Phys Sci 2:112–118Google Scholar
  21. Franklin NM, Glover CN, Nicol JA, Wood CM (2005) Calcium/cadmium interactions at uptake surfaces in rainbow trout: waterborne versus dietary routes of exposure. Environ Toxicol Chem 24:2954–2964. doi:10.1897/05-007R.1 CrossRefGoogle Scholar
  22. 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. doi:10.1016/j.aquatox.2008.05.004 CrossRefGoogle Scholar
  23. Hammerschmidt CR, Wiener JG, Frazier BE, Rada RG (1999) Methylmercury content of eggs in yellow perch related to maternal exposure in four Wisconsin lakes. Environ Sci Technol 33:999–1003. doi:10.1021/es980948h CrossRefGoogle Scholar
  24. He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140. doi:10.1016/j.jtemb.2005.02.010 CrossRefGoogle Scholar
  25. Hopkins WA, DuRant SE, Staub BP, Rowe CL, Jackson BP (2006) Reproduction, embryonic development, and maternal transfer of contaminants in the amphibian Gastrophryne carolinensis. Environ Health Perspect 114:661–666. doi:10.1289/ehp.8457 CrossRefGoogle Scholar
  26. Hughes KD, Ewins PJ, Clark KE (1997) A comparison of mercury levels in feathers and eggs of osprey (Pandion haliaetus) in the North American Great Lakes. Arch Environ Contam Toxicol 33:441–452. doi:10.1007/s002449900275 CrossRefGoogle Scholar
  27. Itow T, Loveland RE, Botton ML (1998a) Developmental abnormalities in horseshoe crab embryos caused by exposure to heavy metals. Arch Environ Contam Toxicol 35:33–40. doi:10.1007/s002449900345 CrossRefGoogle Scholar
  28. Itow T, Igarashi T, Botton ML, Loveland RE (1998b) Heavy metals inhibit limb regeneration in horseshoe crab larvae. Arch Environ Contam Toxicol 35:457–463. doi:10.1007/s002449900402 CrossRefGoogle Scholar
  29. Iwanaga S, Lee B (2005) Recent advances in the innate immunity of invertebrate animals. BMB Rep 38:128–150. doi:10.5483/BMBRep.2005.38.2.128 CrossRefGoogle Scholar
  30. Johnston TA, Bodaly RA, Latif MA, Fudge RJP, Strange NE (2001) Intra-and interpopulation variability in maternal transfer of mercury to eggs of walleye (Stizostedion vitreum). Aquat Toxicol 52:73–85. doi:10.1016/S0166-445X(00)00129-6 CrossRefGoogle Scholar
  31. Kaneko JJ, Ralston NV (2007) Selenium and mercury in pelagic fish in the central north Pacific near Hawaii. Biol Trace Elem Res 119:242–254. doi:10.1007/s12011-007-8004-8 CrossRefGoogle Scholar
  32. Kannan K, Yasunaga Y, Iwata H, Ichihashi H, Tanabe S, Tatsukawa R (1995) Concentrations of heavy metals, organochlorines, and organotins in horseshoe crab, Tachypleus tridentatus, from Japanese coastal waters. Arch Environ Contam Toxicol 28:40–47. doi:10.1007/BF00213967 CrossRefGoogle Scholar
  33. Kelly BC, Ikonomou MG, MacPherson N, Sampson T, Patterson DA, Dubetz C (2011) Tissue residue concentrations of organohalogens and trace elements in adult Pacific salmon returning to the Fraser River, British Columbia, Canada. Environ Toxicol Chem 30:367–376. doi:10.1002/etc.410 CrossRefGoogle Scholar
  34. Kim JH, Gidbb JH, Howe PD (2006) Cobalt and inorganic cobalt compounds. World Health Organisation, Geneva, Swizterland, Concise International Chemical Assessment Document, Vol. 69Google Scholar
  35. King TL, Eackles MS, Spidle AP, Brockmann HJ (2005) Regional differentiation and sex-biased dispersal among populations of the horseshoe crab Limulus polyphemus. T Am Fish Soc 134:441–465. doi:10.1577/T04-023.1 CrossRefGoogle Scholar
  36. Kubota R, Kunito T, Tanabe S, Ogi H, Shibata Y (2002) Maternal transfer of arsenic to eggs of black-tailed gull (Larus crassirostris) from Rishiri Island. Japan Appl Organomet Chem 16:463–468. doi:10.1002/aoc.322 CrossRefGoogle Scholar
  37. Lavradas RT, Hauser-Davis RA, Lavandier RC, Rocha RCC, Saint’ Pierre TD, Seixas T, Kehrig HA, Moreira I (2014) Metal, metallothionein and glutathione levels in blue crab (Callinectes sp.) specimens from southeastern Brazil. Ecotoxicol Environ Saf 107:55–60. doi:10.1016/j.ecoenv.2014.04.013 CrossRefGoogle Scholar
  38. Loveland RE, Botton ML, Shuster Jr CN (1996) Life history of the American horseshoe crab (Limulus polyphemus L.) in Delaware Bay and its importance as a commercial resource. In Proceedings of the Horseshoe Crab Forum: status of the resource. University of Delaware Sea Grant College Program, Lewes, DelawareGoogle Scholar
  39. 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. doi:10.1139/cjfas-2013-0222 CrossRefGoogle Scholar
  40. Marco A, López-Vicente M, Pérez-Mellado V (2004) Arsenic uptake by reptile flexible-shelled eggs from contaminated nest substrates and toxic effect on embryos. Bull Environ Contam Toxicol 72:983–990. doi:10.1007/s00128-004-0340-1 CrossRefGoogle Scholar
  41. Maranho LA, Garrido-Pérez MC, Baena-Nogueras RM, Lara-Martín PA, Antón-Martín R, DelValls TA, Martín-Díaz ML (2015) Are WWTPs effluents responsible for acute toxicity? Seasonal variations of sediment quality at the Bay of Cádiz (SW, Spain). Ecotoxicology 24:368–380. doi:10.1007/s10646-014-1385-5 CrossRefGoogle Scholar
  42. Marsden ID, Rainbow PS, Smith BD (2003) Trace metal concentrations in two New Zealand talitrid amphipods: effects of gender and reproductive state and implications for biomonitoring. J Exp Mar Biol Ecol 290:93–113. doi:10.1016/S0022-0981(03)00072-8 CrossRefGoogle Scholar
  43. Metts BS, Buhlmann KA, Tuberville TD, Scott DE, Hopkins WA (2013) Maternal transfer of contaminants and reduced reproductive success of southern toads (Bufo [Anaxyrus] terrestris) exposed to coal combustion waste. Environ Sci Technol 47:2846–2853. doi:10.1021/es303989u CrossRefGoogle Scholar
  44. Mikkelsen T (1988) The secret in the blue blood. Science Press, Beijing, (No. 134)Google Scholar
  45. Muyssen BT, Brix KV, DeForest DK, Janssen CR (2004) Nickel essentiality and homeostasis in aquatic organisms. Environ Rev 12:113–131. doi:10.1139/a04-004 CrossRefGoogle Scholar
  46. Nichol H, Law JH, Winzerling JJ (2002) Iron metabolism in insects. Annu Rev Entomol 47:535–559. doi:10.1146/annurev.ento.47.091201.145237 CrossRefGoogle Scholar
  47. Neff JM (1997) Ecotoxicology of arsenic in the marine environment. Environ Toxicol Chem 16:917–927. doi:10.1002/etc.5620160511 Google Scholar
  48. Novitsky TJ (1984) Discovery to commercialization-the blood of the Horseshoe-crab. Oceanus 27:13–18Google Scholar
  49. O’Connor TP, Ehler CN (1991) Results from the NOAA national status and trends program on distribution and effects of chemical contamination in the coastal and estuarine United States. Environ Monit Assess 17:33–49. doi:10.1007/BF00402460 CrossRefGoogle Scholar
  50. Oshida PS, Word LS, Mearns AJ (1981) Effects of hexavalent and trivalent chromium on the reproduction of Neanthes arenaceodentata (Polychaeta). Mar Environ Res 5:41–49. doi:10.1016/0141-1136(81)90021-0 CrossRefGoogle Scholar
  51. Peterson SA, Ralston NV, Whanger PD, Oldfield JE, Mosher WD (2009) Selenium and mercury interactions with emphasis on fish tissue. Environ Bioindic 4:318–334. doi:10.1080/15555270903358428 CrossRefGoogle Scholar
  52. Querol X, Fernández-Turiel J, López-Soler A (1995) Trace elements in coal and their behaviour during combustion in a large power station. Fuel 74:331–343. doi:10.1016/0016-2361(95)93464-O CrossRefGoogle Scholar
  53. Rainbow PS (1985) The biology of heavy metals in the sea. Int J Environ Stud 25:195–211. doi:10.1080/00207238508710225 CrossRefGoogle Scholar
  54. Rainbow PS (1993) The significance of trace metal concentrations in marine invertebrates. In: Ecotoxicology of metals in invertebrates, 23Google Scholar
  55. Richards JG, Playle RC (1998) Cobalt binding to gills of rainbow trout (Oncorhynchus mykiss): an equilibrium model. Comp Biochem Physiol C Toxicol Pharmacol 119:185–197. doi:10.1016/S0742-8413(97)00206-5 Google Scholar
  56. Rogers JT, Wood CM (2004) Characterization of branchial lead-calcium interaction in the freshwater rainbow trout Oncorhynchus mykiss. J Exp Biol 207:813–825. doi:10.1242/jeb.00826 CrossRefGoogle Scholar
  57. Sanders JG, Windom HL (1980) The uptake and reduction of arsenic species by marine algae. J Estuar Coast Mar Sci 10:555–567. doi:10.1016/S0302-3524(80)80075-2 CrossRefGoogle Scholar
  58. Saxton HJ, Goodman JR, Collins JN, Black FJ (2013) Maternal transfer of inorganic mercury and methylmercury in aquatic and terrestrial arthropods. Environ Toxicol Chem 32:2630–2636. doi:10.1002/etc.2350 Google Scholar
  59. Singh N, Turner A (2009) Trace metals in antifouling paint particles and their heterogeneous contamination of coastal sediments. Marine Poll Bull 58:559–564. doi:10.1016/j.marpolbul.2008.11.014 CrossRefGoogle Scholar
  60. Srijaya TC, Pradeep PJ, Shaharom F, Chatterji A (2012) A study on the energy source in the developing embryo of the mangrove horseshoe crab, Carcinoscorpius rotundicauda (Latreille). Invertebr Reprod Dev 56:305–314. doi:10.1080/07924259.2011.633621 CrossRefGoogle Scholar
  61. Smith DR, Brousseau LJ, Mandt MT, Millard MJ (2010) Age and sex specific timing, frequency, and spatial distribution of horseshoe crab spawning in Delaware Bay: insights from a large-scale radio telemetry array. Curr Zool 56:563–574Google Scholar
  62. Sugita H (1988) Environmental adaptations of embryos. In: Sekiguchi K (ed) Biology of horseshoe crabs. Science House, Tokyo, pp 195–224Google Scholar
  63. Torres DP, Cadore S, Raab A, Feldmann J, Krupp EM (2014) Evaluation of dietary exposure of crabs to inorganic mercury or methylmercury, with or without co-exposure to selenium. J Anal At Spectrom 29:1273–1281. doi:10.1039/C4JA00072B CrossRefGoogle Scholar
  64. Walls EA, Berkson J, Smith SA (2002) The horseshoe crab, Limulus polyphemus: 200 million years of existence, 100 years of study. Rev Fish Sci 10:39–73. doi:10.1039/C4JA00072B CrossRefGoogle Scholar
  65. Wang WX, Griscom SB, Fisher NS (1997) Bioavailability of Cr (III) and Cr (VI) to marine mussels from solute and particulate pathways. Environ Sci Technol 31:603–611. doi:10.1021/es960574x CrossRefGoogle Scholar
  66. Wang WX, Fisher NS (1999) Delineating metal accumulation pathways for marine invertebrates. Sci Total Environ 237:459–472. doi:10.1016/S0048-9697(99)00158-8 CrossRefGoogle Scholar
  67. Wourms JP, Demski LS (1993) The reproduction and development of sharks, skates, rays and ratfishes: introduction, history, overview, and future prospects. Environ Biol Fishes 38:7–21. doi:10.1007/978-94-017-3450-9_1 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Aaron K. Bakker
    • 1
  • Jessica Dutton
    • 2
    • 3
  • Matthew Sclafani
    • 4
  • Nicholas Santangelo
    • 1
  1. 1.Department of BiologyHofstra UniversityHempsteadUSA
  2. 2.Environmental Studies ProgramAdelphi UniversityGarden CityUSA
  3. 3.Department of BiologyTexas State UniversitySan MarcosUSA
  4. 4.Cornell University Cooperative ExtensionRiverheadUSA

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