The Effects of Water Quality on Horseshoe Crab Embryos and Larvae

  • Mark L. BottonEmail author
  • Tomio Itow


It is well established that horseshoe crab eggs can develop successfully across a wide range of temperatures and salinities. However, many estuaries in which horseshoe crabs spawn have been heavily impacted by pollutants, and degraded water quality may be affecting the survival of horseshoe crab eggs laid in such areas. Laboratory bioassays using Limulus polyphemus embryos and larvae have shown a very high tolerance to a variety of contaminants, including heavy metals, oil, and organic compounds, in comparison to similar stages in other marine arthropods. Of the metals tested, acute toxicity was highest for mercury and tributyltin (TBT), but much lower for cadmium, zinc, and copper. Possible mechanisms of pollution tolerance, including stress proteins (Hsps), are discussed. Sublethal levels of heavy metals (especially mercury and TBT) induced a variety of embryonic malformations and impaired regeneration of walking legs. The frequency of malformed L. polyphemus embryos was low (ca. 1%) both in relatively pristine habitats (lower Delaware Bay, NJ) and in urban estuaries (Sandy Hook Bay, NJ, and Jamaica Bay, NY). In contrast, a much higher percentage of malformed Tachypleus tridentatus embryos have been found from several locations in Japan, and severely polluted water may be hampering Japanese efforts to re-establish horseshoe crab populations. Pollutants accumulated by adult females may become incorporated into their eggs and could conceivably be passed up the food chain to egg predators.


Heavy Metal Horseshoe Crab Laboratory Bioassay Instar Stage Delaware Estuary 
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  1. Albert RC (1988) The historical context of water quality management for the Delaware estuary. Estuaries 11:99–107CrossRefGoogle Scholar
  2. Amiard J-C, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic organisms: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202PubMedCrossRefGoogle Scholar
  3. ASMFC (Atlantic States Marine Fisheries Commission) (1998) Interstate fishery management plan for horseshoe crab. Fish Manage Rep 32:1–39Google Scholar
  4. Avissar NG (2006) Modeling potential impacts of beach replenishment on horseshoe crab nesting habitat suitability. Coast Manage 34:427–441CrossRefGoogle Scholar
  5. Baker AJ, González PM, Piersma T, Niles LJ, de Lima do Nascimento I, Atkinson PW, Clark NA., Minton CDT, Peck MK, Aarts G (2004) Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay. Proc Biol Sci 271:875–882PubMedCrossRefGoogle Scholar
  6. Berkson J, Shuster CN Jr (1999) The horseshoe crab: the battle for a true multiple-use resource. Fisheries 24:6–12CrossRefGoogle Scholar
  7. Boman J, Wagner A, Brauer H, Binh DV (2001) Trace elements in tissues from Vietnamese animals. X-Ray Spectrometry 30:388–392CrossRefGoogle Scholar
  8. Botton ML (2000) Toxicity of cadmium and mercury to horseshoe crab (Limulus polyphemus) embryos and larvae. Bull Environ Contam Toxicol 64:137–143PubMedCrossRefGoogle Scholar
  9. Botton ML (2001) The conservation of horseshoe crabs: What can we learn from the Japanese experience? In Tanacredi JT (ed) Limulus in the Limelight. Kluwer Academic/Plenum, New York, pp 41–51Google Scholar
  10. Botton ML, Loveland RE, Jacobsen TR (1994) Site selection by migratory shorebirds in Delaware Bay, and its relationship to beach characteristics and abundance of horseshoe crab (Limulus polyphemus) eggs. Auk 111:605–616Google Scholar
  11. Botton ML, Johnson K, Helleby L (1998a) Effects of copper and zinc on embryos and larvae of the horseshoe crab, Limulus polyphemus. Arch Environ Contam Toxicol 35:25–32PubMedCrossRefGoogle Scholar
  12. Botton ML, Hodge M, Gonzalez TI (1998b) High tolerance to tributyltin in embryos and larvae of the horseshoe crab, Limulus polyphemus. Estuaries 21:340–346CrossRefGoogle Scholar
  13. Botton, ML, Loveland RE, Tanacredi JT, Itow T (2006a) Horseshoe crabs (Limulus polyphemus) in an urban estuary (Jamaica Bay, New York), and the potential for ecological restoration. Est Coasts 29:820–830Google Scholar
  14. Botton ML, Pogorzelska, M, Smoral L, Shehata A, Hamilton MG (2006b) Thermal biology of horseshoe crab embryos and larvae: A role for heat shock proteins. J Exp Mar Biol Ecol 336:65–73CrossRefGoogle Scholar
  15. Brockmann HJ, Smith M (2009) Reproductive competition and sexual selection in horseshoe crabs. In: Tanacredi JT, Botton ML, Smith DR (eds) Biology and conservation of horseshoe crabs. Springer, New York, pp 199–221Google Scholar
  16. Burger J, Seyboldt S, Morganstein N, Clark K (1993) Heavy metals and selenium in feathers of three shorebird species from Delaware Bay. Environ Monit Assess 28:189–198CrossRefGoogle Scholar
  17. Burger J, Dixon C, Shukla T, Tsipoura N, Gochfeld M (2002) Metal levels in horseshoe crabs (Limulus polyphemus) from Maine to Florida. Environ Res 90:227–236PubMedCrossRefGoogle Scholar
  18. Burger J, Dixon C, Shukla T, Tsipoura N, Jensen H, Fitzgerald M, Ramos R, Gochfeld M (2003) Metals in horseshoe crabs from Delaware Bay. Arch Environ Contam Toxicol 44:36–42PubMedCrossRefGoogle Scholar
  19. Chatterji A, Kotnala S, Mathew R (2004) Effect of salinity on larval growth of horseshoe crab, Tachypleus gigas (Müller). Curr Sci 87:248–250Google Scholar
  20. Chen CP, Yeh HY, Lin PF (2004) Conservation of the horseshoe crab at Kinmen, Taiwan: strategies and practices. Biodivers Conserv 13:1889–1904CrossRefGoogle Scholar
  21. Chiu HMC, Morton B (2003) The status of horseshoe crabs in Hong Kong. In: Morton B (ed.) Perspectives on Marine Environment Change in Hong Kong and Southern China, 1977–2001. Hong Kong University Press, Hong Kong, pp 741–756Google Scholar
  22. Church TM, Tramonano JM, Scudlark JR, Murray SL (1988) Trace metals in the waters of the Delaware estuary. In: Majumdar SK, Miller EW, Sage LE (eds) Ecology and Restoration of the Delaware River Basin. Pennsylvania Academy of Science, p 93–115Google Scholar
  23. Ehlinger GS, Tankersley RA (2004) Survival and development of horseshoe crab (Limulus polyphemus) embryos and larvae in hypersaline conditions. Biol Bull 206:87–94PubMedCrossRefGoogle Scholar
  24. Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Ann Rev Physiol 61:243–282CrossRefGoogle Scholar
  25. George SG (1990) Biochemical and cytological assessments of metal toxicity in marine animals. In: Furness RW, Rainbow PS (eds) Heavy Metals in the Marine Environment. CRC Press, Boca Raton, pp 124–142Google Scholar
  26. Haramis GM, Link WA, Osenton PC, Carter DB, Weber RG, Clark NA, Teece MA, Mizrahi DS (2007). Stable isotope and pen feeding trial studies confirm value of horseshoe crab eggs to spring migrant shorebirds in Delaware Bay. J Avian Biol 38:367–376Google Scholar
  27. Itow T (1997) The pollution of coastal waters and malformations of horseshoe crab embryos. Bull Fac Educ Shizoka Univ Nat Sci 48:15–33Google Scholar
  28. Itow T, Loveland RE, Botton ML (1998a) Developmental abnormalities in horseshoe crab embryos caused by heavy metals. Arch Environ Contam Toxicol 35:33–40PubMedCrossRefGoogle Scholar
  29. Itow T, Igarashi T, Botton ML, Loveland RE (1998b) Heavy metals inhibit limb regeneration in horseshoe crab larvae. Arch Environ Contam Toxicol 35:457–463PubMedCrossRefGoogle Scholar
  30. Jegla TC, Costlow JD (1982) Temperature and salinity effects on development and early posthatch stages of Limulus. In: Bonaventura J, Bonaventura C, Tesh S (eds), Physiology and Biology of Horseshoe Crabs: Studies on Normal and Environmentally Stressed Animals. Alan R. Liss, New York, pp 103–113Google Scholar
  31. 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 28:40–47CrossRefGoogle Scholar
  32. Kungsuwan A, Noguchi T, Arakawa O, Simidu U, Tsukamoto K, Shida Y, Hashimoto K (1988) Tetrodotoxin-producing bacteria from the horseshoe crab Carcinoscorpius rotundicauda. Nippon Suisan Gakkaishi 54:1799–1802CrossRefGoogle Scholar
  33. Kungsuwan A, Nagashima Y, Noguchi T, Shida Y, Suvapeepan S, Suwansakornkul P, Hashimoto K (1987) Tetrodotoxin in the horseshoe crab Carcinoscorpius rotundicauda inhabiting Thailand. Nippon Suisan Gakkaishi 53:261–266CrossRefGoogle Scholar
  34. Laughlin R (1983) The effects of temperature and salinity on larval growth of the horseshoe crab Limulus polyphemus. Biol Bull 164:93–103CrossRefGoogle Scholar
  35. Laughlin RB Jr, Neff JM (1977) Interactive effects of temperature, salinity shock, and chronic exposure to no. 2 fuel oil on survival, development rate and respiration of the horseshoe crab, Limulus polyphemus. In: Wolff DA (ed) Fate and Effects of Petroleum Hydrocarbons in Marine Organisms and Ecosystems. Pergammon Press, Oxford, pp 182–191Google Scholar
  36. Lewis S, Handy RD, Cordi B, Billinghurst Z, Depledge MH (1999) Stress proteins (HSP’s): Methods of detection and their use as an environmental biomarker. Ecotoxicology 8:351–368CrossRefGoogle Scholar
  37. Mizrahi DS, Peters KA (2009) Relationships between sandpipers and horseshoe crab in Delaware Bay: A synthesis. In: Tanacredi JT, Botton ML, Smith DR (eds) Biology and Conservation of Horseshoe Crabs. Springer, New York, pp 65–87Google Scholar
  38. Morton B (1999) On turtles, dolphins and, now, Asia’s horseshoe crabs. Mar Poll Bull 38:845–846CrossRefGoogle Scholar
  39. Neff JM, Giam CS (1977) Effects of Arochlor 1016 and Halowax 1099 on juvenile horseshoe crabs (Limulus polyphemus). In: Vernberg, FJ, Calabrese A, Thurberg FP, Vernberg WB (eds) Physiological Responses of Marine Biota to Pollutants. Academic Press, New York, pp 21–35Google Scholar
  40. Ngy L, Yu C-F, Takatani T, Arakawa O (2007) Toxicity assessment for the horseshoe crab Carcinoscorpius rotundicauda collected from Cambodia. Toxicon 49:843–847PubMedCrossRefGoogle Scholar
  41. Riedel GF, Sanders JG (1998) Trace element speciation and behavior in the tidal Delaware river. Estuaries 21:78–90CrossRefGoogle Scholar
  42. Sekiguchi K (1988) Embryonic development. In: Sekiguchi, K (ed), Biology of Horseshoe Crabs. Science House, Tokyo, pp 145–181Google Scholar
  43. Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037CrossRefGoogle Scholar
  44. Sugita, H, 1988. Environmental adaptation of embryos. In: Sekiguchi, K (ed), Biology of Horseshoe Crabs. Science House, Tokyo, pp195–224Google Scholar
  45. Strobel CJ, Brenowitz AH (1981) Effects of Bunker C oil on juvenile horseshoe crabs (Limulus polyphemus). Estuaries 4:157–159CrossRefGoogle Scholar
  46. Tsipoura N, Burger J (1999) Shorebird diet during spring migration stopover on Delaware Bay. Condor 101:635–644CrossRefGoogle Scholar
  47. Tsuchiya K, Asano M (1989) The present condition and changes of egg-lay positions and breeding points in Kasaoka Bay. In: Sekiguchi K (ed.) The Present Condition of Japanese Horseshoe Crab. Kasaoka, Japan, pp 45–55Google Scholar
  48. Tsuge T, Washida T (2003) Economic valuation of the Seto Inland Sea by using an Internet CV survey. Mar Poll Bull 47:230–236CrossRefGoogle Scholar
  49. Venosa AD, Suidan MT, Wrenn BA, Strohmeier KL, Haines JR, Eberhart BL, King D, Holder E (1996) Bioremediation of an experimental oil spill on the shoreline of Delaware Bay. Environ Sci Technol 30:1764–1775CrossRefGoogle Scholar
  50. Viarengo A (1985) Biochemical effects of trace metals. Mar Poll Bull 16:153–158CrossRefGoogle Scholar
  51. Walls EA, Berkson J, Smith SA. (2002) The horseshoe crab, Limulus polyphemus: 200 million years of existence, 100 years of study. Rev Fish Sci 10:39–73CrossRefGoogle Scholar
  52. Weis JS, Ma A (1987) Effects of the pesticide diflubenzuron on larval horseshoe crabs, Limulus polyphemus. Bull Environ Contam Toxicol 39:224–228PubMedCrossRefGoogle Scholar
  53. White SL, Rainbow PS (1985) On the metabolic requirements for copper and zinc in molluscs and crustaceans. Mar Environ Res 16:215–229CrossRefGoogle Scholar
  54. Widener JW, Barlow RB Jr (1999) Decline of a horseshoe crab population on Cape Cod. Biol Bull 197:300–302PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Natural SciencesFordham College at Lincoln CenterNew YorkUSA
  2. 2.Department of Biology, Faculty of EducationShizuoka UniversityShizuokaJapan

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