Developmental ecology of the American horseshoe crab Limulus polyphemus

Current Zoology

Volumn 56, Issue 5, 2010, Pages 550-562

  Botton, Mark L ^a   Tankersley, Richard A ^b   Loveland, Robert E ^c  

^a FORDHAM UNIVERSITY   (United States)

^b Florida Institute of Technology   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Development; Embryo; Horseshoe crab; Larval dispersal; Limulus

Indexed keywords

LIMULUS; LIMULUS POLYPHEMUS; MEROSTOMATA; TRILOBITOMORPHA;

EID: 77958193134     PISSN: 16745507     EISSN: None     Source Type: Journal    
DOI: 10.1093/czoolo/56.5.550     Document Type: Article

References (103)

1. ASMFC, 1998. Interstate fishery management plan for horseshoe crab. Fishery Management Report No. 32. Washington, DC: Atlantic States Marine Fisheries Commission.
2. Bademan ML, 2009. Tolerance and physiological responses of larval and juvenile horseshoe crabs Limulus polyphemus to hypoxia and anoxia. MS Thesis, Florida Institute of Technology, Melbourne, Florida, 1-58.
3. Bannon GA, Brown GG, 1980. Vesicle involvement in the egg cortical reaction of the horseshoe crab Limulus polyphemus L. Develop. Biol. 76: 418-427.
4. Barlow RB, Powers MK, Howard H, Kass L, 1986. Migration of Limulus for mating: Relation to lunar phase, tide height, and sunlight. Biol Bull 171: 310-329.
5. Barnum SR, Clapper DL, Brown GG, 1985. Modifications of the fertilized egg surface following the cortical reaction in Limulus polyphemus L. as viewed with the scanning electron microscope. J. Morphol. 183: 185-198.
6. Botton ML, 2000. Toxicity of cadmium and mercury to horseshoe crab Limulus polyphemus embryos and larvae. Bull. Environ. Contamin. Toxicol. 64: 137-143.
7. Botton ML, 2009. The ecological importance of horseshoe crabs in estuarine and coastal communities: A review and speculative summary. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 45-63.
8. Botton ML, Johnson K, Helleby L, 1998a. Effects of copper and zinc on embryos and larvae of the horseshoe crab Limulus polyphemus. Arch. Environ. Contamin. Toxicol. 35: 25-32.
9. Botton ML, Hodge M, Gonzalez TI, 1998b. High tolerance to tributyltin in embryos and larvae of the horseshoe crab Limulus polyphemus. Estuaries 21: 340-346.
10. Botton ML, Itow T, 2009. The effects of water quality on horseshoe crab embryos and larvae. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 439-463.
11. Botton ML, Loveland RE, 1992. Body size, morphological constraints, and mated pair formation in four populations of horseshoe crabs Limulus polyphemus along a geographic cline. Mar. Biol. 112: 409-415.
12. Botton ML, Loveland RE, 2003. Abundance and dispersal potential of horseshoe crab Limulus polyphemus larvae in the Delaware estuary. Estuaries 26: 1472-1479.
13. Botton ML, Loveland RE, Jacobsen TR, 1988. Beach erosion and geochemical factors: Influence on spawning success of horseshoe crabs Limulus polyphemus in Delaware Bay. Mar. Biol. 99: 325-332.
14. Botton ML, Loveland RE, Jacobsen TR, 1992. Overwintering by trilobite larvae of the horseshoe crab Limulus polyphemus on a sandy beach of Delaware Bay (New Jersey, USA). Mar. Ecol. Prog. Ser. 88: 289-292.
15. 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: 605-616.
16. Botton ML, Loveland RE, Tiwari A, 2003a. Distribution, abundance, and survivorship of young of the year in a commercially exploited population of horseshoe crabs Limulus polyphemus. Mar. Ecol. Prog. Ser. 265: 175-184.
17. Botton ML, Harrington BA, Tsipoura N, Mizrahi DS, 2003b. Synchronies in migration: Shorebirds, horseshoe crabs, and Delaware Bay. In: Shuster CN Jr, Barlow RB, Brockmann HJ ed. The American Horseshoe Crab. Cambridge, Massachusetts: Harvard University Press, 6-32.
18. Botton ML, Pogorzelska M, Smoral L, Shehata A, Hamilton MG, 2006. Thermal biology of horseshoe crab embryos and larvae: A role for heat shock proteins. J. Exp. Mar. Biol. Ecol. 336: 65-73.
19. Brockmann HJ, 1990. Mating behavior of horseshoe crabs Limulus polyphemus. Behaviour 114: 206-220.
20. Brockmann HJ, 1996. Satellite male groups in horseshoe crabs Limulus polyphemus. Ethology 102: 1-21.
21. Brockmann HJ, 2003a. Nesting behavior: A shoreline phenomenon. In: Shuster CN Jr, Barlow RB, Brockmann HJ ed. The American Horseshoe Crab. Cambridge, Massachusetts: Harvard University Press, 33-49.
22. Brockmann HJ, 2003b. Male competition and satellite behavior. In: Shuster CN Jr, Barlow RB, Brockmann HJ ed. The American Horseshoe Crab. Cambridge, Massachusetts: Harvard University Press, 50-82.
23. Brockmann HJ, Colson T, Potts W, 1994. Sperm competition in horseshoe crabs Limulus polyphemus. Behav. Ecol. Sociobiol. 35: 153-160.
24. Brockmann HJ, Nguyen C, Potts W, 2000. Paternity in horseshoe crabs when spawning in multiple-male groups. Anim. Behav. 60: 837-849.
25. Brockmann HJ, Smith MD, 2009. Reproductive competition and sexual selection in horseshoe crabs. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 199-221.
26. Brown GG, 1976. Scanning electron microscopical and other observations of sperm fertilization redactions in Limulus polyphemus L. (Merostomata: Xiphosura) J. Cell Sci. 22: 547-562.
27. Brown GG, Barnum SR, 1983. Postfertilization changes in the horseshoe crab Limulus polyphemus L. Biol. Bull. 164: 163-175.
28. Brown GG, Clapper DL, 1980. Cortical reaction in inseminated eggs of the horseshoe crab Limulus polyphemus L. Develop. Biol. 76: 410-417.
29. Brown GG, Clapper DL, 1981. Procedures for maintaining adults, collecting gametes, and culturing embryos and juveniles of the horseshoe crab Limulus polyphemus L. In: Hinegardner R, Atz J, Fayet R ed. Laboratory Animal Management, Marine Invertebrates. Washington DC: National Academy Press, 268-290.
30. Brown GG, Knouse JR, 1973. Effects of sperm concentration, sperm aging and other variables on fertilization in the horseshoe crab Limulus polyphemus L. Biol. Bull. 144: 462-470
31. Brusca RC, Brusca GJ, 1990. Invertebrates. Sunderland, Massachusetts: Sinauer Associates.
32. Burger J, Dixon C, Shukla T, Tsipoura N, Jensen H et al., 2003. Metals in horseshoe crabs from Delaware Bay. Arch. Environ. Contamin. Toxicol. 44: 36-42.
33. Burton WH, Kelley FS, Franks EA, 2009. Distribution of juvenile horseshoe crabs in subtidal habitats of Delaware Bay using a suction- dredge sampling device. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 285-293.
34. Chabot CC, Kent J, Watson WH, 2004. Daily, circadian and tidal rhythms of locomotory activity in the horseshoe crab Limulus polyphemus. Biol. Bull. 207: 72-75.
35. Chabot CC, Betournay SH, Braley N, Watson WH, 2007. Circadian and circatidal rhythms of locomotion in the horseshoe crab Limulus polyphemus. J. Exp. Mar. Biol. Ecol. 345: 79-89.
36. Chabot CC, Skinner SJ, Watson WH, 2008. Locomotion rhythms expressed by the horseshoe crab Limulus polyphemus: 1. Synchronization by artificial tides. Biol. Bull 215: 34-45.
37. Chabot CC, Watson WH, 2010. Circatidal rhythms of locomotion in the American horseshoe crab Limulus polyphemus: Underlying mechanisms and cues that influence them. Curr. Zool. 56: 499-517.
38. Coursey Y, Ahmad N, McGee BM, Steimel N, Kimble M, 2003. Amoebocyte production begins at stage 18 during embryogenesis in Limulus polyphemus, the American horseshoe crab. Biol. Bull. 204: 21-27.
39. Duffy EE, Penn DJ, Botton ML, Brockmann HJ, Loveland RE, 2006. Eye and clasper damage influence male mating tactics in the horseshoe crab Limulus polyphemus. J. Ethol. 24: 67-74.
40. Ehlinger GS, Tankersley RA, 2003. Larval hatching in the horseshoe crab Limulus polyphemus: Facilitation by environmental cues. J. Exp. Mar. Biol. Ecol. 292: 199-212.
41. Ehlinger GS, Tankersley RA, 2004. Survival and development of horseshoe crab Limulus polyphemus embryos and larvae in hypersaline conditions. Biol. Bull. 206: 87-94.
42. Ehlinger GS, Tankersley RA, 2006. Endogenous rhythms and entrainment cues of larval activity in the horseshoe crab Limulus polyphemus. J. Exp. Mar. Biol. Ecol. 292337: 205-214.
43. Ehlinger GS, Tankersley RA, 2007. Reproductive ecology of the American horseshoe crab Limulus polyphemus in the Indian River Lagoon: An overview. Florida Scientist 70: 449-463.
44. Ehlinger GS, Tankersley RA, 2009. Ecology of horseshoe crabs in microtidal lagoons. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 149-162.
45. Ehlinger GS, Tankersley RA, Bush MB, 2003. Spatial and temporal patterns of spawning and larval hatching by the horseshoe crab Limulus polyphemus in a microtidal coastal lagoon. Estuaries 26: 631-640.
46. Fisher DC, 1984. The Xiphosurida: Archetypes of bradytely? In: Eldredge N, Stanley SM ed. Living Fossils. New York: Springer-Verlag, 196-213.
47. Forward RB Jr, Tankersley RA, 2001. Selective tidal stream transport of marine animals. Oceanogr. Mar. Biol. Ann. Rev. 39: 305-353.
48. Fraenkel G, 1960. Lethal high temperature for three marine invertebrates: Limulus polyphemus, Littorina littorea, and Pagurus longicarpus. Oikos 11: 171-182.
49. French KA, 1979. Laboratory culture of embryonic and juvenile Limulus. In: Cohen E ed. Biomedical Applications of the Horseshoe Crab (Limulidae). New York: Alan R. Liss, 61-71.
50. Gaines EF, Carmichael RH, Grady SP, Valiela I, 2002. Stable isotopic evidence for changing nutritional sources of juvenile horseshoe crabs. Biol. Bull. 203: 228-230.
51. Graham LJ, Botton ML, Hata D, Loveland RE, Murphy BR, 2009. Prosomal-width-to-weight relationships in American horseshoe crabs Limulus polyphemus: Examining conversion factors used to estimate landings. Fish. Bull. 107: 235-243.
52. Greene MP, Hamilton MG, Botton ML, accepted. Levels of heat shock proteins (HSP70 and HSP90) in horseshoe crab Limulus polyphemus embryos exposed to osmotic stress. Mar. Biol.
53. Hajeb P, Christianus A, Zadeh SS, Saad CR, 2009. Sperm attachment on the egg of Malaysian king crab Carcinoscorpius rotundicauda. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 237-247.
54. Hidu H, Haskin HH, 1971. Setting of the American oyster related to environmental factors and larval behavior. Proc. Nat. Shellfisheries Assoc. 61: 35-50.
55. Itow T, Loveland RE, Botton ML, 1998a. Developmental abnormalities in horseshoe crab embryos caused by heavy metals. Arch. Environ. Contamin. Toxicol. 35: 33-40.
56. Itow T, Igarashi T, Botton ML, Loveland RE, 1998b. Heavy metals inhibit limb regeneration in horseshoe crab larvae. Arch. Environ. Contamin. Toxicol. 35: 457-463.
57. Jackson NL, Smith DR, Nordstrom KF, 2008. Physical and chemical changes in the foreshore of an estuarine beach: Implications for viability and development of horseshoe crab Limulus polyphemus eggs. Mar. Ecol. Prog. Ser. 355: 209-218.
58. James-Pirri MJ, 2010. Seasonal movement of the American horseshoe crab Limulus polyphemus in a semi-enclosed bay on Cape Cod, Massachusetts (USA) as determined by acoustic telemetry. Curr. Zool. 56: 575-586.
59. Jegla TC, 1979. The Limulus bioassay for ecdysteriods. Biol. Bull. 156: 103-114.
60. Jegla TC, 1982. A review of the molting physiology of the trilobite larva of Limulus. In: Bonaventura J, Bonaventura C, Tesh S ed. Physiology and Biology of Horseshoe Crabs. New York: Alan R. Liss, 83-101.
61. Jegla TC, Costlow JD, 1982. Temperature and salinity effects on developmental and early posthatch stages of Limulus. In: Bonaventura J, Bonaventura C, Tesh S ed. Physiology and Biology of Horseshoe Crabs. New York: Alan R. Liss, 103-113.
62. King TL, Eackles MS, Spidle AP, Brockmann HJ, 2005. Regional differentiation and sex-biased dispersal among populations of the horseshoe crab Limulus polyphemus. Trans. Am. Fish. Soc. 134: 441-465.
63. Kingsley JS, 1892. The embryology of Limulus. J. Morphol. 7: 35-66.
64. Kingsley JS, 1893. The embryology of Limulus. J. Morphol. 8: 195-268.
65. 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. Oxford: Pergammon Press, 182-191.
66. Leschen AS, Grady SP, Valiea I, 2006. Fecundity and spawning of the Atlantic horseshoe crab Limulus polyphemus in Pleasant Bay, Cape Cod, Massachusetts, USA. Mar. Ecol. 27: 54-65.
67. Loveland RE, Botton ML, 1992. Size dimorphism and the mating system in horseshoe crabs (Limulus polyphemus L.). Anim. Behav. 44: 907-916.
68. Laughlin R, 1983. The effects of temperature and salinity on larval growth of the horseshoe crab Limulus polyphemus. Biol. Bull. 164: 93-103.
69. Makioka T, 1988. Internal morphology. In: Sekiguchi K ed. Biology of Horseshoe Crabs. Tokyo, Japan: Science House Co Ltd, 104-132.
70. Mizrahi DS, Peters KA, 2009. Relationships between sandpipers and horseshoe crab in Delaware Bay: A synthesis. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 65-87.
71. Moore S, Perrin S, 2007. Seasonal movement and resource-use patterns of resident horseshoe crab Limulus polyphemus populations in a Maine, USA estuary. Est. Coasts 30: 1016-1026.
72. Munson JP, 1898. The ovarian egg of Limulus. J. Morphol. 15: 111-207.
73. 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 ed. Physiological Responses of Marine Biota to Pollutants. New York: Academic Press, 21-35.
74. Packard AS, 1870. The embryology of Limulus polyphemus. Am. Nat. 4: 498-502.
75. Packard AS, 1885. On the embryology of Limulus polyphemus. III. Am. Nat. 19: 722-727.
76. Palumbi SR, Johnson BA, 1982. A note on the influence of life history stage on metabolic adaptation: The responses of Limulus eggs and larvae to hypoxia. In: Bonaventura J, Bonaventura C, Tesh S ed. Physiology and Biology of Horseshoe Crabs. New York: Alan R. Liss, 115-124.
77. Penn D, Brockmann HJ, 1994. Nest-site selection in the horseshoe crab Limulus polyphemus. Biol. Bull. 187: 373-84.
78. Pooler PS, Smith DR, Loveland RE, Botton ML, Michels SF, 2003. Assessment of sampling methods to estimate horseshoe crab Limulus polyphemus egg density in Delaware Bay. Fish. Bull. 101: 698-703.
79. Reynolds WW, Casterlin ME, 1979. Themoregulatory behavior and diel activity of Limulus polyphemus. In: Cohen E ed. Biomedical Applications of the Horseshoe Crab (Limulidae). New York: Alan R. Liss, 47-59.
80. Rudkin DM,Young GA, 2009. Horseshoe crabs: An ancient ancestry revealed. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 25-44.
81. Rudloe A, 1979. Locomotor and light responses of larvae of the horseshoe crab Limulus polyphemus (L.). Biol. Bull. 157: 494-505.
82. Rudloe A, 1980. The breeding behavior and patterns of movement of horseshoe crabs Limulus polyphemus in the vicinity of breeding beaches in Apalachee Bay, Florida. Estuaries 3: 177-183.
83. Rudloe A, 1981. Aspects of the biology of juvenile horseshoe crabs Limulus polyphemus. Bull. Mar. Sci. 31: 125-133.
84. Schaller SY, Watson WH III, Chabot CC, 2010. Seasonal movements of horseshoe crabs Limulus polyphemus in the Great Bay Estuary, New Hampshire (USA). Curr. Zool. 56: 587-598
85. Sekiguchi K, 1988. Biology of Horseshoe Crabs. Tokyo, Japan: Science House Co Ltd.
86. Sekiguchi K, Yamamichi Y, Seshimo H, Sugita H, 1988a. Normal development. In: Sekiguchi K ed. Biology of Horseshoe Crabs. Tokyo, Japan: Science House Co Ltd, 133-224.
87. Sekiguchi K, Seshimo H, Sugita H, 1988b. Post-embryonic development of the horseshoe crab. Biol. Bull. 174: 337-345.
88. Shuster CN Jr, 1979. Distribution of the American horseshoe "crab," Limulus polyphemus (L.). In: Cohen E ed. Biomedical Applications of the Horseshoe Crab (Limulidae). New York: Alan R. Liss, 3-26.
89. Shuster CN Jr, 1982. A pictorial review of the natural history and ecology of the horseshoe crab Limulus polyphemus, with reference to other Limulidae. In: Bonaventura J, Bonaventura C, Tesh S ed. Physiology and Biology of Horseshoe Crabs. New York: Alan R. Liss, 1-52.
90. Shuster CN Jr, Botton ML, 1985. A contribution to the population biology of horseshoe crabs Limulus polyphemus in Delaware Bay. Estuaries 8: 363-372.
91. Shuster CN Jr, Anderson LI, 2003. A history of skeletal structure: Clues to relationships among species. In: Shuster CN Jr, Barlow RB, Brockman HJ ed. The American Horseshoe Crab. Cambridge, Massachusetts: Harvard University Press, 54-188.
92. Shuster CN Jr, Sekiguchi K, 2003. Growing up takes about ten years and eighteen stages. In: Shuster CN Jr, Barlow RB, Brockmann HJ ed. The American horseshoe crab. Cambridge. Harvard University Press, 103-133.
93. Smith DR, 2007. Effect of horseshoe crab spawning density on nest disturbance and exhumation of eggs: A simulation study. Est. Coasts 30: 287-295.
94. Smith DR, Mandt MT, MacDonald PDM, 2009a. Proximate causes of sexual size dimorphism in horseshoe crabs Limulus polyphemus of the Delaware Bay. J. Shellfish Res. 28: 405-417.
95. Smith DR, Millard MJ, Carmichael RH, 2009b. Comparative status and assessment of Limulus polyphemus with emphasis on the New England and Delaware Bay populations. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 361-386.
96. Spraker H, Austin HM, 1997. Diel feeding periodicity of Atlantic silverside Menidia menidia in the York River, Chesapeake Bay, Virginia. J. Elisha Mitchell Sci. Soc. 113: 171-182.
97. Strobel CJ, Brenowitz AH, 1981. Effects of Bunker C oil on juvenile horseshoe crabs Limulus polyphemus. Estuaries 4: 157-159.
98. Sugita H, 1988. Environmental adaptations of embryos. In: Sekiguchi K ed. Biology of Horseshoe Crabs. Tokyo, Japan: Science House Co. Ltd, 195-224.
99. Towle DW, Henry RP, 2003. Coping with environmental changes: Physiological challenges. In: Shuster CN Jr, Barlow RB, Brockmann HJ ed. The American Horseshoe Crab. Cambridge, Massachusetts: Harvard University Press, 224-244.
100. Watson, WH, Bedford L, Chabot CC, 2008. Dissociation between circadian rhythms of visual sensitivity and circatidal rhythms of locomotion in the American horseshoe crab Limulus polyphemus. Biol. Bull. 215: 46-56.
101. Watson WH III, Chabot CC, 2010. High resolution tracking of horseshoe crab Limulus polyphemus movements in an estuary with a fixed array ultrasonic telemetry. Curr. Zool. 56: 599-610.
102. Weber RG, Carter DB, 2009. Distribution and development of Limulus egg clusters on intertidal beaches in Delaware Bay. In: Tanacredi JT, Botton ML, Smith DR ed. Biology and Conservation of Horseshoe Crabs. New York: Springer, 249-266.
103. Weis JS, Ma A, 1987. Effects of the pesticide diflubenzuron on larval horseshoe crabs Limulus polyphemus. Bull. Environ. Contamin. Toxicol. 39: 224-228.