, 266:1 | Cite as

Life cycles of nemerteans that are symbiotic egg predators of decapod Crustacea: adaptations to host life histories

  • Armand M. Kuris


Life cycles of five species of nemerteans that are symbiotic egg predators of decapod crustaceans are reviewed and compared. These life cycles range from the relatively simple life cycle of Carcinonemertes regicides from the red king crab, Paralithodes camtschatica, to the complex life cycle of C. errans on the Dungeness crab, Cancer magister. Increased complexity of these life cycles is evaluated as a series of adaptations to cope with life history features of their respective hosts. These host attributes include seasonal brooding, rapid embryogenesis and brooding in alternate years. Lengthy host brood periods permit autoinfection of the respective nemertean symbionts with resultant loss of many host eggs. Adaptations associated with short or intermittent brooding periods include migrations of regressing adult worms to the gills and their return to the egg mass at the next oviposition, transfer of worms from old to new cuticles at ecdysis, use of male and juvenile female crabs as hosts, and sexual transmission at host copulation. Future research needs are briefly discussed.

Key words

Carcinonemertes Pseudocarcinonemertes Nemertea life cycle egg predator adaptation Crustacea 


  1. Aiken, D. E. & S. L. Waddy, 1980. Maturity and reproduction in the American lobster. Can Tech. Rep. Fish. aquat. Sci. 932: 59–71.Google Scholar
  2. Aiken, D. E. & S. L. Waddy, 1986. Environmental influence on recruitment of the American lobster, Homarus americanus: a perspective. Can. J. Fish. aquat. Sci. 43: 2258–2270.Google Scholar
  3. Aiken, D. E., S. L. Waddy & L. S. Uhazy, 1985. Aspects of the biology of Pseudocarcinonemertes homari and its association with American lobster, Homarus americanus. Can. J. Fish. aquat. Sci. 42: 351–356.Google Scholar
  4. Bauman, L., 1983. The larval biology of Carcinonemertes. Master's Thesis, University of California, Santa Cruz, California.Google Scholar
  5. Blau, S. F., 1986. Recent declines of red king crab (Paralithodes camtschatica) populations and reproductive conditions around the Kodiak Archipelago, Alaska. Can. Spec. Publ. Fish. aquat. Sci. 92: 360–369.Google Scholar
  6. Botsford, L. W. & D. E. Wickham, 1978. Behavior of agespecific, density-dependent models and the northern California Dungeness crab (Cancer magister) fishery. J. Fish. Res. Bd Can. 35: 833–843.Google Scholar
  7. Brattey, J., A. Campbell, A. E. Bagnall & L. S. Uhazy, 1985. Geographic distribution and seasonal occurrence of the nemertean Pseudocarcinonemertes homari on the American lobster, Homarus americanus. Can. J. Fish. aquat. Sci. 42: 360–367.Google Scholar
  8. Brooks, W. K. & F. H. Herrick, 1892. The embryology and metamorphosis of the Macroura Mem. Nat. Acad. Sci. 5: 323–576.Google Scholar
  9. Butler, T. H., 1961. Growth and age determination of the Pacific edible crab Cancer magister Dana. J. Fish. Res. Bd Can. 18: 873–889.Google Scholar
  10. Campbell, A. & J. Brattey, 1986. Egg loss from the American lobster, Homarus americanus, in relation to nemertean, Pseudocarcinonemertes homari, infestation. Can. J. Fish. aquat. Sci. 43: 772–780.CrossRefGoogle Scholar
  11. Campbell, A., R. Gibson & L. H. Evans, 1989. A new species of Carcinonemertes (Nemertea: Carcinonemertidae) ectohabitat on Panulirus cygnus (Crustacea: Palinuridae) from Western Australia. Zool. 95: 257–268.Google Scholar
  12. Chang, E. S., 1989. Endocrine regulation of molting in Crustacea. CRC Critical Rev. aquat. Sci. 1: 131–157.Google Scholar
  13. Coe, W. R., 1902. Nemertean parasites of crabs. Am. Nat. 36: 431–450.CrossRefGoogle Scholar
  14. Comely, C. A. & A. D. Ansell, 1989. The incidence of Carcinonemertes carcinophila (Kölliker) on some decapod crustaceans from the scottish west coast. Ophelia 30: 225–233.Google Scholar
  15. Crowe, J., L. Crowe, P. Roe & D. Wickham, 1982. Uptake of DOM by nemertean worms: Association of worms with arthrodial membranes. Am. Zool. 22: 671–682.Google Scholar
  16. Davis, C. C., 1965. A study of the hatching process in aquatic invertebrates: XX. The blue crab, Callinectes sapidus, Rathbun, XXI. The nemertean, Carcinonemertes carcinophila (Kölliker). Chesapeake Sci. 6: 201–208.CrossRefGoogle Scholar
  17. Dieck, G., 1874. Beitrage zur Entwicklunsgeschichte der Nemertinen. Jena Z. Naturw. 8: 500–520.Google Scholar
  18. Dunham, P. J., 1978. Sex pheromones in Crustacea. Biol. Rev. 53: 555–583.Google Scholar
  19. Fleming, L. C. & R. Gibson, 1981. A new genus and species of monostiliferous hoplonemerteans, ectohabitant on lobsters. J. exp. mar. Biol. Ecol. 52: 79–93.CrossRefGoogle Scholar
  20. Gibson, R. & D. S. Jones, 1990. A new species of Carcinonemertes (Nemertea: Enopla: Carcinonemertidae) from the egg masses of Naxia aurita (Latreille) (Decapoda: Brachyura: Majidae) collected in the Albany region of Western Australia. In F. E. Wells, D. I. Walker, H. Kirkman & R. Lethbridge (eds), Proc. Third Int. Mar. Biol. Workshop. The Marine Flora & Fauna of Albany, Western Australia, Western Australia Mus., Perth. Vol. 1: 195–202.Google Scholar
  21. Hankin, D. G., N. Diamond, M. S. Mohr & J. Ianelli, 1989. Growth and reproductive dynamics of adult female Dungeness crabs (Cancer magister)in northern California. J. Cons. int. Explor. Mer. 46: 94–108.Google Scholar
  22. Herrick, F. H., 1896. The American lobster. A study of its habits and development. Bull. U.S. Fish. Comm. 15: 1–252.Google Scholar
  23. Hobbs, R. C. & L. W. Botsford, 1989. Dynamics of an agestructured prey with density- and predator-dependent recruitment: the Dungeness crab and a nemertean egg predator worm. Theor. Pop. Biol. 36: 1–22.CrossRefGoogle Scholar
  24. Hopkins, S. H., 1947. The nemertean Carcinonemertes as an indicator of the spawning history of the host, Callinectes sapidus. J. Parasit. 33: 146–150.CrossRefGoogle Scholar
  25. Humes, A. G., 1942. The morphology, taxonomy, and bionomics of the nemertean genus Carcinonemertes. Illinois Biol. Monogr. 18: 1–105.Google Scholar
  26. Kölliker, A., 1845. Ueber drei neue Gattungen von Wurmern, Lineola, Chloraima, Polycystia, neue Wurmgattungen, und neue Arten von Nemertes. Verb. Schweiz. Naturf. Ges., Chur, 29 (1844): 86–98.Google Scholar
  27. Kuris, A. M., 1971. Population interactions between a shore crab and two symbionts. Ph.D. Thesis, Univ. California, Berkeley, 431 pp.Google Scholar
  28. Kuris, A. M., 1978. Life cycle, distribution and abundance of Carcinonemertes epialti, a nemertean egg predator of the shore crab, Hemigrapsus oregonensis, in relation to host size, reproduction and molt cycle. Biol. Bull. 154: 121–137.Google Scholar
  29. Kuris, A. M., 1991. A review of patterns and causes of crustacean brood mortality. In: A. M. Wenner & A. M. Kuris [ed.] Crustacean Egg Production, Crustacean Issues 6, Balkema, Rotterdam, pp. 117–141.Google Scholar
  30. Kuris, A. M., S. F. Blau, A. J. Paul, J. D. Shields & D. E. Wickham, 1991. Infestation by brood symbionts and their impact on egg mortality in the red king crab, Paralithodes camtschatica, in Alaska,: geographic and temporal variation. Can. J. Fish aquat. Sci. 48: 559–568.CrossRefGoogle Scholar
  31. Kuris, A. M. & K. D. Lafferty, 1992. Modeling crustacean fisheries: effects of parasites on management strategies. Can. J. Fish. aquat. Sci. 327–336.Google Scholar
  32. Kuris, A. M. & D. E. Wickham, 1987. Effect of nemertean egg predators on crustaceans. Bull. mar. Sci. 41: 151–164.Google Scholar
  33. Laverack, M. S. & J. Dando, 1987. Lecture Notes on Invertebrate Zoology, 3rd edn. Blackwell Scientific Publications, Oxford, 203 pp.Google Scholar
  34. McDermott, J. J., 1966. The biology of a nemertean parasite of pinnotherid crabs. Am. Zool. 6: 331.Google Scholar
  35. McDermott, J. J. & R. Gibson, 1993. Carcinonemertes pinnotheridophila sp. nov. (Nemertea, Enopla, Carcinonemertidae) from the branchial chambers of Pinnixa chaetopterana (Crustacea, Decapoda, Pinnotheridae): description, incidence and biological relationships with the host. Hydrobiologia 266: 57–80.Google Scholar
  36. Morse, D. E., 1986. External molecular signals controlling reproduction, settlement and metamorphosis of benthic marine invertebrates. In M.-F. Thompson, R. Sarojini & R. Nagabhushanam (eds), Biology of Benthic Marine Organisms. Techniques and Methods as Applied to the Indian Ocean, Oxford & IBH Publ. Co., New Delhi: 379–385.Google Scholar
  37. Overstreet, R. M., 1978. Marine Maladies? Worms, Germs, and other Symbionts from the Northern Gulf of Mexico. Mississippi-Alabama Sea Grant Consortium. MASGAP78–021: 1–140.Google Scholar
  38. Perkins, H. C., 1971. Egg loss during incubation from offshore northern lobsters (Decapoda: Homaridae). Fish. Bull. 60: 451–453.Google Scholar
  39. Powell, G. C. & R. B. Nickerson, 1965. Reproduction of king crabs, Paralithodes camtschatica (Tilesius). J. Fish. Res. Bd Can. 22: 101–111.Google Scholar
  40. Roe, P., 1979. Aspects of development and occurrence of Carcinonemertes epialti (Nemertea) from shore crabs in Monterey Bay, California. Biol. Bull. 156: 130–140.Google Scholar
  41. Roe, P., 1986. Parthenogenesis in Carcinonemertes spp. (Nemertea: Hoplonemertea). Biol. Bull. 171: 700–706.Google Scholar
  42. Roe, P., J. Crowe, L. Crowe & D. Wickham, 1981. Uptake of amino acids by juveniles of Carcinonemertes errans (Nemertea). Comp. Biochem. Physiol. 69A: 423–427.CrossRefGoogle Scholar
  43. Shields, J. D., 1991. The reproductive ecology and fecundity of Cancer crabs. In Wenner, A. M. & A. M. Kuris (eds), Crustacean egg production. Crustacean issues 7. Balkema, Rotterdam, pp. 193–213.Google Scholar
  44. Shields, J. D. & A. M. Kuris, 1988. Temporal variation in abundance of the egg predator Carcinonemertes epialti (Nemertea) and its effect on egg mortality of its host, the shore crab, Hemigrapsus oregonensis. Hydrobiologia 156: 31–38.CrossRefGoogle Scholar
  45. Shields, J. D., R. K. Okazaki & A. M. Kuris, 1990a. Brood mortality and egg predation by the nemertean, Carcinonemertes epialti, on the yellow rock crab, Cancer anthonyi, in southern California. Can. J. Fish. aquat. Sci. 47: 1269–1275.CrossRefGoogle Scholar
  46. Shields, J. D., D. E. Wickham, S. F. Blau & A. M. Kuris, 1990b. Some implications of egg mortality caused by symbiotic nemerteans for data acquisition and management strategies of red king crabs Paralithodes camtschatica. Proc. Int. King Tanner Crab Symp. Lowell Wakefield Symp. Ser. Alaska Sea Grant Rep. 90–04: 383–395.Google Scholar
  47. Smith, B. D. & G. S. Jamieson, 1989. Growth of male and female Dungeness crabs near Tofino, British Columbia. Trans. am. Fish. Soc. 118: 556–563.CrossRefGoogle Scholar
  48. Stricker, S. A., 1986. An ultrastructural study of oogenesis, fertilization, and egg laying in a nemertean ectosymbiont of crabs, Carcinonemertes epialti (Nemertea: Hoplonemertea). Can. J. Zool. 64: 1256–1269.Google Scholar
  49. Stricker, S. & C. G. Reed, 1981. Larval morphology of the nemertean Carcinonemertes epialti (Nemertea: Hoplonemertea). J. Morph. 169: 61–70.CrossRefGoogle Scholar
  50. Sundberg, P., 1990. Gibson's reclassification of the enoplan Nemerteans (Enopla, Nemertea): a critique and cladistic analysis. Zool. Scripta 19: 133–140.CrossRefGoogle Scholar
  51. Templeman, W., 1940. Embryonic developmental rates and egg-laying of Canadian lobsters. J. Fish. Res. Bd Can. 5: 71–83.Google Scholar
  52. Uhazy, L. S., D. E. Aiken & A. Campbell, 1985. Morphology and systematics of the nemertean Pseudocarcinonemertes homari (Hoplonemertea: Monostilifera) from the American lobster, Homarus americanus. Can. J. Fish. aquat. Sci. 42: 342–350.Google Scholar
  53. Van Beneden, P. J., 1861. Recherches sur la faune littorale de Belgique. Turbellariés. Mem. Acad. Roy. Soc. Belg. 32: 1–56.Google Scholar
  54. Wickham, D. E., 1979. Predation by the nemertean carcinonemertes errans on eggs of the Dungeness crab, Cancer magister. Mar. Biol. 55: 45–53.CrossRefGoogle Scholar
  55. Wickham, D. E., 1978. A new species of Carcinonemertes (Nemertea: Carcinonemertidae) with notes on the genus from the pacific coast. Proc. Biol. Soc. Wash. 91: 197–202.Google Scholar
  56. Wickham, D. E., 1980. Aspects of the life history of Carcinonemertes errans (Nemertea: Carcinonemertidae), an egg predator of the crab Cancer magister. Biol. Bull. 159: 247–257.Google Scholar
  57. Wickham, D. E., 1986. Epizootic infestations by nemertean brood parasites on commercially important crustaceans. Can J. Fish aquat. Sci. 43: 2295–2302.CrossRefGoogle Scholar
  58. Wickham, D. E. & A. M. Kuris, 1985. The comparative ecology of nemertean egg predators. Am. Zool. 25: 127–134.Google Scholar
  59. Wickham, D. E. & A. M. Kuris, 1988. Diversity among nemertean egg predators of decapod crustaceans. Hydrobiologia 156: 23–30.CrossRefGoogle Scholar
  60. Wickham, D. E. & A. Kuris, 1990. Brood mortality estimation and role of symbionts in egg mortality of the tanner crab Chionoecetes bairdi in Alaskan waters. Proc. Int. King Tanner Crab Symp. Lowell Wakefield Symp. Ser. Alaska Sea Grant Rep. 9004: 397–402.Google Scholar
  61. Wickham, D. E. & P. Roe, 1987. Selectivity in transmission to crab hosts by the symbiotic nemertean, Carcinonemertes epialti. J. Parasit. 73: 697–701.CrossRefGoogle Scholar
  62. Wickham, D. E., P. Roe & A. M. Kuris, 1984. Transfer of nemertean egg predators during host molting and copulation. Biol. Bull. 167: 331–338.Google Scholar
  63. Williams, A. B., 1984. Shrimps, Lobsters, and Crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Smithsonian Institution Press, Washington, 550 pp.Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Armand M. Kuris
    • 1
  1. 1.Department of Biological Sciences and Marine Science InstituteUniversity of CaliforniaSanta BarbaraUSA

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