Skip to main content
SpringerLink
Log in

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

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 

  • 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 

  • 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 

  • Bauman, L., 1983. The larval biology of Carcinonemertes. Master's Thesis, University of California, Santa Cruz, California.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • Brooks, W. K. & F. H. Herrick, 1892. The embryology and metamorphosis of the Macroura Mem. Nat. Acad. Sci. 5: 323–576.

    Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • Chang, E. S., 1989. Endocrine regulation of molting in Crustacea. CRC Critical Rev. aquat. Sci. 1: 131–157.

    Google Scholar 

  • Coe, W. R., 1902. Nemertean parasites of crabs. Am. Nat. 36: 431–450.

    Article  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Dieck, G., 1874. Beitrage zur Entwicklunsgeschichte der Nemertinen. Jena Z. Naturw. 8: 500–520.

    Google Scholar 

  • Dunham, P. J., 1978. Sex pheromones in Crustacea. Biol. Rev. 53: 555–583.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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 

  • Herrick, F. H., 1896. The American lobster. A study of its habits and development. Bull. U.S. Fish. Comm. 15: 1–252.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hopkins, S. H., 1947. The nemertean Carcinonemertes as an indicator of the spawning history of the host, Callinectes sapidus. J. Parasit. 33: 146–150.

    Article  Google Scholar 

  • Humes, A. G., 1942. The morphology, taxonomy, and bionomics of the nemertean genus Carcinonemertes. Illinois Biol. Monogr. 18: 1–105.

    Google Scholar 

  • 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 

  • Kuris, A. M., 1971. Population interactions between a shore crab and two symbionts. Ph.D. Thesis, Univ. California, Berkeley, 431 pp.

    Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • Kuris, A. M. & K. D. Lafferty, 1992. Modeling crustacean fisheries: effects of parasites on management strategies. Can. J. Fish. aquat. Sci. 327–336.

  • Kuris, A. M. & D. E. Wickham, 1987. Effect of nemertean egg predators on crustaceans. Bull. mar. Sci. 41: 151–164.

    Google Scholar 

  • Laverack, M. S. & J. Dando, 1987. Lecture Notes on Invertebrate Zoology, 3rd edn. Blackwell Scientific Publications, Oxford, 203 pp.

    Google Scholar 

  • McDermott, J. J., 1966. The biology of a nemertean parasite of pinnotherid crabs. Am. Zool. 6: 331.

    Google Scholar 

  • 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 

  • 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 

  • 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.

  • Perkins, H. C., 1971. Egg loss during incubation from offshore northern lobsters (Decapoda: Homaridae). Fish. Bull. 60: 451–453.

    Google Scholar 

  • Powell, G. C. & R. B. Nickerson, 1965. Reproduction of king crabs, Paralithodes camtschatica (Tilesius). J. Fish. Res. Bd Can. 22: 101–111.

    Google Scholar 

  • 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 

  • Roe, P., 1986. Parthenogenesis in Carcinonemertes spp. (Nemertea: Hoplonemertea). Biol. Bull. 171: 700–706.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • 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.

    Article  Google Scholar 

  • 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 

  • Stricker, S. & C. G. Reed, 1981. Larval morphology of the nemertean Carcinonemertes epialti (Nemertea: Hoplonemertea). J. Morph. 169: 61–70.

    Article  Google Scholar 

  • Sundberg, P., 1990. Gibson's reclassification of the enoplan Nemerteans (Enopla, Nemertea): a critique and cladistic analysis. Zool. Scripta 19: 133–140.

    Article  Google Scholar 

  • Templeman, W., 1940. Embryonic developmental rates and egg-laying of Canadian lobsters. J. Fish. Res. Bd Can. 5: 71–83.

    Google Scholar 

  • 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 

  • Van Beneden, P. J., 1861. Recherches sur la faune littorale de Belgique. Turbellariés. Mem. Acad. Roy. Soc. Belg. 32: 1–56.

    Google Scholar 

  • Wickham, D. E., 1979. Predation by the nemertean carcinonemertes errans on eggs of the Dungeness crab, Cancer magister. Mar. Biol. 55: 45–53.

    Article  Google Scholar 

  • 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 

  • 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 

  • Wickham, D. E., 1986. Epizootic infestations by nemertean brood parasites on commercially important crustaceans. Can J. Fish aquat. Sci. 43: 2295–2302.

    Article  Google Scholar 

  • Wickham, D. E. & A. M. Kuris, 1985. The comparative ecology of nemertean egg predators. Am. Zool. 25: 127–134.

    Google Scholar 

  • Wickham, D. E. & A. M. Kuris, 1988. Diversity among nemertean egg predators of decapod crustaceans. Hydrobiologia 156: 23–30.

    Article  Google Scholar 

  • 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.

  • Wickham, D. E. & P. Roe, 1987. Selectivity in transmission to crab hosts by the symbiotic nemertean, Carcinonemertes epialti. J. Parasit. 73: 697–701.

    Article  Google Scholar 

  • 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 

  • 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 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences and Marine Science Institute, University of California, 93106, Santa Barbara, CA, USA

    Armand M. Kuris

Authors
  1. Armand M. Kuris
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kuris, A.M. Life cycles of nemerteans that are symbiotic egg predators of decapod Crustacea: adaptations to host life histories. Hydrobiologia 266, 1–14 (1993). https://doi.org/10.1007/BF00013355

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00013355

Key words

Search

Navigation