Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-15T13:26:54.123Z Has data issue: false hasContentIssue false

Infestation with larvae of the sea anemone Edwardsia lineata affects nutrition and growth of the ctenophore Mnemiopsis leidyi

Published online by Cambridge University Press:  06 April 2009

D. Bumann*
Affiliation:
Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA
G. Puls
Affiliation:
Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA
*
*Corresponding author. Tel:+1 508 289 7368. Fax: + 1 508 540 6902. E-mail: [email protected].

Summary

The lobate ctenophore Mnemiopsis leidyi is a periodically abundant and voracious plankton predator in coastal waters along the east coast of the United States. In the 1980s it was accidentally introduced to the Black Sea where it caused a dramatic reduction in fisheries. We investigated how M. leidyi is affected by infestation with parasitic larvae of the sea anemone Edwardsia lineata. Infested M. leidyi contained 1–30 (median 7) E. lineata larvae. Within M. leidyi most larvae had their mouth in the gastrovascular system near the aboral end of the pharynx. Parasitic E. lineata ingested all food previously ingested and pre-digested by M. leidyi. Non-infested M. leidyi had higher growth rates than infested individuals, which had zero or negative growth rates. Egg production was similar for infested and non-infested M. leidyi of similar size. Simulation based on the empirical data suggests that growing, non-infested, M. leidyi are expected to have a larger life-time egg production than infested shrinking individuals. E. lineata could be at least partially responsible for the sharp decline of M. leidyi populations in fall in US coastal waters. Advantages and disadvantages of E. lineata as a potential candidate for the control of the artificially introduced M. leidyi population in the Black Sea are discussed.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baker, L. D. & Reeve, M. R. (1974). Laboratory culture of the lobate ctenophore Mnemiopsis mccradyi with notes on feeding and fecundity. Marine Biology 26, 5762.CrossRefGoogle Scholar
Black, N. A., Szmant, A. M. & Tomchik, R. S. (1994). Planulae of the scyphomedusa Linuche unguiculata as a possible cause of seabather's eruption. Bulletin of Marine Science 54, 955960.Google Scholar
Burell, V. G. & Engel, W. A.Van (1976). Predation by and distribution of a ctenophore, Mnemiopsis leidyi A. Agassiz, in the York River Estuary. Estuarine and Coastal Marine Science 4, 235242.CrossRefGoogle Scholar
Cahoon, L. B., Tronzo, C. R. & Howe, J. C. (1986). Notes on the occurrence of Hyperoche medusarum (Kroeyer) (Amphipoda, Hiperiidae) with Ctenophora off North Carolina, USA. Crustaceana 51, 9596.CrossRefGoogle Scholar
Crowell, S. (1965). A sea anemone parasitic as a larva in a comb jelly. American Zoologist 5, 88.Google Scholar
Crowell, S. (1976). An edwardsiid larva parasitic in Mnemiopsis. In Coelenterate Ecology and Behavior (ed. Mackie, G. O.), pp. 247250. New York: Plenum.CrossRefGoogle Scholar
Crowell, S. & Oates, S. (1980). Metamorphosis and reproduction by transverse fission in an edwardsiid anemone. In Development and Cellular Biology of Coelenterates (ed. Tardent, P. & Tardent, R.), pp. 139142. Amsterdam: Elsevier.Google Scholar
Deason, E. E. & Smayda, T. J. (1982). Experimental evaluation of herbivory in the ctenophore Mnemiopsis leidyi relevant to ctenophore-zooplankton-phytoplankton interactions in Narragansett Bay, Rhode Island, USA. Journal of Plankton Research 4, 219236.CrossRefGoogle Scholar
Freudenthal, A. R. & Joseph, P. R. (1993). Seabather's eruption. New England Journal of Medicine 329, 542544.CrossRefGoogle ScholarPubMed
Gaevskaya, A. V. & Mordvinova, T. N. (1994). Occurrence of nematode larvae as parasites of the ctenophore Mnemiopsis mccardyi in the Black Sea. Hydrobiological Journal 30, 108110.Google Scholar
Gibbons, M. J. & Painting, S. J. (1992). The effects and implications of container volume on clearance rates of the ambush entangling predator Pleurobrachia pileus (Ctenophora: Tentaculata). Journal of Experimental Marine Biology and Ecology 163, 199208.CrossRefGoogle Scholar
Harbison, G. R., Biggs, D. C. & Madin, L. P. (1977). The associations of Amphipoda Hyperiidea with gelatinous zooplankton. 2. Associations with Cnidaria, Ctenophora and Radiolaria. Deep Sea Research 24, 465488CrossRefGoogle Scholar
Harbison, G. R., Madin, L. P. & Swanberg, N. R. (1978). On the natural history and distribution of oceanic ctenophores. Deep Sea Research 25, 233256.CrossRefGoogle Scholar
Harbison, G. R. & Volovik, S. P. (1994 a). The ctenophore, Mnemiopsis leidyi, in the Black Sea: A holoplanktonic organism transported in the ballast water of ships. In Nonindigenous Estuarine and Marine Organisms (NEMO) (ed. NOAA), pp. 2536. Washington: U.S. Government Printing Office.Google Scholar
Harbison, G. R. & Volovik, S. P. (1994 b). Methods for the control of populations of the ctenophore, Mnemiopsis leidyi, in the Black and Azov Seas. FAO Fisheries Report No. 495.Google Scholar
Hernandez-nicaise, M.-L. (1991). Ctenophora. In Microscopy of Invertebrates, Vol. 2: Placozoa, Porifera, Cnidaria, and Ctenophora (ed. Harrison, F. W. & Westfall, J. A.), pp. 359418. New York: Wiley.Google Scholar
Houde, E. D., Gamble, J. C., Dorsey, S. E. & Cowan, J. H. Jr. (1994). The influence of gelatinous zooplankton on mortality of bay anchovy, Anchoa mitchilli, eggs and yolk-sac larvae. ICES Journal of Marine Science 51, 383394.CrossRefGoogle Scholar
Kideys, A. C. (1994). Recent dramatic changes in the Black Sea ecosystem: the reason for the sharp decline in Turkish anchovy fisheries. Journal of Marine Systems 5, 171181.CrossRefGoogle Scholar
Kideys, A. C. & Niermann, U. (1994). Occurrence of Mnemiopsis along the Turkish coast. ICES Journal of Marine Science 51, 423427.CrossRefGoogle Scholar
Khoroshilov, V. S. (1994). Seasonal dynamics of the Black Sea population of the ctenophore Mnemiopsis leidyi. Oceanology 33, 482485.Google Scholar
Kremer, P. (1976). Population dynamics and ecological energetics of a pulsed zooplankton predator, the ctenophore Mnemiopsis leidyi. In Estuarine Processes, Vol. I (ed. Wiley, M.), pp. 197215. New York: Academic Press.CrossRefGoogle Scholar
Kremer, P. (1994). Patterns of abundance for Mnemiopsis in the US coastal waters: a comparative overview. ICES Journal of Marine Science 51, 347354.CrossRefGoogle Scholar
Kremer, P. & Nixon, S. (1976). Distribution and abundance of the ctenophore, Mnemiopsis leidyi in Narragansett Bay. Estuarine and Coastal Marine Science 4, 627639.CrossRefGoogle Scholar
Kremer, P. & Reeve, M. R. (1989). Growth dynamics of a ctenophore (Mnemiopsis) in relation to variable food supply. II. Carbon budgets and growth model. Journal of Plankton Research 11, 553574.CrossRefGoogle Scholar
Lebedeva, L. P. & Shushkina, Eh. A. (1994). Modelling the effect of Mnemiopsis on the Black Sea plankton community. Oceanology 34, 7280.Google Scholar
Melville, R. V. & Smith, J. D. D. (1987). Official List and Index of Names and Works in Zoology. International Commission on Zoological Nomenclature. London: The International Trust for Zoological Nomenclature.Google Scholar
Monteleone, D. M. & Duguay, L. E. (1988). Laboratory studies of predation by the ctenophore Mnemiopsis leidyi on the early stages in the life history of the bay anchovy, Anchoa mitchilli. Journal of Plankton Research 10, 359372.CrossRefGoogle Scholar
Niermann, U., Bingel, F., Gorban, A., Gordina, A. D., Gucu, A. C., Kideys, A. E., Konsulov, A., Radu, G., Subbotin, A. A. & Zaika, V. E. (1994). Distribution of anchovy eggs and larvae (Engraulis encrasicolus Cuv.) in the Black Sea in 1991–1992. ICES Journal of Marine Science 51, 395406.CrossRefGoogle Scholar
Nyholm, K.-G. (1949). On the development and dispersal of athenarian actinia with special reference to Halcampa duodecimcirrata. Zoologiska Bidrag från Uppsala 27, 467505.Google Scholar
Oviatt, C. M. & Kremer, P. (1977). Predation on the ctenophore Mnemiopsis leidyi by butterfish Peprilus tricanthus in Narragansett Bay, Rhode Island. Chesapeake Science 18, 236240.CrossRefGoogle Scholar
Reeve, M. R. (1980). Comparative experimental studies on the feeding of chaetognaths and ctenophores. Journal of Plankton Research 2, 381393.CrossRefGoogle Scholar
Reeve, M. R. & Walter, M. A. (1978). Nutritional ecology of ctenophores – a review of recent research. Advances in Marine Biology 15, 249287.CrossRefGoogle Scholar
Reeve, M. R., Walter, M. A. & Ikeda, T. (1978). Laboratory studies of ingestion and food utilization in lobate and tentaculate ctenophores. Limnology and Oceanography 23, 740751.CrossRefGoogle Scholar
Reeve, M. R., Syms, M. A. & Kremer, P. (1989). Growth dynamics of a ctenophore (Mnemiopsis) in relation to variable food supply. 1. Carbon biomass, feeding, egg production, growth and assimilation efficiency. Journal of Plankton Research 11, 535552.CrossRefGoogle Scholar
Seravin, L. N. (1994 a). The systematic revision of the genus Mnemiopsis (Ctenophora, Lobata). 1. The history of description and study of species belonging to the genus Mnemiopsis. Zoologicheskii Zhurnal 73, 918.Google Scholar
Seravin, L. N. (1994 b). The systematic revision of the genus Mnemiopsis (Ctenophora, Lobata). 2. Species attribution of Mnemiopsis form the Black Sea and the species composition of the genus Mnemiopsis. Zoologicheskii Zhurnal 73, 1934.Google Scholar
Siegel, S. (1956). Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill.Google Scholar
Spaulding, J. G. (1972). The life cycle of Peachia quinquecapitata, an anemone parasitic on medusae during its larval development. Biological Bulletin 143, 440453.CrossRefGoogle Scholar
Stephenson, T. A. (1935) The British Sea Anemones, Vol. II. London: The Ray Society.Google Scholar
Strathmann, M. (1987). Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast. Seattle: University of Washington Press.Google Scholar
Stunkard, H. W. (1980). Successive hosts and developmental stages in the life history of Neopechona cablei–sp.n. (Trematoda: Lepocreadiidae). Journal of Parasitology 66, 636641.CrossRefGoogle Scholar
Sullivan, B. K. & Reeve, M. R. (1982). Comparison of estimates of the predatory impact of ctenophores by two independent techniques. Marine Biology 68, 6165.CrossRefGoogle Scholar
Vinogradov, M. YE., Shushkina, E. A., Musayeva, E. I. & Sorokin, P. YU. (1989). A newly acclimatized species in the Black Sea: The ctenophore Mnemiopsis leidyi (Ctenophora: Lobata). Oceanology 29, 220224.Google Scholar
Williams, R. B. (1979). Edwordsia Costa, 1834 (Arthropoda, Crustacea): proposed suppression under the plenary powers with conservation of Edwardsia de Quatrefages, 1841 and Edwardsiidae Andres, 1881 (Coelenterata: Actiniaria). Bulletin of Zoological Nomenclature 36, 175179.CrossRefGoogle Scholar
Wong, D. E., Meinking, T. L., Rosen, L. B., Taplin, D., Hogan, D. J. & Burnett, J. W. (1994). Seabather's eruption. Clinical, histologic, and immunologic features. Journal of the American Academy of Dermatology 30, 399406.CrossRefGoogle ScholarPubMed
Yip, S. Y. (1984). Parasites of Pleurobrachia pileus Mueller, 1776 (Ctenophora), from Galway Bay, western Ireland. Journal of Plankton Research 6, 107121CrossRefGoogle Scholar