Skip to main content
Log in

Requirement of exogenous inducers for metamorphosis of axenic larvae and buds of Cassiopea andromeda (Cnidaria: Scyphozoa)

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Planula larvae and asexually-produced buds of the rhizostome scyphozoan Cassiopea andromeda (collected throughout the year in Eilat, Israel) have the ability, under axenic conditions, to attach to a substrate and undergo morphogenetic development to form a polyp (=scyphistoma) in: (1) the presence of unidentified inducers found in the adult habitat and (2) the presence of cefined organic compounds. Axenic planulae and buds were unable to settle and complete metamorphosis in autoclaved artificial or natural seawater from the North Sea when maintained without food, but continued swimming while decreasing in size and protein content, eventually dying within three months. When maintained in autoclaved seawater from the Red Sea, between 25 and 46% of the planulae and 4 and 11% of the buds metamorphosed within 30 d. Axenic solutions of cholera toxin, thyroid stimulating hormone, and pancreatic casein hydrolysate peptides in artificial seawater induced morphogenic development of 20 to 100% of planulae and buds within 2 to 18 d. The natural inducer(s) in Red Sea seawater, though unidentified, may have characteristics similar to the large proteins and small peptide inducers used in this study. Planulae and buds older than 20 d metamorphosed sooner and responded to lower concentrations of pancreatic casein hydrolysate peptides than younger individuals. This may be a physiological mechanism for enhancing metamorphosis and survival in nature. The data show that settlement and metamorphosis can be induced by solutions of cholera toxin and thyroid stimulating hormone, suggesting that, as in mammalian systems, the mechanism of action of these chemicals may involve cyclic adenosine monophosphate (cAMP) as an intermediate messenger. However, dibutyric cAMP, which is capable of passing through membranes and functioning normally inside the cell, did not induce metamorphosis of buds, and the levels of intracellular cAMP in buds and larvae typically increased slowly during induction of metamorphosis, unlike the high and rapid increases associated with cAMP-mediated biochemical events in mammalian cells. These results suggest that the observed cAMP changes seen were associated with metamorphic development, but not with the triggering mechanism.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Baloun, A. J. and D. E. Morse: Ionic control of settlement and metamorphosis in larval Haliotis rufescens (Gastropoda). Biol. Bull. mar. biol. Lab., Woods Hole 167, 124–138 (1984)

    Article  CAS  Google Scholar 

  • Brancato, M. S. and R. M. Woollacott: Effect of microbial films on settlement of bryozoan larvae (Bugula simplex, B. stolonifera, B. turrila). Mar. Biol. 71, 51–56 (1982)

    Article  Google Scholar 

  • Brand, U.: Bakterielle und enzymatische Abbauprodukte komplexer Proteine als Auslöser der Metamorphose bei Schwimmknospen von Cassiopea andromeda, 114 pp. Diplomarbeit, Ruhr Universität, Bochum 1984

  • Burke, R. D.: The induction of marine invertebrate larvae: stimulus and response. Can. J. Zool. 61, 1701–1719 (1983)

    Article  Google Scholar 

  • Cameron, A. M. and R. T. Hinegardner: Initiation of metamorphosis in laboratory cultured sea urchins. Biol. Bull. mar. biol. Lab., Woods Hole 146, 335–342 (1974)

    Article  CAS  Google Scholar 

  • Chia, F. S. and M. E. Rice: Settlement and metamorphosis of marine invertebrate larvae, 290 pp. New York: Elsevier/North-Holland Biomedical Press 1978

    Google Scholar 

  • Crisp, D., Jr.: Factors influencing the settling of marine invertebrate larvae. In: Chemoreception in marine organisms, pp 177–265. Ed. by P. T. Grant and A. M. Mackie. New York: Academic Press 1974

    Google Scholar 

  • Crisp, D., Jr.: Settlement responses in marine organisms. In: Adaptations to environment: essays on the physiology of marine animals, pp 83–124. Ed. by R. C. Newell, London: Butterworths 1976

    Chapter  Google Scholar 

  • Fitt, W. K. and D. K. Hofmann: Chemical induction of settlement and metamorphosis of the reef-dwelling coelenterate Cassiopea andromeda. Proc. 5th int. Coral Reef Congr. 5, 239–244 (1985)

    Google Scholar 

  • Gray, J. S.: The attractive factor of intertidal sands to Protodrilus symbioticus Girard. J. mar. biol. Ass. U.K. 46, 627–645 (1966)

    Article  Google Scholar 

  • Gray, J. S.: Substrate selection by the archiannelid Protodrilus rubropharyngeus. Helgoländer wiss. Meeresunters. 15, 253–269 (1967)

    Article  Google Scholar 

  • Hashimoto, P. H., S. Takaesu, N. Chazono and T. Amano: Vascular leakage through intraendothelial channels induced by cholera toxin in the skin of Guinea pigs. Am. J. Pathol. 75, 171–180 (1974)

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hofmann, D. K., K. Bernardy and U. Brand: Asexual reproduction in Cassiopea andromeda (Scyphozoa): induction of settlement and metamorphosis in vegetative buds. In: Advances in invertebrate reproduction, Vol. 3, 592 pp. Ed. by W. Engels. Amsterdam. Elsevier 1984

    Google Scholar 

  • Hofmann, D. K. and B. P. Kremer: Carbon metabolism and strobilation in Cassiopea andromeda (Cnidaria: Scyphozoa): significance of endosymbiotic dinoflagellates. Mar. Biol. 65, 25–33 (1981)

    Article  CAS  Google Scholar 

  • Hofmann, D. K., R. Neumann and K. Henne: Strobilation and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria, Scyphozoa). Mar. Biol. 47, 161–176 (1978)

    Article  Google Scholar 

  • Holmgren, J.: Actions of cholera toxin and the prevention and treatment of cholera. Nature, Lond. 292, 413–417 (1981)

    Article  CAS  Google Scholar 

  • Kirchman, D., S. Graham, D. Reish and R. Mitchell: Bacteria induce settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). J. exp. mar. Biol. Ecol. 56, 153–163 (1982)

    Article  Google Scholar 

  • Knight-Jones, E. W.: Decreased discrimination during setting after prolonged larval life in larvae of Spirorbis borealis (Serpulidae). J. mar. biol. Ass. U.K. 32, 337–345 (1953)

    Article  Google Scholar 

  • Lowry, O. H., H. J. Rosenborough, A. L. Farr and R. J. Randall: Protein measurement with folin phenol reagent. J. biol. Chem. 193, 265–275 (1951)

    CAS  PubMed  Google Scholar 

  • Meadows, P. S. and J. I. Campbell Habitat selection by marine invertebrates. Adv. mar. Biol. 10, 271–361 (1972)

    Article  Google Scholar 

  • Mihm, J. W. and W. C. Banta: Effects of adsorbed organic and primary fouling films on bryozoan settlement. J. exp. mar. Biol. Ecol. 54, 167–179 (1981)

    Article  Google Scholar 

  • Morse, D. E.: Neurotransmitter-mimetic inducers of larval settlement and metamorphosis. Bull. mar. Sci. 37, 697–706 (1985)

    Google Scholar 

  • Müller, W. A.: Auslösung der Metamorphose durch Bakterien bei den Larven von Hydractinia echinata. Zool. Jb. Abt. Anat. Ontog. 86, 84–95 (1969)

    Google Scholar 

  • Müller, W. A.: Metamorphose-Induktion bei Planulalarven I. Der bakterielle Induktor. Wilhelm Roux' Arch. Entwicklungsmech. Org. 173, 107–121 (1973)

    Article  Google Scholar 

  • Naust, G.: Auslösung der Polypenmorphogenese bei Cassiopea andromeda (Scyphozoa): Zur Induktionswirkung von Caseinen und deren proteolytischen Spaltprodukten, 78 pp. Staatsexamensarbeit, Bochum 1985

  • Neumann, R.: Bacterial induction of settlement and metamorphosis in the planulae larvae of Cassiopea andromeda (Cnidaria: Scyphozoa, Rhizostomeae). Mar. Ecol. Prog. Ser. 1, 21–28 (1979)

    Article  Google Scholar 

  • Neumann, R., G. Schmahl and D. K. Hofmann: Bud formation and control of polyp morphogenesis. In: Developmental and cellular biology of coelenterates, pp 217–223, Ed. by P. Tardent and R. Tardent. Amsterdam: Elsevier/North-Holland 1980

    Google Scholar 

  • Rittschof, D. E., J. D. Branscomb and J. D. Costlow: Settlement and behavior in relation to flow and surface in larval barnacles, Balanus amphitrite Darwin. J. exp. mar. Biol. Ecol. 82, 131–146 (1984)

    Article  Google Scholar 

  • Roger, P. P. and J. E. Dumont: Factors controlling proliferation and differentiation of canine thyroid cells cultured in reduced serum albumins: effects of thyrotropin, cyclic AMP and growth factos. Mol. Cell Endocrin. 36, 79–93 (1984)

    Article  CAS  Google Scholar 

  • Scheltema, R. S.: Biological interactions determining larval settlement of marine invertebrates. Thalassia jugosl. 10, 263–296 (1974)

    Google Scholar 

  • Specht, D. T. and W. E. Miller: Modified Burkholder's artificial sea water. Proc. Seminar Methodol. Monit. mar. Envir. Oct. 1974, pp 194–230. Wash. D.C.: U.S. Environmental Protection Agency 1974

    Google Scholar 

  • Sugiura, Y.: On the life history of rhizostome medusae. II. Indispensability of zooxanthellae for strobilation in Mastigias papua. Embryologia 8, 223–233 (1964)

    Article  Google Scholar 

  • Weiner, R. M., A. M. Segall and R. R. Colwell: Characterization of a marine bacterium associated with Crassostrea virginica (the Eastern oyster). Appl. envir. Microbiol. 49, 83–90 (1985)

    CAS  Google Scholar 

  • Wolk, M., M. Rahat, W. K. Fitt and D. K. Hofmann: Cholera toxin and thyrotropine can replace natural inducers required for the metamorphosis of larvae and buds of the scyphozoan Cassiopea andromeda. Roux's Arch. Dev. Biol. 194, 487–490 (1985)

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fitt, W.K., Hofmann, D.K., Wolk, M. et al. Requirement of exogenous inducers for metamorphosis of axenic larvae and buds of Cassiopea andromeda (Cnidaria: Scyphozoa). Mar. Biol. 94, 415–422 (1987). https://doi.org/10.1007/BF00428248

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00428248

Keywords

Navigation