Marine Biology

, Volume 124, Issue 1, pp 147–155 | Cite as

Transmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata

  • M. K. Montgomery
  • P. M. Kremer
Article

Abstract

Intracellular symbiotic dinoflagellates are associated with the tropical scyphozoan Linuche unguiculata (Swartz, 1788) throughout all stages of the host's life cycle. During sexual reproduction, eggs are released in mucus strands that contain symbiotic dinoflagellates. Fertilization and development take place externally in the water column. Epifluorescence and transmission electron microscopy showed that unfertilized eggs did not contain intracellular algae, but that infection of the developing embryo was generally successful by the 128-cell stage (≃10 h after fertilization at 23° C). However, experiments with artificially provided Cellufluor-labeled algae demonstrated that older embryos and planulae could be infected by algae through at least 24 h post-fertilization, indicating that the L. unguiculata symbiosis represents a “semi-closed” system. This novel mode of symbiont acquisition results in most sexually-produced offspring becoming infected with maternally-transmitted algae during early development, but allows for acquisition of non-maternally-provided algae later in development. Most of the algal symbionts during the early stages of embryonic and larval development are located within ectodermal cells. This is in contrast to the other life-cycle stages of L. unguiculata (i.e., scyphistoma, medusa, ephyra), where symbionts are found within the gastrodermis of the host.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Benayahu Y, Achituv Y, Berner T (1988) Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcynocea). Mar Biol 100: 93–101Google Scholar
  2. Benayahu Y, Loya Y (1983) Surface brooding in the Red Sea soft coral, Parerythropodium fulvum fulvum (Forskal, 1997). Biol Bull mar biol Lab, Woods Hole 165: 353–369Google Scholar
  3. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. BioSci 43: 320–326Google Scholar
  4. Colley N, Trench RK (1985) Cellular events in the reestablishment of a symbiosis between a marine dinoflagellate and a coelenterate. Cell Tissue Res 239: 93–103Google Scholar
  5. Conklin EG (1908) The habits and early development of Linerges mercurius. Publs Carnegie Instn 103: 153–170Google Scholar
  6. Costello J, Kremer P (1989) Circadian rhythmicity in the location of zooxanthellae of the scyphomedusa Linuche unguiculata. Mar Ecol Prog Ser 57: 279–286Google Scholar
  7. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2: 129–150Google Scholar
  8. Farrant PA (1985) Reproduction in the temperate Australian soft coral Capnella gaboensis. Proc 5th int coral Reef Congr 5: 314–324 [Gabrie C et al. (eds) Antenne Museum-EPHE, Moorea, French Polynesia]Google Scholar
  9. Hoegh-Guldberg O, McCloskey LR, Muscatine L (1987) Expulsion of zooxanthellae by symbiotic cnidarians from the Red Sea. Coral Reefs 5: 201–204Google Scholar
  10. Kremer P, Costello J, Kremer J, Canino M (1990) Significance of photosynthetic endosymbionts to the carbon budget of the scyphomedusa Linuche unguiculata. Limnol Oceanogr 35: 609–624Google Scholar
  11. Krupp DA (1983) Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2: 159–164Google Scholar
  12. Larson RJ (1992) Riding Langmuir circulations and swimming in circles: a novel form of clustering behavior by the scyphomedusa Linuche unguiculata. Mar Biol 112: 229–235Google Scholar
  13. Mangan J (1909) The entry of zooxanthellae into the ovary of Millepora and some particulars concerning the medusa. Q Jl microsec Sci 33: 697–709Google Scholar
  14. Mayer AG (1910) Medusae of the world. Publs Carnegie Instn 109: 1–735Google Scholar
  15. Ortiz-Corp's E, Cutress CE, Cutress BM (1987) Life history of the coronate scyphozoan Linuche unguiculata (Swartz, 1788). Caribb J Sci 23: 432–443Google Scholar
  16. Rahat M, Adar O (1980) Effect of symbiotic zooxanthellae and temperature on budding and strobilation in Cassiopeia andromeda. Biol Bull mar biol Lab, Woods Hole 159: 394–401Google Scholar
  17. Richmond R (1981) Energetic considerations in the dispersal of Pocillopora damicornis (Linnaeus) planulae. Proc 4th int coral Reef Symp 2: 153–156 [Gomez ED et al. (eds) Marine Sciences, Center University of the Philippines, Quezan City, Philippines]Google Scholar
  18. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science, NY 251: 1348–1351.Google Scholar
  19. Sugiura Y (1963) On the life-history of rhizostome medusae I. Mastigias papua L. Agassiz. Annotnes zool jap 36: 194–202Google Scholar
  20. Spurr A (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31–43Google Scholar
  21. Swartz O (1788) Medusa unguiculata och Actinia pusilla. K svenska VetenskAkad Handl 9: 198–202Google Scholar
  22. Szmant-Froelich A, Yevich P, Pilson MEQ (1980) Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia). Biol Bull mar biol Lab, Woods Hole 158: 257–269Google Scholar
  23. Trench RK (1983) Dinoflagellates in non-parasitic symbioses. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific Publications. Oxford, pp 530–570Google Scholar
  24. Trench RK, Thinh L-v (1995) Gymnodinium linucheae sp. nova the dinoflagellate symbiont of the jellyfish Linuche unguiculata. The J Phycol 30: (in press)Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • M. K. Montgomery
    • 1
  • P. M. Kremer
    • 1
  1. 1.Department of Biological SciencesUniversity of Southern CaliforniaLos AngelesUSA

Personalised recommendations