Marine Biology

, Volume 81, Issue 1, pp 9–17 | Cite as

The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and molluscs with zooxanthellae

  • W. K. Fitt


Symbiotic dinoflagellates, Symbiodinium microadriaticum (=zooxanthellae), may gain access to aposymbiotic hosts (i.e., those lacking zooxanthellae) by chemosensory attraction of the motile algae by the potential host or via an “intermediate” host. Laboratory experiments showed that motile zooxanthellae were attracted to intact aposymbiotic host animals, but not to starved symbiotic hosts. Fed symbiotic hosts and brine shrimp (Artemia sp.) nauplii also attracted motile zooxanthellae. The attraction of these zooxanthellae was directly correlated with nitrogen levels in the seawater surrounding the hosts; thus ammonia and possibly nitrate could be atractants. Brine shrimp nauplii, acting as “intermediate” hosts actively ingested both motile and non-motile zooxanthellae. the ingested zooxanthellae tended to remain morphologically unaltered during and after passage through the gut of the brine shrimp. Capture and ingestion of brine shrimp containing zooxanthellae by aposymbiotic scyphistomae of the jellyfish Cassiopeia xamachana led to infection of the scyphistomae with zooxanthellae. Zooxanthellae isolated from 17 different species of coelenterates and molluscs could be transferred via brine shrimp to the endodermal cells of the scyphistomae. However only 10 of these isolates persisted to establish a permanent association with C. xamachana. Scyphistomae in suspensions of motile zooxanthellae responded by a classical coelenterate feeding response, which may facilitate ingestion of the potential symbionts and establishment of a symbiosis.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Abe, N.: Post-larval development of the coral Fungia aciniformis var. palawensis Doderlein. Palao trop. biol. Stn Stud. 1, 73–93 (1937)Google Scholar
  2. Adler, J.: A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J. gen. Microbiol. 74, 77–91 (1973)Google Scholar
  3. Atoda, K.: The larva and postlarval development of some reef-building corals I. Pocillopora damacornis cespitosa (Dana). Sci. Rep. Tôhoku Univ. 18, 24–47 (1947a)Google Scholar
  4. Atoda, K.: The larva and postlarval development of some reef-building corals II. Stylophora pistillata (Esper). Sci. Rep. Tôhoku Univ. 18, 48–64 (1947b)Google Scholar
  5. Atoda, K.: The larva and postlarval development of the reef-building corals III. Acropora bruggemanni. J. Morph. 89, 1–13 (1951a)Google Scholar
  6. Atoda, K.: The larva and postlarval development of the reef-building corals IV. Galaxea aspera Quelch. J. Morph. 89, 17–30 (1951b)Google Scholar
  7. Atoda, K.: The larva and postlarval development of some reef-building corals V. Seriatopora hystrix Dana. Sci. Rep. Tôhoku Univ. (Ser. 4) 19, 33–39 (1951c)Google Scholar
  8. Atoda, K.: Post larval development of the sea anemone, Anthopleura sp. Sci. Rep. Tôhoku Univ. (Ser. 4) 20, 274–288 (1954)Google Scholar
  9. Bigelow, R. P.: The anatomy and development of Cassiopea xamachana. Mem. Boston Soc. nat. Hist. 5, 191–236 (1904)Google Scholar
  10. Cates, N. and J. J. A. McLaughlin: Differences of ammonia metabolism in symbiotic and aposymbiotic Condylactis and Cassiopea spp. J. exp. mar. Biol. Ecol. 21, 1–5 (1976)Google Scholar
  11. Colley, C. J. and R. K. Trench: Selectivity in phagocytosis and persistence of symbiotic algae in the scyphistomae stage of the jellyfish Cassiopeia xamachana. Proc. R. Soc. (Ser. B) 219, 61–82 (1983)Google Scholar
  12. David, C. N.: A quantitative method for maceration of Hydra tissue. Wilhelm Roux Arch. EntwMech. Org. 171, 259–268 (1973)Google Scholar
  13. D'Elia, C. F., S. L. Domotor and K. L. Webb: Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar. Biol. 75, 157–167 (1983)Google Scholar
  14. Duerden, J. E.: West Indian madreporarean polyps. Mem. natn. Acad. Sci. 7, 403–597 (1902)Google Scholar
  15. Edmundson, E. H.: Growth of Hawaiian corals. Bull. Bernice P. Bishop Mus. 58, 1–38 (1929)Google Scholar
  16. Epp, R. W. and W. M. Lewis, Jr.: Photosynthesis in copepods. Science, N.Y. 214, 1349–1350 (1981)Google Scholar
  17. Eppley, R. W.: Nitrate uptake. In: Handbook of phycological methods. Vol. 2. pp 401–411. Ed. by J. A. Hellebust and J. S. Craigie. Cambridge: Cambridge University Press 1978Google Scholar
  18. Fankboner, P. V. and R. E. Reid: Mass expulsion of zooxanthellae by heat-stressed corals: a source of food for giant clams? Experientia 37, 251–252 (1981)Google Scholar
  19. Faure, C.: Étude des phenomenes de reproduction chez Aglaophenia pluma (L.). Cah. Biol. mar. 1, 185–204 (1960)Google Scholar
  20. Fitt, W. K.: Chemosensory response of the symbiotic dinoflagellate Symbiodinium microadriaticum J. Phycol. (In press). (1984)Google Scholar
  21. Fitt, W. K., S. S. Chang and R. K. Trench: Motility patterns of different strains of the symbiotic dinoflagellate Symbiodinium (=Gymnodinium) microadriaticum Freudenthal in culture. Bull. mar. Sci. 31, 436–443 (1981)Google Scholar
  22. Fitt, W. K., C. R. Fisher and R. K. Trench: Larval biology of tridacnid clams. Aquaculture, Amsterdam (In press). (1984)Google Scholar
  23. Fitt, W. K. and R. K. Trench. Spawning, development, and acquisition of “zooxanthellae” by Tridacna squamosa (Mollusca, Bivalvia). Biol. Bull. mar. biol. Lab., Woods Hole 161, 213–235 (1981)Google Scholar
  24. Fitt, W. K. and R. K. Trench: The relation of diel patterns of cell division to diel patterns of motility in the symbiotic dinoflagellate Symbiodinium microadriaticum freudenthal in culture. New Phytol. 94, 421–432 (1983a)Google Scholar
  25. Fitt, W. K. and R. K. Trench: Endocytosis of the symbiotic dinoflagellate Symbiodinium microadriaticum Freudenthal by endodern cells of the scyphistomae of Cassiopeia xamachana and resistance to host digestion. J. Cell Sci. 64, 195–212 (1983b)Google Scholar
  26. Fraser, E. A.: Observations on the life-history and development of the hydroid Myrionema amboinense. Scient. Rep. Gt Barrier Reef Exped. 3, 135–144 (1931)Google Scholar
  27. Freudenthal, H. D.: Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: taxonomy, life cycle, and morphology. J. Protozool. 9, 45–52 (1962)Google Scholar
  28. Gibor, A.: Some ecological relationships between phyto- and zooplankton. Biol. Bull. mar. biol. Lab., Woods Hole 111, 230–234 (1956)Google Scholar
  29. Gohar, H. A. F.: Studies on the Xeniidae of the Red Sea, their ecology, physiology, taxonomy and phylogeny. Publs mar. biol. Stn Ghardaqa 2, 24–118 (1940)Google Scholar
  30. Gohar, H. A. F. and A. M. Eisawy: The development of Cassiopea andromeda (Scyphomedusae). Publs mar. biol. Stn Ghardaqa 11, 148–190 (1960)Google Scholar
  31. Goreau, T. F.: Mass expulsion of zooxanthellae from Jamaican reef communities after Hurricane Flora. Science, N.Y. 145, 383–386 (1964)Google Scholar
  32. Jaap, W. C.: Observations on zooxanthellae expulsion at middle Sambo Reef, Florida Keys. Bull. mar. Sci. 29, 414–422 (1979)Google Scholar
  33. Jameson, S. C.: Early life history of the giant clams Tridacna crocea Lamarck, Tridacna maxima (Poding) and Hippopus hippopus (Linnaeus). Pacif. Sci. 30, 219–233 (1976)Google Scholar
  34. Kawaguti, S.: On the physiology of reef corals. V. Tropisms of coral planulae, considered as a factor of distribution of the reefs. Palao trop. biol. Stn Stud. 2, 319–328 (1941)Google Scholar
  35. Kawaguti, S.: Observations of the heart shell, Corculum cardissa (L.), and its associated zooxanthellae. Pacif. Sci. 4, 43–49 (1950)Google Scholar
  36. Kinzie, R. A., III: Experimental infection of aposymbiotic gorgonian polyps with zooxanthellae. J. exp. mar. Biol. Ecol. 15, 335–345 (1974)Google Scholar
  37. Kojis, B. L. and N. J. Quinn: Aspects of sexual reproduction and larval development in the shallow water hermatypic coral, Goniastrea australensis (Edwards and Haime, 1857). Bull. mar. Sci. 31, 558–573 (1981a)Google Scholar
  38. Kojis, B. L. and N. J. Quinn: Reproductive strategies in four species of Porites (Scleractinia). Proc. 4th int. Symp coral Reefs 2, 145–151 (1981b). (Ed. by E. D. Gomez et al. Quezon City: Marine Sciences Centre of the Philippines)Google Scholar
  39. Kojis, B. L. and N. J. Quinn: Reproductive ecology of two favid corals (Coelenterata: Scleractinia). Mar. Ecol. Prog. Ser. 8, 251–255 (1982)Google Scholar
  40. Krupp, D.: Sexual reproduction and early development of the solitary coral, Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2, 159–164 (1983)Google Scholar
  41. LaBarbera, M.: Larval and post larval development of the giant clams Tridacna maxima and Tridacna squamosa (Bivalvia: Tridacnidae). Malacologia 15, 69–79 (1975)Google Scholar
  42. Liddicoat, M. I., S. Tibbits and E. Butler: The determination of ammonia in seawater. Limnol. Oceanogr. 20, 131–132 (1975)Google Scholar
  43. Loeblich, A. R., III and J. L. Sherley: Observations on the theca of the motile phase of free-living and symbiotic isolates of Zooxanthella microadriatica (Freudenthal) comb. nov. J. mar. biol. Ass. U.K. 59, 195–205 (1979)Google Scholar
  44. Ludwig, L. D.: Die Zooxanthellen bei Cassiopea andromeda Eschscholtz 1829 (Polyp-Stadium) und ihre Bedeutung für die Strobilation. Zool. Jb. (Abt. Anat. Ont. Tiere) 86, 238–277 (1969)Google Scholar
  45. Mangan, J.: The entry of zooxanthellae into the ovary of Millipora and some particulars concerning the medusa. Q. Jl microse. Sci. 33, 697–709 (1909)Google Scholar
  46. Marshall, S. and T. A. Stephenson: The feeding of reef animals. I. The corals. Scient. Rep. Gt Barrier Reef Exped. 3, 219–245 (1933)Google Scholar
  47. McLaughlin, J. J. A. and P. A. Zahl: Endozoic algae. In: Symbiosis. Vol. 1, pp 257–297. Ed. by S. M. Henry. New York: Academic Press 1966Google Scholar
  48. McMurrich, J.: Contributions on the morphology of the Actinozoa II. On the development of the Hexactiniae. J. Morph. 4, 303–330 (1891)Google Scholar
  49. Muscatine, L.: Nutrition of corals. In: Biology and geology of coral reefs, Vol. II. pp 77–115. Ed. by O. A. Jones and R. Endean. New York: Academic Press 1973Google Scholar
  50. Muscatine, L. and C. F. D'Elia: The uptake, retention, and release of ammonium by reef corals. Limnol. Oceanogr. 23, 225–234 (1978)Google Scholar
  51. Muscatine, L., H. Masuda and R. Burnap: Ammonium uptake by symbiotic and aposymbiotic reef corals. Bull. mar. Sci. 29, 572–575 (1979)Google Scholar
  52. Pearse, V. B.: Modification of sea anemone behavior by symbiotic zooxanthellae: phototaxis. Biol. Bull. mar. biol. Lab., Woods Hole 147, 630–640 (1974)Google Scholar
  53. Porter, K. G.: Enhancement of algal growth and productivity by grazing zooplankton. Science N.Y. 192, 1332–1333 (1976)Google Scholar
  54. Provasoli, L., T. Yamasu and I. Manton: Experiments on the resynthesis of symbiosis in Convoluta roscoffensis with different flagellate cultures. J. mar. biol. Ass. U.K. 48, 465–479 (1968)Google Scholar
  55. Reimer, A. A.: Observation on the relationships between several species of tropical zoanthids (Zoanthidae, Coelenterata) and their zooxanthellae. J. exp. mar. Biol. Ecol. 7, 207–214 (1971)Google Scholar
  56. Siebert, A. E.: A description of the embryology, larval development, and feeding of the sea anemones Anthopleura elegantissima and A. xanthogramica. Can. J. Zool. 52, 1383–1388 (1974)Google Scholar
  57. Steele, R. D.: Stages in the life history of a symbiotic zooxanthella in pellets extruded by its host Aiptasia tagetes (Duch. and Mich.) (Coelenterata, Anthozoa). Biol. Bull. mar. biol. Lab., Woods Hole 149, 590–600 (1975)Google Scholar
  58. Steele, R. D.: Light intensity as a factor int he regulation of the density of symbiotic zooxanthellae in Aiptasia tagetes (Coelenterata, Anthozoa). J. Zool., Lond. 179, 387–405 (1976)Google Scholar
  59. Steele, R. D.: The significance of zooxanthella-containing pellets extruded by sea anemones. Bull. mar. Sci. 27, 591–594 (1977)Google Scholar
  60. Stephenson, T. A.: Development and the formation of colonies in Pocillopora and Porites. I. Scient. Rep. Gt Barrier Reef Exped. 3, 247–272 (1934)Google Scholar
  61. Sugiura, Y.: On the life-history of rhizostome medusae. I. mastigias papua L. Agassiz. Annotnes zool. jap. 36, 194–202 (1963)Google Scholar
  62. Sugiura, Y.: On the life-history of rhizostome medusae. II. Indispensability of zooxanthellae for strobilation in Mastigas papua. Embryologia 8, 223–233 (1964)Google Scholar
  63. Szmant-Froelich, A., P. Yevich and M. E. Q. Pilson: Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia). Biol. Bull. mar. biol. Lab., Woods Hole 158, 257–269 (1980)Google Scholar
  64. Taylor, D. L.: The cellular interactions of algal-invertebrate symbiosis. Adv. mar. Biol. 11, 1–56 (1973)Google Scholar
  65. Taylor, F. J. R.: Possible free-living Symbiodinium microadriaticum (Dinophyceae) in tide pools in Southern Thailand. In: Endocytobiology, Vol. II. pp 1009–1014. Ed. H. E. A. Schenk and W. Schwemmler. Berlin: de Gruyter 1983Google Scholar
  66. Theodor, J.: Contribution a l'étude des gorgones (VIII): Eunicella stricta aphyta sous-espèce nouvelle sans zooxanthelles, proche d'une espèce normalement infestée par ces algues. Vie Milieu 20, 635–638 (1969)Google Scholar
  67. Trench, R. K.: Nutritional potentials in Zoanthus sociathus (Coelenterata, Anthozoa). Helgoländer wiss. Meeresunters. 26, 174–216 (1974)Google Scholar
  68. Trench, R. K.: The cell biology of plant-animal symbiosis. A. Rev. Pl. Physiol. 30, 485–532 (1979)Google Scholar
  69. Trench, R. K., N. J. Colley and W. K. Fitt: Recognition phenomena in symbioses between marine invertebrates and “zooxanthelae”; uptake, sequestration and persistence. Ber. dt. bot. Ges. 94, 568–577 (1981)Google Scholar
  70. Wilkerson, F. P. and L. Muscatine: Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone. Proc. R. Soc. (In press). (1984)Google Scholar

Copyright information

© Springer-verlag 1984

Authors and Affiliations

  • W. K. Fitt
    • 1
    • 2
  1. 1.Department of Biological SciencesUniversity of California at Santa BarbaraSanta BarbaraUSA
  2. 2.Marine Science InstituteUniversity of California at Santa BarbaraSanta BarbaraUSA

Personalised recommendations