Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals

Abstract

Two distinct modes of algal endosymbiont acquisition exist in corals, a direct transmission from the parental colony to the eggs and a larval or post-larval uptake from the environment. The former, maternal-transmission mode is expected to be a more closed system, while the latter is believed to be an open system. Here we test the hypothesis that the diversity of symbionts in closed systems is lower than that in open systems. We examine the identity and diversity of the algal endosymbionts (zooxanthellae) in 25 Montipora species sampled from Irian Jaya (Indonesia) and Magnetic Island (central Great Barrier Reef) and compare the results with those previously obtained from Acropora species, which belong to the same family. All Montipora colonies examined harbour clade C zooxanthellae, with two colonies harbouring both clade C and D zooxanthellae simultaneously. Two algal strains (named C· and D· in this study) present in Montipora have not been observed in Acropora, and may have co-evolved with Montipora. Symbiodinium C· shows approximately 5% sequence divergence from C strains observed in Acropora spp. and occurs in 76% of the colonies examined. Nevertheless, several other C strains commonly found in other corals occur in some of the Montipora colonies. Montipora species transmit their algal endosymbionts directly to the eggs, while Acropora species have to acquire zooxanthellae from the environment every generation. Contrary to our expectations, the diversity of zooxanthellae is similar for the two genera, indicating that the mode of symbiont transmission (i.e. maternal versus horizontal) does not affect symbiont diversity in acroporid corals.

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

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

References

  1. Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116

  2. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawning of 105 coral species on the Great Barrier Reef. Mar Biol 90:379–394

  3. Baker AC (2001) Reefs corals bleach to survive change. Nature 411:765–766

  4. Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two Caribbean acroporid corals. Proc 8th Int Coral Reef Symp 2:1295–1300

  5. Brown BE (1996) Coral bleaching: Causes and consequences. Coral Reefs 16:129–138

  6. Buddemeier RW, Fautin DG (1993) Coral bleaching as an adaptive mechanism. Bioscience 43:320–326

  7. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the World: Coral Reefs. Elsevier, Amsterdam, pp 133–207

  8. Heyward AJ (1986) Sexual reproduction in five species of the coral Montipora. In: Jokiel PL, Richmond RH, Rogers RA (eds) Coral reef population biology. Sea Grant Cooperative Report, Hawaii University, pp 170–178

  9. Hirose M, Kinzie RAI, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280

  10. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

  11. Hunter CL, Morden CW, Smith CM (1997) The utility of ITS sequences in assessing relationships among zooxanthellae and corals. Proc 8th Int Coral Reef Symp 2:1599–1602

  12. Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175

  13. LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a "species level" marker. J Phycol 37:866–880

  14. Lobban CS, Schefter M, Simpson AGB, Pochon X, Pawlowski J, Foissner W (2002) Maristentor dinoferus n. gen., n. sp., a giant heterotrich ciliate (Spirotrichea: Heterotrichida) with zooxanthellae, from coral reefs on Guam, Mariana Islands. Mar Biol 141:207–208

  15. Loh WK, Loi T, Carter D, Hoegh-Guldberg O (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar Ecol Prog Ser 222:97–107

  16. Oppen MJH van, Palstra FP, Piquet AT, Miller DJ (2001) Patterns of coral-dinoflagellate associations in Acropora: significance of local availability and physiology of Symbiodinium strains and host-symbiont selectivity. Proc R Soc Lond B Biol Sci 268:1759–1767

  17. Oppen MJH van, Koolmees EM, Veron JEN (2003) Patterns of evolution in the scleractinian coral genus Montipora (Acroporidae). Mar Biol DOI 10.1007/s00227-003-1188-3

  18. Pawlowski J, Holzmann M, Fahrni JF, Pochon X, Lee JJ (2001) Molecular identification of algal endosymbionts in large miliolid foraminifera. 2. Dinoflagellates. J Eukaryot Microbiol 48:368–373

  19. Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139:1069–1078

  20. Posada D, Crandall KA (1998) Modeltest: Testing the model of DNA substitution. Bioinformatics 14:817–818

  21. Rodriguez-Lanetty M (2003) Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA. Mol Phylogenet Evol (in press)

  22. Rodriguez-Lanetty M, Hoegh-Guldberg O (2002) Genetic variability of Symbiodinium-like dinoflagellates associated with the widespread scleractinian coral, Plesiastrea versipora within the north western Pacific. GenBank sequences AY186560, AY186564, AY186565, AY186568, AY186570 and AY186571

  23. Rodriguez-Lanetty M, Loh W, Carter D, Hoegh-Guldberg O (2001) Latitudinal variability in symbiont specificity within the widespread scleractinian coral Plesiastrea versipora. Mar Biol 138:1175–1181

  24. Rodriguez-Lanetty M, Chang SJ, Cha HR, Song JI (2002) Specificity of two anthozoans-dinoflagellates associations in the western Pacific Ocean. GenBank sequence AY186628

  25. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351

  26. Rowan R, Knowlton N, Baker A, Jara J (1997) Landscape ecology of algal symbionts creates variation in episodes of coral bleaching. Nature 388:265–269

  27. Sambrook J, Fritch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, New York

  28. Sier CJS, Olive PJW (1994) Reproduction and reproductive variability in the coral Pocillopora verrucosa from the Republic of Maldives. Mar Biol 118:713–722

  29. Swofford DL (1999) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer, Sunderland, Mass.

  30. Takabayashi M, Carter D, Loh W, Hoegh-Guldberg O (1998) A coral-specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Mol Ecol 7:928–930

  31. Thompson JN (1999) The evolution of species interactions. Science 284:2116–2118

  32. Trench RK (1993) Microalgal-invertebrate symbioses: A review. Endocytobiosis Cell Res 9:135–175

  33. Veron JEN (2000) Corals of the world. Australian Institute of Marine Science, Townsville

  34. Veron JEN, Wallace CC (1984) Scleractinia of Eastern Australia. Part 5. Acroporidae. Aust Inst Mar Sci Monogr Ser 6:1–485

Download references

Acknowledgements

I thank Charlie Veron for collection of the Indonesian samples and identification of all samples, David Miller for allowing me to undertake a large part of this study in his laboratory at James Cook University (Townsville, Australia), and Melissa Schubert and Lesa Peplow for their contribution to gathering the data. This study was funded by the Australian Research Council and the Australian Institute of Marine Science.

Author information

Correspondence to Madeleine J. H. van Oppen.

Additional information

Communicated by M.S. Johnson, Crawley

Rights and permissions

Reprints and Permissions

About this article

Cite this article

van Oppen, M.J.H. Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Marine Biology 144, 1–7 (2004). https://doi.org/10.1007/s00227-003-1187-4

Download citation

Keywords

  • Great Barrier Reef
  • Algal Symbiont
  • Acropora Species
  • Acroporid Coral
  • Algal Endosymbiont