Abstract
In adult cnidarians, symbiotic dinoflagellate Symbiodinium are usually located in the gastrodermis. However, the onset of this endosymbiotic association and its regulation during larval development are unclear. This study examined the distribution of the Symbiodinium population in tissue layers of planula larvae released from the stony coral Euphyllia glabrescens. Symbiodinium were redistributed from the epidermis to the gastrodermis, at a rate that was fastest during early planulation and then decreased prior to metamorphosis. This process indicates that the endosymbiotic activity of coral tissues is developmentally regulated. During the early larval stage, both the epidermis and gastrodermis contained Symbiodinium; then, as the larvae developed toward metamorphosis, the numbers in the epidermis gradually diminished until they were only found in the gastrodermis. The mechanism of redistribution remains unknown, but may be due to a direct translocation and/or change in the proliferation of symbionts in different tissue layers.
References
Benayahu Y, Schleyer MH (1998) Reproduction in Anthelia glauca (Octocorallia: Xeniidae). II. Transmission of algal symbionts during planular brooding. Mar Biol 131:433–442
Benayahu Y, Achituv Y, Brener T (1988) Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcyonacea). Mar Biol 100:93–101
Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta 1760:1690–1695
Colley NJ, Trench RK (1983) Selectivity in phagocytosis and persistence of symbiotic algae by the scyphistoma stage of the jellyfish Cassiopeia xamachana. Proc R Soc Lond B 219:61–82
Davy SK, Turner JR (2003) Early development and acquisition of zooxanthellae in the temperate symbiotic sea anemone Anthopleura ballii (Cocks). Biol Bull 205:66–72
Dove SG (2004) Scleractinian corals with photoprotective host pigments are hypersensitive to thermal bleaching. Mar Ecol Prog Ser 272:99–116
Fan TY, Li JJ, Ie SX, Fang LS (2002) Lunar periodicity of larval release by pocilloporid corals in southern Taiwan. Zool Stud 41:288–294
Fautin DG, Mariscal RN (1991) Cnidaria: Anthozoa. In: Harrison FW, Westfall JA (eds) Microscopic anatomy of invertebrates. Cnidaria: Anthozoa, vol 2. Wiley-Liss, New York, pp 267–358
Fitt WK (1984) The role of chemosensory behavior of Symbiodinium microadriaticum, intermediate hosts, and host behavior in the infection of coelenterates and mollusks with zooxanthellae. Mar Biol 81:9–17
Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky-Winters E, Mc Laughlin SM, Meteyer CU, Morado JF, Nicholson JH, Parnell PG, Peters EC, Reynolds TL, Rotstein DS, Sileo L, Woodley CM (2006) A report of the CDHC coral histopathology workshop II. National Oceanic and Atmospheric Administration, Silver Spring
Hirose M, Hidaka M (2006) Early development of zooxanthellae-containing eggs of the corals Porites cylindrica and Montipora digitata: the endodermal localization of zooxanthellae. Zool Sci 23:873–881
Hirose M, Kinzie RA, Hidaka M (2000) Early development of zooxanthella-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae. Biol Bull 199:68–75
Hirose M, Kinzie RA, Hidaka M (2001) Timing and process of entry of zooxanthellae into oocytes of hermatypic corals. Coral Reefs 20:273–280
Lin KH (2005) Timing of larval release by fire corals in southern Taiwan: seasonality, lunar and diurnal periodicity. M.Sc. thesis, National Sun Yat-Sen University, p 50
Montgomery MK, Kremer PM (1995) Transmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata. Mar Biol 124:147–155
Rodriguez-Lanetty M, Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Temporal and spatial infection dynamics indicate recognition events in the early hours of a dinoflagellate/coral symbiosis. Mar Biol 149:713–719
Salih A, Larkum A, Cox G, Kuhl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853
Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196:70–79
Szmant-Froelich AM, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892
van Oppen MJH (2004) Mode of zooxanthella transmission does not affect zooxanthella diversity in acroporid corals. Mar Biol 144:1–7
Weis VM, Verde EA, Pribyl A, Schwarz JA (2002) Aspects of the larval biology of the sea anemones Anthopleura elegantissima and A. artemisia. Invertebr Biol 121:190–201
Acknowledgments
This work was supported by grants from the National Science Council (NSC 95-2311-B-291-003-MY2, NSC 93-2311-B-291-003 and NSC 94-2311-B-291-003) and by intramural funding from the National Museum of Marine Biology and Aquarium. We thank Dr T.-H. Chen for the consultation on data analysis. Constructive comments on the manuscript from three anonymous reviewers and the editor are greatly appreciated.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor M.P. Lesser.
Rights and permissions
About this article
Cite this article
Huang, HJ., Wang, LH., Chen, WN.U. et al. Developmentally regulated localization of endosymbiotic dinoflagellates in different tissue layers of coral larvae. Coral Reefs 27, 365–372 (2008). https://doi.org/10.1007/s00338-007-0337-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-007-0337-4