Abstract
Coral planulae settle, then metamorphose and form polyps. This study examined the morphological process of metamorphosis from planulae into primary polyps in the scleractinian corals Acropora nobilis and Acropora microphthalma, using the cnidarian neuropeptide Hym-248. These two species release eggs that do not contain Symbiodinium. The mode of acquisition of freshly isolated Symbiodinium (zooxanthellae) (FIZ) by the non-symbiotic polyp was also examined. Non-Hym-248 treated swimming Acropora planulae did not develop blastopore, mesenteries or coelenteron until the induction of metamorphosis 16 days after fertilization. The oral pore was formed by invagination of the epidermal layer after formation of the coelenteron in metamorphosing polyps. At 3 days after settlement and metamorphosis, primary polyps exposed to FIZ established symbioses with the Symbiodinium. Two–four days after exposure to FIZ, the distribution of Symbiodinium was limited to the gastrodermis of the pharynx and basal part of the polyps. Eight–ten days after exposure to FIZ, Symbiodinium were present in gastrodermal cells throughout the polyps.
References
Ambariyanto, Hoegh-Guldberg O (1997) Effect of nutrient enrichment in the field on the biomass, growth and calcification of the giant clam Tridacna maxima. Mar Biol 129:635–642
Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116
Benayahu Y, Achituv Y, Berner T (1988) Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcyonacea). Mar Biol 100:93–101
Cervino JM, Hayes RL, Honovich M, Goreau TJ, Jones S, Rubec PJ (2003) Changes in zooxanthellae density, morphology, and mitotic index in hermatypic corals and anemones exposed to cyanide. Mar Pollut Bull 46:573–586
Fitt WK, Cook CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Mar Biol 139:507–517
Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs, ecosystem of the world 25. Elsevier, Amsterdam, pp 133–207
Hayashibara T, Ohike S, Kakinuma Y (1997) Embryonic and larval development and planula metamorphosis of four gamete-spawning Acropora (Anthozoa, Scleractinia). Proc 8th Int Coral Reef Symp 2:1231–1236
Heyward AJ, Negri AP (1999) Natural inducers for coral larval metamorphosis. Coral Reefs 18:273–279
Hirose M, Hidaka M (2006) Early development of zooxanthella-containing eggs of the corals Porites cylindrica and Montipora digitata: the endodermal localization of zooxanthellae. Zool Sci 23:873–881
Hirose M, Kinzie III 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
Isomura N, Nishihira M (2001) Size variation of planulae and its effect on the lifetime of planulae in three pocilloporied corals. Coral Reefs 20:309–315
Iwao K, Fujisawa T, Hatta M (2002) A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21:127–129
Jones RJ, Yellowlees D (1997) Regulation and control of intracellular algae (=zooxanthellae) in hard corals. Phil Trans R Soc Lond B 352:457–468
Krupp DA (1983) Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2:159–164
Lesser MP (1997) Oxidative stress cause coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192
Maruyama T, Heslinga GA (1997) Fecal discharge of zooxanthellae in the giant clam Tridacna derasa, with reference to their in situ growth rate. Mar Biol 127:473–477
Mate JL, Wilson J, Field S, Neves EG (1998) Fertilization dynamics and larval development of the scleractinian coral Montipora verrucosa in Hawai’i. In: Cox EF, Krupp DA, Jokiel PL (eds) Reproduction in reef corals. Hawaii Institute of Marine Biology, Kaneohe, Technical report 42, pp 27–39
Morse ANC, Iwao K, Baba M, Shimoike K, Hayashibara T, Omori M (1996) An ancient chemosensory mechanism brings new life to coral reefs. Biol Bull 191:149–154
Morse DE, Hooker N, Morse ANC, Jensen RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193–217
Morse DE, Morse ANC, Raimondi PT, Hooker N (1994) Morphogen-based chemical flypaper for Agaricia humilis coral larvae. Biol Bull 186:172–181
Muscatine L, Pool RR (1979) Regulation of numbers of intracellular algae. Proc R Soc Lond B 204:131–139
Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1351
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
Smith GJ, Muscatine L (1999) Cell cycle of symbiotic dinoflagellates: variation in G1 phase-duration with anemone nutritional status and macronutrient supply in the Aiptasia pulchella-Symbiodinium pulchroroum symbiosis. Mar Biol 134:405–418
Szmant-Froelich AM, Yevich P, Pilson MQ (1980) Gametogenesis and early development of the temperate coral Astrangia danae (Anthozoa: Scleractinia). Biol Bull 158:257–269
Szmant-Froelich A, Reutter M, Riggs L (1985) Sexual reproduction of Favia fragum (Esper): Lunar patters of gametogenesis, embryogenesis and planulation in Puerto Rico. Bull Mar Sci 37:880–892
Titlyanov EA, Titlyanova TV, Kalita TL, Yakovleva IM (2004) Rhythmicity in division and degradation of zooxanthellae in the hermatypic coral Stylophora pistillata. Symbiosis 36:211–224
Tomascik T, Sander F (1987) Effects of eutrophication on reef-building corals III. Reproduction of reef-building coral Porites porites. Mar Biol 94:77–94
van Oppen M (2001) In vitro establishment of symbiosis in Acropora millepora planulae. Coral Reefs 20:200
Veron JEN, Wallace CC (1984) Scleractinia of Eastern Australia. Part 5. Family Acroporidae. Aust Inst Mar Sci Monogr 6:1–422
Webster NS, Smith LD, Heyward AJ, Watts JE, Webb RI, Blackall LL, Negri AP (2004) Metamorphosis of a scleractinian coral in response to microbial biofilms. Appl Environ Microbiol 70:1213–1221
Wilkerson FP, Kobayashi D, Muscatine L (1988) Mitotic index and size of symbiotic algae in Caribbean Reefs corals. Coral Reefs 7:29–36
Yuyama I, Hayakawa H, Endo H, Iwao K, Takeyama H, Maruyama T, Watanabe T (2005) Identification of symbiotically expressed coral mRNAs using a model infection system. Biochem Biophys Res Commun 336:793–798
Acknowledgments
The authors thank Dr. S. Uchida and the staff of the Okinawa Churaumi Aquarium (Motobu, Okinawa) for assistance with gamete fertilization. The authors also thank the staff of Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus (Motobu, Okinawa), where parts of this study were conducted. The authors appreciate the advice and help of Dr. E. Hirose. The authors also appreciate Dr. J.D. Reimer for helpful suggestions for the manuscript. This study was partly supported by the Twenty-first century COE Program of the University of the Ryukyus.
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
Hirose, M., Yamamoto, H. & Nonaka, M. Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp.. Coral Reefs 27, 247–254 (2008). https://doi.org/10.1007/s00338-007-0330-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-007-0330-y