Marine Biology

, 156:1203 | Cite as

Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals

  • Saki Harii
  • Naoko Yasuda
  • Mauricio Rodriguez-Lanetty
  • Takahiro Irie
  • Michio Hidaka
Original Paper

Abstract

The establishment of symbiosis in early developmental stages is important for reef-building corals because of the need for photosynthetically derived nutrition. Corals spawn eggs and sperm, or brood planula larvae and shed them into the water. Some coral eggs or planulae directly inherit symbiotic dinoflagellates (Symbiodinium spp.) from their parents, while others acquire them at each generation. In most species examined to date, the larvae without dinoflagellates (aposymbiotic larvae) can acquire symbionts during the larval stage, but little is known regarding the timing and detailed process of the onset of symbiosis. We examined larval uptake of symbiotic dinoflagellates in nine species of scleractinian corals, the onset of symbiosis through the early larval stages, and the distribution pattern of symbionts within the larval host, while living and with histology, of two acroporid corals under laboratory conditions. The larvae acquired symbiotic dinoflagellates during the planktonic phase in all corals examined which included Acropora digitifera, A. florida, A. intermedia, A. tenuis, Isoporapalifera, Favia pallida, F. lizardensis, Pseudosiderastrea tayamai, and Ctenactis echinata. The larvae of A. digitifera and A. tenuis first acquired symbionts 6 and 5 days after fertilization, respectively. In A. digitifera larvae, this coincided with the formation of an oral pore and coelenteron. The number of symbiotic dinoflagellates increased over the experimental periods in both species. To test the hypothesis that nutrients promotes symbiotic uptake, the number of incorporated dinoflagellates was compared in the presence and absence of homogenized Artemia sp. A likelihood ratio test assuming a log-linear model indicated that Artemia sp. had a significantly positive effect on symbiont acquisition. These results suggest that the acquisition of symbiotic dinoflagellates during larval stages is in common with many coral species, and that the development of both a mouth and coelenteron play important roles in symbiont acquisition.

References

  1. Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116. doi:10.1007/BF00298178 CrossRefGoogle Scholar
  2. Baird AH, Gilmour JP, Kamiki TM, Nonaka M, Pratchett MS, Yamamoto HH, Yamasaki H (2006) Temperature tolerance of symbiotic and non-symbiotic coral larvae. Proc 10th Int Coral Reef Symp 1:38–42Google Scholar
  3. Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  4. Ball EE, Hayward DC, Reece-Hoyes JS, Hislop NR, Samuel G, Saint R, Harrison PL, Miller DJ (2002) Coral development: from classical embryology to molecular control. Int J Dev Biol 46:671–678PubMedGoogle Scholar
  5. Benayahu Y, Achituv Y, Berner T (1988) Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcyonacea). Mar Biol (Berl) 100:93–101. doi:10.1007/BF00392959 CrossRefGoogle Scholar
  6. Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34. doi:10.1016/j.protis.2005.02.004 PubMedCrossRefGoogle Scholar
  7. Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenetic expression of specificity in a cnidarian-algal symbiosis. Mar Ecol Prog Ser 222:85–96. doi:10.3354/meps222085 CrossRefGoogle Scholar
  8. Coffroth MA, Lewis CF, Santos SR, Weaver JL (2006) Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr Biol 16:R985–R987. doi:10.1016/j.cub.2006.10.049 PubMedCrossRefGoogle Scholar
  9. 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 Biol Sci 219:61–82CrossRefGoogle Scholar
  10. Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603. doi:10.1038/sj.hdy.6884550 CrossRefGoogle Scholar
  11. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2:129–150. doi:10.1007/BF00336720 CrossRefGoogle Scholar
  12. Gómez-Cabrera MC, Ortiz JC, Loh WKW, Ward S, Hoegh-Guldberg O (2008) Acquisition of symbiotic dinoflagellates (Symbiodinium) by juveniles of the coral Acropora longicyathus. Coral Reefs 27:219–226. doi:10.1007/s00338-007-0315-x CrossRefGoogle Scholar
  13. Graham EM, Baird AH, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539. doi:10.1007/s00338-008-0361-z CrossRefGoogle Scholar
  14. Harii S, Kayanne H, Takigawa H, Hayashibara T, Yamamoto M (2002) Larval survivorship, competency periods and settlement of two brooding corals, Heliopora coerulea and Pocillopora damicornis. Mar Biol 141:39–46. doi:10.1007/s00227-002-0812-y CrossRefGoogle Scholar
  15. Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis. Mar Ecol Prog Ser 346:89–96. doi:10.3354/meps07114 CrossRefGoogle Scholar
  16. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world 25. Coral reefs. Elsevier, Amsterdam, pp 133–207Google Scholar
  17. Hayashibara T, Shimoike K, Kimura T, Hosaka S, Heyward A, Harrison P, Kudo K, Omori M (1993) Patterns of Coral Spawning at Akajima Island, Okinawa, Japan. Mar Ecol Prog Ser 101:253–262CrossRefGoogle Scholar
  18. 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 2:1231–1236Google Scholar
  19. Hirose M, Yamamoto H, Nonaka M (2008a) Metamorphosis and acquisition of symbiotic algae in planula larvae and primary polyps of Acropora spp. Coral Reefs 27:247–254. doi:10.1007/s00338-007-0330-y CrossRefGoogle Scholar
  20. Hirose M, Reimer JD, Hidaka M, Suda S (2008b) Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar Biol 155:105–112. doi:10.1007/s00227-008-1011-2 CrossRefGoogle Scholar
  21. Jimbo M, Yanohara T, Koike K, Koike K, Sakai R, Muramoto K, Kamiya H (2000) The D-galactose-binding lectin of the octocoral Sinularia lochmodes: characterization and possible relationship to the symbiotic dinoflagellates. Comp Biochem Physiol B Biochem Mol Biol 125:227–236PubMedCrossRefGoogle Scholar
  22. Kasuya E (2004) Angular transformation—another effect of different sample sizes. Ecol Res 19:165–167CrossRefGoogle Scholar
  23. Kitamura M, Koyama T, Nakano Y, Uemura D (2007) Characterization of a natural inducer of coral larval metamorphosis. J Exp Mar Biol Ecol 340:96–102. doi:10.1016/j.jembe.2006.08.012 CrossRefGoogle Scholar
  24. Koike K, Jimbo M, Sakai R, Kaeriyama M, Muramoto K, Ogata T, Maruyama T, Kamiya H (2004) Octocoral chemical signaling selects and controls dinoflagellate symbionts. Biol Bull 207:80–86PubMedCrossRefGoogle Scholar
  25. Kojis BL (1986) Sexual reproduction in Acropora (Isopora) species (Coelenterata: Scleractinia). I. A. cuneata and A. palifera on Heron Island reef, Great Barrier Reef. Mar Biol 91:291–309CrossRefGoogle Scholar
  26. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedCrossRefGoogle Scholar
  27. Littman RA, van Oppen MJH, Willis BL (2009) Methods for sampling free-living Symbiodinium (zooxanthellae) and their distribution and abundance at Lizard Island (Great Barrier Reef). J Exp Mar Biol Ecol. (in press). doi 10.1016/j.jembe.2008.06.034
  28. Loya Y, Sakai K (2008) Bidirectional sex change in mushroom stony corals. Proc R Soc B 275:2335–2343. doi:10.1098/rspb.2008.0675 PubMedCrossRefGoogle Scholar
  29. Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861Google Scholar
  30. Marlow HQ, Martindale MQ (2007) Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evol Dev 9:355–367PubMedGoogle Scholar
  31. Montgomery MK, Kremer PM (1995) Transmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata. Mar Biol 124:147–155CrossRefGoogle Scholar
  32. Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world 25. Coral Reefs. Elsevier, Amsterdam, pp 75–87Google Scholar
  33. Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Mar Ecol Prog Ser 256:87–97CrossRefGoogle Scholar
  34. Nozawa Y, Harrison PL (2005) Temporal settlement patterns of larvae of the broadcast spawning reef coral Favites chinensis and the broadcast spawning and brooding reef coral Goniastrea aspera from Okinawa, Japan. Coral Reefs 24:274–282. doi:10.1007/s00338-005-0476-4 CrossRefGoogle Scholar
  35. Okubo N, Motokawa T (2007) Ernbryogenesis in the reef-building coral Acropora spp. Zool Sci 24:1169–1175. doi:10.2108/zsj.24.1169 PubMedCrossRefGoogle Scholar
  36. Pawitan Y (2001) In all likelihood: statistical modelling and inference using likelihood. Oxford University Press, New York, p 528Google Scholar
  37. Porto I, Granados C, Restrepo JC, Sanchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean Reefs. PLoS ONE 3:e2160PubMedCrossRefGoogle Scholar
  38. Richmond RH (1987) Energetics, competence, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533CrossRefGoogle Scholar
  39. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203CrossRefGoogle Scholar
  40. Rodriguez-Lanetty M, Krupp DA, Weis VM (2004) Distinct ITS types of Symbiodinium in Clade C correlate with cnidarian/dinoflagellate specificity during onset of symbiosis. Mar Ecol Prog Ser 275:97–102CrossRefGoogle Scholar
  41. 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. doi:10.1007/s00227-006-0272-x CrossRefGoogle Scholar
  42. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742PubMedCrossRefGoogle Scholar
  43. Sachs JL, Wilcox TP (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc R Soc B 273:425–429. doi:10.1098/rspb.2005.3346 PubMedCrossRefGoogle Scholar
  44. Schwarz JA, Krupp DA, Weis VM (1999) Late larval development and onset of symbiosis in the scleractinian coral Fungia scutaria. Biol Bull 196:70–79CrossRefGoogle Scholar
  45. Schwarz JA, Weis VM, Potts DC (2002) Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima. Mar Biol 140:471–478. doi:10.1007/s00227-001-0736-y CrossRefGoogle Scholar
  46. van Oppen M (2001) In vitro establishment of symbiosis in Acropora millepora planulae. Coral Reefs 20:200CrossRefGoogle Scholar
  47. Wallace CC (1999) Staghorn corals of the world—a revision of the genus Acropora. CSIRO Publishing, Melbourne, 421 ppGoogle Scholar
  48. Weis VM, Reynolds WS, deBoer MD, Krupp DA (2001) Host-symbiont specificity during onset of symbiosis between the dinoflagellates Symbodinium spp. and planula larvae of the scleractinian coral Fungia scutaria. Coral Reefs 20:301–308. doi:10.1007/s003380100179 CrossRefGoogle Scholar
  49. 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 121:190–201Google Scholar
  50. Wilson JB (2007) Priorities in statistics, the sensitive feet of elephants, and don’t transform data. Folia Geobot 42:161–167CrossRefGoogle Scholar
  51. Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8:1985–1993. doi:10.1111/j.1462-5822.2006.00765.x PubMedCrossRefGoogle Scholar
  52. Yakovleva IM, Baird AH, Yamamoto HH, Bhagooli R, Nonaka M, Hidaka M (2009) Algal symbionts increase oxidative damage and death in coral larvae at high temperature. Mar Ecol Prog Ser (in press)Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Saki Harii
    • 1
  • Naoko Yasuda
    • 1
  • Mauricio Rodriguez-Lanetty
    • 2
  • Takahiro Irie
    • 3
  • Michio Hidaka
    • 4
  1. 1.Graduate School of Engineering and ScienceUniversity of the RyukyusNishiharaJapan
  2. 2.Biology DepartmentThe University of Louisiana at LafayetteLafayetteUSA
  3. 3.Sesoko Station, Tropical Biosphere Research CenterUniversity of the RyukyusMotobuJapan
  4. 4.Department of Chemistry, Biology and Marine Science, Faculty of ScienceUniversity of the RyukyusNishiharaJapan

Personalised recommendations