Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

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, Isopora palifera, 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.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116. doi:https://doi.org/10.1007/BF00298178

    Article  Google Scholar 

  • 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 1:38–42

    Google Scholar 

  • Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

    Article  Google Scholar 

  • 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 46:671–678

    CAS  PubMed  Google Scholar 

  • 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:https://doi.org/10.1007/BF00392959

    Article  Google Scholar 

  • Coffroth MA, Santos SR (2005) Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 156:19–34. doi:https://doi.org/10.1016/j.protis.2005.02.004

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.3354/meps222085

    Article  Google Scholar 

  • 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:https://doi.org/10.1016/j.cub.2006.10.049

    Article  CAS  Google Scholar 

  • 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 219:61–82

    Article  CAS  Google Scholar 

  • Douglas AE (1998) Host benefit and the evolution of specialization in symbiosis. Heredity 81:599–603. doi:https://doi.org/10.1038/sj.hdy.6884550

    Article  Google Scholar 

  • Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2:129–150. doi:https://doi.org/10.1007/BF00336720

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/s00338-007-0315-x

    Article  Google Scholar 

  • Graham EM, Baird AH, Connolly SR (2008) Survival dynamics of scleractinian coral larvae and implications for dispersal. Coral Reefs 27:529–539. doi:https://doi.org/10.1007/s00338-008-0361-z

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/s00227-002-0812-y

    Article  Google Scholar 

  • 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:https://doi.org/10.3354/meps07114

    Article  CAS  Google Scholar 

  • 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 133–207

    Google Scholar 

  • 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 101:253–262

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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:https://doi.org/10.1007/s00338-007-0330-y

    Article  Google Scholar 

  • 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:https://doi.org/10.1007/s00227-008-1011-2

    Article  Google Scholar 

  • 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 125:227–236

    Article  CAS  Google Scholar 

  • Kasuya E (2004) Angular transformation—another effect of different sample sizes. Ecol Res 19:165–167

    Article  Google Scholar 

  • 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:https://doi.org/10.1016/j.jembe.2006.08.012

    Article  Google Scholar 

  • 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 207:80–86

    Article  CAS  Google Scholar 

  • 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 91:291–309

    Article  Google Scholar 

  • Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    Article  CAS  Google Scholar 

  • 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 https://doi.org/10.1016/j.jembe.2008.06.034

    Article  Google Scholar 

  • Loya Y, Sakai K (2008) Bidirectional sex change in mushroom stony corals. Proc R Soc B 275:2335–2343. doi:https://doi.org/10.1098/rspb.2008.0675

    Article  Google Scholar 

  • Manning MM, Gates RD (2008) Diversity in populations of free-living Symbiodinium from a Caribbean and Pacific reef. Limnol Oceanogr 53:1853–1861

    Article  Google Scholar 

  • Marlow HQ, Martindale MQ (2007) Embryonic development in two species of scleractinian coral embryos: Symbiodinium localization and mode of gastrulation. Evol Dev 9:355–367

    Article  Google Scholar 

  • Montgomery MK, Kremer PM (1995) Transmission of symbiotic dinoflagellates through the sexual cycle of the host scyphozoan Linuche unguiculata. Mar Biol 124:147–155

    Article  Google Scholar 

  • 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 75–87

    Google Scholar 

  • 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 256:87–97

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s00338-005-0476-4

    Article  Google Scholar 

  • Okubo N, Motokawa T (2007) Ernbryogenesis in the reef-building coral Acropora spp. Zool Sci 24:1169–1175. doi:https://doi.org/10.2108/zsj.24.1169

    Article  Google Scholar 

  • Pawitan Y (2001) In all likelihood: statistical modelling and inference using likelihood. Oxford University Press, New York, p 528

    Google Scholar 

  • Porto I, Granados C, Restrepo JC, Sanchez JA (2008) Macroalgal-associated dinoflagellates belonging to the genus Symbiodinium in Caribbean Reefs. PLoS ONE 3:e2160

    Article  Google Scholar 

  • Richmond RH (1987) Energetics, competence, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533

    Article  Google Scholar 

  • 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 60:185–203

    Article  Google Scholar 

  • 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 275:97–102

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s00227-006-0272-x

    Article  Google Scholar 

  • Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742

    Article  CAS  Google Scholar 

  • Sachs JL, Wilcox TP (2006) A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc R Soc B 273:425–429. doi:https://doi.org/10.1098/rspb.2005.3346

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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:https://doi.org/10.1007/s00227-001-0736-y

    Article  Google Scholar 

  • van Oppen M (2001) In vitro establishment of symbiosis in Acropora millepora planulae. Coral Reefs 20:200

    Article  Google Scholar 

  • Wallace CC (1999) Staghorn corals of the world—a revision of the genus Acropora. CSIRO Publishing, Melbourne, 421 pp

    Google Scholar 

  • 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:https://doi.org/10.1007/s003380100179

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wilson JB (2007) Priorities in statistics, the sensitive feet of elephants, and don’t transform data. Folia Geobot 42:161–167

    Article  Google Scholar 

  • 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:https://doi.org/10.1111/j.1462-5822.2006.00765.x

    Article  CAS  Google Scholar 

  • 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)

Download references

Acknowledgments

We thank the staff of the Sesoko Station of the Tropical Biosphere Research Center, University of the Ryukyus, for providing research facilities. We also thank Kenji Iwao, Masaya Morita, Akira Iguchi, Yossi Loya, Takeshi Hayashibara, Naoko Isomura, Hironobu Fukami, Nami Okubo, Makoto Kitamura, Kenji Iwai and staff of Okinawa Churaumi Aquarium for providing samples. We are also grateful to Mamiko Hirose for valuable suggestions regarding histological observations and the reviewers who helped to improve this manuscript. This research was funded by the 21st Century Center of Excellence (COE) program of the University of the Ryukyus, a Ministry of Education, Culture, Sports, Science and Technology Grant-in-Aid for Young Scientists (B) No. 20770017 (SH), and the Australian Research Council Centre of Excellence for Coral Reef Studies at the University of Queensland.

Author information

Authors and Affiliations

  1. Graduate School of Engineering and Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    Saki Harii & Naoko Yasuda

  2. Biology Department, The University of Louisiana at Lafayette, Lafayette, LA, 70504, USA

    Mauricio Rodriguez-Lanetty

  3. Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, 3422 Sesoko, Motobu, Okinawa, 905-0227, Japan

    Takahiro Irie

  4. Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    Michio Hidaka

Authors
  1. Saki Harii
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naoko Yasuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mauricio Rodriguez-Lanetty
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takahiro Irie
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michio Hidaka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Saki Harii.

Additional information

Communicated by M. Kühl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harii, S., Yasuda, N., Rodriguez-Lanetty, M. et al. Onset of symbiosis and distribution patterns of symbiotic dinoflagellates in the larvae of scleractinian corals. Mar Biol 156, 1203–1212 (2009). https://doi.org/10.1007/s00227-009-1162-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1162-9

Keywords

Search

Navigation