Abstract
Cladopsammia gracilis (Dendrophylliidae), an ahermatypic coral inhabits the northern Red Sea. Two color morphs (pink and orange) are found aggregated in caves devoid of hermatypic corals, associated with crustose coralline algae (CCA). Sequencing the rDNA ITS region revealed a separate clustering of members of each color morph. Both morphs grow in shallow waters, with orange corals limited to the upper 4 m, while some pink coral aggregates thrive deeper than 30 m. Planulae were released between June and December. Pink planulae treated with antibiotics and exposed at different intervals to CCA, were competent and metamorphosed even 110 days after release. Maximal competency period for orange planulae was 70 days. All planulae were enhanced to metamorphose in presence of CCA. The mean age at metamorphosis of pink and orange planulae treated with CCA differed significantly. Most orange planulae settled directly on the CCA while most pink planulae settled on the wall of the experiment vial. The morphs differed significantly in the calyx cross-section area of primary polyps. Despite being considered a single species according to skeletal based taxonomy, the significant ecological and molecular differences between pink and orange C. gracilis specimens suggest that they may belong to separate species.
Similar content being viewed by others
References
Altieri AH (2003) Settlement cues in the locally dispersing temperate cup coral Balanophyllia elegans. Biol Bull 204:241–245
Andrew NL, Mapstone BD (1987) Sampling and the description of spatial pattern in marine ecology. Oceanogr Mar Biol Ann Rev 25:39–90
Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116
Babcock RC, Baird AH, Piromvaragorn S, Thomson DP, Willis B (2003) Identification of scleractinian coral recruits from Indo-Pacific reefs. Zool Stud 42:211–226
Baird AH, Pratchett MS, Gibson DJ, Koziumi N, Marquis CP (2001) Variable palatability of coral eggs to a planktivorous fish. Mar Freshw Res 52:865–868
Beauchamp KA (1993) Gametogenesis, brooding and planulation in laboratory populations of a temperate scleractinian coral Balanophyllia elegans maintained under contrasting photoperiod regimes. Inver Rep Dev 23:171–182
Cairns SD (1994) Scleractinia of the temperate north Pacific. Smith Cont Zool 557:1–150
Cairns SD (2004) The azooxanthellate Scleractinia (Coelenterata: Anthozoa) of Australia. Rec Aust Mus 56:259–329
Cairns SD, Keller NB (1993) New taxa and distributional records of azooxanthellate Scleractinia from the tropical south-west Indian Ocean, with comments on their zoogeography and ecology. Ann S Afr Mus 103:213–292
Carlon DB, Olson RR (1993) Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals. J Exp Mar Biol Ecol 173:247–263
Chadwick NE (1991) Spatial distribution and the effects of competition on some temperate Scleractinia and Corallimorpharia. Mar Ecol Prog Ser 70:39–48
Coyer JA, Ambrose RF, Engle JM, Carroll JC (1993) Interactions between corals and algae on a temperate zone rocky reef: mediation by sea urchins. J Exp Mar Biol Ecol 167:21–37
Edmonson CH (1929) Growth of Hawaiian corals. Bernice P Bishop Mus Bull 58:1–38
Edmonson CH (1946) Behavior of coral planulae under altered saline and thermal conditions. Occas Pap Berince P Bishop Mus 18:283–304
Fadlallah YH, Pearse JS (1982) Sexual reproduction in solitary corals: overlapping oogenic and brooding cycles, and benthic planulae in Balanophyllia elegans. Mar Biol 71:223–231
Fenner D, Banks K (2004) Orange cup coral Tubastrea coccinea invades Florida and the flower Garden Banks, Northwestern Gulf of Mexico. Coral Reefs 23:505–507
Gerrodette T (1979) Equatorial submergence in a solitary coral Balanophyllia elegans, and the critical life stage excluding the species from shallow water in the south. Mar Ecol Prog Ser 1:227–235
Goffredo S, Zaccanti F (2004) Laboratory observations of larval behavior and metamorphosis in the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae). Bull Mar Sci 74:449–457
Goffredo S, Mezzomonaco L, Zaccanti F (2004) Genetic differentiation among populations of the Mediterranean hermaphroditic brooding coral Balanophyllia europaea (Scleractinia: Dendrophylliidae). Mar Biol 145:1075–1083
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
Harrington L, Fabricius K, De’Ath G, Negri A (2004) Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428–3437
Harrison PL, Babcock RC, Bull GD, Oliver JK, Wallace CC, Willis B (1984) Mass spawning in tropical reef corals. Science 223:1186–1189
Hellberg ME, Taylor MS (2002) Genetic analysis of sexual reproduction in the dendrophylliid coral Balanophyllia elegans. Mar Biol 141:629–637
Imagawa S, Nakano Y, Watanabe T (2004) Molecular analysis of a major soluble egg protein in the scleractinian coral Favites chinensis. Comp Biochem Physiol B-Biochem Molec Biol 137:11–19
Jaeckle WB, Manahan DT (1989) Feeding by a “nonfeeding” larvae: Uptake of dissolved amino acids from seawater by lecitotrophic larvae of the gastropod Haliotis rufescens. Mar Biol 103:87–94
Jenkins SR (2005) Larval habitat selection, not larval supply, determines settlement patterns and adult distribution in two chthamalid barnacles. J Anim Ecol 74:893–904
Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol Syst 24:189–216
Knowlton N (2000) Molecular genetic analysis of species boundaries in the sea. Hydrobiologia 420:73–90
Mackenzie JB, Mundy PL, Willis BL, Miiller DJ, Van Oppen MJH (2004) Unexpected patters of genetic structuring among locations but not colour morphs in Acropora nasuta (Cnidaria; Scleractinia). Mol Ecol 13:9–20
Marshall DJ, Keough MJ (2003) Variation in dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size. Mar Ecol Prog Ser 255:145–153
Miller K, Mundy C (2003) Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22:99–106
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 RT, Hooker N (1994) Morphogen-based chemical flypaper for Agaricia humilis coral larvae. Biol Bull 186:172–181
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Nat Acad Sci USA 76:5269–5273
Neves EG, da Silveira FL (2003) Release of planula larvae, settlement and development of Siderastrea stellata Verrill, 1868 (Anthozoa, Scleractinia). Hydrobiologia 501:139–147
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
Nozawa Y, Harrison PL (2002) Larval settlement patterns, dispersal potential, and the effect of temperature on settlement of larvae of the reef coral, Platygyra daedalea, from the Great Barrier Reef coral. In: Proceedings of the 9th international coral reef symposium, vol 1, pp 409–415
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
Pawlik JR (1992) Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr Mar Biol Ann Rev 30:273–335
Pearce CM, Scheibling RE (1990) Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis, by coralline red algae. Biol Bull 179:304–311
Pechenik JA (1990) Delayed metamorphosis by larvae of benthic marine invertebrates: Does it occur? Is there a price to pay? Ophelia 32:63–94
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Richmond RH (1985) Reversible metamorphosis in coral planula larvae. Mar Ecol Prog Ser 22:181–185
Richmond RH (1987) Energetics, competency, and long—distance dispersal of planulae larvae of the coral Pocillopora damicornis. Mar Biol 93:527–533
Sakai K (1997) Gametogenesis, spawning, and planula brooding by the reef coral Goniastrea aspera (Scleratctinia) in Okinawa, Japan. Mar Ecol Prog Ser 151:67–72
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Schneider S, Roessli D, Excoffier L (2000) A software for population genetics data analysis genetics and biometry laboratory. University of Geneva, Geneva Switzerland
Sebens KP (1983) Settlement and metamorphosis of a temperate soft-coral larvae (Alcyonium siderium Verril) induction by crustose algae. Biol Bull 165:286–304
Sites JW Jr, Marshall JC (2004) Operational criteria for delimiting species. Ann Rev Ecol Syst 35:199–227
Sokal RR, Rohlf JF (1995) Biometry, 3rd edn. Freeman Co, New York
Sullivan KM, Chiappone M (1992) A comparison of belt quadrate and species presence/absence sampling of stony coral (Scleractinia and Milleporina) and sponges for evaluating species patterning on patch reefs of the central Bahamas. Bull Mar Sci 50:464–488
Swofford DL (2000) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4b10. Sinauer Associates, Sunderland
Takabayashi M, Carter DA, Loh WKW, Hoegh-Guldberg O (1998) A coral specific primer for PCR amplification of the internal transcribed spacer region in ribosomal DNA. Mol Ecol 7:925–931
Thompson J, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882
Tranter PRG, Nicholson DN, Kinchington D (1982) A description of spawning and post-gastrula development of the cool temperate coral, Caryophyllia smithi. J Mar Biol Ass UK 62:845–854
Vermeij MJA (2005) Substrate composition and adult distribution determine recruitment patterns in a Caribbean brooding coral. Mar Ecol Prog Ser 295:123–133
Veron JEN (1986) Corals of Australia and the Indo-Pacific. Angus and Robertson Publishers, Australia
Vollmer SV, Palumbi SR (2004) Testing the utility of internally transcribed spacer sequences in coral phylogenetics. Mol Ecol 13:2763–2772
Wei NWV, Wallace CC, Dai CF, Pillay KRM, Chen CA (2006) Analyses of the ribosomal internal transcribed spacers (ITS) and the 5.8S gene indicate that extremely high rDNA heterogeneity is a unique feature in the scleractinian coral genus Acropora (Scleractinia; Acroporidae). Zool Stud 45:404–418
Wellington GM, Trench RK (1985) Persistence and coexistence of a nonsymbiotic coral in an open reef environments. Proc Natl Acad Sci USA 82:2432–2436
Wilson JR, Harrison PL (1998) Settlement-competency periods of larvae of three species of scleractinian corals. Mar Biol 131:339–345
Acknowledgments
We thank Steve Cairns for his help in identifying C. gracilis species. The manuscript benefited from the input given by K. Miller, Y. Nozawa, P. Raimondi, M.J.H. van Oppen and J. Wilson who also shared with us unpublished data. We are also grateful for the assistance and fruitful suggestions of B. Rinkevich, A. Abelson, and especially Y. Barki and M. Fine. The manuscript was much improved by valuable comments made by two reviewers. We acknowledge A. Shoob’s photography, and O. Gillor for underwater assistance and friendship. D. Huchon-Pupko is appreciated for her great help with the phylogenetic analysis. The technical assistance of the staff of the interuniverity institute, Elat, is acknowledged.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by O. Kinne.
Rights and permissions
About this article
Cite this article
Hizi-Degany, N., Meroz-Fine, E., Shefer, S. et al. Tale of two colors: Cladopsammia gracilis (Dendrophylliidae) color morphs distinguished also by their genetics and ecology. Mar Biol 151, 2195–2206 (2007). https://doi.org/10.1007/s00227-007-0653-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-007-0653-9