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Characterization of the zooxanthellate and azooxanthellate morphotypes of the Mediterranean gorgonian Eunicella singularis

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Abstract

The gorgonian Eunicella singularis (Esper, 1794) is abundant on rocky bottoms at Cap de Creus (42°18′49″ N; 003°19′23″ E) in the western Mediterranean, and this study compared zooxanthellate colonies from relatively shallow depths with azooxanthellate colonies living at depths to 60 m. The goal was to determine the taxonomic status of a previously described subspecies, E. singularis aphyta. Sampling at 10-m intervals from 20 to 60 m using scuba or a remotely operated vehicle (ROV) in 2004 and 2010 allowed examination of colony shape, sclerite variability, genetic variability, and the presence/absence of zooxanthellae. Two morphotypes were identified: a shallow morphotype with candelabra-like colonies at 20–30 m has zooxanthellae, while a deep morphotype with more ramified colonies at 40–60 m lacks symbionts. Sclerite differences among colonies were also identified along the depth gradient. The mitochondrial marker msh1 did not discriminate between the two morphotypes and indeed did not discriminate among several Mediterranean species of Eunicella. Other genetic markers will be needed to firmly establish the taxonomic status of the two depth-related morphotypes.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42

    Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ (2005) PERMANOVA: a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, Auckland. http://www.stat.auckland.ac.nz/~mja/Programs.htm

  • Anderson MJ, ter Braak CJF (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comp Sim 73:85–113

    Article  Google Scholar 

  • Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195

    Google Scholar 

  • Bo M, Bavestrello G, Canese S, Giusti M, Salvati E, Angiolillo M, Greco S (2009) Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Mar Ecol Prog Ser 397:53–61

    Article  Google Scholar 

  • Bo M, Bertolino M, Borghini M, Castellano M, Covazzi Harriague A, Di Camillo CG, Gasparini G, Misic C, Povero P, Pusceddu A, Schroeder K, Bavestrello G (2011) Characteristics of the mesophotic megabenthic assemblages of the Vercelli seamount (North Tyrrhenian Sea). PLoS ONE 6:e16357

    Article  CAS  Google Scholar 

  • Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Article  Google Scholar 

  • Brazeau DA, Lasker HR (1988) Inter- and intraspecific variation in gorgonian colony morphology: quantifying branching patterns in arborescent animals. Coral Reefs 7:139–143

    Article  Google Scholar 

  • Calderón I, Garrabou J, Aurelle D (2006) Evaluation of the utility of COI and ITS markers as tools for population genetic studies of temperate gorgonians. J Exp Mar Biol Ecol 336:184–197

    Article  Google Scholar 

  • Carpine C, Grasshoff M (1975) Les gorgonaires de la Méditerranée. Bull Inst Océanogr Monaco 71:1–140

    Google Scholar 

  • Cerrano C, Danovaro R, Gambi C, Pusceddu A, Riva A, Schiaparelli S (2010) Gold coral (Savalia savaglia) and gorgonian forests enhance benthic biodiversity and ecosystem functioning in the mesophotic zone. Biodivers Conserv 19:153–167

    Article  Google Scholar 

  • Einbinder S, Mass T, Brokovich E, Dubinsky Z, Erez J, Tchernov D (2009) Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Mar Ecol Prog Ser 381:167–174

    Article  Google Scholar 

  • Esper EJG (1794) Die pflanzenthiere in abbildungen nach der natur vol 2. Kaspischen Buchhandlung, Nürnberg

  • France SC (2007) Genetic analysis of bamboo corals (Cnidaria: Octocorallia: Isididae). Does lack of colony branching distinguish Lepidisis from Keratoisis? Bull Mar Sci 81:323–333

    Google Scholar 

  • France SC, Hoover LL (2001) Analysis of variation in mitochondrial DNA sequences (ND3, ND4L, MSH) among Octocorallia (= Alcyonaria) (Cnidaria: Anthozoa). Bull Biol Soc Wash 10:110–118

    Google Scholar 

  • Gili JM, Ros J (1985) Study and cartography of the benthic communities of Medes Islands (NE Spain). PSZNI Mar Ecol 6:219–238

    Article  Google Scholar 

  • Gori A, Linares C, Rossi S, Coma R, Gili JM (2007) Spatial variability in reproductive cycle of the gorgonians Paramuricea clavata and Eunicella singularis (Anthozoa, Octocorallia) in the Western Mediterranean Sea. Mar Biol 151:1571–1584

    Article  Google Scholar 

  • Gori A, Rossi S, Berganzo E, Pretus JL, Dale MRT, Gili JM (2011a) Spatial distribution patterns of the gorgonians Eunicella singularis, Paramuricea clavata and Leptogorgia sarmentosa (Cape of Creus, Northwestern Mediterranean Sea). Mar Biol 158:143–158

    Article  Google Scholar 

  • Gori A, Rossi S, Linares C, Berganzo E, Orejas C, Dale MRT, Gili JM (2011b) Size and spatial structure in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Mar Biol 158:1721–1732

    Article  Google Scholar 

  • Grasshoff M (1992) Die Flachwasser-Gorgonarien von Europa und Westafrika (Cnidaria. Anthozoa). Courier Forschunginsiiiui Senckenberg 149:1–135

    Google Scholar 

  • Gutiérrez-Rodríguez C, Hannes AR, Lasker HR (2004) Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Mol Ecol 13:2211–2221

    Article  Google Scholar 

  • Gutiérrez-Rodríguez C, Hannes AR, Lasker HR (2005) Microsatellite variation reveals high levels of genetic variability and population structure in the gorgonian coral Pseudopterogorgia elisabethae across the Bahamas. Corrigendum. Mol Ecol 14:4205–4206

    Article  Google Scholar 

  • Hiscock K (1983) Water movement. In: Earll E, Erwin DG (eds) Sublittoral ecology. The ecology of the shallow sublittoral benthos. Oxford University Press, Oxford, pp 58–96

    Google Scholar 

  • Jeyasuria P, Lewis JC (1987) Mechanical properties of the axial skeleton in gorgonians. Coral Reefs 5:213–219

    Article  Google Scholar 

  • Le Goff-Vitry MC, Pybus OG, Rogers AD (2004) Genetic structure of the deep-sea coral Lophelia pertusa in the northeast Atlantic revealed by microsatellites and internal transcribed spacer sequences. Mol Ecol 13:537–549

    Article  Google Scholar 

  • Lepard A (2003) Analysis of variation in the mitochondrial encoded msh1 in the genus Leptogorgia (Cnidaria: Octocorallia) and implications for population and systematic studies. MS thesis, University of Charleston, Charleston

  • Lewis JC, Von Wallis E (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol Bull 181:275–288

    Article  Google Scholar 

  • Linares C, Coma R, Garrabou J, Díaz D, Zabala M (2008) Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J Appl Ecol 45:688–699

    Article  Google Scholar 

  • Marfenin NN (1997) Adaptation capabilities of marine modular organisms. Hydrobiologia 355:153–158

    Article  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McFadden CS, van Ofwegen LP, Beckman EJ, Benayahu Y, Alderslade P (2009) Molecular systematics of the speciose Indo-Pacific soft coral genus, Sinularia (Anthozoa: Octocorallia). Invertebr Biol 128:303–323

    Article  Google Scholar 

  • McFadden CS, Benayahu Y, Pante E, Thoma JN, Nevarez PA, France SC (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol 11:19–31

    Article  CAS  Google Scholar 

  • Molecular Ecology Resources Primer Development Consortium, Abdoullaye D, Acevedo I, Adebayo AA, Behrmann-Godel J, Benjamin RC, Bock DG, Born C, Brouat C, Caccone A et al (2010) Permanent genetic resources added to molecular ecology resources database 1 August 2009–30 September 2009. Mol Ecol Resourc 10:232–236

    Google Scholar 

  • Muko S, Kawasaki K, Sakai K, Takasu F, Shigesada N (2000) Morphological plasticity in the coral Porites sillimaniani and its adaptive significance. Bull Mar Sci 66:225–239

    Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O’Hara RB (2005) Vegan: community ecology package. Version 1.7-81. http://cran.r-project.org

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051- 07-0. http://www.R-project.org

  • Ribes M, Coma R, Rossi S, Micheli M (2007) Cycle of gonadal development in Eunicella singularis (Cnidaria: Octocorallia): trends in sexual reproduction in gorgonians. Invertebr Biol 126:307–317

    Article  Google Scholar 

  • Rodriguez-Lanetty M, Marquez LM, Losada F (2003) Changes in gorgonian morphology along a depth gradient at Isla Alcatraz, San Sebastian National Park, Venezuela. Bull Mar Sci 72:1019–1023

    Google Scholar 

  • Rossi L (1959) Le specie di Eunicella (Gorgonaria) del Golfo di Genova. Res Ligusticae 118:203–225

    Google Scholar 

  • Rossi S, Gili JM, Garrofé X (2011) Net negative growth detected in a population of Leptogorgia sarmentosa: quantifying the biomass loss in a benthic soft bottom-gravel gorgonian. Mar Biol. doi:10.1007/s00227-011-1675-x

  • Sánchez JA, Aguilar C, Dorado D, Manrique N (2007) Phenotypic plasticity and morphological integration in a marine modular invertebrate. BMC Evol Biol 7:122–130

    Article  Google Scholar 

  • Schols P, Smets E (2001) Carnoy: analysis software for LM, SEM and TEM images. Leuven: distributed by the authors. http://www.carnoy.org

  • Sebens K (1987) The ecology of indeterminate growth in animals. Ann Rev Ecol Syst 18:371–407

    Article  Google Scholar 

  • Shaish L, Abelson A, Rinkevich B (2007) How plastic can phenotypic plasticity be? The branching coral Stylophora pistillata as a model system. PLoS ONE doi:10.1371/journal.pone.0000644

  • Sink KJ, Boshoff W, Samaai T, Timm PG, Kerwath SE (2006) Observations of the habitats and biodiversity of the submarine canyons at Sodwana Bay. S Afr J Sci 102:466–474

    Google Scholar 

  • Skoufas G (2006) Comparative biometry of Eunicella singularis (Gorgonian) sclerites at East Mediterranean Sea (North Aegean Sea, Greece). Mar Biol 149:1365–1370

    Article  Google Scholar 

  • Skoufas G, Poulicek M, Chintiroglou CC (2000) Growth variation of Eunicella singularis (Esper, 1794) (Gorgonacea, Anthozoa). Belg J Zool 130:121–124

    Google Scholar 

  • Smith LW, Barshis D, Birkeland C (2007) Phenotypic plasticity for skeletal growth, density and calcification of Porites lobata in response to habitat type. Coral Reefs 26:559–567

    Article  Google Scholar 

  • Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Am Geophys Union 8:913–920

    Google Scholar 

  • Théodor J (1963) Contribution a l’étude des gorgones (III): Trois formes adaptatives d’Eunicella stricta en fonction de la turbulence et du courant. Vie Milieu 14:815–818

    Google Scholar 

  • Théodor J (1969) Contribution a l’étude des gorgones (VIII): Eunicella stricta aphyta sous-espèce nouvelle sans zooxanthelles proche d’une espèce normalement infestée par ces algues. Vie Milieu 20:635–638

    Google Scholar 

  • Thoma JN, Pante E, Brugler MR, France SC (2009) Deep-sea octocorals and antipatharians show no evidence of seamount-scale endemism in the NW Atlantic. Mar Ecol Prog Ser 397:25–35

    Article  CAS  Google Scholar 

  • Todd PA, Sidle RC, Lewin-Koh NJI (2004) An aquarium experiment for identifying the physical factors inducing morphological change in two massive scleractinian corals. J Exp Mar Biol Ecol 299:97–113

    Article  Google Scholar 

  • van der Ham JL, Brugler MR, France SC (2009) Exploring the utility of an indel-rich, mitochondrial intergenic region as a molecular barcode for bamboo corals (Octocorallia: Isididae). Mar Genomics 2:183–192

    Article  Google Scholar 

  • Velimirov B (1976) Variations in growth forms of Eunicella cavolinii Koch (Octocorallia) related to intensity of water movement. J Exp Mar Biol Ecol 21:109–117

    Article  Google Scholar 

  • Vermeij MJA, Sandin SA, Samhouri JF (2007) Local habitat distribution determines the relative frequency and interbreeding potential for two Caribbean coral morphospecies. Evol Ecol 21:27–47

    Article  Google Scholar 

  • Virgilio M, Airoldi L, Abbiati M (2006) Spatial and temporal variations of assemblages in a Mediterranean coralligenous reef and relationships with surface orientation. Coral Reefs 25:265–272

    Article  Google Scholar 

  • Weinbauer MG, Velimirov B (1995) Morphological variations in the Mediterranean sea fan Eunicella cavolini (Coelenterata: Gorgonacea) in relation to exposure, colony size and colony region. Bull Mar Sci 56:283–295

    Google Scholar 

  • Weinbauer MG, Velimirov B (1998) Comparative morphometry of fan-like colonies of three Mediterranean gorgonians (Cnidaria: Gorgonacea). Cah Biol Mar 39:41–49

    Google Scholar 

  • Weinberg S (1976) Revision of the common Octocorallia of the Mediterranean circalittoral. I. Gorgonacea. Beaufortia 24:63–104

    Google Scholar 

  • Weinberg S, Weinberg F (1979) The life cycle of a gorgonian: Eunicella singularis (Esper, 1794). Bijdr Dierkd 48:127–140

    Google Scholar 

  • West JM, Harvell CD, Walls AM (1993) Morphological plasticity in a gorgonian coral (Briareum asbestinum) over a depth cline. Mar Ecol Prog Ser 94:61–69

    Article  Google Scholar 

  • Whitaker D, Christman (2010) Clustsig: similarity profile analysis. R package version 1.0. http://www.stat.ufl.edu/~whitaker/clustsig/

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Acknowledgments

The authors are grateful for the invaluable assistance of JM Fortuño with the scanning electron miscroscope, of T Garcia, A Olariaga, X Leal, S Ambroso, and J Movilla with field work, of J Sants and A Arias with the CTDs, of the SES Tarragona for their assistance and availability, and of S France (UL Lafayette) for providing laboratory facilities and expertise for sequencing of mitochondrial genes, funded by NOAA’s Office of Ocean Exploration (#NA08OAR4600756) and the NSF project “Assembling the Cnidarian Tree of Life” (grants EF-0531570 to CS McFadden and EF-0531779 to P Cartwright). A Gori was funded by an I3P contract of the Consejo Superior de Investigaciones Cientificas (Ref. I3P-BPD2005), L Bramanti was funded by Marie Curie IEF (Corgard, Project no. 221072), and S Rossi was funded from a Ramón y Cajal Contract (RyC-2007-01327). This work is part of the 2003–2004 INTERREG project between Catalonia-Languedoc Rouissillon “Pirineus Mediterrànis: La muntanya que uneix” of the CSIC and CNRS, and the 2009–2013 European project LIFE + INDEMARES “Inventario y designación de la red natura 2000 en áreas marinas del estado español” (LIFE07/NAT/E/000732) of the European Union.

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Correspondence to Andrea Gori.

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Communicated by J. P. Grassle.

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Online Resource 1 Map of sampling locations in western Mediterranean Sea (JPG 295 kb)

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Online Resource 2 Five degrees of roughness in balloon club heads of Eunicella spp.; completely smooth (1), predominantly smooth but with some peaks (2), almost as smooth as rough (3), completely rough with no pronounced peaks (4), completely rough with pronounced peaks (5) (JPG 2424 kb)

Supplementary material 3 (DOC 25 kb)

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Online Resource 4 Colonies of Eunicella singularis from each depth sampled, Eunicella cavolinii (EC), and Eunicella verrucosa (EV) (JPG 10.1 mb)

Online Resource 5 Balloon clubs from two colonies of Eunicella singularis from 20 m depth (JPG 1.13 mb)

Online Resource 6 Balloon clubs from two colonies of Eunicella singularis from 30 m depth (JPG 937 kb)

Online Resource 7 Balloon clubs from two colonies of Eunicella singularis from 40 m depth (JPG 878 kb)

Online Resource 8 Balloon clubs from two colonies of Eunicella singularis from 50 m depth (JPG 773 kb)

Online Resource 9 Balloon clubs from two colonies of Eunicella singularis from 60 m depth (JPG 509 kb)

Online Resource 10 Balloon clubs from two colonies of Eunicella cavolinii (JPG 789 kb)

Online Resource 11 Balloon clubs from two colonies of Eunicella verrucosa (JPG 620 kb)

Supplementary material 12 (PDF 50 kb)

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Online Resource 13 Histological preparations from colonies of Eunicella singularis fromeach sampled depth; arrows indicate zooxanthellae (JPG 1.87 mb)

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Online Resource 14 Water column characterization at Cap de Creus during study period; grey line represents photosynthetically active radiation (PAR), grey dashed line represents water density, black line represents water temperature, and black dashed line represents salinity (JPG 2.81 mb)

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Gori, A., Bramanti, L., López-González, P. et al. Characterization of the zooxanthellate and azooxanthellate morphotypes of the Mediterranean gorgonian Eunicella singularis . Mar Biol 159, 1485–1496 (2012). https://doi.org/10.1007/s00227-012-1928-3

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