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

Marine Biology - Tập 159 - Trang 1485-1496 - 2012
Andrea Gori1, Lorenzo Bramanti1, Pablo López-González2, Jana N. Thoma3, Josep-Maria Gili1, Jordi Grinyó1, Vanessa Uceira1, Sergio Rossi4
1Institut de Ciències del Mar, Consejo Superior de Investigaciónes Cientificas, Barcelona, Spain
2Facultad de Biología, Universidad de Sevilla, Sevilla, Spain
3Department of Biology, University of Louisiana at Lafayette, Lafayette, USA
4Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Barcelona, Spain

Tóm tắt

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.

Tài liệu tham khảo

Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42 Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46 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 Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195 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 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 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 Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155 Brazeau DA, Lasker HR (1988) Inter- and intraspecific variation in gorgonian colony morphology: quantifying branching patterns in arborescent animals. Coral Reefs 7:139–143 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 Carpine C, Grasshoff M (1975) Les gorgonaires de la Méditerranée. Bull Inst Océanogr Monaco 71:1–140 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 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 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 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 Gili JM, Ros J (1985) Study and cartography of the benthic communities of Medes Islands (NE Spain). PSZNI Mar Ecol 6:219–238 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 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 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 Grasshoff M (1992) Die Flachwasser-Gorgonarien von Europa und Westafrika (Cnidaria. Anthozoa). Courier Forschunginsiiiui Senckenberg 149:1–135 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 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 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 Jeyasuria P, Lewis JC (1987) Mechanical properties of the axial skeleton in gorgonians. Coral Reefs 5:213–219 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 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 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 Marfenin NN (1997) Adaptation capabilities of marine modular organisms. Hydrobiologia 355:153–158 McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297 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 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 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 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 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 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 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 Rossi L (1959) Le specie di Eunicella (Gorgonaria) del Golfo di Genova. Res Ligusticae 118:203–225 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 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 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 Skoufas G (2006) Comparative biometry of Eunicella singularis (Gorgonian) sclerites at East Mediterranean Sea (North Aegean Sea, Greece). Mar Biol 149:1365–1370 Skoufas G, Poulicek M, Chintiroglou CC (2000) Growth variation of Eunicella singularis (Esper, 1794) (Gorgonacea, Anthozoa). Belg J Zool 130:121–124 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 Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Am Geophys Union 8:913–920 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 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 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 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 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 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 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 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 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 Weinbauer MG, Velimirov B (1998) Comparative morphometry of fan-like colonies of three Mediterranean gorgonians (Cnidaria: Gorgonacea). Cah Biol Mar 39:41–49 Weinberg S (1976) Revision of the common Octocorallia of the Mediterranean circalittoral. I. Gorgonacea. Beaufortia 24:63–104 Weinberg S, Weinberg F (1979) The life cycle of a gorgonian: Eunicella singularis (Esper, 1794). Bijdr Dierkd 48:127–140 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 Whitaker D, Christman (2010) Clustsig: similarity profile analysis. R package version 1.0. http://www.stat.ufl.edu/~whitaker/clustsig/