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

Marine Biology

Volumn 159, Issue 7, 2012, Pages 1485-1496

  Gori, Andrea ^a   Bramanti, Lorenzo ^a   López González, Pablo ^b   Thoma, Jana N ^c   Gili, Josep Maria ^a   Grinyó, Jordi ^a   Uceira, Vanessa ^a   Rossi, Sergio ^d  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

^d INSTITUT DE CIÈNCIA I TECNOLOGIA AMBIENTALS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GENETIC MARKER; GENETIC VARIATION; MORPHOTYPE; REMOTELY OPERATED VEHICLE; SAMPLING; SUBSPECIES; TAXONOMY; ZOOXANTHELLA;

CAP DE CREUS; CATALONIA; GERONA [CATALONIA]; MEDITERRANEAN SEA; MEDITERRANEAN SEA (WEST); SPAIN;

EUNICELLA; EUNICELLA SINGULARIS; GORGONIA;

EID: 84862693182     PISSN: 00253162     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00227-012-1928-3     Document Type: Article

References (66)

1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11: 36-42.
2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
3. 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.
4. Anderson MJ, ter Braak CJF (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comp Sim 73: 85-113.
5. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44: 123-195.
6. 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.
7. 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.
8. 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.
9. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13: 115-155.
10. Brazeau DA, Lasker HR (1988) Inter- and intraspecific variation in gorgonian colony morphology: quantifying branching patterns in arborescent animals. Coral Reefs 7: 139-143.
11. 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.
12. Carpine C, Grasshoff M (1975) Les gorgonaires de la Méditerranée. Bull Inst Océanogr Monaco 71: 1-140.
13. 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.
14. 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.
15. Esper EJG (1794) Die pflanzenthiere in abbildungen nach der natur vol 2. Kaspischen Buchhandlung, Nürnberg.
16. 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.
17. 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.
18. Gili JM, Ros J (1985) Study and cartography of the benthic communities of Medes Islands (NE Spain). PSZNI Mar Ecol 6: 219-238.
19. 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.
20. 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.
21. 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.
22. Grasshoff M (1992) Die Flachwasser-Gorgonarien von Europa und Westafrika (Cnidaria. Anthozoa). Courier Forschunginsiiiui Senckenberg 149: 1-135.
23. 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.
24. 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.
25. 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.
26. Jeyasuria P, Lewis JC (1987) Mechanical properties of the axial skeleton in gorgonians. Coral Reefs 5: 213-219.
27. 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.
28. 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.
29. Lewis JC, Von Wallis E (1991) The function of surface sclerites in gorgonians (Coelenterata, Octocorallia). Biol Bull 181: 275-288.
30. 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.
31. Marfenin NN (1997) Adaptation capabilities of marine modular organisms. Hydrobiologia 355: 153-158.
32. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290-297.
33. 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.
34. 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.
35. 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.
36. 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.
37. Oksanen J, Kindt R, Legendre P, O'Hara RB (2005) Vegan: community ecology package. Version 1. 7-81. http://cran. r-project. org.
38. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290.
39. 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.
40. 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.
41. 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.
42. Rossi L (1959) Le specie di Eunicella (Gorgonaria) del Golfo di Genova. Res Ligusticae 118: 203-225.
43. 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.
44. 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.
45. Schols P, Smets E (2001) Carnoy: analysis software for LM, SEM and TEM images. Leuven: distributed by the authors. http://www. carnoy. org.
46. Sebens K (1987) The ecology of indeterminate growth in animals. Ann Rev Ecol Syst 18: 371-407.
47. 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.
48. 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.
49. Skoufas G (2006) Comparative biometry of Eunicella singularis (Gorgonian) sclerites at East Mediterranean Sea (North Aegean Sea, Greece). Mar Biol 149: 1365-1370.
50. Skoufas G, Poulicek M, Chintiroglou CC (2000) Growth variation of Eunicella singularis (Esper, 1794) (Gorgonacea, Anthozoa). Belg J Zool 130: 121-124.
51. 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.
52. Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Am Geophys Union 8: 913-920.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. Weinbauer MG, Velimirov B (1998) Comparative morphometry of fan-like colonies of three Mediterranean gorgonians (Cnidaria: Gorgonacea). Cah Biol Mar 39: 41-49.
63. Weinberg S (1976) Revision of the common Octocorallia of the Mediterranean circalittoral. I. Gorgonacea. Beaufortia 24: 63-104.
64. Weinberg S, Weinberg F (1979) The life cycle of a gorgonian: Eunicella singularis (Esper, 1794). Bijdr Dierkd 48: 127-140.
65. 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.
66. Whitaker D, Christman (2010) Clustsig: similarity profile analysis. R package version 1. 0. http://www. stat. ufl. edu/~whitaker/clustsig/.