Coral Reefs

, Volume 30, Issue 4, pp 991–1003 | Cite as

Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations

  • F. CostantiniEmail author
  • S. Rossi
  • E. Pintus
  • C. Cerrano
  • J.-M. Gili
  • M. Abbiati


This study examines the possible effect of depth on the connectivity and genetic variability in red coral (Corallium rubrum; Octocorallia: Alcyonacea) populations. Patterns of genetic structuring along a depth gradient (from 20 to 70 m) were investigated in two locations of the western Mediterranean coast (northern Catalan and eastern Ligurian Seas) using 10 microsatellite loci. Strong patterns of genetic structuring among the samples were found both within and between the two study sites. In both locations, consistent patterns of reduction in genetic variability along the depth gradient were also observed, suggesting that depth has an important role in determining the patterns of genetic structure in Corallium rubrum. Moreover, a threshold in connectivity was observed among the samples collected across 40–50 m depth, supporting the hypothesis that discrete shallow- and deep-water red coral populations occur. This finding has major implications for management strategies and the conservation of commercially exploited deep red coral populations.


Corallium rubrum Depth cline Microsatellites Genetic structuring Conservation Mediterranean Sea 



FC was supported by Postdoctoral Fellowship of the University of Bologna and by Francesca and Luigi Brusarosco grant. SR was financed with a Ramón y Cajal Contract (RyC-2007-01327). Thanks to Fontana G and Bramanti L for their support during the different stages of this study. Thanks to García T and Gori A for collecting samples in Cap de Creus. ‘Portofino Divers’ help during the deep sampling in Portofino. The comments made by the Topic Editor Dr. Gates and two anonymous reviewers greatly improved the manuscript.


  1. Abbiati M, Buffoni G, Caforio G, Di Cola G, Santangelo G (1992) Harvesting, predation and competition effects on a red coral population. J Sea Res 30:219–228CrossRefGoogle Scholar
  2. Abbiati M, Santangelo G, Novelli S (1993) Genetic variation within and between two Tyrrhenian populations of the Mediterranean alcyonarian Corallium rubrum. Mar Ecol Prog Ser 95:245–250CrossRefGoogle Scholar
  3. Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337PubMedCrossRefGoogle Scholar
  4. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  5. Baco AR, Shank TM (2005) Population genetic structure of the Hawaiian precious coral Corallium lauuense (Octocorallia: Coralliidae) using microsatellites. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Springer-Verlag, Berlin, pp 663–678CrossRefGoogle Scholar
  6. Baco AR, Clark AM, Shank TM (2006) Six microsatellite loci from the deep-sea coral Corallium lauuense (Octocorallia: Coralliidae) from the islands and seamounts of the Hawaiian archipelago. Mol Ecol Notes 6:147–149CrossRefGoogle Scholar
  7. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  8. Bavestrello G, Cerrano C, Cattaneo-Vietti R (2010) Biological interactions affecting the growth rates of red coral (Corallium rubrum) colonies. In: Bussoletti E, Cottingham D, Bruckner A, Roberts G (eds) Proceedings of the international workshop on red coral science, management, and trade: lessons from the Mediterranean. Napoli, September 23–26, 2009, pp 151–158Google Scholar
  9. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568PubMedCrossRefGoogle Scholar
  10. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, MontpellierGoogle Scholar
  11. Bellwood DR, Hughes TP, Folke C, Nystroem M (2004) Confronting the coral reef crisis. Nature 429:827–833PubMedCrossRefGoogle Scholar
  12. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate–a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  13. Bongaerts P, Riginos C, Ridgway T, Sampayo EM, van Oppen MJH, et al. (2010) Genetic divergence across habitats in the widespread coral Seriatopora hystrix and its associated Symbiodinium. PLoS ONE 5(5): e10871. doi: 10.1371/journal.pone.0010871
  14. Bradshaw CJA, Isagi Y, Kaneko S, Brook BW, Bowman DMJS, Frankham R (2007) Low genetic diversity in the bottlenecked population of endangered non-native banteng in northern Australia. Mol Ecol 16:2998–3008PubMedCrossRefGoogle Scholar
  15. Bramanti L, Magagnini G, De Maio L, Santangelo G (2005) Recruitment, early survival and growth of the Mediterranean red coral Corallium rubrum (L 1758), a 4-year study. J Exp Mar Biol Ecol 314:69–78CrossRefGoogle Scholar
  16. Bramanti L, Rossi S, Tsounis G, Gili JM, Santangelo G (2007) Recruitment and early survival of red coral on settlement plates: some clues for demography and restoration. Hydrobiologia 580:219–224CrossRefGoogle Scholar
  17. Bramanti L, Iannelli M, Santangelo G (2009) Mathematical modelling for conservation and management of gorgonians corals: youngs and olds, could they coexist? Ecol Model 220:2851–2856CrossRefGoogle Scholar
  18. Carlon DB, Budd AF (2002) Incipient speciation across a depth gradient in a scleractinian coral? Evolution 56:2227–2242PubMedGoogle Scholar
  19. Cattaneo Vietti R, Albertelli G, Aliani S, Bava S, Bavestrello G, Benedetti Cecchi L, Bianchi CN, Bozzo E, Capello M, Castellano M, Cerrano C, Cutroneo L, Diviacco G, Fabiano M, Faimali M, Ferrari M, Gasparini GP, Locritani M, Mangialajo L, Marin V, Moreno M, Morri C, Orsi Relini L, Pane L, Paoli C, Petrillo M, Povero P, Pronzato R, Relini G, Santangelo G, Tucci S, Tunesi L, Vacchi M, Vassallo P, Vezzulli L, Wurtz M (2010) The Ligurian Sea: present status, problems and perspectives. Chem Ecol 26:319–340CrossRefGoogle Scholar
  20. Cerrano C, Bavestrello G (2008) Medium-term effects of die-off of rocky benthos in the Ligurian Sea. What can we learn from gorgonians? Chem Ecol 24:1–10CrossRefGoogle Scholar
  21. Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean). Ecol Lett 3:284–293CrossRefGoogle Scholar
  22. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  23. Costantini F, Abbiati M (2006) Development of microsatellite markers for the Mediterranean gorgonian coral Corallium rubrum. Mol Ecol Notes 6:521–523CrossRefGoogle Scholar
  24. Costantini F, Fauvelot C, Abbiati M (2007a) Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences. Mol Ecol 16:5168–5182PubMedCrossRefGoogle Scholar
  25. Costantini F, Fauvelot C, Abbiati M (2007b) Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effects of larval dispersal. Mar Ecol Prog Ser 340:100–119CrossRefGoogle Scholar
  26. Costantini F, Taviani M, Remia A, Pintus E, Shembri PJ, Abbiati M (2010) Live colonies of Corallium rubrum from the Mediterranean deep-sea: a preliminary genetic characterisation. Mar Ecol 31:261–269CrossRefGoogle Scholar
  27. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38Google Scholar
  28. 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 381:167–174CrossRefGoogle Scholar
  29. Etter RJ, Rex MA, Chase MR et al (2005) Population differentiation decreases with depth in deep-sea bivalves. Evolution 59:1479–1491PubMedGoogle Scholar
  30. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  31. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567CrossRefGoogle Scholar
  32. Eytan RI, Hayes M, Arbour-Reily P, Miller M, Hellberg ME (2009) Nuclear sequences reveal mid-range isolation of an imperilled deep-water coral population. Mol Ecol 18:2375–2389PubMedCrossRefGoogle Scholar
  33. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  34. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  35. Freiwald A, Beuck L, Rüggeberg A, Taviani M, Hebbeln D and R/V Meteor M70-1 Participants (2009) The white coral community in the Central Mediterranean Sea revealed by ROV surveys. Oceanography 22:58–57Google Scholar
  36. Garrabou J, Ballesteros E, Zabala M (2002) Structure and dynamics of North-Western Mediterranean rocky benthic communities along a depth gradient. Estuar Coast Shelf Sci 55:493–508CrossRefGoogle Scholar
  37. Garrabou J, Coma R, Bensoussan N, Bally M, Chevaldonne P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, Ledoux JB, Lejeusne C, Linares C, Marschal C, Perez T, Ribes M, Romano JC, Serrano E, Teixido N, Torrents O, Zabala M, Zuberer F, Cerrano C (2009) Mass mortality in North western Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biol 15:1090–1103CrossRefGoogle Scholar
  38. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  39. Gori A, Rossi S, Berganzo-González E, Pretus JL, Dale MRT, Gili JM (2011) Spatial distribution, abundance and relationship with environmental variables of the gorgonians Eunicella singularis, Paramuricea clavata and Leptogorgia sarmentosa (Cape of Creus, Northwestern Mediterranean Sea). Mar Biol 158:143–158CrossRefGoogle Scholar
  40. Goudet J, Raymond M, de Meeüs T et al (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  41. Harland AD, Davies PS, Fixter LM (1992) Lipid content of some Caribbean corals in relation to depth and light. Mar Biol 113:357–361CrossRefGoogle Scholar
  42. Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BL (2000) Supply-side ecology works both ways: the link between benthic adults, fecundity, and larval recruits. Ecology 81:2241–2249CrossRefGoogle Scholar
  43. Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623PubMedCrossRefGoogle Scholar
  44. Kalinowski ST (2005) hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  45. Ledoux JB, Mokhtar-Jamaï K, Roby C, Féral JP, Garrabou J, Aurelle D (2010a) Genetic survey of shallow populations of the Mediterranean red coral Corallium rubrum (Linnaeus, 1758): new insights into evolutionary processes shaping nuclear diversity and implications for conservation. Mol Ecol 19:675–690PubMedCrossRefGoogle Scholar
  46. Ledoux JB, Garrabou J, Bianchimani O, Drap P, Féral JP, Aurelle D (2010b) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol 19:4204–4216Google Scholar
  47. Mantel NA (1967) The detection of disease clustering and a generalised regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  48. Marchetti R (1965) Ricerche sul corallo rosso della costa ligure e toscana. Distribuzione geografica. Rend Its Lomb Sci Lett B 99:255–278Google Scholar
  49. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  50. NOAA (2010) Proceedings of the international workshop on red coral science, management, and trade: Lessons from the Mediterranean. NOAA Technical memorandum CRCP-13. Silver Spring, MD, p 233Google Scholar
  51. Palumbi S (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S158CrossRefGoogle Scholar
  52. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  53. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  54. Rossi S, Gili JM (2005) Temporal variation and composition of near-bottom seston features in a Mediterranean coastal area. Estuar Coast Shelf Sci 65:385–395CrossRefGoogle Scholar
  55. Rossi S, Tsounis G, Orejas C, Padrón T, Gili JM, Bramanti L, Teixidó N, Gutt J (2008) Survey of deep-dwelling red coral (Corallium rubrum) populations at Cap de Creus (NW Mediterranean). Mar Biol 54:533–545CrossRefGoogle Scholar
  56. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  57. Santangelo G, Abbiati M (2001) Red coral: conservation and management of an over-exploited Mediterranean species. Aquatic Conserv Mar Freshw Ecosyst 11:253–259CrossRefGoogle Scholar
  58. Santangelo G, Carlietti E, Maggi E, Bramanti L (2003) Reproduction and population sexual structure of the overexploited Mediterranean red coral Corallium rubrum. Mar Ecol Progr Ser 248:99–108CrossRefGoogle Scholar
  59. Santangelo G, Bramanti L, Iannelli M (2007) Population dynamics and conservation biology of the over-exploited Mediterranean red coral. J Theor Biol 244:416–423PubMedCrossRefGoogle Scholar
  60. Tsounis G, Rossi S, Gili JM, Arntz WE (2006a) Population structure of an exploited benthic cnidarian: The case study of red coral (Corallium rubrum L.). Mar Biol 149:1059–1070CrossRefGoogle Scholar
  61. Tsounis G, Rossi S, Aranguren M, Gili JM, Arntz WE (2006b) Effects of spatial variability and colony size on the reproductive output and gonadal development cycle of the Mediterranean red coral (Corallium rubrum L.). Mar Biol 148:513–527CrossRefGoogle Scholar
  62. Tsounis G, Rossi S, Gili JM, Arntz WE (2007) Red coral fishery at the Costa Brava (NW Mediterranean): Case study of an overharvested precious coral. Ecosystems 10:975–986CrossRefGoogle Scholar
  63. Tsounis G, Rossi S, Grigg R, Santangelo G, Bramanti L, Gili JM (2010) The exploitation and conservation of precious corals. Oceanogr Mar Biol Annu Rev 48:161–211CrossRefGoogle Scholar
  64. Vermeij MJA, Bak RPM (2003) Species-specific population structure of closely related coral morphospecies along a depth gradient (5–60 m) over a Caribbean reef slope. Bull Mar Sci 73:725–744Google Scholar
  65. Vielmini I, Bramanti L, Tsounis G, Rossi S, Gili JM, Cattaneo-Vietti R, Santangelo G (2010) Determination of Corallium rubrum population age structure. In: Bussoletti E, Cottingham D, Bruckner A, Roberts G (eds) Proceedings of the International workshop on red coral science, management, and trade: lessons from the Mediterranean. Napoli, September 23–26, 2009, pp 179–182Google Scholar
  66. Vighi M (1972) Etude sur la reproduction du Corallium rubrum. Vie et Milieu 23:21–32Google Scholar
  67. 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 25:265–272CrossRefGoogle Scholar
  68. Weersing KA, Toonen RJ (2009) Population genetics, larval dispersal, and demographic connectivity in marine systems. Mar Ecol Prog Ser 393:1–12CrossRefGoogle Scholar
  69. Weinberg S (1979) The light dependent behaviour of planula larvae of Eunicella singularis and Corallium rubrum and its implication for octocorallian ecology. Bijdr Dierkd 49:145–151Google Scholar
  70. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • F. Costantini
    • 1
    Email author
  • S. Rossi
    • 2
  • E. Pintus
    • 1
  • C. Cerrano
    • 3
  • J.-M. Gili
    • 4
  • M. Abbiati
    • 1
  1. 1.Centro Interdipartimentale di Ricerca per le Scienze Ambientali and Dipartimento di Biologia Evoluzionistica SperimentaleUniversity of BolognaRavennaItaly
  2. 2.Institut de Ciència i Tecnologia AmbientalsUniversitat Autònoma de Barcelona, UABCerdanyola del VallésSpain
  3. 3.Dipartimento per lo Studio del Territorio e delle sue Risorse, Corso Europa 26Università di GenovaGenovaItaly
  4. 4.Institut de Ciències del Mar (CSIC)BarcelonaSpain

Personalised recommendations