, Volume 784, Issue 1, pp 211–224 | Cite as

Does historical harvesting affect colony size distribution and genetic diversity in Corallium rubrum (Linnaeus, 1758)? Evidences from the Southern Mediterranean commercial banks

  • Sabri JaziriEmail author
  • Federica CostantiniEmail author
  • Luca Rugiu
  • Marco Abbiati
  • Othman Jarboui
Primary Research Paper


The precious octocoral Corallium rubrum has a long history of exploitation in the Mediterranean Sea. Historically, harvesting followed the “boom and bust” cycles whereby newly discovered beds were overexploited to depletion. In the past, most of the red coral harvesting came form France, Italy, and Spain. Today, landing data show that Tunisia is the third largest supplier of C. rubrum. The aim of this study was to asses whether and how the exploitation effort affects size distribution and genetic diversity of Tunisian commercial populations. Biometric data and microsatellite markers were used to characterize 113 colonies collected on nine commercial banks. Size and branching pattern indicate that collected colonies are up to 100 years old with a high reproductive rate. Nevertheless, 38% of the colonies were undersized according to FAO-GFCM recommendations (basal diameter <7 mm). Tunisian populations showed a weak genetic structuring and significant differentiation between coastal and offshore populations. Harvesting did not alter the structure of red coral populations. However, technological improvement and intensive harvesting of Tunisian banks, if not properly managed, may lead to their rapid depletion, causing long-lasting shifts in population demography and genetic structure, and the loss of this valuable resource.


Red coral Management Tunisia Population genetics Connectivity Colony size 



This study was carried out in the framework of a cooperation agreement between stakeholders in the red coral fisheries: researchers, administration, and fishermen (UTAP, divers, traders, and ship-owners). A special thanks to all of them. We declare no conflicts of interest. Sabri JAZIRI was supported by a Ph.D grant from the Tunisian Ministry of Agriculture, Institution for Agricultural Research and Higher Education, and National Institute of Marine Sciences and Technologies. This study was also supported by the PRIN 2011 project on “Coastal bioconstructions: structure, function and management,” Ministero dell’Ambiente e della Tutela del Territorio e del Mare (Project 2010, Studio di popolazioni di Corallo rosso profondo), and Ministero delle Politiche Agricole, Alimentari e Forestali (Project 2012, Use of ROV in the management of deep C. rubrum populations). We are also greatly thankful to Dr. J.X.W. Wong and two anonymous reviewers for their constructive suggestions, which greatly improved the quality of the manuscript.


  1. Abbiati, M., S. Novelli, J. G. Harmelin & G. Santangelo, 1997. Struttura genetica di popolamenti simpatrici e allopatrici di corallo rosso. Biologia e tutela del corallo rosso e di altri ottocoralli del Mediterraneo. Ministero delle politiche agricole, Rome: 5–21.Google Scholar
  2. Allendorf, F. W., P. R. England, G. Luikart, P. A. Ritchie & N. Ryman, 2008. Genetic effects of harvest on wild animal populations. Trends in Ecology and Evolution 23: 327–337.CrossRefPubMedGoogle Scholar
  3. Andrello, M., D. Mouillot, J. Beuvier, C. Albouy, W. Thuiller & S. Manel, 2013. Low connectivity between Mediterranean marine protected areas: a biophysical modeling approach for the dusky grouper Epinephelus marginatus. Plos One 7: e68564.CrossRefGoogle Scholar
  4. Angiolillo, M., A. Gori, S. Canese, M. Bo, C. Priori, G. Bavestrello, E. Salvati, F. Erra, M. Greenacre & G. Santangelo, 2016. Distribution and population structure of deep-dwelling red coral in the Northwest Mediterranean. Marine Ecology 37: 294–310.CrossRefGoogle Scholar
  5. Astraldi, M., G. P. Gasparini, A. Vetrano & S. Vignudelli, 2002. Hydrographic characteristics and interannual variability of water masses in the central Mediterranean: a selectivity test for long-term changes in the Mediterranean Sea. Deep Sea Research Part I: Oceanographic Research Papers 49: 661–680.CrossRefGoogle Scholar
  6. Aurelle, D. & J. B. Ledoux, 2013. Interplay between isolation by distance and genetic clusters in the red coral Corallium rubrum: insights from simulated and empirical data. Conservation Genetics 14: 705–716.CrossRefGoogle Scholar
  7. Aurelle, D., J. B. Ledoux, C. Rocher, P. Borsa, A. Chenuil & J. P. Féral, 2011. Phylogeography of the red coral (Corallium rubrum): inferences on the evolutionary history of a temperate gorgonian. Genetica 139: 855–869.CrossRefPubMedGoogle Scholar
  8. Baco, A., A. M. Clark & T. M. Shank, 2006. Six microsatellite loci from the deep-sea coral Corallium lauuense (Octocorallia: Coralliidae) from the islands and seamounts of the Hawaiian archipelago. Molecular Ecology Notes 6: 147–149.CrossRefGoogle Scholar
  9. Beger, M., K. A. Selkoe, E. Treml, P. H. Barber, S. von der Heyden, E. D. Crandall, R. J. Toonen & C. Riginos, 2014. Evolving coral reef conservation with genetic information. Bulletin of Marine Science 90: 159–185.CrossRefGoogle Scholar
  10. Belkhir, K., P. Borsa & L. Chikhi, 2004. GENETIX 4.05, Logiciel sous Windows pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France.Google Scholar
  11. Benedetti, M. C., C. Priori, F. Erra & G. Santangelo, 2016. Growth patterns in mesophotic octocorals: timing the branching process in the highly-valuable Mediterranean Corallium rubrum. Estuarine, Coastal and Shelf Science 171: 106–110.CrossRefGoogle Scholar
  12. Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B: Methodological 57: 289–300.Google Scholar
  13. Boavida, J., D. Paulo, D. Aurelle, S. Arnaud-Haond, C. Marschal, J. Reed, J. M. Gonçalves & E. A. Serrão, 2016. A well-kept treasure at depth: precious red coral rediscovered in Atlantic deep coral gardens (SW Portugal) after 300 years. PLoS One 11: e0147228.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bramanti, L., I. Vielmini, S. Rossi, G. Tsounis, M. Iannelli, R. Cattaneo-Vietti, C. Priori & G. Santangelo, 2014. Demographic parameters of two populations of red coral (Corallium rubrum L. 1758) in the North Western Mediterranean. Marine Biology 161: 1015–1026.CrossRefGoogle Scholar
  15. Brazeau, D. A. & H. R. Lasker, 1988. Inter-and intraspecific variation in gorgonian colony morphology: quantifying branching patterns in arborescent animals. Coral Reefs 7: 139–143.CrossRefGoogle Scholar
  16. Bruckner, A. W., 2009. Rate and extent of decline in Corallium (pink and red coral) populations: existing data meet the requirements for a CITES Appendix II listing. Marine Ecology Progress Series 397: 319–332.CrossRefGoogle Scholar
  17. Bussoletti, E., D. Cottingham, A. Bruckner, G. Roberts & R. Sandulli, 2010. Proceedings of the International Workshop on Red Coral Science, Management, and Trade: Lesson from the Mediterranean, Naples, Italy. September 23–26, 2009.Google Scholar
  18. Cairns, S., 2007. Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science 81: 311–322.Google Scholar
  19. Cannas, R., F. Caocci, M. C. Follesa, C. Pedoni, A. Pendugiu, P. Pesci & A. Cau, 2011. The red coral resource in Sardinian seas: a multidisciplinary survey on Corallium rubrum populations. Studi Trentini di Scienze Naturali 89: 9–18.Google Scholar
  20. Cannas, R., F. Sacco, A. Cau, D. Cuccu, M. C. Follesa & A. Cau, 2014. Genetic monitoring of deep-water exploited banks of the precious Sardinia coral Corallium rubrum (L., 1758): useful data for a sustainable management. Aquatic Conservation: Marine and Freshwater Ecosystems. 26: 236–250.CrossRefGoogle Scholar
  21. Cau, A., L. Bramanti, R. Cannas, M. C. Follesa, M. Angiolillo, S. Canese, M. Bo, D. Cuccu & K. Guizien, 2016. Habitat constraints and self-thinning shape Mediterranean red coral deep population structure: implications for conservation practice. Scientific Report 6: 23322.CrossRefGoogle Scholar
  22. Chang, S. K., Y. C. Yang & N. Iwasaki, 2013. Whether to employ trade controls or fisheries management to conserve precious corals (Coralliidae) in the Northern Pacific Ocean. Marine Policy 39: 144–153.CrossRefGoogle Scholar
  23. Chapuis, M. P. & A. Estoup, 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24: 621–631.CrossRefPubMedGoogle Scholar
  24. Chouba, L. & B. Tritar, 1998. The exploitation level of the stock of red coral (Corallium rubrum) in Tunisian waters. Mesogee 56: 29–35.Google Scholar
  25. Coma, R., M. Zabala & J. M. Gili, 1995. Sexual reproductive effort in the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series 117: 185–192.CrossRefGoogle Scholar
  26. Costantini, F. & M. Abbiati, 2006. Development of microsatellite markers for the Mediterranean gorgonian coral Corallium rubrum. Molecular Ecology Notes 6: 521–523.CrossRefGoogle Scholar
  27. Costantini, F., C. Fauvelot & M. Abbiati, 2007a. Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Marine Ecology Progress Series 340: 109–119.CrossRefGoogle Scholar
  28. Costantini, F., C. Fauvelot & M. Abbiati, 2007b. Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences. Molecular Ecology 16: 5168–5182.CrossRefPubMedGoogle Scholar
  29. Costantini, F., M. Taviani, A. Remia, E. Pintus, P. J. Schembri & M. Abbiati, 2010. Deep-water Corallium rubrum (L., 1758) from the Mediterranean Sea: preliminary genetic characterization. Marine Ecology 31: 261–269.CrossRefGoogle Scholar
  30. Costantini, F., S. Rossi, E. Pintus, C. Cerrano, J. M. Gili & M. Abbiati, 2011. Low connectivity and declining genetic variability along a depth gradient in Corallium rubrum populations. Coral Reefs 30: 991–1003.CrossRefGoogle Scholar
  31. Costantini, F., L. Carlesi & M. Abbiati, 2013. Quantifying Spatial Genetic Structuring in Mesophotic Populations of the Precious Coral Corallium rubrum. PLoS One 8: e61546.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Costantini, F. & M. Abbiati, 2016. Into the depth of population genetics: pattern of structuring in mesophotic red coral populations. Coral Reefs 35: 39–52.CrossRefGoogle Scholar
  33. Dempster, A. P., N. M. Laird & D. B. Rubin, 1977. Maximum likelihood from incomplete data via the EM Algorithm. Journal of the Royal Statistical Society Series B: (Methodological) 39: 1–38.Google Scholar
  34. DGPA, 2013. Annuaire statistique de la pêche et l’aquaculture. Direction Générale de la pêche et l’aquaculture, TunisieGoogle Scholar
  35. Edmands, S., 2007. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16: 463–475.CrossRefPubMedGoogle Scholar
  36. Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.CrossRefPubMedGoogle Scholar
  37. Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.Google Scholar
  38. Falush, D., M. Stephens & J. K. Pritchard, 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.PubMedPubMedCentralGoogle Scholar
  39. Falush, D., M. Stephens & J. K. Pritchard, 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7: 574–578.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Garrabou, J. & J. G. Harmelin, 2002. A 20-year study on life-history traits of a harvested long-lived temperate coral in the NW Mediterranean: insights into conservation and management needs. Journal of Animal Ecology 71: 966–978.CrossRefGoogle Scholar
  41. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3).Google Scholar
  42. Guizien, K. & L. Bramanti, 2014. Modelling ecological complexity for marine species conservation: the effect of variable connectivity on species spatial distribution and age-structure. Theoretical Biology Forum 107: 47–56.PubMedGoogle Scholar
  43. FAO-GFCM, 2011. Report of the Transversal Workshop on Red Coral Ajaccio (Corsica), France, 5–7 October 2011. General Fisheries Commission for the Mediterranean (GFCM)—Scientific Advisory Committee (SAC). Ajaccio (Corsica), France.Google Scholar
  44. Hoban, S. M., O. E. Gaggiotti & G. Bertorelle, 2013. The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: a simulation-based study. Molecular Ecology 22: 3444–3450. doi: 10.1111/mec.12258.CrossRefPubMedGoogle Scholar
  45. Hughes, A. R., B. D. Inouye, M. T. Johnson, N. Underwood & M. Vellend, 2008. Ecological consequences of genetic diversity. Ecology Letters 11: 609–623. doi: 10.1111/j.1461-0248.2008.01179.x.CrossRefPubMedGoogle Scholar
  46. Jombart, T., 2008. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405. doi: 10.1093/bioinformatics/btn129.CrossRefPubMedGoogle Scholar
  47. Jombart, T., S. Devillard & F. Balloux, 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11: 94.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Kalinowski, S. T., 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5: 187–189.CrossRefGoogle Scholar
  49. Knowlton, N. & J. B. Jackson, 1993. Inbreeding and outbreeding in marine invertebrates. In Thornhill, N. (ed.), The Natural History of Inbreeding and Outbreeding. University of Chicago Press, Chicago: 200–249.Google Scholar
  50. Kopelman, N. M., J. Mayzel, M. Jakobsson, N. A. Rosenberg & I. Mayrose, 2015. CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15: 1179–1191.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ledoux, J. B., J. Garrabou, O. Bianchimani, P. Drap, J. P. Féral & D. Aurelle, 2010a. Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Molecular Ecology 19: 4204–4216.CrossRefPubMedGoogle Scholar
  52. Ledoux, J. B., K. Mokhtar-Jamai, C. Roby, J. P. Féral, J. Garrabou & D. Aurelle, 2010b. 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. Molecular Ecology 19: 675–690.CrossRefPubMedGoogle Scholar
  53. Ledoux, J. B., A. Antunes, A. Haguenauer, M. Pratlong, F. Costantini. M. Abbiati & D. Aurelle, 2016. Molecular forensics into the sea: how molecular markers can help to struggle against poaching and illegal trade in precious corals? The Cnidaria, past, present and future. The world of Medusa and her sisters. Springer.Google Scholar
  54. Marti-Puig, P., F. Costantini, L. Rugiu, M. Ponti & M. Abbiati, 2013. Patterns of genetic connectivity in invertebrates of temperate MPA networks. Advances in Oceanography and Limnology 4: 138–149.CrossRefGoogle Scholar
  55. Martínez-Quintana, A., L. Bramanti, N. Viladrich, S. Rossi & K. Guizien, 2015. Quantification of larval traits driving connectivity: the case of Corallium rubrum (L. 1758). Marine Biology 162: 309–318.CrossRefGoogle Scholar
  56. Mitchell, N. D., M. R. Dardeau & W. W. Schroeder, 1993. Colony morphology, age structure, and relative growth of two gorgonian corals, Leptogorgia hebes (Verrill) and Leptogorgia virgulata (Lamarck), from the northern Gulf of Mexico. Coral Reefs 12: 65–70.CrossRefGoogle Scholar
  57. Mousadik, A. & R. J. Petit, 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92: 832–839.CrossRefPubMedGoogle Scholar
  58. Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.Google Scholar
  59. Onken, R., A. R. Robinson, P. F. Lermusiaux, P. J. Haley & L. A. Anderson, 2003. Data-driven simulations of synoptic circulation and transports in the Tunisia-Sardinia-Sicily region. Journal of Geophysical Research: Oceans 108(C9): 8123–8136.CrossRefGoogle Scholar
  60. Piry, S., G. Luikart & J. M. Cornuet, 1999. BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. Journal of Heredity 90: 502–503.CrossRefGoogle Scholar
  61. Priori, C., V. Mastascusa, F. Erra, M. S. Canese & G. Santangelo, 2013. Demography of deep-dwelling red coral populations: age and reproductive structure of a highly valued marine species. Estuarine, Coastal and Shelf Science 118: 43–49.CrossRefGoogle Scholar
  62. Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.PubMedPubMedCentralGoogle Scholar
  63. R Core Team. 2014.R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  64. Rossi, S., G. Tsounis, C. Orejas, T. Padrón, J. M. Gili, L. Bramanti, N. Teixidó & J. Gutt, 2008. Survey of deep-dwelling red coral (Corallium rubrum) populations at Cap de Creus (NW Mediterranean). Marine Biology 154: 533–545.CrossRefGoogle Scholar
  65. Rousset, F., 2008. Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8: 103–106.CrossRefPubMedGoogle Scholar
  66. Ryman, N. & S. Palm, 2006. POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Molecular Ecology Notes 6: 600–602.CrossRefGoogle Scholar
  67. Sammari, C., C. Millot, I. Taupier-Letage, A. Stefani & M. Brahim, 1999. Hydrological characteristics in the Tunisia-Sardinia-Sicily area. Deep Sea Research Part I: Oceanographic Research Papers 46: 1671–1703.CrossRefGoogle Scholar
  68. Santangelo, G. & M. Abbiati, 2001. Red coral: conservation and management of an over-exploited Mediterranean species. Aquatic Conservation: Marine and Freshwater Ecosystems 11: 253–259.CrossRefGoogle Scholar
  69. Santangelo, G. & L. Bramanti, 2010. Quantifying the decline in Corallium rubrum populations. Marine Ecology Progress Series 418: 295–297.CrossRefGoogle Scholar
  70. Santangelo, G., E. Carletti, E. Maggi & L. Bramanti, 2003. Reproduction and population sexual structure of the overexploited Mediterranean red coral Corallium rubrum. Marine Ecology Progress Series 248: 99–108.CrossRefGoogle Scholar
  71. Tescione, G., 1973. The Italians and their coral fishing. Fausto Fiorentino, Naples.Google Scholar
  72. Tsounis, G., S. Rossi, J. M. Gili & W. Arntz, 2006. Population structure of an exploited benthic cnidarian: the case study of red coral (Corallium rubrum L.). Marine Biology 149: 1059–1070.CrossRefGoogle Scholar
  73. Tsounis, G., S. Rossi, J. M. Gili & W. Arntz, 2007. Red coral fishery at the Costa Brava (NW Mediterranean): case study for an over harvested precious coral. Ecosystems 10: 975–986.CrossRefGoogle Scholar
  74. Tsounis, G., S. Rossi, R. Grigg, G. Santangelo, L. Bramanti & J. M. Gili, 2010. The exploitation and conservation of precious corals. Oceanography and Marine Biology: An Annual Review 48: 161–212.CrossRefGoogle Scholar
  75. UNEP-MAP-RAC/SPA, 2015. In Würtz, M. & S. A. S Artescienza (eds) Sicily Channel/Tunisian Plateau: Topography, Circulation and Their Effects on Biological Component. RAC/SPA, Tunis. 39 pp.Google Scholar
  76. Vighi, M., 1972. Etude sur la reproduction du Corallium rubrum (L.). Vie Milieu Vol XXIII fase 1, sér A.: 1–32.Google Scholar
  77. Von der Heyden, S., M. Beger, R. J. Toonen, L. van Herwerden, M. A. Juinio-Meñez, R. Ravago-Gotanco, C. Fauvelot & G. Bernardi, 2014. The application of genetics to marine management and conservation: examples from the Indo-Pacific. Bulletin of Marine Science 90: 123–158.CrossRefGoogle Scholar
  78. Waples, R. S., A. E. Punt & J. M. Cope, 2008. Integrating genetic data into management of marine resources: how can we do it better? Fish and Fisheries 9: 423–449.CrossRefGoogle Scholar
  79. Weir, B. S. & C. C. Cockerham, 1984. Estimating F-Statistics for the analysis of population structure. Evolution 38: 1358–1370.CrossRefGoogle Scholar
  80. Wright, J., 1951. The genetical structure of populations. Annals of Eugenics 15: 322–354.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Institut National des Sciences et Technologie de la Mer (INSTM)SalammbôTunisia
  2. 2.Institut National Agronomique de Tunisie (INAT)MahrajèneTunisia
  3. 3.Dipartimento di Scienze Biologiche, Geologiche e Ambientali, Centro Interdipartimentale di Ricerca per le Scienze AmbientaliUniversità di Bologna,UR CoNISMaRavennaItaly
  4. 4.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  5. 5.ISMAR, Consiglio Nazionale delle Ricerche - Istituto di Scienze MarineBolognaItaly

Personalised recommendations