Marine Biology

, Volume 162, Issue 4, pp 901–912 | Cite as

Structure and biodiversity of coralligenous assemblages over broad spatial and temporal scales

  • Edgar Casas-Güell
  • Núria Teixidó
  • Joaquim Garrabou
  • Emma Cebrian
Original Paper


Coralligenous outcrops rank among the most important ecosystems in the Mediterranean Sea, primarily because of their biodiversity. Information on the spatial and temporal variability of the composition and structure of coralligenous assemblages is essentially lacking for most regions. We explored the variability of the biodiversity patterns of coralligenous outcrops dominated by the red gorgonian Paramuricea clavata in the NW Mediterranean region using a hierarchical sampling design. The study addressed two overlooked spatial and temporal scales: from 1 to >100 km and a 5-year period. Overall, no temporal changes were detected in either species composition or the 12 morphofunctional groups considered. Significant differences in species composition were found at the various spatial scales. However, variation in composition at the locality level (>100 km apart) showed the lowest values in comparison with the differences found at the site level (<1 km apart). Despite the differences, the sites displayed high similarity (average similarity 55.7 %) and shared approximately 50 % of the species. Similarly, the patterns of diversity at different scales, the alpha (site) and gamma (locality) were consistent with the specific composition trends, whereas the beta diversity showed the greatest differences among sites. Our results demonstrate the moderate spatial variability in biodiversity in the NW Mediterranean region and an extremely low temporal variability. This study provides baselines for detecting potential effects due to global change, and it furnishes a basis for the implementation of monitoring schemes of coralligenous assemblages. The development of similar sampling schemes in other Mediterranean regions will provide a global view of the biodiversity of coralligenous outcrops.


Polychaete Great Barrier Reef Beta Diversity Perennial Species Alpha Diversity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors thank C. Linares, J. B. Ledoux and S. Kipson for field assistance. The study has been funded by the Spanish Ministry of Science and Innovation to E. Casas-Güell, a doctoral fellowship linked to the Biorock Project (CTM2009–08045, and the Total Foundation (medDiversa project, ECG thanks helpful and valuable comments on earlier drafts of the manuscript to Dr. M. J. Anderson during a research visit fellow (EEBB-I-13-06897) at NZIAS-INMS (Massey University), and to Dr. M. Pawley and A. N. H. Smith for made my stay especially comfortable. The authors are members of the Marine Conservation Research Group ( of the Generalitat de Catalunya.

Conflict of interest

The authors declare that they have no conflicts of interest concerning this article.

Supplementary material

227_2015_2635_MOESM1_ESM.pdf (294 kb)
Supplementary material 1 (PDF 293 kb)


  1. Abbiati M, Airoldi L, Costantini F, et al (2009) Spatial and temporal variation of assemblages in Mediterranean coralligenous reefs. UNEP-RAC/SPAGoogle Scholar
  2. Acunto S, Balata D, Cinelli F (2001) Variabilità spaziale del coralligeno e considerazioni sul metodo di campionamento. Biologia Marina Mediterranea 8:191–200Google Scholar
  3. Anderson MJ (2001a) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  4. Anderson MJ (2001b) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639CrossRefGoogle Scholar
  5. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. doi: 10.1111/j.1461-0248.2006.00926 CrossRefGoogle Scholar
  6. Anderson MJ, Gorley RN, Clarke RK (2008) Permanova + for primer: guide to software and statistical methods PRIMER-E, PlymouthGoogle Scholar
  7. Anderson MJ, Crist TO, Chase JM et al (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecol Lett 14:19–28. doi: 10.1111/j.1461-0248.2010.01552.x CrossRefGoogle Scholar
  8. Balata D, Piazzi L, Cecchi E, Cinelli F (2005) Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposition. Mar Environ Res 60:403–421CrossRefGoogle Scholar
  9. Balata D, Piazzi L, Benedetti-Cecchi L (2007) Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 88:2455–2461CrossRefGoogle Scholar
  10. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195Google Scholar
  11. Bensoussan N, Romano J-C, Harmelin J-G, Garrabou J (2010) High resolution characterization of northwest Mediterranean coastal waters thermal regimes: to better understand responses of benthic communities to climate change. Estuar Coast Shelf Sci 87:431–441. doi: 10.1016/j.ecss.2010.01.008 CrossRefGoogle Scholar
  12. Bianchi CN, Dore G, Morri C (1995) Guida del subacqueo naturalista: Mediterraneo e tropici. Editrice Archivio Fotografico Sardo, Nuoro, pp 1–278Google Scholar
  13. Bohnsack JA (1979) Photographic quantitative sampling of hard-bottom benthic communities. Bull Mar Sci 29:242–252Google Scholar
  14. Bouduresque CF (2004) Marine biodiversity in the Mediterranean: status of spicies, populations and communities. Sci Rep Port-Cros Natl Park Fr 20:97–146Google Scholar
  15. Casellato S, Stefanon A (2008) Coralligenous habitat in the northern Adriatic Sea: an overview. Mar Ecol 29:321–341. doi: 10.1111/j.1439-0485.2008.00236 CrossRefGoogle Scholar
  16. Cebrián E, Linares C, Marschal C, Garrabou J (2012) Exploring the effects of invasive algae on the persistence of gorgonian populations. Biol Invasions 14:2647–2656. doi: 10.1007/s10530-012-0261-6 CrossRefGoogle Scholar
  17. Cecchi E, Gennaro P, Piazzi L, Ricevuto E, Serena F (2014) Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur J Phycol 49(3):298–312. doi: 10.1080/09670262.2014.918657 CrossRefGoogle Scholar
  18. Clarke KR, Warwick RM (1994) Change in Marine Communities: an approach to statistical analysis and interpretation. Bourne Press Limited, BournemouthGoogle Scholar
  19. Coma R, Pola E, Ribes M, Zabala M (2004) Long-term assessment of temperate octocoral mortality patterns, protected vs unprotected areas. Ecol Appl 14:1466–1478. doi: 10.1890/03-5176 CrossRefGoogle Scholar
  20. Costantini F, Fauvelot C, Abbiati M (2007) Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences. Mol Ecol 16:5168–5182. doi: 10.1111/j.1365-294X.2007.03579 CrossRefGoogle Scholar
  21. Crain CM, Halpern BS, Beck MW, Kappel CV (2009) Understanding and managing human threats to the coastal marine environment. Ann NY Acad Sci 1162:39–62. doi: 10.1111/j.1749-6632.2009.04496 CrossRefGoogle Scholar
  22. Deter J, Descamp P, Boissery P et al (2012) A rapid photographic method detects depth gradient in coralligenous assemblages. J Exp Mar Bio Ecol 418–419:75–82. doi: 10.1016/j.jembe.2012.03.006 CrossRefGoogle Scholar
  23. Duran S (2003) Phylogeography, gene flow and population structure of (Porifera : Poecilosclerida) Disseration, University of BarcelonaGoogle Scholar
  24. Ferdeghini F, Acunto S, Cocito S, Cinelli F (2000) Variability at different spatial scales of a coralligenous assemblage at Giannutri Island (Tuscan Archipelago, northwest Mediterranean). Hydrobiologia 440:27–36CrossRefGoogle Scholar
  25. Foster MS, Harrold C, Hardin DD (1991) Point vs. photo quadrat estimates of the cover of sessile marine organisms. J Exp Mar Bio Ecol 146:193–203. doi: 10.1016/0022-0981(91)90025-R CrossRefGoogle Scholar
  26. Garrabou J (1999) Life-history traits of Alcyonium acaule and Parazoanth us axinellae (Cnidaria, Anthozoa), with emphasis on growth. Mar Ecol Prog Ser 178:193–204CrossRefGoogle Scholar
  27. Garrabou J, Harmelin J-G (2002) A 20-year study on life-history traits of a harvested long-lived temperate coral in the NW Mediterranean: and management needs insights into conservation and management needs. J Anim Ecol 71:966–978CrossRefGoogle Scholar
  28. Garrabou J, Sala E, Arcas A, Zabala M (1998) The impact of diving on Rocky Sublittoral Communities: a case study of a bryozoan population. Conserv Biol 12:302–312CrossRefGoogle Scholar
  29. 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 55:493–508. doi: 10.1006/ecss.2001.0920 CrossRefGoogle Scholar
  30. Garrabou J, Coma R, Bensoussan N et al (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103. doi: 10.1111/j.1365-2486.2008.01823 CrossRefGoogle Scholar
  31. Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. doi: 10.1038/35012228 CrossRefGoogle Scholar
  32. Gennaro P, Piazzi L (2011) Synergism between two anthropic impacts: Caulerpa racemosa var. cylindracea invasion and seawater nutrient enrichment. Mar Ecol Prog Ser 427:59–70. doi: 10.3354/meps09053 CrossRefGoogle Scholar
  33. Giaccone G (2007) Coralligenous assemblage as underwater seascape: distribution off Italian coasts. Biol Mar Mediterr 14:124–141Google Scholar
  34. Giakoumi S, Sini M, Gerovasileiou V et al (2013) Ecoregion-based conservation planning in the Mediterranean: dealing with large-scale heterogeneity. PLoS ONE 8:e76449. doi: 10.1371/journal.pone.0076449 CrossRefGoogle Scholar
  35. Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321. doi: 10.1016/S0169-5347(98)01365-2 CrossRefGoogle Scholar
  36. Halpern BS, Walbridge S, Selkoe KA et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952. doi: 10.1126/science.1149345 CrossRefGoogle Scholar
  37. Harmelin J-G, Marinopoulos J (1994) Population structure and partial mortality of the gorgonian Paramuricea clavata (Risso) in the north-western Mediterranean (France, Port-Cros Island). Mar Life 4:5–13Google Scholar
  38. Hughes TP, Baird AH, Dinsdale EA et al (2012) Assembly rules of reef corals are flexible along a steep climatic gradient. Curr Biol 22:736–741. doi: 10.1016/j.cub.2012.02.068 CrossRefGoogle Scholar
  39. Hughes TP, Linares C, Dakos V, Van de Leemput I, Van Nes E (2013) Living dangerously on borrowed time during slow, unrecognized regime shifts. Trends Ecol Evol 28:149–155CrossRefGoogle Scholar
  40. Huston M (1979) A general hypothesis of species diversity. Am Nat 113:81–101CrossRefGoogle Scholar
  41. Jackson JBC (2010) The future of the oceans past. Philos Trans R Soc Lond B Biol Sci 365:3765–3778. doi: 10.1098/rstb.2010.0278 CrossRefGoogle Scholar
  42. Kipson S, Fourt M, Teixidó N, Cebrián E, Casas E et al (2011) Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of Mediterranean coralligenous outcrops. PLoS ONE 6(11):e27103. doi: 10.1371/journal.pone.0027103 CrossRefGoogle Scholar
  43. Knowlton and Jackson (2001) Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Inc., SunderlandGoogle Scholar
  44. Laubier L (1965) Le “coralligène” des Albères: monographie biocénotique. Ann Instit Océanogr Monaco 43:139–316Google Scholar
  45. Ledoux J-B, Garrabou J, Bianchimani O et al (2010a) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol. doi: 10.1111/j.1365-294X.2010.04814 Google Scholar
  46. Ledoux J-B, Mokhtar-Jamaï K, Roby C et al (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. Mol Ecol 19:675–690. doi: 10.1111/j.1365-294X.2009.04516 CrossRefGoogle Scholar
  47. Linares C, Doak DF, Coma R et al (2007) Life history and viability of a long-lived marine invertebrate: the octocoral Paramuricea clavata. Ecology 88:918–928CrossRefGoogle Scholar
  48. Lourie SA, Vincent ACJ (2004) Using biogeography to help set priorities in marine conservation 18:1004–1020Google Scholar
  49. Magurran AE, Baillie SR, Buckland ST et al (2010) Long-term datasets in biodiversity research and monitoring: assessing change in ecological communities through time. Trends Ecol Evol 25:574–582. doi: 10.1016/j.tree.2010.06.016 CrossRefGoogle Scholar
  50. Mariani S, Uriz M-J, Turon X, Alcoverro T (2006) Dispersal strategies in sponge larvae: integrating the life history of larvae and the hydrologic component. Oecologia 149:174–184. doi: 10.1007/s00442-006-0429-9 CrossRefGoogle Scholar
  51. Martin CS, Giannoulaki M, De Leo F et al (2014) Coralligenous and maërl habitats: predictive modelling to identify their spatial distributions across the Mediterranean Sea. Sci Rep. doi: 10.1038/srep05073 Google Scholar
  52. Mokhtar-Jamaï K, Pascual M, Ledoux J-B et al (2011) From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal. Mol Ecol 20:3291–3305. doi: 10.1111/j.1365-294X.2011.05176 CrossRefGoogle Scholar
  53. Parravicini V, Micheli F, Montefalcone M et al (2010) Rapid assessment of epibenthic communities: a comparison between two visual sampling techniques. J Exp Mar Bio Ecol 395:21–29. doi: 10.1016/j.jembe.2010.08.005 CrossRefGoogle Scholar
  54. Pérès JM, Picard J (1964) Nouveau Manuel de Bionomie Benthique de la Méditerranée. Rec Trav St Mar Endoume 47:5–137Google Scholar
  55. Piazzi L, Balata D, Pertusati M, Cinelli F (2004) Spatial and temporal variability of Mediterranean macroalgal coralligenous assemblages in relation to habitat and substratum inclination. Bot Mar 47:105–115. doi: 10.1515/BOT.2004.010
  56. Piazzi L, Balata D, Cecchi E et al (2010) Species composition and patterns of diversity of macroalgal coralligenous assemblages in the north-western Mediterranean Sea. J Nat Hist 44:1–22. doi: 10.1080/00222930903377547 CrossRefGoogle Scholar
  57. Piazzi L, Gennaro P, Balata D (2011) Effects of nutrient enrichment on macroalgal coralligenous assemblages. Mar Poll Bul 62:1830–1835. doi: 10.1016/j.marpolbul.2011.05.004 CrossRefGoogle Scholar
  58. Piazzi L, Gennaro P, Balata D (2012) Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar Poll Bul 64:2623–2629. doi: 10.1016/j.marpolbul.2012.07.027 CrossRefGoogle Scholar
  59. Piazzi L, Balata D, Cecchi E, Gennaro P, Serena F (2014) Effectiveness of different investigation procedures in detecting anthropogenic impacts on coralligenous assemblages. Sci Mar 78(3):319–328. doi: 10.3989/scimar.03989.28A CrossRefGoogle Scholar
  60. Ponti M, Fava F, Abbiati M (2011) Spatial–temporal variability of epibenthic assemblages on subtidal biogenic reefs in the northern Adriatic Sea. Mar Biol 158:1447–1459. doi: 10.1007/s00227-011-1661-3 CrossRefGoogle Scholar
  61. Ros JD, Romero J, Ballesteros E, Gill JM (1985) Diving in blue water. The benthos. In: Margalef R (ed) Western Mediterranean. Pergamon Press, Oxford, pp 233–295Google Scholar
  62. Teixidó N, Pineda M-C, Garrabou J (2009) Decadal demographic trends of a long-lived temperate encrusting sponge. Mar Ecol Prog Ser 375:113–124. doi: 10.3354/meps07757 CrossRefGoogle Scholar
  63. Teixidó N, Garrabou J, Harmelin J-G (2011) Low dynamics, high longevity and persistence of sessile structural species dwelling on Mediterranean coralligenous outcrops. PLoS ONE 6:e23744. doi: 10.1371/journal.pone.0023744 CrossRefGoogle Scholar
  64. Teixidó N, Casas E, Cebrián E, Linares C, Garrabou J (2013) Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE 8(1):e53742. doi: 10.1371/journal.pone.0053742 CrossRefGoogle Scholar
  65. Terlizzi A, Anderson MJ, Fraschetti S, Benedetti-cecchi L (2007) Scales of spatial variation in Mediterranean subtidal sessile assemblages at different depths. Mar Ecol Prog Ser 332:25–39CrossRefGoogle Scholar
  66. Uriz M-J (1998) How do reproductive output, larval behaviour, and recruitment contribute to adult spatial patterns in Mediterranean encrusting sponges ? Mar Ecol Prog Ser 167:137–148CrossRefGoogle 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 25:265–272. doi: 10.1007/s00338-006-0100-2 CrossRefGoogle Scholar
  68. Witman JD, Dayton PK (2001) Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Inc., SunderlandGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Edgar Casas-Güell
    • 1
  • Núria Teixidó
    • 1
  • Joaquim Garrabou
    • 1
    • 2
  • Emma Cebrian
    • 3
    • 4
  1. 1.Institut de Ciències del Mar (ICM-CSIC)BarcelonaSpain
  2. 2.UM110, CNRS/INSU, IRD, Université du Sud Toulon Var, Mediterranean Institute of Oceanography (MIO)Aix-Marseille UniversitéMarseilleFrance
  3. 3.Centre d’Estudis Avançats de Blanes (CEAB-CSIC)Blanes, GironaSpain
  4. 4.Departament de Ciències Ambientals, Facultat de CiènciesUniversitat de GironaGironaSpain

Personalised recommendations