Abstract
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.
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References
Abbiati M, Airoldi L, Costantini F, et al (2009) Spatial and temporal variation of assemblages in Mediterranean coralligenous reefs. UNEP-RAC/SPA
Acunto S, Balata D, Cinelli F (2001) Variabilità spaziale del coralligeno e considerazioni sul metodo di campionamento. Biologia Marina Mediterranea 8:191–200
Anderson MJ (2001a) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson MJ (2001b) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639
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
Anderson MJ, Gorley RN, Clarke RK (2008) Permanova + for primer: guide to software and statistical methods PRIMER-E, Plymouth
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
Balata D, Piazzi L, Cecchi E, Cinelli F (2005) Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposition. Mar Environ Res 60:403–421
Balata D, Piazzi L, Benedetti-Cecchi L (2007) Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 88:2455–2461
Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195
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
Bianchi CN, Dore G, Morri C (1995) Guida del subacqueo naturalista: Mediterraneo e tropici. Editrice Archivio Fotografico Sardo, Nuoro, pp 1–278
Bohnsack JA (1979) Photographic quantitative sampling of hard-bottom benthic communities. Bull Mar Sci 29:242–252
Bouduresque CF (2004) Marine biodiversity in the Mediterranean: status of spicies, populations and communities. Sci Rep Port-Cros Natl Park Fr 20:97–146
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
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
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
Clarke KR, Warwick RM (1994) Change in Marine Communities: an approach to statistical analysis and interpretation. Bourne Press Limited, Bournemouth
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
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
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
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
Duran S (2003) Phylogeography, gene flow and population structure of (Porifera : Poecilosclerida) Disseration, University of Barcelona
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 440:27–36
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
Garrabou J (1999) Life-history traits of Alcyonium acaule and Parazoanth us axinellae (Cnidaria, Anthozoa), with emphasis on growth. Mar Ecol Prog Ser 178:193–204
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 71:966–978
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 12:302–312
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
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
Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. doi:10.1038/35012228
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
Giaccone G (2007) Coralligenous assemblage as underwater seascape: distribution off Italian coasts. Biol Mar Mediterr 14:124–141
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
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
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
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 4:5–13
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
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 28:149–155
Huston M (1979) A general hypothesis of species diversity. Am Nat 113:81–101
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
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
Knowlton and Jackson (2001) Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Inc., Sunderland
Laubier L (1965) Le “coralligène” des Albères: monographie biocénotique. Ann Instit Océanogr Monaco 43:139–316
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
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
Linares C, Doak DF, Coma R et al (2007) Life history and viability of a long-lived marine invertebrate: the octocoral Paramuricea clavata. Ecology 88:918–928
Lourie SA, Vincent ACJ (2004) Using biogeography to help set priorities in marine conservation 18:1004–1020
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
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
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
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
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
Pérès JM, Picard J (1964) Nouveau Manuel de Bionomie Benthique de la Méditerranée. Rec Trav St Mar Endoume 47:5–137
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
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
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
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
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
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
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 233–295
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
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
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
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 332:25–39
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 167:137–148
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
Witman JD, Dayton PK (2001) Rocky subtidal communities. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Inc., Sunderland
Acknowledgments
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, http://biorock.medrecover.org/) and the Total Foundation (medDiversa project, http://meddiversa.medrecover.org/). 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 (http://medrecover.org) of the Generalitat de Catalunya.
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Communicated by F. Bulleri.
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Casas-Güell, E., Teixidó, N., Garrabou, J. et al. Structure and biodiversity of coralligenous assemblages over broad spatial and temporal scales. Mar Biol 162, 901–912 (2015). https://doi.org/10.1007/s00227-015-2635-7
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DOI: https://doi.org/10.1007/s00227-015-2635-7