Marine Biology

, 163:120 | Cite as

The role of gorgonians on the diversity of vagile benthic fauna in Mediterranean rocky habitats

  • Massimo Ponti
  • Daniele Grech
  • Mario Mori
  • Rossella A. Perlini
  • Vincenzo Ventra
  • Pier Augusto Panzalis
  • Carlo Cerrano
Original paper


Mediterranean gorgonian forests are threatened by several human activities and climatic anomalies that increase their susceptibility to pathogens and epibionts, potentially leading to mass mortality events. Although these phenomena have been largely documented, the effects of the loss of gorgonian colonies on temperate reef assemblages have been poorly evaluated until now, especially those that concern the vagile fauna. This is the first study comparing vagile fauna assemblages living in Mediterranean rocky bottoms between patches with and without the gorgonians Eunicella cavolini and Paramuricea clavata. Vagile fauna were analysed at the end of a field experiment where patches with and without gorgonians were simulated by transplanting gorgonian branches on to plastic recruitment panels. Panels were deployed for 4 months at two depths (24 m for E. cavolini and 40 m for P. clavata) at two sites in the north-western Mediterranean Sea (Tavolara Island and Portofino Promontory). Overall, 211 taxa belonging to the phyla Platyhelminthes, Nemertea, Mollusca, Brachiopoda, Nematoda, Anellida, Arthropoda and Echinodermata were found. Despite high local heterogeneity and large differences between sites, the abundance of some vagile species was related to the presence of gorgonians. For instance, the shrimp Periclimenes aegylios, absent at Tavolara, was facilitated by the presence of E. cavolini at Portofino, while the tanaid Leptochelia sp. was absent/scarce in the presence of gorgonians at both sites. Overall, at 40 m depth, vagile community structures did not differ significantly between experimental patches with and without P. clavata; at 24 m depth, vagile assemblages in the presence of E. cavolini were different and less heterogeneous compared to those found in patches without transplanted gorgonians. Ultimately, gorgonians could directly and indirectly affect vagile assemblages.


Spinosa Crustose Coralline Alga Experimental Patch Increase Habitat Complexity Plastic Panel 
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.



Sampling at Tavolara and Portofino was undertaken in accordance with Italian laws, and no endangered or protected species were involved. We wish to thank Augusto Navone, Director of the MPA Tavolara–Punta Coda Cavallo (, and Giorgio Fanciulli, Director of the MPAs Portofino (, for the authorisations, and Egidio Trainito, Maurizio Pansini, Monica Previati, Marco Palma and Carla Huete Stauffer for the valuable field and diving assistance. This work has been partially supported by the 2010–11 PRIN project “Coastal bioconstructions: structures, functions, and management” (prot. 2010Z8HJ5 M) and the Flagship Project RITMARE—The Italian Research for the Sea—coordinated by the Italian National Research Council and funded by the Italian Ministry of Education, University and Research within the National Research Program 2011–2013. The authors are grateful to the editor and two anonymous reviewers for their constructive comments and to David Cuming and Martin Sayer for their English-language editing support.

Supplementary material

227_2016_2897_MOESM1_ESM.pdf (288 kb)
Supplementary material 1 (PDF 288 kb)


  1. Anderson MJ, ter Braak CJF (2003) Permutation tests for multi-factorial analysis of variance. J Stat Comput Sim 73:85–113. doi: 10.1080/0094965021000015558 CrossRefGoogle Scholar
  2. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E Ltd, PlymouthGoogle Scholar
  3. Antoniadou C, Voultsiadou E, Chintiroglou C (2010) Benthic colonization and succession on temperate sublittoral rocky cliffs. J Exp Mar Biol Ecol 382:145–153. doi: 10.1016/j.jembe.2009.11.004 CrossRefGoogle Scholar
  4. Antoniadou C, Voultsiadou E, Chintiroglou C (2011) Seasonal patterns of colonization and early succession on sublittoral rocky cliffs. J Exp Mar Biol Ecol 403:21–30. doi: 10.1016/j.jembe.2011.04.001 CrossRefGoogle Scholar
  5. Ballesteros E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr Mar Biol Annu Rev 44:123–195. doi: 10.1201/9781420006391 CrossRefGoogle Scholar
  6. Bavestrello G, Cerrano C, Cattaneo-Vietti R, Sarà M (1996) Relations between Eudendrium glomeratum (Cnidaria, Hydromedusae) and its associated vagile fauna. Sci Mar 60:137–143Google Scholar
  7. Bavestrello G, Cerrano C, Zanzi D, Cattaneo-Vietti R (1997) Damage by fishing activities in the gorgonian coral Paramuricea clavata in the Ligurian Sea. Aquat Conserv 7:253–262. doi: 10.1002/(SICI)1099-0755(199709)7:3<253:AID-AQC243>3.0.CO;2-1 CrossRefGoogle Scholar
  8. Bouma TJ, Ortells V, Ysebaert T (2009) Comparing biodiversity effects among ecosystem engineers of contrasting strength: macrofauna diversity in Zostera noltii and Spartina anglica vegetations. Helgoland Mar Res 63:3–18CrossRefGoogle Scholar
  9. Buhl-Mortensen L, Mortensen PB (2004) Crustaceans associated with the deep-water gorgonian corals Paragorgia arborea (L., 1758) and Primnoa resedaeformis (Gunn., 1763). J Nat Hist 38:1233–1247. doi: 10.1080/0022293031000155205 CrossRefGoogle Scholar
  10. Burkepile D, Hay M (2007) Predator release of the gastropod Cyphoma gibbosum increases predation on gorgonian corals. Oecologia 154:167–173. doi: 10.1007/s00442-007-0801-4 CrossRefGoogle Scholar
  11. 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 24:73–82. doi: 10.1080/02757540801979648 CrossRefGoogle Scholar
  12. Cerrano C, Bavestrello G, Bianchi CN, Cattaneo-Vietti R, Bava S, Morganti C, Morri C, Picco P, Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (Northwestern Mediterranean), summer 1999. Ecol Lett 3:284–293. doi: 10.1046/j.1461-0248.2000.00152.x CrossRefGoogle Scholar
  13. Cerrano C, Arillo A, Azzini F, Calcinai B, Castellano L, Muti C, Valisano L, Zega G, Bavestrello G (2005) Gorgonian population recovery after a mass mortality event. Aquat Conserv 15:147–157. doi: 10.1002/aqc.661 CrossRefGoogle Scholar
  14. 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. doi: 10.1007/s10531-009-9712-5 CrossRefGoogle Scholar
  15. Cerrano C, Cardini U, Bianchelli S, Corinaldesi C, Pusceddu A, Danovaro R (2013) Red coral extinction risk enhanced by ocean acidification. Sci Rep. doi: 10.1038/srep01457 Google Scholar
  16. Coma R, Gili JM, Zabala M, Riera T (1994) Feeding and prey capture cycles in the aposymbiontic gorgonian Paramuricea clavata. Mar Ecol Prog Ser 115:257–270. doi: 10.3354/meps115257 CrossRefGoogle Scholar
  17. 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
  18. Coma R, Linares C, Ribes M, Diaz D, Garrabou J, Ballesteros E (2006) Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria : Octorallia) in Menorca (NW Mediterranean). Mar Ecol Prog Ser 327:51–60. doi: 10.3354/meps327051 CrossRefGoogle Scholar
  19. Cupido R, Cocito S, Barsanti M, Sgorbini S, Peirano A, Santangelo G (2009) Unexpected long-term population dynamics in a canopy-forming gorgonian coral following mass mortality. Mar Ecol Prog Ser 394:195–200. doi: 10.3354/meps08260 CrossRefGoogle Scholar
  20. Cúrdia J, Carvalho S, Pereira F, Guerra-García JM, Santos MN, Cunha MR (2015) Diversity and abundance of invertebrate epifaunal assemblages associated with gorgonians are driven by colony attributes. Coral Reefs 34:611–624. doi: 10.1007/s00338-015-1283-1 CrossRefGoogle Scholar
  21. De Clippele LH, Buhl-Mortensen P, Buhl-Mortensen L (2015) Fauna associated with cold water gorgonians and sea pens. Cont Shelf Res 105:67–78. doi: 10.1016/j.csr.2015.06.007 CrossRefGoogle Scholar
  22. Dias IM, Cúrdia J, Cunha MR, Santos MN, Carvalho S (2015) Temporal variability in epifaunal assemblages associated with temperate gorgonian gardens. Mar Environ Res 112:140–151. doi: 10.1016/j.marenvres.2015.10.006 CrossRefGoogle Scholar
  23. Duris Z, Ates AS, Ozalp HB, Katagan T (2013) New records of decapod crustaceans (Decapoda: Pontoniinae and Inachidae) associated with sea anemones in Turkish waters. Mediterr Mar Sci 14:49–55. doi: 10.12681/mms.620 Google Scholar
  24. Faulkner DJ (1996) Marine natural products. Nat Prod Rep 13:75–125. doi: 10.1039/np9961300075 CrossRefGoogle Scholar
  25. 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 Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Change Biol 15:1090–1103. doi: 10.1111/j.1365-2486.2008.01823.x CrossRefGoogle Scholar
  26. Giannini F, Gili JM, Santangelo G (2003) Relationships between the spatial distribution of red coral Corallium rubrum and coexisting suspension feeders at Medas Islands Marine Protected Area (Spain). Ital J Zool 70:233–239. doi: 10.1080/11250000309356523 CrossRefGoogle Scholar
  27. 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
  28. Goh NKC, Ng PKL, Chou LM (1999) Notes on the shallow water gorgonian-associated fauna on coral reefs in Singapore. Bull Mar Sci 65:259–282Google Scholar
  29. Gower JC (1966) Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53:325–338CrossRefGoogle Scholar
  30. Huete-Stauffer C, Vielmini I, Palma M, Navone A, Panzalis P, Vezzulli L, Misic C, Cerrano C (2011) Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Mar Ecol Evol Persp 32:107–116. doi: 10.1111/j.1439-0485.2011.00429.x CrossRefGoogle Scholar
  31. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386. doi: 10.2307/3545850 CrossRefGoogle Scholar
  32. Kelaher BP (2003) Changes in habitat complexity negatively affect diverse gastropod assemblages in coralline algal turf. Oecologia 135:431–441. doi: 10.1007/s00442-003-1196-5 CrossRefGoogle Scholar
  33. Kumagai NH, Aoki MN (2003) Seasonal changes in the epifaunal community on the shallow-water gorgonian Melithaea flabellifera. J Mar Biol Assoc UK 83:1221–1222. doi: 10.1017/s002531540300852x CrossRefGoogle Scholar
  34. Linares C, Coma R, Diaz D, Zabala M, Hereu B, Dantart L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar Ecol Prog Ser 305:127–137. doi: 10.3354/meps305127 CrossRefGoogle Scholar
  35. 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. doi: 10.1111/j.1365-2664.2007.01419.x CrossRefGoogle Scholar
  36. Magurran AE (2004) Measuring biological diversity. Blakwell Science Ltd, HobokenGoogle Scholar
  37. Manconi R, Mori M (1990) New records of Balssia gasti (Balss, 1921) (Decapoda, Palaemonidae) in the western Mediterranean Sea. Crustaceana 59:96–100. doi: 10.1163/156854090x00345 CrossRefGoogle Scholar
  38. Manconi R, Mori M (1992) Caridean shrimps (Decapoda) found among Corallium rubrum (L, 1758). Crustaceana 62:105–110. doi: 10.1163/156854092x00109 CrossRefGoogle Scholar
  39. Martin Y, Bonnefort JL, Chancerelle L (2002) Gorgonians mass mortality during the 1999 late summer in french Mediterranean coastal waters: the bacterial hypothesis. Water Res 36:779–782. doi: 10.1016/S0043-1354(01)00251-2 CrossRefGoogle Scholar
  40. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297. doi: 10.1890/0012-9658 CrossRefGoogle Scholar
  41. McDonald GR, Nybakken JW (1997) List of the worldwide food habits of nudibranchs. UC Santa Cruz Previously Published Works, Santa CruzGoogle Scholar
  42. Montefalcone M, Morri C, Parravicini V, Bianchi C (2015) A tale of two invaders: divergent spreading kinetics of the alien green algae Caulerpa taxifolia and Caulerpa cylindracea. Biol Inva. doi: 10.1007/s10530-015-0908-1 Google Scholar
  43. Mori M, Morri C, Bianchi CN (1994) Notes on the life history of the pontonine shrimp Balssia gasti (Balss, 1921). Oebalia 20:129–137Google Scholar
  44. Musard O, Le Dû-Blayo L, Francour P, Beurier J-P, Feunteun E, Talassinos L (2014) Underwater seascapes. From geographical to ecological perspectives. Springer International Publishing, BerlinGoogle Scholar
  45. Patton WK (1972) Studies on the animal symbionts of the gorgonian coral, Leptogorgia virgulata (Lamarck). Bull Mar Sci 22:419–431Google Scholar
  46. 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. doi: 10.1515/BOT.2004.010 Google Scholar
  47. Ponti M, Fava F (2008) Molluschi. In: Ponti M, Mescalchin P (eds) Meraviglie sommerse delle “Tegnùe”. Guida alla scoperta degli organismi marini. Associazione “Tegnùe di Chioggia”—onlus. Editrice La Mandragora, Imola, pp 187–246Google Scholar
  48. 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
  49. Ponti M, Perlini RA, Ventra V, Grech D, Abbiati M, Cerrano C (2014) Ecological shifts in Mediterranean coralligenous assemblages related to gorgonian forest loss. PLoS ONE. doi: 10.1371/journal.pone.0102782 Google Scholar
  50. Poursanidis D, Koutsoubas D (2015) A computerized database (CorMol) on the molluscan fauna from the Mediterranean reef ecosystems: Part I, the coralligenous formations. Quat Int 390:29–43. doi: 10.1016/j.quaint.2015.07.029 CrossRefGoogle Scholar
  51. Priori C, Erra F, Angiolillo M, Santangelo G (2015) Effects of gastropod predation on the reproductive output of an overexploited deep octocoral. Coral Reefs 34:59–63. doi: 10.1007/s00338-014-1223-5 CrossRefGoogle Scholar
  52. Purser A, Ontrup J, Schoening T, Thomsen L, Tong R, Unnithan V, Nattkemper TW (2013) Microhabitat and shrimp abundance within a Norwegian cold-water coral ecosystem. Biogeosciences 10:5779–5791. doi: 10.5194/bg-10-5779-2013 CrossRefGoogle Scholar
  53. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  54. Relini G (2008) Checklist della flora e della fauna dei mari italiani (parte I) Biologia Marina Mediterranea. Società Italiana di Biologia Marina, GenovaGoogle Scholar
  55. Relini G (2010) Checklist della flora e della fauna dei mari italiani (parte II) Biologia Marina Mediterranea. Società Italiana di Biologia Marina, GenovaGoogle Scholar
  56. Ribes M, Coma R, Gili JM (1999) Heterogeneous feeding in benthic suspension feeders: the natural diet and grazing rate of the temperate gorgonian Paramuricea clavata (Cnidaria: Octocorallia) over a year cycle. Mar Ecol Prog Ser 183:125–137. doi: 10.3354/meps183125 CrossRefGoogle Scholar
  57. Rivetti I, Fraschetti S, Lionello P, Zambianchi E, Boero F (2014) Global warming and mass mortalities of benthic invertebrates in the Mediterranean Sea. PLoS ONE. doi: 10.1371/journal.pone.0115655 Google Scholar
  58. Russo AR (1985) Ecological observations on the gorgonian sea fan Eunicella cavolinii in the Bay of Naples. Mar Ecol Prog Ser 24:155–159. doi: 10.3354/meps024155 CrossRefGoogle Scholar
  59. Scinto A, Bavestrello G, Boyer M, Previati M, Cerrano C (2008) Gorgonian mortality related to a massive attack by caprellids in the Bunaken Marine Park (North Sulawesi, Indonesia). J Mar Biol Assoc UK 88:723–727. doi: 10.1017/S002531540800129X CrossRefGoogle Scholar
  60. Scinto A, Bertolino M, Calcinai B, Huete-Stauffer C, Previati M, Romagili T, Cerrano C (2009) Role of a Paramuricea clavata forest in modifying the coralligenous assemblages. In: Pergent-Martini C, Brichet M (eds) Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. UNEP-MAP-RAC/SPA, Tabarka, pp 136–140Google Scholar
  61. Sini M, Kipson S, Linares C, Koutsoubas D, Garrabou J (2015) The yellow gorgonian Eunicella cavolini: Demography and disturbance levels across the Mediterranean Sea. PLoS ONE. doi: 10.1371/journal.pone.0126253 Google Scholar
  62. Smith RE, Grutter AS, Tibbetts IR (2012) Extreme habitat specialisation and population structure of two gorgonian-associated pygmy seahorses. Mar Ecol Prog Ser 444:195–206. doi: 10.3354/meps09471 CrossRefGoogle Scholar
  63. Teixido 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. Teixido N, Casas E, Cebrian E, Linares C, Garrabou J (2013) Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE. doi: 10.1371/journal.pone.0053742 Google Scholar
  65. Underwood AJ (1997) Experiments in ecology. Cambridge University Press, CambridgeGoogle Scholar
  66. Urra J, Rueda JL, Gofas S, Marina P, Salas C (2012) A species-rich molluscan assemblage in a coralligenous bottom of the Alboran Sea (south-western Mediterranean): intra-annual changes and ecological considerations. J Mar Biol Assoc UK 92:665–677. doi: 10.1017/s0025315411001391 CrossRefGoogle Scholar
  67. Valisano L, Notari F, Mori M, Cerrano C (2016) Temporal variability of sedimentation rates and mobile fauna inside and outside a gorgonian garden. Mar Ecol Evol Persp. doi: 10.1111/maec.12328 Google Scholar
  68. Vezzulli L, Previati M, Pruzzo C, Marchese A, Bourne DG, Cerrano C (2010) Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environ Microbiol 12:2007–2019. doi: 10.1111/j.1462-2920.2010.02209.x CrossRefGoogle Scholar
  69. Vezzulli L, Pezzati E, Huete-Stauffer C, Pruzzo C, Cerrano C (2013) 16SrDNA pyrosequencing of the Mediterranean gorgonian Paramuricea clavata reveals a link among alterations in bacterial holobiont members, anthropogenic influence and disease outbreaks. PLoS ONE 8:e67745. doi: 10.1371/journal.pone.0067745 CrossRefGoogle Scholar
  70. Wang JR, He WF, Guo YW (2013) Chemistry, chemoecology, and bioactivity of the South China Sea opisthobranch molluscs and their dietary organisms. J Asian Nat Prod Res 15:185–197. doi: 10.1080/10286020.2012.746960 CrossRefGoogle Scholar
  71. Weinbauer MG, Velimirov B (1996) Relative habitat suitability and stability of the Mediterranean gorgonian coral Eunicella cavolini (Coelenterata: Octocorallia). Bull Mar Sci 58:786–791Google Scholar
  72. Weinberg S (1976) Revision of the common Octocorallia of the Mediterranean circalittoral. I Gorgonacea Beaufortia 24:63–104Google Scholar
  73. Wirtz P, Diesel R (1983) The social structure of Inachus phalangium, a spider crab associated with the sea anemone. Z Tierpsychol 62:209–234. doi: 10.1111/j.1439-0310.1983.tb02152.x CrossRefGoogle Scholar
  74. Wirtz P, d’Udekem-d’Acoz C (2001) Decapoda from Antipatharia, Gorgonaria and Bivalvia at the Cape Verde Islands. Helgoland Mar Res 55:112–115. doi: 10.1007/s101520100073 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Massimo Ponti
    • 1
  • Daniele Grech
    • 2
  • Mario Mori
    • 3
  • Rossella A. Perlini
    • 1
  • Vincenzo Ventra
    • 1
  • Pier Augusto Panzalis
    • 4
  • Carlo Cerrano
    • 3
  1. 1.Dipartimento di Scienze Biologiche, Geologiche e AmbientaliUniversity of Bologna, UO CoNISMaRavennaItaly
  2. 2.Integrative Marine Ecology - Benthos Lab (IME-BLAB)Stazione Zoologica Anton Dohrn di NapoliIschia, NaplesItaly
  3. 3.Dipartimento di Scienze della Vita e dell’AmbientePolytechnic University of Marche, UO CoNISMaAnconaItaly
  4. 4.Ufficio AmbienteConsorzio di Gestione dell’Area Marina Protetta di Tavolara – Punta Coda CavalloOlbiaItaly

Personalised recommendations