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Comparing sessile benthos on shallow artificial versus natural hard substrates in the Eastern Mediterranean Sea

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Artificial structures cover a considerable part of the Mediterranean coasts. In the Aegean Sea, most studies related to artificial structures have focused in vagile fauna on harbors and marinas but little attention has been given to the sessile biota on coastal defense structures. The aim of this work was to describe for the first time the shallow sublittoral sessile benthos on coastal defense structures in Crete (Eastern Mediterranean Sea) in order to identify potential differences in comparison to natural rocky substrates, adopting both a taxonomic and functional (i.e. macroalgal structural complexity) approach. Three shallow (1-3 m) localities were studied in the north coast and three in the south coast of the island (six localities in total). At each locality, two types of hard substrate were selected: an artificial coastal defense structure (rip-rap) and the nearest natural rocky substrates. The percent cover of sessile taxa was calculated using random points counts over photoquadrats (20 x 20 cm). The structure of the assemblage differed between artificial and natural habitats. Values of Shannon-Wiener’s diversity index and number of taxa were higher in natural substrates. In addition, cover of arborescent macroalgae was lower on artificial substrates. In conclusion, rip-raps do not function as surrogates of natural hard substrates in the study area since their shallow subtidal assemblages differ in terms of community structure, diversity and functionality. The deficient performance of such artificial structures could be attributed to the combined effects of abiotic factors and biotic processes, including substrate nature and roughness as well as differential grazing pressure.


Assemblage structure; defense structures; rip-rap; rocky reefs; surrogates;macroalgae; structural complexity.

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Airoldi, L., 2000. Effects of disturbance, life histories, and overgrowth on coexistence of algal crusts and turfs. Ecology, 81 (3), 798-814.

Airoldi, L., Beck, M.W., 2007. Loss, status and trends for coastal marine habitats of Europe. Oceanography and Marine Biology: An Annual Review, 45, 345-405.

Airoldi, L., Bulleri, F., 2011. Anthropogenic disturbance can determine the magnitude of opportunistic species responses on marine urban infrastructures. PLoS One, 6 (8), e22985.

Anderson, M.J., Gorley R.N., Clarke K.R., 2008. PERMANOVA for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, 214 pp.

Anderson, M.J., Walsh, D.C.I., 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monographs, 83 (4), 557-574.

Arenas, F., Sánchez, I., Hawkins, S.J., Jenkins, S.R., 2006. The invasibility of marine algal assemblages: role of functional diversity and identity. Ecology, 87 (11), 2851-2861.

Bacchiocchi, F., Airoldi, L., 2003. Distribution and dynamics of epibiota on hard structures for coastal protection. Estuarine Coastal and Shelf Science, 56, 1157-1166.

Ballesteros, E., 1993. Species composition and structure of a photophilic algal community dominated by Halopteris scoparia (L.) Sauvageau from the North-Western Mediterranean. Collectanea Botanica, 22, 5-24.

Ballesteros, E., Torras, X., Pinedo, S., García, M., Mangialajo, L. et al., 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Marine Pollution Bulletin, 55 (1-6), 172-180.

Benedetti-Cecchi, L., Pannacciulli, F., Bulleri, F., Moschella, P.S., Airoldi, L. et al., 2001. Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Marine Ecology Progress Series, 214, 137-150.

Bianchi, C.N., Pronzato, R., Cattaneo-Vietti, R., Benedetti Cecchi, L., Morri, C. et al., 2004. Hard bottoms. p. 185-215. In: Mediterranean marine benthos: a manual of methods for its sampling and study. Gambi, M.C., Dappiano, M. (Eds.). Biologia Marina Mediterranea 11 (Suppl. 1). SIBM, Genoa.

Boetius, A., Scheibe, S., Tselepides, A., Thiel, H., 1996. Microbial biomass and activities in deep-sea sediments of the Eastern Mediterranean: trenches and benthic hotspots. Deep-Sea Research, 43 (9), 1439-1460.

Boudouresque, C.F., 1971. Contribution à l'étude phytosociologique des peuplements algaux des côtes varoises. Vegetatio, 22 (1-3), 83-184.

Bulleri, F., 2005. Experimental evaluation of early patterns of colonisation of space on rocky shores and seawalls. Marine Environmental Research, 60 (3), 355-374.

Bulleri, F., 2006. Duration of overgrowth affects survival of encrusting coralline algae. Marine Ecology Progress Series, 321, 79-85.

Bulleri, F., Chapman, M.G., 2010. The introduction of coastal infrastructure as a driver of change in marine environments. Journal of Applied Ecology, 47 (1), 26-35.

Bulleri, F., Tamburello, L., Benedetti‐Cecchi, L., 2009. Loss of consumers alters the effects of resident assemblages on the local spread of an introduced macroalga. Oikos, 118 (2), 269-279.

Cacabelos, E., Martins, G.M., Thompson, R., Prestes, A.C., Azevedo, J.M.N. et al., 2016. Material type and roughness influence structure of inter‐tidal communities on coastal defenses. Marine Ecology, 37 (4), 801-812.

Chapman, M.G., Underwood, A.J., 2011. Evaluation of ecological engineering of “armoured” shorelines to improve their value as habitat. Journal of Experimental Marine Biology and Ecology, 400 (1-2), 302-313.

Chatzigeorgiou, G., Faulwetter, S., López, E., Sardá, R., Arvanitidis, C., 2012. Can coastal biodiversity measured in four Mediterranean sites be representative of the region? A test for the robustness of the NaGISA protocol by using the hard substrate syllid (Annelida, Polychaeta) taxo-communities as a surrogate. Hydrobiologia, 691, 147-156.

Chatzinikolaou, E., Arvanitidis, C., 2016. Status, values and present threats in Heraklion harbour (Crete, Greece). Regional Studies in Marine Science, 8, 252-258.

Chatzinikolaou, E., Mandalakis, M., Damianidis, P., Dailianis, T., Gambineri, S. et al., 2018. Spatio-temporal benthic biodiversity patterns and pollution pressure in three Mediterranean touristic ports. Science of The Total Environment, 624, 648-660.

Cheminée, A., Pastor, J., Bianchimani, O., Thiriet, P., Sala, E. et al., 2017. Juvenile fish assemblages in temperate rocky reefs are shaped by the presence of macro-algae canopy and its three-dimensional structure. Scientific Reports, 7 (1), 14638.

Chintiroglou, C.C., Antoniadou, C., Baxevanis, A., Damianidis, P., Karalis, P. et al., 2004. Peracarida populations of hard substrate assemblages in ports of the NW Aegean Sea (eastern Mediterranean). Helgoland Marine Research, 58 (1), 54.

Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology, 18, 17-143.

Coleman, R.A., Underwood, A.J., Benedetti-Cecchi, L., Åberg, P., Arenas, F. et al., 2006. A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia, 147 (3), 556-564.

Coombes, M.A., La Marca, E.C., Naylor, L.A., Thompson, R.C., 2015. Getting into the groove: opportunities to enhance the ecological value of hard coastal infrastructure using fine-scale surface textures. Ecological Engineering, 77, 314-323.

Corsini-Foka, M., Zenetos, A., Crocetta, F., Çinar, M.E., Koçak, F. et al., 2015. Inventory of alien and cryptogenic species of the Dodecanese (Aegean Sea, Greece): collaboration through COST action training school. Management of Biological Invasions, 6 (4), 351-366.

Crooks, J.A., 2002. Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos, 97, 153-166.

Dafforn, K.A., Glasby, T.M., Airoldi, L., Rivero, N.K., Mayer-Pinto, M. et al., 2015. Marine urbanization: an ecological framework for designing multifunctional artificial structures. Frontiers in Ecology and the Environment, 13 (2), 82-90.

Dafforn, K.A., Johnston, E.L., Glasby, T.M., 2009. Shallow moving structures promote marine invader dominance. Biofouling, 25 (3), 277-287.

Dal Bello, M., Leclerc, J.C., Benedetti-Cecchi, L., De Lucia, G.A., Arvanitidis, C. et al., 2016. Consistent patterns of spatial variability between NE Atlantic and Mediterranean rocky shores. Journal of the Marine Biological Association of the United Kingdom, 97 (3), 539-547.

Deudero, S., Frau, A., Cerda, M., Hampel, H., 2005. Distribution and densities of the decapod crab Percnon gibbesi, an invasive Grapsidae, in western Mediterranean waters. Marine Ecology Progress Series, 285, 151-156.

Fabi, G., Spagnolo, A., Bellan-Santini, D., Charbonnel, E., Çiçek, B.A. et al., 2011. Overview on artificial reefs in Europe. Brazilian Journal of Oceanography, 59 (SPE1), 155-166.

Fernandez-Gonzalez, V., Sanchez-Jerez, P., 2017. Fouling assemblages associated with off-coast aquaculture facilities: an overall assessment of the Mediterranean Sea. Mediterranean Marine Science, 18 (1), 87-96.

Ferrario, F., Iveša, L., Jaklin, A., Perkol‐Finkel, S., Airoldi, L., 2016. The overlooked role of biotic factors in controlling the ecological performance of artificial marine habitats. Journal of Applied Ecology, 53 (1), 16-24.

Ferrario, J., Caronni, S., Occhipinti-Ambrogi, A., Marchini, A., 2017. Role of commercial harbours and recreational marinas in the spread of non-indigenous fouling species. Biofouling, 33 (8), 651-660.

Firth, L.B., Thompson, R.C., Bohn, K., Abbiati, M., Airoldi, L. et al., 2014. Between a rock and a hard place: environmental and engineering considerations when designing coastal defence structures. Coastal Engineering, 87, 122-135.

Firth, L.B., Knights, A.M., Bridger, D., Evans, A., Mieskowska, N. et al., 2016a. Ocean sprawl: challenges and opportunities for biodiversity management in a changing world. Oceanography and Marine Biology: An Annual Review, 54, 193-269.

Firth, L.B., White, F.J., Schofield, M., Hanley, M.E., Burrows, M.T. et al., 2016b. Facing the future: the importance of substratum features for ecological engineering of artificial habitats in the rocky intertidal. Marine and Freshwater Research, 67 (1), 131-143.

Forrest, B.M., Fletcher, L.M., Atalah, J., Piola, R.F., Hopkins, G.A., 2013. Predation limits spread of Didemnum vexillum into natural habitats from refuges on anthropogenic structures. PLoS One, 8 (12), e82229.

Foster, M.S., Nigg, E.W., Kiguchi, L.M., Hardin, D.D., Pearse, J.S., 2003. Temporal variation and succession in an algal-dominated high intertidal assemblage. Journal of Experimental Marine Biology and Ecology, 289 (1), 15-39.

Fraschetti, S., Terlizzi, A., Benedetti-Cecchi, L., 2005. Patterns of distribution of marine assemblages from rocky shores: evidence of relevant scales of variation. Marine Ecology Progress Series, 296, 13-29.

Gacia, E., Satta, M.P., Martín, D., 2007. Low crested coastal defence structures on the Catalan coast of the Mediterranean Sea: how they compare with natural rocky shores. Scientia Marina, 71 (2), 259-267.

García‐Gómez, J.C., Guerra‐García, J.M., Espinosa, F., Maestre, M.J., Rivera‐Ingraham, G. et al., 2015. Artificial marine micro‐reserves networks (AMMRNs): an innovative approach to conserve marine littoral biodiversity and protect endangered species. Marine Ecology, 36 (3), 259-277.

Gerovasileiou, V., Akel, E.H.KH., Akyol, O., Alongi, G., Azevedo, F. et al., 2017. New Mediterranean biodiversity records (July 2017). Mediterranean Marine Science, 18 (2), 355-384.

Glasby, T.M., 2000. Surface composition and orientation interact to affect subtidal epibiota. Journal of Experimental Marine Biology and Ecology, 248(2), 177-190.

Glasby, T.M., Connell, S.D., 2001. Orientation and position of substrata have large effects on epibiotic assemblages. Marine Ecology Progress Series, 214, 127-135.

Glasby, T.M., Connell, S.D., Holloway, M.G., Hewitt, C.L., 2007. Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Marine biology, 151(3), 887-895.

Ido, S., Shimrit, P.F., 2015. Blue is the new green–ecological enhancement of concrete based coastal and marine infrastructure. Ecological Engineering, 84, 260-272.

Karalis, P., Antoniadou, C., Chintiroglou, C.C., 2003. Structure of the artificial hard substrate assemblages in ports in Thermaikos Gulf (North Aegean Sea). Oceanologica Acta, 26 (3), 215-224.

Katsanevakis, S., Poursanidis, D., Issaris, Y., Tsiamis, K., Salomidi, M. et al., 2010. The invasive crab Percnon gibbesi (Crustacea: Decapoda: Plagusiidae) is spreading in the Aegean and Ionian Seas. Marine Biodiversity Records, 3, e53.

Katsanevakis, S., Sini, M., Dailianis, T., Gerovasileiou, V., Koukourouvli, N. et al., 2017. Identifying where vulnerable species occur in a data-poor context: combining satellite imaging and underwater occupancy surveys. Marine Ecology Progress Series, 577, 17-32.

Klaoudatos, D.S., Anastasopoulou, A., Papaconstantinou, C., Conides, A.I., 2012. The Greek experience of artificial reef construction and management. Journal of Environmental Protection and Ecology, 13 (3A), 1647-1655.

Kruskal, J.B., Wish, M., 1978. Multidimensional Scaling. Series on Quantitative Applications in the Social Sciences, 07-011. Sage Publications, Beverly Hills and London, 98 pp.

Lam, N.W., Huang, R., Chan, B.K., 2009. Variations in Intertidal assemblages and zonation patterns between vertical artificial seawalls and natural rocky shores: A case study from Victoria Harbour, Hong Kong. Zoological Studies, 48 (2), 184-195.

Lazaridou, E., Orfanidis, S., Haritonidis, S., Seferlis, M., 1997. Impact of eutrophication on species composition and diversity of macrophytes in the gulf of Thessaloniki, Macedonia, Greece: first evaluation of the results of one year study. Fresenius Environmental Bulletin, 6, 54-59.

Lök, A., Gül, B., Ulas, A., Düzbastılar, F.O., Metin, C., 2008. Diel variations on the fish assemblages at artificial reefs in two different environments of the Aegean Sea (Western Coast of Turkey). Turkish Journal of Fisheries and Aquatic Sciences, 8, 79-85.

Loke, L.H., Ladle, R.J., Bouma, T.J., Todd, P.A., 2015. Creating complex habitats for restoration and reconciliation. Ecological Engineering, 77, 307-313.

López, I., Tinoco, H., Aragonés, L., Garcia-Barba, J., 2016. The multifunctional artificial reef and its role in the defence of the Mediterranean coast. Science of the Total Environment, 550, 910-923.

Maggi, E., Bertocci, I., Vaselli, S., Benedetti-Cecchi, L., 2009. Effects of changes in number, identity and abundance of habitat-forming species on assemblages of rocky seashores. Marine Ecology Progress Series, 381, 39-49.

Martínez-Laiz, G., Ros, M., Guerra-García, J.M., 2018. Marine exotic isopods from the Iberian Peninsula and nearby waters. PeerJ, 6, e4408.

Marzinelli, E.M., Underwood, A.J., Coleman, R.A., 2011. Modified habitats influence kelp epibiota via direct and indirect effects. PLoS One, 6 (7), e21936.

McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biological Conservation, 127, 247-260.

Mercader, M., Mercière, A., Saragoni, G., Cheminée, A., Crec’hriou, R., et al., 2017. Small artificial habitats to enhance the nursery function for juvenile fish in a large commercial port of the Mediterranean. Ecological Engineering, 105, 78-86.

Moreira, J., Chapman, M.G., Underwood, A.J., 2006. Seawalls do not sustain viable populations of limpets. Marine Ecology Progress Series, 322, 179-188.

Moschella, P.S., Abbiati, M., Åberg, P., Airoldi, L., Anderson, J.M. et al., 2005. Low-crested coastal defence structures as artificial habitats for marine life: using ecological criteria in design. Coastal Engineering, 52 (10-11), 1053-1071.

Odum, E.P., 1985. Trends Expected in Stressed Ecosystems. BioScience, 35 (7), 419-422.

Ólafsson, E. (Ed.), 2017. Marine Macrophytes as Foundation Species. CRC Press, USA, 285 pp.

Orfanidis, S., Panayotidis, P., Siakavara, A., 2005. Benthic macrophytes: main trends in diversity and distribution. p. 226-235. In: State of the Hellenic Environment (SoHelME). Papathanassiou, E., Zenetos, A. (Eds). HCMR Publication.

Orfanidis, S., Panayotidis, P., Stamatis, N., 2001. Ecological evaluation of transitional and coastal waters: A marine benthic macrophytes-based model. Mediterranean Marine Science, 2 (2), 45-65.

Orfanidis, S., Panayotidis, P., Stamatis, N., 2003. An insight to the ecological evaluation index (EEI). Ecological Indicators, 3 (1), 27-33.

Ostalé-Valriberas, E.; Sempere-Valverde, J.; Coppa, S.; García-Gómez, J.C.; Espinosa, F., In press. Creation of microhabitats (tidepools) in ripraps with climax communities as a way to mitigate negative effects of artificial substrate on marine biodiversity. Ecological Engineering

Peckol, P., Rivers, J.S., 1995. Physiological responses of the opportunistic macroalgae Cladophora vagabunda (L.) van den Hoek and Gracilaria tikvahiae (McLachlan) to environmental disturbances associated with eutrophication. Journal of Experimental Marine Biology and Ecology, 190 (1), 1-16.

Pérès, J.M., Picard, J., 1958. Recherches sur les peuplements benthiques de la Miditerranιe nord-orientale. Annales de l’Institute Oceanographique, 34, 213-291.

Perkins, M.J., Ng, T.P., Dudgeon, D., Bonebrake, T.C., Leung, K.M., 2015. Conserving intertidal habitats: what is the potential of ecological engineering to mitigate impacts of coastal structures? Estuarine, Coastal and Shelf Science, 167, 504-515.

Perkol-Finkel, S., Benayahu, Y., 2004. Community structure of stony and soft corals on vertical unplanned artificial reefs in Eilat (Red Sea): comparison to natural reefs. Coral reefs, 23 (2), 195-205.

Poursanidis, D., Koutsoubas, D., Arvanitidis, C., Chatzigeorgiou, G., 2016. ReefMedMol: Mollusca from the infralittoral rocky shores - the biocoenosis of photophilic algae - in the Mediterranean Sea. Biodiversity Data Journal 4, e7516.

Puccio, V., Relini, M., Azzurro, E., Relini, L.O., 2006. Feeding habits of Percnon gibbesi (H. Milne Edwards, 1853) in the Sicily Strait. Hydrobiologia, 557, 79.

Rilov, G., Galil, B., 2009. Marine Bioinvasions in the Mediterranean Sea – History, Distribution and Ecology. p. 549-575. In: Biological Invasions in Marine Ecosystems: Ecological, Management, and Geographic Perspectives. Rilov, G., Crooks, J.A. (Eds). Springer, Berlin.

Ros, M., Guerra-García., J.M., Navarro-Barranco., C., Cabezas, M.P., Vázquez-Luis, M., 2014. The spreading of the non-native caprellid (Crustacea: Amphipoda) Caprella scaura Templeton, 1836 into southern Europe and northern Africa: a complicated taxonomic history. Mediterranean Marine Science, 15 (1), 145-155.

Salomidi, M., Giakoumi, S., Gerakaris, V., Issaris, Y., Sini, M. et al., 2016. Setting an ecological baseline prior to the bottom-up establishment of a marine protected area in Santorini Island, Aegean Sea. Mediterranean Marine Science, 17 (3), 720-737.

Salomidi, M., Katsanevakis, S., Issaris, Y., Tsiamis, K., Katsiaras, N., 2013. Anthropogenic disturbance of coastal habitats promotes the spread of the introduced scleractinian coral Oculina patagonica in the Mediterranean Sea. Biological Invasions, 15(9), 1961-1971.

Sempere-Valverde, J., Ostalé-Valrriberas, E., Farfán, G.M., Espinosa, F., 2018. Substratum type affects recruitment and development of marine assemblages over artificial substrata: A case study in the Alboran Sea. Estuarine, Coastal and Shelf Science, 204, 56-65.

Sinis, A.I., Chintiroglou, C.C., Stergiou, K.I., 2000. Preliminary results from the establishment of experimental artificial reefs in the N. Aegean Sea (Chalkidiki, Greece). Belgian Journal of Zoology, 130 (Supplement), 143-147.

Strain, E.M., Olabarria, C., Mayer‐Pinto, M., Cumbo, V., Morris, R.L. et al., 2018. Eco‐engineering urban infrastructure for marine and coastal biodiversity: Which interventions have the greatest ecological benefit? Journal of Applied Ecology, 55 (1), 426-441.

Theocharis, A., Balopoulos, E., Kioroglou, S., Kontoyiannis, H., Iona, A., 1999. A synthesis of the circulation and hydrography of the South Aegean Sea and the Straits of the Cretan Arc (March 1994–January 1995). Progress in Oceanography, 44 (4), 469-509.

Thiriet, P.D., Di Franco, A., Cheminée, A., Guidetti, P., Bianchimani, O. et al., 2016. Abundance and diversity of crypto-and necto-benthic coastal fish are higher in marine forests than in structurally less complex macroalgal assemblages. PloS One, 11 (10), e0164121.

Tofts, R., Silvertown, J., 2000. A phylogenetic approach to community assembly from a local species pool. Proceedings of the Royal Society B, 267, 363-369.

Trygonis, V., Sini, M., 2012. PhotoQuad: a dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. Journal of Experimental Marine Biology and Ecology, 424-425, 99-108.

Tsirintanis, K., Sini, M., Doumas, O., Trygonis, V., Katsanevakis, S., 2018. Assessment of grazing effects on phytobenthic community structure at shallow rocky reefs: An experimental field study in the North Aegean Sea. Journal of Experimental Marine Biology and Ecology, 503, 31-40.

Ulman, A., Ferrario, J., Occhpinti-Ambrogi, A., Arvanitidis, C., Bandi, A. et al., 2017. A massive update of non-indigenous species records in Mediterranean marinas. PeerJ, 5, e3954.

Underwood, A.J., 1981. Techniques of analysis of variance in experimental biology and ecology. Oceanography and Marine Biology: An Annual Review, 19, 513-605.

Underwood, A.J., 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, 504 pp.

Underwood, A.J., Chapman, M.G., Richards, S.A., 2002. GMAV-5 for Windows. An Analysis of Variance Programme. University of Sydney, Australia.

Underwood, A.J., Jernakoff, P., 1984. The effects of tidal height, wave-exposure, seasonality and rock-pools on grazing and the distribution of intertidal macroalgae in New South Wales. Journal of Experimental Marine Biology and Ecology, 75 (1), 71-96.

Ushiama, S., Smith, J.A., Suthers, I.M., Lowry, M., Johnston, E.L., 2016. The effects of substratum material and surface orientation on the developing epibenthic community on a designed artificial reef. Biofouling, 32 (9), 1049-1060.

Verlaque, M., Ruitton, S., Mineur, F., Boudouresque, C.F., 2015. Vol.4. Macrophytes. In: Briand, F., (Ed.), CIESM Atlas of exotic species in the Mediterranean, CIESM Publishers, Monaco, 360 pp.

WORMS, 2018. World Register of Marine Species. http://www.marinespecies.org (Accessed 28 June 2018).