Infralittoral coralligenous reefs: a modified ESCA index for the ecological quality assessment


Published: Jul 15, 2025
Keywords:
infralittoral coralligenous reefs ecological quality Mediterranean Sea spatial variability
LUIGI PIAZZI
MARIA FRANCESCA CINTI
PAOLA GENNARO
Abstract

Coralligenous reefs characterize the circalittoral zone of the Mediterranean Sea, but, in many areas, they are also distributed within the infralittoral zone. Despite their wide distribution, the infralittoral coralligenous reefs are less considered in monitoring programs and no specific methods have yet been developed for their assessment. This study aims at testing a modified ESCA index (I-ESCA) on the infralittoral coralligenous reefs in order to propose a new tool suitable to evaluate the ecological quality of this habitat. Thirteen sites were sampled in the western Mediterranean Sea and the relationship between I-ESCA and the Anthropization Index was tested with a regression model in order to evaluate the response of the index to human pressures. Infralittoral coralligenous assemblages were dominated by macroalgae, while the bryozoan Myriapora truncata and the cnidarian Parazoanthus axinellae were the most widespread animals. The I-ESCA index allowed to highlight the level of human pressures of the sites similarly to ESCA. Thus, results of this study suggested the possibility of applying the index also to the infralittoral habitat using an adequate calibration of the original method on the new spatial scale and reference conditions.

Article Details
  • Section
  • Early View_vol. 26, n. 3, 2025
Downloads
Download data is not yet available.
References
Anderson, M.J., Willis, T.J., 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology, 84 (2), 511-524.
Anderson, M.J., 2006. Distance-based test for homogeneity of multivariate dispersions. Biometrics, 62, 245-253.
Anderson, M.J., Ellingsen, K.E., McArdle, B.H., 2006. Multivariate dispersion as a measure of β diversity. Ecology Letters, 9, 683-693.
Ballesteros, E., 1991. Structure of a deep-water community of Halimeda tuna (Chlorophyceae, Caulerpales) from the northwestern Mediterranean. Collectanea Botanica, 20, 5-21.
Ballesteros, E., 2006. Mediterranean Coralligenous assemblages: a synthesis of present knowledge. Oceanography and Marine Biology: An Annual Review, 44, 123-195.
Bevilacqua, S., Katsanevakis, S., Micheli, F., Sala, E., Rilov, G. et al., 2020. The Status of Coastal Benthic Ecosystems in the Mediterranean Sea: Evidence From Ecological Indicators. Frontiers in Marine Science, 7, 475.
Birk, S., Bonne, W., Borja, A., Brucet, S., Courrat, A. et al., 2012. Three hundred ways to assess Europe’s surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecological Indicators, 18, 31-41.
Borja, A., Elliott, M., Carstensen, J., Heiskanen, A.S., van de Bund, W., 2010. Marine management towards an integrated implementation of the European Marine Strategy Framework and the Water Framework Directives. Marine Pollution Bulletin, 60, 2175-2186.
Borja, A., Mader, J., Muxika, I., Rodríguez, J.G., Bald, J., 2008. Using M-AMBI in assessing benthic quality within the Water Framework Directive: Some remarks and recommendations. Marine Pollution Bulletin, 56, 1377–1379.
Cánovas-Molina, A., Montefalcone, M., Bavestrello, G., Cau, A., Bianchi C.N. et al., 2016. A new ecological index for the status of mesophotic megabenthic assemblages in the Mediterranean based on ROV photography and video footage. Continental Shelf Research, 121, 13-20.
Casas-Güell, E., Teixidó, N., Garrabou, J., Cebrian, E., 2015. Structure and biodiversity of coralligenous assemblages over broad spatial and temporal scales. Marine Biology, 162, 901-912.
Casoli, E., Piazzi, L., Nicoletti, L., Jona-Lasinio, G., Cecchi, E. et al., 2020. Ecology, distribution and demography of erect bryozoans in Mediterranean coralligenous reefs. Estuarine Coastal and Shelf Sciences, 235,106573.
Casoli, E., Moro, S., Falasca, M., Montefalcone, M., Rizzo, L. et al., 2024. Structure and diversity patterns of coralligenous cliffs across three ecoregions in the Central-Western Mediterranean Sea. Diversity and Distribution, 00, e13833.
Ceccherelli, G., Pinna, F., Pansini, A., Piazzi, L., La Manna, G., 2020. The constraint of ignoring the subtidal water climatology in evaluating the changes of coralligenous reefs due to heating events. Scientific Reports, 10, 17332.
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. European Journal of Phycology, 49, 298-312.
Cinar, M.E., Féral, J.P., Arvanitidis, C., Davis, R., Sini, M. et al., 2020. Coralligenous assemblages along their geographical distribution: Testing of concepts and implications for management. Aquatic Conservation: Marine and Freshwater Ecosystems, 30, 1578-1594.
Cocito, S., 2004. Bioconstruction and biodiversity: their mutual influence. Scientia Marina, 68, 137-144.
De Falco, G., Conforti, A., Brambilla, W., Budillon, F., Ceccherelli, G. et al., 2022. Mapping of coralligenous banks along the western and northern continental shelf of Sardinia Island (Mediterranean Sea). Journal of Maps, 18 (3), 1-10.
Deter, J., Descamp, P., Ballesta, L., Boissery, P., Holon, F., 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecological Indicators, 20, 345-352.
EU, 2000. Water Framework Directive 2000/60/EC of the European parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. Official Journal of the European Commission L 327, 1-72.
EU, 2008. Marine Strategy Framework Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for Community action in the field of marine environmental policy. Official Journal of the European Commission L 164/19, 22 pp.
Enrichetti, F., Bo, M., Morri, C., Montefalcone, M., Toma, M. et al., 2019. Assessing the environmental status of temperate mesophotic reefs: a new, integrated methodological approach. Ecological Indicators, 102, 218-229.
Ferrigno, F., Russo, G.F., Sandulli, R., 2017. Coralligenous bioconstructions Quality Index (CBQI): a synthetic indicator to assess the status of different types of coralligenous habitats. Ecological Indicators, 82, 271-279.
Gatti, G., Bianchi, C.N., Morri, C., Montefalcone, M., Sartoretto, S., 2015. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecological Indicators, 52, 567-576.
Gennaro, P., Piazzi, L., Cecchi, E., Montefalcone, M., Morri, C. et al., (Eds.), 2020. Monitoring and assessment of the ecological status of coralligenous habitat. The coralligenous cliff. ISPRA, Manuali e Linee Guida n.191bis/2020, 64 pp.
Gobert, S., Sartoretto, S., Rico-Raimondino, V., Andral, B., Chery, A. et al., 2009. Assessment of the ecological status of Mediterranean French coastal waters as required by the Water Framework Directive using the Posidonia oceanica Rapid Easy Index (PREI). Marine Pollution Bulletin, 58, 1727-1733.
Kipson, S., Fourt, M., Teixido, N., Cebrian, E., Casas, E., 2011. Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of Mediterranean coralligenous outcrops. PLoS ONE, 6, e27103.
Langlois, J., Guilhaumon, F., Bockel, T., Boissery, P., De Almeida Braga, C. et al., 2021. An integrated approach to estimate aesthetic and ecological values of coralligenous reefs. Ecological Indicators, 129, 107935.
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. Journal of Applied Ecology, 45, 688-699.
Martin, C.S., Giannoulaki, M., De Leo, F., Scardi, M., Salomidi, M. et al., 2014. Coralligenous and maërl habitats: predictive modelling to identify their spatial distributions across the Mediterranean Sea. Scientific Reports, 4, 5073.
Montefalcone, M., Morri, C., Bianchi, C.N., Bavestrello, G., Piazzi, L., 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Marine Pollution Bulletin, 117, 229-238.
Montefalcone, M., Tunesi, L., Ouerghi, A., 2021. A review of the classification systems for marine benthic habitats and the new updated Barcelona Convention classification for the Mediterranean. Marine Environmental Research, 169, 105387.
Penna, M., Gennaro, P., Bacci, T., Trabucco, B., Cecchi, E. et al., 2017. Multiple environmental descriptors to assess ecological status of sensitive habitats in the area affected by the Costa Concordia shipwreck (Giglio Island, Italy). Journal of Marine Biological Association of the United Kingdom, 98, 51-59.
Peres, J., Picard, J.M., 1964. Nouveau manuel de bionomie benthique de la mer Mediterranee. Recueil des Travaux de la Station Marine d’Endoume, 31, 1-131.
Piazzi, L., Gennaro, P., Cecchi, E., Serena, F., 2015. Improvement of the ESCA index for the evaluation of ecological quality of coralligenous habitat under the European Framework Directives. Mediterranean Marine Science, 16 (2), 419-426.
Piazzi, L., Gennaro, P., Cecchi, E., Serena, F., Bianchi, C.N., et al., 2017. Integration of ESCA index through the use of sessile invertebrates. Scientia Marina, 81, 283-290.
Piazzi, L., Atzori, F., Cadoni, N., Cinti, M.F., Frau, F. et al., 2018. Benthic mucilage blooms threaten coralligenous reefs. Marine Environmental Research, 140, 145-151.
Piazzi, L., Cecchi, E., Cinti, M.F., Stipcich, P., Ceccherelli, G., 2019a. Impact assessment of fish cages on coralligenous reefs: an opportunity to use the STAR sampling procedure. Mediterranean Marine Science, 20, 627-635.
Piazzi, L., Gennaro, P., Montefalcone, M., Bianchi, C.N., Cecchi, E. et al., 2019b. STAR: an integrated and standardized procedure to evaluate the ecological status of coralligenous reefs. Aquatic Conservation: Marine and Freshwater Ecosystems, 29, 189-201.
Piazzi, L., Cecchi, E., Cinti, M.F., Ceccherelli, G., 2021a. Extreme events and conservation of subtidal habitats: Effects of a rainfall flood on coralligenous reefs. Marine Pollution Bulletin, 165, 112106.
Piazzi, L., Gennaro, P., Cecchi, E., Bianchi, C.N., Cinti, M.F. et al., 2021b. Ecological Status of Coralligenous Assemblages: ten years of application of the ESCA index from local to wide scale validation. Ecological Indicators, 121, 107077.
Piazzi, L., Ferrigno, F., Guala, I., Cinti, M.F., Conforti, A. et al., 2022. Inconsistency in community structure and ecological quality between platform and cliff coralligenous assemblages. Ecological Indicators, 136, 108657.
Piazzi, L., Pacciardi, L., Pertusati, M., Pretti, C., De Biasi, A.M., 2023a. Infralittoral coralligenous reefs: structure and spatial variability of macroalgal assemblages. Scientia Marina, 87, e065.
Piazzi, L., Turicchia, E., Rindi, F., Falace, A., Gennaro, P. et al., 2023b. NAMBER: A biotic index for assessing the ecological quality of mesophotic biogenic reefs in the northern Adriatic Sea. Aquatic Conservation: Marine and Freshwater Ecosystems, 3, 298-311.
Piazzi, L., Gennaro, P., Azzola, A., Cinti M.F., Montefalcone, M., 2025. Advancing STAR: a revised protocol for assessing the ecological status of coralligenous cliffs. Marine Pollution Bulletin, 213, 117684.
Pinna, F., Piazzi, L., Cinti, M.F., Pansini, A., Stipcich, P. et al., 2021. Vertical variation of coralligenous cliff assemblages in marine biogeographic areas. Estuarine, Coastal and Shelf Science, 261, 107554.
Sartoretto, S., Schohn, T., Bianchi, C.N., Morri, C., Garrabou, J. et al., 2017. An integrated method to evaluate and monitor the conservation state of coralligenous habitats: the INDEX-COR approach. Marine Pollution Bulletin, 120, 222-231.
Sini, M., Garrabou, J., Trygonis, V., Koutsoubas, D., 2019. Coralligenous formations dominated by Eunicella cavolini (Koch, 1887) in the NE Mediterranean: biodiversity and structure. Mediterranean Marine Science, 20, 174-188.
SPA/RAC-UN ENVIRONMENT/MAP, 2021. Interpretation Manual of Marine Habitat Types in the Mediterranean Sea. UNEP/MAP-SPA/RAC publ., Tunis, 426 pp.
Teixidó, N., Casas, E., Cebrian, E., Linares, C., Garrabou, J., 2013. Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE, 8, e53742.
Thierry de Ville d’Avray, L., Ami, D., Chenuil, A., David, R., Féral, J.-P., 2019. Application of the ecosystem service concept at a small-scale: The cases of coralligenous habitats in the North-western Mediterranean Sea. Marine Pollution Bulletin, 138, 160-170.
Turicchia, E., Cerrano, C., Ghetta, M., Abbiati, M., Ponti, M., 2021. MedSens index: The bridge between marine citizen science and coastal management. Ecological Indicators, 122, 107296. UNEP, 2017. Action plan for the conservation of the coralligenous and other calcareous bio-concretions in the Mediterranean Sea. UNEP/MAP Athens, Greece, 20 pp.
Zapata-Ramírez, P.A., Scaradozzi, D., Sorbi, L., Palma, M., Pantaleo, U. et al., 2013. Innovative study methods for the Mediterranean coralligenous habitats. Advances in Oceanography and Limnology, 4, 102-119.
Most read articles by the same author(s)