sm81n2-4565

Integration of ESCA index through the use of sessile invertebrates

Luigi Piazzi 1, Paola Gennaro 2, Enrico Cecchi 3, Fabrizio Serena 3-5, Carlo Nike Bianchi 4, Carla Morri 4, Monica Montefalcone 4

1 Dipartimento di Scienze della Natura e del Territorio, Università di Sassari, Via Piandanna 4, 07100 Sassari, Italy.
(LP) (Corresponding author) E-mail: lpiazzi@uniss.it. ORCID-iD: http://orcid.org/0000-0003-3061-0187
2 Italian National Institute for Environmental Protection and Research (ISPRA ex ICRAM), Via di Castel Romano 100, 00128, Roma, Italy.
(PG) E-mail: paola.gennaro@isprambiente.it. ORCID-iD: http://orcid.org/0000-0002-4569-8209
3 ARPAT - Agenzia Regionale per la Protezione Ambientale della Toscana, Via Marradi 114, 57126 Livorno, Italy.
(EC) E-mail: e.cecchi@arpat.toscana.it. ORCID-iD: http://orcid.org/0000-0002-8910-891X
(FS) E-mail: fabrizio.serena@arpat.toscana.it. ORCID-iD: http://orcid.org/0000-0001-5198-7288
4 DISTAV, University of Genoa, Corso Europa 26, 16132 Genoa, Italy.
(CNB) E-mail: nbianchi@dipteris.unige.it. ORCID-iD: http://orcid.org/0000-0003-1071-3285
(CM) E-mail: morric@dipteris.unige.it. ORCID-iD: http://orcid.org/0000-0003-4520-2741
(MM) E-mail: montefalcone@dipteris.unige.it. ORCID-iD: http://orcid.org/0000-0002-3851-1880
5 CNR–IAMC, Via Vaccara 61, 91026 Mazara del Vallo (TP), Italy.

Summary: The ESCA (Ecological Status of Coralligenous Assemblages) index was developed to assess the ecological quality of coralligenous habitat using macroalgae as a biological indicator. The aim of this study was to evaluate the response to human-induced pressures of macroalgae and sessile macro-invertebrates shaping the coralligenous habitat and to integrate their sensitivity into the ESCA index. Coralligenous assemblages were sampled at 15 locations of the NW Mediterranean Sea classified into three groups: i) marine protected areas; ii) low urbanized locations; and iii) highly urbanized locations. A sensitivity level value was assigned to each taxon/group on the basis of its abundance in each environmental condition, the data available in the literature and the results of an expert judgement survey. The index that includes the totality of the assemblages (named ESCA-TA), calculated using both macroalgae and sessile macro-invertebrates, detected the levels of human pressure more precisely than the index calculated with only macroalgae or with only invertebrates. The potential for assessing the ecological quality of marine coastal areas was thus increased with the ESCA-TA index thanks to the use of a higher variety of descriptors.

Keywords: coralligenous assemblages; ESCA and ESCA-TA indices; ecological quality; macroalgae; macro-invertebrates; Mediterranean Sea.

Integración de el índice ESCA por medio de los macro-invertebrados sésiles

Resumen: El índice ESCA (Estado Ecológico de las Comunidades Coralígenas) ha sido desarrollado para determinar el estado ecológico de los hábitats coralígenos utilizando macro-algas como indicador biológico. El objetivo de este estudio fue evaluar la respuesta, ante presiones antropogénicas, de macro-algas y macro-invertebrados sésiles moldeadores de la comunidad coralígena y su sensibilidad al índice ESCA. Se muestrearon comunidades coralígenas en 15 localizaciones del Mediterráneo Nord-Occidental clasificadas en 3 grupos: i) áreas marinas protegidas; ii) poco urbanizadas; iii) muy urbanizadas. Un valor de Nivel de Sensibilidad fue asignado a cada taxón/grupo en base a su abundancia en cada condición medioambiental, a información bibliográfica disponible y a los resultados de juicios por parte de expertos. El índice que integra la totalidad de las comunidades (llamado ESCA-TA), calculado usando tanto macro-algas como macro-invertebrados sésiles, detectó los diferentes niveles de presión humana de manera más precisa que el índice calculado solo con macro-algas o solo con invertebrados. El potencial para determinar el estado ecológico de las áreas marinas protegidas se incrementó con el índice ESCA-TA gracias al uso de una mayor variedad de descriptores.

Palabras clave: comunidades coralígenas; índices ESCA y ESCA-TA; estado ecológico; macro-algas; macro-invertebrados; mar Mediterráneo.

Citation/Como citar este artículo: Piazzi L., Gennaro P., Cecchi E., Serena F., Bianchi C.N., Morri C., Montefalcone M. 2017. Integration of ESCA index through the use of sessile invertebrates. Sci. Mar. 81(2): 283-290. doi: http://dx.doi.org/10.3989/scimar.04565.01B

Editor: E. Cebrián.

Received: October 10, 2016. Accepted: January 18, 2017. Published: April 26, 2017.

Copyright: © 2017 CSIC. This is an open-access article distributed under the terms of the Creative Commons Attribution (CC-by) Spain 3.0 License.

Contents

Summary
Resumen
Introduction
Materials and methods
Results
Discussion
Acknowledgements
References

INTRODUCTIONTop

Coralligenous habitat is a biocostruction composed primarily by calcareous red algae belonging to Corallinales and Pessonneliales and secondarily by Cnidaria, Polychaeta and Bryozoa (Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Annu. Rev. 44: 123-195.). It is one of the most important coastal ecosystems of the Mediterranean Sea for distribution, biodiversity, productivity and role in the CO2 cycle (Bertolino et al. 2013Bertolino M., Cerrano C., Bavestrello G., et al. 2013. Diversity of Porifera in the Mediterranean coralligenous accretions, with description of a new species. ZooKeys 336: 1-37., Martin et al. 2014Martin C.S., 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. 4: 5073., Casas-Guell et al. 2015Casas-Guell E., Teixidó N., Garrabou J., et al. 2015. Structure and biodiversity of coralligenous assemblages over broad spatial and temporal scales. Mar. Biol. 162: 901-912.). Coralligenous habitat is considered sensitive to human activities (Piazzi et al. 2012Piazzi L., Gennaro P., Balata D. 2012. Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar. Pollut. Bull. 64: 2623-2629., Cánovas Molina et al. 2016Cánovas Molina A., Montefalcone M., Vassallo P., et al. 2016. Combining literature review, acoustic mapping and in situ observations: an overview of coralligenous assemblages in Liguria (NW Mediterranean Sea). Sci. Mar. 80: 7-16.) and has been included in the protection programme of European legislation (e.g. the Habitats Directive 92/43/EEC; the Marine Strategy Framework Directive 2008/56/EEC) as a habitat of high scientific interest and biodiversity (“special habitat type” sensu MSFD 2008/56/EEC) (EC 2008EC. 2008. 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 (Marine Strategy Framework Directive). Official Journal of the European Commission, G.U.C.E. 25/6/2008, L 164/19.). The development of monitoring programmes to manage and conserve special marine habitats requires effective descriptors to evaluate their ecological status and to detect changes in their ecological quality (Birk et al. 2012Birk S., Bonne W., Borja 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. Ecol. Ind. 18: 31-41.). Several indices have been proposed for assessing the ecological quality of coralligenous assemblages: the Coralligenous Assemblage Index (CAI) (Deter et al. 2012Deter J., Descamp P., Ballista L., et al. 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecol. Ind. 20: 345-352.), the Coralligenous Assessment by ReefScape Estimate (COARSE) (Gatti et al. 2015aGatti G., Bianchi C.N., Morri C., et al. 2015a. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol. Ind. 52: 567-576.), the INDEX-COR (Sartoretto et al. 2014Sartoretto S., David R., Aurelle D., et al. 2014. An integrated approach to evaluate and monitor the conservation state of coralligenous bottoms: the INDEX-COR method. In: Bouafif C., Langar H., Ouerghi A. (eds), Proceedings of the second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio-Concretions (Portorož, Slovenia, 29-30 October 2014). UNEP/MAP – RAC/SPA, RAC/SPA publ., Tunis: pp. 159-165.) and the Ecological Status of Coralligenous Assemblages (ESCA) (Cecchi et al. 2014Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717., Piazzi et al. 2015Piazzi L., Gennaro P., Cecchi E., et al. 2015. Improvement of the ESCA index for the evaluation of ecological quality of coralligenous habitat under the European Framework Directives. Medit. Mar. Sci. 16: 419-426.).

Several studies concerning responses of coralligenous assemblages to environmental stress have considered macroalgae as an effective biological indicator (Balata et al. 2007aBalata D., Piazzi L., Benedetti-Cecchi L. 2007a. Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 8: 2455-2461., Piazzi et al. 2011Piazzi L., Gennaro P., Balata D. 2011. Effects of nutrient enrichment on macroalgal coralligenous assemblages. Mar. Pollut. Bull. 62: 1830-1835., 2012Piazzi L., Gennaro P., Balata D. 2012. Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar. Pollut. Bull. 64: 2623-2629.) and results of these studies were used to develop the ESCA index. Conversely, little is known about the response of sessile coralligenous macro-invertebrates to stress, even if some taxa are recognized to be sensitive to human-induced alterations (Bavestrello et al. 1997Bavestrello G., Cerrano C., Zanzi D., et al. 1997. Damage by fishing activities in the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aq. Conserv. Mar. Freshwater Ecosyst. 7: 253-262., Garrabou et al. 1998Garrabou J., Sala E., Arcas A., et al. 1998. The impact of diving on rocky sub-littoral communities: a case study of a bryozoan population. Conserv. Biol. 12: 302-312., Gatti et al. 2015bGatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581.). The concurrent use of both macroalgae and sessile macro-invertebrates allows a wider spectrum of human-induced alterations to be detected than when a single component is used, thus better evaluating the ecological quality of coralligenous assemblages (Kipson et al. 2011Kipson S., Fourt M., Teixidó N., et al. 2011. Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of Mediterranean coralligenous outcrops. PLoS ONE 6: e27103., Sartoretto et al. 2014Sartoretto S., David R., Aurelle D., et al. 2014. An integrated approach to evaluate and monitor the conservation state of coralligenous bottoms: the INDEX-COR method. In: Bouafif C., Langar H., Ouerghi A. (eds), Proceedings of the second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio-Concretions (Portorož, Slovenia, 29-30 October 2014). UNEP/MAP – RAC/SPA, RAC/SPA publ., Tunis: pp. 159-165., Gatti et al. 2012Gatti G., Montefalcone M., Rovere A., et al. 2012. Seafloor integrity down the harbor waterfront: the coralligenous shoals off Vado Ligure (NW Mediterranean). Adv. Limnol. 3: 51-67.).

The aim of this study was to evaluate the response to environmental alterations of macroalgae and sessile macro-invertebrates shaping the coralligenous habitat and to integrate their sensitivity into the ESCA index. To achieve these objectives, coralligenous assemblages subjected to three different levels of human-induced pressure (protected, low urbanized and highly urbanized) were studied within a large geographic area of the western Mediterranean Sea. We adopted the scale of sensitivity of coralligenous species to human pressures developed by Montefalcone et al. (2017)Montefalcone M., Morri C., Bianchi C.N., et al. 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar. Pollut. Bull. 117: 229-238. on the basis of expert judgement. We compared the effectiveness of the three ESCA indices, calculated using only macroalgae, only macro-invertebrates, and the total assemblage.

MATERIALS AND METHODSTop

Coralligenous assemblages were sampled at 15 locations of the NW Mediterranean Sea classified into three groups according to the level of human-induced pressure they are affected by. Five locations were in marine protected areas (MPAs) (Portofino, Montecristo Island, Pianosa Island, Tavolara Island and Asinara Island), five locations were unprotected but with a low level of urbanization (l-U) (Vada Shoals, Elba Island, Giglio Island, Argentario and Costa Paradiso) and five locations were subjected to a high level of urbanization (h-U) (Livorno, Piombino, Sant’Agostino, Civitavecchia and Santa Marinella) (Fig. 1). The level of urbanization for each location was determined according to the presence of local pressures (e.g. industries, ports and rivers) and the distance of the studied locations from these sources of pressure (Lopez y Royo et al. 2009Lopez y Royo C., Silvestri C., Pergent G., et al. 2009. Assessment of human-induced pressures on the coastal zone, using publicly available data. J. Environ. Manag. 90: 1494-1501., Piazzi et al. 2015Piazzi L., Gennaro P., Cecchi E., et al. 2015. Improvement of the ESCA index for the evaluation of ecological quality of coralligenous habitat under the European Framework Directives. Medit. Mar. Sci. 16: 419-426.). Although pristine ecosystems in the Mediterranean Sea can no longer be expected (Jackson and Sala 2001Jackson J.B., Sala E. 2001. Unnatural oceans. Sci. Mar. 65: 273-281., Stachowitsch 2003Stachowitsch M. 2003. Research on intact marine ecosystems: a lost era. Mar. Pollut. Bull. 46: 801-805.) and the boundaries of MPAs do not protect them from the effects of global impacts such as climate change and water turbidity (Montefalcone et al. 2009Montefalcone M., Albertelli G., Morri C., et al. 2009. Legal protection is not enough: Posidonia oceanica meadows in marine protected areas are not healthier than those in unprotected areas of the northwest Mediterranean Sea. Mar. Pollut. Bull. 58: 515-519., Parravicini et al. 2013Parravicini V., Micheli F., Montefalcone M., et al. 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. PLoS ONE 8: e75767., Mateos-Molina et al. 2015Mateos-Molina D., Palma M., Ruiz-Valentín I., et al. 2015. Assessing consequences of land cover changes on sediment deliveries to coastal waters at regional level over the last two decades in the northwestern Mediterranean Sea. Ocean Coast. Manage. 116: 435-442.), the five locations selected within MPAs are characterized by low levels of urbanization and are protected from impacts related to human activities such as fishing and anchoring.

sm4565fig1.jpg

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Fig. 1. – Map of the study locations: Portofino (PO), Livorno (LI), Vada Shoals (VA), Piombino (PM), Elba Island (EL), Pianosa Island (PI), Montecristo Island (MO), Giglio Island (GI), Argentario (AR), Sant’Agostino (AG), Civitavecchia (CI), Santa Marinella (SM), Asinara Island (AS), Costa Paradiso (CP), Tavolara Island (TA).

At each location, two sites of about 100 m2 that were hundreds of metres apart were randomly selected on vertical rocky bottom between 30 and 40 m depth, and at each site three areas of 4 m2 and tens of metres apart were selected. In each area, ten photographic samples of 0.2 m2 were collected. Organisms easily detected by photographic samples were considered as taxa, while those displaying similar morphological features were assembled into morphological groups (Parravicini et al. 2010Parravicini V., Micheli F., Montefalcone M., et al. 2010. Rapid assessment of benthic communities: a comparison between two visual sampling techniques. J. Exp. Mar. Biol. Ecol. 395: 21-29., Cecchi et al. 2014Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717., Piazzi et al. 2014Piazzi L., Balata D., Cecchi E., et al. 2014. Effectiveness of different investigation procedures in detecting anthropogenic impacts on coralligenous assemblages. Sci. Mar. 78: 319-328.). The percentage cover of the main taxa/morphological groups was evaluated by a manual contouring technique through the ImageJ software (Cecchi et al. 2014Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717.).

The structure of assemblages was analysed by permutational analysis of variance (Primer6 + PERMANOVA, Anderson 2001Anderson M.J. 2001. A new method for a non-parametric multivariate analysis of variance. Aust. Ecol. 26: 32-46.) based on Bray-Curtis resemblance matrix of untransformed data. Data were not transformed in order to stress the importance of the abundance of taxa/groups in determining the differences among conditions (Clarke and Gorley 2006Clarke K.R., Gorley R.N. 2006. Primer v6: user manual/tutorial. PRIMER-E, Plymouth.). A four-way model was used with Condition (3 levels: MPAs, l-U and h-U) as a fixed factor, Location (5 levels) as a random factor nested in Condition, Site (2 levels) as a random factor nested in Location, and Area (3 levels) as a random factor nested in Site. Pairwise tests were used to compare levels of significant factors. Homogeneity of multivariate dispersions was verified with PERMDISP (Anderson 2006Anderson M.J. 2006. Distance-based test for homogeneity of multivariate dispersions. Biometrics 62: 245-253.) to test the robustness of PERMANOVA analysis with respect to sample dispersion (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods.).

A canonical analysis of principal coordinates (CAP) conducted on a log(x+1) transformed Bray-Curtis resemblance matrix (Anderson and Robinson 2003Anderson M.J., Robinson J. 2003. Generalised discriminant analysis based on distances. Aust. N. Z. J. Statistics 45: 301-318., Anderson and Willis 2003Anderson M.J., Willis T.J. 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-524.) was performed in order to discriminate the differences of assemblages structure among conditions, highlighting species or taxa/groups as indicators accounting for this discrimination. A SIMPER analysis (Clarke 1993Clarke K.R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. Ecol. 18: 117-143.) was performed to identify percentage contribution of each species to the Bray-Curtis similarity among conditions.

A sensitivity level (SL) value was assigned to each taxon/group on the basis of its abundance in each environmental condition, data available in the literature (Hong 1983Hong J.S. 1983. Impact of pollution on the benthic community. Environmental impact of the pollution on the benthic coralligenous community in the Gulf of Fos, north-western Mediterranean. Bull. Korean Fish. Soc. 16: 273-290., Balata et al. 2005Balata D., Piazzi L., Cecchi E., et al. 2005. Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposits. Mar. Environ. Res. 60: 403-421., Gatti et al. 2015bGatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581.) and results from an expert judgement survey (Montefalcone et al. 2017Montefalcone M., Morri C., Bianchi C.N., et al. 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar. Pollut. Bull. 117: 229-238.), following an approach similar to that reported for the evaluation of shallow subtidal assemblages by the CARLIT index (Ballesteros et al. 2007Ballesteros E., Torras X., Pinedo S., et al. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of European Water Framework Directive. Mar. Pollut. Bull. 55: 172-180.). SL values varied according to a numerical scale ranging from 1 to 10, with minimum values corresponding to the most tolerant organisms and maximum values to the most sensitive ones (Cecchi et al. 2014Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717.). The cover values of the main taxa/morphological groups in each photographic sample were classified according to eight classes of abundance: 1) 0% to 0.01%; 2) 0.01% to 0.1%; 3) 0.1% to 1%; 4) 1% to 5%; 5) 5% to 25%; 6) 25% to 50%; 7) 50% to 75%; and 8) 75% to 100%. The total SL of each photographic sample (SLsa) was calculated by multiplying the sensitivity value of each taxon/group by its class of abundance (from 1 to 8) and adding values of all taxa/groups present in the sample.

For the calculation of the ESCA (considering only macroalgae), the ESCA-A (considering only macro-invertebrates) and the ESCA-TA (considering the total assemblage, i.e. both macroalgae and macro-invertebrates) indices, the correspondent value of SL for a study site (SLsi) was obtained by averaging the SLsa values of all samples (Cecchi et al. 2014Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717.). Alpha-diversity was defined as the mean number of the main taxa/groups obtained in each photographic sample. Beta-diversity was evaluated as the mean distance of all photographic samples from centroids calculated in the PERMDISP analysis (Primer 6 + PERMANOVA, Anderson et al. 2006Anderson M.J., Ellingsen K.E., McArdle B.H. 2006. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9: 683-693.). The indices were expressed as ecological quality ratio (EQR), calculated as the mean of the three EQRi obtained for the assemblage descriptors [(EQRSL+EQRalpha+EQRbeta)/3]. The EQRi were calculated as ratios between values of each of the SL, alpha-diversity and beta-diversity obtained in the study site and values obtained for the same descriptors at a reference location (Montecristo Island; Cecchi et al. 2014Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717.). According to the values of the indices, the ecological quality was classified following boundaries proposed by Piazzi et al. (2015)Piazzi L., Gennaro P., Cecchi E., et al. 2015. Improvement of the ESCA index for the evaluation of ecological quality of coralligenous habitat under the European Framework Directives. Medit. Mar. Sci. 16: 419-426.: high quality (EQR≥ 0.8); good quality (0.6≤EQR<0.8); moderate quality (0.4≤EQR<0.6); poor quality (0.2≤EQR<0.4); and bad quality (EQR<0.2). One-way PERMANOVA analyses based on Euclidean distance of untransformed data (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods.) were used to compare index values among conditions. Pair-wise tests were used to compare levels of significant factors.

A linear regression was performed in order to test the strength of the relationships between ESCA-TA and both ESCA and ESCA-A. The degree of correlation between EQR values was calculated and reported as the value of square correlation coefficient (determination coefficient, R2). Significance of regression was tested by means of the Fisher-Snedecor test performed by the Statistica 10 software.

RESULTSTop

PERMANOVA analysis detected significant differences in the coralligenous assemblages among conditions, locations, sites and areas (Table 1). The pairwise test showed that differences were significant between h-U locations and the others but not between MPA and l-U locations (Table 1).

Table 1. – Results of PERMANOVA analysis on coralligenous assemblages. MPAs, marine protected areas; l-U, low urbanized locations; h-U, highly urbanized locations. Significant effects are in bold.

Source df MS Pseudo-F P(perm)
Condition = C 2 138000 2.76 0.014

Location (C) = L(C) 12 49992 3.02 0.001

Site (L(C)) = S(L(C)) 15 16543 3.58 0.001

Area (S(L(C))) 60 4609 3.42 0.001

Residual 810 1345
Pairwise test (C) P(perm)
MPAs, l-U 0.252
MPAs, h-U 0.018

l-U, h-U 0.048

CAP analysis showed a clear and significant disjunction (permutation tests <0.05) along the CAP1 axis between groups of MPA/l-U locations and the h-U ones; secondly, discrimination between MPA and l-U locations along the CAP2 axis, can be detected, but on the basis of only a few taxa (Fig. 2). In fact, both MPA and l-U locations were generally characterized by a dominance of the Chlorophyta Halimeda tuna (J. Ellis et Solander) J.V. Lamouroux, Flabellia petiolata (Turra) Nizamuddin and Palmophyllum crassum (Naccari) Rabenhorst, erect Rhodophyta, erect bryozoans such as Reteporella grimaldii (Jullien, 1903), Smittina cervicornis (Pallas, 1766) and Pentapora fascialis (Pallas, 1766), and the Gorgoniidae Eunicella cavolini (Koch, 1887). Conversely, h-U locations were mostly characterized by turf macroalgae, Peyssonnelia spp, Hydrozoa, encrusting Bryozoa, encrusting Porifera and the Chlorophyta Pseudochlorodesmis furcellata (Zanardini) Børgesen. The SIMPER test confirmed the dominance of the main taxa/groups responsible for the CAP grouping (Table 2).

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Fig. 2. – Canonical analysis of principal coordinates (CAP), showing the discriminant-type ordination of assemblages subjected to different levels of human pressure. MPAs, white circles; l-U, white triangles; h-U, black circles.

Table 2. – Results of SIMPER test. MPAs, marine protected areas; l-U, low urbanized locations; h-U, highly urbanized locations.

Taxa/Groups Av. Abundance Av. dissimilarity

MPAs h-U

Erect Rhodophyta 10.2 0.3 14.39
Turf 9.7 32.9 14.06
Halimeda tuna

4.4 0 9.89
Peyssonnelia spp.

11.4 24.3 8.68
Flabellia petiolata

3.1 0.8 7.68
Encrusting Porifera 2.2 3.2 4.68
Erect Bryozoa 0.9 0.1 4.64
Dictyotales 0.6 0.1 4.09
Pseudochlorodesmis furcellata

0.3 0.6 3.77
Palmophyllum crassum

0.4 0 3.35
Eunicella cavolini

0.8 0.4 2.44
Paramuricea clavata

1.3 0.1 1.55
l-U h-U
Turf 15.7 32.9 15.51
Peyssonnelia spp.

7.8 24.3 14.14
Erect Rhodophyta

2.6 0.3 10.4
Alcyonacea 1.4 0.8 7.2
Flabellia petiolata

1.4 0.8 6.24
Encrusting Porifera 1.8 3.2 5.79
Pseudochlorodesmis furcellata

0.5 0.6 5.45
Halimeda tuna

0.6 0 5.36
Palmophyllum crassum

0.3 0 3.83
Encrusting Bryozoa 0.2 0.4 2.96
Eunicella cavolini

0.6 0.4 1.44

The SL assigned to each taxon/group is shown in Table 3. Values of the three ESCA indices ranged between high and moderate quality (Fig. 3). PERMANOVA highlighted significant differences among conditions for ESCA, ESCA-A and ESCA-TA. However, the pair-wise test showed that differences between MPA and l-U conditions were significant only when the ESCA-TA was used, while the same means comparison was not significant for the other two indices (ESCA and ESCA-A) (Table 4). Significant differences among other conditions (MPAs vs h-U and l-U vs h-U) were detected for all three indices (Table 4).

Table 3. – Sensitivity Level (SL) of the main taxa/morphological groups in the coralligenous assemblages.

Taxa/Groups SL
Algal turf 1
Hydrozoans (e.g. Eudendrium spp.)

2
Pseudochlorodesmis furcellata

2
Perforating sponges (e.g. Cliona spp.)

2
Dyctiotales 3
Encrusting sponges 3
Encrusting bryozoans 3
Encrusting ascidians (also epibiontic) 3
Encrusting Corallinales, articulated Corallinales 4
Peyssonnelia spp.

4
Valonia spp, Codium spp.

4
Sponges prostrate (e.g. Chondrosia reniformis, Petrosia ficiformis)

5
Large serpulids (e.g. Protula tubularia, Serpula vermicularis)

5
Parazoanthus axinellae

5
Leptogorgia sarmentosa

5
Flabellia petiolata

6
Erect corticated terete Ochrophyta (e.g. Sporochnus pedunculatus)

6
Encrusting Ochrophyta (e.g. Zanardinia typus)

6
Azooxantellate individual scleractinians (e.g. Leptopsammia pruvoti)

6
Ramified bryozoans (e.g. Caberea boryi, Cellaria fistulosa)

6
Palmophyllum crassum

7
Arborescent and massive sponges (e.g. Axinella polypoides)

7
Salmacina-Filograna complex

7
Myriapora truncata

7
Erect corticated terete Rodophyta (e.g. Osmundea pelagosae)

8
Bushy sponges (e.g. Axinella damicornis, Acanthella acuta)

8

Eunicella verrucosa, Alcyonium acaule

8
Erect ascidians 8
Corallium rubrum, Paramuricea clavata, Alcyonium coralloides

9
Zooxantellate scleractinians (e.g. Cladocora caespitosa)

9
Pentapora fascialis

9
Flattened Rhodophyta with cortication (e.g. Kallymenia spp.)

10
Halimeda tuna

10
Fucales (e.g. Cystoseira spp., Sargassum spp.), Phyllariopsis brevipes, Laminaria rodriguezii

10
Eunicella singularis, Eunicella cavolini, Savalia savaglia

10
Aedonella calveti, Reteporella grimaldii, Smittina cervicornis

10

sm4565fig3.jpg

Full size image

Fig. 3. – Values of the ESCA index calculated using only macroalgae and using only sessile macro-invertebrates (ESCA-A), and values of the integrated ESCA-TA index calculated using both macroalgae and sessile macro-invertebrates (i.e. the total assemblage) at the locations grouped according to their condition (MPAs, low urbanized and highly urbanized). White, high ecological quality; grey, good ecological quality; black, moderate ecological quality.

Table 4. – Results of PERMANOVA analyses on the three indices (ESCA-TA, ESCA, ESCA-A). MPAs, marine protected areas; l-U, low urbanized locations; h-U, highly urbanized locations. Significant effects are in bold.

ESCA-TA ESCA ESCA-A
Source df MS Pseudo-F P(perm) MS Pseudo-F P(perm) MS Pseudo-F P(perm)
Condition 2 795 53.74 0.001 1253 30.47 0.001 165 7.02 0.014
Residual 12 14 41 23
Pairwise test P(perm) P(perm) P(perm)
MPAs, l-U 0.023 0.168 0.266
MPAs, h-U 0.010 0.008 0.016
l-U, h-U 0.015 0.008 0.033

Significant positive correlations between the ESCA-TA index and both the ESCA and the ESCA-A indices were highlighted, with a higher correlation (P<0.0001, Fig. 4A) with ESCA than with ESCA-A (P<0.001, Fig. 4B). Values of the determination coefficient and line slope confirmed a strong association between the two variables in the case of ESCA-TA and ESCA (b=1.2; R2=0.9206), while the linear relation between ESCA-TA and ESCA-A was weaker (b=0.52; R2=0.613).

sm4565fig4.jpg

Full size image

Fig. 4. – Relationships between the ESCA-TA index and the ESCA (A) and the ESCA-A (B) indices. The equations and the values of the determination coefficients (R2) are reported, n=15.

DISCUSSIONTop

Results showed differences in the structure of coralligenous assemblages between locations characterized by different levels of human-induced pressure, and these differences were related to different abundances of both macroalgae and sessile macro-invertebrates. These patterns confirm the sensitivity of coralligenous assemblages to human pressure (Balata et al. 2007bBalata D., Piazzi L., Cinelli F. 2007b. Increase of sedimentation in a subtidal system: effects on the structure and diversity of macroalgal assemblages. J. Exp. Mar. Biol. Ecol. 351: 73-82., Piazzi et al. 2012Piazzi L., Gennaro P., Balata D. 2012. Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar. Pollut. Bull. 64: 2623-2629., Gatti et al. 2015bGatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581.), highlighting the suitability of these assemblages to be used as ecological indicators in monitoring survey and impact evaluation studies (Deter et al. 2012Deter J., Descamp P., Ballista L., et al. 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecol. Ind. 20: 345-352., Sartoretto et al. 2014Sartoretto S., David R., Aurelle D., et al. 2014. An integrated approach to evaluate and monitor the conservation state of coralligenous bottoms: the INDEX-COR method. In: Bouafif C., Langar H., Ouerghi A. (eds), Proceedings of the second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio-Concretions (Portorož, Slovenia, 29-30 October 2014). UNEP/MAP – RAC/SPA, RAC/SPA publ., Tunis: pp. 159-165., Gatti et al. 2015aGatti G., Bianchi C.N., Morri C., et al. 2015a. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol. Ind. 52: 567-576.). Also, local protection might be not enough to prevent impacts on the structure and the ecological quality of coralligenous assemblages, as many organisms are more sensitive to large-scale alterations of water quality than to local disturbances (Parravicini et al. 2013Parravicini V., Micheli F., Montefalcone M., et al. 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. PLoS ONE 8: e75767.).

Changes in macroalga abundance and composition among the studied environmental conditions were in agreement with patterns widely described (Piazzi et al. 2012Piazzi L., Gennaro P., Balata D. 2012. Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar. Pollut. Bull. 64: 2623-2629. and references therein). The main differences between conditions were related to the abundance of algal turfs, which increased at the high urbanized locations where, instead, the erect Rhodophyta and Udoteaceae (Halimeda tuna and Flabellia petiolata) decreased significantly. Turfs are mostly constituted by filamentous species that reproduce asexually and are well adapted to environmental stress (Balata et al. 2011Balata D., Piazzi L., Rindi F. 2011. Testing a new classification of morphological functional groups of marine macroalgae for the detection or responses to disturbance. Mar. Biol. 158: 2459-2469.). In fact, filamentous forms are favoured by eutrophication, thanks to their high uptake efficiency, and are adapted to high sedimentation rates because they are able to quickly recover after disturbance (Taylor et al. 1998Taylor R.B., Peek J.T.A., Rees T.A.V. 1998. Scaling of ammonium uptake by seaweeds to surface area: volume ratio: geographical variation and the role of uptake by passive diffusion. Mar. Ecol. Progr. Ser. 169: 143-148., Airoldi 2003Airoldi L. 2003. The effects of sedimentation on rocky coastal assemblages. Oceanogr. Mar. Biol. Annu. Rev. 41: 161-203.). Conversely, erect macroalgae reproducing by spores suffer conditions induced by high urbanization as they are damaged directly by eutrophication and high sedimentation rates, and indirectly because they are out-competed by turfs that become dominant under stress conditions (Balata et al. 2011Balata D., Piazzi L., Rindi F. 2011. Testing a new classification of morphological functional groups of marine macroalgae for the detection or responses to disturbance. Mar. Biol. 158: 2459-2469.).

This study also highlighted changes in the abundance of several taxa/groups of sessile macro-invertebrates among conditions, confirming patterns suggested by previous investigations (Hong 1983Hong J.S. 1983. Impact of pollution on the benthic community. Environmental impact of the pollution on the benthic coralligenous community in the Gulf of Fos, north-western Mediterranean. Bull. Korean Fish. Soc. 16: 273-290., Ponti et al. 2011Ponti 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., Piazzi et al. 2016Piazzi L., La Manna G., Cecchi E., et al. 2016. Protection changes the relevancy of scales of variability in coralligenous assemblages. Estuar. Coast. Shelf Sci. 175: 62-69.). In particular, erect bryozoans and some gorgonians showed lower abundance at highly urbanized sites, while hydrozoans, sponges and encrusting bryozoans seemed to be the most tolerant taxa. The sensitivity of erect bryozoans to different kinds of pressure linked with water quality alteration or mechanical disturbance has already been reported (Sala et al. 1996Sala E., Garrabou J., Zabala M. 1996. Effects of diver frequentation on marine sub-littoral population of the bryozoan Pentapora fascialis. Mar. Biol. 126: 451-459., Garrabou et al. 1998Garrabou J., Sala E., Arcas A., et al. 1998. The impact of diving on rocky sub-littoral communities: a case study of a bryozoan population. Conserv. Biol. 12: 302-312., de la Nuez-Hernández et al. 2014de la Nuez-Hernández D., Valle C., Forcada A., et al. 2014. Assessing the erect bryozoan Myriapora truncata (Pallas, 1766) as indicator of recreational diving impact on coralligenous reef communities. Ecol. Ind. 46: 193-200.), although the level of tolerance varies among species (Harmelin and Capo 2001Harmelin J.G., Capo S. 2001. Effects of sewage on bryozoan diversity in Mediterranean rocky bottoms. In: Wyse J., Spencer J. (eds), Bryozoan, Studies 2001. Swets and Zeitlinger, pp. 151-156.). Thus, these organisms may be considered as valuable indicators of isolated or chronic impacts (Deter et al. 2012Deter J., Descamp P., Ballista L., et al. 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecol. Ind. 20: 345-352., Gatti et al. 2015aGatti G., Bianchi C.N., Morri C., et al. 2015a. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol. Ind. 52: 567-576.). Gorgonians, because of their long life and slow dynamics, are particularly vulnerable to large-scale alterations such as climatic anomalies (Linares et al. 2008Linares C., Coma R., Garrabou J., et al. 2008. Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J. Appl. Ecol. 45: 688-699., Garrabou et al. 2009Garrabou J., Coma R., Bensoussan N., et al. 2009. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biol. 15: 1090-1103., Teixidó et al. 2013Teixidó N., Casas E., Cebrian E., et al. 2013. Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE 8: e53742.), which are independent of the level of local protection (Cerrano et al. 2000Cerrano C., Bavestrello G., Bianchi C.N., et al. 2000. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecol. Lett. 3: 284-293., Coma et al. 2006Coma R., Linares C., Ribes M., et al. 2006. Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Mar. Ecol. Progr. Ser. 327: 51-60., Huete-Stauffer et al. 2011Huete-Stauffer C., Vielmini I., Palma M., et al. 2011. Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Mar. Ecol. 32: 107-116.). However, local disturbances (such as sedimentation, anchoring and fishing activities) can also affect gorgonian populations, causing damage of varying extent (Bavestrello et al. 1997Bavestrello G., Cerrano C., Zanzi D., et al. 1997. Damage by fishing activities in the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aq. Conserv. Mar. Freshwater Ecosyst. 7: 253-262.) and explaining the patterns highlighted in the study.

The increase in the distribution of encrusting sponges at highly urbanized locations confirms patterns already described (Hong 1983Hong J.S. 1983. Impact of pollution on the benthic community. Environmental impact of the pollution on the benthic coralligenous community in the Gulf of Fos, north-western Mediterranean. Bull. Korean Fish. Soc. 16: 273-290., Ponti et al. 2011Ponti 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.); in fact, high abundances of these organisms have been reported for degraded areas characterized by high levels of fine sediments and organic matter (Falace et al. 2015Falace A., Kaleb S., Curiel D., et al. 2015. Calcareous bio-concretions in the northern Adriatic Sea: habitat types, environmental factors that influence habitat distributions, and predictive modeling. PLoS ONE 10: e0140931.). By contrast, erect sponges did not appear as tolerant opportunistic species (Teixidó et al. 2011Teixidó 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., Gatti et al. 2015bGatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581.).

Algae and animals are known to respond differently to environmental stressors due to their different life histories and life cycles (Grime 1977Grime J.P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111: 1169-1194., Darling et al. 2012 Darling E.S., Alvarez-Filip L., Oliver T.A., et al. 2012. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15: 1378-1386.and references therein). Thus, depending on which of the two components is dominant in a coralligenous assemblages, the two individual indices considering only animals (ESCA-A) or only algae (ESCA) can be used accordingly and then also compared to understand which of the two components has been mostly affected. On the other hand, the concurrent use of the two components in the integrated ESCA-TA index can be effective in all the most common situations of high biodiverse coralligenous assemblages, as well as in situations where periodical fluctuations between animal-dominated and algal-dominated assemblages occur due to synergistic effects of local and global impacts (Parravicini et al. 2013Parravicini V., Micheli F., Montefalcone M., et al. 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. PLoS ONE 8: e75767., Gatti et al. 2015bGatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581.). The results of this paper also showed that, although both the ESCA and ESCA-A indices, when used alone, clearly separated the highly urbanized locations from the other ones, the ESCA-TA index detected more finely the three environmental conditions, also revealing those subtle differences between locations under a regime of protection and locations affected by low levels of urbanization. The higher degree of correlation between ESCA-TA and ESCA suggests a higher sensitivity of macroalgae, compared with macro-invertebrates, to those environmental alterations that usually occur in the urbanized areas, such as the increase in nutrients and water turbidity (Lopez y Royo et al. 2009Lopez y Royo C., Silvestri C., Pergent G., et al. 2009. Assessment of human-induced pressures on the coastal zone, using publicly available data. J. Environ. Manag. 90: 1494-1501.). By contrast, sessile animals can be more sensitive than macroalgae to other kinds of stress, such as effects of climate changes and mechanical disturbances due to fishing, recreational diving and anchoring (Cerrano et al. 2000Cerrano C., Bavestrello G., Bianchi C.N., et al. 2000. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecol. Lett. 3: 284-293., Coma et al. 2006Coma R., Linares C., Ribes M., et al. 2006. Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Mar. Ecol. Progr. Ser. 327: 51-60., de la Nuez-Hernández et al. 2014de la Nuez-Hernández D., Valle C., Forcada A., et al. 2014. Assessing the erect bryozoan Myriapora truncata (Pallas, 1766) as indicator of recreational diving impact on coralligenous reef communities. Ecol. Ind. 46: 193-200.). Thus, combining macroalgae and macro-invertebrates into the ESCA-TA index may increase the efficiency of the index in determining the ecological quality of marine coastal areas, as the response spectrum of the index to human pressures can be extended by the use of a higher number of descriptors. Moreover, the use of the ESCA-TA index may allow a finer intercalibration with other monitoring methods that consider the whole coralligenous assemblages (Kipson et al. 2011Kipson S., Fourt M., Teixidó N., et al. 2011. Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of Mediterranean coralligenous outcrops. PLoS ONE 6: e27103., Deter et al. 2012Deter J., Descamp P., Ballista L., et al. 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecol. Ind. 20: 345-352., Gatti et al. 2015aGatti G., Bianchi C.N., Morri C., et al. 2015a. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol. Ind. 52: 567-576.), and therefore meet the requirements of the European directives.

Due to the high biodiversity that characterizes coralligenous assemblages (Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Annu. Rev. 44: 123-195.), the list we proposed is based on the most characteristic taxa and on a number of morphological groups that, according to the main literature and to our data, can be easily recognized and classified in photographic samples. The SLs of each taxon/group used for the calculation of the ESCA indices are then based on results of the present and previous studies related to the northwestern Mediterranean Sea, as well as on results of an expert judgement survey (Montefalcone et al. 2017Montefalcone M., Morri C., Bianchi C.N., et al. 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar. Pollut. Bull. 117: 229-238.). The scores of sensitivity we assumed can be shared within a broad group of species but, sometimes, sensitivity cannot be synthesized into an univocal score that is suitable for all members of a group (Montefalcone et al. 2017Montefalcone M., Morri C., Bianchi C.N., et al. 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar. Pollut. Bull. 117: 229-238.): this is why our list of taxa/groups, with their relative scores of sensitivity, should be tested in other geographical situations in order to be consistently adapted, case by case, and then improved. Further studies would therefore be desirable. Should the method be considered effective, the SLs, as well as the reference site for computing the EQR, could be modified following an approach already used for other ecological quality indices (Bermejio et al. 2013Bermejio R., Fuente G., Vergara J.J., et al. 2013. Application of the CARLIT index along a biogeographical gradient in the Alboran Sea (European Coast). Mar. Pollut. Bull. 72: 107-118., Nikolic et al. 2013Nikolic V., Zuljevic A., Mangialajo L., et al. 2013. Cartography of littoral rocky-shore communities (CARLIT) as a tool for ecological quality assessment of coastal waters in the Eastern Adriatic Sea. Ecol. Ind. 34: 87-93.) and testing the sensitivity of coralligenous organisms to different kinds of stress and within a larger geographic area.

ACKNOWLEDGEMENTSTop

The authors are very grateful to C. Huete-Stauffer and M. Ponti for their comments, which improved the quality of the paper. We also wish to thank E. Burgos for the Spanish translation. L. Piazzi was funded by the project “Desertificazione marina da sovrapascolo di ricci: indagine sulla transizione di stadi stabili bentonici alternativi” financed by P.O.R. SARDEGNA F.S.E. 2007-2013 - Obiettivo competitività regionale e occupazione, Asse IV Capitale umano, Linea di Attività l.3.1.

REFERENCESTop

Airoldi L. 2003. The effects of sedimentation on rocky coastal assemblages. Oceanogr. Mar. Biol. Annu. Rev. 41: 161-203.

Anderson M.J. 2001. A new method for a non-parametric multivariate analysis of variance. Aust. Ecol. 26: 32-46.
https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x

Anderson M.J. 2006. Distance-based test for homogeneity of multivariate dispersions. Biometrics 62: 245-253.
https://doi.org/10.1111/j.1541-0420.2005.00440.x

Anderson M.J., Robinson J. 2003. Generalised discriminant analysis based on distances. Aust. N. Z. J. Statistics 45: 301-318.
https://doi.org/10.1111/1467-842X.00285

Anderson M.J., Willis T.J. 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-524.
https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2

Anderson M.J., Ellingsen K.E., McArdle B.H. 2006. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9: 683-693.
https://doi.org/10.1111/j.1461-0248.2006.00926.x

Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods.

Balata D., Piazzi L., Cecchi E., et al. 2005. Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposits. Mar. Environ. Res. 60: 403-421.
https://doi.org/10.1016/j.marenvres.2004.12.005

Balata D., Piazzi L., Benedetti-Cecchi L. 2007a. Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 8: 2455-2461.
https://doi.org/10.1890/07-0053.1

Balata D., Piazzi L., Cinelli F. 2007b. Increase of sedimentation in a subtidal system: effects on the structure and diversity of macroalgal assemblages. J. Exp. Mar. Biol. Ecol. 351: 73-82.
https://doi.org/10.1016/j.jembe.2007.06.019

Balata D., Piazzi L., Rindi F. 2011. Testing a new classification of morphological functional groups of marine macroalgae for the detection or responses to disturbance. Mar. Biol. 158: 2459-2469.
https://doi.org/10.1007/s00227-011-1747-y

Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Annu. Rev. 44: 123-195.
https://doi.org/10.1201/9781420006391.ch4

Ballesteros E., Torras X., Pinedo S., et al. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of European Water Framework Directive. Mar. Pollut. Bull. 55: 172-180.
https://doi.org/10.1016/j.marpolbul.2006.08.038

Bavestrello G., Cerrano C., Zanzi D., et al. 1997. Damage by fishing activities in the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aq. Conserv. Mar. Freshwater Ecosyst. 7: 253-262.
https://doi.org/10.1002/(SICI)1099-0755(199709)7:3<253::AID-AQC243>3.0.CO;2-1

Bermejio R., Fuente G., Vergara J.J., et al. 2013. Application of the CARLIT index along a biogeographical gradient in the Alboran Sea (European Coast). Mar. Pollut. Bull. 72: 107-118.
https://doi.org/10.1016/j.marpolbul.2013.04.011

Bertolino M., Cerrano C., Bavestrello G., et al. 2013. Diversity of Porifera in the Mediterranean coralligenous accretions, with description of a new species. ZooKeys 336: 1-37.
https://doi.org/10.3897/zookeys.336.5139

Birk S., Bonne W., Borja 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. Ecol. Ind. 18: 31-41.
https://doi.org/10.1016/j.ecolind.2011.10.009

Cánovas Molina A., Montefalcone M., Vassallo P., et al. 2016. Combining literature review, acoustic mapping and in situ observations: an overview of coralligenous assemblages in Liguria (NW Mediterranean Sea). Sci. Mar. 80: 7-16.
https://doi.org/10.3989/scimar.04235.23A

Casas-Guell E., Teixidó N., Garrabou J., et al. 2015. Structure and biodiversity of coralligenous assemblages over broad spatial and temporal scales. Mar. Biol. 162: 901-912.
https://doi.org/10.1007/s00227-015-2635-7

Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717.
https://doi.org/10.1080/09670262.2014.918657

Cerrano C., Bavestrello G., Bianchi C.N., et al. 2000. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecol. Lett. 3: 284-293.
https://doi.org/10.1046/j.1461-0248.2000.00152.x

Clarke K.R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. Ecol. 18: 117-143.
https://doi.org/10.1111/j.1442-9993.1993.tb00438.x

Clarke K.R., Gorley R.N. 2006. Primer v6: user manual/tutorial. PRIMER-E, Plymouth.

Coma R., Linares C., Ribes M., et al. 2006. Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Mar. Ecol. Progr. Ser. 327: 51-60.
https://doi.org/10.3354/meps327051

Darling E.S., Alvarez-Filip L., Oliver T.A., et al. 2012. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15: 1378-1386.
https://doi.org/10.1111/j.1461-0248.2012.01861.x

de la Nuez-Hernández D., Valle C., Forcada A., et al. 2014. Assessing the erect bryozoan Myriapora truncata (Pallas, 1766) as indicator of recreational diving impact on coralligenous reef communities. Ecol. Ind. 46: 193-200.
https://doi.org/10.1016/j.ecolind.2014.05.035

Deter J., Descamp P., Ballista L., et al. 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecol. Ind. 20: 345-352.
https://doi.org/10.1016/j.ecolind.2012.03.001

EC. 2008. 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 (Marine Strategy Framework Directive). Official Journal of the European Commission, G.U.C.E. 25/6/2008, L 164/19.

Falace A., Kaleb S., Curiel D., et al. 2015. Calcareous bio-concretions in the northern Adriatic Sea: habitat types, environmental factors that influence habitat distributions, and predictive modeling. PLoS ONE 10: e0140931.
https://doi.org/10.1371/journal.pone.0140931

Garrabou J., Sala E., Arcas A., et al. 1998. The impact of diving on rocky sub-littoral communities: a case study of a bryozoan population. Conserv. Biol. 12: 302-312.
https://doi.org/10.1111/j.1523-1739.1998.96417.x

Garrabou J., Coma R., Bensoussan N., et al. 2009. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biol. 15: 1090-1103.
https://doi.org/10.1111/j.1365-2486.2008.01823.x

Gatti G., Montefalcone M., Rovere A., et al. 2012. Seafloor integrity down the harbor waterfront: the coralligenous shoals off Vado Ligure (NW Mediterranean). Adv. Limnol. 3: 51-67.
https://doi.org/10.1080/19475721.2012.671190

Gatti G., Bianchi C.N., Morri C., et al. 2015a. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol. Ind. 52: 567-576.
https://doi.org/10.1016/j.ecolind.2014.12.026

Gatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581.
https://doi.org/10.1371/journal.pone.0118581

Grime J.P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111: 1169-1194.
https://doi.org/10.1086/283244

Harmelin J.G., Capo S. 2001. Effects of sewage on bryozoan diversity in Mediterranean rocky bottoms. In: Wyse J., Spencer J. (eds), Bryozoan, Studies 2001. Swets and Zeitlinger, pp. 151-156.

Hong J.S. 1983. Impact of pollution on the benthic community. Environmental impact of the pollution on the benthic coralligenous community in the Gulf of Fos, north-western Mediterranean. Bull. Korean Fish. Soc. 16: 273-290.

Huete-Stauffer C., Vielmini I., Palma M., et al. 2011. Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Mar. Ecol. 32: 107-116.
https://doi.org/10.1111/j.1439-0485.2011.00429.x

Jackson J.B., Sala E. 2001. Unnatural oceans. Sci. Mar. 65: 273-281.
https://doi.org/10.3989/scimar.2001.65s2273

Kipson S., Fourt M., Teixidó N., et al. 2011. Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of Mediterranean coralligenous outcrops. PLoS ONE 6: e27103.
https://doi.org/10.1371/journal.pone.0027103

Linares C., Coma R., Garrabou J., et al. 2008. Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J. Appl. Ecol. 45: 688-699.
https://doi.org/10.1111/j.1365-2664.2007.01419.x

Lopez y Royo C., Silvestri C., Pergent G., et al. 2009. Assessment of human-induced pressures on the coastal zone, using publicly available data. J. Environ. Manag. 90: 1494-1501.
https://doi.org/10.1016/j.jenvman.2008.10.007

Martin C.S., 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. 4: 5073.
https://doi.org/10.1038/srep05073

Mateos-Molina D., Palma M., Ruiz-Valentín I., et al. 2015. Assessing consequences of land cover changes on sediment deliveries to coastal waters at regional level over the last two decades in the northwestern Mediterranean Sea. Ocean Coast. Manage. 116: 435-442.
https://doi.org/10.1016/j.ocecoaman.2015.09.003

Montefalcone M., Albertelli G., Morri C., et al. 2009. Legal protection is not enough: Posidonia oceanica meadows in marine protected areas are not healthier than those in unprotected areas of the northwest Mediterranean Sea. Mar. Pollut. Bull. 58: 515-519.
https://doi.org/10.1016/j.marpolbul.2008.12.001

Montefalcone M., Morri C., Bianchi C.N., et al. 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar. Pollut. Bull. 117: 229-238.
https://doi.org/10.1016/j.marpolbul.2017.01.072

Nikolic V., Zuljevic A., Mangialajo L., et al. 2013. Cartography of littoral rocky-shore communities (CARLIT) as a tool for ecological quality assessment of coastal waters in the Eastern Adriatic Sea. Ecol. Ind. 34: 87-93.
https://doi.org/10.1016/j.ecolind.2013.04.021

Parravicini V., Micheli F., Montefalcone M., et al. 2010. Rapid assessment of benthic communities: a comparison between two visual sampling techniques. J. Exp. Mar. Biol. Ecol. 395: 21-29.
https://doi.org/10.1016/j.jembe.2010.08.005

Parravicini V., Micheli F., Montefalcone M., et al. 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. PLoS ONE 8: e75767.
https://doi.org/10.1371/journal.pone.0075767

Piazzi L., Gennaro P., Balata D. 2011. Effects of nutrient enrichment on macroalgal coralligenous assemblages. Mar. Pollut. Bull. 62: 1830-1835.
https://doi.org/10.1016/j.marpolbul.2011.05.004

Piazzi L., Gennaro P., Balata D. 2012. Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar. Pollut. Bull. 64: 2623-2629.
https://doi.org/10.1016/j.marpolbul.2012.07.027

Piazzi L., Balata D., Cecchi E., et al. 2014. Effectiveness of different investigation procedures in detecting anthropogenic impacts on coralligenous assemblages. Sci. Mar. 78: 319-328.
https://doi.org/10.3989/scimar.03989.28A

Piazzi L., Gennaro P., Cecchi E., et al. 2015. Improvement of the ESCA index for the evaluation of ecological quality of coralligenous habitat under the European Framework Directives. Medit. Mar. Sci. 16: 419-426.
https://doi.org/10.12681/mms.1029

Piazzi L., La Manna G., Cecchi E., et al. 2016. Protection changes the relevancy of scales of variability in coralligenous assemblages. Estuar. Coast. Shelf Sci. 175: 62-69.
https://doi.org/10.1016/j.ecss.2016.03.026

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.
https://doi.org/10.1007/s00227-011-1661-3

Sala E., Garrabou J., Zabala M. 1996. Effects of diver frequentation on marine sub-littoral population of the bryozoan Pentapora fascialis. Mar. Biol. 126: 451-459.
https://doi.org/10.1007/BF00354627

Sartoretto S., David R., Aurelle D., et al. 2014. An integrated approach to evaluate and monitor the conservation state of coralligenous bottoms: the INDEX-COR method. In: Bouafif C., Langar H., Ouerghi A. (eds), Proceedings of the second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio-Concretions (Portorož, Slovenia, 29-30 October 2014). UNEP/MAP – RAC/SPA, RAC/SPA publ., Tunis: pp. 159-165.

Stachowitsch M. 2003. Research on intact marine ecosystems: a lost era. Mar. Pollut. Bull. 46: 801-805.
https://doi.org/10.1016/S0025-326X(03)00109-7

Taylor R.B., Peek J.T.A., Rees T.A.V. 1998. Scaling of ammonium uptake by seaweeds to surface area: volume ratio: geographical variation and the role of uptake by passive diffusion. Mar. Ecol. Progr. Ser. 169: 143-148.
https://doi.org/10.3354/meps169143

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.
https://doi.org/10.1371/journal.pone.0023744

Teixidó N., Casas E., Cebrian E., et al. 2013. Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE 8: e53742.
https://doi.org/10.1371/journal.pone.0053742



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