sm80n1-4235

Combining literature review, acoustic mapping and in situ observations: an overview of coralligenous assemblages in Liguria (NW Mediterranean Sea)

Almudena Cánovas Molina, Monica Montefalcone, Paolo Vassallo, Carla Morri, Carlo Nike Bianchi, Giorgio Bavestrello

DiSTAV, Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Università di Genova, Corso Europa 26, 16132 Genova, Italy. E-mail: almucanovass@gmail.com

Summary: A review and update of the existing knowledge on the coralligenous assemblages of Liguria (NW Italy) was conducted as an essential step towards management measures for their conservation according to the EU Marine Strategy Framework Directive. By combining a literature review, acoustic mapping and in situ observations on a geographic information systems platform, we were able to assess the distribution and heterogeneity of coralligenous assemblages and the main pressures affecting them. The reliability of the literature was previously estimated using a dependability index. The coralligenous assemblages cover an area of 130.9 ha and range from 10 to 113 m depth. Twelve different biological facies (five of them not included in the EUNIS list) were identified and four main geomorphotypes (plungingcliffs, paleocliffs, rockfalls and shoals) were recognized. Incident light values influenced the distribution of four facies in Portofino promontory. Pressures were found on 33% of the coralligenous assemblages investigated, mainly due to fishing activities, mass mortality events, invasive species and occasional mucilaginous events. Our results showed a high spatial, geomorphological and biological heterogeneity of coralligenous assemblages in Liguria.

Keywords: mapping; literature review; heterogeneity; coralligenous assemblages; NW Mediterranean Sea.

Combinando revisión bibliográfica, mapas acústicos y observaciones in situ: sinopsis de las formaciones coralígenas en Liguria (NO del mar Mediterráneo)

Resumen: Una revisión y actualización del conocimiento existente sobre las formaciones coralígenas en Liguria (NO de Italia) ha sido implementado como paso esencial con vistas a las medidas de gestión para su conservación de acuerdo con la Directiva Marco sobre la Estrategia Marina. Combinando en plataforma SIG revisión bibliográfica, mapas acústicos y observaciones in situ hemos sido capaces de determinar la distribución de las formaciones coralígenas, su heterogeneidad y sus principales presiones. La fiabilidad de la bibliografía fue estimada a través del índice de confianza (DI). Las formaciones coralígenas cubren un área de 130.9 ha en un rango de profundidad que va desde los 10 m a los 113 m. 12 facies biológicas diferentes (5 de ellas no incluidas en la lista EUNIS) fueron identificadas y 4 geomorfotipos principales (acantilado actual, paleoacantilado, cúmulo de rocas y bajos) fueron reconocidos. Los valores de luz incidente influenciaron la distribución de 4 facies en el promontorio de Portofino. Fueron encontradas presiones en el 33% de las formaciones coralígenas investigados, principalmente debidas a actividades de pesca, episodios de muerte masiva, especies invasoras y proliferación de algas mucilaginosas. Nuestros resultados mostraron una elevada heterogeneidad espacial, geomorfológica y biológica de las formaciones coralígenas en Liguria.

Palabras clave: mapeo; revisión bibliográfica; heterogeneidad; formaciones coralígenas; NO del mar Mediterraneo.

Citation/Como citar este artículo: Cánovas Molina A., Montefalcone M., Vassallo P., Morri C., Bianchi C.N., Bavestrello G. 2016. Combining literature review, acoustic mapping and in situ observations: an overview of coralligenous assemblages in Liguria (NW Mediterranean Sea). Sci. Mar. 80(1): 7-16. doi: http://dx.doi.org/10.3989/scimar.04235.23A

Editor: R. Sardà.

Received: March 2, 2015. Accepted: July 31, 2015. Published: December 11, 2015.

Copyright: © 2016 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Commercial Lisence (by-nc) Spain 3.0.

Contents

Summary
Resumen
Introduction
Materials and methods
Results
Discussion
Acknowledgements
References

INTRODUCTIONTop

Since Marion (1883)Marion A.F. 1883. Esquisse d’une topographie zoologique du Golfe de Marseille. Ann. Mus. Marseille 1: 6-108. first coined the word “coralligène”, coralligenous assemblages have been studied, classified and defined as hard substrata of biogenic origin that are mainly produced by the accumulation of calcareous encrusting algae, light being the main environmental factor affecting their development (Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Ann. Rev. 44: 123-195.). Considered one of the most important and characteristic habitats of the Mediterranean Sea (Laborel 1961Laborel J. 1961. Le concrétionnement algal “coralligène” et son importance géomorphologique en Méditerranée. Rec. Trav. Stat. Mar. Endoume 23 (37): 37-60., 1987Laborel J. 1987. Marine biogenic constructions in the Mediterranean, a review. Sci. Rep. Port-Cros natl. Park. Fr., 13: 97-127., Laubier 1966Laubier L. 1966. Le coralligène des Albères. Monographie biocénotique. Ann. Inst. Océanogr. Paris 43: 137-316.), coralligenous assemblages represent the climax biocenosis of the circalittoral zone (Pérès and Picard 1964Pérès J.M., Picard J. 1964. Nouveau manuel de bionomie benthique de la Mer Méditerranée. Rec. Trav. Stat. Mar. Endoume 14: 1-137.), where endangered or commercially important fish species are known to live, feed or reproduce (Salomidi et al. 2012Salomidi M., Katsanevakis S., Borja Á., et al. 2012. Assessment of goods and services, vulnerability, and conservation status of European seabed biotopes: a stepping stone towards ecosystem-based spatial management. Med. Mar. Sci. 35 (1): 49-88.). Coralligenous communities are considered of high conservation interest because of their biogeographic uniqueness, their highly varied physical structure, their high species biodiversity, their highly diversified occurrence stratified throughout the different benthic marine zones and their slow growth (Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Ann. Rev. 44: 123-195., Agnesi et al. 2008Agnesi S., Annunziatellis A., Cassese M.L., et al. 2008. Synthesis of the cartographic information on the coralligenous assemblages and other biogenic calcareous formations in the Mediterranean Sea. In: Pergent-Martini C. and Brichet M. (eds), Avenant Nº3/2008/RAC/SPA en référence au Mémorandum de coopération Nº6/2002/RAC/SPA. 50 pp., Salomidi et al. 2012>Salomidi M., Katsanevakis S., Borja Á., et al. 2012. Assessment of goods and services, vulnerability, and conservation status of European seabed biotopes: a stepping stone towards ecosystem-based spatial management. Med. Mar. Sci. 35 (1): 49-88.).

Trawling has effects on seafloor that resemble those of forest clear-cutting (Watling and Norse 1998Watling L., Norse E.A. 1998. Disturbance of the seabed by mobile fishing gear: A comparison to forest clearcutting. Conserv. Biol. 12: 1180-1197.). It is the most destructive impact affecting the coralligenous habitat, but it is not the only one. Artisanal fishing, anchoring, diving, waste water discharges, aquaculture facilities, changes in land use, coastal infrastructure construction, urbanization, anomalous high water temperatures, proliferation of mucilage and invasive species are currently affecting the biodiversity and structure of coralligenous assemblages (Baldacconi and Corriero 2009Baldacconi R., Corriero G. 2009. Effects of the spread of the alga Caulerpa racemosa var. cylindracea on the sponge assemblage from coralligenous concretions of the Apulian coast (Ionian Sea, Italy). Mar. Ecol. 30: 337-345., Ballesteros 2009Ballesteros E. 2009. Threats and conservation of coralligenous assemblages. In: Pergent-Martini C. and Brichet M. (eds), Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. RAC/SPA Publ. Tunis, pp. 25-27., Linares et al. 2010Linares C., Zabala M., Garrabou J., et al. 2010. Assessing the impact of diving in coralligenous communities: The usefulness of demographic studies of red gorgonian populations. Sci. Rep. Port-Cros natl. Park, Fr., 24: 161-184.).

Although the importance of coralligenous assemblages and the threats affecting them are commonly accepted within the scientific community and among managers, they were not listed among the priority habitats defined by the EU Habitat Directive (92/43/EEC), thus remaining without formal protection. Only one European law (Council Regulation (EC) Nº 1967/2006) prohibits destructive fishing over Mediterranean coralligenous and mäerl communities but it remains ineffective in the current scenario of a lack of relevant geospatial data (UNEP-MAP-RAC/SPA 2008UNEP-MAP-RAC/SPA. 2008. Action plan for the conservation of the coralligenous and other calcareous bio-concretions in the Mediterranean Sea. In: Pergent-Martini C. and Brichet M. (eds), RAC/SPA Tunis, 21 pp., Salomidi et al. 2012Salomidi M., Katsanevakis S., Borja Á., et al. 2012. Assessment of goods and services, vulnerability, and conservation status of European seabed biotopes: a stepping stone towards ecosystem-based spatial management. Med. Mar. Sci. 35 (1): 49-88.). Although some efforts have been made to increase information on the distribution of this sensitive habitat (Georgiadis et al. 2009Georgiadis M., Papatheodorou G., Tzanatos E., et al. 2009. Coralligene formations in the eastern Mediterranean Sea: Morphology, distribution, mapping and relation to fisheries in the southern Aegean Sea (Greece) based on high-resolution acoustics. J. Exp. Mar. Biol. Ecol. 368: 44-58., Giakoumi et al. 2013Giakoumi S., Sini M., Gerovasileiou V., et al. 2013. Ecoregion-based conservation planning in the Mediterranean: Dealing with large scale heterogeneity. PLoS One 8: e76449., 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.), knowledge of the geographical and depth distribution of coralligenous assemblages as well as their biodiversity and its relation to their functioning is still needed for their conservation and sustainable use (UNEP-MAP-RAC/SPA 2009UNEP-MAP-RAC/SPA. 2009. Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. In: Pergent-Martini C. and Brichet M. (eds), RAC/SPA Tunis, 273 pp., European Commission 2011European Commission. 2011. Commission staff working paper. Relationship between the initial assessment of marine waters and the criteria for good environmental status, European Commission, Brussels, 14.10.2011 SEC, 95 pp., Pergent 2011Pergent G. 2011. Proposal for the definition of standard methods for inventorying and monitoring coralligenous and maerl populations. UNEP-MAP, RAC/SPA Report. UNEP (DEPI)/MED WG.362/4. Tunis, 20 pp.). The current situation is not helped by the fragmented geopolitical scenario characterizing the Mediterranean basin, with weak, uncoordinated, conflicting approaches or non-existent regulatory frameworks, policy mechanisms and enforcement (Fraschetti et al. 2011Fraschetti S., Guarnieri G., Bevilacqua S., et al. 2011. Conservation of Mediterranean habitats and biodiversity countdowns: What information do we really need? Aquat. Conserv. Mar. Freshw. Ecosyst. 21: 299-306.). Improving the current and future monitoring of marine biodiversity is essential in order to implement the Marine Strategy Framework Directive (MSFD) and to achieve Good Environmental Status (GES). In addition to enhancing regional cooperation, there is a need to further develop innovative and cost-effective monitoring methods and to incorporate state-of-the-art technological developments into current monitoring practices (Patrício et al. 2014Patrício J., Teixeira H., Borja A., et al. 2014. DEVOTES recommendations for the implementation of the Marine Strategy Framework Directive. Deliverable 1.5, DEVOTES project. JRC92131, 71 pp.).

Habitat mapping is crucial in order to obtain reliable estimates of the total area occupied by each habitat, so as to reach the required conservation targets and to implement appropriate management measures (UNEP-MAP-RAC/SPA 2008UNEP-MAP-RAC/SPA. 2008. Action plan for the conservation of the coralligenous and other calcareous bio-concretions in the Mediterranean Sea. In: Pergent-Martini C. and Brichet M. (eds), RAC/SPA Tunis, 21 pp., Costello 2009Costello M.J. 2009. Distinguishing marine habitat classification concepts for ecological data management. Mar. Ecol. Prog. Ser. 397: 253-268.). A bibliographic database plays a major role in the study of habitat distribution and its changes over time. In some Mediterranean regions, information on coralligenous distribution is available in the literature but its reliability must be estimated (Leriche et al. 2001Leriche A., Boudouresque C. F., Bernard G., et al. 2001. A one-century suite of seagrass bed maps: can we trust ancient maps? Estuar. Coast. Shelf Sci. 59: 353-362.). Acoustic technologies are increasingly being used for monitoring benthic habitats (Zapata-Ramirez et al. 2013Zapata-Ramirez P.A., Scaradozzi D., Sorbi L., et al. 2013. Innovative study methods for the Mediterranean coralligenous habitats. Adv. Oceanol. Limnol. 4(2): 102-119.), and those used for mapping coralligenous communities normally include side-scan sonars and multibeam sonars (Bonacorsi et al. 2012Bonacorsi M., Pergent-Martini C., Clabaut P., et al. 2012. Coralligenous ‘atolls’: Discovery of a new morphotype in the Western Mediterranean Sea, Comptes. Rendus. Biologie 335(10-11): 668-672., Gordini et al. 2012Gordini E., Falace A., Kaleb S., et al. 2012. Methane related carbonate cementation of marine sediments and related macroalgal coralligenous assemblages in the Northern Adriatic Sea. Elsevier, London, 183-198.). Acoustic mapping using multibeam echo sounders allows us to infer seafloor topography, and therefore the geomorphologies on which coralligenous assemblages thrive, and the best locations for ground truthing. The European Commission decision on descriptors for the MSFD states that data of geographic information systems (GIS) are a prerequisite for ecosystem-based management of human activities and for developing related spatial tools. Modelling and mapping using GIS provide the basis for informed decision making (Sardá et al. 2012Sardá R., Rossi S., Martí X., et al. 2012. Marine benthic cartography of the Cap de Creus (NE Catalan Coast, Mediterranean Sea). Sci. Mar. 76(1): 159-171.).

In this work we combined a literature review, acoustic mapping and in situ observations to (i) build a map of the distribution of coralligenous assemblages in Liguria (NW Italy) using GIS; (ii) characterize their biology and geomorphology and study the influence of geomorphology and light conditions on biological features; and (iii) consider the main pressures affecting coralligenous assemblages and provide some management recommendations.

MATERIALS AND METHODSTop

Study area

The Ligurian coast falls into the Ligurian Sea, the northernmost part of the western Mediterranean Sea, with 350 km of arch-shaped coastline from Ventimiglia at the west border with Provence-Alpes-Côte d’Azur (France) to La Spezia at the east border with Tuscany, Italy. Almost two thirds of the coast is composed of cliffs and promontories alternating with sandy to gravelly pocket beaches, especially along the Eastern Riviera. Soft coasts are less developed and are typically found adjacent to small coastal plains along the Western Riviera (Cattaneo-Vietti et al. 2010Cattaneo-Vietti R., Albertelli G., Aliani S., et al. 2010. The Ligurian Sea: present status, problems and perspectives. Chem. Ecol. 26: 319-340., Rovere 2011Rovere A. 2011. Rocky coast in the Ligurian Sea: morphology, evolution and management aspects. PhD thesis, Univ. Genoa, 236 pp.).

Literature review and database creation

We combined a literature review, acoustic mapping and in situ observations to build a data layer of coralligenous presence using the ArcGIS® software by Esri (Environmental Systems Resource Institute), ArcMap 10.2 (www.esri.com). The existing literature was collected from scientific publications, technical reports (“grey literature”), diving and fishing books; we also considered unpublished in situ observations by experts and recreational divers (Cánovas-Molina et al. 2014Cánovas Molina A., Montefalcone M., Canessa M., et al. 2014. Proceedings of the 2nd Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. In: Pergent-Martini C. and Brichet M. (eds). RAC/SPA Publ. Tunis, pp. 55-60.). In order to estimate the reliability of the literature reviewed, a dependability index (DI) was applied, considering two parameters: geospatial positioning (five points) and method adopted for data acquisition (five points) (Table 1). The DI was not calculated for documents taken from the literature reviews because of the variety of methods used for data acquisition. A score of 1 for at least one of the parameters measured in the DI, was considered the critical value for low dependability and therefore rejection. Where digital spatial information was not available, polygons of presence of coralligenous assemblages were created by extracting spatial information from textual descriptions, helped by acoustic mapping (multibeam echo sounder) provided by Regione Liguria, when available. We carried out ground truthing through SCUBA diving at selected sites (Vado Ligure, Cogoleto, Arenzano and Punta Manara), following expert divers’ observations and/or seafloor topography revealed by multibeam echo sounder.

Table 1. – Scores of the dependability index (up to 5+5 points) from the literature.

Geospatial positioning Scores
very approximate descriptive spatial information 1
descriptive spatial information with selected terrestrial points and bathymetric data 2
descriptive spatial information and acoustic mapping (multibeam echo sounder) 3
GPS coordinates and acoustic mapping (multibeam echo sounder) 4
files already georeferenced 5
Data acquisition
fishing material 1
recreational diving before 2000 2
scientific diving before 2000 3
recreational diving after 2000 4
scientific diving after 2000 5

Database analysis

A list of characteristic sessile megabenthos species of coralligenous assemblages, identified from the literature review and in situ observations, was compiled. Facies were identified following the EUNIS Habitat Classification (Davies et al. 2004Davies C.E., Moss D., Hill M.O. 2004. EuNIS Habitat Classification revised 2004. Report to the European Topic Centre on Nature Protection and Biodiversity, European Environmental Agency, October 2004.). The habitat classification developed and managed by the European Topic Centre for Nature Protection and Biodiversity (ETC/NPB in Paris) provides a comprehensive typology for the habitats of Europe and its adjoining seas. EUNIS habitats are arranged in a hierarchy, from level 1 to 4 for marine habitats. Information on the most conspicuous species was used to identify the facies for each site with coralligenous.

Geomorphotypes where coralligenous assemblages in Liguria thrive were identified using multibeam echo sounder, when available, and textual descriptions from the literature gathered. Four geomorphotypes were considered: i) cliffs, vertical or near-vertical walls from a steep rock face, either active (plunging cliffs) or inactive (paleocliffs), ending occasionally in a flat bottom; ii) rockfalls, sets of masses of rocks of different sizes and shapes that lay on a bedding plane that originated from the face collapse of the cliff; and iii) shoals, isolated outcrops surrounded by sand or biodetrital sediments, which originated through past erosional events of the cliff, sea level rise and deposition of sediments.

To study the influence of incident light on coralligenous assemblages, we calculated incident light values on coralligenous assemblages from satellite imagery and long term-Secchi Disc records in Liguria available for the Portofino coastal area (Rapallo, Genoa). Percent light values of surface irradiance at each station in Portofino were calculated using standard methods with the formula Ez=E0e-kz (Kirk 1994Kirk J.T.O. 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge Univ. Press, 500 pp.), where Ez is the irradiance at depth z, E0 is the surface irradiance, K is the vertical attenuation coefficient and z is the depth. K was approximate to KdPAR and obtained using Secchi Disc transparency records (January 2002-December 2012) using the formula KdPAR=1.7/Secchi Depth (m). E0 was approximated to photosynthetically active radiation and obtained from Goddard Earth Sciences Data and Information Services Centre (GES DISC) Interactive Online Visualization and Analysis Infrastructure, “Giovanni” (January 2002-December 2012). Percent light values of surface irradiance on facies of coralligenous assemblages for each station were calculated as the mean value among incident light values at the shallowest and the deepest distribution. To test the influence of incident light on the distribution of coralligenous facies in Portofino, a one-way ANOVA was applied.

Information on presence of mechanical and biological pressures, as well as signs of mass mortality events due to water temperature increasing, was reported for each site with coralligenous assemblages.

RESULTSTop

Literature reliability

From 1937 to date, 58 documents described some aspects of the coralligenous habitat in Liguria (Supplementary material Table S1), mainly scientific papers or technical reports written in Italian. The Eastern Riviera and Marine Protected Areas (MPAs), i.e. Portofino (Rapallo, Genoa), Punta Mesco (Cinque Terre, La Spezia), and Isole di Portovenere (La Spezia), were among the most studied localities, accounting for 70% and 58% of the documents respectively. Data were acquired mainly by means of scientific SCUBA diving during the last two decades. Acoustic mapping was available for 10 localities. Eleven documents showed score 1 for at least one of the parameters of the DI and therefore have low dependability.

Distribution of coralligenous assemblages

A total of 90 sites within 18 localities were found to have coralligenous assemblages with an extent of 130.9 ha (Fig. 1 and Supplementary material Table S2). Seven localities (59.6 ha) were found along the Eastern Ligurian Riviera and 11 localities (71.3 ha) along the Western Riviera, the furthest location being 4 km from the coast at Capo Berta (Imperia) and the closest near the shoreline at Portofino. Regional and National protection laws applied for 48.3 ha (37%) situated in Portofino, Cinque Terre and Portovenere. The shallowest coralligenous assemblages in Liguria were those of Portovenere and Portofino at 10 m depth, the deepest that of Bergeggi at 113 m depth.

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Fig. 1. – Presence of coralligenous assemblages in Liguria. To make small-scale presence visible, boundaries of polygon features have been artificially enhanced. Surface areas covered by these habitats appear much larger than they are in reality. CaMo, Capo Mortola; SaSt, Santo Stefano; PoMa, Porto Maurizio; CaBe, Capo Berta; CaMe, Capo Mele; IsGa, Isola Gallinara; IsBe, Isola Bergeggi; VaLi, Vado Ligure; Vara, Varazze; Cogo, Cogoleto; Aren, Arenzano; PoFi, Portofino; PuMa, Punta Manara; PuBa, Punta Baffe; Leva, Levanto; PuMe, Punta Mesco; CaMt, Capo Montenegro; PoVe, Portovenere.

Biology, geomorphology and incident light values

A preliminary attempt to estimate the total number of sessile megabenthos taxa in the Ligurian coralligenous habitat is presented in Supplementary material Table S3. Sponges were the dominant group in terms of species richness (Fig. 2). The literature review permitted us to identify 12 facies of coralligenous communities (Table 2).

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Fig. 2. – Taxonomic composition of coralligenous sessile megabenthos in Liguria.

Table 2. – Population units identified in coralligenous assemblages of Liguria. *massive/erect sponges includes Spongia lamella, Sarcotragus foetidus, Scalarispongia scalaris, Axinella polypoides, Chondrosia reniformis and/or Petrosia ficiformis.

EUNIS Habitat 2004: A4.26 Mediterranean coralligenous communities moderately exposed to hydrodynamic action
A4.261 Association with Cystoseira zosteroides
A4.266 Association with Mesophyllum lichenoides
A4.269 Facies with Eunicella cavolini
A4.26A Facies with Eunicella singularis
A4.26B Facies with Paramuricea clavata
A4.26C Facies with Parazoanthus axinellae
EUNIS Habitat 2004: A4.32 Mediterranean coralligenous communities sheltered from hydrodynamic action
A4.322 Facies with Leptogorgia sarmentosa
Not included in the EUNIS Habitat 2004
Facies with Eunicella verrucosa
Facies with Leptopsammia pruvoti
Facies with massive/erect sponges*
Facies with Corallium rubrum
Facies with Pentapora fascialis

In Liguria four different coralligenous geomorphotypes were identified (Fig. 3). Shoals were the dominant morphology in Liguria in terms of extent, with 50.6 ha, and were mainly represented in the Western Riviera. Plunging cliffs, paleocliffs and rockfalls covered 32.6, 29.8 and 17.9 ha, respectively (Table 3). Paleocliffs and rockfalls were mainly colonized by facies with Paramuricea clavata. In fact, this facies was the most conspicuous, found in all geomorphotypes with the highest extension. Units of assemblages with Mesophyllum lichenoides, Parazoanthus axinellae, Cystoseira zosteroides and Eunicella verrucosa showed a more constrained distribution, being found only on shoals.

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Fig. 3. – Geomorphotypes found in Liguria. A, Shoals of Vado Ligure. B, Rockfalls of Casa del Sindaco, Portofino. C, Plunging cliff of Isola Gallinara. D, Paleocliff of Secca dei Maledetti, Isola di Bergeggi.

Table 3. – Distribution of coralligenous facies on the different geomorphotypes in Liguria (values in hectares). N/A, no data available.

Plunging cliff Paleocliff Rockfalls Shoals
Corallium rubrum 4.84
Cystoseira zosteroides 1.30
Eunicella cavolini 3.88 0.71 2.33
Eunicella singularis 0.91 0.58
Eunicella spp. 0.91 3.86
Eunicella verrucosa 1.14
Leptogorgia sarmentosa 6.54 0.21
Leptopsammia pruvoti 0.43
Massive/erect sponges 2.54 2.69
Mesophyllum lichenoides 0.29
N/A 1.03 0.94
Paramuricea clavata 11.02 29.11 17.86 36.86
Parazoanthus axinellae 0.06
Pentapora fascialis 0.46 0.29
Total 32.56 29.82 17.86 50.55

In Portofino, incident light values on coralligenous communities varied from 0.003% to 28.37% of surface irradiance (Fig. 4). Eight facies of coralligenous assemblages thrived in Portofino promontory at different % values of surface irradiance (Fig. 5). A one-way ANOVA on incident light values showed significant differences between the facies with Paramuricea clavata, Eunicella cavolini, Corallium rubrum and Leptogorgia sarmentosa (p<0.01, F=6.13, df=3). Facies with Eunicella cavolini showed the highest distribution range of incident light values. On the other hand, Corallium rubrum, Paramuricea clavata and Leptogorgia sarmentosa thrived on lower and narrower ranges of light conditions.

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Fig. 4. – Incident light values on coralligenous assemblages of Portofino. A, Punta Cervara; B, Punta Coppo; C, Punta dell’Aurora; D, Dorsale Portofino; E, Punta Faro; F, Chiesa San Giorgio; G, Casa del Sindaco; H, Punta Vessinaro; I, Punta dell’Altare; J, Punta Fregante; K, Testa del Leone; L, Scoglio del Raviolo; M, Secca Gonzatti; N, Punta Carega; O, Scogliera del Dragone; P, Tetto del Dragone; Q, Cristo degli Abissi; R, San Fruttuoso; S, Punta Volpe; T, Punta Torretta; U, Cala dell’Oro Est; V, Cala dell’Oro Ovest; W, Punta Bussago; X, Punta Targuetta; Y, Secca dell’Isuela; Z, Punta Chiappa.

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Fig. 5. – Incident light values for the different facies thriving at Portofino promontory.

Main pressures

Pressures reported in the literature were mainly due to fishing activities, such as the presence of abandoned gears such as nets, traps and “palamiti” (a type of longliner). Other pressures were anchors, plastic bags, invasive species such as the macroalgae Caulerpa cylindracea and Womersleyella setacea, occasional mucilaginous events, and mass mortality events linked to climate warming. In Liguria, evidence of one or more such pressures was found in 30 of 90 sites.

DISCUSSIONTop

Database of coralligenous assemblages

A total of 47 documents describing aspects of coralligenous habitats in Liguria were considered reliable after applying the DI for literature, and were therefore used to assess the distribution, biology, geomorphology and pressures. As digital spatial information and GPS positioning were scarce in the literature review, combining it with acoustic mapping and in situ observations helped improve accurate positioning on a GIS platform. Literature dealing with coralligenous assemblages in Liguria is more detailed for the Eastern Riviera, accounting for 70% of the documents, where their distribution is mainly associated with cliffs. The Western Riviera has been poorly studied and rarely characterized due to its particular distribution on isolated rocky outcrops of little extent found patchily along the coast.

Distributional, biological and geological aspects

Coralligenous habitats can be defined as highly heterogeneous systems, where the environmental variables together with distribution and abundances of taxa can differ greatly on both a geographical and a local (tens of metres) scale (Ferdeghini et al. 2000Ferdeghini F., Acunto S., Cocito S., et al. 2000. Variability at different spatial scales of a coralligenous assemblage at Giannutri Island (Tuscan Archipelago, northwest Mediterranean). Hydrobiologia 440: 27-36., Balata et al. 2005Balata D., Piazzi L., Cecchi E., et al. 2005. Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposition. Mar. Environ. Res. 60: 403-421., Virgilio et al. 2006Virgilio M., Airoldi L., Abbiati M. 2006. Spatial and temporal variations of assemblages in a Mediterranean coralligenous reef and relationships with surface orientation. Coral Reefs 25: 265-272.). The coralligenous assemblages in Liguria therefore show high spatial, morphological and biological variability (Fig. 6).

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Fig. 6. – Coralligenous assemblages in Liguria. A, facies with Paramuricea clavata thriving on shoal geomorphotype (Corallo Nero, Vado Ligure) at 32 m depth. B, facies with Eunicella cavolini on cliff geomorphotype (Cala dell’Oro, Portofino) at 14 m depth. C, Facies with Leptopsammia pruvoti (Punta Cervara, Portofino) at 18 m depth. D, facies with massive/erect sponges (Punta Manara) at 36 m depth. E, Savalia savaglia colony (Punta Manara) at 39 m depth. F, presence of lost fishing gears (Punta Manara) at 35 m depth. G, Facies with Corallium rubrum (Punta dell’Altare, Portofino) at 38 m depth. H, presence of mucilaginous event (Punta dell’Altare, Portofino) at 38 m depth.

The shallowest distribution of coralligenous communities in Liguria was found in Portovenere, where they developed from 10 to 30 m depth associated with low light irradiance. Sediment load coming from the Magra River, located about 10 km away, explains the high turbidity in the water, with Secchi Disc values of 6.2±1.6 m (Bassano et al. 2000Bassano E., Boniforti R., Pezzani A. 2000. Parametri meteorologici e idrologici. In: Peroni C. (ed), Sistema informativo e di monitoraggio marino costiero della provincia della Spezia. ENEA, Rapp. Tec, pp. 17-55.). Twelve facies were identified in the Ligurian coralligenous assemblages. Eunicella verrucosa and massive/erect sponges could be assigned to EUNIS Habitat 2004 classification as A4.32 Mediterranean coralligenous communities sheltered from hydrodynamic action and Corallium rubrum, Leptopsammia pruvoti and Pentapora fascialis to A4.26 Mediterranean coralligenous communities moderately exposed to hydrodynamic action. An update of the EUNIS list is needed in order to consider the real biological heterogeneity of coralligenous communities (Bianchi et al. 2010Bianchi C.N., Morri C., Navone A. 2010. The biological assemblages of submerged rocky reefs in the Marine Protected Area of Tavolara Punta Coda Cavallo (north-east Sardinia, Italy). Sci. Rep. Port-Cros Nat. Park, 24: 39-85.).

In the marine environment, light is a key environmental variable coupling physics to biogeochemistry and ecology. According to Ballesteros (1992)Ballesteros E. 1992. Els vegetals i la zonació litoral: espècies, comunitats i factors que influeixen en la seva distribució. Arx. Sec. Cièn. Inst. Est. Catalans 101: 1-616., coralligenous communities develop between 0.05% and 3% of the surface irradiance. “Dorsale Portofino” reaches light values below 0.05% (0.003-0.14%) where coralligenous assemblages grow on shoals between 52 and 84 m depth and are dominated by suspension feeders: gorgonians, antipatharians and sponges with few calcareous concretions. Light values greater than 3% correspond to coralligenous communities above 27 m depth with a high frequency of so-called “precoralligenous” species (Bianchi et al. 2004Bianchi C.N., Boero F., Fraschetti S., et al. 2004. Il popolamento sommerso. In: Minelli A. (eds), Coste marine rocciose: la vita tra rocce e salsedine. Ministero dell’Ambiente e della tutela del Territorio e del Mare, Roma, and Museo Friulano di Storia Naturale, Udine, Quaderni Habitat, 7: 105-134.), such as Cladocora caespitosa, Codium bursa, Flabellia petiolata, Halimeda tuna and Sarcotragus fasciculatus as components of coralligenous communities with high light tolerance.

In coralligenous assemblages two main geomorphologies have been described (Pérès and Picard 1964Pérès J.M., Picard J. 1964. Nouveau manuel de bionomie benthique de la Mer Méditerranée. Rec. Trav. Stat. Mar. Endoume 14: 1-137., Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Ann. Rev. 44: 123-195.): i) banks, which can fall into the coralligène de plateau definition and consist of flat frameworks with a variable thickness (0.5 to 4 m) built on horizontal substrate; and ii) rims, which can fall into the coralligène de l’horizon inférieur de la roche littorale definition and consist of structures developed along vertical cliffs with a thickness range of 0.2 to 2 m. Some problems arise in trying to classify coralligenous formations into these two categories due to the high variability of the build-ups in terms of geometry, dimension, areal distribution and settled substrate (Bracchi et al. 2014Bracchi V.A., Basso D., Savini A., et al. 2014. Coralligenous: insights for a new geomorphological definition. In: Pergent-Martini C. and Brichet M. (eds), Proceedings of the 2nd Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. RAC/SPA Publ. Tunis, pp. 49-54.). In Liguria, the high variability of origin, extension, slope and shape of geomorphologies led us to identify, as did Laborel (1961)Laborel J. 1961. Le concrétionnement algal “coralligène” et son importance géomorphologique en Méditerranée. Rec. Trav. Stat. Mar. Endoume 23 (37): 37-60., four different geomorphotypes: cliffs (paleocliffs and plunging cliffs), shoals, and rockfalls.

Main pressures

Pressures were found at 33% of the sites, mainly due to professional and recreational fishing activities, mass mortality events, presence of invasive species and mucilaginous events. In Portofino, a major cause of mortality in Paramuricea clavata is damage by fishing lines, followed by the attachment of numerous epibionts (Bavestrello et al. 1997Bavestrello G., Cerrano C., Zanzi D., et al. 1997. Damage by fishing activities to the gorgonian coral Paramuricea clavata in the Ligurian Sea. Aquat. Conserv. Mar. Freshw. Ecosyst. 7: 253-262.). Coralligenous habitats have been invaded by alien species such as Caulerpa cylindracea (Piazzi et al. 2007Piazzi L., Balata D., Cinelli F. 2007. Invasions of alien macroalgae in Mediterranean coralligenous assemblages. Cryptogam. Algol. 28: 289-301.) and/or Womersleyella setacea (Gatti et al. 2015Gatti G., Bianchi C.N., Parravicini V., et al. 2015. 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 (2): e0118581.), with consequent loss of structure and biodiversity of the original assemblages. In the late summer of 1999, when a sudden increase in sea water temperature in the Ligurian Sea occurred down to 50 m depth, an extensive mortality of gorgonians and other epibenthic organisms was observed in Liguria: the proportion of affected gorgonians ranged from 60% to 100%, suggesting that millions of sea fans died (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.).

Management recommendations

We highly recommend including coralligenous habitats in the EU Habitats Directive (92/43/EEC) as a priority natural habitat type. In addition, MPAs must be established in order to protect representative coralligenous assemblages by applying the protection and management measures recommended by Articles 6 and 7 of the SPA protocol (Ballesteros 2009Ballesteros E. 2009. Threats and conservation of coralligenous assemblages. In: Pergent-Martini C. and Brichet M. (eds), Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. RAC/SPA Publ. Tunis, pp. 25-27.). In Liguria, 48.3 ha (37%) of coralligenous habitats are inside national or regional MPAs. Among the 82.6 ha of coralligenous assemblages without a specific conservation plan, the assemblages of Bergeggi and the deep (>70 m) assemblages of Portofino lie outside the limits of the MPAs of “Isola di Bergeggi” and “Portofino”, respectively. Therefore, we recommend the extension of the two MPAs in order to include them.

To enforce the MSFD and achieve GES, we suggest the implementation of a common monitoring programme for coralligenous habitats of Liguria. This monitoring programme should fulfil the following requirements:

- It should take into account their high geographic and biological heterogeneity and therefore be applied also in the poorly studied shoals of the Western Riviera.

- It should be able to assess ecological status and pressures and their linkage. Ecological status assessment should consider coralligenous structure (e.g. species richness and percentage cover), as well as functioning (e.g. connectivity and population dynamics).

- It should include new methods and technologies. The use of photo-video mosaicing can provide information on both landscape level (metre-scale) maps and high-resolution (sub-millimetre) images of individual colonial organisms (Reid et al. 2010Reid R.P., Lirman D., Gracias N., et al. 2010. Application of landscape mosaic technology to complement coral reef resource mapping and monitoring. SERDP Project RC-1333, 189 pp.). If further validated, the photo mosaic techniques and 3D reconstructions would provide a cost-effective tool for assessing ecological status and monitoring changes due to natural or anthropogenic disturbance in these environments (Zapata-Ramirez et al. 2013Zapata-Ramirez P.A., Scaradozzi D., Sorbi L., et al. 2013. Innovative study methods for the Mediterranean coralligenous habitats. Adv. Oceanol. Limnol. 4(2): 102-119.).

Combining a literature review (scientific publications, unpublished documents and books), acoustic mapping and in situ observations (ground truthing and personal communications) on a GIS platform resulted in an efficient, powerful tool for the assessment of the distribution and heterogeneity of coralligenous communities and the pressures affecting them. This methodology could give information on the real extent and diversity of these assemblages to help governments and stakeholders implement appropriate management measures to guarantee sustainable development of coastal areas.

ACKNOWLEDGEMENTSTop

The study was carried out within the framework of the project PRIN 2010-11 Bioconstructions funded by the Italian Ministero dell’Istruzione, dell’Università e della Ricerca. We wish to thank the Regione Liguria for giving us multibeam data and bibliographic information. We thank Paolo Povero (Genoa) and Felice Zanini (Genoa) for providing information and Roy Armstrong, William Hernández (Puerto Rico), Daniel Mateos Molina (Murcia) and Matteo Vacchi (Marseille) for their advice.

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Suplementary material

The following material is available through the online version of this article and at the following link:
http://www.icm.csic.es/scimar/supplm/sm04235esm.pdf

Table S1. – Literature review on coralligenous assemblages in Liguria. Scarce, scarce biological information or just focused on one species. DI (GP+DA), dependability index of literature (Geospatial Positioning + Data Acquisition).*Score=1 for at least one of the parameters considered in the DI.

Table S2. – Ligurian localities with coralligenous and main characteristics. N/A, No data available. * Facies not included in the EUNIS Habitat 2004 classification for Mediterranean coralligenous communities.

Table S3. – List of sessile megabenthos taxa reported by different authors for the Ligurian coralligenous community.



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