Marine Environmental Research 192 (2023) 106211 Contents lists available at ScienceDirect Marine Environmental Research journal homepage: www.elsevier.com/locate/marenvrev Coexistence of megabenthic assemblages and artisanal fishers: The case of Cap de Creus Marine Protected Area (North-Western Mediterranean Sea) A. Higueruelo a, *, A. Santín b, c, J. Salazar b, d, S. Ambroso e, A. Soler-Membrives a, J. Grinyó f a Departament de Biologia Animal, de Biologia Vegetal i d’Ecologia, Universitat Autònoma de Barcelona, Cerdanyola Del Vallès, 08193, Barcelona, Spain b Institut de Ciències Del Mar (ICM-CSIC), Passeig Marítim de La Barceloneta, 37-49, 08003, Barcelona, Catalonia, Spain c CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Matosinhos, Portugal d Programa de Ciències Del Mar, Facultat de Ciències de La Terra, Universitat de Barcelona, Av. Diagonal, 643, 08028, Barcelona, Spain e Departament de Biologia Evolutiva, Ecologia I Ciències Ambientals, Universitat de Barcelona, Av. Diagonal, 643, 08028, Barcelona, Spain f Department of Ocean Systems, Royal Netherlands Institute for Sea Research (NIOZ), Den Burg, Netherlands A R T I C L E I N F O A B S T R A C T Keywords: Artisanal fisheries, although considered less harmful, can still endanger marine ecosystems, especially in areas Artisanal fishing with long-standing tradition. In Cap de Creus, where artisanal fisheries has likely occurred for centuries, the Benthic ecology status of benthic communities in fishing grounds was poorly understood. Through collaboration with local Community composition fishers, the benthic assemblages in three artisanal fishing grounds within Cap de Creus Marine Protected Area Fishing impacts (MPA) were studied. Using video transects recorded by a remotely operated vehicle (ROV), the diversity and Fishing gear Marine protected area distribution of species were analysed in relation to substrate type, slope, and depth. The study also assessed the ROV-Imaging impacts on these communities by examining marine litter, lost fishing gear, and the condition of gorgonian Western mediterranean sea populations. The findings identified three megabenthic assemblages and revealed higher fishing pressure and impact in the Maça d’Oros area, likely due to multiple fishing guilds converging. However, the study demon­ strated lower impact in MPAs compared to unprotected Mediterranean areas, highlighting the importance of coastal management. 1. Introduction Endangered (EN), or Vulnerable (VU)), including species like Para­ muricea clavata (VU) and Corallium rubrum (EN) in rocky habitats, or Benthic communities comprise a wide variety of habitats funda­ Pennatula rubra (VU) and Pteroides spinosum (VU) in soft bottoms, which mental to aquatic ecosystems, playing a major role in ecological pro­ play important structuring roles in NW Mediterranean littoral and inner cesses (Crespo et al., 2020; Snelgrove, 1997). These communities, shelf habitats (Otero et al., 2017). Their classification as endangered is especially in coastal areas, are crucial for benthic-pelagic coupling largely due to the reduction of some Mediterranean populations caused processes, important for nutrient cycling and energy transfer in food by the effects of global change over the last three decades (thermal webs (Griffiths et al., 2017). Additionally, they provide habitat, refuge anomalies, summer development of invasive algae and mucilage, and and nursery grounds to a wide range of associated species, some of exceptional storms), as well as a wide range of direct and indirect fishing which of commercial value (Henseler et al., 2019; Kritzer et al., 2016; impacts (Angiolillo et al., 2015; Betti et al., 2020; Bo et al., 2014; Gar­ Rufino et al., 2017). World benthic ecosystems are being degraded to rabou et al., 2022). Consequently, it is of paramount importance to different extents by the detrimental effects caused by climate change, preserve and protect these highly ecologically important areas (Nav­ nutrient loading and fishing practices (Griffiths et al., 2017; Lotze et al., arro-Barranco et al., 2023). 2006). In the Mediterranean the degraddation of benthic ecosystems Fishing impacts include habitat destruction, direct extraction and appears to occur faster than in other temperate areas of the world mortality of non-target species due to accidental non-target catches (Garrabou et al., 2022). In fact, according to the recent Mediterranean (Enrichetti et al., 2019), and chronic contact with fishing gears due to IUCN Red List evaluations, 25% of the Mediterranean anthozoans are recreational and professional demersal fishing activities (Bavestrello estimated to be threatened with extinction (Critically Endangered (CR), et al., 1997; Betti et al., 2020; Cebrian et al., 2012; Otero et al., 2017). If * Corresponding author. E-mail addresses: Andrea.Higueruelo@uab.cat, andreahigueruelof@gmail.com (A. Higueruelo). https://doi.org/10.1016/j.marenvres.2023.106211 Received 27 June 2023; Received in revised form 14 September 2023; Accepted 26 September 2023 Available online 1 October 2023 0141-1136/© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by- nc/4.0/). A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 the effects of these activities are prolonged over time, they can lead to Confraries; the name given to professional fishers’ organizations) of Port evolutionary shifts in population demographics and changes in the de la Selva and Cadaqués (Alt Empordà, Catalonia) have cooperated function and structure of megabenthic assemblages (Pikitch et al., with researchers by letting them collect data on the by-catch benthic 2004). Even though artisanal fisheries are often considered to have species during their practices, while parallelly participating on a joint lesser impact on marine habitats than other fishing activities such as ROV exploration of the main fishing grounds of both guilds in order to trawling, they still pose a threat to marine ecosystems, especially in evaluate their conservation status. The purpose of this study is, thus, i) to areas where they have been practised for long periods of time (Lokrantz analyse the diversity and abundance of benthic species in the artisanal et al., 2010). Historically, small-scale fisheries usually work on shallow fishing grounds of Cap de Creus and characterise their assemblages, ii) to marine bottoms that consist of a mosaic of rocky substrate combined assess and compare the impacts of artisanal fishing on the different with some deeper soft sediment assemblages (Demestre et al., 2000). fishing grounds, and iii) to infer into the potential impacts on gorgonian The bathymetric distribution and rugged morphology of artisanal fish­ populations (based on size structure, epibiosis and necrosis) as bio­ ing grounds generally restricts the presence of bottom trawling, allowing indicators of anthropogenic and fishing impacts. the development of relatively complex animal forests mostly formed by gorgonians (Díaz et al., 2015). Two of the most common habitat-forming 2. Material and methods gorgonians in the Mediterranean, Eunicella cavolini (up to 60 cm high) (Montseny et al., 2021; Sini et al., 2015) and Paramuricea clavata (up to 2.1. Study area 100 cm high) (Linares et al., 2008), are often caught in fishing nets due to their fan-shaped morphology and size (Dias et al., 2020). As gorgo­ The Cap de Creus area (42◦ 19′12″ N, 03◦ 19′34″ E) is located in the nians are usually long-lived and slow-growing organisms, this fishing Gulf of Lions, in the North-Western Mediterranean Sea, being the first activity can have far-reaching and long-lasting effects on their pop­ maritime-terrestrial Natural Park established in Catalonia. The park ulations (Bennecke and Metaxas, 2017). Furthermore, lost ropes, long­ covers a total area of 13,886 ha, of which only 3073 ha belong to the lines and demersal nets may either detach the colonies or become marine realm (Law April 1998 (BOE, 1998)). In 2014, Cap de Creus area entangled, favouring the development of epibionts and leading to was also declared a Special Protection Area (SPA) (Area ES5120007) of increased mechanical stress (Bavestrello et al., 1997; Bo et al., 2014). All the Natura 2000 Network (Acord GOV/150/2014 (DOGC, 2014)). these reasons, together with the fact that they are sessile and cannot The Cap de Creus littoral and shallow continental shelf includes a migrate, make gorgonians suitable as bioindicators of anthropogenic wide variety of substrates, being sandy and muddy sediments the most impacts (Kupfner Johnson and Hallock, 2020; Murillo et al., 2020). frequent ones and also an abrupt morphology, with rocky outcrops, Marine Protected Areas (MPAs) in the Mediterranean Sea pretend to relict bioherms, erosive features, and planar bedforms (Lo Iacono et al., preserve the environment, traditional activities, and to help recover­ 2012). stocks. In North-Eastern Catalonia we encounter the Cap de Creus area Regarding its hydrological setting, the Liguro-Provenzal-Catalan (NW Mediterranean Sea) which is under several figures of protection, current (aka Northern Current) from the Gulf of Lions and the input with two contiguous Sites of Community Importance (SCIs), the ‘Park from the Rhône River, together with strong dominant north winds del Cap de Creus’, which covers the land and coastal area of the cape and causing water mixing, make this area a highly productive zone (Courp the ‘Sistema de cañones submarinos occidentales del Golfo de León’, and Monaco, 1990; Lloret et al., 2008). Consequently, it is an area which extends from waters below 60 m and beyond (Sardá et al., 2017). conducive to the agglomeration of pelagic fish and other species of The Cap de Creus SCI was also the first terrestrial-maritime reserve commercial interest (Purroy et al., 2014). established in Spain (Official State Gazette [BOE], 1998), thus, having Specifically, after the exchange of information with local fishers, our had its coastal waters under protection for almost three decades. Yet, study focused on the main artisanal fishing grounds identified on this artisanal fisheries have remained active in the area uninterruptedly, area, those being in Farallons and Illa Portaló (zone A and B, respec­ being of great importance and cultural significance to the local com­ tively) and Maça d’Oros (zone C), with no more than 100 m depth munities. This activity does not only provide food resources, but has also (Fig. 1). been a source of employment and economic growth for the people living in the coastal villages (Lloret et al., 2010). This type of fishing is nor­ 2.2. Sampling procedure mally carried out in small boats (less than 8 m length) and, due to the complexity of the area, fishermen may employ various types of fishing A total of 18 video transects were recorded onboard the “Atlantic gears, yet trammel nets, gillnets, and pots are the most extensively used Explorer” vessel between the 24th and July 30, 2018 using a Perseo ROV targeting species like spiny lobster (Palinurus elephas) or the common (Fig. 1). octopus (Octopus vulgaris) (Lloret et al., 2010). The ROV was equipped with a high-definition (HD) camera, an A study conducted on Cap the Creus, identified the fringe coast and additional 4 K camera, depth sensors and two parallel laser beams that canyon margins to be the most potentially impacted by fishing pressure provided a fixed scale of 30 cm distance used in the subsequent video within the area. Apart from that, not much is known about the conser­ analyses. Transect length varied between 150 and 1150 m, with a total vation state of the benthic assemblages occurring in the artisanal fishing distance of 8,5 km recorded. The bathymetric range covered was 10–76 grounds of the Cap de Creus (Purroy et al., 2014). However, recent m depth. technological advances and increased availability of remotely operated Initially, seven transects were targeted for each fishing ground (Fig. 1 vehicles (ROVs) and video-equipped towed gears have made possible to A, B, C), but due to bad weather conditions, only four transects could be carry out accurate and quantitative in-situ investigations, allowing performed in area C (Maça d’Oros). The rocky areas were prioritised controlled samplings and quantitative studies of bottom communities over the sandy areas due to the concentration of artisanal fishing prac­ beyond the depth range of traditional scuba diving (~40 m depth) (Gori tices in the former. The position of the sampling units was estimated et al., 2011; Orejas et al., 2009). from the recorded geographical coordinates of the initial and final point Within this context, the MITICAP project (Implementación de medidas of each transect. Each transect was recorded starting from the deepest innovadoras de cooperación entre pescadores y científicos para una mejor point and proceeding towards the coastline with a constant speed of gestión de la pesca artesanal con el objetivo de mitigar sus impactos en approximately 0.4 knots. Maximum depth assessed in this study was hábitats marinos sensibles) has emerged with the goal of implementing selected to cover almost the entire sublittoral zone in the study area, measures to mitigate the fishing impacts caused by artisanal fishing in from the littoral to the start of the continental shelf. This methodology Cap de Creus Marine Protected Area (Santín et al., 2022a). As part of the has been also used in other studies in the same area, such as Ambroso objectives of the MITICAP project, the artisanal fishers guilds (known as et al. (2013); Coppari et al. (2016); Gori et al. (2011). 2 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 Fig. 1. Map of the study area. Red dots corresponding to sampling transects. A) Farallons B) Illa Portaló and C) Maça d’Oros fishing grounds. Projected view: UTM Zone 31 N (WGS84), with coordinates in decimal degrees. 2.3. Video analysis Each sampling unit was characterised by the fishing ground, the number of the present megabenthic species, as well as by its depth and Quantitative video analysis was performed following the methodol­ coverage percentage for each substrate and slope type. Species occurring ogy described by Gori et al. (2011), using Final Cut Pro 7 software less than 3 times were excluded, as they could compromise statistical (Apple Inc.) and VLC media player. Pauses and loops were removed from analyses. Megabenthic assemblages were analysed using a non-metric the footage to avoid overestimations. Video sequences with poor image multidimensional scaling ordination (nMDS), with species abundances quality (e.g. recorded too far away from the sea floor) were discarded square root transformed, and ordination performed over a Bray–Curtis from the analysis. A total of 12 h and 10 min was considered suitable for dissimilarity matrix. the analysis. Furthermore, PERMANOVA (Adonis function) and subsequent pair­ All megabenthic species observed between de 0.3 m laser beams wise tests were performed to test for significant differences amongst along the video transect were identified to the lowest taxonomic level assemblages. The nMDS and Adonis test were performed using the R- possible. All species were assigned a time reference based on the language function “metaMDS” and “Adonis”, available in the vegan li­ beginning of the video transect which was recorded, and posteriorly brary of the R software platform (Oksanen et al., 2015). Once assem­ converted into a position along the transect using the constant speed of blages were identified, the Indicator value Index (IndVal) (Dufrêne and the ROV. Legendre, 1997) was used to determine which species were represen­ Moreover, along each transect additional information was recorded, tative from each assemblage. The IndVal method allows to identify such as: the type of seabed substrate (soft bottoms, rock and cor­ combinations of species that permit discriminating a group of samples alligenous), seabed slope (horizontal, sloping or vertical) and depth, from other samples in the analysis. IndVal measures were computed recorded every 2 m change. using the function “indval” included in the labdsv package of the R software (Roberts, 2019). 2.4. Data treatment 2.4.2. Impact assessment 2.4.1. Species occupancy, distribution and megabenthic assemblage Given the difficulty in evaluating the effects of fishing on soft-bottom composition organisms like pennatulaceans and cerianthids, which tend to retract To analyse the species distribution and composition within the study when disturbed, this study was focused on the main gorgonian species area, each transect track was divided into a string of 2 m2 (0.3 m width conforming hard habitat assemblages. and 6.66 m long) sampling units, to allow comparison with previous The population size structure analysis was conducted on the most studies on Mediterranean species (Ambroso et al., 2013; Gori et al., abundant gorgonians, namely Eunicella singularis, Paramuricea clavata, 2011; Grinyó et al., 2016). and Eunicella cavolini. During the video analysis, when a colony was seen 3 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 in-between the laser beams and perpendicular to them, an image was assemblage representing 43% of all observed organisms and reaching taken. Colonies size was measured using the software ImageJ, and densities of 51 col m− 2. further data on gorgonian colony status based on partially epibiosis, The complete results of species contributing to each assemblage is partially necrosed, or completely dead gorgonians were recorded. This shown in Table S1. information together with all the fishing gear and other marine litter identified during the video transects were noted into different cate­ 3.2. Impact assessment gories, to quantify the anthropogenic impacts in each transect. Size structure of gorgonian populations was analysed in terms of 3.2.1. Gorgonian size structure descriptive statistics using distribution parameters such as Skewness and The height of 2202 colonies were measured along the 18 transects. Kurtosis. Skewness is a measure of the symmetry of a distribution using Most populations of E. cavolini and E. singularis were positively skewed, its mean, here reflecting the proportion of small versus large colonies in indicating the dominance of small colonies (mostly between 0 and 30 a gorgonian population. If Skewness is significant (p < 0.05) population cm). A third part of E. cavolini and nearly half of E. singularis colonies size structure is asymmetrical. Positive Skewness denotes the prevalence showed significant kurtosis indicating that they were slightly more of small size colonies, while negative Skewness denotes the dominance peaked or over centralized than normal distributions. The gorgonian of large size colonies in the population. Kurtosis is a measure of the P. clavata showed no significant values in Skewness neither in Kurtosis peakiness of a distribution near its central mode. A significant Kurtosis test, which indicates the dominance of medium-sized colonies and no value (p < 0.05) indicates longer tails than would be expected for apparent prevalence of a particular size class (Table S. 2 and Figs. S2–S4. anormal distribution, and therefore the prevalence of a particular size Significance of kurtosis and skewness for each of these three species do class in the population (Grinyó et al., 2016; Linares et al., 2008; Santín not seem to be different among fishing grounds. et al., 2019). Skewness and Kurtosis were calculated by means of the Instead, size differences among fishing grounds were found. Eunicella R-language functions agostino.test (Komsta and Novomestky, 2012) and singularis and E. cavolini colonies were significantly smaller in Maça anscombe.test (Anscombe and Glynn, 1983), which are available in the d’Oros and P. clavata colonies were smaller in Maça d’Oros and Far­ “moments” library of the R software platform. Additionally, size dif­ allons rather than in Illa Portaló (p-value <0.05) (Table 2). ferences among the three different fishing grounds were tested with Kruskal-Wallis and Dunn’s Test. Finally, a correlation (R of Pearson) was 3.2.2. Impacts on benthic assemblages made between the density of anthropogenic litter found and the rates of Within the marine debris recorded, material related to artisanal or epibiosis, necrosis and dead colonies. recreational fishing was predominant, with 80.7% being lines and the other 7.2% other fishing gears such as trammel nets or pots. Other 3. Results marine debris (e.g. plastics or glass bottles) comprised the 12% of all litter found. Most items (87.5%) were found in hard habitats (cor­ 3.1. Species occupancy and distribution alligenous or rocky ones). The highest percentage of litter related to fishing was found in Maça d’Oros (95%), followed by Farallons fishing Three different megabenthic assemblages could be identified in the ground (94%). In Illa Portaló it represented the 75% (Fig. 3). nMDS according to the 955 sampling units with 48 different main spe­ The density of anthropogenic litter seen ranged between 0 and 0.13 cies, mainly segregated by depth and substrate (Fig. 2). The fishing items/m2 (mean = 0.05 ± 0.04 items/m2). Apart from that, 742 dead ground does not appear to affect the segregation of assemblages gorgonians were observed along the transects (6.26% of the total col­ (Fig. S1). onies), ranging between 0.01 and 1.75 dead gorgonians/m2 (mean = The first assemblage is represented by horizontal soft bottoms sub­ 0.30 ± 0.39 dead gorgonians/m2). In general, low percentages of ne­ strates between 50 and 80 m depth. The second is represented by slop­ crosis were observed, with a mean of 1.46% necrosed gorgonians and no ping rocky substrates, mostly between 30 and 80 m depth, while the last transect exceeding 5% (Table 3). Epibiosis rates on gorgonian pop­ one corresponded to coralligenous bottoms between 10 and 50 m depth ulations ranged between 0 and 25.48% of colonies affected, with a mean (Fig. 2). The Adonis and subsequent pairwise tests revealed that species of 16.01% (density between 0 and 0.15 n/m2; mean = 0.08 ± 0.09 n/ assemblages were significantly different for each of the environmental m2). In terms of abundance, the most common epibionts were categorizations, with a p-value <0.001. The only exception was between A. coralloides, Pentapora sp., several bryozoans and Filograna implexa. No slope and vertical sampling units (p-value < 0.1). significant correlations were found between the density of anthropo­ IndVal analysis showed that soft bottoms were characterised by three genic debris and the other variables studied. main species: the soft coral Alcyonium palmatum, the pennatuleacean Regarding comparisons among fishing grounds, Maça d’Oros showed Veretillum cynomorium and the large hydrozoan Lytocarpia myriophyllum a higher density of anthropogenic items (approximately double), (p < 0.001). Sampling units hosting these species presented higher together with twice as many dead colonies. The percentage of colonies species richness (1–10 species) and significantly higher densities (6.7 ± with epiphytes is also slightly higher in this area (Table 3). 0.4 Average ± SE; PERMANOVA; p-value = 0.003, PSEUDO-F = 9.716) Results of the main epiphyte species found in each area are shown in than units without them (species richness: 1–3; 3.4 ± 0.33 Average ± Table 4. A strong predominance of Alcyonium coralloides as epibiont was SE). detected in Maça d’Oros (70.3%) compared to Farallons (16.6%) and Illa On hard bottoms the most characteristic species were gorgonians. Portaló (24%) (Table 4). For coralligenous assemblages, we found P. clavata and E. singularis, followed by unidentified orange incrusting Porifera and sponges from 4. Discussion the genus Axinella. On coralligenous concretions between 10 and 50 m depth we encountered an assemblage constituted by the gorgonians 4.1. Species occupancy and distribution Paramuricea calvata and Eunicella singularis, the soft coral Alyonium acaule, different porifera species, of which two demosponge species of The segregation by depth and substrate of megabenthic assemblages the genus Axinella stand out, among others (Table 1). The red coral identified in the present study is in agreement with previous studies on (Corallium rubrum) could also be found, although in lower densities Mediterranean shelfs (e.g. Enrichetti et al., 2019; Grinyó et al., 2018). (Table S1). On the contrary, rocky bottoms were characterised by Eunicella 4.1.1. Soft sediment assemblages cavolini followed by Astrospartus mediterraneus and Alcyonium coralloides The most representing species of soft sediment assemblages (p < 0.001) (Table 1). The gorgonian E. cavolini clearly dominated this (A. palmatum, V. cynomorium and L. myriophyllum) (Fig. 4A and B) are 4 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 Fig. 2. Non-metric multidimensional scaling (nMDS) ordination plot. Species abundance was square root transformed and analysis performed on Bray–Curtis dissimilarity matrix. Every dot corresponding to a sampling unit (n = 955) containing different species is represented considering (a) depth range, (b) bottom type and (c) seabed slope. A stress estimate of 0.115 was obtained. 5 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 Table 1 (Di Camillo et al., 2013; Dominguez-Carrió et al., 2022; Grinyó et al., IndVal analysis, with the average and maximum density of the most contrib­ 2020). These organisms are extremely susceptible to bottom trawling uting species to each community (IndVal >0.1). Density values are only given and in other areas of the Mediterranean exposed to trawling they have for those species which were reliably identified. Avg.: average density ± stan­ become scarce (De Juan et al., 2007; Di Camillo et al., 2013). It is likely dard deviation; Max: maximum density. that these higher abundances indicate that these communities are well IndVal Probability Avg. (ind./ Max. (ind./ preserved and artisanal fishing does not pose a substantial toll as it m2) m2) mostly targets rock dwelling species (e.g. common octopus, spiny lob­ Coralligenous ster, rockfish). Paramuricea clavata 0.5280 0.001 2.94 ± 2.7 13 Eunicella singularis 0.4688 0.001 5.81 ± 5.1 23 4.1.2. Inner-shelf rock assemblages Orange encrusting 0.2695 0.001 – – Porifera The dominance of E. cavolini (Fig. 4C) in rocky outcrops between 30 Axinella spp. 0.2327 0.001 2.04 ± 3.15 20 and 80 m depth is in accordance with previous observations (Grinyó Axinella polypoides 0.1715 0.001 1 ± 0.82 5 et al., 2016). Indeed, this species has shown to play a paramount role in Red encrusting Porifera 0.1599 0.001 – – coral gardens in mesophotic and circalittoral environments in outer Alcyonium acaule 0.1411 0.001 2.98 ± 3.15 11 shelf, shelf edge and seamount environments in other areas of the Halocynthia papillosa 0.1408 0.001 0.81 ± 0.42 2 Holothuria spp. 0.1328 0.001 0.84 ± 0.52 2 western Mediterranean (Bo et al., 2011; Cau et al., 2017; Domi­ Myriapoda truncata 0.1328 0.001 0.82 ± 0.47 2 nguez-Carrió et al., 2022; Grinyó et al., 2016; Lo Iacono et al., 2020). Rock Paramuricea clavata (and P. macrospina) were also present in this Eunicella cavolini 0.5139 0.001 7.30 ± 8.45 51 assemblage, though they occurred at lower densities than in other areas Astrospartus 0.3947 0.001 1.15 ± 1.25 4 mediterraneus of the Western Mediterranean (Bo et al., 2011; Grinyó et al., 2016). In Alcyonium coralloides 0.2363 0.001 0.44 ± 1.46 10 fact, P. clavata, has been described to occur at lower densities in shelf Soft bottom environments (Grinyó et al., 2016). Contrary, prior observations of Alcyonium palmatum 0.3918 0.001 1.15 ± 0.93 6 P. macrospina on the Balearic Islands or in the Tyrrhenian Sea, revealed Veretillum cynomorium 0.2890 0.001 0.78 ± 0.50 3 large densities of this species monopolising wide extensions, in contrast Lytocarpia myriophyllum 0.1385 0.001 1.78 ± 2.31 15 with the modest P. macrospina densities found in this study. Further­ more, the importance of A. mediterraneusin this assemblage (Table 1, commonly reported in soft sediment shelve environments of the western Fig. 4D) agrees with Biel-Cabanelas et al., 2023, who already reported and central Mediterranean (De Juan et al., 2013; Dominguez-Carrió that this ophiuroid occurs at unusual high densities in inner-shelf rocky et al., 2022; Petović et al., 2021). environments in the study area. These species are particularly important in soft sediment habitats as they provide three-dimensional structure in an otherwise homogeneous 4.1.3. Coralligenous assemblage environment increasing local diversity and biomass (Bastari et al., 2018; All of the species found in coralligenous concretions are common Di Camillo et al., 2013), as suggested by the higher species richness and components of coralligenous assemblages in Western Mediterranean densities of associated species found in sampling units hosting these environments (Ballesteros, 2006). The most abundant species found in species. this assemblage, i. e. E. singularis and P. clavata (Fig. 4eE and F) repre­ Additionally, these species’ densities (Table 1) were higher than in senting respectively 39% and 16% of all observed organism, in agree­ previous studies conducted in outer shelf environments (>80 m depth) ment with previous observations on the Western Mediterranean (Gori Table 2 Demographic parameters (minimum, average and maximum height) of the main gorgonian species occurring on the evaluated fishing grounds. All values are given in cm; average values include standard deviation. Mean values per fishing ground were calculated using only the transects where the species were recorded. Populations with an asterisk ‘*’ indicates a gorgonian abundance below 30 individuals, considered to be the minimal threshold for properly estimating gorgonian demography (Linares et al., 2008; Gori et al., 2011). Fishing Ground E. singularis E. cavolini P. clavata Transect Depth (m) Min. Avg. Max. Min. Avg. Max. Min. Avg. Max. A. Farallons 1 66–74 – – – 8 18.5 ± 11.4* 44.5 – – – 2 40–60 3.1 24 ± 15.8 71 4.5 31.6 ± 13.1* 52 25.8 44.4 ± 11.8* 57 3 20–40 7 26.3 ± 15 79.1 – – – 22 40.4 ± 13.31* 56.8 4 25–65 11.3 26.8 ± 10.6 47.3 5.1 21.7 ± 8.05 40.9 15.1 24.9 ± 12.32* 40.7 9 40–60 – – – 5.6 27.4 ± 12.2 58.7 – – – 10 10–50 8.7 27 ± 11.6 62.6 – – – 14.1 45.5 ± 22.8* 81.6 11 50–60 – – – 4.2 26.8 ± 17.17 87.9 – – – Mean 10–74 3.1 25.9 ± 13.6 79.1 4.2 26 ± 13.1 87.9 14.1 41.2 ± 13.9 81.6 B. Illa Portaló 5 70–80 – – – 14 28.3 ± 11 75.5 – – – 6 65–80 – – – 4.8 26.1 ± 10.2 55.4 – – – 7 65–75 – – – 5 25 ± 10.8 76.7 – – – 8 65–75 4.6 24.7 ± 12.1 64.4 6.2 23.9 ± 9.7 53.7 6.2 67.9 ± 29.1* 113 15 45–60 – – – – – – – – – 16 35–45 4.1 23.9 ± 14.2 91 6.2 23.9 ± 9.7 53.7 10 49.2 ± 25.4 117.9 17 15–45 4.6 27 ± 14 72.8 4.6 26.2 ± 13.9 72.8 15.5 66.7 ± 37.6* 124.3 Mean 15–80 4.1 24.5 ± 13.6 91 4.6 25.8 ± 10.4 76.7 6.2 57.2 ± 29 124.3 C. Maça d’Oros 12 55–70 – – – 4.8 22 ± 10.2 58.7 – – – 13 55–60 5.5 19.6 ± 9.5 59.6 – – – – – – 14 35–55 – – – 7 24.1 ± 10.1 66.8 17.5 34.6 ± 12.4* 56 18 60–75 5.2 24.1 ± 12.2 59.4 – – – – – – Mean 35–75 5.2 21.9 ± 11.2 59.6 22.6 ± 10.2 34.6 ± 12.4* 6 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 Fig. 3. Percentage composition of marine litter found on the sea bottom in each fishing ground. Table 3 Summary table including the density of anthropogenic items (fishing gears, human debris, etc.) and proxies for gorgonian population health (percentage of dead, necrosed and colonies with epiphytes within a population) observed during the ROV video analysis for each transect and each fishing ground. Numbers in brackets indicate the abundance of anthropogenic items, dead necrosed and colonies with epiphytes per transect. Transect Depth (m) Anthropogenic items (Nº/m2) Dead colonies (%) Necrosed colonies (%) Colonies with epiphytes (%) A. Farallons 1 66–74 0.013 (1) 1.7 (1) 0 (0) 0 (0) 2 40–60 0.000 (0) 1.3 (6) 0.7 (3) 6.9 (31) 3 20–40 0.042 (4) 0.4 (2) 1.3 (6) 11.2 (50) 4 25–65 0.026 (9) 1.6 (6) 1.3 (5) 18.6 (70) 9 40–60 0.045 (8) 4.6 (58) 1.3 (16) 16.7 (201) 10 10–50 0.089 (4) 7.1 (19) 1.6 (4) 18.6 (46) 11 50–60 0.000 (0) 7.9 (25) 1.4 (4) 25.2 (73) Mean 10–74 0.027 (26) 3.67 (117) 1.2 (38) 15.3 (471) B. Illa Portaló 5 70–80 0.077 (4) 2.6 (4) 0 (0) 12.6 (19) 6 65–80 0.134 (7) 3.8 (26) 3.2 (21) 14.3 (95) 7 65–75 0.018 (2) 4.3 (27) 2.7 (16) 14.7 (88) 8 65–75 0.004 (1) 15.8 (59) 4.8 (15) 25.5 (80) 15 45–60 0.014 (3) 3.4 (24) 0.7 (5) 20.8 (144) 16 35–45 0.117 (11) 3.3 (32) 1.5 (14) 12.2 (114) 17 15–45 0.000 (0) 1.5 (7) 0.6 (3) 14.6 (68) Mean 15–80 0.031 (28) 4.47 (179) 1.9 (74) 15.9 (608) C. Maça d’Oros 12 55–70 0.024 (6) 8.2 (96) 0.5 (5) 15.3 (165) 13 55–60 0.059 (8) 14.1 (237) 0.3 (4) 22.3 (322) 14 35–55 0.090 (15) 5.3 (67) 0.8 (9) 12.4 (149) 18 60–75 0.085 (12) 8.4 (46) 3.6 (18) 13.0 (65) Mean 35–75 0.059 (41) 9.55 (446) 0.852 (36) 16.6 (701) densities were lower than those previously reported along Cap de Creus Table 4 (Gori et al., 2011; Ambroso et al., 2013; Coppari et al., 2016). It is un­ Main epiphyte species on gorgonian colonies in each fishing ground. A colony clear if these lower densities respond to local variability, fishing pressure may have more than one species of epibiont. Abbreviated species are Alcyonium coralloides (A. coralloides) and Filograna implexa (F. implexa) or derive from mass mortality events that have been occurring over the past decade in the study area (Garrabou et al., 2022). A. coralloides % Bryozoa % F. implexa % Pentapora sp. % A. Farallons 16,6 22,5 12,3 25,9 B. Illa Portaló 24,0 15,0 5,1 16,0 4.2. Impact assessment C. Maça d’Oros 70,3 10,8 6,6 14,1 4.2.1. Gorgonian size structure Three key ecosystem engineers – E. singularis, E. cavolini, and P. et al., 2011; Grinyó et al., 2016). Mostly, E. singularis occurred on sloping clavata – were described. Despite playing a crucial role in marine benthic grounds (55% of colonies) and P. clavata on horizontal (51% of colonies) ecosystems and offering refuge to a wide variety of other species, ones. This stands in contrast to earlier research on other coralligenous member species of the order Malacalcyonacea (McFadden et al., 2022) grounds, which mostly linked P. clavata to vertical grounds and have also been identified as the species most negatively impacted by E. singularis to horizontal ones (Gori et al., 2011; Grinyó et al., 2016). It artisanal fisheries (Dias et al., 2020). is likely that this unusual pattern reflects small scale variability in the A previous study on E. cavolini at various sites of the Mediterranean area. Furthermore, E. singularis, P. clavata, A. palmatum and A. polypoides Sea pointed to higher densities but also smaller colonies (Sini et al., 7 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 Fig. 4. Most contributing species to the assemblages. (A) Alcyonium palmatum, (B) Veretillum cynomorium, (C) Eunicella cavolini, (D) Astrospartus mediterraneus, (E) Paramuricea clavata, and (F) Eunicella singularis. Images from the ROV video recordings. 2015). This can be due to higher environmental instability (e.g. hydro­ than P. clavata, which had no prevalence for any size-class (Linares et al., dynamism, food supply, temperature, light exposure), typical from 2008). Some studies suggest that the prevalence of small colonies could shallower waters (<40 m). Contrary, our colonies were found beyond be associated with impacted populations due to fishing activities 37.5 m. Nonetheless, our data agrees with the conclusion of Sini and (Althaus et al., 2009; Grinyó et al., 2016). In the study area, it was collaborators, in which density is overall inversely related to height, observed that size class 2 (10–20 cm) prevailed among E. singularis supporting the idea that recruitment is driven by intra-specific compe­ populations, while size class 3 (20–30 cm) was predominant in tition mechanisms, where the lack of large colonies enhances recruit­ E. cavolini populations. This stands in contrast to E. singularis populations ment success (Sini et al., 2015). If we compare our data to the nearby found in shallower waters within the same area, where size class 1 Balearic Islands (Grinyó et al., 2016), it seems that Cap de Creus is able (0–10 cm) dominated (Linares et al., 2008). to sustain higher densities and considerably bigger colonies. This could be attributed to the fact that in the Balearic Islands this species mostly 4.2.2. Impact on benthic assemblages occurred alongside other anthozoans (Grinyó et al., 2016, 2018), thus The dominance of fishing lines among the marine debris found in having to compete for substrate, whereas in the study area this species most fishing locations (see Fig. 3) is consistent with those of a prior mostly occurred forming monospecific aggregations. investigation in adjacent areas (Dominguez-Carrió et al., 2020) and with The same happened with E. singularis in the study area compared to research developed in the Tyrrhenian Sea (Angiolillo et al., 2015). denser populations but also smaller colonies than in the Menorca Nevertheless, other areas with similar artisanal fishing tradition appear Channel (Grinyó et al., 2016). However, most E. singularis colonies in the to be more impacted, such as the “Maledetti Shoal” in the Ligurian Sea, Menorca Channel grew on maërl whereas in the study area they mainly with a density of marine debris 10 times a higher than the present study grew on rock. It is likely that substrate stability may reinforce the (Enrichetti et al., 2019). For instance, the study conducted in the development of denser E. singularis populations. Additionally, unlike the “Maledetti Shoal”, revealed that, on average, 40% of the structuring Balearic Archipelago, the study area is under the influence of anthozoans showed signs of impact, such as necrotic portions, over­ nutrient-rich waters derived from river runoff in the gulf of Lions, growth of epibiotic organisms, and direct entanglements of colonies by creating suitable conditions for gorgonian-dominated assemblages to fishing gears (Enrichetti et al., 2019). Another case study in Portofino fully develop (Gori et al., 2017). In fact, in shallower waters around Cap MPA (NW Mediterranean Sea) reported that 53% of the colonies of de Creus (13–27 m), the colonies of E. singularis are smaller but grow in P. clavata and 36% of the colonies of E. cavolini showed traces of impact denser populations (Linares et al., 2008). Moreover, it has been (Betti et al., 2020). In contrast, the predominant use of trammel nets demonstrated the preference of the larvae of E. singularis to seek for a with lower lengths and pots by fishers in the study area accounts for lighter place to settle (Weinberg, 1979b), which could lead to igher benthic ecosystems associated with lower damage (Baena et al., 2022). recruitment rates and densities in lower depths. In European seas, around 30% of all marine litter that accumulates On the contrary, P. clavata colonies were found in less dense pop­ on shelf, slope and canyon habitats can be attributed to abandoned, lost, ulations but higher heights compared to other studies in the same area in or discarded fishing gear (ALDFG; Pham et al., 2014). This percentage shallower waters (25–30 m, Maça d’Oros) (Linares et al., 2008). This can reach 50–90% in traditional fishing grounds as seen in the present differences of height and densities in Cap de Creus can be due to the study or in other areas, such as Campania, Sicily or Liguria (Angiolillo existence of a carrying capacity (maximum population size of a species et al., 2015; Consoli et al., 2018; Enrichetti et al., 2020). that can be sustained in a specific environment) (Linares et al., 2008) but Present results of epibiosis rates on gorgonian populations match also to the ecological preference of low light conditions of P. clavata with a previous study conducted near the study area, in Medes Islands (Ballesteros, 2006). (South from Cap de Creus) which indicated that between 10% and 33% Population size structures of E. singularis and E. cavolini were mostly of the colonies in unprotected populations were partially colonised by asymmetrical and positively skewed suggesting higher recruitment rates epibionts, most likely resulting from tissue injury (Tsounis et al., 2012). 8 A. Higueruelo et al. Marine Environmental Research 192 (2023) 106211 On the contrary, only between 4% and 10% of the populations in a areas previously studied in the Mediterranean under fishing and other Marine Protected Area were affected (Tsounis et al., 2012), suggesting anthropogenic pressures. Even though the presence of high individuals that fishing activities or other disturbances of anthropogenic origin is an indicator of hope we should remember that marine sessile benthic contribute to the damage and consequent epibiosis of the gorgonian species are highly vulnerable to all anthropogenic pressures and should colonies (Bavestrello et al., 1997; Tsounis et al., 2012). not be underestimated. A better understanding of recreational fisheries In this regard, the proportion of colonies with Alcyonium coralloides in coexistence with other activities that could harm and threaten the as epiphytes in Maça d’Oros was three and four times higher than in the marine benthic ecosystems are essential, as well as better management other fishing grounds (Table 4). This octocoral epibiont is likely to grow measures and new ways to mitigate the existing impacts. on the apical axis of injured or dead gorgonian colonies (Quintanilla et al., 2013; Weinberg, 1979a) so in high proportions it could be an Funding indicator of an impacted ecosystem. Maça d’Oros fishing ground is an area of confluence for artisanal vessels from different fishermen’s guilds This work was performed under the MitiCap and ResCap projects, (Gómez and Riera Aragó, 2007) in accordance with the greater presence which are funded by the Fundación Biodiversidad [Biodiversity Foun­ of ALDG, and therefore it could be subjected to a harder anthropogenic dation] of the Ministerio para la Transición Ecológica [Spanish Ministry pressure. This could result in more impacted populations, as suggested for Ecological Transition], through the Pleamar Program, co-funded by by the significantly smaller colonies and the higher proportions of dead the European Maritime and Fisheries Fund. In addition, the authors colonies and colonies with epibionts. affiliated to the Institut de Ciències del Mar [Institute of Marine Sci­ Overall, the results of the present study reaffirm the vulnerability ences] had the institutional support of the “Severo Ochoa Centre of and the high degree of exposure to fishing impacts that gorgonian spe­ Excellence” accreditation (CEX 2019-000928-S). cies specially, but also other structural sessile marine benthic organisms, face. Moreover, species that rely on structural benthic organisms Sample CRediT author statement providing them habitat and resources can be indirectly affected by the loss of live corals (Lokrantz et al., 2010; Bonin et al., 2011). In fact, some Andrea Higueruelo: Conceptualization, Investigation, data acquisi­ studies observed a decline of coral specialized fish species, changes in tion, data curation, formal analysis, Writing - original draft, Writing - the feeding behaviour or direct impacts by the ingestion or entangle­ review & editing, Andreu Santín: Investigation, conceptualization, ment of ALDG on different species in degradated habitats (Alvarez-Filip methodology, data acquisition, data curation, supervision, Writing - et al., 2015; Beneli et al., 2020; Link et al., 2019); highlighting its review & editing, Janire Salazar: Writing - Review & Editing, Stefano importance. Ambroso: Writing - Review & Editing, Anna Soler-Membrives: Investi­ The fishing impacts and affections (rates of epibiosis and necrosis) in gation, conceptualization, methodology, data acquisition, data curation, gorgonians detected in our study are lower compared to previous studies supervision, Writing - review & editing, Jordi Gruinyó: Funding acqui­ in other Mediterranean areas. Also, the presence of large sizes of sition, project administration, conceptualization, methodology, data gorgonian species is an indicator of good preservation. Different reasons acquisition, supervision, writing-review & editing. could explain the lower impact in the study area versus other areas previously studied, but mainly, fishers reported among their habits to Declaration of competing interest frequently change the draft area and do not usually fish during the winter, so the impact may also be reduced. To fully comprehend the The authors declare the following financial interests/personal re­ conservation status of the studied area and its link to anthropogenic lationships which may be considered as potential competing interests: disturbances, additional research and a more complete and continuous Jordi Grinyo reports financial support was provided by Biodiversity on-time dataset is needed. Also, due to the higher number of impacts Foundation. found in other Mediterranean fishing grounds with different fishing habits, we insist as has been done by previous authors (e.g., Tsounis Data availability et al., 2012; Giovos et al., 2018; Gómez et al., 2021) on the importance of better reporting the characteristics of recreational activities con­ Data will be made available on request. ducted in the area to better assess the possible impacts of fishing ac­ tivities and set adequate conservation and mitigation measures in Acknowledgements accordance with the other stakeholders of maritime activities (Lloret et al., 2008; Gómez et al., 2021). Collaborative efforts with experienced The authors would like to thank the crew of the R/V “Atlantic Ex­ local fishers and scuba divers, who possess extensive knowledge of the plorer”, the artisanal fishers from Port de la Selva, Port Lligat and benthic communities, could enhance the recovery of ALDG. Simulta­ Cadaqués and Cap de Creus Natural Park for their aid. Authors would neously, collaboration with fishers would contribute to raising aware­ like to thank Dr. Andrea Gori, Dr. Núria Viladrich, Dr Enrique Isla, Dr. ness about the potential impacts their activities might have on benthic Ana Sabates and Prof. Josep-Maria Gili for their support during the ecosystems and, consequently, on the catches they are interested in Miticap I project. (Dominguez-Carrió et al., 2020; Santín et al., 2022a, 2022b). Nevertheless, it is important not to drop our guard too far and remember the high vulnerability of those ecosystems and so, continue Appendix A. Supplementary data monitoring fishing activities and progressively introduce measures to mitigate their impacts. Supplementary data to this article can be found online at https://doi. org/10.1016/j.marenvres.2023.106211. 5. 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