Introduction
Habitat-forming species (HFS) play a crucial role in shaping communities by creating stable conditions for other species and influencing the processes within those ecosystems (Dayton, Reference Dayton1972; Stachowicz, Reference Stachowicz2001; Crain and Bertness, Reference Crain and Bertness2006). Therefore, they are of great environmental importance due to their contribution in maintaining biodiversity and ecosystem function (Bulleri et al., Reference Bulleri, Eriksson, Queirós, Airoldi, Arenas, Arvanitidis, Bouma, Crowe, Davoult, Guizien, Iveša, Jenkins, Michalet, Olabarria, Procaccini, Serrão, Wahl and Benedetti-Cecchi2018). The loss of these species can have a dramatic effect on natural habitats with consequences on associated biota, ecosystem function and stability (Ellison et al., Reference Ellison, Bank, Clinton, Colburn, Elliott, Ford, Foster, Kloeppel, Knoepp, Lovett, Mohan, Orwig, Rodenhouse N, Sobczak, Stinson, Stone, Swan, Thompson, Von Holle and Webster2005).
Cold-water corals (CWC) are considered HFS because they exhibit complex branching morphology and sufficient size to provide substrate and/or shelter for other species (Freiwald and Roberts, Reference Freiwald and Roberts2005). Indeed, coral systems have a wide ecological relevance, given the large number of interactions that occur in them (Díaz et al., Reference Díaz, Díaz-Pulido, Garzón-Ferreira, Geister, Sánchez and Zea1996). CWC play an important structural and functional role (Wildish and Kristmanson, Reference Wildish and Kristmanson1997), as they are engineers of deep-water ecosystems (Jones et al., Reference Jones, Lawton and Shachak1994) and are found in all oceans (Freiwald et al., Reference Freiwald, Fossa, Grehan, Koslow and Roberts2004). In addition, organisms provide structurally complex that allows for greater diversity than in areas where they are not found (Buhl-Mortensen et al., Reference Buhl-Mortensen, Vanreusel, Gooday, Levin, Priede, Buhl-Mortensen, Gheerardyn, King and Raes2010).
The distribution and abundance of CWC in the marine benthos is the result of evolutionary processes, environmental conditions, the extent of the ecological niche of each species and the dynamics of each coral population, which, in turn, are determined by the ecological relationships between the species that coexist in that environment (Brown, Reference Brown1995; Lo Iacono et al., Reference Lo Iacono, Savini, Huvenne and Gràcia2019). These parameters are defined by the specific bathymetric range in which each group of organisms is distributed, which in turn depends on the geomorphology of the location (Chimienti et al., Reference Chimienti, Bo, Taviani and Mastrototaro2019).
Several CWC species have inhabited the Mediterranean Sea since the Miocene epoch, experienced significant changes over time (Altuna and Poliseno, Reference Altuna, Poliseno, Orejas and Jiménez2019). Seabed complexity, determined by the physical and chemical properties of the water column, is an important factor contributing to the distribution and development of CWC communities in this Sea (Hayes et al., Reference Hayes, Schroeder, Poulain, Testor, Mortier, Bosse, du Madron, Orejas and Jimenez2019). However, few studies provide a spatial context for CWC habitats in the Mediterranean and more data from less explored areas are needed to better define their overall regional distribution and relate them to environmental factors (Lo Iacono et al., Reference Lo Iacono, Savini, Huvenne and Gràcia2019). In some parts of the Mediterranean and adjacent areas (e.g. Strait of Gibraltar, Gulf of Cadiz) the CWC-associated fauna is not well known (Lastras et al., Reference Lastras, Sanchez-Vidal and Canals2019). As a consequence, the lack of knowledge about the ecology of these species undermines conservation efforts (Enrichetti et al., Reference Enrichetti, Toma, Bavestrello, Betti, Giusti, Canese, Moccia, Quarta, Calcagnile, Andaloro, Greco and Bo2023).
Dendrophyllia ramea (Linnaeus 1758), is an anthozoan of the order Scleractinia, belonging to the family Dendrophylliidae. This species is distributed in most of the Mediterranean Sea and in the Atlantic Ocean (Zibrowius, Reference Zibrowius1980). The presence of D. ramea has been recorded mainly in the Western Mediterranean basin, on the Italian coasts from the Sea of Sicily (Salvati et al., Reference Salvati, Giusti, Canese, Esposito, Romeo, Andaloro, Bo and Tunesi2021; Angiolillo et al., Reference Angiolillo, Giusti, Rossi and Tunesi2022) to the Gulf of Naples (Zibrowius, Reference Zibrowius1980), on the Catalan coasts of the Balearic Sea (Sánchez et al., Reference Sánchez, Demestre and Martın2004) and the Gulf of León (Zibrowius, Reference Zibrowius1980); as well as in the Alborán Sea (Zibrowius, Reference Zibrowius1980; Ocaña et al., Reference Ocaña, Tocino and González2000; Cebrián and Ballesteros, Reference Cebrián and Ballesteros2004). Recently, this species was found attached to soft sediments (Salomidi et al., Reference Salomidi, Zibrowius, Issaris and Milionis2010; Orejas et al., Reference Orejas, Gori, Jiménez, Rivera, Lo Iacono, Hadjioannou, Andreou and Petrou2017), though usually D. ramea in the Mediterranean was considered to be associated with rocky substrates. This suggests that its distribution could be wider than considered so far. In the Atlantic Ocean, it is present in Portugal (Zibrowius, Reference Zibrowius1980), on the Atlantic coast of Morocco (Patriti, Reference Patriti1970; Zibrowius, Reference Zibrowius1981), the Canary Islands (Brito and Ocaña, Reference Brito and Ocaña2004), Western Sahara, Senegal (Chevalier, Reference Chevalier1966), the Azores, Cape Verde, Ghana, the Gulf of Guinea and Nigeria (Zibrowius, Reference Zibrowius1980).
Additionally, D. ramea has been classified as ‘Vulnerable’ in the Red List of Threatened Species of the Mediterranean by the International Union for Conservation of Nature (IUCN) and has also been included in the list of endangered or threatened species in Annex II of the Mediterranean Action Plan (MAP) of the Barcelona Convention. Because of its scarcity and deep bathymetric distribution, this coral is listed as ‘Vulnerable’ to extinction by the Red Data Book of Invertebrates in Andalusia, which is included in Appendix II of the CITES Convention. However, it is not included in the National Catalogue of Endangered Species because there is no scientific basis on the status of its populations to justify the necessity of protection. This fact highlights the urgent importance of carrying out this type of study to characterise its populations.
The Special Conservation Zone of Seabeds and Cliffs of Punta de la Mona is an area located in La Herradura (Granada, Spain), where the presence of cliffs and seabed form a favourable habitat for the growth of D. ramea (Cebrián and Ballesteros, Reference Cebrián and Ballesteros2004) and it constitutes one of the westernmost points of distribution for this species in the Mediterranean Sea (Salvati et al., Reference Salvati, Giusti, Canese, Esposito, Romeo, Andaloro, Bo and Tunesi2021). The coverage of these corals hosts a high biodiversity (Longo et al., Reference Longo, Mastrototaro and Corriero2005; Mastrototaro et al., Reference Mastrototaro, D'Onghia, Corriero, Matarrese, Maiorano, Panetta, Gherardi, Longo, Rosso, Sciuto, Sanfilippo, Gravili, Boero, Taviani and Tursi2010), providing shelter for other species, as well as suitable substrate for the recruitment and adults settlement of associated species (Baillon et al., Reference Baillon, Hamel, Wareham and Mercier2012; Rueda et al., Reference Rueda, Urra, Aguilar, Angeletti, Bo, García-Ruiz, Taviani, Orejas and Jiménez2019). Therefore, the environmental and biological complexity provided by D. ramea is fundamental for the development of a hotspot. From this, it is inferred that the study of the structure and distribution of this assemblage is of utmost importance to develop assertive management and conservation plans. However, in the Alboran Sea, the species associated with CWC are still not well characterised (Rueda et al., Reference Rueda, Urra, Aguilar, Angeletti, Bo, García-Ruiz, Taviani, Orejas and Jiménez2019).
Due to this, it is important to understand what role D. ramea plays in the ecosystem, its bathymetric distribution and density patterns. Additionally, the size ranges could provide information on the abundance of juveniles or adults, which, if studied at different depths, would help to infer the colonisation processes that this species undergoes (Guzmán and Guevara, Reference Guzmán and Guevara1998). Although this cnidarian is a dominant species in the study area below depths of 20 m (Cebrián and Ballesteros, Reference Cebrián and Ballesteros2004), the distribution patterns of this assemblage and the size structure are not yet well described in this area.
For several years now, anthropogenic pressure on a global scale has been causing the deterioration of CWC habitats and, as a consequence, the decline of entire biological communities (Haapkylä et al., Reference Haapkylä, Ramade and Salvat2007; Hoegh-Guldberg, Reference Hoegh-Guldberg2011; Eakin et al., Reference Eakin, Sweatman and Brainard2019). The environments inhabited by D. ramea harbour high biodiversity and biomass, so fishing pressure is significantly higher compared to adjacent areas (Buhl-Mortensen et al., Reference Buhl-Mortensen, Vanreusel, Gooday, Levin, Priede, Buhl-Mortensen, Gheerardyn, King and Raes2010). Trawling particularly affects these populations, both in their size structure, age composition, abundance and structural complexity (Clark and Koslow, Reference Clark, Koslow, Pitcher, Morato, Hart, Clark, Haggan and Santos2007).
Due to the current lack of information on this species (Salvati et al., Reference Salvati, Giusti, Canese, Esposito, Romeo, Andaloro, Bo and Tunesi2021) and its importance for marine biodiversity locally and regionally, the aims of this study were: (1) to survey the bathymetric distribution, abundance and size ranges of the coral species D. ramea in the coast of Granada; (2) to study the non-epibiotic communities (hereafter, macro-benthonic communities) associated with this HFS; (3) to assess the epibionts on D. ramea; (4) to evaluate the marine litter and possible threats to the D. ramea assemblage; and (5) to provide information to help in the development of an appropriate management and conservation plan.
Materials and Methods
Study area
The study area was the Special Conservation Zone of Seabeds and Cliffs of Punta de la Mona (PM hereafter), on the Northern coast of the Alboran Sea (Figure 1). In terms of its ecosystem importance, this place was catalogued among the ‘Zonas Especiales de Conservación con Hábitats Marinos del Litoral Andaluz’ (Special Conservation Zones with Marine Habitats on the Andalusian Coast), a Marine Protected Figure recognised by the Spanish government, and has been included in the ‘Red Natura’, classified as a site of community interest.
Figure 1. Study area: (A) Mediterranean Sea; (B) northern coast of the Alboran Sea; (C) bathymetry of the seabed at Punta de la Mona showing the locations of the video transects and epibiont sampling sites.
Dendrophyllia ramea assemblage description
The seabed of Punta de la Mona hosts a wide variety of habitats. In the deeper regions, a reef dominates the landscape, extending through three southeast-oriented underwater canyons with vertical limestone walls. These walls descend to a soft sandy substrate at depths reaching −48 m. The rocky substrate is continuous throughout the area, but marine currents and upwellings resuspend the soft substrate in the deep zone, creating small, mobile sandbanks on the canyon floors.
In the study area, a survey was carried out by SCUBA diving rebreather and videos. Video transects, 50 m long and 1.5 m wide, were performed at a constant speed, 1 m above the seabed parallel to the coastline, every 6 m in depth from 30 to 48 m. Three random video transects were recorded per depth (see Figure 1). The survey took place in April 2021. To estimate the abundance, size and distribution of D. ramea in the study area, the number of colonies and branches were counted, as well as the coverage of each colony by analysing the images obtained from the videos with ImageJ software (version 1.4.3.67). For the scale reference, a special system was designed with a scooter support, consisting of two lasers pointing at a known distance of 1.5 m.
To study the D. ramea assemblage, the number of colonies and branches per transect were analysed using a generalised-linear model (GLM). The cover of colonies per transect was analysed using a linear model analysis (LM). These variables were considered a response variable and ‘Depth’ was a fixed factor with four levels: 30, 36, 42 and 48 m.
Macro-benthic communities
Visual identification of the macro-species associated with the D. ramea reef was determined from the sampling videos (see Figure 1). To study the composition, structure, and diversity of these benthic communities at each depth, the abundance of the individuals was estimated by frequency of occurrence (Bianchi et al., Reference Bianchi, Pronzato, Cattaneo-Vietti, Benedetti-Cecchi, Morri, Pansini, Chemello, Milazzo, Fraschetti, Terlizzi, Peirano, Salvati, Benzoni, Calcinai, Cerrano, Bavestrello, Gambi and Dappiano2004).
The number of species of the macro-benthic community per transect was analysed using GLM. To study the multivariate structure of the community of macro-benthic organisms associated to D. ramea reef, a Permuted Multivariate Analysis of Variance (PERMANOVA) (Anderson, Reference Anderson2001; McArdle and Anderson, Reference McArdle and Anderson2001) was used, where the data were organised into species/abundance matrices, considering the experimental design previously explained. Abundance values were square-root transformed to prevent highly abundant species from overly influencing the analyses and causing the contribution of less abundant species to be insignificant (Clarke and Warwick, Reference Clarke and Warwick2001). To determine the percentage contribution of each taxon or species to the similarity measures within the ‘Depth’ factor levels, the SIMPER (Similarity Percentage; Clarke, Reference Clarke1993) similarity partitioning analysis was used. The homogeneity of variances was also tested with the PERMDISP test (Anderson, Reference Anderson2006).
Epibiont community
Epibiont samples were taken using a scraping technique, where a scalpel blade was arranged perpendicular to the surface of the coral, so as not to damage its living tissue and, with a sample bottle, the mass of epibiont dragged in each scraping was collected. It's important to note that mobile species might have had the chance to escape during this process. Due to the time needed to sample epibionts without damaging the D. ramea colonies and the difficulty of diving deeper than 40 m, the number of transects were reduced. The depths for sampling were selected to be intermediate to those of the video transects (see Figure 1). Eight samples were collected along each three 100 m long transects at three different depths: 34, 40, and 45 m (making a total of 24 samples). The samples were fixed in 96% ethanol and subsequently analysed in the laboratory under binocular magnification and optical microscopy. Organisms were identified to the highest possible taxonomic resolution, in most cases to the species level.
The number of species of epibionts per depth was analysed using GLM and the multivariate structure of the epibiont community was tested using PERMANOVA. In this case, the experimental design considered the presence/absence of organisms at ‘Depth’ with three levels (34, 40, and 45 m). The homogeneity of variances was also tested with the PERMDISP analysis.
Threats to the integrity of the CWC habitat: marine litter on the seafloor
In addition, the recognition and description of the types of litter according to each category, according to Fleet et al., Reference Fleet, Vlachogianni and Hanke2021, and the debris coverage present in the area, were used to estimate the anthropogenic impact suffered by these communities of organisms. The litter was classified on Rubber, Glass/Ceramic, Cloth/Textile, Artificial Plastic Polymers (predominantly originating from fishing activities) and Metals, considering five main categories of materials (Fleet et al., Reference Fleet, Vlachogianni and Hanke2021). The litter coverage per transect was analysed using LM and considering two fixed factors: ‘Depth’ with four levels (30, 36, 42, and 48 m) and ‘Type of litter’ with five levels (the categories previously named). The normality and homogeneity of the residuals were checked with a Shapiro–Wilk and Bartlett's tests, respectively. The coverage of each of these categories was plotted in a bar chart separated by depth.
Univariate analyses (LM and GLM) were carried out with the R software version v4.1.1 (CoreTeam R, 2021). To make the graphs, the ‘ggplot2’ package (Wickham, Reference Wickham2016) was used. All multivariate analyses were carried out with PRIMER-E v6.1.11 and PERMANOVA+ v1.0.1 software (Clarke and Gorley, Reference Clarke and Gorley2006).
Results
D. ramea assemblage at PM
In the study area, a total of 311 colonies of D. ramea were identified and distributed as follows: 25 colonies at a depth of 30 m, 178 at a depth of 36 m, 93 at 42 m, and 15 colonies at a depth of 48 m. The mean number of colonies per transect showed the existence of two groups of depths: one formed by the intermediate (36 and 42 m) depths and the other formed by the extreme depths (30 and 48 m), which showed significant differences between them (Table 1). Colonies exhibit variable coverage, ranging from 2300 cm2 to some individuals of only 3 cm2, consisting of a single polyp. There was a greater number of individuals with smaller coverage than with larger coverage, a pattern that is followed throughout the depth gradient studied (Figure 2A). In addition, coral abundance at 36 and 42 m was higher than the remaining depths, which is consistent with the zone with the greater number of colonies. However, these differences were not statistically significant. Furthermore, it can be observed that the colonies contain a lower number of branches at 30 and 48 m (Figure 2B), although the differences between depths were also not significant.
Table 1. Generalised Linear Model for the mean number of Dendrophyllia ramea colonies per depth (m).
SE, standard errors.
For the categorical variable ‘Depth’, 30 m was used as reference level.
a Significant differences at P < 0.05.
Figure 2. Dendrophyllia ramea assemblage in Punta de la Mona: (A) coverage values (cm2); (B) number of branches per depth (m).
Macro-benthic community
A total of 47 species belonging to 9 taxonomic groups were identified in the study area, which characterised the organisms associated to D. ramea reef (Table S1). According to the nMDS graph, there is a transition in this benthic community with a zonation pattern as a function of depth gradient. The composition and abundance of species associated with the coral assemblage at 48 m deep is clearly different from the other depths (Figure 3) and follows a gradient determined by the bottom depth. The multivariate PERMANOVA analysis showed that there are significant differences in the composition and abundance of the species at the analysed depths [Pseudo-F 3 = 6.30; P(perm) = 0.001].
Figure 3. nMDS representing the differences in the community of macro-benthic organisms associated with Dendrophyllia ramea per depth (m). Stress = 0.05.
The a posteriori PERMANOVA analysis showed the existence of three groups: one composed of the depths of 30 and 36 m together, another with a depth of 42 m and the last group with a depth of 48 m (Table 2). No dispersion problems were found in the study [PERMDISP: F 3 = 2.97; P(perm) = 0.1].
Table 2. A posteriori pair-wise permutation multivariate analysis of the variance comparison for the different levels of the factor ‘Depth’ for macro-benthic organisms associated with Dendrophyllia ramea.
From the SIMPER analysis, it was found that 17 species are the ones that contribute the most to the differences found between depth groups, with 13 of them corresponding to the group of 30 and 36 m, 14 to 42 m, and 10 to 48 m (Table S2). Among these species, those that were common at all depth groups with similar abundances were: the gorgonia Eunicella verrucosa (Pallas, 1766), the porifera Aplysina aerophoba (Nardo, 1833), Crambe crambe (Schmidt, 1862), and Timea sp. The most abundant species that characterised the depth groups of 30 and 36 m were: the algae Mesophyllum alternans (Foslie), Cabioch and M. L., Mendoza, 1998 or the bryozoans Myriapora truncata (Pallas, 1766) and Pentapora fascialis (Pallas, 1766); at 42 m: Axinella damicornis (Esper, 1794) or Parazoanthus axinellae (Schmidt, 1862); and at the 48 m level: the sponges Cliona viridis (Schmidt, 1862) or Haliclona (Reniera) mediterranea Griessinger, 1971.
When analysing the variation in the number of species that make up the community macro-benthic organisms the number of species did not differ significantly between the different depth groups. In any case, it can be observed that the number of species is lower at 48 m with respect to the other depth groups. However, the depths of 30 and 36 m showed similar values of diversity, the 42 depth showed the higher number of species and the 48 m depth the lower values of diversity (Figure 4).
Figure 4. Number of species associated with Dendrophyllia ramea reef per depth (m).
Epibiont community
A total of 88 epibiont taxa associated with D. ramea, belonging to 12 different taxonomic groups, were identified (Table S1). The nMDS graphical representation shows that the composition of the epibiont community varies according to the depth gradient. It seems that the species composition corresponding to the extreme depths are different from each other, while at the intermediate zone the communities are in a transitional position, with no differences in the other two depths (Figure 5). The PERMANOVA analysis showed that there are significant differences in the composition of the species of epibiont at the analysed depths [Pseudo-F 2 = 1.72; P(perm) = 0.017]. The a posteriori analysis confirmed that there are differences in the composition of this community in the shallowest zone (34 m) in relation to the deep zone (45 m), while the intermediate depth (40 m) showed no difference to the previous ones (Table 3). No dispersion problems were noted in the study [PERMDISP: F 2 = 1.64; P(perm) = 0.276].
Figure 5. nMDS representing the differences in the epibiont community on Dendrophyllia ramea per depth (m). Stress = 0.22.
Table 3. A posteriori pair-wise permutation multivariate analysis of the variance comparison for the different levels of the factor ‘Depth’ for epibionts growing on Dendrophyllia ramea.
In accordance with the SIMPER analysis (Table S3), 20 species of epibionts contributed to the differences between the depths of 34 and 45 m. Of these species, 11 were those that characterised the first depth, and 12 species characterised the second. The only organism common to all depths analysed (34, 40, and 45 m), with analogous similarities, was the bryozoan Cellepora pumicosa (Pallas, 1766). The species that characterised the depth of 34 m, with higher similarities, were juveniles and recruits of the bivalve Gregariella semigranata (Reeve, 1858), the bryozoan of genus Bugula Oken, 1815 or the echinoderm of genus Ophiura Lamarck, 1801. For the depth of 45 m, the hydrozoans Campanularia hincksii Alder, 1856 and Clytia linearis (Thorneley, 1900) or the sponge Hymedesmia sp. were characteristic. Finally, the species that presented analogous similarities and that contributed to the fact that the depth of 40 m is not different from that of 34 m were: the amphipods from the families Caprellidae, Ischyroceridae, Aoridae, Sthenothoidae, Dexaminidae, and Corophiidae, alongside the hydrozoan Laomedea sp.; and at the depth of 45 m: the bryozoan Pentapora fascialis and the poriferous Timea sp.
In congruence with the multivariate analysis, the number of species of epibionts showed similar results. It is lower in the shallowest zone (34 m) compared to the deepest area studied (45 m) and the intermediate depth (40 m) showed no significant difference with any of the previous ones (Figure 6).
Figure 6. Number of epibiont species on Dendrophyllia ramea per depth (m), showing the results of the Generalised Linear Model.
Threats to the integrity of the CWC habitat: marine litter on the seafloor
The anthropogenic impact on the study area was evaluated by analysing the coverage of litter, which showed the highest average coverage at a depth of 42 m and a lowest coverage at 48 m. Artificial polymers (plastics from fishing waste, such as nets, ropes, fishing lines and to a lesser extent, and plastic bags) had the largest average litter coverage (cm2), but high amounts of glass (bottles) and ceramic debris, fabric and textile debris, metals (from free anchorages) and rubber were also identified (Figure 7). In our video observations, we noted that a significant portion of marine litter originated from longlines and other gears used in fishing activities. The results of the LM analyses showed significant interactions between the factors ‘Depth’ and ‘Type of litter’ (F 12 = 2.99; P = 0.004), indicating that the differences in cover of each type of litter were not homogeneous across levels of the factor ‘Depth’. The transects spanned a total length of 100 m at each depth of 30, 36, 42, and 48 m, positioned at distances from the coastline as shown in the map (Figure 1). Given the significant interactions, the analyses were conducted by type of litter. Only artificial plastic polymer showed significant differences among depths. The lowest abundance of artificial plastic polymers was recorded at 48 m, the highest at 42 m, and its coverage at 36 m was also significantly different from that at 48 m, although this result was only marginally significant (Table 4). Furthermore, it was found that 73% of the total colonies were entangled in ropes or human debris, resulting in various types of harm or impairment.
Figure 7. Average coverage of litter (cm2) for each depth (m) level according to the category.
Table 4. Linear model for the mean average coverage of artificial polymer per depth (m).
SE, standard errors.
For the categorical variable ‘Depth’, 48 m was used as reference level.
a Marginally significant.
b Significant differences at P < 0.05.
Discussion
The present study quantitatively describes Dendrophyllia ramea assemblage in Western Mediterranean area, at the locality of PM, considering abundance, colony size range, and distribution patterns, as well as the diversity of organisms associated with it and the anthropogenic impact. In this area, the 311 colonies surveyed (representing only a fraction of a much larger population, pers. obs.) exhibited a greater abundance at a depth unusually shallow in relation to that recorded so far (40–400 m) in the Mediterranean Sea (Bonfitto et al., Reference Bonfitto, Bigazzi, Fellegara, Impiccini, Gofas, Oliverio, Taviani and Taviani1994; Kružić et al., Reference Kružić, Zibrowius and Pozar-Domac2002; Requena and Gili, Reference Requena and Gili2014).
The D. ramea assemblage in the four depths selected in this study seems to be conditioned by the mixing of water masses from the Atlantic Ocean with those from the Mediterranean Sea. The Alboran Sea is highly influenced, on one hand by the inflowing Atlantic waters (Candela, Reference Candela1991), which presents an asymmetric circulation through the Strait and through the Alboran Sea (Echevarría et al., Reference Echevarría, Bruno, Gorsky, Goutx, Fernando, Vargas, Picheral, Striby, Varela, Prieto, Alonso, Reul, Cózar, Prieto, Sarhan, Plaza and Jiménez-Gómez2002; Skliris and Beckers, Reference Skliris and Beckers2009). The Atlantic water passes eastward along the northern part of the Alboran Sea (the Atlantic Jet) and forms 2 anticyclonic gyres (Western Alboran Gyre and Eastern Alboran Gyre) which reach the African Coast (Millot, Reference Millot1992; Vargas-Yáñez et al., Reference Vargas-Yáñez, Plaza, García-Lafuente, Sarhan, Vargas and Vélez-Belchi2002). On the other hand, the northern coast of the Alboran Sea, is also influenced by Mediterranean Water (Northern Current), coming from the Catalan Sea, and running down the Spanish Mediterranean Coast towards the Strait of Gibraltar (Bouzinac et al., Reference Bouzinac, Font and Johannessen2003). This water mass loses its influence close to the Strait (there, the Atlantic Jet blocks it; Sarhan et al., Reference Sarhan, Lafuente, Vargas and Plaza2000), and it seems to give a typical Mediterranean character to the northern coast. Thus, Alboran Sea presents intermediate condition between Atlantic and Mediterranean in regard to dissolved nutrients and plankton biomass (Gómez et al., Reference Gómez, González, Echevarría and García2000), sea surface temperature, and sea level (Bouzinac et al., Reference Bouzinac, Font and Johannessen2003; Nykjaer, Reference Nykjaer2009).
Dendrophyllia ramea reaches shallower depths in the Atlantic Ocean where, for example, a colony of this species was recorded in the Sagres Caves (Portugal – North Atlantic) at a depth of only 14 m (Boury-Esnault et al., Reference Boury-Esnault, Harmelin, Ledoyer, Saldanha and Zibrowius2001). While in the Mediterranean Sea, its assemblages are mainly distributed below 40 m. In the eastern Basin it is distributed in Greece from 39 m (Salomidi et al., Reference Salomidi, Zibrowius, Issaris and Milionis2010), in Turkey 40 m (pers. comm. Dr Mehmet Baki Yokes), in Croatia 43 m (Kružić, Reference Kružić2002), in the Ionian Sea at Sicily 70 m (Angiolillo et al., Reference Angiolillo, Giusti, Rossi and Tunesi2022), while in Cyprus it starts at 125 m (Orejas et al., Reference Orejas, Gori, Jiménez, Rivera, Lo Iacono, Hadjioannou, Andreou and Petrou2017). In the western Basin it is distributed in Nicotera (Italy) at 80 m (Arpacal, 2017), reaching up to 173 m in eastern Sardinia (Bonfitto et al., Reference Bonfitto, Bigazzi, Fellegara, Impiccini, Gofas, Oliverio, Taviani and Taviani1994) and up to 161 m in Menorca – Spain (Requena and Gili, Reference Requena and Gili2014).
The Alboran Sea is strongly influenced by the Atlantic Ocean (Candela, Reference Candela1991), where the denser and saltier Mediterranean water mass flows under the Atlantic water mass westward through the Strait of Gibraltar (Bormans et al., Reference Bormans, Garrett and Thompson1986). Upon entering the Mediterranean, the Atlantic water masses flow eastward along the northern part of the Alboran Sea (generating the Atlantic Jet) and form two anticyclonic gyres (Western Alboran Gyre and Eastern Alboran Gyre), which reach the southern coast of Morocco (Vargas-Yáñez et al., Reference Vargas-Yáñez, Plaza, García-Lafuente, Sarhan, Vargas and Vélez-Belchi2002). The multivariate structure of various species assemblages in the Strait of Gibraltar region, such as opisthobranchs, anthozoans, tunicates and cnidarians, has been observed to possess intermediate characteristics between the Atlantic and central or eastern Mediterranean, potentially extending to the Alboran Sea area (Naranjo, Reference Naranjo1995; Naranjo et al., Reference Naranjo, Carballo and García-Gómez1998; Cervera et al., Reference Cervera, Calado, Gavaia, Malaquias, Templado, Ballesteros, García-Gómez and Megina2004, González-Duarte et al., Reference González-Duarte, Megina, Piraino and Cervera2013). The assemblage of D. ramea in the study area also shows these intermediate bathymetric distribution characteristics, since this area has an average bathymetric distribution between that of the Portuguese and Western Mediterranean populations, reaching depths of between 25 and 30 m at PM (Cebrián et al., Reference Cebrián, Ballesteros and Canals2000; Ocaña et al., Reference Ocaña, Tocino and González2000; Cebrián and Ballesteros, Reference Cebrián and Ballesteros2004), 24 m in Morocco (Salvati et al., Reference Salvati, Tunesi and Molinari2004) and 30 m in Chafarinas Islands (Pers. Obs. González-Duarte). Based on the quantitative sampling of the video transects and multivariate analyses, we distinguished three depth zones defined by the composition and abundance of macro-benthic organisms associated with the D. ramea reef. This variation appears to be primarily driven by the bathymetry of the area, aligning with the depth gradient of the seabed, while additionally being influenced by the presence of D. ramea.
CWC are generally associated with other HFS of lower frame-building potential (Zibrowius, Reference Zibrowius1980; Roberts et al., Reference Roberts, Wheeler, Freiwald and Cairns2009). This feature produces a high biodiversity in the areas where they are present because they can often be explored by other organisms due to their shelter, nursery or feeding interest (D'Onghia, Reference D'Onghia, Orejas and Jiménez2019; Otero and Marín, Reference Otero, Marin, Orejas and Jiménez2019; Rueda et al., Reference Rueda, Urra, Aguilar, Angeletti, Bo, García-Ruiz, Taviani, Orejas and Jiménez2019). Some of these are bryozoans of the species Myriapora truncata and Pentapora fascialis, which are recognised as both primary structure builders (i.e. they build structures alone) or in combination with other organisms, and secondary structure builders. These organisms are important in providing habitat for diverse species and assemblages, playing an important role in promoting biodiversity and habitat heterogeneity (Lombardi et al., Reference Lombardi, Taylor, Cocito, Goffredo and Dubinsky2014). Both species characterised the shallowest community (30 m) groups and seem to be conditioned by the availability of hard substrates for settlement.
We have also observed the presence of Parazoanthus axinellae and Axinella damicornis at a depth of 42 m, where they are typically found in a symbiotic relationship with D. ramea as described by Cachet et al. (Reference Cachet, Genta-Jouve, Regalado, Mokrini, Amade, Culioli and Thomas2009). This association between the cnidarian and sponge species is characteristic of the intermediate depth group studied in the community structure of species at PM, highlighting the important role of symbiosis in shaping the ecology of marine communities.
As previously mentioned, the result of the PERMANOVA showed that species appear to be conditioned by the availability of rocky substrates. Below 48 m depth, algae are not relevant and suspensivorous organisms become more abundant, such as the sponges Cliona viridis or Haliclona (Reniera) mediterranea. The exception is the invasive alga Rugulopteryx okamurae (E. Y. Dawson) I. K. Hwang, W. J. Lee y H. S. Kim, 2009, which is more abundant at greater depths, probably due to algal downwellings where it is mostly detached from the rocky bottom and dragged by marine currents (Estévez et al., Reference Estévez, Palacios, Cervera and González-Duarte2022; Mateo-Ramírez et al., Reference Mateo-Ramírez, Iñiguez, Fernández-Salas, Sánchez-Leal, Farias, Bellanco, Gil and Rueda2023).
The present study adds 63 new species and 15 genera to the list of CWC associated fauna of Rueda et al. (Reference Rueda, Urra, Aguilar, Angeletti, Bo, García-Ruiz, Taviani, Orejas and Jiménez2019). The species we identified as most abundant include: Rugulopteryx okamurae (Algae), Crambe crambe and Axinella damicornis (Porifera), Cerianthus membranaceus (Gmelin, 1791) and Parazoanthus axinellae (Cnidaria), Pentapora fascialis and Cellepora pumicosa (Bryozoa), Octopus vulgaris Cuvier, 1797 and Flabellina sp. (Mollusca), Spirobranchus triqueter (Linnaeus, 1758) (Annelida), Balanus trigonus Darwin, 1854 (Arthropoda), Arbacia lixula (Linnaeus, 1758) (Echinodermata), Aplidium punctum (Giard, 1873) (Chordata). In the description of the deep-sea communities of the Mediterranean Sea, hydrozoans are a group that are generally not described at the species level and are often grouped together as ‘hydroids’ (Rueda et al., Reference Rueda, Urra, Aguilar, Angeletti, Bo, García-Ruiz, Taviani, Orejas and Jiménez2019). This study is one of the few that has identified 15 species of these cnidarians, contributing unique information to previous descriptions of organisms present in the studied ecosystem (Cebrián and Ballesteros, Reference Cebrián and Ballesteros2004; González-Duarte et al., Reference González-Duarte, Megina, Piraino and Cervera2013, Reference González-Duarte, Megina and Piraino2014). Among them, Clytia linearis, Campanularia hincksii, Obelia dichotoma, Laomedea sp., Sertularia sp., and Antennella secundaria (Gmelin, 1791) were the most abundant.
In regard to the epibiont community, in the Eastern Mediterranean Sea, bryozoans are the most abundant collected group of epibionts living on the coral D. ramea (Jiménez et al., Reference Jiménez, Achilleos, Abu Alhaija, Gili and Orejas2016). In concordance with these results, bryozoans were also the most characteristic epibionts of the coral at all depths studied, particularly the species Cellepora pumicosa. This could be evidence of a close relationship between bryozoans and D. ramea; however, the difficult access to CWC communities limits the extension of our knowledge about their associated species.
Moreover, another significant group of epibionts associated with deep-sea corals in the Mediterranean are the mobile peracarid species (Cartes et al., Reference Cartes, Díaz-Viñolas, González-Irusta, Serrano, Mohamed and Lombarte2022). In our study, we identified six different families of peracarids: Caprellidae, Ischyroceridae, Aoridae, Sthenothoidae, Dexaminidae, and Corophiidae. Although we did not find representatives of the Pontogeneiidae family, which is noted to be highly abundant along the coasts of Mallorca in the western Mediterranean, near Punta de la Mona, it is worth mentioning that these findings pertain to much greater depths, exceeding 1000 m (Cartes et al., Reference Cartes, Díaz-Viñolas, González-Irusta, Serrano, Mohamed and Lombarte2022).
The result of the SIMPER analysis on the epibiont community showed that the shallower depth groups are important as nursery sites (many recruits and juveniles were observed, including ophiuroids like Ophiothrix fragilis and Ophiura sp., and crabs like Pisidia longicornis and Inachus sp.), including for other HFS such as P. fascialis, especially in the deeper zone (40 and 45 m). The importance of D. ramea as a substrate for many species is reflected in the fact that the number of epibionts increases with depth (Figure 6), where rocky substrates are less frequent. At 45 m, species like Clytia linearis and Campanularia hincksii seem to contribute significantly to the observed differences, while at shallower depths, species such as Antennella secundaria and Cellepora pumicosa play important roles. In addition, in the deeper zone, corals are largely fractured and wounded due to high anthropogenic impact, especially when compared to the low colony abundance, which also promotes the growth of epibionts on their calcareous skeleton. The combination of both conditions, substrate scarcity and coral injury, explains the increase in the presence of epibionts with depth.
Although D. ramea is a HFS hosting community of native associated organisms (Dayton, Reference Dayton1972), this species also serves as a substrate for non-native species, which can be one of the main threats to biodiversity in marine environments (Galil et al., Reference Galil, Marchini, Occhipinti-Ambrogi, Minchin, Narščius, Ojaveer and Olenin2014). In the studied population, two non-native species were found as epibionts of D. ramea. One of these was the barnacle Balanus trigonus Darwin, 1854, a species introduced into the Mediterranean Sea, probably before 1850 (Zullo, Reference Zullo1992). The other species is the brown seaweed R. okamurae, which could be a risk for the coral due to its highly competitive capacity (Estévez et al., Reference Estévez, Palacios, Cervera and González-Duarte2022).
Our findings describe how D. ramea colonies are negatively affected by human activity in the PM area, mainly by artisanal fishery, even though it has been listed as a Special Area of Conservation. In particular, fishing lines and ropes may damage or cut coral branches and nets may completely uproot large colonies from the substrate. As a result, urgent action is required to implement a conservation management plan to prevent these detrimental activities in the region. Although marine litter on the seafloor may originate from river discharge (González-Fernández et al., Reference González-Fernández, Cózar, Hanke, Viejo, Morales-Caselles, Bakiu, Barceló, Bessa, Bruge, Cabrera, Castro-Jiménez, Constant, Crosti, Galletti, Kideys, Machitadze, Pereira de Brito, Pogojeva, Ratola, Rigueira, Rojo-Nieto, Savenko, Schöneich-Argent, Siedlewicz, Suaria and Tourgeli2021) or depend on the hydrodynamic regimen that causes the deposition of plastics and debris in the ocean (Zambianchi et al., Reference Zambianchi, Iermano, Suaria and Aliani2014), fishing line and entagled nets are the results of unregulated fishing activities for this reason, actions are required to implement plans to prevent these detrimental activities.
Other studies have shown that in the Mediterranean Sea, the main types of waste found are, plastics, glass, metal and clinker (Ramirez-Llodra et al., Reference Ramirez-Llodra, De Mol, Company, Coll and Sardà2013). Among the most abundant types of waste, we have identified debris made of rubber, glass/ceramics, and artificial plastic polymers, with a large number of fishing lines and nets which pluck the branches off the corals. In addition, plastics are of particular importance given they eventually fragment into small particles (microplastics, <5 mm) (Andrady, Reference Andrady2011), which may accumulate in scleractinian corals when mistaken for food particles (Saliu et al., Reference Saliu, Montano, Leoni, Lasagni and Galli2019), causing coral disease (Nama et al., Reference Nama, Shanmughan, Nayak, Bhushan and Ramteke2023). Furthermore, artificial plastic polymers were found to be more abundant at depths of 36 and 42 m, posing a risk to the D. ramea communities as these depths coincide with the highest coral abundance. The proximity of Marina del Este port suggests it as a primary source of marine debris impacting Punta de la Mona's marine environment. Despite this, there are so far no adequate management plans in the area to prevent waste from reaching the marine environment, although it has long been known that once deposited on the seabed it can modify the surrounding habitat (Saldanha et al., Reference Saldanha, Sancho, Santos, Puente, Gaspar, Bilbao and Arregi2003). Therefore, the particular and unique coral reef living in PM requires protection given the great anthropogenic impact suffered by the area.
In conclusion, this study emphasises the importance of D. ramea and the necessity of implementing management plans to regulate relevant activities. It provides a quantitative description of the D. ramea assemblage in the Western Mediterranean, on its abundance, distribution patterns, associated biodiversity and the impact from human activities. Notably, the species exhibits higher abundance at shallower depths than typical, which is likely influenced by water mass mixing between the Atlantic Ocean and Mediterranean Sea. Despite the ecological importance of this ecosystem, coral colonies in the study area are under significant threats from fishing and the accumulation of waste and plastics. Urgent conservation management plans are crucial to safeguard this ecologically crucial coral reef and effectively address the negative effects of human impact. Taking prompt action is essential to preserve this valuable coral ecosystem and uphold its vital ecological role in the region.
Supplementary Material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315424000626.
Data
All relevant data are included in the manuscript and Supplementary Materials files. The raw data extracted from the videos were used to generate the results and figures. We will consider sharing the videos and images upon request.
Acknowledgements
We thank the scientific divers from Coral Soul who assisted us in sampling and the underwater photographers Rafael Camacho (Figure S1-A), Luis Sánchez Tocino (Figure S1-B), Javier Sánchez (Figure S1-C) and Stefano Celini (Figure S1-D).
Author Contributions
R. M. E., M. P., L. C. and M. G.-D. conceived the idea and designed the study. M. P. carried out the sampling. R. M. E. and M. G. D. obtained and analysed the data. R. M. E. wrote the first draft of the manuscript and all authors contributed critically to the drafts and gave final approval for publication.
Financial Support
This work was supported by the Deep Core Project from the NGOs Coral Soul, and Coral Guardian and ESMARES2-INFRA from the Instituto Español de Oceanografía (IEO-CSIC), under the framework ordered to the IEO-CSIC by the Ministerio para la Transición Ecológica y el Reto Demográfico (MITECO) of the Spanish government for the application of the Marine Strategy Framework Directive (MSFD) in Spanish waters.
Competing interests
None.
Ethical Standards
No vertebrates or regulated invertebrates were involved in our research.
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