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Article

The Diversity, Structure, and Development of the Epibiont Community of Paramuricea clavata (Risso, 1826) (Cnidaria, Anthozoa)

by
Martina Canessa
1,2,*,
Ilaria Amedeo
3,
Giorgio Bavestrello
1,2,
Pier Panzalis
4 and
Egidio Trainito
5
1
Dipartimento di Scienze della Terra dell’Ambiente e della Vita (DISTAV), Università di Genova, Corso Europa 26, 16132 Genoa, Italy
2
National Biodiversity Future Center (NBFC), Piazza Marina 61, 90133 Palermo, Italy
3
Via Santa Chiara 11, 07026 Olbia, Italy
4
Tavolara Punta Coda Cavallo MPA, Via S. Giovanni 14, 07026 Olbia, Italy
5
Genoa Marine Centre-Stazione Zoologica Anton Dohrn Istituto Nazionale di Biologia, Ecologia e Biotecnologie Marine, Villa del Principe, Piazza del Principe 4, 16126 Genoa, Italy
*
Author to whom correspondence should be addressed.
Water 2023, 15(14), 2664; https://doi.org/10.3390/w15142664
Submission received: 16 June 2023 / Revised: 13 July 2023 / Accepted: 14 July 2023 / Published: 23 July 2023
(This article belongs to the Special Issue Anthropogenic Impacts on Benthic Marine Ecosystems)
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Abstract

:
Mass mortality events and anthropogenic impacts affecting Paramuricea clavata (Risso, 1826) have been increasingly documented during the last decades. These impacts have enhanced the settling of epibiont organisms on injured colonies. This epibiosis was studied using photographic sampling carried out on the granitic outcrops of the Tavolara Channel within the Tavolara–Punta Coda Cavallo marine-protected area (NE Sardinia) between 2017 and 2023 at 35–55 m. The number of colonies and percentage of surface involved in the epibiosis, the specific richness of the epibiont community, and the temporal evolution of the phenomenon were studied. Almost all the investigated gorgonians (93%) showed parts involved in epibiosis, with high percentages of surface covering (one-third of the surface). Out of the 37 epibiont species recorded, the most recurrent ones demonstrated an ecological succession dominated by Hydrozoa, Porifera, Bryozoa, Serpulidae, and the parasitic soft coral Alcyomiun coralloides. Nevertheless, single colonies studied over time revealed the unpredictability of the colonization process. The peculiar habitat of the granitic outcrops hosting the P. clavata forests is of a high naturalistic value and demonstrates a widespread condition of suffering, supported by both environmental and anthropogenic sources of stress. Such considerations make it necessary to review the current zonation of the area, where the actual vulnerability and usability evaluations are based on incomplete information.

1. Introduction

The purple gorgonian Paramuricea clavata (Risso, 1826) is an endemic Mediterranean species [1] considered “vulnerable” in the Red List of the International Union for Conservation of Nature [2] because of its large size, branched shape, and limited flexibility that render it highly susceptible to a wide range of natural and human impacts [3,4,5,6]. A pool of evidence regarding the reduction in some Mediterranean populations in the last three decades has addressed a mix of consequences due to the increase in positive thermal anomalies with summer diseases and the development of filamentous algae, mucilage, and invertebrate epibionts [7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22].
Moreover, it has been recognized that P. clavata forests are highly sensitive to direct and indirect anthropogenic impacts (boat anchoring, recreational and commercial fishing, and SCUBA diving) [19]. In 1997, Bavestrello et al. [4] described the multiple damages inflicted on these gorgonians by fishing activity: lost lines in contact with colonies scrape the coenenchyme, and these abrasions create suitable conditions for the settlement of numerous epibiont organisms that weigh down the branches until the total or partial breaking of the colony occurs under the action of the currents. This issue has been reported by several authors who suggest that the number of colonies involved in epibiosis is an index of the stress of the population due to fishing [2,5,6,23,24]. In fact, Linares et al. [25] stated that, without extraordinary events, the extent of colony injury and the proportions of affected gorgonian colonies have remained low over time; therefore, any substantial increase in these parameters may serve as a good indicator of recent disturbances.
The Tavolara–Punta Coda Cavallo Marine Protected Area (40.8830 N, 9.7020 E, Sardinia, Italy) hosts a large population of P. clavata settled on both Tavolara Island’s limestones and the Tavolara Channel’s granitic outcrops [26,27]. This P. clavata population has been widely studied in recent years, with several surveys conducted since the 2000s to evaluate its health status after the occurrence of diseases/mortality events [14,16,21,28]. Unfortunately, this pool of data covers only shallow sites (up to 35 m in depth) under the medium–high protection regime (A–B Zones) and does not include gorgonians settled on deeper granitic shoals at depths ranging from 35 to 55 m [27], characterized by low protection levels (C Zone) and prone to intense fishing activity [29,30].
This paper aims to obtain data about the levels of epibiosis in the gorgonians present in this charismatic MPA and also concerning different regimes of protection. Moreover, a particular focus is provided on the diversity, structure, and development of the epibiont community. In fact, despite the wide use of epibiosis as an index of injuries, few data are available regarding descriptions of the community.

2. Materials and Methods

The Tavolara MPA was established in 1997, and the zoning definition, based on various campaigns documented by Bianchi et al. [31], has not subsequently changed. This MPA provides three levels of protection with definitive regulations (decree n°299, issued by the Ministero dell’Ambiente e della Tutela del Territorio del Mare on 30 December 2014): the A Zone, the no-entry/no-take reserve; the B Zone, the general protection reserve; and the C Zone, the partial protection reserve. Artisanal fishing performed only with selective gears that preserve the seafloor integrity is allowed in the B and C Zones. In the latter, recreational fishing is also allowed, though with some restrictions.
Our study area involved granitic outcrops that emerge from a detrital plain located in the middle of the Tavolara Channel (C Zone) between the Tavolara and Molara Islands, in the depth range of 35–55 m (Figure 1).
During scuba dives performed from 2017 to 2023, 10 granitic sites (out of 57 where Paramuricea clavata is present) were selected on the basis of gorgonian abundance (>5 col. m−2). For each shoal, on average, 40 photos were obtained, applying the multi-zoom photographic approach [32] to evaluate the occurrence of damages to and epibionts on gorgonians. Images were taken using a Sony A6000 camera (24 megapixels, two Inon Z330 flashes, color temperature of 5000 K) with a Sony 16–50 lens (focal length of 19 mm), a Nauticam WW1 wet wide lens (130° rectilinear field angle) and a Sea & Sea MDX-A6000 underwater case with a flat porthole. Photos were post-processed with Adobe Photoshop©, while formal analysis was performed with ImageJ Software [33].
Out of 410 photographs, 582 colonies of P. clavata with frontal perspectives were examined to evaluate the recurrence percentage of single epibionts, the diversity of the epibiont assemblage, and the relative surface of the gorgonian involved in epibiosis. The epibiont coverage was estimated as a percentage of the planar colony surface to avoid problems due to the angular distortion of the images. The three-dimensional development of the epibionts was not considered, as our focus was the relative area of each colony involved in epibiosis. Only colonies with more than 5% of the surface area subjected to epibiont coverage were considered in our study. Finally, we recorded the presence of entangled and abandoned fishing gear.
Epibiont organisms were identified and classified at the lower taxonomic level; when specific or generic identification was not possible, other taxonomic and morphological units (OTUs) were adopted. Only taxa with a recurrence higher than 10% of the whole photographic dataset were employed in the formal analysis.
Moreover, owing to the wide photographic archive (1986-2023) (ET), we had the opportunity to analyze images of the same colonies (easily recognizable by the overlapping of the main ramifications) taken over a long period. These data allowed us to reconstruct the temporal evolution of the epibiosis process. All images present in the archive and selected for this study were obtained with the same technique.

3. Results

3.1. Paramuricea Clavata of the Tavolara Channel Granitic Shoals

The granitic outcrops emerging from the detritic bottom of the Tavolara Channel are characterized by a modest development of the basal coralline algal layer that only occasionally forms the typical coralligenous bioherms. The density of the Paramuricea clavata varied from 5 to 25 colonies m−2. Moreover, the macrobenthic community is mainly represented by other gorgonians (Eunicella cavolini (Koch, 1887), E. singularis (Esper, 1791), E. verrucosa (Pallas, 1776), erected sponges (Axinella polypoides Schmidt, 1862, Spongia (Spongia) officinalis Linnaeus, 1759, Sarcotragus foetidus Schmidt, 1862) and branched bryozoans (Adeonella calveti Canu and Bassler, 1930, and Turbicellepora avicularis (Hincks, 1860)) (Figure 2a,b).
During the period of observations, serious damages to colonies resulting from heat waves, with necrosis and loss of coenenchyme, were documented in 2018 (Figure 2c,d); other less intense episodes were recorded in 2017, 2019, and 2020. The P. clavata spawning (Figure 2e) was recorded between 2009 and 2022 (ET personal observations), with the exceptions of 2010, 2018, and 2019. Recruits, as small unbranched colonies composed of less than ten polyps (Figure 2f), were observed in 2017, 2018, and 2020.

3.2. Epibiosis

Of the 582 studied colonies of P. clavata, 541 presented some degree of epibiosis (93.0%), and only 41 (7.0%) were intact (Figure 3a–c); 455 (78.2%) showed epibiosis on more than 5% of the colony’s surface, 15 (2.6%) were recorded completely dead in standing position, 31 (4.6%) were found entangled in lost fishing gear (Figure 3d), and 58 (8.8%) were uprooted (Figure 3e). On average, epibiosis affected 27.3 ± 1.2% of the colony surface.
From the diversity point of view, the epibiont assemblages on the gorgonians of the Tavolara MPA accounted for 37 species (or OTUs), of which 5 were vagile (Table 1).
The most diversified group was Porifera, with 11 species (or OTUs), followed by Bryozoa and Ascidiacea, respectively, with 7 and 5 species (or OTUs). About 13% of the observed colonies showed only one epibiont species (OTUs), about 45% hosted two to three species, while 23% were found with four to five species (OTUs). The highest value of species (OTUs) per colony was 16, which was recorded in one colony. The most common species/OTUs (Figure 4) resulted in the ubiquitarians Hydrozoa recorded in 91.9% of the epibiont colonies, four Porifera (Dysidea fragilis (Montagu, 1814) (43.8%), Crella (Crella) elegans Schmidt, 1862) (10.4%), D. perfistulata Pulitzer-Finali and Pronzato, 1980 (10.2%), (Pleraplysilla spinifera (Schulze, 1879) (9.9%)), three Bryozoa (Adeonella calveti (52.3%), Turbicellepora avicularis (26.9%), Flustra sp. (9.6%)), parasitic Alcyonacea Alcyonium coralloides (Pallas, 1766) (22.9%), and Serpulidae Filograna/Salmacina spp. (33.3%) (Figure 5).
These species produced different growth patterns on the gorgonian branches (Figure 5). The observed Hydrozoa generally did not make large colonies but a carpet of small creeping colonies involving the entire naked skeleton. A. calveti, T. avicularis, and Filograna/Salmacina spp. were able to produce large subspherical colonies that develop starting from a small portion of the free skeleton. Finally, Porifera and A. coralloides grew, covering entire branches of the gorgonians.
Single epibiont species adopted a different pattern of colonization in relation to the richness of the assemblage. Hydrozoa were always recorded as pioneers and occurred in the epibiont community independently of their richness. The group of bushy species (Bryozoa and Serpulidea) followed Hydrozoa, and their occurrence quickly increased according to the number of species present in the community. A similar trend was shown by a pair of Porifera (D. fragilis and C. elegans) that grew, covering a wide portion of the gorgonian’s branches. Finally, other species such as D. perfistulata, P. spinifera, and A. coralloides, needed more than four species or OTUs of the assemblage for their settling (Figure 6).
During the colonization process, new species were added to the community that became more and more complex without substitution (Figure 7a): in fact, the average percentage of the gorgonian surface involved in epibiosis colonies increased according to the diversity of the epibiont community (Figure 7b).

3.3. Observations on Single Gorgonians through Time

By observing single colonies through time (months, seasons, and years), it was possible to describe the development of epibiosis on P. clavata, which showed great variability in mode and time, even if some general patterns can be described.
When the lesions of the coenenchyme originate from thermal stress, the fate of the epibiosis depends on the extension of the denudated scleraxis. In fact, if the involved surface was not too extended, the coenenchyme was able to re-grow on the naked skeleton, even if already covered by the hydrozoan carpet. Two colonies photographed in 2020 showed a complete recovery in two years (Figure 8a–d). When the lesions were too wide, recovery was not possible, and epibiosis developed very quickly, involving the entire colony (Figure 8e,f).
In some rare cases, the epibiont community did not increase its complexity, and branches remained covered by Hydrozoa for several years. A colony in 2018 showed several naked portions of the skeleton partially covered by Hydrozoa (18.9% of the colony surface); two years after (2020), the epibionted surface decreased to 9.1% owing to a re-growth of coenenchyme on the involved branches. After four years (2023), the colony surface again showed a modest increase in epibiosis (19.3%) (Figure 8g–j).
Quick colonization was also observed when epibiosis was due to the scraping of entangled lines. A colony photographed in March 2023 entangled by a lost line, already colonized by Hydrozoa and A. calveti, showed a very fast development of the epibiont community: in 47 days (May 2023), it also included D. fragilis, Terpios fugax Duchassaing and Michelotti, 1864, Serpulidea, and Beania magellanica (Busk, 1852) with a covered surface shifting from 15.7% to 24.4% (Figure 9a,b).
Another colony recorded entangled in April 2018 by a line showed an epibiont community composed of A. calveti, T. avicularis, and Filograna/Salmacina spp. In the following December, the epibiotic community progressively developed in size without increasing the number of species or OTUs. In this period, the Filograna/Salmacina spp. appeared drastically reduced. The comparison with an image obtained four years after (October 2022) showed the settlement of the sponge D. fragilis and a shift in the involved surface from 22.73% to 50.74% (Figure 9c–e).
In March 2018, a colony was recorded with some nude branches partially covered by Hydrozoa and A. calveti; at the end of the year (November/December 2018), naked parts were covered by a massive development of Filograna/Salmacina spp. (Figure 9f–h). In some cases, when the scraping of the lost line is blocked by the growth of the carbonatic epibionts, the colonies are able, after several years, to recover damaged portions (Figure 9i,j).
The observation of one dead extirpated colony (line still in situ) showed a long persistence of the gorgonian skeleton (five years) that became heavily colonized by sponges and encrusting coralline algae (Figure 9k–m).

4. Discussion

In natural assemblages, epibiosis increases biodiversity by improving the coexistence of different species [34]. In general, gorgonians are particularly involved in this phenomenon [35]. Nevertheless, in the Mediterranean Sea, it is clear that epibiosis on Paramuricea clavata is enhanced by disturbances due to thermal stress or anthropogenic injuries such as fishing activity; therefore, it has to be considered as a sentinel of environmental degradation [8,19].
The first impressive evidence emerging from the study of epibionts on the P. clavata forests in Tavolara MPA was the high percentage of involved colonies: more than 70% of the studied specimens showed, on average, one-third of the surface covered by epibionts. For comparison, a study conducted in the Medes Islands MPA (Catalan Sea) indicated that between 10% and 33% of the colonies of unprotected populations were partially colonized by epibionts, whereas only 4% to 10% of the populations in the MPA were affected [36]. Inside the Portofino MPA (Ligurian Sea), 51% of colonies showed epibionts [19]; along the eastern Adriatic coasts, less than 10% of the observed colonies presented denuded branches or epibiosis [37]. Very probably, the present data indicate that the Tavolara MPA is the Mediterranean area with the highest recorded values. This high presence of injured colonies induced, in 2008, an experiment in restoration by pruning the forest [38].
It was already stated that epibiosis originates from the loss of coenenchyme integrity, which creates exposed portions on the gorgonian skeleton on which epibionts can settle. Gorgonian diseases and fishing impact are considered the main causes of this phenomenon involving P. clavata [3,10,25,39]. In the area of Tavolara MPA, diseases/mass mortalities have occurred at least since 2001 [28], and other episodes followed in 2008 [16], 2018 [14], and 2019–2020 [21]. Recent mortality events have been shown to be increasingly damaging, as previous anomalies did not hit populations at 35−40 m depth [25,40,41]. These phenomena had a wide impact on the populations: for example, during the 2008 event, about 100% of the colonies living between 20 and 30 m depth were damaged, and this value decreased between 40 and 60% under a 35 m depth [16]. Currently, 15 years after the 2008 event, no colony of P. clavata can be found at depths of less than 29 m.
Regarding the fishing impact, demersal fishing activities represent one of the major causes of gorgonian mortality, causing entanglements, partial breakages, and detachment [19,24,42]. The persistent abrasion of the lost lines may cause wounds and infections and lead to extended epibiosis and/or necrosis [4,5,43,44,45,46]. Artisanal fishing activity is particularly intense within the Tavolara Channel, an area under a low protection regime, as demonstrated by the presence of lost fishing gear in 81 of the 82 visited sites [30] and the high percentage of impacted erect organisms [27,29].
Previous evaluation of the environmental quality of the Tavolara MPA [47] assigned low values to the Tavolara Channel because of the absence of a biogenic secondary substrate due to the lithological nature of the bedrock [26]. Considering the data presented here, the same priority habitat value of typical coralligenous reefs should be assigned to this area.
Although it is not easy to determine the causative event through the observation of epibiont colonization, some hints can be obtained. Generally, diseases caused by heat waves occur in short periods of time, causing acute stress, while damages related to entangled lines work over a long time period, producing chronic stress. In the first case, the fate of the epibiosis process depends on the percent of involved gorgonian surface [48]: when the affected portions are small, the coenenchyme is able to re-grow on the naked skeleton, plausibly quickly, despite the presence of pioneer epibionts (hydroids) [25,48,49,50,51]. Fast tissue regeneration in about one month was observed after the mass mortality event in the Portofino MPA in 2008 in the case of minor injuries [52]. Studies on soft corals [53] demonstrated that they could activate recovery mechanisms to quickly heal minor and momentary injuries and prevent the settlement of pioneer epibiont species, such as hydroids, on lesioned surfaces [54]. Recolonization of necrotic tissue might be faster and less expensive in terms of energy consumption than the production of new colony branches or tissue and is, therefore, influenced mainly by competition for space with epibionts. If the lesions involve a large portion of the denudated skeleton, the recovery is not sufficient to contrast the settling and development of calcified organisms that make epibiosis permanent.
On the other hand, for the entangled colonies, the continuous stress produced by the friction of lines, as well as friction applied to a small coenenchyme surface, completely prevents tissue recovery, favoring the development of complex epibiotic assemblages characterized by several calcified organisms (Bryozoa, Serpulidea), Porifera, and Alcyonium coralloides. In fact, a chronic injury enables a permanent colonization phase of a diversified epibiont community [4,55,56].
Although several authors have recorded the epibiosis process involving P. clavata, less attention has been dedicated to the diversity of the epibiont community: during this study, the 37 species (OTUs) found demonstrated a flourishing situation. Although we identified numerous species, some groups, virtually unidentifiable through photos, were considered as higher taxa (e.g., Hydrozoa) or as OTUs (e.g., encrusting sponges); this fact clearly indicates that the described diversity is underestimated. The recorded assemblage is similar to that previously observed in the Ligurian Sea [4].
No species are strictly related to gorgonians, although the Porifera Pleraplysilla spinifera and the bivalve Pteria hirundo (Linnaeus, 1758) were frequently recorded as acrophilic on P. clavata [57,58,59,60]. The Alcyonacea A. coralloides, a typical parasite of many gorgonians, grows by fouling (“runner” type) the apical axis of colonies [61,62]. A. coralloides exploit the stressed conditions of its host due to the reproductive window and oligotrophy of the water column during summertime, synchronizing its reproduction cycle with those of P. clavata [63]. Indeed, the emission of sexual products by A. coralloides has been documented in the Tavolara MPA area in the middle of May (Figure 2g), with the settling of recruits a couple of weeks after (ET, unpublished), occurring simultaneously with the spawning of P. clavata. The study conducted in the Medes MPA suggested that epibiosis of this species was caused by the intense diving activity and not directly by fishing impact; this is not the situation in the Tavolara Channel, where diving activity is negligible and sporadically limited to two sites, while, on the contrary, fishing is widely performed [30]. Other frequent epibionts are the opportunistic tube-dwelling polychaetes Filograna/Salmacina spp., particularly recorded after summertime [64,65].
Lacking the possibility to observe a temporal pattern of colonization, we related the presence of each epibiont with the total diversity of the epibiont community. Our observations clearly indicate that when the assemblage consists of only one species, it was generally represented by pioneer Hydrozoa turf (72%) and more rarely by Bryozoa (9%) and Porifera (4%). At this stage, the parasitic Alcyonacea A. coralloides was never found. When the assemblage increased in complexity, the species already present continued to be recorded with the progressive addition of other taxa following this order: Hydrozoa, Bryozoa, Serpulidea, Porifera, and A. coralloides. Considering the gorgonians with more than seven epibiont species/OTUs, this anthozoan was present in more than 90% of them. In general, in a hypothetical model of community development, new species are added without substitution of the previous ones. The general scenario recalls a facilitative model of succession. It has been well documented that a tolerance model, based upon recruitment dynamics and life history characteristics without later species requiring earlier ones to become established, can lead to a predictable sequence [66,67].
Another problem concerns the age estimation of epibiont assemblages. Some data are available in the literature for the first phases after mass mortality. Perez et al. [9] recorded microorganism colonization after a few days, while Hydrozoa, followed by Bryozoa and Serpulidea, were observed some weeks later. This evolution was confirmed by other authors [4,13,16,68]. Our data, obtained on single colonies photographed in different years, indicate that the epibiont assemblage persists for several years. According to Wahl [69], epibiont species commonly grow fast. This is certainly true for pioneer species (filamentous green and/or red algae and⁄or Hydrozoa) that colonize wide stripped portions of the colonies in a few weeks [4,13,16]. Enrichetti et al. [42] studied the evolution of epibiosis on lost nylon lines: after four years, the diversity of the recorded community was very similar to that of those found on P. clavata, but only after a couple of years when large colonies of calcified Bryozoa were found. These data suggest the possibility of obtaining a rough age of epibionts of gorgonians, as indicated by the temporal sequence of images of single colonies.
These results highlight how the development of epibiosis appears as a partially stochastic phenomenon. The understanding of the dynamics of the processes requires continuous monitoring techniques on a consistent number of colonies. The possibility of obtaining images over long periods of time requires a high effort in terms of resources, but on the other hand, it can allow the acquisition of fundamental information for the conservation of important and fragile habitats.

Author Contributions

Conceptualization, G.B., M.C. and E.T.; methodology, M.C. and E.T.; validation, M.C. and E.T.; formal analysis, M.C. and I.A.; investigation, E.T. and P.P; resources, E.T. and P.P.; data curation, E.T. and I.A.; writing—original draft preparation, M.C., E.T. and G.B.; writing—review and editing, M.C., E.T., I.A. and G.B.; visualization, M.C. and E.T.; supervision, G.B.; project administration, G.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. This research was supported by the National Biodiversity Future Center.

Data Availability Statement

The data collected during and/or analyzed for the present study are available from the corresponding author upon request.

Acknowledgments

The authors would like to thank the Tavolara MPA management for the permission to use the GIS environment and for the possibility to independently develop the underwater surveys. The authors would like to thank the “Slow Dive” team for its support during the diving activities.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Coelho, M.A.G.; Pearson, G.A.; Boavida, J.R.H.; Paulo, D.; Aurelle, D.; Arnaud-Haond, S.; Gόmez-Gras, D.; Bensoussan, N.; Lόpez-Sendino, P.; Cerrano, C.; et al. Not out of the Mediterranean: Atlantic populations of the gorgonian Paramuricea clavata are a separate sister species under further lineage diversification. Ecol. Evol. 2023, 13, e9740. [Google Scholar] [CrossRef]
  2. Otero, M.M.; Numa, C.; Bo, M.; Orejas, C.; Garrabou, J.; Cerrano, C.; Kružicål, P.; Antoniadou, C.; Aguilar, R.; Kipson, S.; et al. Overview of the Conservation Status of Mediterranean Anthozoans; IUCN: Málaga, Spain, 2017; pp. 1–73. ISBN 978-2-8317-1845-3. [Google Scholar] [CrossRef] [Green Version]
  3. Harmelin, J.G.; Marinopoulos, J. Population structure and partial mortality of the gorgonian Paramuricea clavata (Risso) in the north-western Mediterranean (France, Port-Cros Island). Mar. Life 1994, 4, 5–13. [Google Scholar]
  4. Bavestrello, G.; Cerrano, C.; Zanzi, D.; Cattaneo-Vietti, R. Damage by fishing activities to the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aquat. Conserv. Mar. Freshw. Ecosyst. 1997, 7, 253–262. [Google Scholar] [CrossRef]
  5. Bo, M.; Bava, S.; Canese, S.; Angiolillo, M.; Cattaneo-Vietti, R.; Bavestrello, G. Fishing impact on deep Mediterranean rocky habitats as revealed by ROV investigation. Biol. Conserv. 2014, 171, 167–176. [Google Scholar] [CrossRef]
  6. Angiolillo, M.; di Lorenzo, B.; Farcomeni, A.; Bo, M.; Bavestrello, G.; Santangelo, G.; Cau, A.; Mastascusa, V.; Cau, A.; Sacco, F.; et al. Distribution and assessment of marine debris in the deep Tyrrhenian Sea (NW Mediterranean Sea, Italy). Mar. Pollut. Bull. 2015, 92, 149–159. [Google Scholar] [CrossRef]
  7. Bavestrello, G.; Bertone, S.; Cattaneo-Vietti, R.; Cerrano, C.; Gaino, E.; Zanzi, D. Mass mortality of Paramuricea clavata (Anthozoa, Cnidaria) on Portofino Promontory cliffs, Ligurian Sea, Mediterranean Sea. Mar. Life 1994, 4, 15–19. [Google Scholar]
  8. Cerrano, C.; Bavestrello, G.; Bianchi, C.N.; Cattaneo-Vietti, R.; Bava, S.; Morganti, C.; Morri, C.; Picco, P.; Sara, G.; Schiaparelli, S.; et al. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (NW Mediterranean), summer. Ecol. Lett. 2000, 3, 284–293. [Google Scholar] [CrossRef]
  9. Perez, T.; Garrabou, J.; Sartoretto, S.; Harmelin, J.G.; Francour, P.; Vacelet, J. Massive mortality of marine invertebrates: An unprecedented event in northwestern Mediterranean. Comptes Rendus De L’academie Des Sciences. Ser. III Sci. De La Vie 2000, 323, 853–865. [Google Scholar] [CrossRef]
  10. Coma, R.; Pola, E.; Ribes, M.; Zabala, M. Long-term assessment of temperate octocoral mortality patterns, protected vs. unprotected areas. Ecol. Appl. 2004, 14, 1466–1478. [Google Scholar] [CrossRef] [Green Version]
  11. Coma, R.; Ribes, M.; Serrano, E.; Jiménez, E.; Salat, J.; Pascual, J. Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proc. Natl. Acad. Sci. USA 2009, 106, 6176–6181. [Google Scholar] [CrossRef]
  12. Schiaparelli, S.; Castellano, M.; Povero, P.; Sartoni, G.; Cattaneo-Vietti, R. A benthic mucilage event in North-Western Mediterranean Sea and its possible relationships with the summer 2003 European heatwave: Short term effects on littoral rocky assemblages. Mar. Ecol. 2007, 28, 341–353. [Google Scholar] [CrossRef]
  13. Garrabou, J.; Coma, R.; Bensoussan, N.; Bally, M.; Chevaldonné, P.; Cigliano, M.; Díaz, D.; Harmelin, J.G.; Gambi, M.C.; Kersting, D.K.; et al. Mass mortality in Northwestern Mediterranean rocky benthic communities: Effects of the 2003 heat wave. Glob. Chang. Biol. 2009, 15, 1090–1103. [Google Scholar] [CrossRef]
  14. Garrabou, J.; Gómez-Gras, D.; Ledoux, J.B.; Linares, C.; Bensoussan, N.; López-Sendino, P.; Bazairi, H.; Espinosa, F.; Ramdani, M.; Grimes, S.; et al. Collaborative database to track mass mortality events in the Mediterranean Sea. Front. Mar. Sci. 2019, 6, 478167. [Google Scholar] [CrossRef] [Green Version]
  15. Garrabou, J.; Gómez-Gras, D.; Medrano, A.; Cerrano, C.; Ponti, M.; Schlegel, R.; Bensoussan, N.; Turicchia, E.; Sini, M.; Gerovasileiou, V.; et al. Marine heatwaves drive recurrent mass mortalities in the Mediterranean Sea. Glob. Chang. Biol. 2022, 28, 5708–5725. [Google Scholar] [CrossRef]
  16. Huete-Stauffer, C.; Vielmini, I.; Palma, M.; Navone, A.; Panzalis, P.; Vezzulli, L.; Misic, C.; Cerrano, C. Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Mar. Ecol. 2011, 32, 107–116. [Google Scholar] [CrossRef]
  17. Teixido, N.; Casas, E.; Cebrian, E.; Linares, C.; Garrabou, J. Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE 2013, 8, e53742. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Turicchia, E.; Abbiati, M.; Sweet, M.; Ponti, M. Mass mortality hits gorgonian forests at Montecristo Island. Dis. Aquat. Org. 2018, 131, 79–85. [Google Scholar] [CrossRef] [PubMed]
  19. Betti, F.; Bavestrello, G.; Bo, M.; Ravanetti, G.; Enrichetti, F.; Coppari, M.; Cappanera, V.; Venturini, S.; Cattaneo-Vietti, R. Evidences of fishing impact on the coastal gorgonian forests inside the Portofino MPA (NW Mediterranean Sea). Ocean. Coast. Manag. 2020, 187, 105105. [Google Scholar] [CrossRef]
  20. Casoli, E.; Ventura, D.; Mancini, G.; Cardone, S.; Farina, F.; Donnini, L.; Pace, D.S.; Shaul, R.; Belluscio, A.; Ardizzone, G. Rehabilitation of Mediterranean animal forests using gorgonians from fisheries by-catch. Restor. Ecol. 2022, 30, e13465. [Google Scholar] [CrossRef]
  21. Chimienti, G.; De Padova, D.; Adamo, M.; Mossa, M.; Bottalico, A.; Lisco, A.; Ungaro, N.; Mastrototaro, F. Effects of global warming on Mediterranean coral forests. Sci. Rep. 2021, 11, 20703. [Google Scholar] [CrossRef]
  22. Chimienti, G.; Maiorca, M.; Digenis, M.; Poursanidis, D. Conservation status of upper-mesophotic octocoral habitats at Sporades Archipelago (Aegean Sea). Mar. Pollut. Bull. 2023, 190, 114868. [Google Scholar] [CrossRef]
  23. Angiolillo, M.; Fortibuoni, T. Impacts of marine litter on Mediterranean reef systems: From shallow to deep waters. Front. Mar. Sci. 2020, 7, 581966. [Google Scholar] [CrossRef]
  24. Sini, M.; Kipson, S.; Linares, C.; Koutsoubas, D.; Garrabou, J. The yellow gorgonian Eunicella cavolini: Demography and disturbance levels across the Mediterranean Sea. PLoS ONE 2015, 10, e0126253. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Linares, C.; Coma, R.; Diaz, D.; Zabala, M.; Hereu, B.; Dantart, L. Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Mar. Ecol. Prog. Ser. 2005, 305, 127–137. [Google Scholar] [CrossRef] [Green Version]
  26. Canessa, M.; Bavestrello, G.; Bo, M.; Trainito, E.; Panzalis, P.; Navone, A.; Caragnano, A.; Betti, F.; Cattaneo-Vietti, R. Coralligenous assemblages differ between limestone and granite: A case study at the Tavolara-Punta Coda Cavallo Marine Protected Area (NE Sardinia, Mediterranean Sea). Reg. Stud. Mar. Sci. 2020, 35, 101159. [Google Scholar] [CrossRef]
  27. Canessa, M.; Bavestrello, G.; Trainito, E.; Bianchi, C.N.; Morri, C.; Navone, A.; Cattaneo-Vietti, R. A large and erected sponge assemblage on granite outcrops in a Mediterranean Marine Protected Area (NE Sardinia). Reg. Stud. Mar. Sci. 2021, 44, 101734. [Google Scholar] [CrossRef]
  28. Calvisi, G.; Trainito, E.; Pais, M.; Franci, G.; Schiaparelli, S. Prima segnalazione di un episodio di mortalità di Gorgonacei lungo la costa dell’isola di Tavolara (Sardegna settentrionale). Biol. Mar. Mediterr. 2003, 10, 506–508. [Google Scholar]
  29. Canessa, M.; Bavestrello, G. Valutazione sperimentale dello stato di conservazione del coralligeno dell’AMP Tavolara—Punta Coda Cavallo nell’ambito della Strategia Marina, Relazione finale. Genova, Italy, 28 Novembre 2018.
  30. Amedeo, I.; Canessa, M.; Panzalis, P.; Trainito, E. The need for change in a changing world: Fishing impact within the Tavolara-Punta Coda Cavallo MPA. In Proceedings of the 4th Mediterranean Symposium on the Conservation of the Coralligenous and Other Calcareous Bio-Concretions, Genova, Italy, 20–21 September 2022; p. 11. [Google Scholar]
  31. Bianchi, C.N.; Morri, C.; Navone, A. I popolamenti delle scogliere rocciose sommerse dell’Area Marina Protetta di Tavolara Punta Coda Cavallo (Sardegna nord-orientale). Travaux Scientifiques du Parc National de Port-Cros 2010, 24, 39–85. [Google Scholar]
  32. Pititto, F.; Trainito, E.; Macic, V.; Rais, C.; Torchia, G. The resolution in benthic carthography: A detailed mapping technique and a multiscale GIS approach with applications to coralligenous assemblages. In Proceedings of the Conference: 2° Mediterranean Symposium on the Conservation of Coralligenous & Other Calcareous Bio-Concretions, Portorož, Slovenia, 29–30 October 2014. [Google Scholar] [CrossRef]
  33. Rasband, W.S. ImageJ: Image Processing and Analysis in Java. 2012. Available online: https://ui.adsabs.harvard.edu/abs/2012ascl.soft06013R/abstract (accessed on 15 April 2023).
  34. Bavestrello, G. Competizione e cooperazione nelle storie vitali degli organismi marini. Ist. Lomb.-Accad. Di Sci. E Lett.-Rend. Di Sci. 2017, 151, 109–120, eISSN 2384-986X. [Google Scholar] [CrossRef] [Green Version]
  35. Calcinai, B.; Bavestrello, G.; Bertolino, M.; Pica, D.; Wagner, D.; Cerrano, C. Sponges associated with octocorals in the Indo-Pacific, with the description of four new species. Zootaxa 2013, 3617, 1–61. [Google Scholar] [CrossRef] [Green Version]
  36. Tsounis, G.; Martinez, L.; Bramanti, L.; Viladrich, N.; Gili, J.M.; Martinez, Á.; Rossi, S. Anthropogenic effects on reproductive effort and allocation of energy reserves in the Mediterranean octocoral Paramuricea clavata. Mar. Ecol. Prog. Ser. 2012, 449, 161–172. [Google Scholar] [CrossRef] [Green Version]
  37. Kipson, S.; Linares, C.; Čižmek, H.; Cebrián, E.; Ballesteros, E.; Bakran-Petricioli, T.; Garrabou, J. Population structure and conservation status of the red gorgonian Paramuricea clavata (Risso, 1826) in the Eastern Adriatic Sea. Mar. Ecol. 2015, 36, 982–993. [Google Scholar] [CrossRef] [Green Version]
  38. Previati, M.; Magliozzi, C.; Palma, M.; Navone, A.; Pantaleo, U.; Landi, G.; Cerrano, C. Sperimentazione di tecniche di recupero (pruning) su una popolazione di Paramuricea clavata colpita da eventi di moria. Biol. Mar. Medit. 2011, 18, 40–43. [Google Scholar]
  39. Arnoux, A.; Harmelin, J.G.; Monod, J.L.; Romaña, L.A.; Zibrowius, H. Altérations des peuplements benthiques de roches profondes en Méditerranée nord-occidentale: Quelques aspects biologiques et molysmologiques. Comptes Rendus De L’académie Des Sciences. Série 3 Sci. De La Vie 1992, 314, 219–225. Available online: http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=5153892 (accessed on 15 April 2023).
  40. Bramanti, L.; Magagnini, G.; De Maio, L.; Santangelo, G. Recruitment, early survival and growth of the Mediterranean Red Coral Corallium rubrum 1758, a four-year study. J. Exp. Mar. Biol. Ecol. 2005, 314, 69–78. [Google Scholar] [CrossRef]
  41. Cupido, R.; Cocito, S.; Sgorbini, S.; Bordone, A.; Santangelo, G. Response of a gorgonian (Paramuricea clavata) population to mortality events: Recovery or loss. In Aquatic Conservation Marine and Freshwater Ecosystems; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2008; Volume 18, pp. 984–992. ISSN 1052-7613. [Google Scholar]
  42. Enrichetti, F.; Bavestrello, G.; Betti, F.; Rindi, F.; Tregrosso, A.; Bo, M. Fate of lost fishing gears: Experimental evidence of biofouling colonization patterns from the northwestern Mediterranean Sea. Environ. Pollut. 2021, 268, 115746. [Google Scholar] [CrossRef]
  43. Asoh, K.; Yoshikawa, T.; Kosaki, R.; Marschall, E.A. Damage to cauliflower coral by monofilament fishing lines in Hawaii. Conserv. Biol. 2004, 18, 1645–1650. [Google Scholar] [CrossRef] [Green Version]
  44. Yoshikawa, T.; Asoh, K. Entanglement of monofilament fishing lines and coral death. Biol. Conserv. 2004, 117, 557–560. [Google Scholar] [CrossRef]
  45. Chiappone, M.; Dienes, H.; Swanson, D.W.; Miller, S.L. Impacts of lost fishing gear on coral reef sessile invertebrates in the Florida Keys National Marine Sanctuary. Biol. Conserv. 2005, 121, 221–230. [Google Scholar] [CrossRef]
  46. Hinz, H. Impact of bottom fishing on animal forests: Science, conservation, and fisheries management. In Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots; Rossi, S., Ed.; Springer: Cham, Switzerland, 2017; pp. 1041–1059. [Google Scholar]
  47. Rovere, A.; Ferraris, F.; Parravicini, V.; Navone, A.; Morri, C.; Bianchi, C.N. Characterization and evaluation of a marine protected area: ‘Tavolara–Punta Coda Cavallo’ (Sardinia, NW Mediterranean). J. Maps 2013, 9, 279–288. [Google Scholar] [CrossRef]
  48. Cupido, R.; Cocito, S.; Barsanti, M.; Sgorbini, S.; Peirano, A.; Santangelo, G. Unexpected long-term population dynamics in a canopy-forming gorgonian coral following mass mortality. Mar. Ecol. Prog. Ser. 2009, 394, 195–200. [Google Scholar] [CrossRef]
  49. Lindsay, S.M. Frequency of injury and the ecology of regeneration in marine benthic invertebrates. Integr. Comparat. Biol. 2010, 50, 479–493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Wahle, C.M. Regeneration of injuries among Jamaican gorgonians: The roles of colony physiology and environment. Biol. Bull. 1983, 165, 778–790. [Google Scholar] [CrossRef] [PubMed]
  51. Castanaro, J.; Lasker, H.R. Colony growth responses of the Caribbean octocoral, Pseudopterogorgia elisabethae, to harvesting. Invertebr. Biol. 2003, 122, 299–307. [Google Scholar] [CrossRef]
  52. Cerrano, C.; Bavestrello, G. Medium-term effects of die-off of rocky benthos in the Ligurian Sea. What can we learn from gorgonians? Chem. Ecol. 2008, 24, 73–82. [Google Scholar] [CrossRef]
  53. Sánchez, J.A.; Lasker, H.R. Do multi–branched colonial organisms exceed normal growth after partial mortality? Proc. R. Soc. London. Ser. B Biol. Sci. 2004, 271 (Suppl. S3), S117–S120. [Google Scholar] [CrossRef]
  54. Loya, Y. Skeletal regeneration in a Red Sea scleractinian coral population. Nature 1976, 261, 490–491. [Google Scholar] [CrossRef]
  55. Riegl, B.; Riegl, A. Studies on coral community structure and damage as a basis for zoning marine reserves. Biol. Conserv. 1996, 77, 269–277. [Google Scholar] [CrossRef]
  56. Cerrano, C.; Arillo, A.; Azzini, F.; Calcinai, B.; Castellano, L.; Muti, C.; Valisano, L.; Zega, G.; Bavestrello, G. Gorgonian population recovery after a mass mortality event. Aquat. Conserv. 2005, 15, 147–157. [Google Scholar] [CrossRef]
  57. Ros, J.D.; Romero, J.; Ballesteros, E.; Gili, J.M. Diving in blue water. The benthos. In Western Mediterranean; Margalef, R., Ed.; Pergamon Press: Oxford, UK, 1985; pp. 233–295. [Google Scholar]
  58. Hrs-Brenko, M.; Legac, M. Inter-and intra-species relationships of sessile bivalves on the eastern coast of the Adriatic Sea. Nat. Croat. 2006, 15, 203. [Google Scholar]
  59. Basile, G.; Cerrano, C.; Radjasa, O.; Povero, P.; Zocchi, E. ADP-ribosyl cyclase and abscisic acid are involved in the seasonal growth and in post-traumatic tissue regeneration of Mediterranean sponges. J. Exp. Mar. Biol. Ecol. 2009, 381, 10–17. [Google Scholar] [CrossRef]
  60. Chimienti, G. Vulnerable forests of the pink sea fan Eunicella verrucosa in the Mediterranean Sea. Diversity 2000, 12, 176. [Google Scholar] [CrossRef]
  61. McFadden, C.S. Genetic and taxonomic relationships among Northeastern Atlantic and Mediterranean populations of the soft coral Alcyonium coralloides. Mar. Biol. 1999, 133, 171–184. [Google Scholar] [CrossRef]
  62. McFadden, C.S.; Donahue, R.; Hadland, B.K.; Weston, R. A molecular phylogenetic analysis of reproductive trait evolution in the soft coral genus Alcyonium. Evolution 2001, 55, 54–67. [Google Scholar] [CrossRef]
  63. Quintanilla, E.; Gili, J.M.; López-González, P.J.; Tsounis, G.; Madurell, T.; Fiorillo, I.; Rossi, S. Sexual reproductive cycle of the epibiotic soft coral Alcyonium coralloides (Octocorallia, Alcyonacea). Aquat. Biol. 2013, 18, 113–124. [Google Scholar] [CrossRef] [Green Version]
  64. Ten Hove, H.A. Different causes of mass occurrence in serpulids. Biol. Syst. Colonial Org. 1979, 11, 281–298. [Google Scholar]
  65. Ten Hove, H.A.; Van den Hurk, P. A review of fecent and fossil serpulid reefs; actuopalaeontology and the Upper Malm serpulid limestones in NW Germany. Geologie en Mijnbouw 1993, 72, 23–67. [Google Scholar]
  66. Connell, J.H.; Slatyer, R.O. Mechanisms of succession in natural communities and their role in community stability and or-ganization. Am. Nat. 1977, 111, 1119–1144. [Google Scholar] [CrossRef]
  67. Farrell, T.M. Models and mechanisms of succession: An example from a rocky intertidal community. Ecol. Monogr. 1991, 61, 95–113. [Google Scholar] [CrossRef]
  68. Denoual, D. Mortalité Massive de Gorgones Rouges (Paramuricea clavata) en Méditerranée Durant L’été 1999. Ph.D. Thesis, Ecole Nationale Vétérinaire de Toulouse—ENVT, Toulouse, France, 2004; 86p. [Google Scholar]
  69. Wahl, M. Marine epibiosis. I. Fouling and antifouling: Some basic aspects. Mar. Ecol. Prog. Ser. 1989, 58, 175–189. [Google Scholar] [CrossRef] [Green Version]
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Figure 1. The investigated area within the Tavolara–Punta Coda Cavallo MPA. Red spots indicate granitic shoals with the presence of Paramuricea clavata; yellow spots indicate the shoals considered in this study.
Figure 1. The investigated area within the Tavolara–Punta Coda Cavallo MPA. Red spots indicate granitic shoals with the presence of Paramuricea clavata; yellow spots indicate the shoals considered in this study.
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Figure 2. (a,b) The benthic community settled on the granitic shoals of the Tavolara Channel is mainly characterized by large sponges (Sarcotragus foetidus, Axinella species) and gorgonians (Eunicella verrucosa, Paramuricea clavata). (c,d) Diseased colonies showed a massive coenenchyme loss during the mass mortality of 2018. (e) Spawning and (f) recruits of P. clavata; (g) spawning of the parasitic soft coral Alcyonium coralloides.
Figure 2. (a,b) The benthic community settled on the granitic shoals of the Tavolara Channel is mainly characterized by large sponges (Sarcotragus foetidus, Axinella species) and gorgonians (Eunicella verrucosa, Paramuricea clavata). (c,d) Diseased colonies showed a massive coenenchyme loss during the mass mortality of 2018. (e) Spawning and (f) recruits of P. clavata; (g) spawning of the parasitic soft coral Alcyonium coralloides.
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Figure 3. (a-c) Paramuricea clavata forests showing a high level of epibiosis due to Hydrozoa carpet (Hy), false black coral Savalia savaglia (Bertoloni, 1819) (Ss), Filograna/Salmacina spp. (FS), and calcified branched Bryozoa Adeonella calveti (Aca). (d) Colonies recorded entangled in lost fishing gear and (e) totally uprooted.
Figure 3. (a-c) Paramuricea clavata forests showing a high level of epibiosis due to Hydrozoa carpet (Hy), false black coral Savalia savaglia (Bertoloni, 1819) (Ss), Filograna/Salmacina spp. (FS), and calcified branched Bryozoa Adeonella calveti (Aca). (d) Colonies recorded entangled in lost fishing gear and (e) totally uprooted.
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Figure 4. Percent of recurrence of the recorded species/OTUs with values greater than 10%, calculated based on the whole photographic dataset.
Figure 4. Percent of recurrence of the recorded species/OTUs with values greater than 10%, calculated based on the whole photographic dataset.
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Figure 5. The main epibionts recorded on Paramuricea clavata: (a) Hydrozoa turf (Hy), (b) large masses of Serpulidae Filograna/Salmacina spp. (FS), (c) Porifera Crella elegans (Ce), (d–h) complex epibiont communities composed of Porifera Dysidea fragilis (Df), D. perfistulata (Dp), and Pleraplysilla spinifera (Ps), parasitic Alcyonacea Alcyonium coralloides (Aco), Serpulidae Filograna/Salmacina spp., Bryozoa Adeonella calveti (Aca), Flustra sp. ((Fl) and Turbicellepora avicularis Ta), and Tunicata Aplidium undulatum (Au).
Figure 5. The main epibionts recorded on Paramuricea clavata: (a) Hydrozoa turf (Hy), (b) large masses of Serpulidae Filograna/Salmacina spp. (FS), (c) Porifera Crella elegans (Ce), (d–h) complex epibiont communities composed of Porifera Dysidea fragilis (Df), D. perfistulata (Dp), and Pleraplysilla spinifera (Ps), parasitic Alcyonacea Alcyonium coralloides (Aco), Serpulidae Filograna/Salmacina spp., Bryozoa Adeonella calveti (Aca), Flustra sp. ((Fl) and Turbicellepora avicularis Ta), and Tunicata Aplidium undulatum (Au).
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Figure 6. Percent of recurrence of the main species/OTUs showing different colonization strategies in relation to the diversity of the assemblage. (a) Hydrozoa is the main pioneer species and remains dominant at all the colonization phases; (b–i) branched Bryozoa (Adeonella calveti, Flustra sp., and Turbicellepora avicularis), Serpulidae Filograna/Salmacina spp., and Porifera Dysidea fragilis and Crella elegans settled immediately after Hydrozoa and quickly increased according to the community richness. (j) D. perfistulata, Pleraplysilla spinifera, and Alcyonium coralloides need a certain degree of diversity of the assemblage for their settling (>4 species/OTUs); after that, their growth is continuous.
Figure 6. Percent of recurrence of the main species/OTUs showing different colonization strategies in relation to the diversity of the assemblage. (a) Hydrozoa is the main pioneer species and remains dominant at all the colonization phases; (b–i) branched Bryozoa (Adeonella calveti, Flustra sp., and Turbicellepora avicularis), Serpulidae Filograna/Salmacina spp., and Porifera Dysidea fragilis and Crella elegans settled immediately after Hydrozoa and quickly increased according to the community richness. (j) D. perfistulata, Pleraplysilla spinifera, and Alcyonium coralloides need a certain degree of diversity of the assemblage for their settling (>4 species/OTUs); after that, their growth is continuous.
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Figure 7. (a) Percent of recurrence of the main species/OTUs according to the diversity of the epibiont community. (b) The average percentage of the gorgonian surface involved in epibiosis shows a progressive increase according to the diversity of the epibiont community, as shown by the correlation line (r: 0.98).
Figure 7. (a) Percent of recurrence of the main species/OTUs according to the diversity of the epibiont community. (b) The average percentage of the gorgonian surface involved in epibiosis shows a progressive increase according to the diversity of the epibiont community, as shown by the correlation line (r: 0.98).
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Figure 8. Examples of different evolutions of the coenenchyme lesions and consequent epibiosis due to thermal stress. (a–d) Two cases of damage on small portions of branches were recovered after two years. (e–f) Extensive lesions were not recovered by the gorgonian, and epibiosis developed very quickly, involving the entire colony. (g–j) A colony involved in the thermal disease of 2018 showed minor damage severity changes across four years.
Figure 8. Examples of different evolutions of the coenenchyme lesions and consequent epibiosis due to thermal stress. (a–d) Two cases of damage on small portions of branches were recovered after two years. (e–f) Extensive lesions were not recovered by the gorgonian, and epibiosis developed very quickly, involving the entire colony. (g–j) A colony involved in the thermal disease of 2018 showed minor damage severity changes across four years.
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Figure 9. Development of epibiosis linked to lost fishing line entanglement. (a,b) Quick colonization (47 days) by Porifera and Bryozoa. (c–e) Increasing complexity of the epibiont community on a gorgonian entangled in a line (arrows) for 54 months; note that the sponge Dysidea fragilis appears later. (f–h) The settlement of Filograna/Salamacina spp. covered almost the entire naked parts (arrows) of a colony after the summertime of 2018. (i,j) The settling of calcified organisms stops the movement of the entangled lines, thus preventing further damage. (k–m) A dead colony totally covered by sponges and encrusting coralline algae after five years.
Figure 9. Development of epibiosis linked to lost fishing line entanglement. (a,b) Quick colonization (47 days) by Porifera and Bryozoa. (c–e) Increasing complexity of the epibiont community on a gorgonian entangled in a line (arrows) for 54 months; note that the sponge Dysidea fragilis appears later. (f–h) The settlement of Filograna/Salamacina spp. covered almost the entire naked parts (arrows) of a colony after the summertime of 2018. (i,j) The settling of calcified organisms stops the movement of the entangled lines, thus preventing further damage. (k–m) A dead colony totally covered by sponges and encrusting coralline algae after five years.
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Table
Table 1. Species/OTUs found on Paramuricea clavata and their percent of recurrence, calculated based on the whole photographic dataset. (*) Vagile species and taxa with a recurrence of <10% were not taken into account for the formal analysis.
Table 1. Species/OTUs found on Paramuricea clavata and their percent of recurrence, calculated based on the whole photographic dataset. (*) Vagile species and taxa with a recurrence of <10% were not taken into account for the formal analysis.
Species/OTUsRecurrence
(%)		Species/OTUsRecurrence
(%)
Algae Anellida
Crustose Corallinales2.5Filograna/Salmacina spp.33.3
Flabellia petiolata0.2Serpulidae5.6
Valonia sp.0.2Bryozoa
Porifera Adeonella calveti52.3
Anchinoe tenacior0.2Beania magellanica0.9
Crella elegans10.4Cellaria salicornioides0.5
Dysidea avara0.2Flustra sp.9.6
Dysidea fragilis43.8Pentapora fascialis1.6
Dysidea perfistulata10.2Turbicellepora avicularis26.9
Haliclona mediterranea1.4Encrusting Bryozoans1.4
Ircinia variabilis0.2Crustacea
Oscarella lobularis2.5Periclimenes scriptum *0.5
Pleraplysilla spinifera9.9Echinodermata
Terpios fugax2.8Antedon mediterranea *0.2
Encrustig Sponges14.4Astrospartus mediterraneus *0.2
Cnidaria Chordata
Hydrozoa91.9Aplidium undulatum7.9
Alcyonium coralloides22.9Clavelina dellavallei1.6
Epizoanthus species0.2Clavelina oblonga0.9
Mollusca Didemnidae 0.9
Pteria hirundo0.7Pycnoclavella communis0.7
Calliostoma conulus *0.2
Flabellina ischitana *0.5
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Canessa, M.; Amedeo, I.; Bavestrello, G.; Panzalis, P.; Trainito, E. The Diversity, Structure, and Development of the Epibiont Community of Paramuricea clavata (Risso, 1826) (Cnidaria, Anthozoa). Water 2023, 15, 2664. https://doi.org/10.3390/w15142664

AMA Style

Canessa M, Amedeo I, Bavestrello G, Panzalis P, Trainito E. The Diversity, Structure, and Development of the Epibiont Community of Paramuricea clavata (Risso, 1826) (Cnidaria, Anthozoa). Water. 2023; 15(14):2664. https://doi.org/10.3390/w15142664

Chicago/Turabian Style

Canessa, Martina, Ilaria Amedeo, Giorgio Bavestrello, Pier Panzalis, and Egidio Trainito. 2023. "The Diversity, Structure, and Development of the Epibiont Community of Paramuricea clavata (Risso, 1826) (Cnidaria, Anthozoa)" Water 15, no. 14: 2664. https://doi.org/10.3390/w15142664

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