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Article

Preliminary Assessment of Macrobenthos Associated with Red Coral Corallium rubrum (Linnaeus, 1758) Populations in the Northeastern Ionian Sea

1
Department of Biosciences Biotechnologies and Environment, University of Bari Aldo Moro, Via Orabona, 4, 70125 Bari, Italy
2
Regional Nature Reserve “Palude la Vela”, 74121 Taranto, Italy
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2024, 12(10), 1825; https://doi.org/10.3390/jmse12101825
Submission received: 15 September 2024 / Revised: 8 October 2024 / Accepted: 11 October 2024 / Published: 13 October 2024
(This article belongs to the Special Issue Advances in Marine Biodiversity and Conservation)

Abstract

:
The taxonomic composition, structure, and distribution patterns of the macrobenthos associated with Corallium rubrum were studied along the coast of Taranto (Ionian Sea), together with the main features of their red coral population. Underwater video transects were performed by professional divers at three sites in correspondence with coralligenous formations at depths from 50 to 65 m. The results revealed a patchy distribution of red coral, with colonies predominantly located in cavities on sub-vertical cliffs and large boulders. Biometric analysis indicated that young colonies predominated at all sites, while older colonies were lacking, likely because of illegal harvesting. The lower density values were recorded at S1, while S2 and S3 presented higher values. A total of 76 taxa were recorded. S1, the shallowest site, showed a prevalence of calcareous algae, while S2 and S3 showed a greater abundance of filter-feeding invertebrates (Porifera and Cnidaria) with the highest presence of Porifera at S3. The results emphasize the heterogeneity of the macrobenthos together with the high vulnerability of the red coral population, highlighting the necessity of site-specific conservation strategies to contribute to the conservation and management of benthic ecosystems in the northern Ionian Sea.

1. Introduction

Marine benthic communities provide various ecosystem services essential for ecological balance, including carbon cycling processes, secondary production, organic matter enrichment, and habitat provision [1,2,3]. By maintaining these functions, benthic communities support food provision (i.e., fisheries), shelter, and biodiversity preservation [4,5] and contribute to the overall resilience of marine ecosystems.
Despite their importance, various anthropogenic pressures, such as overfishing, pollution, physical habitat disturbance [6], and climate change [7], are harming marine benthic communities, particularly by reducing the abundance and size of targeted species [8]. Thus, in recognition of the urgent need to mitigate these impacts on a global scale and as a critical step towards the conservation and management of marine ecosystems, thousands of marine protected areas (MPAs) have been designated in recent years, currently covering 8.2% of oceans worldwide [9]. In the Mediterranean, a similar percentage (8.33%) is under the official designation of a protected statute [10].
MAPs “have been reserved by law or other effective means to protect part or all of the enclosed environment, together with its overlying water and associated flora and fauna” [11]. In Europe, the establishment of marine protected areas (MPAs) has been driven by various legislative and regulatory frameworks, including EU directives such as the Barcelona Convention [12], the Habitats Directive [13], and the Marine Strategy Framework Directive [14]. When effectively designed and managed, MPAs have the potential to enhance ecological resilience against the numerous anthropogenic impacts. However, despite the critical role that marine benthic assemblages play in maintaining ecosystem functioning, they have not been a primary consideration in the designation of a significant portion of MPAs. Indeed, MPAs have predominantly been selected based on the presence of charismatic species such as fish, turtles, cetaceans, and seals, while data on benthic invertebrates have been largely overlooked. This has led to gaps in the selection, management, and monitoring of MPAs, where key aspects essential for the effective conservation of benthic ecosystems, such as the exclusive presence of species and habitat of conservation interest, remain underrepresented [15]. For example, Klein et al. [16] showed in their gap analysis that several major invertebrate phyla, such as Porifera, Cnidaria, Mollusca, Arthropoda, and Echinodermata had less than 10% of their range represented within MPAs.
Along the Apulian coast (Southern Italy), three marine protected areas (MPAs) have already been established. The local government has identified the Taranto area as a priority for the creation of an additional MPA, as outlined in the national framework law on protected areas (L. 394/91), proposing the “Isole Cheradi e Mar Piccolo” MPA. Before the boundaries of this upcoming marine protected area are definitively outlined, it is crucial to develop a comprehensive understanding of the structure and ecological condition of the existing macrobenthic communities to inform effective conservation and management strategies.
The coasts of Taranto (Ionian Sea) represent a typical situation in which the marine ecosystem is exposed to different anthropogenic activities, including sewage output, industrial activities, heavy naval traffic, and fishing, particularly trawling. Small-scale fishing activity is also documented by the presence of abandoned fishing gear (gillnets, longlines, and anchor lines from small boats) on the seabed, which is capable of continuing to produce an impact on the benthic community, including red coral [17]. Trawling fishing is conducted far from the coastline (beyond 3 nm, according to local regulations) and does not impact the coastal benthic communities. Although several studies have been carried out on the benthic communities in this area, most of them have focused on the Mar Grande and Mar Piccolo of Taranto [18,19,20,21,22,23,24,25,26,27,28,29,30,31,32]. Apart from a few studies [33,34,35,36], the surroundings remain relatively understudied. Most studies are quite dated, particularly those focusing on benthic biocenosis [33,36], with more recent efforts concentrating on bathyal benthopelagic fauna [34] and sponge communities associated with Apulian coralligenous formations [35]. The Taranto coasts have received fewer scientific contributions regarding coralligenous outcrops when compared with other areas of southern Italy [37,38,39,40], where the megabenthos have been well characterized.
Preliminary observations on this region [41,42] indicate a high biodiversity of benthic organisms, including sponges, corals, and macroalgae, which form complex and productive habitats. Moreover, the presence of red coral (Corallium rubrum (Linnaeus, 1758)), one of the most representative species of coralligenous habitats [43,44,45], has recently been recorded [46]. Over the past 15 years, the distribution of red coral populations along the Italian coasts has become better-understood thanks to recent research programs focusing on mesophotic and bathyal benthic communities [2,37,46,47,48,49,50,51]. In 2018, a dedicated project on Apulian red coral, funded by the Apulia Region (POR PUGLIA FESR-FSE 2014-2020, Project n. A0605.8), provided the first opportunity to investigate the distribution and conservation status of the red coral local population [46].
The present study aimed to assess the macrobenthos associated with C. rubrum at three sites along the coast of Taranto (Ionian Sea). The composition and distribution of macrobenthos, together with the main features of the red coral population, were investigated to gather essential data that will contribute to the conservation and management of benthic ecosystems in the northern Ionian Sea.

2. Materials and Methods

2.1. Study Area

The study area was located along the NW Ionian Sea (central Mediterranean Sea), which extends from Capo d’Otranto to Capo Passero along a coastline of about 1000 km and across an area of approximately 16,500 km2 in a depth range between 10 and 800 m (Figure 1). From a hydrographic point of view, the Ionian Sea is characterized by a complex system of water circulation in surface and deep layers [52], showing a general cyclonic circulation markedly influenced by the cold, dense deep-water masses of the Adriatic Sea flowing in through the Otranto Channel. Particularly in the study area, the coastal currents follow a seasonal pattern, flowing in an NW-SE direction from autumn to winter and reversing to an SE-NW direction in spring and summer [53].
The investigated area is characterized by a low rocky coastline with deep inlets that shelter small sandy beaches. The seabed maintains a depth of up to 25 m for approximately 0.5 nautical miles from the coast, sloping downward to a sandy bottom at around 70 m depth. The coralligenous develops on a cliff, on horizontal platforms, or overhangs at the base of the cliff. Along this slope, three sites (Figure 1, Table 1) were selected based on preliminary investigations about the presence of Corallium rubrum colonies. Site 1 (S1) has a rocky bottom with a cliff that stretches gradually from 38 to 52 m, characterized by large blocks of coralligenous and numerous cavities. Site 2 (S2) consists of large coralligenous boulders, spaced approximately 10–15 m apart and aligned parallel to the coast, arising from a sandy seabed that reaches a depth of nearly 65 m. Site 3 (S3) has a rocky seabed with coralligenous formations developing along a cliff descending to a depth of 60 m and characterized by ravines and fractures.

2.2. Megabenthos Characterization

At each site, two horizontal transects were established along the vertical sections of the cliff, where Corallium rubrum colonies were present. A remotely operated vehicle (ROV) was used to perform preliminary exploratory surveys to identify the most suitable location for the video recording. The main characteristics of the investigated sites are reported in Table 1. Professional divers, equipped with high-definition video cameras (Sony XDCAM Full HD 4K) and two lasers for metric reference, conducted 20 m long video transects to study the red coral population, which is distributed in patches along vertical cliffs approximately 200 m long. Videos were recorded at a distance of 50 cm from the vertical part of the surface to ensure uniform data collection.
The characterization of the macrobenthos present at each study site was conducted through the analysis of the video transects recorded at each site. From each video, a total of 20 frames were randomly extracted and analyzed to identify taxa at the lowest possible taxonomic level. Specimens were identified by expert taxonomists affiliated with the research group using private image databases. The percentage coverage of each of the benthic species present was then estimated by using PhotoQuad software V1.4 (Mytilene, Greece) [54].

2.3. Red Coral Population Characterization

Each video was analyzed using the open-source software ImageJ (IJ 1.46r) to assess the main features of the red coral population. The red coral density at each site was determined by counting the colonies present within the frame of the video footage, using laser pointers set 10 cm apart as a metric reference for accurate measurements. Additionally, 20 red coral colonies were collected by professional divers at each site for biometric data yield and to assess the main morphological parameters. For each colony, the following measurements were collected: (1) basal diameter, measured with a caliper, 1 cm from the base, following the method of García-Rodríguez and Massó [55]; and (2) the branching pattern of intact colonies, calculated as the number of branches of different orders, according to Brazeau and Lasker [56].

2.4. Data Analysis

The analysis of the megabenthic assemblages was based on the matrix of the presence/absence of species at each studied site, from which the relative contribution of each taxon to the total number of species per site was obtained. Moreover, a quantitative percentage matrix of substrate coverage was also created from the averaged percent cover quantified over all images, from which the relative abundance of benthic taxa was calculated in a plot. The non-parametric Kruskal–Wallis test was used to assess for significant differences in means, followed by a post-hoc Dunn’s Test for multiple comparisons, with p-values adjusted using the Bonferroni correction.
Benthic assemblage multivariate data were analyzed using Canonical Analysis of Principal Coordinates (CAP) and permutational multivariate analyses of variance with the PERMANOVA [57] add-on in PRIMER v6 [58]. Dissimilarity matrices based on the Bray-Curtis measure of square-root transformed relative abundances were generated for the analyses. The taxa responsible for multivariate patterns were overlaid on the plot as vectors.

3. Results

3.1. Megabenthos Features

A total of 76 macrobenthic taxa belonging to 11 phyla were detected, with 65 taxa identified at the species level (Table S1). Phylum Porifera was highly represented (32 taxa), followed by Cnidaria (11 taxa). S1 showed the highest number of identified taxa (59), followed by S3 (52) and S2 (48). The detailed distribution of megabenthic taxa at each site is shown in Figure 2.
Regarding coverage values, overall, Porifera had the highest coverage mean (33%). Rhodophyta (24%) and Cnidaria (19%) also showed high values of substrate coverage in the studied sites. Lower values were found for Chlorophyta (4%) and Bryozoa (3%), while Annelida, Echinodermata, and Chordata constituted the remaining animal fraction (Figure 3).
S1 has the highest coverage of macroalgae (38%) and a balanced distribution of Porifera (24%) and Cnidaria (22%). S2 has similar coverage values of Porifera (27%) and macroalgae (28%) and presents lower Cnidaria and Annelida coverage values. S3 shows a high coverage of Porifera (45%) and Cnidaria (25%). Bryozoans and echinoderms are equally represented in all the studied sites. Chlorophyta presents the highest coverage in S1 and S2, with S3 showing significantly lower coverage (Figure 4).
The Canonical Analysis of Principal coordinates (CAP) used to visualize the differences in species composition among the study sites based on the benthic species present presented three distinct clusters (Figure 5) corresponding to the three study sites: S1 (cyan triangles), S2 (orange squares), and S3 (pink circles). At S3, points are clustered on the left side of the plot, indicating a distinct community composition. Leptopsammia/Cladopsammia complex, Suberitidae sp., Dendroxea lenis, and Haliclona fulva are more associated with this site, forming sponge facies, while Peyssonnelia rubra and Lithophyllum are instead more associated with S1. Finally, Axinella verrucosa, algal turf, and ECR (encrusting calcified rhodophytes) are associated with S2. The global Permanova revealed significant differences across sites (pseudoF = 9.61, p = 0.001), and pairwise comparisons showed that all of them were statistically significant (p = 0.001).

3.2. Red Coral Population Features

Corallium rubrum colonies were patchily distributed at all the sites studied, mainly occupying ravines and cavities at depths ranging from 50 to 60 m. The species was also found on large boulders along a sandy slope extending to a depth of around 65 m.
At Site 1 (S1) (Figure 6A), the red coral colonies were mostly concentrated at a depth of 51 m.
At Site 2 (S2), Corallium rubrum colonies were mainly observed at a depth of 56 m in cavities of large boulders aligned parallel to the coast (Figure 6B).
Site 3 (S3) is characterized by numerous ravines and fractures hosting red coral colonies (Figure 6C), mainly found at a depth of 54 m.
In all sites, most of the basal diameter of the colonies had values between 5 and 10 mm (Figure 7a), and more than 75% of the colonies showed values below the minimum harvesting size (10 mm of basal diameter). The basal diameter reaches a maximum of 13 mm at S1, while it is minor at S3 (10.5 mm) and S2 (12 mm). The average basal diameter was higher at S1 (8.9 mm), followed by S3 (7.5 mm) and S2 (7.1 mm) (Figure 7b). These differences, however, were not statistically significant (p = 0.2).
The density of Corallium rubrum colonies averages 185.4/m2 and 186.5/m2 at S2 and S3, respectively (Figure 8). At S1, instead, colonies showed a low density of colonies (85/m2). These differences were statistically significant (H = 11.95, p = 0.002). Post-hoc Dunn’s tests revealed that all pairwise comparisons between the sites were also statistically significant (S1 vs. S2: p = 0.008, S1 vs. S3: p = 0.008 and S2 vs. S3: p = 0.007).
The branching pattern showed that at S2 and S3 third-order branches prevail, with an important presence of colonies (31%) with fourth-order branches at S3. At S1, the branching distribution is more homogeneous, with a slight increase in the percentage of colonies having first-order branching (Figure 9).

4. Discussion

Understanding both the dynamics and structure of bioconstruction-associated communities is a key element in the field of conservation biology and it is fundamental for identifying, planning, and protecting marine areas [59]. In this context, the current study, though preliminary, provides valuable insights into the variability of coralligenous communities in the Ionian Sea off Taranto, offering an extensive dataset that will allow long-term monitoring and assessment of epibenthic communities on coralligenous bioconstructions along the Ionian Coast.
These results emphasize the importance of conducting detailed studies, even on a small scale, considering environmental features that should be integrated into MPAs planning (e.g., the nature of the substrate, the characteristics of the communities, the presence of species of conservation interest, the degree of maturity of the communities and their heterogeneity, the distribution of the biocenoses). The variability and the state of conservation exhibited in the investigated red coral population offers information for direct resource management for commercial purposes while also underscoring the necessity for administrators to include in MPAs deep zones that exhibit high levels of biodiversity and ecological complexity.
The megabenthos found along the northern coast of the Ionian Sea are typical of coralligenous habitats [35,43,44], developing on a biogenic substrate realized by calcareous red algae. Invertebrates, even contributing significantly, do not act as structural components of the bioconstructions. At comparable depths, in other areas of Apulia characterized by higher turbidity and nutrients, invertebrates (two scleractinians species and one bivalve species) assume a main structural role leading to the creation of animal-based mesophotic bioconstructions [37,40,60].
The coralligenous bottoms form here a heterogeneous mosaic that varies on a small spatial scale, allowing multiple assemblages to coexist in a reduced space, a common scenario across all the Mediterranean bioconstructions [44,61,62]. According to Montefalcone et al. [45], these habitats can show a dominance of invertebrate species that, although not structuring, can form real specific facies (e.g., sponges, bryozoans, and anthozoans facies). Many of these taxa are often overlooked in MPA planning [16].
The red coral constitutes a typical facies of coralligenous habitats, widely distributed throughout circalittoral semi-dark caves and overhangs all over the Mediterranean Sea [44,46]. A recent study by Toma et al. [46] investigated the occurrence, relative abundance, and habitat characteristics of Corallium rubrum along the Italian coasts, reporting that red coral colonies settle both on coralligenous concretions and rocky substrates, with a preference for biogenic sub-vertical habitats. According to the authors, along the Apulian coasts, the occurrence of red coral populations was fragmented but characterized by relatively high values of density, forming at some places real facies (e.g., Otranto and Santa Maria di Leuca). At Taranto, the C. rubrum population predominantly develops on coralligenous concretions within cavities located on sub-vertical cliffs and overhangs. The red coral densities observed are relatively high compared with some Italian overexploited populations [46]. The coverage values, on the contrary, are rather low not justifying a real facies. Among the three study sites, the lowest density was observed at S1, where the algal component was more prevalent. In contrast, the red coral densities at S2 and S3 were similar, with an average of around 185 colonies/m2.
Red coral is a very slow-growing species, with the minimum harvestable size reached in approximately 30–35 years [55,63,64]. The general average basal diameter recorded in this study corresponds to an age of 21–26 years, considering an annual growth rate (increase in basal diameter) of approximately 0.33 mm/year [63,64,65,66,67], comparable to younger red coral populations in deeper waters [68]. Most colonies were below the legal harvest size (medium-sized individuals with basal diameters <10 mm) and had a branching pattern below 4° order. At S3, 31% and 10% of the colonies exhibit fourth and fifth-order branches, respectively, indicating a more mature population [67] that appears to be a little less affected by harvesting pressures.
The absence of larger, older colonies with higher reproductive output [69] is often associated with populations subjected to selective harvesting for commercial purposes [68]. Local divers have reported illegal harvesting of red coral in the Taranto area, including colonies below the minimum harvest size. Currently, however, the local Port Authority does not declare any active operating license for the underwater collection of red coral. The lack of data on selective harvesting and small-scale artisanal and professional fishing in the area makes it difficult to assess the past or ongoing impact of these activities on local red coral populations. The presence of abandoned fishing gear, although not abundant, denotes a persistent but unquantifiable impact on these populations.
Environmental factors can explain the heterogeneity of the macrobenthos in general. Since the general exposure and current patterns of the analyzed populations have a regular direction and intensity in the area in relation to the seasons, depth (as a proxy for the light intensity) and substrate inclination could act as key ecological drivers. Differences among sites were also evident in the composition of the fauna associated with the red coral. The CAP analysis revealed distinct benthic community compositions at the three sites. S1, the shallowest, showed a higher prevalence of calcareous algae and a lower presence of mesophotic invertebrate species. In contrast, S2 and S3 were dominated by a greater abundance of filter-feeding animals. Overall, S3 exhibited a unique community structure dominated by Porifera and Cnidaria, with distinct sponge facies (MC1.511b Facies with small sponges [45]), with a lower contribution of algae in both species number and coverage.
The great heterogeneity of the assemblages highlights the need for site-specific conservation and management strategies to protect these diverse marine habitats. Effective monitoring and assessment programs for MPAs require accurate baseline data, which includes identifying key species of interest and major ecological relationships [70,71].
The biometric analysis of red coral colonies from the studied sites presents a worrying picture for the Corallium rubrum populations in the northern Ionian Sea. The exploitation of this resource along the Apulian coast has been going on for decades, often in an illegal way, and has significantly reduced the size and spatial distribution of larger colonies. Immediate protection of these populations and their associated fauna is crucial, and the establishment of the “Isole Cheradi e Mar Piccolo” MPA is urgently needed to preserve these vulnerable ecosystems.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse12101825/s1, Table S1: Checklist of the benthic taxa recorded at each site (* = presence of species).

Author Contributions

Conceptualization, C.P., G.C. and M.M.; methodology, C.P., G.A.G. and M.D.; formal analysis, G.A.G. and C.P.; resources, M.M.; data curation, C.P. and G.A.G.; writing—original draft preparation, G.A.G. and M.M.; writing—review and editing, C.P., G.A.G. and M.M.; project administration, M.M.; funding acquisition, G.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by POR PUGLIA FESR-FSE 2014–2020, Asse VI “Tutela dell’Ambiente e promozione delle risorse naturali e culturali–Azione 6.5–6.5.1 “Interventi per la tutela e valorizzazione della biodiversità terrestre e marina”. “Piano di gestione ai fini della conservazione del corallo rosso pugliese”. Project n. A0605.8.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.

Acknowledgments

The authors wish to thank Riccardo Cingillo, Massimiliano Piccolo, Filippo Panico and the entire Murena Diving staff for the logistical help in performing underwater videos.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Map of the study area along the Ionian Sea, with the three defined sites: S1, S2, and S3.
Figure 1. Map of the study area along the Ionian Sea, with the three defined sites: S1, S2, and S3.
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Figure 2. Relative contribution (%) of each taxon in each study site.
Figure 2. Relative contribution (%) of each taxon in each study site.
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Figure 3. Total percentage of coverage (mean ± SD) of the taxa recorded during the study.
Figure 3. Total percentage of coverage (mean ± SD) of the taxa recorded during the study.
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Figure 4. Relative contribution (%) of each taxon to the total percentage of substrate coverage in each study site.
Figure 4. Relative contribution (%) of each taxon to the total percentage of substrate coverage in each study site.
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Figure 5. Canonical Analysis of Principal coordinates (CAP) showing the differences in community composition among the study sites.
Figure 5. Canonical Analysis of Principal coordinates (CAP) showing the differences in community composition among the study sites.
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Figure 6. Examples of red coral colonies patchily distributed at S1 (A), S2 (B), and S3 (C).
Figure 6. Examples of red coral colonies patchily distributed at S1 (A), S2 (B), and S3 (C).
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Figure 7. Basal diameter of Corallium rubrum populations per site. (a) Size-class distribution of the basal diameter of the colonies. (b) Distribution of basal diameter measures in each site.
Figure 7. Basal diameter of Corallium rubrum populations per site. (a) Size-class distribution of the basal diameter of the colonies. (b) Distribution of basal diameter measures in each site.
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Figure 8. Density of Corallium rubrum populations per site.
Figure 8. Density of Corallium rubrum populations per site.
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Figure 9. Branching pattern of red coral colonies at each site. Ordinal numbers indicate the order of branching.
Figure 9. Branching pattern of red coral colonies at each site. Ordinal numbers indicate the order of branching.
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Table 1. Main characteristics of the investigated sites.
Table 1. Main characteristics of the investigated sites.
SiteMaximum DepthBottom MorphologyTransects Depth
S152 mCliff with ravines51 ± 1 m
S265 mBoulder ridge 4 m high56 ± 1 m
S360 mCliff with ravines and fractures54 ± 1 m
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Mercurio, M.; Corriero, G.; Giménez, G.A.; Dadamo, M.; Pierri, C. Preliminary Assessment of Macrobenthos Associated with Red Coral Corallium rubrum (Linnaeus, 1758) Populations in the Northeastern Ionian Sea. J. Mar. Sci. Eng. 2024, 12, 1825. https://doi.org/10.3390/jmse12101825

AMA Style

Mercurio M, Corriero G, Giménez GA, Dadamo M, Pierri C. Preliminary Assessment of Macrobenthos Associated with Red Coral Corallium rubrum (Linnaeus, 1758) Populations in the Northeastern Ionian Sea. Journal of Marine Science and Engineering. 2024; 12(10):1825. https://doi.org/10.3390/jmse12101825

Chicago/Turabian Style

Mercurio, Maria, Giuseppe Corriero, Guadalupe Anahi Giménez, Marco Dadamo, and Cataldo Pierri. 2024. "Preliminary Assessment of Macrobenthos Associated with Red Coral Corallium rubrum (Linnaeus, 1758) Populations in the Northeastern Ionian Sea" Journal of Marine Science and Engineering 12, no. 10: 1825. https://doi.org/10.3390/jmse12101825

APA Style

Mercurio, M., Corriero, G., Giménez, G. A., Dadamo, M., & Pierri, C. (2024). Preliminary Assessment of Macrobenthos Associated with Red Coral Corallium rubrum (Linnaeus, 1758) Populations in the Northeastern Ionian Sea. Journal of Marine Science and Engineering, 12(10), 1825. https://doi.org/10.3390/jmse12101825

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