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Composition and abundance of octocorals in the Sea of Marmara, where the Mediterranean meets the Black Sea

Eda N. Topçu 1,2, Bayram Öztürk 1,2

1 Istanbul University Fisheries Faculty, Ordu cad No 200 Laleli, 34470 Istanbul, Turkey. E-mail: edatopcu@istanbul.edu.tr
2 Turkish Marine Research Foundation, No 10, Beykoz, 81650, Istanbul, Turkey.

Summary: Species composition and abundance of octocoral assemblages were investigated in the Sea of Marmara, which forms the connection between the Mediterranean and the Black Seas, two semi-enclosed seas with peculiar oceanographic conditions. Fourteen octocoral species were collected in the saline layer of the Marmara Sea (20-40 m), with a mean coral abundance of 5.21±5.11 colonies m–2 (mean ± SD) calculated from a total of 1390 colonies counted in transects. In spite of severe anthropogenic disturbances, dense assemblages of corals/gorgonians were observed during this study. The coralligenous communities—one of the most valuable structures of the Mediterranean Sea—harbored either Eunicella cavolini or Paramuricea macrospina as the dominant gorgonian in the Marmara Sea. Furthermore, the gorgonian assemblages of the Marmara Sea differed from those of the Mediterranean in their high abundance of P. macrospina and Spinimuricea klavereni, two species rarely encountered in the Mediterranean Sea at the studied depth range. The factors behind the observed differences are discussed in regard to the particular oceanographic conditions of the Marmara Sea. Finally, we revised the main threats to corals/gorgonians in the Marmara Sea and provided some insights on management recommendations for coral conservation in this area.

Keywords: octocoral; soft coral; gorgonian; sea pen; coralligenous; Marmara Sea.

Composición y abundancia de especies de octocorales en el mar de Mármara, donde el Mediterráneo confluye con el mar Negro

Resumen: En este trabajo se ha analizado la composición y abundancia de especies de octocorales de las comunidades bentónicas del mar de Mármara. Este mar conecta el Mediterráneo y el mar Negro, dos mares semicerrados con condiciones oceanográficas particulares. En la capa salina del mar de Mármara (20-40 m) se encontraron un total de catorce especies de octocorales. La abundancia media de colonias de las diferentes especies se obtuvo mediante la realización de transectos. En total se censaron 1390 colonias resultando en una abundancia media de corales de 5.21±5.11 colonias m–2 (media±DE). A pesar de que el mar de Mármara está sometido a severas perturbaciones antropogénicas, se observaron densas agregaciones de corales/gorgonias durante este estudio. En las comunidades de coralígeno—una de las comunidades más emblemáticas del mar Mediterráneo—que se desarrollan en el mar de Mármara están dominadas por dos especies de gorgonias Eunicella cavolini o Paramuricea macrospina. Además las agregaciones de gorgonias del mar de Mármara diferían de las del Mediterráneo por su alta abundancia de P. macrospina y Spinimuricea klavereni, dos especies raramente encontradas en el mar Mediterráneo en el rango de profundidades estudiado. Los factores que podrían explicar los resultados se discuten teniendo en cuenta las condiciones oceanográficas particulares del mar de Mármara y las principales amenazas para los corales/gorgonias en el mar de Mármara. Finalmente, ofrecemos algunas recomendaciones de gestión para la conservación de los corales en esta área.

Palabras clave: octocoral; coral blando; gorgonia; pluma de mar; coraligenos; mar de Mármara.

Citation/Como citar este artículo: Topçu E.N., Öztürk B. 2015. Composition and abundance of octocorals in the Sea of Marmara, where the Mediterranean meets the Black Sea. Sci. Mar. 79(1): 123-135. doi: http://dx.doi.org/10.3989/scimar.04120.09A

Editor: J. Garrabou.

Received: July 3, 2014. Accepted: October 27, 2014. Published: January 14, 2015.

Copyright: © 2015 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Commercial Lisence (by-nc) Spain 3.0.

Contents

Summary
Resumen
Introduction
Materials and methods
Results
Discussion
Acknowledgements
References

INTRODUCTIONTop

Octocorals in the Mediterranean Sea constitute a small group of 51 species (Vafidis in Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS One 5: e11842.: Table S13) but are widespread from shallow to significant depths (Freiwald et al. 2009Freiwald A., Beuck L., Rüggeberg A., et al. 2009. The white coral community in the central Mediterranean Sea revealed by ROV surveys. Oceanography 22: 58-74., Mastrototaro et al. 2010Mastrototaro F., D’Onghia G., Corriero G., et al. 2010. Biodiversity of the white coral bank off Cape Santa Maria di Leuca (Mediterranean Sea): An update. Deep Sea Res. PT II 57: 412-430.) on both hard and soft substrates (Aguilar 2004Aguilar R. 2004. The corals of the Mediterranean. Oceana, Fundación Biodiversidad, Madrid, 86 pp.) and are important components of the valuable Mediterranean coralligenous communities (Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. 44: 123-195.). Among them, some long-living species are considered as ‘‘ecosystem engineers’’ (Jones et al. 1994Jones C.J., Lawton J.H., Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69: 373-386., Ponti et al. 2014Ponti M., Perlini R.A., Ventra V., et al. 2014. Ecological Shifts in Mediterranean Coralligenous Assemblages Related to Gorgonian Forest Loss. PLoS ONE 9(7): e102782) in Mediterranean marine hard-bottom communities, with significant effects on the structure, biomass and biodiversity of coralligenous communities (Ballesteros 2006Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. 44: 123-195.). Although scientific studies and conservation efforts focus increasingly on octocorals and mainly gorgonians, our knowledge on their presence and distribution in the eastern Mediterranean is yet insufficient (Salomidi et al. 2009Salomidi M., Smith C., Katsanevakis S., et al. 2009. Some observations on the structure and distribution of gorgonian assemblages in the eastern Mediterranean Sea. In: UNEP – MAP – RAC/SPA, Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. Tabarka, Tunis, pp 242-245.).

Octocoral species from the Marmara Sea have been previously reported (Demir 1954Demir M. 1954. Boğaz ve Adalar Sahillerinin omurgasız dip hayvanları. Istanbul Univ, Faculty of Science, Hydrobiol. Res. Inst. Publ. 2A: 1-654 (in Turkish)., Öztürk and Bourguet 1990Öztürk B., Bourguet J.P. 1990. Données préliminaires sur le corail noir de la Mer de Marmara (Turquie) Gerardia savaglia (Bertolini, 1819). Ist. Univ. J. of Fish. 4: 45-48., Topçu and Öztürk 2013Topçu E.N., Öztürk B. 2013. Octocoral diversity of Balıkçı Island, the Marmara Sea. J. Black Sea/Medit. Environ. 19: 46-57.) but studies on the abundance and distribution of the species in the Marmara Sea have been rarely addressed. Although the Marmara Sea is connected to the Mediterranean via the Çanakkale Strait (Dardanelles), it has peculiar oceanographic, ecological and geomorphologic characteristics (Öztürk and Öztürk 1996Öztürk B., Öztürk A.A. 1996. On the biology of the Turkish straits system. Bull. Inst. Océanogr. Spec. No 17: 205-221.). This semi-enclosed sea, connecting the Black Sea to the Aegean Sea via the Turkish Straits System (TSS), is characterized by a two-layer stratification, with the brackish surface layer formed by the Black Sea water mass flowing into the Marmara Sea through the Istanbul Strait with a salinity of 18-24 and a temperature of 20-24°C in summer and 8-9°C in winter. More saline (up to 38.5) Mediterranean Sea water with a constant temperature of about 15°C resides 15-20 m below this layer (Beşiktepe et al. 1994Beşiktepe Ş.T., Sur H.İ., Özsoy E., et al. 1994. The circulation and hydrography of the Marmara Sea. Prog. Oceanogr. 34: 285-334). The TSS serves as an ecological barrier, a biological corridor and an acclimatization zone for the biota of the Mediterranean and the Black Sea (Öztürk and Öztürk 1996Öztürk B., Öztürk A.A. 1996. On the biology of the Turkish straits system. Bull. Inst. Océanogr. Spec. No 17: 205-221.). Suspended particulate organic matter and zooplankton, which constitute the bulk of octocorals’ diet, are very abundant in the whole Marmara Sea (Çoban-Yıldız et al. 2000Çoban-Yıldız Y., Tuğrul S., Ediger D., et al. 2000. A comparative study on the abundance and elemental composition of POM in three interconnected basins: the Black, the Marmara and the Mediterranean Seas. Mediterr. Mar. Sci. 1: 51-63., İşinibilir et al. 2011İşinibilir M., Svetlichny L., Hubareva E., et al. 2011. Adaptability and vulnerability of zooplankton species in the adjacent regions of the Black and Marmara Seas. J. Mar. Syst. 84: 18-27.), although the phytoplankton and microzooplankton biomass and production show a decreasing trend from the Istanbul Strait to the Aegean Sea (Zervoudaki et al. 2011Zervoudaki S., Christou E.D., Assimakopoulou G., et al. 2011. Copepod communities, production and grazing in the Turkish Straits System and the adjacent northern Aegean Sea during spring. J. Mar. Syst 86: 45-56.).

The aim of this study was to determine species composition and abundances of octocoral assemblages in the Marmara Sea and to compare the communities in the southern parts (closer to the Çanakkale strait connecting to the Aegean Sea) and northern parts (closer to the Istanbul Strait [Bosphorus] connecting to the Black Sea) with those in the Mediterranean Sea.

MATERIALS AND METHODSTop

Sampling design

Thirty-one stations were sampled by SCUBA diving in coastal areas of various islands in the Marmara Sea (Fig. 1) from April 2012 to September 2013 in order to determine the presence of octocoral species. A total of 74 dives were performed and the first dives were dedicated to specimen collection and photography. A total of 17 stations (stations N1 to N17) were located in the northern group of islands (Prince Islands) and 14 (stations S1 to S14) in the Southern Marmara Islands (Table 1). Stations in the north were chosen to the south of the Prince Islands because there is not enough depth to reach the Mediterranean water layer on the northern coasts. Since the upper layer of the Marmara Sea is formed by Black Sea waters, all stations were surveyed for octocorals from the halocline (where the Mediterranean waters reside, starting from 15-20 m) to a maximum of 40 m depth. The presence of abandoned fishing gears was noted only at the northern stations due to the difficulty of working conditions and limited time in the south, although similar fishing pressure is active in the region. All octocoral species encountered at a station were photographed in situ before a segment of approximately 10 cm was cut from the colony. The collected specimens were preserved in ethanol and the species were identified by microscope slide preparations of sclerite morphology according to Carpine and Grasshoff (1975)Carpine C., Grasshoff M. 1975. Les Gorgonaires de la Méditerranée. Bull. Inst. Océanogr. Monaco 71: 1-140., Weinberg (1976Weinberg S. 1976. Revision of the common Octocorallia of the Mediterranean circalittoral. I. Gorgonacea. Beaufortia 313: 63-104., 1977)Weinberg S. 1977. Revision of the common Octocorallia of the Mediterranean circalittoral. II. Alcyonacea. Beaufortia 25: 131-166., Bayer (1981)Bayer F.M. 1981. Key to the genera of Octocorallia exclusive of Pennatulacea (Coelenterata: Anthozoa), with diagnoses of new taxa. Proc. BioI. Soc. Wash. 94: 902-947. and Williams (1995)Williams G.C. 1995. Living genera of sea pens (Coelenterata: Octocorallia: Pennatulacea) – illustrated key and synopses. Zool. J. Linn. Soc. 113: 93-140..

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Fig. 1. – Map showing the location of the Sea of Marmara, the Prince Islands [PI] (right) and the Southern Marmara Islands [SMI] (left) and the stations.

Table 1. – Detailed description and geographical coordinates of the sampling sites. All sites were surveyed for presence of octocorals from 15/20 m to 40 m depth. The quantitative sampling was performed between 32 and 36 m, depending on the station. The type of bottom where the transect was laid is indicated by the following acronyms: hard substrate composed of hard beds and rocks (H), soft substrate composed of sandy/muddy bottom (S) and mixed substrate (M) composed of pebbles, shells and small rocks on a muddy bottom.

Code Location Description Transect Coordinates
N1 Balıkçı Adası - Tektaş The site is composed of very large to large / medium size rocks exhibiting small caves and crevices. Among the rocks, the bottom is composed of coarse sand/gravel/dead shells with a very slight slope H 40°49’12.95”N 29° 6’38.29”E
N2 Kufos taşı The site is composed of large to medium size rocks. Among the rocks, the bottom is composed of coarse sand/gravel/dead shells with a very slight slope M 40°49’15.56”N 29° 6’36.25”E
N3 Burgazada - Yelkenkaya The bottom is composed of sand with pebbles and dead shells, occasionally interrupted by small boulders, with a slope of approximately 15° M 40°52’24.59”N 29° 3’45.29”E
N4 Sedef Adası The bottom is composed of sand with pebbles and dead shells, occasionally interrupted by small boulders, with a slope of approximately 15° M 40°50’ 47.84’’N 29° 08’ 50.37’’E
N5 Sedef Adası The bottom is composed of sand with pebbles and dead shells, occasionally interrupted by small boulders, with a slope of approximately 15° M 40°50’ 50.90’’N 29°08’54.05’’E
N6 Sedef Adası The bottom is composed of sand with pebbles and dead shells, occasionally interrupted by small boulders, with a slope of approximately 15° M 40°50’51.23’’N 29° 08’ 38.84’’E
N7 Balıkçı Adası - Liskari The site is composed of large to medium size rocks until 35-40 m with a slope of approximately 30°. The bottom is then composed of fine sand with dead shells H 40°49’5.01”N 29° 6’49.53”E
N8 Büyükada - Manastır The site is 400 m from the nearest shore. Large to medium size rocks are present from 35 m and continue deep with a slight slope H 40°50’04”N 29° 06’55.3”E
N9 Büyükada - Eşkina taşı The site is composed of very large to large/medium size rocks with a slope of 40-50° H 40°50’25.30”N 29° 7’31.10”E
N10 Sedef Adası-Karaev The site is 1.3 km from the nearest shore. The very large rocks start from 35 m and continue to 50 m, surrounded by sandy bottom H 40°51’0.97” N
29°09’3.17”E
N11 Yassıada Batı The site is composed of large to medium size rocks with a slope of approximately 40° H 40°51’50.47”N 28°59’28.63”E
N12 Sivriada The site is composed of very large rocks starting from 15 m, offering large walls that descend to 40-50 m where rocks are surrounded by coarse sand/gravel/dead shells H 40°52’26.15”N 28°58’14.30”E
N13 Yassıada Güney The bottom is composed of sand with few pebbles and dead shells with a slope of approximately 10-15° S 40°51’48.93”N 28°59’41.33”E
N14 Kınalıada The bottom is composed of fine sand/mud with few pebbles with a slope of approximately 10-15° S 40°54’10.40”N 29° 2’21.56”E
N15 Burgazada - Kalpazankaya The bottom is composed of fine sand/mud with a slope of approximately 10-15° S 40°52’41.52”N 29° 3’7.36”E
N16 Heybeliada The bottom is composed of fine sand/mud with a slope of approximately 10-15° S 40°52’3.91”N 29° 4’29.28”E
N17 Büyükada - Kurşunburnu The bottom is composed of fine sand/mud with a slope of approximately 10-15° S 40°50’13.95”N 29° 7’18.67”E
S1 Paçanoz Kayalıkları The bottom is composed of pebbles and dead shells interrupted with polychaete bioconcretions, with a slope of approximately 15° M 40°36’31.47”N 27°31’31.33”E
S2 Laz Kayası The site is 230 m off the coast. The very large rocks start from 3 m and continue to 40-50 m, surrounded by coarse sand/gravels H 40°36’11.91”N 27°41’10.94”E
S3 Hayırsız Ada Kuzey The site is composed of a wall descending to 30 m where large to medium size rocks are present on the bottom with a 10-30° slope H 40°38’47.71”N 27°29’12.47”E
S4 Badalan Dağaltı The site is 200 m off the coast. Large rock starts from approximately 10 m and descends to 35 m, surrounded by gravels and dead shells H 40°39’18.41”N 27°34’23.96”E
S5 Hayırsız Ada Güney The site is composed of a wall descending to 30 m where the bottom is composed of medium size rocks with a slope of approximately 40° H 40°38’8.48”N 27°29’19.20”E
S6 Mamali Adası The rocks descends to 20 m where the bottom is composed of large to medium size rocks covered with bioconcretions with a slope of 15° H 40°31’30.08”N 27°35’16.48”E
S7 Çınarlı The bottom is composed of fine sand/mud with a slope of approximately 10-15° S 40°37’11.55”N 27°31’44.35”E
S8 Avşa Adası The bottom is composed of fine sand/mud with a slope of approximately 5-10° S 40°30’1.47”N 27°28’53.42”E
S9 Ekinlik Adası The bottom is composed of fine sand/mud rarely interrupted with small boulders on a slope of approximately 5-10° S 40°33’10.45”N 27°30’17.53”E
S10 Domuz burnu feneri The bottom is composed of fine sand/mud with a slope of approximately 5-10° S 40°40’4.52”N 27°37’52.45”E
S11 Gündoğdu The bottom is composed of fine sand/mud with a slope of approximately 5-10° S 40°34’36.94”N 27°36’3.36”E
S12 Karabiga Cendere The site is composed of a wall descending to 30 m where large to medium size rocks are present on the bottom with a slope of 10-30° H 40°25’34.92”N 27°19’14.10”E
S13 Karabiga Toptaş Kumsalı The bottom is composed of sand with pebbles and dead shells occasionally interrupted by small boulders, with a slope of approximately 15° M 40°25’20.38”N 27°19’25.13”E
S14 Topağaç The bottom is composed of fine sand/mud with a slope of approximately 10° S 40°36’14.64”N 27°41’7.32”E

The abundance of octocorals was assessed by measuring density of colonies for each species found along transects (see below). We considered three types of substrates: hard substrate composed of hard beds and rocks [H], soft substrate composed of sandy/muddy bottom [S] and mixed substrate [M] composed of pebbles, shells and small rocks on muddy bottom. The slope in degrees and the structure of hard bottoms (whether wall or rocks) were also noted (Table 1). The rocks were categorized as “very large” when they were larger than 3×5 m (vertical×horizontal); “large” when they were 1-3 m (vertical) and 1-5 m (horizontal); “medium” when they measured 1×1 m; and “small” when they measured less than 1×1 m. A total of 17 stations in the north and 10 in the south were quantitatively sampled for octocoral diversity and abundance. Four stations in the south were not quantitatively sampled due to the sole presence of encrusting alcyonarian and stoloniferan species or very scarce gorgonians to be enumerated. Transects were conducted following a fixed depth line that varied from 32 to 36 m depending on the station. Octocoral colonies were enumerated in 1 m2 quadrats placed every metre (20 quadrats) on either side of the 20-m-long transect tape laid on the substrate. In case of vertical walls or large boulders, 20 quadrats were placed haphazardly on the substrate at the same depth range. The numbers of colonies in each quadrat of a station (including the quadrats with 0 colonies) were summed together, and then divided by 20 m2 to achieve density values in units of colonies m–2.

Statistical analysis

The hypothesis that octocoral density and diversity (Simpson index in the form 1/λ) of stations do not differ among each other was tested by the univariate non-parametric Kruskal-Wallis (N=27) test with the SPSS software (SPSS, Chicago, IL).

To explore potential differences across geographic regions and habitat types on octocoral assemblages (composition and abundance), we used a two-factor permutational multivariate analysis of variance (PERMANOVA, Anderson 2001Anderson M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral. Ecol. 26: 32-46.) in which each term was tested using 9999 random permutations. The two factors were Geographic Zone (north-south) and Habitat (Hard-Soft-Mixed). Station S14, where only one specimen of Funiculina quadrangularis was observed at the limit of observation (41 m), was excluded from the analyses. Species composition and abundance data were analysed separately because abundance data were not available at all stations. The analyses were based on Bray-Curtis similarity of previously transformed data (presence/absence in case of the species composition; fourth root in case of the abundances). The resemblance matrices informed principal coordinates analysis (PCO) plots in order to identify the relationships between sampling stations based on biological information. Pairwise comparisons were also carried out in order to ascertain patterns in the composition or abundances among stations. Finally, similarity percentage analysis (SIMPER) was performed to identify the taxa that best explain the variations observed among stations. All the above analyses were carried out with the Primer v6 software (Clarke and Gorley 2006Clarke K., Gorley R. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, 91 pp.).

RESULTSTop

A total of 14 octocoral species were collected from the Sea of Marmara (Supplementary Material Table S1), with 11 of them from the Prince Islands coasts and 14 from the Southern Marmara Islands. Abundance values were obtained for only 9 species (Table 2) because rare species were generally not encountered in transects and encrusting corals were not counted. Octocoral abundance in the Marmara Sea was 5.21±5.11 colonies m–2 (mean±SD) on average calculated from a total of 1390 colonies counted in transects. Total octocoral abundance varied among stations from 0.30 to 17.70 colonies m–2 and octocoral abundance was higher in the north of the Marmara than in the south, though not significantly. Although more species were found in the south, the north of the Marmara Sea (Simpson mean=1.98±0.88) was significantly more diverse than the south (Simpson mean=1.24±0.38) (p<0.05).

Table 2. – Densities of the species in colonies m–2 and the mean density (± standard deviation) for the stations where the species was present in transect. Species acronyms: AA, Alcyonium acaule; AP, Alcyonium palmatum; EC, Eunicella cavolini; PC, Paramuricea clavata; PG, Pteroeides griseum; PM, Paramuricea macrospina; PS, Paralcyonium spinulosum; SK, Spinimuricea klavereni; VC, Veretillum cynomorium.

VC PG AP AA PS EC PM PC SK
N1 0 0 0.5 0 6.1 0.9 3.9 0.5 1.4
N2 0 0 0 0 7.1 0 0.7 0 0.3
N3 0.9 0 0.1 0 0 0 0 0 0.1
N4 0.3 0 0.3 0 1.3 0.1 1.2 0 0.8
N5 0 0 1.2 0 6.9 0 2.3 0 3.1
N6 0 0 0.4 0 5.6 0 1.7 0 1.1
N7 0 0 0.2 0 2.7 0 1.7 0 0.9
N8 0 0 0.2 0 1.8 0 0.5 0.4 0.1
N9 0 0 0.2 0 0 0 0.1 0 1.1
N10 0 0 0.7 0 4.1 0.2 1.5 0.2 0.4
N11 0 0 0.6 0.1 0.5 12.8 2.0 0 0.4
N12 0 0 1.0 0 0 13.9 2.1 0.1 0.6
N13 0.4 0 0.1 0 0 0 0 0 0.1
N14 1.2 0 0 0 0 0 0 0 0
N15 1.6 0 0 0 0 0 0 0 0
N16 3.9 0 0.1 0 0 0 0 0 0.2
N17 3.6 0 0 0 0 0 0 0 0
S1 0 0 0 3.4 0 0 0 0 0
S3 0 0 0 0 1.4 0 0 0 0
S3 0 0 0 0 0 10.7 0 0.4 0.1
S6 0 0 0 2.5 0 0 0 0 0
S7 1.4 0 0 0 0 0 0 0 0
S8 0.2 0 0.2 0 0 0 0 0 0
S9 0 1.2 0 0 0 0 0 0 0
S10 4.2 1.1 0 0 0 0 0 0 0
S11 0.2 0 0.1 0 0 0 0 0 0
S13 0 0 0 0.8 0 0 0 0 0
Mean±sd 1.63±1.54 1.15±0.07 0.40±0.30 1.70±1.51 3.75±2.52 6.43±6.69 1.61±1.03 0.32±0.16 0.71±0.77

Species composition differed significantly between the north and the south as well as among different substrate types (Table 3). 60.5% of the variation was explained in axis 1 of the PCO plot (Fig. 2), where the discrimination of stations in the horizontal direction was by groups of substrate types.

Table 3. – Results of the PERMANOVA testing for the effects of the zone (north [N] and south [S]) and substrates (hard [H]; mixed [M]; soft [S]) on the composition and abundances of Marmara soft coral assemblages.

PERMANOVA (Species Composition)
Source df SS MS Pseudo-F P(perm)
ZO 1 7844.9 7844.9 9.9859 0.0002
SU 2 30282 15141 19.273 0.0001
ZOxSU 2 6363.1 3181.6 4.0499 0.0037
Res 24 18854 785.6
Total 29 62502
Pairwise comparisons
Within level ‘N’ of factor ‘ZONE’ Within level ‘S’ of factor ‘ZONE’
Groups t P(perm) Groups t P(perm)
H. M 2.1801 0.0105 H. M 2.1392 0.0339
H. S 6.2103 0.0014 H. S 3.0846 0.002
M. S 3.9635 0.0075 M. S 1.1489 0.3826
Within level ‘H’ of factor ‘SUBS’ Within level ‘M’ of factor ‘SUBS’ Within level ‘S’ of factor ‘SUBS’
Groups t P(perm) Groups t P(perm) Groups t P(perm)
N. S 2.2486 0.0032 N. S 4.723 0.045 N. S 1.3599 0.2382
PERMANOVA (Species Abundances)
Source df SS MS Pseudo-F P(perm)
Zo 1 14303 14303 10.205 0.0001
Ha 2 29247 14623 10.434 0.0001
ZoxHa 2 9705.9 4852.9 3.4626 0.0005
Res 21 29432 1401.5
Total 26 80938
Pairwise comparisons
Within level ‘N’ of factor ‘ZONE’ Within level ‘S’ of factor ‘ZONE’
Groups t P(perm) Groups t P(perm)
H. M 1.2634 0.1912 H. M 1.0796 0.3997
H. S 5.7271 0.0023 H. S 1.693 0.0187
M. S 3.7129 0.024 M. S 2.5067 0.0497
Within level ‘H’ of factor ‘SUBS’ Within level ‘M’ of factor ‘SUBS’ Within level ‘S’ of factor ‘SUBS’
Groups t P(perm) Groups t P(perm) Groups t P(perm)
N. S 1.8072 0.0155 N. S 3.8565 0.049 N. S 1.2635 0.3083

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Fig. 2. – PCO plot of the relationships between sampling stations based on species composition data. The acronyms for substrate types are as follows: hard substrate composed of hard beds and rocks (H), soft substrate composed of sandy/muddy bottom (S), and mixed substrate composed of pebbles, shells and small rocks on muddy bottom (M).

The stations with soft substrates were not significantly different between north and south in terms of either species composition or abundance but were significantly different between hard and mixed substrates (Table 3). Veretillum cynomorium was responsible alone for 86% of the similarity observed between stations of soft substrates (Table 4). Both species composition and abundances differed significantly on hard substrates and mixed substrates of the north and south (Table 3).

Table 4. – Results of the SIMPER analyses showing similarities within substrate groups; dissimilarities between pairs of substrate groups and the species mostly responsible for the observed differences. PM, Paramuricea macrospina; PC, Paramuricea clavata; SK, Spinimuricea klavereni; EC, Eunicella cavolini; AP, Alcyonium palmatum; AA, Alcyoium acaule; PS, Paralcyonium spinulosum; VC, Veretillum cynomorium.

Species Sim/SD Contrib% Cum.% Species Av.Diss Diss/SD Contrib% Cum.%
Group H Groups H and M
Average similarity: 59.10 Average dissimilarity = 42.62
PM 2.35 27.03 27.03 PS 9.76 0.81 22.89 22.89
SK 1.99 24.07 51.1 EC 8.8 0.81 20.65 43.54
AP 2.36 22.38 73.48 AA 4.9 0.4 11.5 55.05
PS 0.79 14.68 88.15 PC 4.68 0.91 10.99 66.04
EC 0.5 6.87 95.03 PM 4.36 0.8 10.23 76.27
Group M Groups H and S
Average similarity: 62.61 Average dissimilarity = 90.43
SK 2.85 26.43 26.43 VC 20.47 1.95 22.64 22.64
PS 0.98 25.79 52.21 PS 13.79 0.97 15.25 37.88
PM 1.04 19.21 71.43 PM 11.48 1.46 12.69 50.57
AP 1.04 13.67 85.09 EC 11.23 0.81 12.42 62.99
AA 0.3 11.92 97.02 AP 9.23 1.19 10.2 73.19
SK 8.91 1.13 9.85 83.04
Group S Groups M and S
Average similarity: 54.82 Average dissimilarity = 79.60
VC 1.61 86.17 86.17 VC 18.5 1.41 23.24 23.24
AP 0.31 6.25 92.41 PS 14.13 1.05 17.75 40.99
AA 13.06 0.61 16.41 57.4
PM 10.22 1.12 12.83 70.23
AP 9.27 1.06 11.65 81.88
SK 8.85 1.09 11.12 93

Species composition on hard and mixed bottoms was significantly different from each other in the north and south but abundances of the common taxa were not significantly different from each other in both zones (Table 3). Paramuricea macrospina, Spinimuricea klavereni, Alcyonium palmatum and to a certain extent Paralcyonium spinulosum seem to be the most common taxa on either hard or mixed substrates of the northern Marmara Sea (Fig. 3; Table 4) but P. macrospina and S. klavereni were rarely observed in the south. Alcyonium acaule was a common species on mixed and hard substrates of the south, with abundances of 0.8 to 3.4 colonies m–2 (Fig. 4A), whereas it was rarely observed in the north.

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Fig. 3. – Percentage composition of the coral assemblages at hard substrate stations of the north (NH) and south (SH); at mixed substrate stations of the north (NM) and the south (SM); at soft substrate stations of the north (NS) and south (SS).

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Fig. 4.A. acaule assemblage at S1 station (A). E. cavolini dominated assemblage at N12 station. A S. klavereni colony is at the front of image (B). P. macrospina, S. klavereni, and P. spinulosum assemblage at station N5. The picture is covered with white spots due to the turbidity (C). Ghost purse seine nets wrapping rocky substrates and covering gorgonian colonies at stations N1 and N10 (D-F). Epibiont-covered dead S. klavereni colony at station N9 (G).

Abandoned fishing gears were encountered in 9 of the 17 stations (N1; N2; N4; N5; N7; N8; N9; N10; N14) on the Prince Islands coasts. The gears found most were purse seine nets, followed by set nets and fish lines.

DISCUSSIONTop

The most extensive study concerning corals/gorgonians in the Sea of Marmara dates back to the 1950s (Demir 1954Demir M. 1954. Boğaz ve Adalar Sahillerinin omurgasız dip hayvanları. Istanbul Univ, Faculty of Science, Hydrobiol. Res. Inst. Publ. 2A: 1-654 (in Turkish).) and there are very few recent studies focusing on corals (Öztürk and Bourguet 1990Öztürk B., Bourguet J.P. 1990. Données préliminaires sur le corail noir de la Mer de Marmara (Turquie) Gerardia savaglia (Bertolini, 1819). Ist. Univ. J. of Fish. 4: 45-48., Özalp 2012Özalp B.H. 2012. Manta-tow studies of the coral fauna of the Çanakkale Strait. Proceedings of the Fisheries and Aquatic Sciences Symposium. Eskişehir, Turkey, psst 197., Topçu and Öztürk 2013Topçu E.N., Öztürk B. 2013. Octocoral diversity of Balıkçı Island, the Marmara Sea. J. Black Sea/Medit. Environ. 19: 46-57.). In this regard, this study greatly enhances the knowledge on the composition and abundance of octocorals in the Marmara Sea.

Information available for the neighbouring areas of the Marmara Sea indicate that octocorals are present and diverse in the Aegean Sea (Vafidis in Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS One 5: e11842.: Table S13), whereas only one species is present in the Black Sea. Virgularia mirabilis is found only in the small section of the southern Black Sea shelf close to the Istanbul Strait that creates a zone of high salinity and provides living conditions for many Mediterranean species (Zaitsev and Mamaev 1997Zaitsev Yu P., Mamaev V. 1997. Biological diversity in the Black Sea. Black Sea Environ Ser, Vol. 3, UN Publ, New York 208 pp.). In the Marmara Sea, connecting the Aegean and the Black Seas, 23 species were found in various studies (Table 5). The high number of species in the Marmara Sea in the Turkish literature is mainly due to the lack of research effort in other areas. The number of species is higher than in the Ionian Basin (15) and similar to that in the Adriatic Sea (20 species) and in the Aegean Sea (28) (species numbers/region were obtained from Vafidis in Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS One 5: e11842.: Table S13). The Prince Islands form a boundary of the spatial distributions of octocorals in the Mediterranean Sea, except for V. mirabilis.

Table 5. – Check-list of octocoral species for the Turkish coasts (Sea of Marmara, Aegean and Mediterranean (Medit.) coasts of Turkey).

Species Marmara Aegean Medit. Reference
Order Alcyonacea
Suborder Stolonifera
Cornularia cornucopiae (Pallas, 1766) + Uysal et al. 2002Uysal A., Yüksek A., Okuş E., et al. 2002. Benthic community structure of the Bosphorus and surrounding area. Water Sci. Technol. 46: 37-44.
Clavularia crassa (Milne Edwards, 1848) + Demir 1954Demir M. 1954. Boğaz ve Adalar Sahillerinin omurgasız dip hayvanları. Istanbul Univ, Faculty of Science, Hydrobiol. Res. Inst. Publ. 2A: 1-654 (in Turkish).
Sarcodictyon catenatum Forbes, 1847 + This study
Sarcodictyon roseum (Philippi, 1842) + Ostroumoff 1894Ostroumoff A., 1894. Proceeding materials for the Bosporus natural history. Notes of the Imperial Academy of Sciences, St. Petersburg 74: 1-46.
Suborder Alcyoniina
Alcyonium palmatum Pallas, 1766 + + Colombo 1885Colombo A. 1885. Racolte Zoologiche eseguite del R. Piroscofa Washington nelle campagna-abissale talassografica dell’anno 1885. Riv Marit, 1-34., Geldiay and Kocataş 1972Geldiay R., Kocataş A. 1972. Note préliminaire sur les peuplements benthiques du golfe d’Izmir. Sci. Monog. Fac. Sci. Ege Univ. 12: 3-33.
Alcyonium acaule Marion, 1878 + + Topçu and Öztürk 2013Topçu E.N., Öztürk B. 2013. Octocoral diversity of Balıkçı Island, the Marmara Sea. J. Black Sea/Medit. Environ. 19: 46-57., Gözcelioğlu 2011Gözcelioğlu B. 2011. Denizlerimizin sakinleri. Gökçe Ofset Basım Yayın, Ankara (in Turkish).
Alcyonium coralloides (Pallas, 1766) + + Ostroumoff 1894Ostroumoff A., 1894. Proceeding materials for the Bosporus natural history. Notes of the Imperial Academy of Sciences, St. Petersburg 74: 1-46., Çınar et al. 2014Çınar M.E., Yökeş M.B., Açık Ş., et al. 2014. Check-list of Cnidaria and Ctenophora from the coasts of Turkey. Turk. J. Zool. 38: 677-697
Maasella edwardsii (de Lacaze-Duthiers, 1888) + Özalp 2012Özalp B.H. 2012. Manta-tow studies of the coral fauna of the Çanakkale Strait. Proceedings of the Fisheries and Aquatic Sciences Symposium. Eskişehir, Turkey, psst 197.
Paralcyonium spinulosum Delle Chiaje, 1822 + Topçu and Öztürk 2013Topçu E.N., Öztürk B. 2013. Octocoral diversity of Balıkçı Island, the Marmara Sea. J. Black Sea/Medit. Environ. 19: 46-57.
Suborder Scleraxonia
Corallium rubrum (Linnaeus, 1758) + Öztürk 2010bÖztürk B. 2010b. Red coral and its actual situation in Turkey. In: Bussoletti E., Cottingham D., Bruckner A., et al. (eds), Proceedings of the International Workshop on Red Coral Science, Management, and Trade: Lesson from the Mediterranean. Naples, Italy, pp. 119.
Suborder Holaxonia
Bebryce mollis Philippi, 1842 + Ostroumoff 1896Ostroumoff A., 1896. Comptes rendus des dragages et du plancton de l’expédition de “Selianik”. Bulletin de l’Académie impériale des sciences de St.-Pétersbourg 5: 33-92
Paramuricea clavata (Risso, 1826) + + + Öztürk and Bourguet 1990Öztürk B., Bourguet J.P. 1990. Données préliminaires sur le corail noir de la Mer de Marmara (Turquie) Gerardia savaglia (Bertolini, 1819). Ist. Univ. J. of Fish. 4: 45-48., Öztürk et al. 2004Öztürk B., Aktan Y., Topaloğlu B., et al. 2004. Marine life of Turkey in the Aegean and Mediterranean Seas. TÜDAV Publ. No 10, Istanbul, Turkey, 200 pp.
Paramuricea macrospina (Koch, 1882) + Ostroumoff 1896Ostroumoff A., 1896. Comptes rendus des dragages et du plancton de l’expédition de “Selianik”. Bulletin de l’Académie impériale des sciences de St.-Pétersbourg 5: 33-92.
Spinimuricea klavereni (Carpine and Grasshoff, 1975) + Ostroumoff 1896Ostroumoff A., 1896. Comptes rendus des dragages et du plancton de l’expédition de “Selianik”. Bulletin de l’Académie impériale des sciences de St.-Pétersbourg 5: 33-92.
Eunicella singularis (Esper, 1791) + + + Yurtsever 2002Yurtsever A. 2002. Kuzey Ege Denizi’nde bulunan bazı yumuşak mercan (gorgon) türlerinin popülasyon yapısı üzerine araştırmalar. M.Sc thesis, Istanbul Univ Grad Sch of Nat and Appl Sci, İstanbul, 23 pp. (in Turkish)., Öztürk et al. 2004Öztürk B., Aktan Y., Topaloğlu B., et al. 2004. Marine life of Turkey in the Aegean and Mediterranean Seas. TÜDAV Publ. No 10, Istanbul, Turkey, 200 pp.
Eunicella cavolini (Koch, 1887) + + + Yurtsever 2002Yurtsever A. 2002. Kuzey Ege Denizi’nde bulunan bazı yumuşak mercan (gorgon) türlerinin popülasyon yapısı üzerine araştırmalar. M.Sc thesis, Istanbul Univ Grad Sch of Nat and Appl Sci, İstanbul, 23 pp. (in Turkish)., Öztürk et al. 2004Öztürk B., Aktan Y., Topaloğlu B., et al. 2004. Marine life of Turkey in the Aegean and Mediterranean Seas. TÜDAV Publ. No 10, Istanbul, Turkey, 200 pp.
Eunicella verrucosa (Pallas, 1766) + Demir 1954Demir M. 1954. Boğaz ve Adalar Sahillerinin omurgasız dip hayvanları. Istanbul Univ, Faculty of Science, Hydrobiol. Res. Inst. Publ. 2A: 1-654 (in Turkish).
Order Pennatulacea
Veretillum cynomorium (Pallas, 1766) + + Ostroumoff 1894Ostroumoff A., 1894. Proceeding materials for the Bosporus natural history. Notes of the Imperial Academy of Sciences, St. Petersburg 74: 1-46., Geldiay and Kocataş 1972Geldiay R., Kocataş A. 1972. Note préliminaire sur les peuplements benthiques du golfe d’Izmir. Sci. Monog. Fac. Sci. Ege Univ. 12: 3-33.
Kophobelemnon leucharti Cecchini, 1917 + Demir 1954Demir M. 1954. Boğaz ve Adalar Sahillerinin omurgasız dip hayvanları. Istanbul Univ, Faculty of Science, Hydrobiol. Res. Inst. Publ. 2A: 1-654 (in Turkish).
Funiculina quadrangularis (Pallas, 1766) + Ostroumoff 1896Ostroumoff A., 1896. Comptes rendus des dragages et du plancton de l’expédition de “Selianik”. Bulletin de l’Académie impériale des sciences de St.-Pétersbourg 5: 33-92
Virgularia mirabilis (Müller, 1776) + + (sp.) Uysal et al. 2002Uysal A., Yüksek A., Okuş E., et al. 2002. Benthic community structure of the Bosphorus and surrounding area. Water Sci. Technol. 46: 37-44., Okuş et al. 2004Okuş E., Sur H.I., Yüksek A., et al. 2004. Datça-Bozburun Özel Çevre Koruma Bölgesinin denizel ve kıyısal alanlarının biyolojik çeşitliliğinin tespiti. Project Final Report: 698 pp (in Turkish).
Pennatula phosphorea Linnaeus, 1758 + + Colombo 1885Colombo A. 1885. Racolte Zoologiche eseguite del R. Piroscofa Washington nelle campagna-abissale talassografica dell’anno 1885. Riv Marit, 1-34., Çınar et al. 2012Çınar M.E., Katağan T., Öztürk B., et al. 2012. Spatio-temporal distributions of zoobenthos in Mersin Bay (Levantine Sea, eastern Mediterranean) and the importance of alien species in benthic communities. Mar. Biol. Res. 8: 954-968.
Pennatula rubra Ellis, 1761 + + Topaloğlu et al. 2004Topaloğlu B., Öztürk B., Karakulak S.F. 2004. The macrozoobenthic invertebrate fauna in the Marmara Sea. Rapp. Comm. Int. Mer. Médit. 37: 554., Mutlu and Ergev 2008Mutlu E., Ergev M.B. 2008. Spatio-temporal distribution of soft-bottom epibenthic fauna on the Cilician shelf (Turkey), Mediterranean Sea. Rev. Biol. Trop. 56: 1919-1946.
Pteroeides griseum (Linnaeus, 1767) + + Demir 1954Demir M. 1954. Boğaz ve Adalar Sahillerinin omurgasız dip hayvanları. Istanbul Univ, Faculty of Science, Hydrobiol. Res. Inst. Publ. 2A: 1-654 (in Turkish)., Çınar et al. 2014Çınar M.E., Yökeş M.B., Açık Ş., et al. 2014. Check-list of Cnidaria and Ctenophora from the coasts of Turkey. Turk. J. Zool. 38: 677-697

The soft bottoms of the Marmara Sea in the diving limits of depth seem to be colonized mainly by Pennatulaceans, most commonly V. cynomorium, followed by Pteroeides griseum, the two shallow-water species. These sea pens form large beds of a single species on the soft bottoms of the Marmara Sea, occasionally disrupted by a few alcyonaceans, as is frequently observed in the Mediterranean (Gili and Pagès 1987Gili J., Pagès F. 1987. Pennatuláceas (Cnidaria, Anthozoa) recolectados en la plataforma continental catalana (Mediterráneo occidental). Misc. Zool. 11: 25-39 (in Spanish).) and globally (Pérès 1982Pérès J.M. 1982. Major benthic assemblages. In: O. Kinne (Ed.) Marine Ecology. J. Wiley & Sons London 5: 373-522.).

The main rocky habitats of the Marmara Sea covered by coralligenous outcrops were composed of (1) vertical walls or large rocks on steep bottom colonized mainly by Eunicella cavolini with high abundances (10.7-13.9 colonies m–2) (Fig. 4B) and (2) large-medium size boulders on a slightly steep or flat bottom colonized by P. macrospina, S. klavereni, and P. spinulosum (3-13.3 colonies m–2) (Fig. 4C). The first type corresponds to one of the common coralligenous assemblages for the Mediterranean Sea, dominated by E. cavolini, as is often the case in the (rarely) gorgonian-dominated eastern Mediterranean coralligenous assemblages (Kružić 2007Kružić P. 2007. Anthozoan fauna of Telascica Nature Park (Adriatic Sea, Croatia). Nat. Croat. 16: 233-266., Salomidi et al. 2009Salomidi M., Smith C., Katsanevakis S., et al. 2009. Some observations on the structure and distribution of gorgonian assemblages in the eastern Mediterranean Sea. In: UNEP – MAP – RAC/SPA, Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. Tabarka, Tunis, pp 242-245., Gerovasileiou et al. 2009Gerovasileiou V., Sini M.I., Poursanidis D., et al. 2009. Contribution to the knowledge of Coralligenous communities in the NE Aegean Sea. Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. Tabarka, Tunis, pp 205-207.). E. verrucosa and E. singularis were rare observations in the southern Marmara Sea, as is also generally observed in the eastern Mediterranean.

The Sea of Marmara is highly impacted by various anthropogenic activities, such as wastewater discharge, agricultural run-off, illegal fishing and overfishing, marine litter and shipping (Öztürk et al. 2000Öztürk B., Kadıoğlu M., Öztürk H. 2000. Marmara Denizi 2000 Sempozyumu bildiriler kitabı. TUDAV Publ 5, 607 pp (in Turkish)., Öztürk 2010aÖztürk B. 2010a. Marmara Denizi 2010 Sempozyumu bildiriler kitabı. TUDAV Publ 32, 521 pp (in Turkish).). The semi-enclosed sea recently suffered from red-tides (Türkoğlu 2013Türkoğlu M. 2013. Red tides of the dinoflagellate Noctiluca scintillans associated with eutrophication in the Sea of Marmara (the Dardanelles, Turkey) Oceanologia 55:709-732.) and mucilage events (Aktan et al. 2008Aktan Y., Dede A., Çiftci P.S. 2008. Mucilage event associated with diatoms and dinoflagellates in Sea of Marmara, Turkey. Harmful Algae News 36: 1-3., Balkıs et al. 2011Balkis N., Atabay H., Türetgen I., et al. 2011. Role of single-celled organisms in mucilage formation on the shores of Büyükada Island (the Marmara Sea). J. Mar. Biol. Assoc. UK 91: 771-781.). In spite of such severe anthropogenic disturbances, dense assemblages of endemic gorgonians in the Marmara Sea were observed during this study, although gorgonian densities were lower than those of the western Mediterranean (e.g. in Linares et al. 2008Linares C., Coma R., Garrabou J., et al. 2008. Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J. Appl. Ecol. 45(2): 688-699.). E. cavolini populations can reach densities as high as 180 colonies m–2 in the bay of Calvi (Corsica, France) (Weinbauer and Velimirov 1996Weinbauer M.G., Velimirov B. 1996. Population dynamics and overgrowth of the sea fan Eunicella cavolini (Coelenterata: Octocorallia). Est. Coast. Shelf Sci. 42(5): 583-595.), whereas the highest density in the Marmara Sea was approximately 14 colonies m–2.

P. macrospina is a Mediterranean endemic known to occur on rocks, detritic or sandy/muddy bottoms, mainly at depths of 40 to 100 m but also deeper (Carpine and Grasshoff 1975Carpine C., Grasshoff M. 1975. Les Gorgonaires de la Méditerranée. Bull. Inst. Océanogr. Monaco 71: 1-140.). This species is mentioned in the literature dealing mainly with deep sea fauna of the Mediterranean Sea (Watling et al. 2005Watling L., Auster P.J. 2005. Distribution of deep-water Alcyonacea off the Northeast Coast of the United States. Cold-Water Corals and Ecosystems Erlangen Earth Conference Series pp. 279-296., Aguilar et al. 2009Aguilar R., Pastor X., De la Torriente A., et al. 2009. Deep sea coralligenous beds observed with ROV on four seamounts in the western Mediterranean. In: UNEP – MAP – RAC/SPA, Proceedings of the 1st Mediterranean symposium on the conservation of the coralligenous and other calcareous bio-concretions. Tabarka, Tunis, pp 148-150., Mastrototaro et al. 2010Mastrototaro F., D’Onghia G., Corriero G., et al. 2010. Biodiversity of the white coral bank off Cape Santa Maria di Leuca (Mediterranean Sea): An update. Deep Sea Res. PT II 57: 412-430., Bo et al. 2012Bo M., Canese S., Spaggiari C., et al. 2012. Deep Coral Oases in the South Tyrrhenian Sea. PloS One 7: e49870., Angeletti et al. 2014Angeletti L., Taviani M., Canese S., et al. 2014. New deep-water cnidarian sites in the southern Adriatic Sea. Mediterr. Mar. Sci. 15: 263-273.) except in the Aegean Sea, where it was collected between 20 and 90 m (Vafidis et al. 1994Vafidis D., Koukouras A., Voultsiadou-Koukoura E. 1994. Octocoral fauna of the Aegean Sea with a check list of the Mediterranean species: new information, faunal comparisons. Ann. Inst. Oceanogr. 70(2): 217-229.); P. macrospina–dominated assemblages were abundant, especially in the north of the Marmara Sea, and this species was suggested to have greater adaptability than other gorgonians in relation to a relatively fast growing rate (Bo et al. 2012Bo M., Canese S., Spaggiari C., et al. 2012. Deep Coral Oases in the South Tyrrhenian Sea. PloS One 7: e49870.).

On the other hand, S. klavereni, another common species in the northern Marmara Sea, is an endemic Mediterranean species on which very limited information is available. It occurs on hard substrates of the circalittoral zone between 50-80 m deep (Carpine and Grasshoff 1975Carpine C., Grasshoff M. 1975. Les Gorgonaires de la Méditerranée. Bull. Inst. Océanogr. Monaco 71: 1-140., Grasshoff 1992Grasshoff M. 1992. Die Flachwasser-Gorgonarien von Europa und Westafrika (Cnidaria, Anthozoa). Courier Forsch. Int., Senckenberg, 149: 1-135.). It was recently reported from the Tyrrhenian Sea as a rare occurrence, on muddy substrates with patches of organogenic detritus at depths deeper than 70 m (Bo et al. 2012Bo M., Canese S., Spaggiari C., et al. 2012. Deep Coral Oases in the South Tyrrhenian Sea. PloS One 7: e49870.). In the northern Marmara Sea, it occurs on hard substrates like rocks or small pebbles/shells on sandy/muddy bottom starting from 25 m until our limit of observation (42 m), with abundances varying from 1 to 3.1 colonies m–2.

The Marmara Sea faced severe disturbances, particularly from the 1980s onward, due to rapid population growth and industrial revolution in the surrounding region (Burak 2008Burak S. 2008. Evaluation of pollution abatement policies in the Marmara Sea with water quality monitoring. Asian J. Chem. 20(5): 4117.) and in parallel to the catastrophic degradation period in the Black Sea (Bakan and Büyükgüngör 2000Bakan G., Büyükgüngör H. 2000. The Black Sea. Mar. Pollut. Bull. 41(1-6): 24-43.). In order to compare the present status of corals in the Sea of Marmara to that of the post-disturbances period (1960 to the 1970s), local divers and fishermen were questioned. Although we could not obtain quantitative data, they all agreed that they used to see more abundant dense gorgonian assemblages in the past. We also obtained a short video (Supplementary Material Video S1) taken in 1975 at Balıkçı Island by a local diver. In the video, a very dense assemblage of Savalia savaglia/P. clavata is clearly seen, revealing large colonies. Today, though both species are still present in the Marmara Sea, such dense assemblages are not encountered. Abandoned purse seine nets were pointed out by divers and small scale fishermen as the main reason behind the decrease of gorgonians and corals. In fact, this problem is continuous in the whole Marmara Sea (Yıldız and Karakulak 2010Yıldız T., Karakulak S. 2010. İstanbul Adalarında Hayalet Avcılık. In Öztürk B (ed.), Marmara Denizi 2010 Sempozyumu bildiriler kitabı. TUDAV Publ 32: 282-288.), causing serious damage to the ecosystem despite fishing net cleaning operations by local and environmental associations. Abandoned fishing gears highly impact corals and gorgonians via entanglement and overgrowth by epibionts (Bavestrello et al. 1997Bavestrello G., Cerrano C., Zanzi D., et al. 1997. Damage by fishing activities to the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aquat. Conserv. 7: 253-262., Bo et al. 2014Bo M., Bava S., Canese S., et al. 2014. Fishing impact on deep Mediterranean rocky habitats as revealed by ROV investigation. Biol. Conserv. 171: 167-176.). Abandoned nets were encountered at 53% of the stations in the north of the Marmara Sea during this study (Fig. 4D, E, F), causing harm to octocoral species and other sessile fauna.

The continuous disturbances by fishing gears, together with the peculiar oceanographic conditions in the Marmara Sea, could be responsible for the abundance of the opportunistic gorgonians. The Marmara Sea has received a significant pollution load in the last 30 years from both the Black Sea inflow and increased anthropogenic input (Tuğrul and Polat 1995Tuğrul S., Polat Ç. 1995. Quantitative comparison of the influxes of nutrients and organic carbon into the Sea of Marmara both from anthropogenic sources and from the Black Sea. Water Sci. Technol. 32: 115-121.). The semi-enclosed Marmara Sea is highly turbid, preventing daylight at very shallow depths (Çoban-Yıldız et al. 2000Çoban-Yıldız Y., Tuğrul S., Ediger D., et al. 2000. A comparative study on the abundance and elemental composition of POM in three interconnected basins: the Black, the Marmara and the Mediterranean Seas. Mediterr. Mar. Sci. 1: 51-63.) and the temperature below 20 m is lower (approximately 14.5°C) than at depths of the same range in the Mediterranean, so the conditions are similar to those of higher depths in the Mediterranean Sea. This could be the reason for high abundances at 25-40 m of P. macrospina and S. klavereni, which are found at greater depths in the Mediterranean. These relatively fast-growing gorgonians might be colonizing more easily the habitats emptied by other species due to the disturbances by fishing gears under the highly turbid conditions of the Marmara Sea since the 1970s.

A series of thermal anomalies recently affected Mediterranean benthic assemblages, causing mass mortalities at some locations and gorgonians were among the organisms most affected (Perez et al. 2000Perez T., Garrabou J., Sartoretto S., et al. 2000. Mortalité massive d’invertébrés marins: un événement sans précédent en Méditerranée nord-occidentale. Cr. Acad. Sci. III-Vie 323: 853-865., Garrabou et al. 2009Garrabou J., Coma R., Bensoussan N., et al. 2009. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob. Change Biol. 15: 1090-1103.). In the Marmara Sea, temperature variances below 20 m are very low and the temperature is generally about 15°C. Therefore, gorgonian assemblages do not risk mortality events related to thermal stress as in the Mediterranean Sea, but an important threat arises from mucilage events. Mucilage events resulting from single-cell organisms are periodically observed in the Marmara Sea (Aktan et al. 2008Aktan Y., Dede A., Çiftci P.S. 2008. Mucilage event associated with diatoms and dinoflagellates in Sea of Marmara, Turkey. Harmful Algae News 36: 1-3., Balkıs et al. 2011Balkis N., Atabay H., Türetgen I., et al. 2011. Role of single-celled organisms in mucilage formation on the shores of Büyükada Island (the Marmara Sea). J. Mar. Biol. Assoc. UK 91: 771-781.) and the sedimentation of the aggregates causes negative effects by covering benthic organisms (Aktan et al. 2008Aktan Y., Dede A., Çiftci P.S. 2008. Mucilage event associated with diatoms and dinoflagellates in Sea of Marmara, Turkey. Harmful Algae News 36: 1-3.). The impact of mucilage on gorgonians has been previously reported, though it was caused by a different type of mucilage formed by the aggregation of filamentous algae; mucilage gets trapped on gorgonian branches positioned perpendicularly to currents and causes damage (sometimes irreparable) to gorgonians (Giuliani et al. 2005Giuliani S., Virno Lamberti C., Sonni C., et al. 2005. Mucilage impact on gorgonians in the Tyrrhenian Sea. Sci. Total Environ. 353: 340-349.). We observed in 2011 mucilage fragments on S. klavereni colonies and local divers informed us that several S. klavereni colonies died after the severe mucilage events of 2007-2008. The dead branches can still be observed at station N9, which is covered by epibionts (Fig. 4G).

Most of the octocoral species found in the Marmara Sea, such as A. coralloides, A. acaule, P. clavata and E. cavolini, are considered typical components of Mediterranean coralligenous communities, which are stated as the most important biocoenosis in “Guidelines for the Establishment and Management of Mediterranean Marine and Coastal Protected Areas” (Lopez Ornat 2006López Ornat A. (ed.) 2006. Guidelines for the Establishment and Management of Mediterranean Marine and Coastal Protected Areas. MedMPA Project Ed: UNEP-MAP RAC\SPA. Tunis.). According to Council Regulation 1967/2006 of the European Union (EU), fishing with trawl nets, dredges, shore seines or similar nets above coralligenous habitats shall be prohibited. Recently, purse seine fisheries were prohibited around the Prince Islands Area; however that ban does not cover all of the vulnerable assemblages. In the Marmara Sea, there is no regional or national legislation for the protection of corals and gorgonians except the complete prohibition of fisheries of Corallium rubrum and S. savaglia, according to the Statements 2012/66 and 2012/65. In order to ensure the conservation of coral assemblages in the Marmara Sea, we emphasize the need for specific measures such as the removal of abandoned fishing nets, enlargement of the prohibited area for purse seining, prohibition of anchoring, placement of mooring buoys and better prosecution of offenders. This study provides scientific support to complete some tasks required by the EU Marine Strategy Framework Directive in order to achieve and maintain Good Environmental Status (GES) by 2020 in Turkish waters.

ACKNOWLEDGEMENTSTop

The authors are grateful to Serço Ekşiyan for the short video of Balıkçı Island from 1975 and his underwater guidance at the area. Many thanks to K. Mert Eryalçın, Ateş Evirgen, Suat Apuşoğlu and all volunteers for accompanying the diving and to the captains of the diving boats, Ali Önel and Hüseyin Demirbaş. We acknowledge the helpful assistance of the Ministry of Culture and Tourism officer Serkan Gedük in areas prohibited to diving. The financial support of Istanbul University Scientific Research Fund (BAP Project No 4944) is acknowledged. This study was partly supported by the European Union FP7 COCONET project (Grant agreement No. 287844, http://www.coconet-fp7.eu/) and the TUBITAK project 111Y268.

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SUPPLEMENTARY MATERIAL

The following material is available through the online version of this article and at the following link:
http://www.icm.csic.es/scimar/supplm/sm04120esm.pdf

Table S1. – Taxonomic list of collected species with data of the material examined and notes on its ecology.

Fig. S1. – Red Alcyonium acaule colony on rocky bottom at station S1 (A); colony on bioconcretion at station S9 (B); colony on the crab Maja crispata at station S6 (C); orange colony at station S6 (D); two small colonies on a dead mussel shell at station S13 (E); surface brooder colony at station S1 on august 2013 (F) and shark egg cases attached colony at station S1 (G).

Video S1. – Video taken in 1975 at Balıkçı Island by a local diver. In the video, a very dense assemblage of Savalia savaglia/P. clavata is clearly seen, revealing large colonies.



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