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Impact of excessive sedimentation caused by anthropogenic activities on benthic suspension feeders in the Sea of Marmara

Published online by Cambridge University Press:  18 December 2018

Nur Eda Topçu ,
Emre Turgay ,
Remziye Eda Yardımcı ,
Bülent Topaloğlu ,
Ahsen Yüksek ,
Terje M. Steinum ,
Süheyla Karataş  and
Bayram Öztürk
Nur Eda Topçu*
Affiliation:
Department of Marine Biology, Istanbul University Faculty of Aquatic Sciences, Ordu cad No 8 34470 Laleli/Fatih Istanbul, Turkey
Emre Turgay*
Affiliation:
Department of Fish Diseases, Istanbul University Faculty of Aquatic Sciences, Ordu cad No 8 34470 Laleli/Fatih Istanbul, Turkey
Remziye Eda Yardımcı
Affiliation:
Department of Fish Diseases, Istanbul University Faculty of Aquatic Sciences, Ordu cad No 8 34470 Laleli/Fatih Istanbul, Turkey
Bülent Topaloğlu
Affiliation:
Department of Marine Biology, Istanbul University Faculty of Aquatic Sciences, Ordu cad No 8 34470 Laleli/Fatih Istanbul, Turkey Turkish Marine Research Foundation No 10, 81650 Beykoz/Istanbul, Turkey
Ahsen Yüksek
Affiliation:
Institute of Marine Sciences and Management, Istanbul University, Müşküle Sok. No:17, 34134 Vefa/Fatih Istanbul, Turkey
Terje M. Steinum
Affiliation:
Department of Molecular Biology and Genetics, Istanbul University Faculty of Sciences, Ordu cad No 8 Laleli, 34470 Istanbul, Turkey
Süheyla Karataş
Affiliation:
Department of Fish Diseases, Istanbul University Faculty of Aquatic Sciences, Ordu cad No 8 34470 Laleli/Fatih Istanbul, Turkey
Bayram Öztürk
Affiliation:
Department of Marine Biology, Istanbul University Faculty of Aquatic Sciences, Ordu cad No 8 34470 Laleli/Fatih Istanbul, Turkey Turkish Marine Research Foundation No 10, 81650 Beykoz/Istanbul, Turkey
*
Author for correspondence: Nur Eda Topçu, E-mail: edatopcu@istanbul.edu.tr and Emre Turgay, E-mail: eturgay@istanbul.edu.tr
Author for correspondence: Nur Eda Topçu, E-mail: edatopcu@istanbul.edu.tr and Emre Turgay, E-mail: eturgay@istanbul.edu.tr
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Abstract

A massive die-off of benthic suspension feeders (BSF) covered by large amounts of sediments was observed along Prince Islands coasts (north-eastern Sea of Marmara) in August 2015. Alcyonarians, pennatulaceans, bivalves and sponges were severely affected. Many BSF probably died from burial and clogging of their feeding and respiratory apparatus. Of the gorgonian colonies, 66 ± 34% (mean ± SD) were dead, while 15 ± 16% (mean ± SD) displayed recent necrosis on the colony surface. In addition, histopathological and microbial examinations of the affected gorgonians and gold corals (Savalia savaglia) suggest that stress caused by sedimentation made them vulnerable to exploitation by consistently isolated opportunistic microorganisms. We isolated Vibrio splendidus and Vibrio neptunius from diseased gold coral colonies, but the bacterial isolates obtained from gorgonians could only be identified to genus Vibrio level. The presumably artificially introduced fungus Mucor circinelloides was common on both gold coral and gorgonians. This mould and opportunistic bacteria may have colonized BSF by taking advantage of low oxygen levels leading to impaired coral immune responses and thereby exacerbated the BSF mortality. Construction and landfill operations at Yassıada seem to be the greatest contributor to the observed sedimentation, as shown by silicate concentrations in nearby waters. These observations imply that preventive measures are necessary when construction operations take place in the vicinity of sensitive marine habitats.

Keywords

Coralsdisturbancegorgoniansmass mortalityMucorVibrio
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 5 , August 2019 , pp. 1075 - 1086
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

Austin, B, Austin, D, Sutherland, R, Thompson, F and Swings, J (2005) Pathogenicity of vibrios to rainbow trout (Oncorhynchus mykiss, Walbaum) and Artemia nauplii. Environmental Microbiology 7, 1488–1495.Google Scholar
Ballesteros, E (2006) Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanography and Marine Biology 44, 123–195.Google Scholar
Bally, M and Garrabou, J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Global Change Biology 13, 2078–2088.Google Scholar
Bell, JJ, McGrath, E, Biggerstaff, A, Bates, T, Bennett, H, Marlow, J and Shaffer, M (2015) Sediment impacts on marine sponges. Marine Pollution Bulletin 94, 5–13.Google Scholar
Ben-Haim, Y and Rosenberg, E (2002) A novel Vibrio sp. pathogen of the coral Pocillopora damicornis. Marine Biology 141, 47–55.Google Scholar
Ben-Haim, Y, Thompson, F, Thompson, C, Cnockaert, M, Hoste, B, Swings, J and Rosenberg, E (2003) Vibrio coralliilyticus sp. nov., a temperature-dependent pathogen of the coral Pocillopora damicornis. International Journal of Systematic and Evolutionary Microbiology 53, 309–315.Google Scholar
Bertolino, M, Cerrano, C, Bavestrello, G, Carella, M, Pansini, M and Calcinai, B (2013) Diversity of Porifera in the Mediterranean coralligenous accretions, with description of a new species. ZooKeys 336, 1–37.Google Scholar
Beşiktepe, ŞT, Sur, Hİ, Özsoy, E, Latif, MA, Oǧuz, T and Ünlüata, Ü (1994) The circulation and hydrography of the Marmara Sea. Progress in Oceanography 34, 285–334.Google Scholar
Blanquer, A, Uriz, MJ, Cebrian, E and Galand, PE (2016) Snapshot of a bacterial microbiome shift during the early symptoms of a massive sponge die-off in the Western Mediterranean. Frontiers in Microbiology 7, 1–10.Google Scholar
Bo, M, Bavestrello, G, Canese, S, Giusti, M, Angiolillo, M, Cerrano, C, Salvati, E and Greco, S (2010) Coral assemblage off the Calabrian Coast (South Italy) with new observations on living colonies of Antipathes dichotoma. Italian Journal of Zoology 78, 231–242.Google Scholar
Bonhomme, D, Garrabou, J, Pérez, T, Sartoretto, S and Harmelin, J (2003) Impact and recovery from a mass mortality event of the gorgonian Paramuricea clavata populations on the French Mediterranean coasts. Geophysical Research Abstracts 5, 10676.Google Scholar
Bruno, JF, Petes, LE, Drew Harvell, C and Hettinger, A (2003) Nutrient enrichment can increase the severity of coral diseases. Ecology Letters 6, 1056–1061.Google Scholar
Burke, L, Reytar, K, Spalding, M and Perry, A (2011) Reefs at Risk Revisited. Washington, DC: World Resources Institute.Google Scholar
Cerrano, C, Bavestrello, G, Bianchi, CN, Cattaneo-Vietti, R, Bava, S, Morganti, C, Morri, C, Picco, P, Sara, G, Schiaparelli, S, Siccardi, A and Sponga, F (2000) A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecology Letters 3, 284–293.Google Scholar
Cerrano, C, Arillo, A, Azzini, F, Calcinai, B, Castellano, L, Muti, C, Valisano, L, Zega, G and Bavestrello, G (2005) Gorgonian population recovery after a mass mortality event. Aquatic Conservation: Marine and Freshwater Ecosystems 15, 147–157.Google Scholar
Cervino, JM, Hayes, RL, Polson, SW, Polson, SC, Goreau, TJ, Martinez, RJ and Smith, GW (2004) Relationship of Vibrio species infection and elevated temperatures to yellow blotch/band disease in Caribbean corals. Applied and Environmental Microbiology 70, 6855–6864.Google Scholar
Coles, SL and Ruddy, L (1995) Comparison of water quality and reef coral mortality and growth in southeastern Kane'ohe Bay, O'ahu, Hawai'i, 1990 to 1992, with conditions before sewage diversion. Pacific Science 49, 247–265.Google Scholar
Coma, R, Ribes, M, Zabala, M and Gili, J-M (1995) Reproduction and cycle of gonadal development in the Mediterranean gorgonian Paramuricea clavata. Marine Ecology Progress Series 117, 173–183.Google Scholar
Coma, R, Linares, C, Ribes, M, Diaz, D, Garrabou, J and Ballesteros, E (2006) Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Marine Ecology Progress Series 327, 51–60.Google Scholar
Culling, CFA (1963) Handbook of Histopathological Techniques, 2nd edition. London: Butterworth and Co.Google Scholar
Cupido, R, Cocito, S, Sgorbini, S, Bordone, A and Santangelo, G (2008) Response of a gorgonian (Paramuricea clavata) population to mortality events: recovery or loss? Aquatic Conservation: Marine and Freshwater Ecosystems 18, 984–992.Google Scholar
Dizbay, M, Adisen, E, Kustimur, S, Sari, N, Cengiz, B, Yalcin, B, Kalkanci, A, Gonul, II and Sugita, T (2009) Fungemia and cutaneous zygomycosis due to Mucor circinelloides in an intensive care unit patient: case report and review of literature. Japanese Journal of Infectious Diseases 62, 146–148.Google Scholar
Erftemeijer, PLA, Riegl, B, Hoeksema, BW and Todd, PA (2012) Environmental impacts of dredging and other sediment disturbances on corals: a review. Marine Pollution Bulletin 64, 1737–1765.Google Scholar
Fabricius, KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Marine Pollution Bulletin 50, 125–146.Google Scholar
Fabricius, KE, Golbuu, Y and Victor, S (2007) Selective mortality in coastal reef organisms from an acute sedimentation event. Coral Reefs 26, 69.Google Scholar
Garrabou, J, Bensoussan, N, Pairaud, I, Garreau, P, Somot, S, Linares, C, Kersting, D, Cebrian, D, de Caralt, S, Kipson, S, Ledoux, JB and Frleta-Valić, M (2013) Assessing climate change impacts on marine biodiversity conservation: the case study of mass mortality events in the NW Mediterranean basin. CLIMCARES CLimate Impacts on Mediterranean Coastal AREaS Project Final report, June 2013, 49 pp.Google Scholar
Garrabou, J, Coma, R, Bensoussan, N, Bally, M, Chevaldonné, P, Cigliano, M, Diaz, D, Harmelin, JG, Gambi, MC, Kersting, DK, Ledoux, JB, Lejeusne, C, Linares, C, Marschal, C, Pérez, T, Ribes, M, Romano, JC, Serrano, E, Teixido, N, Torrents, O, Zabala, M, Zuberer, F and Cerrano, C (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biology 15, 1090–1103.Google Scholar
Gatesoupe, F-J, Lambert, C and Nicolas, J-L (1999) Pathogenicity of Vibrio splendidus strains associated with turbot larvae, Scophthalmus maximus. Journal of Applied Microbiology 87, 757–763.Google Scholar
Geiser, DM, Taylor, JW, Ritchie, KB and Smith, GW (1998) Cause of sea fan death in the West Indies. Nature 394, 137–138.Google Scholar
Gómez-León, J, Villamil, L, Lemos, M, Novoa, B and Figueras, A (2005) Isolation of Vibrio alginolyticus and Vibrio splendidus from aquacultured carpet shell clam (Ruditapes decussatus) larvae associated with mass mortalities. Applied and Environmental Microbiology 71, 98–104.Google Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Proceedings of the Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hall-Spencer, JM, Pike, J and Munn, CB (2007) Diseases affect cold-water corals too: Eunicella verrucosa (Cnidaria: Gorgonacea) necrosis in SW England. Diseases of Aquatic Organisms 76, 87–97.Google Scholar
Hanley, J (2011) Environmental monitoring programs on recent capital dredging projects in the Pilbara (2003–10): a review. Australian Petroleum Production & Exploration Association (APPEA) 51, 273–294.Google Scholar
Harvell, CD, Mitchell, CE, Ward, JR, Altizer, S, Dobson, AP, Ostfeld, RS and Samuel, MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.Google Scholar
Haywood, MDE, Dennis, D, Thomson, DP and Pillans, RD (2016) Mine waste disposal leads to lower coral cover, reduced species richness and a predominance of simple coral growth forms on a fringing coral reef in Papua New Guinea. Marine Environmental Research 115, 36–48.Google Scholar
Hendrick, VJ, Hutchison, ZL and Last, KS (2016) Sediment burial intolerance of marine macroinvertebrates. PLoS ONE 11, e0149114.Google Scholar
Huete-Stauffer, C, Vielmini, I, Palma, M, Navone, A, Panzalis, P, Vezzulli, L, Misic, C and Cerrano, C (2011) Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Marine Ecology 32(s1), 107–116.Google Scholar
Iwen, PC, Sigler, L, Noel, RK and Freifeld, AG (2007) Mucor circinelloides was identified by molecular methods as a cause of primary cutaneous zygomycosis. Journal of Clinical Microbiology 45, 636–640.Google Scholar
Karan, MA, Tunçcan, ÖG, Kalkancı, A, Arman, D and Kuştimur, S (2014) Widespread colonization of Mucor circinelloides in a patient with type 2 diabetes and colon cancer: case report. Turkiye Klinikleri Journal of Case Reports 22, 186–190.Google Scholar
Kayisoglu, M (2016) Investigation of the Interaction Between the Black Sea and the Sea of Marmara with Monthly Data Series of Temperature and Salinity (Master thesis). Istanbul University Institute of Marine Sciences and Management, Turkey.Google Scholar
Ke, X, Wang, J, Li, M, Gu, Z and Gong, X (2009) First report of Mucor circinelloides occurring on yellow catfish (Pelteobagrus fulvidraco) from China. FEMS Microbiology Letters 302, 144–150.Google Scholar
Krediet, CJ, Ritchie, KB, Paul, VJ and Teplitski, M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proceedings of the Royal Society of London B: Biological Sciences 280, 20122328.Google Scholar
Kurt, S, Karaburun, A and Demirci, A (2010) Coastline changes in Istanbul between 1987 and 2007. Scientific Research and Essays 5, 3009–3017.Google Scholar
Kushmaro, A, Banin, E, Loya, Y, Stackebrandt, E and Rosenberg, E (2001) Vibrio shiloi sp. nov., the causative agent of bleaching of the coral Oculina patagonica. International Journal of Systematic and Evolutionary Microbiology 51, 1383–1388.Google Scholar
Lacoste, A, Jalabert, F, Malham, S, Cueff, A, Gelebart, F, Cordevant, C, Lange, M and Poulet, S (2001) A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Diseases of Aquatic Organisms 46, 139–145.Google Scholar
Larkin, MA, Blackshields, G, Brown, N, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A and Lopez, R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Li, X, Huang, H, Lian, J, Yang, J, Ye, C, Chen, Y and Huang, L (2013) Coral community changes in response to a high sedimentation event: a case study in southern Hainan Island. Chinese Science Bulletin 58, 1028–1037.Google Scholar
Linares, C, Coma, R, Diaz, D, Zabala, M, Hereu, B and Dantart, L (2005) Immediate and delayed effects of a mass mortality event on gorgonian population dynamics and benthic community structure in the NW Mediterranean Sea. Marine Ecology Progress Series 305, 127–137.Google Scholar
Linares, C, Coma, R, Garrabou, J, Diaz, D and Zabala, M (2008 a) Size distribution, density and disturbance of two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. Journal of Applied Ecology 45, 688–699.Google Scholar
Linares, C, Coma, R, Mariani, S, Díaz, D, Hereu, B and Zabala, M (2008 b) Early life history of the Mediterranean gorgonian Paramuricea clavata: implications for population dynamics. Invertebrate Biology 127, 1–11.Google Scholar
Linares, C, Coma, R and Zabala, M (2008 c) Effects of a mass mortality event on gorgonian reproduction. Coral Reefs 27, 27–34.Google Scholar
Lohrer, A, Hewitt, J, Thrush, S, Lundquist, C, Nicholls, P and Liefting, R (2003) Impact of Terrigenous Material Deposition on Subtidal Benthic Communities. Hamilton: Auckland Regional Council, Technical Publication No. 217.Google Scholar
Luna, G, Biavasco, F and Danovaro, R (2007) Bacteria associated with the rapid tissue necrosis of stony corals. Environmental Microbiology 9, 1851–1857.Google Scholar
Luna, GM, Bongiorni, L, Gili, C, Biavasco, F and Danovaro, R (2010) Vibrio harveyi as a causative agent of the White Syndrome in tropical stony corals. Environmental Microbiology Reports 2, 120–127.Google Scholar
Maina, J, de Moel, H, Zinke, J, Madin, J, McClanahan, T and Vermaat, JE (2013) Human deforestation outweighs future climate change impacts of sedimentation on coral reefs. Nature Communications 4, 1986.Google Scholar
Nagelkerken, I, Buchan, K, Smith, G, Bonair, K, Bush, P, Garzon-Ferreira, J, Botero, L, Gayle, P, Harvell, C and Heberer, C (1997) Widespread disease in Caribbean sea fans: II. Patterns of infection and tissue loss. Marine Ecology Progress Series 160, 255–263.Google Scholar
Nepote, E, Bianchi, CN, Morri, C, Chiantore, M and Montefalcone, M (2016) Pattern and intensity of human impact on coral reefs depend on depth along the reef profile and on the descriptor adopted. Estuarine Coastal and Shelf Science 178, 86–91.Google Scholar
Nepote, E, Bianchi, CN, Morri, C, Ferrari, M and Montefalcone, M (2017) Impact of a harbour construction on the benthic community of two shallow marine caves. Marine Pollution Bulletin 114, 35–45.Google Scholar
Özsoy, E, Çağatay, MN, Balkıs, N, Balkıs, N and Öztürk, B (eds) (2016) The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Istanbul: Turkish Marine Research Foundation (TUDAV). Publication No: 42.Google Scholar
Pascual, J, Macián, MC, Arahal, DR, Garay, E and Pujalte, MJ (2010) Multilocus sequence analysis of the central clade of the genus Vibrio by using the 16S rRNA, recA, pyrH, rpoD, gyrB, rctB and toxR genes. International Journal of Systematic and Evolutionary Microbiology 60, 154–165.Google Scholar
Pastorok, RA and Bilyard, GR (1985) Effects of sewage pollution on coral-reef communities. Marine Ecology Progress Series. Oldendorf 21, 175–189.Google Scholar
Perez, T, Garrabou, J, Sartoretto, S, Harmelin, J-G, Francour, P and Vacelet, J (2000) Mortalité massive d'invertébrés marins : un événement sans précédent en Méditerranée nord-occidentale. Comptes Rendus de l'Académie des Sciences – Series III – Sciences de la Vie 323, 853–865.Google Scholar
Peters, EC (2015) Diseases of coral reef organisms. In Birkeland C. (ed.), Coral Reefs in the Anthropocene. Dordrecht: Springer, pp 147–178.Google Scholar
Ponti, M, Perlini, RA, Ventra, V, Grech, D, Abbiati, M and Cerrano, C (2014) Ecological shifts in Mediterranean coralligenous assemblages related to gorgonian forest loss. PLoS ONE 9, e102782.Google Scholar
Prado, S, Romalde, JL, Montes, J and Barja, JL (2005) Pathogenic bacteria isolated from disease outbreaks in shellfish hatcheries. First description of Vibrio neptunius as an oyster pathogen. Diseases of Aquatic Organisms 67, 209–215.Google Scholar
Raymundo, L, Couch, C and Harvell, CD (eds) (2008) Coral Disease Handbook: Guidelines for Assessment, Monitoring and Management. Melbourne: Currie Communications.Google Scholar
Richardson, M (2009) The ecology of the Zygomycetes and its impact on environmental exposure. Clinical Microbiology and Infection 15(s5), 2–9.Google Scholar
Rivetti, I, Fraschetti, S, Lionello, P, Zambianchi, E and Boero, F (2014) Global warming and mass mortalities of benthic invertebrates in the Mediterranean Sea. PLoS ONE 9, e115655.Google Scholar
Rivetti, I, Boero, F, Fraschetti, S, Zambianchi, E and Lionello, P (2017) Anomalies of the upper water column in the Mediterranean Sea. Global and Planetary Change 151, 68–79.Google Scholar
Rubio-Portillo, E, Izquierdo-Muñoz, A, Gago, JF, Rosselló-Mora, R, Antón, J and Ramos-Esplá, AA (2016) Effects of the 2015 heat wave on benthic invertebrates in the Tabarca Marine Protected Area (southeast Spain). Marine Environmental Research 122, 135–142.Google Scholar
Santangelo, G, Cupido, R, Cocito, S, Bramanti, L, Priori, C, Erra, F and Iannelli, M (2015) Effects of increased mortality on gorgonian corals (Cnidaria, Octocorallia): different demographic features may lead affected populations to unexpected recovery and new equilibrium points. Hydrobiologia 759, 171–187.Google Scholar
Santos, SR and Ochman, H (2004) Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environmental Microbiology 6, 754–759.Google Scholar
Schoch, CL, Seifert, KA, Huhndorf, S, Robert, V, Spouge, JL, Levesque, CA, Chen, W, Bolchacova, E, Voigt, K and Crous, PW (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences USA 109, 6241–6246.Google Scholar
Shahidul Islam, M and Tanaka, M (2004) Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Marine Pollution Bulletin 48, 624–649.Google Scholar
Sheppard, C, Al-Husiani, M, Al-Jamali, F, Al-Yamani, F, Baldwin, R, Bishop, J, Benzoni, F, Dutrieux, E, Dulvy, NK and Durvasula, SRV (2010) The Gulf: a young sea in decline. Marine Pollution Bulletin 60, 13–38.Google Scholar
Sheridan, C, Kramarsky-Winter, E, Sweet, M, Kushmaro, A and Leal, MC (2013) Diseases in coral aquaculture: causes, implications and preventions. Aquaculture 396, 124–135.Google Scholar
Smith, GW, Ives, LD, Nagelkerken, IA and Ritchie, KB (1996) Caribbean sea-fan mortalities. Nature 383, 487–487.Google Scholar
Stabili, L, Cardone, F, Alifano, P, Tredici, SM, Piraino, S, Corriero, G and Gaino, E (2012) Epidemic mortality of the sponge Ircinia variabilis (Schmidt, 1862) associated to proliferation of a Vibrio bacterium. Microbial Ecology 64, 802–813.Google Scholar
Suau, A, Bonnet, R, Sutren, M, Godon, J-J, Gibson, GR, Collins, MD and Doré, J (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environmental Microbiology 65, 4799–4807.Google Scholar
Thompson, FL, Iida, T and Swings, J (2004) Biodiversity of vibrios. Microbiology and Molecular Biology Reviews 68, 403–431.Google Scholar
Thrush, SF, Hewitt, JE, Cummings, VJ, Ellis, JI, Hatton, C, Lohrer, A and Norkko, A (2004) Muddy waters: elevating sediment input to coastal and estuarine habitats. Frontiers in Ecology and the Environment 2, 299–306.Google Scholar
Topaloğlu, B (2016) Sponges of the Sea of Marmara with a new record for Turkish sponge fauna. In Özsoy, E, Çağatay, MN, Balkıs, N, Balkıs, N and Öztürk, B (eds), The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Istanbul: Turkish Marine Research Foundation (TUDAV). Publication No. 42, pp. 418–450.Google Scholar
Topaloğlu, B, Evcen, A and Çınar, ME (2016) Sponge fauna in the Sea of Marmara. Turkish Journal of Fisheries and Aquatic Sciences 16, 51–59.Google Scholar
Topçu, NE and Öztürk, B (2013) Octocoral diversity of Balıkçı Island, the Marmara Sea. Journal of the Black Sea/Mediterranean Environment 19, 46–57.Google Scholar
Topçu, NE and Öztürk, B (2015) Composition and abundance of octocorals in the Sea of Marmara, where the Mediterranean meets the Black Sea. Scientia Marina 79, 125–135.Google Scholar
Topçu, NE and Öztürk, B (2016 a) First insights into the demography of the rare gorgonian Spinimuricea klavereni in the Mediterranean Sea. Marine Ecology 37, 1154–1160.Google Scholar
Topçu, NE and Öztürk, B (2016 b) Reproduction in the Mediterranean endemic gorgonian Spinimuricea klavereni (Anthozoa, Octocorallia, Plexauridae). Invertebrate Biology 135, 13–19.Google Scholar
Topçu, NE, Martell, LF, Yılmaz, İN and İşinibilir, M (2016) Hydrozoans as pioneer colonizers after a mass mortality event in the Sea of Marmara. Rapp. Comm. int. Mer Médit. 41, 369.Google Scholar
Turkoglu, M (2016) Bloom dynamics of Emiliania Huxleyi (Lohmann) Hay & Mohler, 1967 in the Sea of Marmara: a review. In Thajuddin, N and Dhanasekaran, D (eds), Algae, Organisms for Imminent Biotechnology. IntechOpen. Published online 29 June 2016.Google Scholar
Ushijima, B, Smith, A, Aeby, GS and Callahan, SM (2012) Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata. PLoS ONE 7, e46717.Google Scholar
Vezzulli, L, Previati, M, Pruzzo, C, Marchese, A, Bourne, DG and Cerrano, C (2010) Vibrio infections triggering mass mortality events in a warming Mediterranean Sea. Environmental Microbiology 12, 2007–2019.Google Scholar
Vezzulli, L, Pezzati, E, Huete-Stauffer, C, Pruzzo, C and Cerrano, C (2013) 16SrDNA pyrosequencing of the Mediterranean gorgonian Paramuricea clavata reveals a link among alterations in bacterial holobiont members, anthropogenic influence and disease outbreaks. PLoS ONE 8, e67745.Google Scholar
Ward, JR and Lafferty, KD (2004) The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? PLOS Biology 2, e120.Google Scholar
White, TJ, Bruns, T, Lee, S and Taylor, J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: a Guide to Methods and Applications 18, 315–322.Google Scholar
Zhang, Z, Schwartz, S, Wagner, L and Miller, W (2000) A greedy algorithm for aligning DNA sequences. Journal of Computational Biology 7, 203–214.Google Scholar
Zhao, Y, Zhang, W, Xu, W, Mai, K, Zhang, Y and Liufu, Z (2012) Effects of potential probiotic Bacillus subtilis T13 on growth, immunity and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus. Fish and Shellfish Immunology 32, 750–755.Google Scholar
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