Research Article

DOI :10.26650/ASE20241434217   IUP :10.26650/ASE20241434217    Full Text (PDF)

Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data

Onur DoğanAnıl Doğan ÖrünRaşit BilginMelek İşinibilir Okyar

Mucilage events are among the most conspicuous phenomena in marine ecosystems and present numerous challenges in determining the composition of communities associated with them. To overcome this problem, we used environmental DNA (eDNA) metabarcoding approaches to reveal the species-level resolution of community composition. Mucilaginous aggregates were sampled at six collecting sites during a novel mucilage event (autumn 2021–summer 2022) in the Sea of Marmara, Türkiye. A wide range of plankton community compositions was detected in mucilage samples. eDNA metabarcoding was effective in predicting the community composition of mucilage, which is composed of a wide variety of organisms from mucilaginous aggregates.

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  • Aksu, A., Balkis, N., Taşkin, Ö. S., & Erşan, M. S. (2011). Toxic metal (Pb, Cd, As and Hg) and organochlorine residue levels in hake (Merluccius merluccius) from the Marmara Sea, Turkey. Environmental monitoring and assessment, 182, 509-521. google scholar
  • Albayrak, S., Balkis, H., Zenetos, A., Kurun, A., & Kubanç, C. (2006). Ecological quality status of coastal benthic ecosystems in the Sea of Marmara. Marine Pollution Bulletin, 52(7), 790-799. https://doi. org/10.1016/j.marpolbul.2005.11.022 google scholar
  • Algan, O., Balkıs, N., Çağatay, M. N., & Sarı, E. (2004). The sources of metal contents in the shelf sediments from the Marmara Sea, Turkey. Environmental Geology, 46, 932-950. s00254-004-1104-2 google scholar
  • Almeda, R., Baca, S., Hyatt, C., & Buskey, E. J. (2014). Ingestion and sublethal effects of physically and chemically dispersed crude oil on marine planktonic copepods. Ecotoxicology, 23, 988-1003. https:// google scholar
  • Almeda, R., Connelly, T. L., & Buskey, E. J. (2016). How much crude oil can zooplankton ingest? Estimating the quantity of dispersed crude oil defecated by planktonic copepods. Environmental pollution, 208, 645-654. google scholar
  • Altiok, H., & Kayişoğlu, M. (2015). Seasonal and interannual variability of water exchange in the Strait of Istanbul. Mediterranean Marine Science, 16(3), 644-655. google scholar
  • Amsler, C. D., Iken, K., McClintock, J. B., Amsler, M. O., Peters, K. J., Hubbard, J. M., ... & Baker, B. J. (2005). Comprehensive evaluation of the palatability and chemical defenses of subtidal macroalgae from the Antarctic Peninsula. Marine Ecology Progress Series, 294, 141159. google scholar
  • Balint, M., Pfenninger, M., Grossart, H. P., Taberlet, P., Vellend, M., Leibold, M. A., ... & Bowler, D. (2018). Environmental DNA time series in ecology. Trends in Ecology & Evolution, 33(12), 945-957. https:// google scholar
  • Balkıs, N., & Çağatay, M. N. (2001). Factors controlling metal distributions in the surface sediments of the Erdek Bay, Sea of Marmara, Turkey. Environment international, 27(1), 1-13. google scholar
  • Balkis, N., Atabay, H., Türetgen, I., Albayrak, S., Balkis, H., & Tüfekçi, V. (2011). Role of single-celled organisms in mucilage formation on the shores of Büyükada Island (the Marmara Sea). Journal of the Marine Biological Association of the United Kingdom, 91(4), 771-781. https:// google scholar
  • Balkis-Ozdelice, N., Durmuş, T., & Balci, M. (2021). A preliminary study on the intense pelagic and benthic mucilage phenomenon observed in the Sea of Marmara. International Journal of Environment and Geoinformatics, 8(4), 414-422. google scholar
  • Barbour, M. T. (1999). Rapid bioassessment protocols for use in wadeable streams and rivers: periphyton, benthic macroinvertebrates and fish. US Environmental Protection Agency, Office of Water. google scholar
  • Berry, T. E., Saunders, B. J., Coghlan, M. L., Stat, M., Jarman, S., Richardson, A. J., ... & Bunce, M. (2019). Marine environmental DNA biomonitoring reveals seasonal patterns in biodiversity and identifies ecosystem responses to anomalous climatic events. PLoS genetics, 15(2), e1007943. google scholar
  • Beşiktepe, Ş. T., Sur, H. I., Özsoy, E., Latif, M. A., Oğuz, T., & Ünlüata, Ü. (1994). The circulation and hydrography of the Marmara Sea. Progress in Oceanography, 34(4), 285-334. google scholar
  • Bik, H. M., Porazinska, D. L., Creer, S., Caporaso, J. G., Knight, R., & Thomas, W. K. (2012). Sequencing our way towards understanding global eukaryotic biodiversity. Trends in ecology & evolution, 27(4), 233-243. google scholar
  • Bosch, T. C. (2013). Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Annual review of microbiology, 67,499-518. google scholar
  • Brodeur, R. D., Sugisaki, H., & Hunt Jr, G. L. (2002). Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Marine Ecology Progress Series, 233, 89-103. meps233089 google scholar
  • Buchner, D., & Leese, F. (2020). BOLDigger-a Python package to identify and organise sequences with the Barcode of Life Data systems. Metabarcoding and Metagenomics, 4, e53535. https://doi. org/10.3897/mbmg.4.53535 google scholar
  • Buchner, D., Macher, T. H., & Leese, F. (2022). APSCALE: advanced pipeline for simple yet comprehensive analyses of DNA metabarcoding data. Bioinformatics, 38(20), 4817-4819. https://doi. org/10.3897/mbmg.4.53535 google scholar
  • Burak, S., Unlu, S., & Gazıoglu, C. (2009). Environmental stress created by chemical pollution in the Marmara sea (Turkey). Asian Journal of Chemistry, 21(4), 3166-3174. google scholar
  • Burd, A. B., Chanton, J. P., Daly, K. L., Gilbert, S., Passow, U., & Quigg, A. (2020). The science behind marine-oil snow and MOSSFA: past, present, and future. Progress in Oceanography, 187, 102398. https:// google scholar
  • Burkholder, J. M., & Glasgow Jr, H. B. (1997). Pfiesteria piscicida and other Pfiesreria-like dinoflagellates: Behavior, impacts, and environmental controls. Limnology and Oceanography, 42(5part2), 1052-1075. google scholar
  • Buxton, A., Matechou, E., Griffin, J., Diana, A., & Griffiths, R. A. (2021). Optimising sampling and analysis protocols in environmental DNA studies. Scientific Reports, 11(1), 11637. s41598-021-91166-7 google scholar
  • Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., ... & Naeem, S. (2012). Biodiversity loss and its impact on humanity. Nature, 486(7401), 59-67. google scholar
  • Conover, R. J. (1971). Some relations between zooplankton and bunker C oil in Chedabucto Bay following the wreck of the tanker Arrow. Journal of the Fisheries Board of Canada, 28(9), 1327-1330. google scholar
  • Çağatay, M. N., Eriş, K., Ryan, W. B. F., Sancar, Ü., Polonia, A., Akçer, S., ... & Bard, E. (2009). Late Pleistocene-Holocene evolution of the northern shelf of the Sea of Marmara. Marine Geology, 265(3-4), 87100. google scholar
  • Çağatay, M. N., Wulf, S., Sancar, Ü., Özmaral, A., Vidal, L., Henry, P., ... & Gasperini, L. (2015). The tephra record from the Sea of Marmara for the last ca. 70 ka and its palaeoceanographic implications. Marine Geology, 361, 96-110. google scholar
  • Castejon-Silvo, I., & Terrados, J. (2017). Experimental assessment of Posidonia oceanica-associated gastropods grazing on an early-successional biofilm community: nutrient availability and species-specific effects. Marine Ecology, 38(1), e12381. https://doi. org/10.1111/maec.12381 google scholar
  • D’alelio, D., Cante, M. T., Russo, G. F., Totti, C., & De Stefano, M. (2011). Epizoic diatoms on gastropod shells: when substrate complexity selects for microcommunity complexity. All flesh is grass: Plant-animal interrelationships, 345-364. google scholar
  • Dahms, H. U., & Dobretsov, S. (2017). Antifouling compounds from marine macroalgae. Marine Drugs, 15(9), 265. google scholar
  • Dang, H., & Lovell, C. R. (2016). Microbial surface colonization and biofilm development in marine environments. Microbiology and molecular biology reviews, 80(1), 91-138. google scholar
  • Danovaro, R., Fonda Umani, S., & Pusceddu, A. (2009). Climate change and the potential spreading of marine mucilage and microbial pathogens in the Mediterranean Sea. PLoS One, 4(9), e7006. google scholar
  • Darling, J. A., & Mahon, A. R. (2011). From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environmental research, 111(7), 978-988. google scholar
  • Das, T., Sehar, S., & Manefield, M. (2013). The roles of extracellular DNA in the structural integrity of extracellular polymeric substance and bacterial biofilm development. Environmental microbiology reports, 5(6), 778-786. google scholar
  • Davenport, J., Smith, R. J., & Packer, M. (2000). Mussels Mytilus edulis: significant consumers and destroyers of mesozooplankton. Marine Ecology Progress Series, 198, 131-137. meps198131 google scholar
  • Del Campo, J., Sieracki, M. E., Molestina, R., Keeling, P., Massana, R., & Ruiz-Trillo, I. (2014). The others: our biased perspective of eukaryotic genomes. Trends in ecology & evolution, 29(5), 252-259. https://doi. org/10.1016/j.tree.2014.03.006 google scholar
  • Demirel, N., Akoglu, E., Ulman, A., Ertor-Akyazi, P., Gül, G., Bedikoğlu, D., ... & Yilmaz, I. N. (2023). Uncovering ecological regime shifts in the Sea of Marmara and reconsidering management strategies. Marine Environmental Research, 183, 105794. marenvres.2022.105794 google scholar
  • Deniz, N., Taş, S., & Koray, T. (2006). New records of the Dictyocha antarctica Lohmann, Dictyocha crux Ehrenberg and Nitzschia rectilonga Takano species from the Sea of Marmara. Turkish Journal of Botany, 30(3), 213-216. google scholar
  • D^az, E., Güldenzoph, C., Molis, M., McQuaid, C., & Wahl, M. (2006). Variability in grazer-mediated defensive responses of green and red macroalgae on the south coast of South Africa. Marine Biology, 149, 1301-1311. google scholar
  • Dobretsov, S. (2010). Marine biofilms. Biofouling, 123-136. https://doi. org/10.1002/9781444315462.ch9 google scholar
  • Dogan, O., Örün, D. A., Bilgin, R., İşinibilir, M., Using the metabarcoding approach for characterization of community diversity in the Sea of Marmara. Ecological Changes in the Sea of Marmara. (In press). google scholar
  • Duarte, M. E., Cauduro, J. P., Noseda, D. G., Noseda, M. D., Gonçalves, A. G., Pujol, C. A., ... & Cerezo, A. S. (2004). The structure of the agaran sulfate from Acanthophora spicifera (Rhodomelaceae, Ceramiales) and its antiviral activity. Relation between structure and antiviral activity in agarans. Carbohydrate Research, 339(2), 335-347. google scholar
  • Elbrecht, V. (2022, January 7). Just Another Metabarcoding Pipeline. Retrieved from Github: google scholar
  • Ergul, H. A., Balkis-Ozdelice, N., Koral, M., Aksan, S., Durmus, T., Kaya, M., ... & Canli, O. (2021). The early stage of mucilage formation in the Marmara Sea during spring 2021. Journal of the Black Sea/ Mediterranean Environment, 27(2). google scholar
  • Faganeli, J., Mohar, B., Kofol, R., Pavlica, V., Marinsek, T., Rozman, A., ... & Vuk, A. S. (2010). Nature and lability of Northern Adriatic macroaggregates. Marine drugs, 8(9), 2480-2492. https://doi. org/10.3390/md8092480 google scholar
  • Finkel, S. E., & Kolter, R. (2001). DNA as a nutrient: novel role for bacterial competence gene homologs. Journal of bacteriology, 183(21), 62886293. google scholar
  • Fisher, C. R., Demopoulos, A. W., Cordes, E. E., Baums, I. B., White, H. K., & Bourque, J. R. (2014). Coral communities as indicators of ecosystem-level impacts of the Deepwater Horizon spill. Bioscience, 64(9), 796807. google scholar
  • Fr0slev, T. G., Kjoller R., Bruun, H. H., Ejrn^s, R., Brunbjerg, A. K., Pietroni, C., & Hansen, A. J. (2017). Algorithm for post-clustering curation of DNA amplicon data yields reliable biodiversity estimates. Nature communications, 8(1), 1188. google scholar
  • Fuks, D., Radic, J., Radic, T., Najdek, M., Blazina, M., Degobbis, D., & Smodlaka, N. (2005). Relationships between heterotrophic bacteria and cyanobacteria in the northern Adriatic in relation to the mucilage phenomenon. Science of the total environment, 353(1-3), 178-188. google scholar
  • Gacia, E., Costalago, D., Prado, P., Piorno, D., & Tomas, F. (2009). Mesograzers in Posidonia oceanica meadows: an update of data on gastropod-epiphyte-seagrass interactions. bot.2009.054 google scholar
  • Genitsaris, S., Stefanidou, N., Sommer, U., & Moustaka-Gouni, M. (2019). Phytoplankton blooms, red tides and mucilaginous aggregates in the urban Thessaloniki Bay, Eastern Mediterranean. Diversity, 11(8), 136. google scholar
  • Gobler, C. J., Berry, D. L., Anderson, O. R., Burson, A., Koch, F., Rodgers, B. S., ... & Nuzzi, R. (2008). Characterization, dynamics, and ecological impacts of harmful Cochlodinium polykrikoides blooms on eastern Long Island, NY, USA. Harmful Algae, 7(3), 293-307. https://doi. org/10.1016/j.hal.2007.12.006 google scholar
  • Gram, L., Grossart, H. P., Schlingloff, A., & Ki0rboe, T. (2002). Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Applied and Environmental Microbiology, 68(8), 4111-4116. google scholar
  • Güneralp, B., Xu, X., & Lin, W. (2021). Infrastructure development with (out) ecological conservation: the Northern Forests in İstanbul. Regional Environmental Change, 21(3), 86. https://doi. org/10.1007/s10113-021-01807-w google scholar
  • Haavisto, F., Vâlikangas, T., & Jormalainen, V. (2010). Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore. Oecologia, 162, 685-695. https://doi. org/10.1007/s00442-009-1494-7 google scholar
  • Isinibilir, M., Kideys, A. E., Tarkan, A. N., & Yilmaz, I. N. (2008). Annual cycle of zooplankton abundance and species composition in Izmit Bay (the northeastern Marmara Sea). Estuarine, Coastal and Shelf Science, 78(4), 739-747. google scholar
  • Jennings, S., & Kaiser, M. J. (1998). The effects of fishing on marine ecosystems. In Advances in marine biology (Vol. 34, pp. 201-352). Academic Press. google scholar
  • Karaca, F. (2013). Mapping the corrosion impact of air pollution on the historical peninsula of Istanbul. Journal of Cultural Heritage, 14(2), 129-137. google scholar
  • Kelly, R. P., Port, J. A., Yamahara, K. M., Martone, R. G., Lowell, N., Thomsen, P. F., ... & Crowder, L. B. (2014). Harnessing DNA to improve environmental management. Science, 344(6191), 1455-1456. https:// google scholar
  • Keskin, E. (2014). Detection of invasive freshwater fish species using environmental DNA survey. Biochemical Systematics and Ecology, 56, 68-74. google scholar
  • Korkmaz, N. E., Savun-Hekimoğlu, B., Aksu, A., Burak, S., & Caglar, N. B. (2022). Occurrence, sources and environmental risk assessment of pharmaceuticals in the Sea of Marmara, Turkey. Science of The Total Environment, 819, 152996. google scholar
  • Kos Kramar, M., Tinta, T., Lucic, D., Malej, A., & Turk, V. (2019). Bacteria associated with moon jellyfish during bloom and post-bloom periods in the Gulf of Trieste (northern Adriatic). PloS one, 14(1), e0198056. google scholar
  • Kovac, N., Viers, J., Faganeli, J., Bajt, O., & Pokrovsky, O. S. (2023). Elemental Composition of Plankton Exometabolites (Mucous Macroaggregates): Control by Biogenic and Lithogenic Components. Metabolites, 13(6), 726. metabo13060726 google scholar
  • Leray, M., Yang, J. Y., Meyer, C. P., Mills, S. C., Agudelo, N., Ranwez, V., ... & Machida, R. J. (2013). A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gutcontents. Frontiers in zoology, 10(1), 1-14. google scholar
  • Lotze, H. K., Lenihan, H. S., Bourque, B. J., Bradbury, R. H., Cooke, R. G., Kay, M. C., ... & Jackson, J. B. (2006). Depletion, degradation, and recovery potential of estuaries and coastal seas. Science, 312(5781), 1806-1809. google scholar
  • Macher, T. H., Beermann, A. J., & Leese, F. (2021). TaxonTableTools: A comprehensive, platform-independent graphical user interface software to explore and visualise DNA metabarcoding data. Molecular Ecology Resources, 21(5), 1705-1714. google scholar
  • Mâchler, E., Deiner, K., Steinmann, P., & Altermatt, F. (2014). Utility of environmental DNA for monitoring rare and indicator macroinvertebrate species. Freshwater Science, 33(4), 1174-1183. google scholar
  • MacKenzie, L., Sims, I., Beuzenberg, V., & Gillespie, P. (2002). Mass accumulation of mucilage caused by dinoflagellate polysaccharide exudates in Tasman Bay, New Zealand. Harmful algae, 1(1), 69-83. google scholar
  • Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal, 17(1), 10-12. Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal, 17(1), 10-12. https:// google scholar
  • Mecozzi, M., Pietroletti, M., Scarpiniti, M., Acquistucci, R., & Conti, M. E. (2012). Monitoring of marine mucilage formation in Italian seas investigated by infrared spectroscopy and independent component analysis. Environmental Monitoring and Assessment, 184, 6025-6036. google scholar
  • Metzger, U., Lankes, U., Fischpera, K., & Frimmel, F. H. (2009). The concentration of polysaccharides and proteins in EPS of Pseudomonas putida and Aureobasidum pullulans as revealed by 13 C CPMAS NMR spectroscopy. Applied microbiology and biotechnology, 85, 197-206. google scholar
  • Mitra, S., Kimmel, D. G., Snyder, J., Scalise, K., McGlaughon, B. D., Roman, M. R., ... & Campbell, P. L. (2012). Macondo-1 well oil-derived polycyclic aromatic hydrocarbons in mesozooplankton from the northern Gulf of Mexico. Geophysical Research Letters, 39(1). https:// google scholar
  • Montagna, P. A., Baguley, J. G., Cooksey, C., Hartwell, I., Hyde, L. J., Hyland, J. L., ... & Rhodes, A. C. (2013). Deep-sea benthic footprint of the Deepwater Horizon blowout. PloS one, 8(8), e70540. https://doi. org/10.1371/journal.pone.0070540 google scholar
  • Muhammad, M. H., Idris, A. L., Fan, X., Guo, Y., Yu, Y., Jin, X., ... & Huang, T. (2020). Beyond risk: bacterial biofilms and their regulating approaches. Frontiers in microbiology, 11, 928. https://doi. org/10.3389/fmicb.2020.00928 google scholar
  • Nagasoe, S., Toda, S., Shimasaki, Y., Oshima, Y., Uchida, T., & Honjo, T. (2006). Growth inhibition of Gyrodinium instriatum (Dinophyceae) by Skeletonema costatum (Bacillariophyceae). African Journal of Marine Science, 28(2), 325-329. google scholar
  • NASA Earth Observatory. (2015, May 17). Blooms in the Sea of Marmara. Retrieved from NASA Earth Observatory: https://earthobservatory. google scholar
  • Ogram, A., Sayler, G. S., & Barkay, T. (1987). The extraction and purification of microbial DNA from sediments. Journal of microbiological methods, 7(2-3), 57-66. google scholar
  • Okay, O. S., Legovic, T., Tüfekçi, V., Egesel, L., & Morkoç, E. (1996). Environmental impact of land-based pollutants on Izmit Bay (Turkey): short-term algal bioassays and simulation of toxicity distribution in the marine environment. Archives of Environmental Contamination and Toxicology, 31, 459-465. google scholar
  • Okay, O. S. (1998). Investigation of three wastewaters entering Izmit Bay (Turkey) by means of batch and chemostat culture algal bioassays. google scholar
  • Marine environmental research, 46(1-5), 283-288. https://doi. org/10.1016/s0141-1136(97)00115-3 google scholar
  • Okay, O. S., Egesel, L., Tüfekçi, V., Morkoç, E., & Gaines, A. (1998). Investigation of three wastewaters entering Izmit Bay (Turkey) by means of batch and chemostat culture algal bioassays. Marine environmental research, 46(1-5), 283-288. s0141-1136(97)00115-3 google scholar
  • İşinibilir-Okyar, M., Üstün, F., & Orun, D. A. (2015). Changes in abundance and community structure of the zooplankton population during the 2008 mucilage event in the northeastern Marmara Sea. Turkish Journal of Zoology, 39(1), 28-38. google scholar
  • Onar, V., Alpak, H., Pazvant, G., Armutak, A., Gezer İnce, N. A. Z. A. N., & Kızıltan, Z. (2013). A bridge from Byzantium to modern day Istanbul: An overview of animal skeleton remains found during Metro and Marmaray excavations. Istanbul Univ Vet Fak Derg, 39, 1-8. https:// google scholar
  • Pochon, X., Bott, N. J., Smith, K. F., & Wood, S. A. (2013). Evaluating detection limits of next-generation sequencing for the surveillance and monitoring of international marine pests. PloS one, 8(9), e73935. google scholar
  • Pompei, M., Mazziotti, C., Guerrini, F., Cangini, M., Pigozzi, S., Benzi, M., ... & Pistocchi, R. (2003). Correlation between the presence of Gonyaulax fragilis (Dinophyceae) and the mucilage phenomena of the Emilia-Romagna coast (northern Adriatic Sea). Harmful algae, 2(4), 301-316. google scholar
  • Purcell, J. E. (2005). Climate effects on formation of jellyfish and ctenophore blooms: a review. Journal of the Marine Biological Association of the United kingdom, 85(3), 461-476. https://doi. org/10.1017/s0025315405011409 google scholar
  • Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahe, F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584. google scholar
  • Salta, M., Wharton, J. A., Blache, Y., Stokes, K. R., & Briand, J. F. (2013). Marine biofilms on artificial surfaces: structure and dynamics. Environmental microbiology, 15(11), 2879-2893. https:// google scholar
  • Schwing, P. T., Romero, I. C., Brooks, G. R., Hastings, D. W., Larson, R. A., & Hollander, D. J. (2015). A decline in benthic foraminifera following the Deepwater Horizon event in the northeastern Gulf of Mexico. PloS one, 10(3), e0120565. google scholar
  • Shanks, A. L., & Walters, K. (1997). Holoplankton, meroplankton, and meiofauna associated with marine snow. Marine Ecology Progress Series, 156, 75-86. google scholar
  • Smith, V. H. (2003). Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research, 10, 126-139. google scholar
  • Sommer, U., & Lengfellner, K. (2008). Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom. Global Change Biology, 14(6), 1199-1208. https://doi. org/10.1111/j.1365-2486.2008.01571.x google scholar
  • Taberlet, P., Bonin, A., Zinger, L., & Coissac, E. (2018). Environmental DNA: For biodiversity research and monitoring. Oxford University Press. google scholar
  • Taberlet, P. C. (2012). Environmental dna. Molecular ecology, 21(8), 17891793. google scholar
  • Tas, S., Kus, D., & Yilmaz, I. N. (2020). Temporal variations in phytoplankton composition in the northeastern Sea of Marmara: potentially toxic species and mucilage event. Mediterranean Marine Science, 21(3), 668-683. google scholar
  • Thomsen, P F., & Willerslev, E. (2015). Environmental DNA-An emerging tool in conservation for monitoring past and present biodiversity. Biological conservation, 183, 4-18. google scholar
  • Thomsen, P. F., M0ller, P. R., Sigsgaard, E. E., Knudsen, S. W., J0rgensen, O. A., & Willerslev, E. (2016). Environmental DNA from seawater samples correlate with trawl catches of subarctic, deepwater fishes. PloS one, 11(11), e0165252. pone.0165252 google scholar
  • Toklu-Alicli, B., Balkis-Ozdelice, N., Durmus, T., & Balci, M. (2021). Relationship between environmental factors and zooplankton diversity in the Gulf of Bandırma (the Sea of Marmara). Biologia, 76(6), 1727-1736. google scholar
  • Toklu-Alicli, B., Polat, S., & Balkis-Ozdelice, N. (2020). Temporal variations in the abundance of picoplanktonic Synechococcus (Cyanobacteria) during a mucilage event in the Gulfs of Bandırma and Erdek. Estuarine, Coastal and Shelf Science, 233, 106513. ecss.2019.106513 google scholar
  • Tüfekçi, V., Balkis, N., Beken, C. P., Ediger, D., & Mantikci, M. (2010). Phytoplankton composition and environmental conditions of the mucilage event in the Sea of Marmara. Turkish Journal of Biology, 34(2), 199-210. google scholar
  • Turk, V, Hagström, Â., Kovac, N., & Faganeli, J. (2010). Composition and function of mucilage macroaggregates in the northern Adriatic. Aquatic microbial ecology, 61(3), 279-289. https://doi. org/10.3354/ame01447 google scholar
  • Türkiye İstatistik Kurumu. (2023). Retrieved from google scholar
  • Turley, C. M. (1991). Protozoa Associated with Marine ‘Snow’and ‘Fluff’— Session Summary. In Protozoa and their role in marine processes (pp. 309-326). Berlin, Heidelberg: Springer Berlin Heidelberg. https://doi. org/10.1007/978-3-642-73181-5_19 google scholar
  • Turner, J. T. (2004). The importance of small planktonic copepods and their roles in pelagic marine food webs. Zool. Stud, 43(2), 255-266. google scholar
  • Tuzcu Kokal, A., Olgun, N., & Musaoğlu, N. (2022). Detection of mucilage phenomenon in the Sea of Marmara by using multi-scale satellite data. Environmental Monitoring and Assessment, 194(8), 585. https:// google scholar
  • Ünlülata, Ü., Oğuz, T., Latif, M. A., & Özsoy, E. (1990). On the physical oceanography of the Turkish Straits. The physical oceanography of sea straits, 25-60. google scholar
  • Usov, A. I. (2011). Polysaccharides of the red algae. In Advances in carbohydrate chemistry and biochemistry (Vol. 65, pp. 115-217). Academic Press. google scholar
  • Weiland-Brâuer, N., Neulinger, S. C., Pinnow, N., Künzel, S., Baines, J. F., & Schmitz, R. A. (2015). Composition of bacterial communities associated with Aurelia aurita changes with compartment, life stage, and population. Applied and environmental microbiology, 81(17), 6038-6052. google scholar
  • Wong, H. K., Lüdmann, T., Ulug, A., & Görür, N. (1995). The Sea of Marmara: a plate boundary sea in an escape tectonic regime. Tectonophysics, 244(4), 231-250. google scholar
  • Wood, S. A., Smith, K. F., Banks, J. C., Tremblay, L. A., Rhodes, L., Mountfort, D., ... & Pochon, X. (2013). Molecular genetic tools for environmental monitoring of New Zealand’s aquatic habitats, past, present and the future. New Zealand Journal of Marine and Freshwater Research, 47(1), 90-119. 0.2012.745885 google scholar
  • Wotton, R. S. (2004). The utiquity and many roles of exopolymers (EPS) in aquatic systems. Scientia marina, 68(S1), 13-21. https://doi. org/10.3989/scimar.2004.68s113 google scholar
  • Yaşar, D. (2001). Anthropogenic pollution in Izmit Bay: heavy metal concentrations in surface sediments. Turkish Journal of Engineering and Environmental Sciences, 25(4), 299-313. google scholar
  • Yilmaz, I. N. (2015). Collapse of zooplankton stocks during Liriope tetraphylla (Hydromedusa) blooms and dense mucilaginous aggregations in a thermohaline stratified basin. Marine Ecology, 36(3), 595-610. google scholar
  • Zaiko, A., Samuiloviene, A., Ardura, A., & Garcia-Vazquez, E. (2015). Metabarcoding approach for nonindigenous species surveillance in marine coastal waters. Marine Pollution Bulletin, 100(1), 53-59. google scholar
  • Zingone, A., Escalera, L., Aligizaki, K., Fernândez-Tejedor, M., Ismael, A., Montresor, M., ... & Totti, C. (2021). Toxic marine microalgae and noxious blooms in the Mediterranean Sea: A contribution to the Global HAB Status Report. Harmful Algae, 102, 101843. https://doi. org/10.1016/j.hal.2020.101843 google scholar


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Doğan, O., Örün, A.D., Bilgin, R., & İşinibilir Okyar, M. (2024). Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data. Aquatic Sciences and Engineering, 39(2), 106-120.


Doğan O, Örün A D, Bilgin R, İşinibilir Okyar M. Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data. Aquatic Sciences and Engineering. 2024;39(2):106-120.


Doğan, O.; Örün, A.D.; Bilgin, R.; İşinibilir Okyar, M. Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data. Aquatic Sciences and Engineering, [Publisher Location], v. 39, n. 2, p. 106-120, 2024.

Chicago: Author-Date Style

Doğan, Onur, and Anıl Doğan Örün and Raşit Bilgin and Melek İşinibilir Okyar. 2024. “Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data.” Aquatic Sciences and Engineering 39, no. 2: 106-120.

Chicago: Humanities Style

Doğan, Onur, and Anıl Doğan Örün and Raşit Bilgin and Melek İşinibilir Okyar. Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data.” Aquatic Sciences and Engineering 39, no. 2 (Apr. 2024): 106-120.

Harvard: Australian Style

Doğan, O & Örün, AD & Bilgin, R & İşinibilir Okyar, M 2024, 'Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data', Aquatic Sciences and Engineering, vol. 39, no. 2, pp. 106-120, viewed 23 Apr. 2024,

Harvard: Author-Date Style

Doğan, O. and Örün, A.D. and Bilgin, R. and İşinibilir Okyar, M. (2024) ‘Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data’, Aquatic Sciences and Engineering, 39(2), pp. 106-120. (23 Apr. 2024).


Doğan, Onur, and Anıl Doğan Örün and Raşit Bilgin and Melek İşinibilir Okyar. Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data.” Aquatic Sciences and Engineering, vol. 39, no. 2, 2024, pp. 106-120. [Database Container],


Doğan O, Örün AD, Bilgin R, İşinibilir Okyar M. Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data. Aquatic Sciences and Engineering [Internet]. 23 Apr. 2024 [cited 23 Apr. 2024];39(2):106-120. Available from: doi: 10.26650/ASE20241434217


Doğan, Onur - Örün, AnılDoğan - Bilgin, Raşit - İşinibilir Okyar, Melek. Revealing Mucilage Event-Linked Community Composition in the Sea of Marmara from eDNA Metabarcoding Data”. Aquatic Sciences and Engineering 39/2 (Apr. 2024): 106-120.


Published Online29.03.2024


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