The early stage of mucilage formation in the Marmara Sea during spring 2021
Halim Aytekin Ergul, Neslihan Balkis-Ozdelice, Merve Koral, Serdar Aksan, Turgay Durmus, Mert Kaya, Melih Kayal, Fatih Ekmekci, Oltan Canli
ORCID IDs: H.A.E. 0000-0002-9313-1426; N.B.O. 0000-0001-8030-7480; M.K. 0000-0003-3869-4522; S.A. 0000-0002-8842-9332; T.D. 0000-0002-8242-1823; M.K. 0000-0001-8429-842X; M.K. 0000-0003-0656-7684; F.E. 0000-0003-2305-9163; O.C. 0000-0002-2652-844X
Department of Biology, Science and Arts Faculty, KocaeliUniversity, 41001, İzmit, Kocaeli, TURKEY
Department of Biology, Division of Hydrobiology, Faculty of Science, İstanbul University, 34134 İstanbul, TURKEY
Investigating, Planning and Allocations Department, General Directorate of State Hydraulic Works, 06100 Ankara, TURKEY
TUBITAK Marmara Research Centre, Environment and Cleaner Production Institute, 41470 Kocaeli, TURKEY
In the present study, phytoplankton composition in relation to mucilage and accompanied physicochemical conditions were investigated in the sea water samples collected from four stations in İzmit-Kocaeli, Fatih-İstanbul, Biga-Çanakkale (in the Marmara Sea), and Riva-İstanbul (in the Black Sea). Samplings were carried out before (i.e., during September 2020) and at the beginning stage of the mucilage formations (i.e., during April 2021) which was observed in the Marmara Sea during spring and summer months of 2021. Seawater temperature, salinity, pH, and dissolved oxygen levels were measured in situ. Inorganic nitrogen, orthophosphate, and chlorophyll-a concentrations were analyzed spectrophotometrically. In total 83 phytoplankton species (44 Bacillariophyceae-BAC, 36 Dinophyceae-DIN, 2 Dictyochophyceae-DIC, and 1 Chlorophyceae-CHL) were identified during the study. BAC species were generally dominant. Among the 83 phytoplankton taxa identified, Cerataulina pelagica, Cylindrotheca closterium, Pseudo-nitzschia sp., Skeletonema costatum, Thalassiosira rotula, Alexandrium tamarense, Dinophysis acuminata, Dinophysis caudata, Dinophysis fortii, Gonyaulax fragilis, Gonyaulax spinifera, Gymnodinium sp., Gyrodinium sp., and Prorocentrum micans are known as the species associated with mucilage formation. The highest number of species was determined at the Biga-Çanakkale station (MDG25) with 38 taxa in September 2020. Skeletonema costatum (11200 cells/L) was the most abundant species at 10 m depth in the İzmit-Kocaeli station (MDG22) in April 2021. The mucilage formations in MDG22, and MDG25 stations were observed at their beginning stage as a tule curtain form in April 2021 while the seawater temperature and salinity levels were below 15°C and around 30‰, respectively. While the taxa dominance of the BAC in the total phytoplankton remained similar from September to April (i.e., 56%), its number of species decreased dramatically from 59 to 28 in the Marmara Sea. Despite the decreasing biodiversity, there was an increase in total abundance in the sampling stations, particularly in MDG22 and MDG25. In both stations, total abundance increased from 12000 to 42000, and 2000 to 50000 cells/L, respectively, compared to September 2020 and April 2021. Despite the decrease in biodiversity, and increase in the number of cells suggests that eutrophication and, as a result, mucilage formation occurred in the Marmara Sea. TRIX values showed that while the eutrophic conditions increased, the ecological quality in the region generally decreased from September 2020 to April 2021, and it was described as Bad for all stations in the Marmara Sea. The data indicated that the limiting factor for phytoplankton was nitrogen during April 2021 simultaneously with the mucilage formation in the Marmara Sea.
Keywords: Mucilage, sea snot, phytoplankton, Marmara Sea, nutrient, Cylindrotheca closterium, Skeletonema costatum
Aktan, Y., Dede, A., Ciftci, P.S. (2008) Mucilage event associated with diatoms and dinoflagellates in Sea of Marmara, Turkey. Harmful Algae News 36: 1-3.
Balkis, N., Atabay, H., Turetgen, I., Albayrak, S., Balkis, H., Tüfekçi, V. (2011) Role of single-celled organisms in mucilage formation on the shores of Buyukada Island (the Sea of Marmara). J Mar Biol Assoc UK 91: 771-781.
Balkis, N., Sivri, N., Fraim, N.L., Balci, M., Durmus, T., Sukatar, A. (2013) Excessive growth of Cladophora laetevirens (Dillwyn) Kutzing and enteric bacteria in mats in the Southwestern Istanbul coast, Sea of Marmara. IUFS J Biol 72(2): 43-50.
Balkis-Ozdelice, N., Durmus, T., Balci, M. (2021) A preliminary study on the ıntense pelagic and benthic mucilage phenomenon observed in the Sea of Marmara. Int Journal of Environment and Geoinformatics 8(4): 414-422.
Bendschneider, K., Robinson, R.J. (1952) A new spectrophotometric method for the determination of nitrite in sea water. J Mar Res 11: 87-96.
Besiktepe, S., Sur, H., Özsoy, E., Latif, M., Oguz, T., Ünlüata, Ü. (1994) The circulation and hydrography of the Marmara Sea. Prog Oceanogr 34: 285-334.
Bianchi, G. (1746) Jani Planci Ariminensis De Mola pisce ad Josephum Montium bononiensem. De Bononiensi Scientiarum Et Artium Instituto Atque Academia Commentarii 2: 297-303.
Chin, W., Orellana, M.V., Verdugo, P. (1998) Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391: 568-572.
Daniel, G.F., Chamberlain, A.H.L., Jones, E.B.G. (1980) Ultrastructural observations on the marine fouling diatom Amphora. Helgoländer Meeresunters 34: 123-149.
Ehrhardt, G.M., Burns, K.A. (1993) Hydrocarbons and related photo-oxidation products in Saudi Arabian Gulf coastal waters and hydrocarbons in underlying sediments and bioindicator bivalves. Mar Poll Bull 27: 187-197.
Ergul, H.A. (2016) Evaluation of seasonal physicochemical conditions and chlorophyll-a concentrations in İzmit Bay, Marmara Sea. Journal of the Black Sea/Medit Environ 22: 201-217.
Ergul, H.A., Aksan, S., İpşiroğlu, M. (2018) Assessment of the consecutive harmful dinoflagellate blooms during 2015 in the İzmit Bay (the Marmara Sea). Acta Oceanol Sin 37: 91-101.
Ergul, H.A., Aksan, S., İpşiroğlu-Koral, M., Baysal, A. (2014) Assessment of consecutive plankton blooms on March and April 2014 in İzmit Bay (The Marmara Sea). Hydromedit 1: 127-131.
Ergul, H.A., Çelebi, N.G., İpşiroğlu-Koral, M. (2013) A study on plankton proliferation in İzmit Bay (March 2013). In: 17. Ulusal Su Ürünleri Sempoyumu, İstanbul 1: 74 (in Turkish).
Ergul, H.A., Küçük, A., Terzi, M. (2010) A research on an algae bloom in İzmit Bay. In: Proceedings of the Symposium “the Marmara Sea 2010” (ed., Öztürk, B.), Turkish Marine Research Foundation, Publication no: 32, İstanbul, Turkey, pp. 464-468 (in Turkish).
Giuliani, S., Lamberti, C.V., Sonni, C., Pellegrini, D. (2005) Mucilage impact on gorgonians in the Tyrrhenian Sea. Sci Total Env 353: 340-349.
Küçük, A., Ergul, H.A. (2011) Seasonal variations of microplankton composition in İzmit Bay (Sea of Marmara). J Black Sea/Medit Environ 17: 216-222.
Lorenti, M., Buia, M.C., Martino, V., Modigh, M. (2005) Occurrence of mucous aggregates and their impact on Posidonia oceanica beds. Sci Total Env 353: 369-379.
Mullin, J.B., Riley, J.P. (1955) The colorimetric determination of silicate with special reference to sea and natural waters. Anal Chim Acta 12: 162-176.
Murphy, J., Riley, J.P. (1962) A modified single solution method for the determination of phosphate in natural-waters. Anal Chim Acta 27: 31-36.
Özalp, H.B. (2021) First massive mucilage event observed in deep waters of Çanakkale Strait (Dardanelles), Turkey. J Black Sea/Medit Environ 27(1): 49-66.
Piazzi, L., Atzori, F., Cadoni, N., Cinti, M.F., Frau, F., Ceccherelli, G. (2018) Benthic mucilage blooms threaten coralligenous reefs. Mar Environ Res 140: 145-151.
Pistocchi, R., Cangini, M., Totti, C., Urbani, R., Guerrini, F., Romagnoli, T., Sist, P., Palamidesi, S., Boni, L., Pompei, M. (2005) Relevance of the dinoflagellate Gonyaulax fragilis in mucilage formations of the Adriatic Sea. Sci Total Env 353(1-3): 307-316.
Ricci, F., Penna, N., Capellaci, S., Penna, A. (2014) Potential environmental factors influencing mucilage formation in the northern Adriatic Sea. Chem Ecol 30(4): 364-375.
Rinaldi, A., Vollenweider, R.A., Montanaria, G., Ferraria, C.R., Ghetti, A. (1995) Mucilages in Italian seas: the Adriatic and Tyrrhenian Seas, 1988-1991. Sci Total Env 165: 165-183.
Schiaparelli, S., Castellano, M., Povero, P., Sartoni, G., Vietti, R.C. (2007) A benthic mucilage event in North-Western Mediterranean Sea and its possible relationships with the summer 2003 European heatwave: short term effects on littoral rocky assemblages. Mar Ecol 28(3): 341-353.
Svetličić, V., Žutić, V., Radić, T.M., Pletikapić, G., Zimmermann, A.H., Urbani, R. (2011) Polymer networks produced by marine diatoms in the Northern Adriatic Sea. Marine Drugs 9: 666-679.
Taş, S., Ergul, H.A., Balkis, N. (2016) Harmful algal blooms (HABs) and mucilage formations in the Sea of Marmara. In: The Sea of Marmara Marine Biodiversity, Fisheries, Conservation and Governance, (eds., Özsoy, E., Çağatay, M.N., Balkis, N., Balkıs, N., Öztürk, B.), Turkish Marine Research Foundation, Publication No: 42, Turkey, pp. 768-786.
Tas, S., Kus, D., Yilmaz, I.N. (2020) Temporal variations in phytoplankton composition in the north-eastern Sea of Marmara: potentially toxic species and mucilage event. Mediterranean Marine Science 21: 668-683.
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. Estuar Coast Shelf Sci 233: 1-12.
Tüfekçi, V., Balkis, N., Beken, C.P., Ediger, D., Mantıkçı, M. (2010) Phytoplankton composition and environmental conditions of a mucilage event in the Sea of Marmara. Turk J Biol 34: 199-210.
TUIK (2018) Municipality Wastewater Statistics, 2018. Available at: https://biruni.tuik.gov.tr/medas/?kn=120&locale=tr (accessed 14 Aug 2021)
Turk, V., Hagström, A., Kova, N., Faganeli, J. (2010) Composition and function of mucilage macroaggregates in the northern Adriatic. Aquat Microb Ecol 61(3): 279-289.
Umani, S.F., Ghirardelli, E., Specchi, M. (1989) Gli episodi di” mare sporco” nell’Adriatico dal 1729 ai giorni nostri. Regione Autonoma Friuli Venezia Giulia. Direzione Regionale dell’Ambiente, 178 pp.
Urbani, R., Magaletti, E., Sist, P., Cicero, A.M. (2005) Extracellular carbohydrates released by the marine diatoms Cylindrotheca closterium, Thalassiosira pseudonana and Skeletonema costatum: Effect of P-depletion and growth status. Sci Total Env 353: 300-306
Vollenweider, R.A., Giovanardi, F., Montanari, G., Rinaldi, A. (1998) Characterization of the trophic conditions of marine coastal waters, with special reference to the NW Adriatic Sea: proposal for a trophic scale, turbidity and generalized water quality index. Environmetrics 9(3): 329-357.
Zingone, A., Escalera, L., Aligizaki, K., Tejedor, M.F., Ismael, A., Montresor, M., Mozetic, P., Taş, S., Totti, C. (2021) Toxic marine microalgae and noxious blooms in the Mediterranean Sea: A contribution to the Global HAB Status Report. Harmful Algae 102(1): 101843.