Vertical and temporal distribution of phytoplankton marker pigments during massive mucilage event

Yaprak Gürkan, Ahsen Yüksek

ORCID IDs: Y.G. 0000-0001-7949-3001; A.Y. 0000-0001-7949-3001

Institute of Marine Sciences and Management, İstanbul University, 34134 Vefa/İstanbul, TÜRKİYE

Abstract

This study examines the temporal and vertical distribution of phytoplankton marker pigments in coastal marine ecosystem for one year. Chl-a had high masses in the upper layer, except in June 2021. Chl c₁+c₂ peaked at 0.75 µg L^-1 in April 2021 above 20 m. Frequent pigment, fucoxanthin, reached its highest mass of 0.66 µg L^-1 in April 2021 within upper 20 m. Peridinin’s peak values were 0.28 µg L^-1 in January 2021. Temperature had a negative correlation with pigments, particularly with fucoxanthin (r= -0.5). Fucoxanthin exhibited strong positive correlations with chl-a and chl-c₁+c₂ (r = ~0.75), and peridinin correlated with ß-carotene (r=0.67). Median pigment values within the first 10 m were slightly lower than the first 20 m. Pigment mass within 20-38 m was notably lower than 10-38 m. An increasing chl-a pattern from November 2020 to March 2021, with fluctuations thereafter was detected. Permutational multivariate variance analysis showed significant differences (p<0.05) in marker pigment masses between sampling months. This study illuminates the intricate temporal and vertical dynamics of phytoplankton marker pigments, providing insights into the phytoplankton activity in the central İzmit Bay during a mucilage ongoing period.

Keywords: The Sea of Marmara, phytoplankton marker pigments, chlorophylls, fucoxanthin, İzmit Bay

References

Ağirbas, E., Feyzioglu, A.M., Kopuz, U., Llewellyn, C.A. (2015) Phytoplankton community composition in the south-eastern Black Sea determined with pigments measured by HPLC-CHEMTAX analyses and microscopy cell counts. Journal of the Marine Biological Association of the United Kingdom 95(1): 35-52.

Aktan, Y., Dede, A., Çiftci, P.S. (2008) Mucilage event associated with diatoms and dinoflagellates in Sea of Marmara. Harmful Algae News 36: 1-3.

Aktan, Y., Tüfekçi, V., Tüfekçi, H., Aykulu, G. (2005) Distribution patterns, biomass estimates and diversity of phytoplankton in İzmit Bay (Turkey). Estuarine, Coastal and Shelf Science 64(2-3): 372-384.

Altiok, H., Can, L., Mutlu, S. (2020) Daily variations in stratification in İzmit Bay. Turkish Journal of Earth Sciences 29(5): 815-829.

Balci, M., Balkis, N. (2017) Assessment of phytoplankton and environmental variables for water quality and trophic state classification in the Gemlik Gulf, Marmara Sea (Turkey). Marine Pollution Bulletin 115(1–2): 172-189.

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: 771-781.

Balkıs, N., Toklu-Alıçlı, B. (2014) Changes in phytoplankton community structure in the Gulf of Bandirma, Marmara Sea in 2006-2008. Fresenius Environmental Bulletin 23(12): 2976 – 2983

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.

Bayram, F. (2022) Investigation of Phytoplankton Composition of İzmit Bay and the Northeastern Marmara Sea with Water Quality Variables. Ph.D. Thesis, Istanbul University Institute of Marine Sciences and Management (in Turkish).

Beşiktepe, Ş.T., Sur, H.I., Özsoy, E., Latif, M.A., Oǧuz, T., Ünlüata, Ü. (1994) The circulation and hydrography of the Marmara Sea. Progress in Oceanography 34(4): 285-334.

Bianchi, T.S., Rolff, C., Widbom, B., Elmgren, R. (2002) Phytoplankton pigments in Baltic Sea seston and sediments: seasonal variability, fluxes, and transformations. Estuarine, Coastal and Shelf Science 55(3): 369-383.

Dursun, F., Tas, S., Bayram Partal, F., Ediger, D. (2020) Determination of phytoplankton composition by microscopy and HPLC-derived pigment analysis in the Sea of Marmara. Mediterranean Marine Science 21(3): 653-663.

Dursun, F., Tas, S., Ediger, D. (2021) Assessment of phytoplankton group composition in the Golden Horn Estuary (Sea of Marmara, Turkey) determined with pigments measured by HPLC-CHEMTAX analyses and microscopy. Journal of the Marine Biological Association of the United Kingdom 101(4): 649-665.

Ediger, D., Beken, Ç., Yüksek, A., Tuğrul, S. (2016) Eutrophication in the Sea of Marmara. In: The Sea of Marmara Marine Biodiversity, Fisheries, Conservation and Governance, (eds., Özsoy, E., Çağatay, M.N., Balkıs, N., Balkıs, N., Öztürk, B.). Turkish Marine Research Foundation, Publication No: 42, İstanbul, Turkey, pp. 723-736.

Ediger, D., Raine, R., Weeks, A.R., Robinson, I.S., Sagan, S. (2001) Pigment signatures reveal temporal and regional differences in taxonomic phytoplankton composition off the west coast of Ireland. Journal of Plankton Research 23(8): 893-902.

Ediger, D., Soydemir, N., Kideys, A.E. (2006) Estimation of phytoplankton biomass using HPLC pigment analysis in the southwestern Black Sea. Deep Sea Research Part II: Topical Studies in Oceanography 53(17-19): 1911-1922.

Ergül, H.A., Aksan, S., İpşiroğlu, M. (2018) Assessment of the consecutive harmful dinoflagellate blooms during 2015 in the Izmit Bay (the Marmara Sea). Acta Oceanologica Sinica 37(8): 91-101.

Flander-Putrle, V., Malej, A. (2008) The evolution and phytoplankton composition of mucilaginous aggregates in the northern Adriatic Sea. Harmful Algae 7(6): 752-761.

Flander-Putrle, V., Terszic, S., Malej, A., Ahel, M. (2000) Effects of mucilage event on the distribution of summer phytoplankton as reflected by phytoplankton pigments. Periodicum Biologorium 102(2): 169-177.

Flombaum, P., Gallegos, J.L., Gordillo, R.A., Rincón, J., Zabala, L.L., Jiao, N., Karl, D.M., Li, W.K.W., Lomas, M.W., Veneziano, D., Vera, C.S., Vrugt, J.A., Martiny, A.C. (2013) Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proceedings of the National Academy of Sciences of the United States of America 110(24): 9824-9829.

Giani, M., Rinaldi, A., Degobbis, D. (2005) Mucilages in the Adriatic and Tyrrhenian Sea: an introduction. The Science of the Total Environment 353(1-3): 3-9.

Jeffrey, S., Mantoura, R., Wright, S. (1997) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods. United Nations Educational, Scientific and Cultural Organization, Paris, France.

Joint, I., Henriksen, P., Fonnes, G.A., Bourne, D., Thingstad, T.F., Riemann, B. (2002) Competition for inorganic nutrients between phytoplankton and bacterioplankton in nutrient manipulated mesocosms. Aquatic Microbial Ecology 29(2): 145-159.

Juin, C., Bonnet, A., Nicolau, E., Bérard, J.B., Devillers, R., Thiéry, V., Cadoret, J.P., Picot, L. (2015) UPLC-MSE Profiling of phytoplankton metabolites: application to the identification of pigments and structural analysis of metabolites in Porphyridium purpureum. Marine Drugs 13(4): 2541-2558.

Kanamoto, A., Kato, Y., Yoshida, E., Hasunuma, T., Kondo, A. (2021) Development of a method for fucoxanthin production using the haptophyte marine microalga Pavlova sp. OPMS 30543. Marine Biotechnology 23(2): 331-341.

Konucu, M., Eker-Develi, E., Örek, H., Başduvar, Ş. (2019) Microalgal pigments and their relation with phytoplankton carbon biomass on the northeastern Mediterranean Sea shore, with special emphasis on nanophytoplankton. Preprint in BioRxiv 745588. doi: https://doi.org/10.1101/745588 (accessed 10 Aug 2023).

Konucu, M., Eker-Develi, E., Örek, H., Başduvar, Ş., Kideys, A.E. (2022) Marker pigments and carbon biomass of phytoplankton on the northeastern Mediterranean Sea coast. Journal of Experimental Marine Biology and Ecology 550: 151718.

Küçük, A., Ergül, H.A. (2011) Seasonal variations of microplankton compositionin İzmit Bay (Sea of Marmara). Journal of Black Sea/Mediterranean Environment 17(3): 216-222.

Lagaria, A., Mandalakis, M., Mara, P., Frangoulis, C., Karatsolis, B.T., Pitta, P., Triantaphyllou, M., Tsiola, A., Psarra, S. (2017) Phytoplankton variability and community structure in relation to hydrographic features in the NE Aegean frontal area (NE Mediterranean Sea). Continental Shelf Research 149: 124-137.

Mantoura, R.F.C., Llewellyn, C.A. (1983) The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high-performance liquid chromatography. Analytica Chimica Acta 151(C): 297-314.

Marty, J.C., Chiavérini, J., Pizay, M.D., Avril, B. (2002) Seasonal and interannual dynamics of nutrients and phytoplankton pigments in the western Mediterranean Sea at the DYFAMED time-series station (1991–1999). Deep Sea Research Part II: Topical Studies in Oceanography 49(11): 1965-1985.

Morkoç, E., Okay, O. S., Tolun, L., Tüfekçi, V., Tüfekçi, H., Legoviç, T. (2001) Towards a clean Izmit Bay. Environment International 26(3): 157-161.

Nadushan, M., Hosseinzade, I.R. (2020) Optimization of production and antioxidant activity of fucoxanthin from marine haptophyte algae, Isochrysis galbana. Iranian Journal of Fisheries Sciences 19(6): 2901-2908.

Öztürk, İ.D., Ediger, D. (2023) Effects of mucilage on the optical properties of water column in the Sea of Marmara. Journal of the Black Sea/Mediterranean Environment 29(1): 73–86.

Öztürk, İ.D., Mutlu, S., Kaman, G., Partal, F.B., Demirtaş, A., Caglar, S., Kuzyaka, E., Altiok, H., Ediger, D. (2021) Vertical distribution of mucilage typology in the water column after a massive mucilage formation in the surface waters of the Sea of Marmara. Journal of the Black Sea/Mediterranean Environment 27(2): 184-201.

Paerl, H.W., Valdes, L. M., Pinckney, J. L., Piehler M. F., Dyble, J., Moisander. P.H. (2003) Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. BioScience 53(10): 953-964.

Pan, X., Mannino, A., Russ, M.E., Hooker, S.B., Harding, L.W. (2010) Remote sensing of phytoplankton pigment distribution in the United States northeast coast. Remote Sensing of Environment 114(11): 2403-2416.

Pekey, H. (2006) The distribution and sources of heavy metals in Izmit Bay surface sediments affected by a polluted stream. Marine Pollution Bulletin 52(10): 1197-1208.

Riley, J.P., Wilson, T.R.S. (1967) The pigments of some marine phytoplankton species. Journal of the Marine Biological Association of the United Kingdom 47(2): 351-362.

Savun-Hekimoğlu, B., Gazioğlu, C. (2021) Mucilage Problem in the semi-enclosed seas recent outbreak in the Sea of Marmara. International Journal of Environment and Geoinformatics 8(4): 402-413.

Schlitzer, R. (2022) Ocean Data View. https://odv.awi.de, 2022.

Schlüter, L., Møhlenberg, F., Havskum, H., Larsen, S. (2000) The use of phytoplankton pigments for identifying and quantifying phytoplankton groups in coastal areas: testing the influence of light and nutrients on pigment/chlorophyll a ratios. Marine Ecology Progress Series 192: 49-63.

Seoane, S., Garmendia, M., Revilla, M., Borja, Á., Franco, J., Orive, E., Valencia, V. (2011) Phytoplankton pigments and epifluorescence microscopy as tools for ecological status assessment in coastal and estuarine waters, within the Water Framework Directive. Marine Pollution Bulletin 62(7): 1484-1497.

Serive, B., Nicolau, E., Bérard, J.B., Kaas, R., Pasquet, V., Picot, L., Cadoret, J.P. (2017) Community analysis of pigment patterns from 37 microalgae strains reveals new carotenoids and porphyrins characteristic of distinct strains and taxonomic groups. PLoS ONE 12(2): e0171872.

Tas, S. (2015) A prolonged red tide of Heterocapsa triquetra (Ehrenberg) F. Stein (Dinophyceae) and phytoplankton succession in a eutrophic estuary in Turkey. Mediterranean Marine Science 16(3): 621-627.

Tas, S., Yilmaz, I.N. (2015) Potentially harmful microalgae and algal blooms in a eutrophic estuary in Turkey. Mediterranean Marine Science 16(2): 432-443.

Tolun, L.G., Ergenekon, S., Hocaoglu, S.M., Donertas, A.S., Cokacar, T., Husrevoglu, S., Polat Beken, Ç., Baban, A. (2012) Socioeconomic response to water quality: a first experience in science and policy integration for the Izmit Bay coastal system. Ecology and Society 17(3): 40, doi: http://dx.doi.org/10.5751/ES-04984-170340.

Tüfekçi, V., Balkis, N., Polat Beken, Ç., Ediger, D., Mantikçi, M. (2010) Phytoplankton composition and environmental conditions of the mucilage event in the Sea of Marmara. Turkish Journal of Biology 34(2): 199-210.

Uysal, Z., Ünsal, M. (1996) Spatial distribution of net diatoms along adjacent water masses of different origin. Turkish Journal of Botany 20: 519-527.

Ünlülata, Ü., Oğuz, T., Latif, M.A., Özsoy, E. (1990) On the Physical Oceanography of the Turkish Straits. In: The Physical Oceanography of Sea Straits, (eds., Pratt, L.J.), NATO ASI Series, vol 318. Springer, Dordrecht, pp. 25-60.

Vidussi, F., Marty, J.C., Chiavérini, J. (2000) Phytoplankton pigment variations during the transition from spring bloom to oligotrophy in the northwestern Mediterranean Sea. Deep Sea Research Part I: Oceanographic Research Papers 47(3): 423-445.

Wong, K.C., Wong, K.C. (2004) Study of phytoplankton characteristics in Tolo Harbour, Hong Kong, by HPLC analysis of chemotaxonomic pigments. Journal of Applied Phycology 16(6): 469-476.

Wright, S.W., Jeffrey, S.W. (2006) Pigment Markers for Phytoplankton Production. In: Marine Organic Matter: Biomarkers, Isotopes and DNA, (eds., Volkman, J.K.), The Handbook of Environmental Chemistry, vol 2N. Springer, Berlin, Heidelberg, pp. 71-104.