Determination of phytoplankton composition by microscopy and HPLC-derived pigment analysis in the Sea of Marmara


Published: Oct 30, 2020
Keywords:
Phytoplankton chlorophyll-a marker pigment HPLC Sea of Marmara.
FUAT DURSUN
https://orcid.org/0000-0002-7729-5893
SEYFETTİN TAS
https://orcid.org/0000-0002-5661-1439
FATMA BAYRAM PARTAL
DİLEK EDİGER
Abstract

This study is an integrated overview of pigment and microscopic analysis of phytoplankton composition in the Sea of Marmara. The study was conducted from 27 sampling stations during spring (May 2017 and 2018) and summer (August 2016 and 2018). The phytoplankton community was represented mostly by diatoms and dinoflagellates, as the major groups, and also other phytoflagellate groups as shown by both techniques. Chlorophyll-a, chlorophyll-c1+c2, peridinin, 19’-butanoyloxyfucoxanthin, fucoxanthin, zeaxanthin, alloxanthin, 19’-hexanoyloxyfucoxanthin, diadinoxanthin, chlorophyll-b and ß-carotene concentratios were determined by High Performance Liquid Chromatography (HPLC). A total of 124 eukaryotic taxa belonging to eight algal classes were found through microscopic analysis. 60 taxa of them were dinoflagellates, 52 taxa were diatoms and 12 taxa were other phytoflagellates. The number of diatoms and dinoflagellates, as the major groups, accounted for 90.4% of the total phytoplankton species. Chlorophyll-a, fucoxanthin and peridinin concentrations varied between 0.03-7.20, 0.01-5.23 and 0.01-2.14 μg L-1, throughout the research period, respectively. The highest chlorophyll-a values were measured at stations MD26 (7.20 µg L-1) and MD22 (6.61 µg L-1) in May 2018, which were located at Gemlik and Bandirma bays. There was a significant correlation (r:0.87, p<0.001 n:54) between HPLC determined fucoxanthin concentrations and diatom abundances in August 2016 and 2018. Also, higher chlorophyll-c1+c2 concentrations revealed consistency with high diatom abundances and fucoxanthin concentrations in August 2016 and 2018. This result confirmed that diatoms are the most important carrier of fucoxanthin and it can be used for taxonomic evaluation of diatom community of the Sea of Marmara.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
References
Agirbas, 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.
Agirbas E., Koca, L., Aytan, U., 2017. Spatio-temporal pattern of phytoplankton and pigment composition in surface waters of south-eastern Black Sea. Oceanologia, 59, 283-299.
Aiken, J., Pradhan, Y., Barlow, R., Lavender, S., Poulton, A. et al., 2009. Phytoplankton pigments and functional types in the Atlantic Ocean: a decadal assessment, 1995-2005. Deep Sea Research Part II: Topical Studies in Oceanography, 56 (15), 899-917.
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, 372-384.
Ansotegui, A., Sarobe, A., Trigueros, J.M., Urrutxurtu, I., Orive, E., 2003. Size distribution of algal pigments and phytoplankton assemblages in a coastal-estuarine environment: contribution of small eukaryotic algae. Journal of Plankton Research, 25 (4), 341-355.
Balkis, N., 2003. Seasonal variations in the phytoplankton and nutrient dynamics in the neritic water of Büyükçekmece Bay, Sea of Marmara. Journal of Plankton Research, 25 (7), 703-717.
Balkis, N., 2004. List of phytoplankton of the Sea of Marmara. Journal of the Black Sea / Mediterranean Environment, 10, 123-141.
Balkis, N., Toklu Alicli, B., 2014. Changes in phytoplankton community structure in the Gulf of Bandırma, Marmara Sea in 2006-2008. Fresenius Environmental Bulletin, 12, 2976- 2983.
Barlow, R.G., Mantoura, R.F.C., Gough, M.A., Fheman, T.W., 1993. Pigment signatures of the phytoplankton composition in the north-eastern Atlantic during the 1990 spring bloom. Deep-Sea Research II, 40, 459-477.
Besiktepe, S., Sur, H.I., Ozsoy, E., Abdullatif, M.A., Oguz, T. et al., 1994. The circulation and hydrography of the Marmara Sea. Progress in Oceanography, 34, 285-334.
Chai, C., Jiang, T., Cen, J., Ge, W., Lu, S., 2016. Phytoplankton pigments and functional community structure in relation to environmental factors in the Pearl River Estuary. Oceanologia, 58 (3), 201-211.
Dandonneau, Y., Niang, A., 2007. Assemblages of phytoplankton pigments along a shipping line through the North Atlantic and tropical Pacific. Progress in Oceanography, 73 (2), 127-144.
Deniz, N., Tas, S., 2009. Seasonal variations in the phytoplankton community in the North-eastern Sea of Marmara and a species list. Journal of the Marine Biological Association of the United Kingdom, 89, 269-276.
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.
Ediger, D., Hüsrevoğlu, S., Tüfekçi, V., Tolun, L., Atabay, H. et al., 2013. Monitoring of Water Quality and Territorial Inputs in the İzmit Bay. TÜBİTAK MRC, Technical report No 13, 158 pp.
Eker-Develi, E., Berthon, J.F., Canuti, E., Slabakova, N., Moncheva, S. et al., 2012. Phytoplankton taxonomy based on CHEMTAX and microscopy in the northwestern Black Sea. Journal of Marine Systems, 94, 18-32.
Eker-Develi, E., Konucu, M., 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. BioRxiv. 745588.
Ergul, H.A., Aksan, S., Ipsiroglu, M., Kucuk, A., 2015. Assessment of the spring 2015 phytoplankton blooms in Izmit Bay (the Marmara Sea). In: 3rd Science for the Environment Conference, Aarhus, 1-2 October 2015. Denmark.
Krivokapić, S., Bosak, S., Viličić, D., Kušpilić, G., Drakulović, D. et al., 2018. Algal pigments distribution and phytoplankton group assemblages in the coastal transitional environment– Boka Kotorska Bay (Southeastern Adriatic Sea). Acta Adriatica: International Journal of Marine Sciences, 59 (1), 35-49.
Loret, P., Pastoureaud, A., Bacher, C., Delesalle, B., 2000. Phytoplankton composition and selective feeding of the pearl oyster Pinctada margaritifera in the Takapoto lago on (Tuamotu Archipelago, French Polynesia): in situ study using optical microscopy and HPLC pigment analysis. Marine Ecology Progress Series, 199, 55-67.
Mackey, M.D., Mackey, D.J., Higgins, H.W., Wright, S.W., 1996. CHEMTAX-a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Marine Ecology Progress Series, 144, 265-283.
Madhu, N.V., Ullas, N., Ashwini, R., Meenu, P., Rehitha, T.V. et al., 2014. Characterization of phytoplankton pigments and functional community structure in the Gulf of Mannar and the Palk Bay using HPLC–CHEMTAX analysis. Continental Shelf Research, 80, 79-90.
Mantoura, R. F.C., Llewellyn, C.A., 1983. The rapid determination of algal chlorophyll-a and carotenoid pigments and their breakdown products in natural waters by reverse-phase high performance liquid chromatography. Analytica Chimica Acta, 151, 297-314.
Mendes, C.R., Sá, C., Vitorino, J., Borges, C., Garcia, V.M.T. et al., 2011. Spatial distribution of phytoplankton assemblages in the Nazaré submarine canyon region (Portugal): HPLC CHEMTAX approach. Journal of Marine Systems, 87 (1), 90-101.
Mendes, C.R.B., Kerr, R., Tavano, V.M., Cavalheiro, F.A., Garcia, C.A.E. et al., 2015. Cross-front phytoplankton pigments and chemotaxonomic groups in the Indian sector of the Southern Ocean. Deep Sea Research Part II: Topical Studies in Oceanography, 118, 221-232.
Millie, D.F., Paerl, H.W., Hurley, J.P., 1993. Microalgal pigment assessments using high performance liquid chromatography: a synopsis of organismal and ecological applications. Canadian Journal of Fisheries and Aquatic Sciences, 50, 2513-2527.
Miranda-Alvarez, C., González-Silvera, A., Santamaría-del-Angel, E., López-Calderón, J., Godínez, V.M. et al., 2020. Phytoplankton pigments and community structure in the northeastern tropical pacific using HPLC-CHEMTAX analysis. Journal of Oceanography, 76 (2), 91-108.
Okuş, E., Taş, S., 2007. Diatom increase in phytoplankton community observed in winter in the north-eastern Marmara Sea (Beylikdüzü). Journal of the Black Sea/Mediterranean Environment, 13 (1).
Oseji, O.F., Fan, C., Chigbu, P., 2019. Composition and dynamics of phytoplankton in the coastal bays of Maryland, USA, revealed by microscopic counts and diagnostic pigments analyses. Water, 11 (2), 368.
Özsoy, E., Oğuz, T., Latif, M.A., Ünlüata, Ü., Sur, H.I. et al., 1988. Oceanography of Turkish straits. The Middle East Technical University, Institute of Marine Sciences (METU- IMS), Technical report, Second annual report.
Özsoy, E., Çağatay, M.N., Balkıs, N., Balkıs, N., Öztürk, B. (Ed.), 2016. The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine Research Foundation (TUDAV), Istanbul.
Paerl, H.W., Valdes, L.M., Pinckney, J.L., Piehler, M.F., Dyble, J. et al., 2003. Phytoplankton photopigments as indicators of estuarine and coastal eutrophication. BioScience, 53 (10), 953-964.
Paerl, H.W., Valdes-Weaver, L.M., Joyner, A.R., Winkelmann, V., 2007. Phytoplankton indicators of ecological change in the eutrophying Pamlico Sound system, North Carolina. Ecological Applications, 17, 88-101.
Pérez, V., Fernández, E., Marañón, E., Morán, X.A.G., Zubkov, M.V., 2006. Vertical distribution of phytoplankton biomass, production and growth in the Atlantic subtropical gyres. Deep Sea Research Part I: Oceanographic Research Papers, 53 (10), 1616-1634.
Polat, Ç., Tuğrul, S., 1995. Nutrient and organic carbon exchanges between the Black and Marmara Seas through the Bosphorus Strait. Continental Shelf Research, 15 (9), 1115-1132.
Seoane, S., Laza, A., Urrutxurtu, I., Orive, E., 2005. Phytoplankton assemblages and their dominant pigments in the Nervion River estuary. Hydrobiologia, 549 (1), 1-13.
Seoane, S., Garmendia, M., Revilla, M., Borja, Á., Franco, J. et al., 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.
Schlüter, L., Mohlenberg, 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.
Sieburth, J.M., Smetacek, V., Lenz, J., 1978. Pelagic ecosystem structure: Heterotrophic compartments of the plankton and their relationship to plankton size fractions 1. Limnology and Oceanography, 23 (6), 1256-1263.
Silva, A., Mendes, C.R., Palma, S., Brotas, V., 2008. Short-time scale variation of phytoplankton succession in Lisbon bay (Portugal) as revealed by microscopy cell counts and HPLC pigment analysis. Estuarine, Coastal and Shelf Science, 79 (2), 230-238.
Sur, H.I., Okus, E., Sarikaya, H.Z., Altiok, H., Eroğlu, V. et al., 2002. Rehabilitation and water quality monitoring in the Golden Horn. Water Science and Technology, 46, 29-36.
Takishita, K., Kolke, K., Maruyama, T., Ogata, T., 2002. Molecular evidence for plastid robbery (kleptoplastidy) in Dinophysis, a dinoflagellate causing diarrhetic shellfish poisoning. Protist, 153 (3), 293-302.
Tas, S., Okus, E., 2004. Phytoplanktonarbeiten im Golf İzmit, Türkei. Mikrokosmos, 93 (1) 21-24. Throndsen, J., 1978. Preservation and storage. In: Phytoplankton manual. Sournia, A. (Eds). UNESCO.
Totti, C., Civitarese, G., Acri, F., Barletta, D., Candelari, G. et al., 2000. Seasonal variability of phytoplankton populations in the middle Adriatic sub-basin. Journal of Plankton Research, 22 (9), 1735-1756.
Tufekci, V., Balkis, N., Polat Beken, C., Ediger, D., Mantikci, M., 2010. Phytoplankton composition and environmental conditions of a mucilage event in the Sea of Marmara. Turkish Journal of Biology, 34, 199-210.
Tuğrul, S., Morkoç, E., 1990. Transport and water quality modeling in the Bay of İzmit. TÜBİTAK-MRC, Technical report.
Turkoglu, M., Unsal, M., Ismen, A., Mavili, S., Sever, T.M. et al., 2004. Dinamics of lower and high food chain of the Dardanelles and Saros Bay (North Aegean Sea). TUBITAK- YDABÇAG-101Y081, Final Report.
Turkoglu, M., 2010. Temporal variations of surface phytoplankton, nutrients and chlorophyll-a in the Dardanelles (Turkish Straits System): A coastal station sample in weekly time intervals. Turkish Journal of Biology, 34 (3), 319-333.
Turkoglu, M., Erdogan, Y., 2010. Diurnal variations of summer phytoplankton and interactions with some physicochemical characteristics under eutrophication of surface water in the Dardanelles (Çanakkale Strait, Turkey). Turkish Journal of Biology, 34 (2), 211-225.
Turkoglu, M., Oner, C., 2010. Short time variations of winter phytoplankton, nutrient and chlorophyll a of Kepez harbor in the Dardanelles (Çanakkale Strait, Turkey). Turkish Journal of Fisheries and Aquatic Sciences, 10 (4), 537-548.
Unsal, M., Turkoglu, M., Yenici, E., 2003. Biological and physicochemical researches in the Dardanelles. TUBITAK- YDABÇAG-100Y075, Final Report.
Utermöhl, H. 1958. Zur Vervollkommnung der quantitativen phytoplankton: Methodik Mitteilung Internationale Vereinigung Theoretische und Angewandte. Limnologie, 9, 1-38.
Viličić, D., Terzić, S., Ahel, M., Burić, Z., Jasprica, N. et al., 2008. Phytoplankton abundance and pigment biomarkers in the oligotrophic, eastern Adriatic estuary. Environmental Monitoring and Assessment, 142 (1-3), 199-218.
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, 329-357.
Wang, L., Ou, L., Huang, K., Chai, C., Wang, Z. et al., 2018. Determination of the spatial and temporal variability of phytoplankton community structure in Daya Bay via HPLC-CHEMTAX pigment analysis. Journal of Oceanology and Limnology, 36 (3), 750-760.
Yücel, N., Uysal, Z., Tuğrul, S., 2017. Variability in phytoplankton pigment composition in Mersin Bay. Aquatic Sciences and Engineering, 32 (1), 49-70.
Zapata, M., Jeffrey, S.W., Wright, S.W., Rodríguez, F., Garrido, J.L. et al., 2004. Photosynthetic pigments in 37 species (65 strains) of Haptophyta: implications for oceanography and chemotaxonomy. Marine Ecology Progress Series, 270, 83-102.
Most read articles by the same author(s)