Abstract
The present work describes microalgal blooms that occurred in a eutrophic estuary (Golden Horn, Sea of Marmara, Turkey) between October 2013 and September 2014 following a remediation effort. The relationships between bloom-forming microalgal species and environmental factors were investigated during the study period. The changing environmental conditions (e.g. increasing water transparency and salinity) after seawater transfer to the Golden Horn Estuary stimulated phytoplankton growth with dense algal blooms. Annual average values of Secchi depth, salinity and dissolved oxygen increased in comparison with those in an earlier study in 2009–2010. Nine microalgal species, which consisted of four diatoms, two dinoflagellates, one cryptophycean, one raphidophycean and one euglenophycean, formed the blooms with water discolorations during spring and summer. The species that reached the highest bloom density were Plagioselmis prolonga (62.4 × 106 cells l−1) among crytophyceans, Heterocapsa triquetra (21.8 × 106 cells l−1) among dinoflagellates and Skeletonema marinoi (39 × 106 cells l−1) among diatoms. The abundance of dinoflagellates and phytoflagellates increased particularly in the upper estuary when compared to diatoms and their rapid growth and bloom formation revealed that they have a wide range of tolerance to changing environmental conditions and a strong ability to compete with other species in this study area.
Funding source: Scientific and Technological Research Council of Turkey
Award Identifier / Grant number: TUBITAK-113Y091
Funding statement: The author wishes to thank Dr. Ahsen Yuksek for nutrient data, Dr. Fuat Dursun, scholarship student Turgay Durmus and technician Sezgin Camurcu for their efforts in field and laboratory during this project. This work was supported by the Scientific and Technological Research Council of Turkey (grant no.: TUBITAK-113Y091, Funder Id: http://dx.doi.org/10.13039/501100004410).
About the author
Seyfettin Tas works at the Institute of Marine Sciences and Management, University of Istanbul. His main research topic is taxonomy and ecology of marine phytoplankton. He is particularly interested in potentially harmful microalgae and harmful algal blooms (HABs). He conducted some research projects on potentially harmful species and algal blooms associated with environmental factors in coastal and estuarine waters. He is a member of International Society for the Study of Harmful Algae.
References
Anderson, D.M., A.D. Cembella and G.M. Hallegraeff. 2012. Progress in understanding harmful algal blooms: paradigm shifts and new technologies for research, monitoring, and management. Ann. Rev. Mar. Sci. 4: 143–176.10.1146/annurev-marine-120308-081121Search in Google Scholar
APHA, 1999. Standard methods for the examination of water and wastewater. 20th edition. Washington DC, USA.Search in Google Scholar
Barbosa, A.B., R.B. Domingues and H.M. Galvão. 2010. Environmental forcing of phytoplankton in a mediterranean estuary (Guadiana Estuary, South-western Iberia): a decadal study of anthropogenic and climatic ınfluences. Estuar. Coasts33: 324–341.10.1007/s12237-009-9200-xSearch in Google Scholar
Cetinić, I., D. Viličić, Z. Burić and G. Olujić. 2006. Phytoplankton seasonality in a highly stratifi ed karstic estuary (Krka, Adriatic Sea). Hydrobiol. 555: 31–40.10.1007/s10750-005-1103-7Search in Google Scholar
Clarke, K.R. and R.N. Gorley. 2006. PRIMER v6: User Manual/Tutorial (Plymouth Routines in Multivariate Ecological Research). PRIMER-E, Plymouth, UK.Search in Google Scholar
Cloern, J.E. 1987. Turbidity as a control on phytoplankton biomass and productivity in estuaries. Cont. Shelf Res.7: 1367–1381.10.1016/0278-4343(87)90042-2Search in Google Scholar
Davidson, K., R.J. Gowen, P.J. Harrison, L.E. Fleming, P. Hoagland and G. Moschonas. 2014. Anthropogenic nutrients and harmful algae in coastal waters. J. Environ. Manag. 146: 206–216.10.1016/j.jenvman.2014.07.002Search in Google Scholar PubMed
Dolbeth, M., P.G. Cardoso, S.M. Ferreira, T. Verdelhos, D. Raffaelli and M.A. Pardal. 2007. Anthropogenic and natural disturbance effects on a macrobenthic estuarine community over a 10-year period. Mar. Poll. Bull. 54: 576–585.10.1016/j.marpolbul.2006.12.005Search in Google Scholar PubMed
Domingues, R.B., T.P. Anselmo, A.B. Barbosa, U. Sommer and H.M. Galvão. 2010. Light as a driver of phytoplankton growth and production in the freshwater tidal zone of a turbid estuary. Estuar. Coast. Shelf Sci. 91: 526–535.10.1016/j.ecss.2010.12.008Search in Google Scholar
Domingues, R.B., T.P. Anselmo, A.B. Barbosa, U. Sommer and H.M. Galvão. 2011. Nutrient limitation of phytoplankton growth in the freshwater tidal zone of a turbid, Mediterranean estuary. Estuar. Coast. Shelf Sci. 91: 282–297.10.1016/j.ecss.2010.10.033Search in Google Scholar
Domingues, R.B., A.B. Barbosa, U. Sommer and H.M. Galvão. 2012. Phytoplankton composition, growth and production in the Guadiana estuary (SW Iberia): unraveling changes induced after dam construction. Sci. Total Environ. 416: 300–313.10.1016/j.scitotenv.2011.11.043Search in Google Scholar PubMed
Dortch, Q., R. Robichaux, S. Pool, D. Milsted, G. Mire, N.N. Rabalais, T.M. Soniat, G.A. Fryxell, R.E. Turner and M.L. Parsons. 1997. Abundance and vertical flux of Pseudo-nitzschia in the northern Gulf of Mexico. Mar. Ecol. Prog. Ser. 146: 249–264.10.3354/meps146249Search in Google Scholar
Dursun, F., S. Tas and T. Koray. 2016. Spring bloom of the raphidophycean Heterosigma akashiwo in the Golden Horn Estuary at the northeast of Sea of Marmara. Ege J. Fish. Aqua. Sci. 3: 201–207.10.12714/egejfas.2016.33.3.03Search in Google Scholar
Hallegraeff, G.M. 2002. Aquaculturists’ guide to harmful Australian Microalgae. 2nd edition. Printed by the Print Centre, Hobart, Tasmania, Australia. pp. 135.Search in Google Scholar
Hallegraeff, G.M. 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge. J. Phycol. 46: 220–235.10.1111/j.1529-8817.2010.00815.xSearch in Google Scholar
Hallegraeff, G.M., D.M. Anderson and A.D. Cembella. 2003. Manual on harmful marine microalgae. UNESCO, France. pp. 793.Search in Google Scholar
Hällfors, G. 2004. Checklist of Baltic Sea phytoplankton species. Baltic Sea Environment Proceeding No. 95, Helsinki Commission. pp. 208.Search in Google Scholar
Irvalı, N. and N. Çağatay. 2008. Late Pleistocene-Holocene history of the Golden Horn Estuary, Istanbul. Geo-Mar. Lett. 29: 151–160.10.1007/s00367-008-0129-zSearch in Google Scholar
Ishikawa, A. and A. Taniguchi. 1996. Contribution of benthos cysts to the population dynamics of Scrippsiella spp. (Dinophyceae) in Onagawa Bay, Northeast Japan. Mar. Ecol. Prog. Ser. 140: 169–178.10.3354/meps140169Search in Google Scholar
Jasprica, N., M. Carić, F. Kršinić, T. Kapetanović, M. Batistić and J. Njire. 2012. Planktonic diatoms and their environment in the lower Neretva River estuary (Eastern Adriatic Sea, NE Mediterranean). Nova Hed. Bei. 141: 405–430.Search in Google Scholar
Kim, H.G., J.S. Park and S.G. Lee. 1990. Coastal algal blooms caused by the cyst-forming dinoflagellates. Bull. Korean Fish. Soc. 23: 468–474.Search in Google Scholar
Koyuncu, A. 2018. The Seawater transfer from the Bosporus to the Golden Horn. In: Symposium book. Third marmara sea symposium. November 2017, Istanbul, Turkey. pp. 147–158. (In Turkish)Search in Google Scholar
Kudela, R.M., E. Berdalet, S. Bernard, M. Burford, L. Fernand, S. Lu, S. Roy, P. Tester, G. Usup, R. Magnien, D.M. Anderson, A. Cembella, M. Chinain, G. Hallegraeff, B. Reguera, A. Zingone, H. Enevoldsen and Ed Urban. 2015. Harmful algal blooms. A scientific summary for policy makers. IOC/UNESCO, Paris (IOC/INF-1320).Search in Google Scholar
Lam, C.W.Y. and K.C. Ho. 1989. Red tides in Tolo Harbor, Hong Kong. In: (T. Okaichi, D.M. Anderson and T. Nemoto, eds) Red tides, biology, environmental science and toxicology. Elsevier, New York. pp. 49–52.Search in Google Scholar
Legrand, C., E. Granéli and P. Carlsson. 1998. Induced phagotrophy in the photosynthetic dinoflagellate Heterocapsa triquetra. Aqua. Mic. Ecol. 15: 65–75.10.3354/ame015065Search in Google Scholar
Liefer, J.D., H.L. MacIntyre, L. Novoveská, W.L. Smith and C.P. Dorsey. 2009. Temporal and spatial variability in Pseudo-nitzschia spp. in Alabama coastal waters: a ‘‘hot spot’’ linked to submarine groundwater discharge? Harmful Algae 8: 706–714.10.1016/j.hal.2009.02.003Search in Google Scholar
Lindholm, T. and C. Nummelin. 1999. Red tide of the dinoflagellate Heterocapsa triquetra (Dinophyta) in a ferry-mixed coastal inlet. Hydrobiol. 393: 245–251.10.1007/978-94-017-0912-5_25Search in Google Scholar
Litaker, R.W., P.A. Tester, C.S. Duke, B.E. Kenney, J.L. Pinckney and J. Ramus. 2002. Seasonal niche strategy of the bloom-forming dinoflagellate Heterocapsa triquetra. Mar. Ecol. Prog. Ser. 232: 45–62.10.3354/meps232045Search in Google Scholar
Liu, D., J. Sun, J. Zou and J. Zhang. 2005. Phytoplankton succession during a red tide of Skeletonema costatum in Jiaozhou Bay of China. Mar. Poll. Bull. 50: 91–94.10.1016/j.marpolbul.2004.11.016Search in Google Scholar PubMed
Lu, S. and I.J. Hodgkiss. 2004. Harmful algal bloom causative collected from Hong Kong waters. Hydrobiol. 512: 231–238.10.1007/978-94-007-0944-7_30Search in Google Scholar
Mallin, M.A., L.B. Cahoon, M.R. Mciver, D.C. Parsons and G.C. Shank. 1999. Alternation of factors limiting phytoplankton production in the Cape Fear River Estuary. Estuaries22: 825–836.10.2307/1353064Search in Google Scholar
Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone, eds. 2009 onwards. IOC-UNESCO Taxonomic Reference List of Harmful Micro Algae. Accessed at http://www.marinespecies.org/hab on 2019-01-09.Search in Google Scholar
Okaichi, T. 1989. Red tide problems in the Seto Inland Sea, Japan. In: (T. Okaichi, D.M. Anderson and T. Nemoto, eds) Red tides. Biology, environmental science and toxicology. Elsevier, New York. pp. 137–144Search in Google Scholar
Okus, E., A. Aslan, S. Tas, N. Yılmaz and C. Polat. 2001. Nutrient and chlorophyll a distribution of Golden Horn. In: (I. Ozturk, E. Okus, H.Z. Sarıkaya, C. Gazioglu and A.F. Aydın, eds) Golden Horn 2001 symposium, 3–4 May 2001, Istanbul, Turkey, pp. 145–152. (In Turkish).Search in Google Scholar
Olli, K. 2004. Temporary cyst formation of Heterocapsa triquetra (Dinophceae) in natural populations. Mar. Biol.145: 1–8.10.1007/s00227-004-1295-9Search in Google Scholar
Olli, K., A.S. Heiskanen and J. Seppälä. 1996. Development and fate of Eutreptiella gymnastica bloom in nutrient-enriched enclosures in the coastal Baltic Sea. J. Plank. Res. 18: 1587–1604.10.1093/plankt/18.9.1587Search in Google Scholar
Parsons, T.R., Y. Maita and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, UK. pp. 173.Search in Google Scholar
Qi, Y., J. Chen, Z. Wang, N. Xu, Y. Wang, S. Pingping, L. Songhui and I.J. Hodgkiss. 2004. Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, southern China in 1998. Hydrobiol. 512: 209–214.10.1007/978-94-007-0944-7_28Search in Google Scholar
Rensel, J. 2007. Fish kills from the harmful alga Heterosigma akashiwo in Puget Sound: Recent blooms and review. A technical report. National Oceanic and Atmospheric Administration Center for Sponsored Coastal Ocean Research (CSCOR), pp. 58.Search in Google Scholar
Rensel, J.E., N. Haigh and T.J. Tynan. 2010. Fraser river sockeye salmon marine survival decline and harmful blooms of Heterosigma akashiwo. Harmful Algae 10: 98–115.10.1016/j.hal.2010.07.005Search in Google Scholar
Smayda, T.J. 1990. Novel and nuisance phytoplankton blooms in the sea: Evidence for a global epidemic. In: (E. Granéli, B. Sundström, L. Edler and D.M. Anderson, eds) Toxic marine phytoplankton. Elsevier, New York. pp. 29–40.Search in Google Scholar
Sur, H.I., E. Okuş, H.Z. Sarikaya, H. Altiok, V. Eroğlu and I. Öztürk. 2002. Rehabilitation and water quality monitoring in the Golden Horn. Wat. Sci. Tech. 46: 29–36.10.2166/wst.2002.0138Search in Google Scholar
Tas, S. 2015. A prolonged red tide of Heterocapsa triquetra (Ehrenberg) F. Stein (Dinophyceae) and phytoplankton succession in a eutrophic estuary (Turkey). Medit. Mar. Sci. 16: 21–627.10.12681/mms.1049Search in Google Scholar
Tas, S. and N. Lundholm. 2017. Temporal and spatial variability of the potentially toxic Pseudo-nitzschia spp. in a eutrophic estuary (Sea of Marmara). J. Mar. Biol. Assoc. 97: 1483–1494.10.1017/S0025315416000837Search in Google Scholar
Tas, S. and E. Okus. 2003. The effects of pollution on the distribution of phytoplankton in the surface water of the Golden Horn. Turk. J. Mar. Sci. 9: 163–176.Search in Google Scholar
Tas, S. and E. Okus. 2011. A review on the Bloom Dynamics of a Harmful Dinoflagellate Prorocentrum minimum in the Golden Horn Estuary. Turk. J. Fish. Aqua. Sci. 11: 523–531.Search in Google Scholar
Tas, S. and I.N. Yilmaz. 2015. Potentially harmful microalgae and algal blooms in a eutrophic estuary in the Sea of Marmara (Turkey). Medit. Mar. Sci. 16: 432–443.10.12681/mms.1042Search in Google Scholar
Tas, S., E. Okus and A. Aslan-Yilmaz. 2006. The blooms of a cyanobacterium, Microcystis cf. aeruginosa in a severely polluted estuary, the Golden Horn, Turkey. Estuar. Coast. Shelf Sci. 68: 593–599.10.1016/j.ecss.2006.02.025Search in Google Scholar
Tas, S., I.N. Yilmaz and E. Okus. 2009. Phytoplankton as an indicator of improving water quality in the Golden Horn Estuary. Estuar. Coasts 32: 1205–1224.10.1007/s12237-009-9207-3Search in Google Scholar
Tas, S., H.A. Ergul and N. Balkıs. 2016a. Harmful algal blooms (HABs) and mucilage formations in the Sea of Marmara. In: (E. Özsoy, N. Çağatay, N. Balkıs, N. Balkıs and B. Öztürk, eds) The Sea of Marmara: marine biodiversity, fisheries, conservation and governance. Turkish Marine Research Foundation (TUDAV), Istanbul, Turkey. pp. 768–786.Search in Google Scholar
Tas, S., F. Dursun, A. Aksu and N. Balkis. 2016b. Presence of the diatom genus Pseudo-nitzschia and particulate domoic acid in the Golden Horn Estuary (Sea of Marmara, Turkey). Dia. Res. 31: 339–349.10.1080/0269249X.2016.1247020Search in Google Scholar
Terenko, L. and G. Terenko. 2012. Dominant Pseudo-nitzschia (Bacillariophyta) species in the Black Sea (Ukraine). Bot. Lithuan. 18: 27–34.10.2478/v10279-012-0004-8Search in Google Scholar
Thessen, A.E., Q. Dortch, M.L. Parsons and W. Morrison. 2005. Effect of salinity on Pseudo-nitzschia species (Bacillariophyceae) growth and distribution. J. Phycol. 41: 21–29.10.1111/j.1529-8817.2005.04077.xSearch in Google Scholar
Trainer, V.L., N.G. Adams, B.D. Bill, C.M. Stehr and J.C. Wekell. 2000. Domoic acid production near Californian coastal upwelling zones, June 1998. Limnol. Ocean. 45: 1818–1833.10.4319/lo.2000.45.8.1818Search in Google Scholar
Trainer, V.L., S.S. Bates, N. Lundholm, A.E. Thessen, W.P. Cochlan, N.G. Adams and C.G. Trick. 2012. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae 14: 271–300.10.1016/j.hal.2011.10.025Search in Google Scholar
Utermöhl, H. 1958. Zur Vervollkommung der quantitativen Phytoplankton-Methodik. Mitt int. Ver. Theor. Angew. Limnol. 9: 1–38.10.1080/05384680.1958.11904091Search in Google Scholar
Uysal, Z. 1996. A net-plankton study in the Bosporus junction of the Sea of Marmara. Turk. J. Bot. 20: 321–327.10.55730/1300-008X.2623Search in Google Scholar
Wang, Z.H., Y.Z. Oi and Y.F. Yang. 2007. Cyst formation: an important mechanism for the termination of Scrippsiella trochoidea (Dinophyceae) bloom. J. Plank. Res. 29: 209–218.10.1093/plankt/fbm008Search in Google Scholar
Yamaguchi, M., S. Itakura, K. Nagasaki, Y. Matsuyama, T. Uchida and I. Imai. 1997. Effects of temperature and salinity on the growth of the red tide flagellates Heterocapsa circularisquama (Dinophyceae) and Chattonella verruculosa (Raphidophyceae). J. Plank. Res. 19: 1167–1174.10.1093/plankt/19.8.1167Search in Google Scholar
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