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Alternation of diatoms and coccolithophores in the north-eastern Black Sea: a response to nutrient changes

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Abstract

In many regions phosphorus limits coccolithophore growth, whereas nitrogen generally controls development of diatoms. We tested the hypothesis that a change in nutrient composition defines the alternation of these algae. Data on phytoplankton, nutrients, chlorophyll and primary production were obtained in May–June from 2002 to 2012. Coccolithophore bloom dynamics were analysed using satellite images of particular inorganic carbon (PIC). In some years coccolithophore bloom occupied the sea interior and has spread on shelf areas. Most frequently blooms occurred in the coastal waters and were absent in the deep basin. Diatoms and coccolithophores interchangeably prevailed in phytoplankton. In the coastal waters, high biomass of diatoms corresponded to the increased ammonium. In the deep basin, PIC was positively correlated with phosphate and negatively with the sea air temperature in February indicating that the bottom-up flux of pycnocline waters during winter convection is the main driver of coccolithophore bloom. In the coastal zone, high concentrations of phosphate and PIC corresponded to high precipitation periods. Thus, independent from origin, phosphorus might have determined the development of coccolithophores both in the coastal and deep waters. In general, diatoms predominated in phytoplankton at high nitrogen:phosphorus ratio, whereas coccolithophores at low.

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References

  • Bodeanu, N., 2002. Algal blooms in Romania Black Sea waters in the last two decades of the XX Century. Cercetari Marine, IRCM Constanta 34: 7–22.

    Google Scholar 

  • Bodeanu, N., C. Andrei, L. Boicenco, L. Popa & A. Sburlea, 2004. A new trend of the phytoplankton structure and dynamics in the Romanian marine waters. Recherches Marines 35: 77–86.

    Google Scholar 

  • Bordovskiy, O. K. & A. M. Chernyakova (eds), 1992. Modern Methods of the Ocean Hydrochemical Investigations. P.P.Shirshov Institute of Oceanology, Moscow. (in Russian).

    Google Scholar 

  • Burenkov, V. I., O. V. Kopelevich & S. V. Sheberstov, 2011. Seasonal and interannual variations of the biooptical characteristics of the Black Sea from satellite data. Current Problems of Remote Sensing from Space 8: 190–199. (in Russian).

    Google Scholar 

  • Chasovnikov, V. K., E. Yakushev, N. M. Menshikova, V. P. Chzy & N. L. Kuprikova, 2011. Variability of nutrients in the coastal zone of the Black Sea. In Esin, N. V. & B. S. Lomazov (eds), Multidisciplinary Studies in the Black Sea. Nauchny Mir, Moscow: 255–268. (in Russian).

    Google Scholar 

  • Cokacar, T., N. Kubilay & T. Oguz, 2001. Structure of Emiliania huxleyi blooms in the Black Sea surface waters as detected by SeaWIFS imagery. Geophysical Research Letters 28: 4607–4610.

    Article  Google Scholar 

  • Cokacar, T., T. Oguz & N. Kubilay, 2004. Satellite-detected early summer coccolithophore blooms and their interannual variability in the Black Sea. Deep-Sea Research I 54: 1017–1031.

    Article  Google Scholar 

  • Dortch, Q., 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology Progress Series 61: 181–203.

    Article  Google Scholar 

  • Eker-Develi, E. & A. E. Kideys, 2003. Distribution of phytoplankton in the southern Black Sea in summer 1996, spring and autumn 1998. Journal of Marine Systems 39: 203–211.

    Article  Google Scholar 

  • Eppley, R. W., J. N. Rogers & J. J. McCarthy, 1969. Half-saturation constants for uptake of nitrate and ammonium by marine phytoplankton. Limnology & Oceanography 14: 912–920.

    Article  CAS  Google Scholar 

  • Finenko, Z. Z., V. V. Syslin & T. Ya. Churilova, 2009. The regional model to calculate the Black Sea primary production using satellite color scanner SeaWiFS. Morski Ecological Journal 8: 81–106.

    Google Scholar 

  • Georgieva, L. V., 1993. Phytoplankton. Species composition and dynamics. In Kovalev, A. V. & Z. Z. Finenko (eds), Plankton of the Black Sea. Naukova Dymka, Kiev: 31–55. (in Russian).

    Google Scholar 

  • Georgieva, L. V. & L. G. Senichkina, 1996. Phytoplankton of the Black Sea: current research and prospects. Ekologiya Morya 45: 6–12. (in Russian).

    Google Scholar 

  • Grashoff, K., K. Kremling & M. Ehrhard, 1999. Methods of Seawater Analysis. Wiley-VCH, Weinheim-NewYork-Chichester-Brisbane-Singapore-Toronto.

    Book  Google Scholar 

  • Gvarishvili, T., 1988. Species composition and biodiversity of Georgian Black Sea phytoplankton. In Kollyakov, V., M. Uppenbrink & V. Metreveli (eds), Conservation of the Biological Diversity as a Prerequisite for Sustainable Development in the Black Sea Region, Vol. 46. Kluwer Academic Publishers, Dordrecht: 95–100.

    Google Scholar 

  • Holm-Hansen, O. & B. Riemann, 1978. Chlorophyll a determination: improvements in methodology. Oikos 30: 438–447.

    Article  CAS  Google Scholar 

  • Iglesias-Rodrigez, M. D., C. W. Brown, S. C. Doney, J. Kleypas, D. Kolber, Z. Kolber, P. K. Hayes & P. G. Falkowski, 2002. Representing key phytoplankton functional groups in ocean cycle models: Coccolithophorids. Global Biogeochemical Cycles 16: 1–20.

    Article  Google Scholar 

  • Jaoshvili, S., 2002. The rivers of the Black Sea. In Khomerki, I., G. Gigineishvili & A. Kordzadze (eds), European Environment Agency, Technical Report 71: 1–58.

  • JGOFS-protocols, 1994. In Protocols for the joint global ocean flux study (JGOFS) core measurements, manuals and guides, UNESCO 29: 119–122.

  • Kokurkina, E. V. & A. S. Mikaelyan, 1994. Composition and distribution of picocyanobacteria in the Black Sea in winter. Oceanology 34: 67–72.

    Google Scholar 

  • Kopelevich, O. V., V. I. Burenkov & S. V. Sheberstov, 2008. Case studies of optical remote sensing in the Barents Sea, Black Sea, and Caspian Sea. In Barale, V. & M. Grade (eds), Remote Sensing of the European Seas. Springer, Dordrecht: 53–66.

    Chapter  Google Scholar 

  • Kopelevich, O. V., V. I. Burenkov, S. V. Sheberstov & S.V. Vazyulya, 2012. Remote sensing of coccolithophore particles: regional features. PiE 2012. Particles in Europe. Program and Abstract Volume, ICM, Barcelona, Spain [available on internet at http://www.sequoiasci.com/wp-content/uploads/2013/10/PIE2012_ABSTRACT_VOLUME.pdf].

  • Kopelevich, O. V., V. I. Burenkov, S. V. Sheberstov, S. V. Vazyulya, M. Kravchishina, L. A. Pautova, V. A. Silkin, V. Artemiev & A. Grigoriev, 2014. Satellite monitoring of coccolithophore blooms in the Black Sea from ocean color data. Remote Sensing of the Environment 146: 113–123.

    Article  Google Scholar 

  • Korotaev, G., T. Oguz, A. Nikiforov & C. Koblinsky, 2003. Seasonal, interannual, and mesoscale variability of the Black Sea upper layer circulation derived from altimeter data. Journal of Geophysical Research-Oceans 108: 3122.

    Article  Google Scholar 

  • Krivenko, O. V., 2008. Contents and uptake of inorganic nitrogen in the Black Sea. Morski Ecological Journal VII: 13–26. (in Russian).

    Google Scholar 

  • Krylenko, V. V., R. D. Kosyan, M. V. Krylenko & I. S. Podymov, 2014. Transport of the solid material into the coastal zone near Gelendzhik as a result of extremely heavy rain. Oceanology 54: 97–104.

    Article  Google Scholar 

  • Lessard, E. J., A. Merico & T. Tyrell, 2005. Nitrate: phosphate ratios and Emiliania huxleyi blooms. Limnology & Oceanography 50: 1020–1024.

    Article  CAS  Google Scholar 

  • Litchman, E., C. A. Klausmeier, J. R. Miller, O. M. Schofield & P. G. Falkowski, 2006. Multi-nutrient, multi-group model of present and future oceanic phytoplankton communities. Biogeosciences 3: 585–606.

    Article  CAS  Google Scholar 

  • Lukashev, Y. F. & N. V. Shenderov, 1998. The role of the river discharge in the formation of the nutrient regime in the coastal zone of the Russian part of the Black Sea. Oceanology 38: 554–556.

    CAS  Google Scholar 

  • Mashtakova, G. P., 1985. Long-term changes of phytoplankton in the eastern part of the Black Sea. In Fishery and Oceanographic studies of the Black Sea. Nauka, Moscow 27: 50–61 (in Russia).

  • Medinets, S. & V. Medinets, 2012. Investigations of atmospheric wet and dry nutrient deposition to marine surface in western part of the Black Sea. Turkish Journal of Fisheries and Aquatic Sciences 12: 497–505.

    Article  Google Scholar 

  • Mikaelyan, A. S., V. A. Silkin & L. A. Pautova, 2011. Coccolithophorids in the Black Sea: their interannual and long-term changes. Oceanology 51: 39–48.

    Article  Google Scholar 

  • Mikaelyan, A. S., A. G. Zatsepin & V. K. Chasovnikov, 2013. Long-term changes in nutrient supply of phytoplankton growth in the Black Sea. Journal of Marine System 117–118: 53–64.

    Article  Google Scholar 

  • Moncheva, S. & A. Krastev, 1997. Phytoplankton long term alterations off Bulgarian Black Sea shelf. In Ozsoy, E. & A. S. Mikaelyan (eds), Sensitivity to Change: Black Sea, Baltic Sea and North Sea. Kluwer Academic Publishers, Dordrecht: 79–93.

    Chapter  Google Scholar 

  • Moncheva, S., O. Gotsis-Skretas, K. Pagou & A. Krastev, 2001. Phytoplankton blooms in Black Sea and Mediterranean coastal ecosystems subjected to anthropogenic eutrophication: similarities and differences. Estuarine, Coastal and Shelf Science 53: 281–295.

    Article  CAS  Google Scholar 

  • Moncheva, S., S. Gorinstein, G. Shtereva, F. Toledo, P. Arancibia, W. A. Booth, I. Goshev, M. Weisz & S. Trakhtenberg, 2003. Seasonal variability of phytoplankton at Varna Bay (Black Sea). Phytochemical Analysis 14: 245–250.

    Article  CAS  PubMed  Google Scholar 

  • Morozova-Vodyanitskaya, N. V. & E. V. Belogorskaya, 1957. About meaning of coccolithophorids and especially Pontosphaera in the Black Sea. Trudi of Sevstopol Biological Station IX: 14–21 (in Russian).

  • Morozova-Vodyanitskaya, N. V., 1957. Phytoplankton in the Black Sea and its quatitative development. Trudi of Sevstopol Biological Station IX: 1–13 (in Russian).

  • Nezlin, N. P. & V. Yu. Dyakonov, 1998. Seasonal and interaanual variations of surface chlorophyll concentration in the Black Sea. In Ivanov, L. & T. Oguz (eds), Ecosystem Modelling as a Management Tool for the Black Sea. Kluwer Academic Publishers, Dordrecht: 137–150.

    Google Scholar 

  • Oguz, T., 2008. General oceanographic properties: physico-chemical and climatic features. In Oguz, T. (Ed.), State of the Environment of the Black Sea (2001–2006/7). BSC, Istanbul: 39–60.

    Google Scholar 

  • Oguz, T., V. Velikova, A. Cosiasu & A. Korchenko, 2008. The state of eutrophication. In Oguz, T. (Ed.), State of the Environment of the Black Sea (2001–2006/2007). BSC, Istanbul: 83–112.

    Google Scholar 

  • Pakhomova, S., E. Vinogradova, E. Yakushev, A. Zatsepin, G. Shtereva, V. Chasovnikov & O. Podymov, 2014. Interannual variability of the Black Sea proper oxygen and nutrients regime: the role of climatic and anthropogenic forcing. Estuarine, Coastal and Shelf Science 140: 134–145.

    Article  CAS  Google Scholar 

  • Pautova, L. A., A. S. Mikaelyan & V. A. Silkin, 2007. Structure of plankton phytocoenoses in the shelf waters of the northeastern Black Sea during the Emiliania huxleyi bloom in 2002–2005. Oceanology 47: 477–480.

    Article  Google Scholar 

  • Rat’kova, T. N., 1989. Phytoplankton of the open areas of the Black Sea. In Vinogradov, M. E. & M. V. Flint (eds), Structure and Production Characteristics of the Black Sea Plankton Communities. Nauka, Moscow: 38–52. (in Russian).

    Google Scholar 

  • Riegman, R., W. Stolte, A. A. M. Noordeloos & D. Slezak, 2000. Nutrient uptake and alkaline phosphatase (EC 3:1:3:1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. Journal of Phycology 36: 87–96.

    Article  CAS  Google Scholar 

  • Sahin, F., L. Bat, F. Ustun, Z. Birinci Ozdemir, H. H. Satilmis, A. E. Kideys & E. Eker Develi, 2007. The dinoflagellate-diatom ratio in the southern Black Sea off Sinop in the years 1999-2000. Rapport Commission International Mer Mediterranee 38: 388.

    Google Scholar 

  • Sapozhnikov, V. V., 1990. Ammonia in the Black Sea. Oceanology 38: 53–58.

    Google Scholar 

  • Senicheva, M. I., 1980. Seasonal dynamics of the phytoplankton number, biomass and production in the Sevastopol Bay. Ekologiya Morya 1: 3–11. (in Russia).

    Google Scholar 

  • Sheberstov, S. V. & E. A. Lucanova, 2007. A system for acquisition, processing and storage of satellite and field biooptical data. In Proceedings of IY International Conference: current problems on optics of natural waters. Nizhny Novgorod: 179–183.

  • Silkin, V. A., L. A. Pautova & A. S. Mikaelyan, 2009. Role of phosphorus in regulation of Emiliania huxleyi (Lohm.) Hay et Mohl. (Haptophyta) blooms in the northeastern Black Sea. International Journal on Algae 11: 211–221.

    Article  CAS  Google Scholar 

  • Silkin, V. A., L. A. Pautova, S. V. Pakhomova, A. V. Lifanchuk, E. V. Yakushev & V. K. Chasovnikov, 2014. Environmental control on phytoplankton community structure in the NE Black Sea. Journal of Experimental Marine Biology and Ecology 461: 267–274.

    Article  Google Scholar 

  • Steemann Nielsen, E., 1952. The use of radioactive carbon (C14) for measuring organic production in the sea. Journal du Conseil Permanent International pour l’Exploration de la Mer 18: 117–140.

    Article  Google Scholar 

  • Sukhanova, I. N. & T. N. Rat’kova, 1977. A comparison of the abundance of phytoplankton in samples collected by the double filtration method and standard settling technique. Oceanology 17: 691–693.

    Google Scholar 

  • Sukhanova, I. N., A. S. Mikaelyan & L. V. Georgieva, 1991. Spatial distribution and temporal variability of the Black Sea phytoplankton in spring (March–April 1988). In Agapova, I. Ya. (Ed.), Studies of phytoplankton in system of monitoring of the Baltic and other seas of USSR. Hydrometeoizdat, Moscow: 86–96 (in Russian).

  • Titov, V. B., 2004. Formation of the upper convective layer and the cold intermediate layer in the Black Sea in relation to the winter severity. Oceanology 44: 327–330.

    Google Scholar 

  • Tomas, C. R. (Ed.), 1997. Identifying Marine Phytoplankton. Academic Press, San-Diego.

    Google Scholar 

  • Vasiliu, D., L. Boicenco, M. T. Gomoiu, L. Lazar & M. E. Mihailov, 2012. Temporal variation of surface chlorophyll a in the Romanian near-shore waters. Mediterranean Marine Science 13(2): 213–226.

    Article  Google Scholar 

  • Vedernikov, V. I., 1976. Effect of environmental factors on the values of assimilation number in natural populations of marine phytoplankton. Trudi of Oceanologia, IO RAN, Moscow 105: 106–129 (in Russian).

  • Vedernikov, V. I. & A. S. Mikaelyan, 1989. Structural and functional characters of the different size groups of the Black Sea phytoplankton. In Vinogradov, M. E. & M. V. Flint (eds), Structure and Production Characteristics of the Black Sea Plankton Communities. Nauka, Moscow: 84–104. (in Russian).

    Google Scholar 

  • Yayla, M., A. Yilmaz & E. Morkoc, 2001. The dynamics of nutrient enrichment and primary production related to recent changes in the ecosystem of the Black Sea. Aquatic Ecosystem Health and Management Society 4: 31–49.

    Google Scholar 

  • Yunev, O. A., S. Moncheva & J. Carstensen, 2005. Long-term variability of vertical chlorophyll a and nitrate profiles in the open Black Sea: eutrophication and climate change. Marine Ecology Progress Series 294: 95–107.

    Article  CAS  Google Scholar 

  • Yunev, O. A., J. Carstensen, S. Moncheva, A. Khaliulin, G. Ærtebjerg & S. Nixon, 2007. Nutrient and phytoplankton trends on the western Black Sea shelf in response to cultural eutrophication and climate changes. Estuarine, Coastal and Shelf Science 74: 63–76.

    Article  Google Scholar 

  • Zaitsev, Yu. & V. Mamaev, 1997. Marine Biological Diversity in the Black Sea: A Study of Change and Decline. GEF Black Sea Environmental Programme, United Nations Publications, New York.

    Google Scholar 

  • Zatsepin, A. G., A. I. Ginzburg, A. G. Kostianoy, V. V. Kremenetskiy, V. G. Krivosheya, P. M. Poulain & S. V. Stanichny, 2003. Observation of Black Sea mesoscale eddies and associated horizontal mixing. Journal of Geophysical Research 108: 1–27.

    Article  Google Scholar 

  • Zavialov, P. O., P. N. Makkaveev, B. V. Konovalov, A. A. Osadchiev, P. V. Khlebopashev, V. V. Pelevin, A. B. Grabovskiy, A. S. Izhitskiy, I. V. Goncharenko, D. M. Soloviev & A. A. Polukhin, 2014. Hydrophysical and hydrochemical characteristics of the sea areas adjacent to the estuaries of small rivers of the Russian coast of the Black Sea. Oceanology 54: 293–308.

    Article  CAS  Google Scholar 

  • Zhang, Q. & G. Hu, 2011. Effect on nitrogen to phosphorus ratios on cell proliferation in marine micro algae. Chinese Journal of Oceanology & Limnology 29: 739–745.

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partly financially supported by EU-funded projects PERSEUS (Contract No. 287600), COCCONET (Contract No. 287844) and Russian Foundation for Basic Research (Grants No. 13-05-00029). The authors are grateful to anonymous referee for very valuable critical comments and the editing of the paper.

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  1. P.P. Shirshov Institute of Oceanology RAS, Moscow, Russia

    Alexander S. Mikaelyan, Larisa A. Pautova & Sergey A. Mosharov

  2. Southern Branch of P.P. Shirshov Institute of Oceanology RAS, Gelendzhik, Russia

    Valeriy K. Chasovnikov & Vladimir A. Silkin

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  1. Alexander S. Mikaelyan
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  2. Larisa A. Pautova
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  3. Valeriy K. Chasovnikov
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  4. Sergey A. Mosharov
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  5. Vladimir A. Silkin
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Correspondence to Alexander S. Mikaelyan.

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Mikaelyan, A.S., Pautova, L.A., Chasovnikov, V.K. et al. Alternation of diatoms and coccolithophores in the north-eastern Black Sea: a response to nutrient changes. Hydrobiologia 755, 89–105 (2015). https://doi.org/10.1007/s10750-015-2219-z

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