Development an Blooms of Peridinea Akashivo sanguinea in the Bulgarian Marine Aquatories  

Daniela  Klisarova , Dimitar  Gerdzhikov
Institute of fish resources - Varna, Bulgaria
Author    Correspondence author
International Journal of Marine Science, 2016, Vol. 6, No. 49   doi: 10.5376/ijms.2016.06.0049
Received: 21 Sep., 2016    Accepted: 30 Nov., 2016    Published: 05 Dec., 2016
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Klisarova D., and Gerdzhikov D., 2016, Development and Blooms of Peridinea Akashivo sanguinea in the Bulgarian Marine Aquatories, International Journal of Marine Science, 6(49): 1-7 (doi:10.5376/ijms.2016.06.0049)


The article presents results of empirical field research on the development and distribution of the ''unarmoured'' peridinea Akashivo sanguinea in the Bulgarian marine aquatories during the period 1995-2015. The analysis has established that A. sanguinea is a phytoplankton species relatively rarely met in the water in front of the Bulgarian coast. The development and blooms of the species have been identified both in the surface water layer and up to 25 m (layer above the thermocline). It developed mainly in water areas rich in nutrients (Varna Bay, Burgas Bay, Balchik), but also in open sea areas (10-30 miles offshore), probably under the influence of the Danube inflow. Basically the blooms of the species were recorded in the mid-90s and at the beginning of the new century (2001). After this period the concentrations of A. sanguinea were minimal. A constant trend of reducing the size of the cells of the species has been registered.


The purpose of this study was to describe, track and analyze the patterns in the development and distribution of the phytoplankton species A. sanguinea in the Bulgarian marine aquatories during that 20 year period.

Black sea; Bulgarian marine aquatories; Blooms; Peridineas; Akashivo sanguinea; Spatial and temporal distribution


Many phytoplankton species cause blooms and red tides in the aquatic ecosystems. Marine coastal areas are important ecosystems and are source for fishing, aquaculture and tourism. However, they are subject of pollution, eutrophication and harmful algal blooms which cause a widespread problem (Smayda, 1997).


Through the eutrophication period (1970-1995) of the Black Sea ecosystem in the water in front of the Bulgarian coast were observed numerous cases of intense and prolonged phytoplankton blooms leading to reduced biodiversity and destruction of bottom biocenoses (Kamburska et al., 2003; Moncheva and Doncheva, 1998; Moncheva et al., 1995; Nesterova, 1987; Petrova - Karadjova, 1984; Shiganova et al., 2008; Velikova et al., 1999; Zaitsev and Mamaev, 1997;). Dozens of phytoplankton species were recorded into a state of blooms.


Reduction of phytoplankton development in the Bulgarian marine aquatories has started after 1995 (Bodeanu et al., 1998; Velikova et al., 2001). Specifically in Varna Bay, cape Galata and cape Emine reduction of phytoplankton quantitative development has been registered after 1998 (so called post-eutrophication period) (Gerdzhikov and Petrova, 2008).


Reduction in the number of blooming phytoplankton species, e.g., in Varna Bay for the period of the 90’s a total of 37 "blooming" species were observed (Velikova and Petrova, 1999), and in the period 2005-2014 were registered only 10 species, growing at much lower quantitative values (Klisarova et al., 2015).


Akashiwo sanguinea is a cosmopolitan dinoflagellate that has been observed to form major blooms in coastal ecosystems around the world. A. sanguinea plays a major role in the ecology of many marine environments, including coastal ecosystems with variable salinities, where its euryhaline character makes it competitive (Badylak et al., 2014).


Akashiwo sanguinea (K.Hirasaka) G.Hansen & Ø.Moestrup in N.Daugbjerg, G.Hansen, J.Larsen, & Ø.Moestrup 2000 (Daugbjerg et al., 2000) Synonyms: Gymnodinium sanguineum K.Hirasaka 1922, Gymnodinium splendens Lebour 1925, Gymnodinium nelsonii Martin, 1929. The genus name akashiwo is Japanese for red tide.


A. sanguinea is exclusively planktonic and has a worldwide distribution in temperate and tropical waters. It is nearly always found in coastal and estuarine locations. It is one of the largest dinoflagellates with about 40-80 µm length and 30-50 µm width. According to Bockstahler and Coats (1993), A. sanguinea is mixotrophic, being primarily photosynthetic but also feeding on ciliate protozooplankton if necessary.  It is also susceptible to parasitic dinoflagellates such as Amoebophrya (Coats and Park, 2002). In general, this species is not considered to be toxic. Reports of toxicity in A. sanguinea are mostly anecdotal and based on its abundance in natural populations in which mortality has occurred. However, toxicity of mice was reported by Tindall et al., (1984). Jessup et al., (2009) reported extensive seabird mortality caused by surfactant-like protein exudates derived from A. sanguinea, which coated their feathers and neutralized natural water repellency and insulation (Hargraves P. E, 2011, Akashiwo sanguinea. Protists of the Indian River Lagoon. Smithsonian Institution, For instance, Gymnodinium splendens and Gonyaulax polyedra release toxins that kill or exclude zooplankton and fish. Without herbivores, such blooms may be quasi-permanent (Longhurst, 2007).


Gymnodinium splendens (A.sanguinea) is a common Black Sea phytoplankton species but was observed in bloom concentrations for the first time in the 90's (1995, 1999) (Moncheva et al, 2001; Velikova et al., 1999). Near the coast of Florida blooms of A.sanguinea are detected at salinities from 7 to 23 ‰ (Phlips et al., 2012), in Monterey Bay the species blooms even at 33.53 ‰. In its mass development A.sanguinea can cause sea bird kills due to surfactant-like proteins that coat feathers and neutralize water repellency and insulation (Lewitus et al., 2012).


The estimated duration of cell division was 1.29 h, and the estimated in situ growth rate was 0.45 d -1, cells of A. sanguinea actively divided in the deeper layer (3.5 to 5 m) from 18:00 (Katano et al., 2011).


Although the number of species in the Bulgarian marine aquatories rarely crosses the border of 100x106 cells.m-3 due to its relatively large size (L = ~ 80μm), with its mass development the produced biomass reaches and exceeds bloom level of 10 000 mg.m-3 according to Moncheva and Parr (2010).



In tracing the available at IRR Varna data for the development of the species since 1993, a tendency for reduction of its quantitative development in the Bulgarian marine aquatories was established (Figure 1). Its biomass decreases with linear trend y = -387.6x + 7004.2 and R² = 0.1789, range= 53.64 ÷ 24018.82 mg.m-3, mean= 2740.56 mg.m-3, 5685.58 and the number with y = -3.2589x + 71.116 and R² = 0.1393, range=2.54 ÷ 216.33 mln. cells.m-3, mean=35.27 mln. cells.m-3, 54.17 (Figure 1).


The development of A. sanguinea in the brackish, hyper-eutrophic water areas of Varna and Beloslav Lakes is with lower values (3 times) (Figure 2). In the lakes, a decrease of development values over the years is also observed: the biomass decreases depending on regression y = -180.12x + 1696.6 and R² = 0.1107, range= 8.09÷ 4661.44 mg.m-3, mean= 795.99 mg.m-3, 1482.89 and the number with y = -1.944x + 22.817 and R² = 0. 0525, range= 0.25÷ 74.23 mln. cells.m-3, mean= 13.097 mln. cells.m-3, 23.24 (Figure 2).


The development of A.sanguinea takes place mainly in the surface water layer 0-10 m (Figure 3) and only in the periods from February to August, 1995 and from October, 2000 to June, 2001 exhibited high values in depth (till 25 m, thermocline and bottom) (Figure 4 and 5). In 2015 A. sanguinea was not detected in the samples.



Figure 1 Maximum annual values of number (mln. cells.m-3, right axis) and biomass (mg.m-3, left axis), of Akashivo sanguinea in the Bulgarian marine aquatories, 1993-2015



Figure 2 Maximum annual values of number (mln. cells.m-3, right axis) and biomass (mg.m-3, left axis), of Akashivo sanguinea in the Varna and Beloslav lakes, 1993-2015(data of IFR-Varna)



Figure 3 Distribution of the maximum numbers (mln. cells.m-3) and biomass (mg.m-3) of A.sanguinea by depth, 1995-2015


In the long-term set of samples from the water area along the entire Bulgarian coast, the highest bloom values of A. sanguinea were established in Varna Bay (24018.82 mg.m-3),  (1995, August, station B-3, 0m), (Technical Reports of Institute of fish resources, 1995); 30 miles in front of cape Galata (12240 mg.m-3), (2001, June, G-30, 5 m), (Velikova et al., 2004) and 10 miles in front of cape Emine (10644 mg.m-3), (2001, June, E-10, 10 m) (Technical Reports of Institute of fish resources, 2001) (Figure 6). In all other cases the species is present in the samples, but develops below the bloom concentrations.



Figure 4 Distribution of the maximum number (mln. cells.m-3) of A. sanguinea in years, months and depths from 1995 to 2015



Figure 5  Distribution of the maximum biomass (mg.m-3) of A. sanguinea in years, months and depths from 1995 to 2015


In the investigated 20-year period, the maximum length of the observed A. sanguinea cells decreases (Figure 7) under a linear relationship: y = -2.2624x + 91.023 and R² = 0.6181.



In the period 1995 - 2015 A.sanguinea was present in 740 numbers of analyzed samples. A. sanguinea is a relatively rare phytoplankton species in the Bulgarian marine aquatories with frequency of occurrence 18.54%.


After 1995, the only blooms of A. sanguinea were registered in 2001 (Velikova et al., 2004). On the contrary, during the Knorr cruise in spring, 2001 (Soydemir et al., 2002) was registered high abundance of dinoflagellates (98% of the total biomass) due to the proliferation of Gymnodinium splendens, co-dominated by the coccolothophoride E. huxley (42% of the total abundance) and an average biomass and abundance much higher than the reported values in the western Black Sea offshore area during the last decade (Moncheva S., State of knowledge of eutrophication and biological response in the Black Sea Ecosystem, Report-biology.doc,


Since 2002 blooms of A. sanguinea have not been registered (Figure 1). This coincides with the general reduction of phytoplankton development in the Bulgarian Black Sea water (Bodeanu et al., 1998; Gerdzhikov and Petrova, 2008; Klisarova et al., 2015; Velikova et al., 2001). Another reason could be the lack of samples precisely at the time of high concentrations of the species, because of the standard scheme of monthly sampling.



Figure Distribution of the maximum biomass (mg.m-3) of A. sanguinea along the Bulgarian coast, 1995-2015 (Ocean Data View v4.7.4, 2015 Reiner Schlitzer)



Figure 7 Dynamics of maximum linear dimensions (MLD) (µm) of the observed in the Bulgarian marine aquatories cells of A. sanguinea


According to Longhurst (2007), Gymnodinium splendens specially adapts to high nutrients and low turbulence. The ideal case to represent this quadrant are the red tides that occur in permanently stratified coastal waters where nutrient input is both continuous and strong. 


These characteristics of the development of A. sanguinea can explain the established by us 3 times lower concentrations of the species in nutrient-rich water of Varna and Beloslav lakes where due to no great depth and intense shipping traffic, a higher level of turbulence might be suggested compared with the water of the coastal areas (Figure 1 and 2).


In comparison, many developing in front of the Bulgarian coast blooming species were registered with fold higher concentrations in the catchment areas of lakes (Petrova and Gerdzhikov, 2006; 2007; 2011; 2012; 2013; Velikova and Petrova, 1999).


In contrast, blooms of A. sanguinea in the Bulgarian marine aquatories were registered only in Varna Bay and in water influenced by the Danube inflow (10-30 sea miles away from the coast). High numbers of the species were recorded also in Burgas Bay and one-mile area in front of Balchik, areas traditionally defined as "hot spots" in the coastal ecosystem (Figure 6).


The reducing of the size (Figure 7) of the representatives of A. sanguinea developing in the Bulgarian marine aquatories can probably be explained by the tendency of reduction of anthropogenic pressure. From this perspective, the average size of the species could be used as an index of measuring the degree of eutrophication of our sea water areas.


Materials and methods

The study was carried out within the period 1995 - 2015 in the Bulgarian Black Sea aquatories. The scientific expeditions were conducted on board the R/V Prof. Al. Valkanov. 3991 phytoplankton samples were collected from 127 stations at standard horizons (0, 10, 25, 50, 75 and 100 m) by bathometers type Niskin-5L or in shallow water (up to 15 m depth) at surface – bottom horizons (Figure 8). The samples were fixed onboard the ship in 2% formalin solution and concentrated by the sedimentary method (Morozova-Vodyanitskaya, 1954).


The qualitative and quantitative analyses of the samples were performed with a light microscope Nikon E400 and Olympus BX41 in counting cells Sedgewick Rafter - 1 ml and Palmer – Maloney - 0.05 ml, using standard methods (Moncheva and Parr, 2010). Software Phytomar 2.0 (IFR - Varna, 2008), Ocean Data View (v4.7.4, 2015 Reiner Schlitzer) and Excel 12 (Microsoft Office 2007) were used for calculations and graphs.



Figure 8 Map with sampling stations (Ocean Data View v4.7.4, 2015 Reiner Schlitzer)



Badylak S., Phlips E.J.,and Mathews A. L., 2014, Akashiwo sanguinea (Dinophyceae) blooms in a sub-tropical estuary: An alga for all seasons, Plankton Benthos Research, 9(3):147–155


Bockstahler  K.R., and Coats D.W., 1993, Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates, Journal of Eukaryotic Microbiology, 40: 49-60


Bodeanu N., Moncheva S., Ruta G., and Popa L., 1998, Long-term evolution of the algal blooms in Romanian and Bulgarian Black sea waters, Cercetari marine, 31: 37-55


Coats D.W. and Park M.G., 2002, Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity, Journal of Phycology, 38: 520-528


Daugbjerg N., Hansen G., Larsen J., and Moestrup, Ø., 2000, Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates, Phycologia, 39: 302-317


Gerdzhikov D., and Petrova D., 2008, Current trends in the development of phytoplankton community along the Bulgarian coast, Proceedings of Union of Scientists, Varna, 2`2003-1`2004: 91-96. (Bg)


Jessup D.A., Miller M.A., Ryan J.P., Nevins H.M., Kerkering H.A., Mekebri A., Crane D.B., Johnson T.A.,  and Kudela R.M., 2009, Mass stranding of marine birds caused by a surfactant-producing red tide, PLoS ONE 4: e4550. doi:10.1371/journal.pone.0004550


Kamburska L., Moncheva S., Konsulov A., Krastev A., and Prodanov K., 2003, The invasion of Beroe ovata in the Black Sea a warning signal for ecosystem concern, Proceedings of Institute of Oceanology, 4:111-123


Katano T., Yoshida  M., Yamaguchi  S., Hamada T., Yoshino  K., and Hayami, Y., 2011, Diel vertical migration and cell division of bloom-forming dinoflagellate Akashiwo sanguinea in the Ariake Sea, Japan, Plankton Benthos Res, 6(2): 92–100


Klisarova D., Gerdzhikov D., Kostadinova G., and Petkov G., 2015, Investigation of phytoplankton in the Varna bay (2005-2014), In: E. Özhan (ed.), Proceedings of the Twelfth International Conference on the Mediterranean Coastal Environment, MEDCOAST 2015, Varna, Bulgaria, pp.299-308


Lewitus A.J., Horner  R. A., Caron  D.A., Garcia-Mendoza  E., Hickey B.M., Huntere, M., Huppert D.D., Kudela R.M., Langlois G.W., Largier J.L., Lessard E.J., RaLonde R., Jack Rensel J.E., Strutton P.G., Trainerm V.L.,  and Tweddle J.F., 2012, Harmful algal blooms along the North American west coast region: History, trends, causes, and impacts, Harmful Algae, 19:133–159


Longhurst A.R., 2007, Ecological geography of the sea, Sec.ed, Elsevier Academic Press, Burlington and San Diego, USA, pp.575


Moncheva S., and Doncheva V., 1998, Dinollagellates blooms and succession - an indicator of the enviromental changes in the Black Sea Ecosystem,  In: DINO - 6 -Sixth Int. Conf. Modern and Fossil Dinoflagellates, Trondheim. Norway, pp. 111-112


Moncheva S., Doncheva V., and Kamburska L., 2001, On the long-term response of harmful algal blooms to the evolution of eutrophication off the Bulgarian black sea coast: are the recent changes a sign of recovery of the ecosystem-the uncertainties, In: Hallegraeff, G., et al. (Eds.), Harmful Algal Blooms 2000, Intergovernmental Oceanographic Commission of UNESCO, Hobart, Tasmania, pp. 177-182


Moncheva S., and Parr B., 2005, Manual for Phytoplankton Sampling and Analysis in the Black Sea, (updated-2010), GEF/UNDP Black Sea Ecosystem Recovery Project (BSERP)-RER/01/G33/A/1G/31 & UPGRADE BLACK SEA SCENE Project, GA 226592, FP7, EC network-phytoplankton/Phytoplankton mannual-final.doc,  pp. 67


Moncheva S., Petrova-Karadjova V., and Palasov A., 1995, Harmful algal blooms along the bulgarian Black Sea coast and Possible patterns of Fish and Zoobenthic Mortalities, In: Lassus, P. et al. (eds ), Harmful Marine Algal Blooms, Lavoisier Publ. Inc., Paris, pp.193-198


Morozova - Vodyanitskaya N.V., 1954, Phytoplankton of the Black Sea, Part II, Proceedings of the Sevastopol Biological Station, 8:11-99. (Ru)


Nesterova D.A., 1987, Peculiarites of phytoplankton succession in the north-western Black Sea, Hydrobiology Journal, 23:16-21


Petrova - Karadjova V.Y., 1984, Amendment of planktonic flora in the Bulgarian water area of the Black Sea under the influence of the eutrophication, Proceedings of the Institute of Fish Resources - Varna, 21:105-112.(Bg)


Petrova D., and Gerdzhikov D., 2006, Distribution of Heterocapsa triquetra along the Bulgarian coast, Proceedings of Union of Scientists - Varna, 2`2005-1`2006: 58-64. (Bg)


Petrova D., and Gerdzhikov D., 2007, Dynamics of Cyclotella caspia development in the Bulgarian part of the Black Sea basin (1993-2004), Proceedings of the Institute of Fish Resources - Varna, 26:13-18


Petrova D., and Gerdzhikov D., 2011, Blooms of phytoplankton in coastal and brackish Black Sea waters, Proceedings of Union of Scientists - Varna, 56-60. (Bg)


Petrova D., and Gerdzhikov D., 2012, Dynamics in the qualitative composition of phytoplankton from different water areas along the Bulgarian Black Sea coast in 2009, Agricultural Science and Technology, 4(1):62-72


Petrova D., and Gerdzhikov D., 2013, Development of a traditional blooming phytoplankton species Prorocentrum cordatum Dodge, 1975 along the Bulgarian coast (2008-2010), Proceedings of Union of Scientists - Varna, 12-17. (Bg)


Phlips E.J., Badylak S., Hart J., Haunert D., Lockwood J., O’Donnell K., Sun D., Viveros P., and Yilmaz M., 2012, Climatic Influences on Autochthonous and Allochthonous Phytoplankton Blooms in a Subtropical Estuary, St. Lucie Estuary, Florida, USA, Estuaries and Coasts, 35:335–352


Shiganova T., E. Musaeva, E. Araskievich, Kamburska L., Stefanova K., Mihneva V., Polishchuk L., Timofte F., Ustun F., Oguz T., Khalvashi M., and Tarkan A.N., 2008, The state of zooplankton. In: Oguz T. (ed.), State of the Environment of the Black Sea (2001–2006/7), The Commission on the Protection of the Black Sea Against Pollution publication, pp. 148–197


Smayda T.J., 1997, What is a bloom? A commentary, Limnology and Oceanography, 42:1132-1136


Soydemir N., Kideys A., and Ekinger G., 2002, Phytoplankton composition of the western Black Sea during May-June, 2001, In: II Int. Conference “Oceanography of the Eastern Mediterranean and the Black Sea – Similarities and differences of two interconnected basins”, Ankara, Turkey, pp.360


Tindall D.R., Dickey R.W., Carlson R.D., and Morey-Gaines G., 1984, Ciguatoxigenic Dinoflagellates from the Caribbean Sea, In:  E.P. Ragelis (Ed.) Seafood Toxins. ACS Symposium Series 262, American Chemical Society. Washington, DC. pp.225-240


Velikova V., Boicenco L., Cociasu A., Popa L., Davidov A., and Petrova D., 2004, The Black Sea phytoplankton community in a period of reduced anthropogenic pressure, In: 11th International Harmful Algal Blooms Conference (HAB), Cape Town, South Africa


Velikova V., Petrova D., Mihneva V., Dineva S., and Ouzounova S., 2001, Recent state of the Bulgarian Black Sea – signs of improvement of the ecosystem, In: Fifth International Conference on the Mediterranean Coastal Environment, MEDCOAST 01, Hammamet, Tunisia pp. 893-905


Velikova V., and Petrova D., 1999, Multiannual dynamics of phytoplankton in the Gulf Varna bay during 1991-1997, Proceedings of the Institute of Fish Resources - Varna, 25:89-102. (Bg)


Velikova V., Moncheva S., and Petrova D., 1999, Phytoplankton Dynamics and Red Tides 1987-1997 in the Bulgarian Black Sea, Water Science and Technology, 39(8): 27 – 36


Zaitsev Yu. and Mamaev V., 1997, Biological diversity in the Black sea, A study of Change and Decline, Unated Nations Publication, Black sea Environmental series, Vol.: 3, New York, pp.208

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