The Europaen Commission The Commission on the Protection of the Black Sea Against Pollution
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Report Contents

Preface Chapter 1A Chapter 1B Chapter 2 Chapter 3 Chapter 4 Chapter 5 Chapter 6 Chapter 7 Chapter 8 Chapter 9 Chapter 10 Chapter 11 Chapter 12
List of Tables List of Figures

State of Environment Report 2001 - 2006/7

Chief Editor, Prof. Dr. Temel Oguz, Institute of Marine Sciences, Middle East Technical University, Erdemli, Turkey

Chapter 5 - State of Phytoplankton

State of the Environment of the Black Sea - 2009

CHAPTER 5 THE STATE OF PHYTOPLANKTON

D. Nesterova

Odessa Branch, Institute of Biology of the Southern Seas, NASU, Odessa, Ukraine

S. Moncheva

Institute of Oceanology, Bulgarian Academy of Sciences, Varna, Bulgaria

A. Mikaelyan1, A. Vershinin1 and V. Akatov2

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

2 Maykop State Technological University,Maykop, Russia

L. Boicenco

National Institute for Marine Research and Development ?Grigore Antipa? (NIMRD), Constanta, Romania

Y. Aktan3 and F. Sahin4

3 Marine Sciences, Faculty of Fisheries, Istanbul University, Istanbul, Turkey

4 Sinop University, Fisheries Faculty, 57000 Sinop, Turkey

T. Gvarishvili

Georgian Marine Ecology and Fisheries Research Institute (MEFRI),

Batumi, Georgia

5.1. Introduction

Phytoplankton as the foundation of marine trophic chain is among the best indicators for assessment of the state of eutrophication. Nutrient enrichment/eutrophication often gives rise to shifts in phytoplankton species composition (e.g. from diatoms to dinoflagellates) and an increase in the frequency and/or magnitude and/or duration of phytoplankton (including nuisance/potentially toxic) blooms. The present chapter analyzes the recent trends of changes in phytoplankton species composition and then highlights main features of its contemporary state along the Black Sea shelf waters. The assessments are based on the evaluation of historical data as well as those collected during the present decade within the framework of various international and regional field campaigns as well as national monitoring programs.?

5.2. Species composition

Data compiled by many sources documented 750 phytoplankton species in the Black Sea (Ivanov 1965, Pitsyk 1950, Sorokin, 2002). Owing to considerable differences in hydrological and hydrochemical properties, phytoplankton composition differed considerably in different parts of the sea. In particular, the shallow, less saline and heavily euthrophied northwestern part of the sea sustained large number of brackish and freshwater species as compared with other parts (Ivanov, 1967).

Northwestern and Crimean shelves: A summary of the lists of phytoplankton species studied in 1973-2005 in the northwestern Black Sea shelf (NWS) (Nesterova, 1998; Guslyakov and Terenko, 1999; Nesterova and Terenko, 2000; Terenko, 2004; Nesterova and Terenko, 2007) showed that phytoplankton is represented by 697 species and interspecies pertaining to 11 phyla (Table 5.1). During 1973 ? 2005, diatoms and dinophytes constituted main species as observed prior to 1973, but their ratio has changed in comparison to 1950s (Ivanov, 1967). The diatom species decreased from 48.3% to 34.9%, while dinophytes increased from 20.4 % to 28.5 %. Freshwater green algae species increased from 16.7% to 22.5%, while blue-green algae remained around 5-6%. Due to revised phytoplankton composition, representatives of new phyla of Cryptophyceae Hillea fusiformis, Prasinophyceae Pterosperma cristatum, Pt. jorgensenii and a Choanoflagellida Bicosta spinifera species appeared. An increase in the species diversity of dinophytes was noted in 1973 ? 1993 when 36 new species were listed in the NWBS (Nesterova, 1998). Later, 48 species were added to the list of which 37 were new to the Black Sea (Terenko, 2004; 2005). The dinophytes included potentially toxic species Alexandrium psedogonyaulax, Cochlodinium polykrikoides, Gyrodinium cf. aureolum (Terenko, 2005, 2005 а) as well as a new species (Prorocentrum ponticus) and a new variety (Prorocentrum micans var. micans f. duplex) (Krakhmalniy and Terenko, 2002). Similarly, new green algae appeared as the genera Monoraphidium (M. contortum, M. obtusum) and Scenedesmus (Sc. polyglobulus). At present, the number of marine and marine-brackish species decreased from 60.3% to 50.5%. Simultaneously, there has been an increase in freshwater and freshwater-brackish species ? 49.5% and 39.7%, respectively.

The bulk of phytoplankton abundance and biomass is represented by a massive development of a small group of species in certain seasons. In the 1950s ? 1960s, it was 41 species (Ivanov, 1967), and increased to 85 species in the past two decades (Black Sea, 1998). Besides the usual representatives as Skeletonema costatum, Cerataulina pelagica, Chaetoceros socialis, Leptocylindrus danicus, Prorocentrum cordatum, Pr.micans, other species like Leptocylindrus minimus, Chaetoceros insignis, Gyrodinium cornutum, cryptophytes Hillea fusiformis, coccolithophorides Emiliania huxleyi, freshwater diatoms Skeletonema subsalsum, Stephanodiscus hantzschii, blue-green algae of the genera Gleocapsa Merismopedia have entered into the NWBS phytoplankton bloom events. Common species including Heterocapsa triquetra, Scripsiella trochoidea were found in the NWBS in 1957-1961 (Ivanov, 1963). Besides, typical summer ? autumn phytoplankton species like Thalassionema nitzschioides, Chaetoceros curvisetus were observed in 1950 ? 1960, while Pseudosolenia calcar avis tended to decrease in frequency and abundance (Nesterova, 1987).

Table 5.1. Taxonomic composition of Black Sea phytoplankton in Ukraine waters

Phyla

Northwestern part

Southeastern coast of Crimea

1954-60*

1973-05**

1938-59***

1979-98****

Bacillariophyceae

180

243

73

63

Dinophyceae

76

199

39

69

Cryptophyceae

-

8

3

-

Chlorophyceae

62

158

4

3

Cyanophyceae

24

37

4

2

Prymnesiophyceae

9

25

19

-

Chrysophyceae

4

6

5

27

Dictyochophyceae

5

7

-

-

Prasinophyceae

-

2

-

-

Euglenophyceae

12

11

-

1

Choanoflagellidea

-

1

-

-

Total

372

697

125

165

         
         

*?? Ivanov (1967); **?? Nesterova (2006); Nesterova, Terenko, 2007; ***?? Proshkina-Lavrenko (1955) and Ivanov (1965); **** ? Senichkina et al. (2001)

Phytoplankton species in the southeastern coast of Crimea during the 1940?1960s included 125 species and interspecies taxa from 5 algal phyla (Table 5.1) (Stroykina, 1950; Koshevoy, 1959; Mironov, 1961). In more recent years (1979?1998), it increased to 165 species and varieties, which all indicated some changes in taxonomic composition. In contrast to the previous phase, dinophytes increased from 31.2 % to 41.8 and chrysophytes from 4% to 15.1%, while diatoms decreased from 58.4% to 38.1%. The species diversity of coccolithophorids rose to 74 new species which were common for the whole Black Sea, while 21 species were observed for the first time.

Compared to 211 species and varieties of planktonic algae recorded in the Sevastopol Bay in 1948 (Senicheva, 2000), there were 84 species in 1996 - 1997 and 173 species and varieties in 2001 ? 2004. The latter was represented by 11 classes and 2 taxonomic groups; small flagellate algae and olive green cells. The basis of species diversity was similar to that of the NWBS and mainly composed of diatoms (45%), dinophytes (35%), and also Prasinophyceae (11%) (Polikarpov et al., 2003). The composition of dominant species of Skeletonema costatum, Leptocylindrus danicus, Chaetoceros socialis near Sevastopol for a period of 65 years has not undergone significant changes (Polikarpov et al., 2003). Pseudo-nitzschia delicatissima was an exception replacing Cerataulina pelagica in 2001 ? 2004. Changes have been noted mainly in the composition of subdominant species replacing the dinophyte algae of the genera Glenodinium, Protoperidinium, Prorocentrum for Prymnesiophyceae genera of Syracosphaera and Emiliania. At the same time new diatom species have been encountered along the coast of Crimea, and a new variety has been described as Chaetoceros diversus var. papilionis (Senicheva, 2002) as well as dinophytes and silicoflagellates (Kuzmenko, 1966; Senichkina, 1973).

Western Black Sea shelf: The revision of phytoplankton check-list in 1980-2005 documented 544 species distributed among 8 classes (Fig. 5.1) which indicated more than two-fold increase as compared to 230 species listed in the 1954-1980 period. Although a part of this change was related to improved sampling strategy, microscope quality, frequency and regions of sampling, changing environmental conditions and introduction of exotic species also played a role (Moncheva, Kamburska, 2002). Diatoms (212 species) and dinoflagellates (162 species) constituted bulk of the phytoplankton pool; the Dinophyceae species contribution rose to about 40% of the total number, e.g. an increase of more than 3 times. The same also applies to other classes; for example, species from Cryptophyceae and Choanoflagellates groups have not been reported at all before 1980s. The presence of rare and new Bacillariophyceae (Thallasiotrix longissima, Th. antarctica Lioloma elongatum, L. pacificum,Triblionella acuminate),? Dinophyceae (Ceratium furca var. bergii, Ceratium furca var. eugramma, Cochlodinium archimedes, C. citron, Kofoidinium lebourae), a number of Gymnodinium species? (Gymnodinium canus, G. cintum, G. dominans, Gymnodinium fuscum etc.) Gyrodinium (Gyrodinium spirale), and numerous Cryptophyceae (mainly from genus Chroomonas, Cryptomonas, Rhodomonas, Leucocryptos etc), Chlorophyceae (Kirchneriella, Trochiscia, Treubaria), Chrysophyceae (Braarudosphaera bigelowi, Octactis octonaria, Calciosolenia granii v. cylindrotheca, etc.), and different microflagellates add significantly to the diversification of phytoplankton assembly. Most of the species listed above are mixo-heterothrophs, that might have important functional bearings at ecosystem level (Moncheva et al., 2005; 2006; Velikova et al., 1999; 2005). An apparent feature of phytoplankton communities after 2000 was further increase of species diversity and species richness per sample (normally above 40) as detected since the mid-1990?s (Moncheva, 1999, Moncheva, 2003, 2005, 2006, 2007, Velikova et al., 1999, Velikova, 2004). More than 70% of the Shannon-Weaver biodiversity index was below the critical value of 2 in the 80-ies - the lowest being in summer of 1983-1985. This index dropped below 2 only during the winter-spring phytoplankton blooms in the 1990s, and this trend was maintained after 2000.

Fig. 5.1. Phytoplankton species diversity by taxonomic classes in the Bulgarian shelf.

BAC - Bacillariophyceae; DIN - Dinophyceae; CHR - Chrysophyceae; CYA - Cyanophyceae; CRY - Cryptophyceae; EUG - Euglenophyceae; CHL - Chlorophyceae; CHO - Choanoflagellates

The long-term taxonomic structure of phytoplankton biomass shows a likely shift from a diatom dominant system (constituting 60-90% of total biomass in the 60-ies) to an apparent dominance of opportunistic dinoflagellates in the 80-ies (mixo/heterothrophs) building between 60-80% of the biomass in spring), a partly regained dominance of diatoms in the late 90-ies- early 2000s to an increased share of chrysophytes and microflagellates (about 20 %) during 2001-2007 (Fig. 5.2). Thus, the Bacillariophyceae to Dinophyceae taxonomic biomass ratio in spring diverged from the reference ratio (Petrova-Karadjova ,1984) of (10:1).?

In winter, albeit the predominance of typical diatoms (Skeletonema costatum, Detonula confervaceae, Pseudonitzschia seriata, Pseudonitzschia delicatissima) by about 80%, species from other taxonomic groups (chrysophytes, microflagellates and mixothrophic dinoflagellates) often contributed to more than 50% of the total density and the large size dinoflagellates in the biomass (Fig. 5.2). In February 2005 the dinoflagellate Alexandrium ostenfeldii dominated the community (90%) in the Bay of Sozopol (Mavrodieva et al., 2007), and, Akashiwo sanguinea proliferated along the entire coastal area in February 2001, while Apedinella spinifera was a co-dominant species during the winter bloom of Skeletonema costatum in March 2003. The contribution of chrysophytes (Emiliania huxlei) in spring-summer 2003 oscillated between 40-80% of the total abundance, microflagellates between 20-50%. Dominance of Cyanophyceae and Chrysophytes marked atypical composition of phytoplankton community in autumn, along with the blooms of dinoflagellates (Gymnodinium sp., Prorocentrum minimum, Alexandrium monilatum) with biomass exceeding 15 g/m3 in Cape Kaliakra and Cape Galata in November 2003 that resembles the eutrophication period, irrespective of the reduction of the total abundance as compared to the 1990s.

The species composition of algal blooms tended to have significant decadal changes in the Romanian shelf as well. The late 1980s were characterized by relatively low (<30%) diatom content but dominated mainly (about 60%) by dinoflagellates (Fig. 5.2b; upper). This structure reversed in favour of diatoms by the early 1990s. Between 2001 and 2005, diatoms covered 48-66% of the total algal density except 2002-2003 in which two Cyanophyceae species Microcystis pulverea and M. aeruginosa dominated the blooms during the warm season. In the biomass, the dinoflagellates were more often dominant due to their large bio-volume, representing up to 65% of the whole biomass (Fig. 5.2b; lower).

Southern Black Sea: Compared to the NWS, 172 taxa were identified until 1995, of which 103 belonged to Bacillariophyceae, 52 to Dinophyceae, 12 to Chlorophyceae, 3 to Cyanophyceae and 2 to Chrysophyceae. The studies conducted between 1995-2000 introduced 115 additional taxa - 1? from Cyanophyceae, 65 from Dinophyceae, 4 from Dictyochophyceae, 33 from Bacillariophyceae, 10 from Prymnesiophyceae, as well as 1 species of Euglenophyceae and 1 species of Acantharea. Only 6 taxa of Bacillariophyceae have been given as a new record for the Turkish coast after 2000. In total, 294 phytoplankton species consisting of 48.3% diatoms and 39.8 % dinoflagellates were identified in the Southern Black Sea so far (Table 5.3). The most important change observed within the last 10 years was the slight domination of dinoflagellates and other micro-nanoplankton species with respect to diatoms. The increase in the ratio of dinoflagellates could be related to the change in nutrient balance in addition to the temperature regime of the seawater.

Table 5.3. Phytoplankton species distributed along the Turkish Coast of Black Sea.

Table 5.3. Phytoplankton species distributed along the Turkish Coast of Black Sea.

(1: Feyzioğlu, 1990. 2: Feyzioglu, 1996. 3: Türkoğlu, 1998. 4: Büyükhatipoğlu et al., 2002. 5: Bircan et al., 2005. 6: Şahin, 2005. 7: Baytut, 2005. 8: Bat et al., 2005. SW-BS: South Western Black Sea. S-BS: Southern Black Sea)

Georgia shelf region: According to the data from the 1970s, 99 phytoplankton species were registered in the south-eastern part of the Black Sea: 116 phytoplankton species were identified in 1982-1987, and 155 species in the 1990s. The present species composition included 203 species and subspecies of Bacillariophyceae, Dinophyceae, Chlorophyceae, Cyanophyceae, Chrysophyceae, Euglenophyceae. Species diversity and total biomass was built mainly by? representatives of 2 large groups: Bacillariophyceae (diatoms) and Dinophyceae ( dinoflagellates). Most dominant diatom species included Skeletonema costatum, Chaetoceros socialis, Ch.curvisetus Ch.affinis Cyclotella caspia, whereas the dominant dinoflagellates were Prorocentrum cordatum, Pr. micans, Prorocentrum compressum, Protoperidinium pellucidum, P.steinii, Hetercocapsa triguetra, P.bipes, Cetarium fusus, C. furca. In some? years, high abundance of?? blue green, green and euglena algae such as Microcystis acruginosa, Anabaena flos-aquae, Ankistrodesmus falcatus, Scenedesmus acuminatus, Trachaelomonas volvocina var. punctata and Euglena viridis was documented Most of them were recorded in estuaries where water salinity was as low as 8-10psu, in ports and sewage discharge regions.

Northeastern Black Sea: According to 2001-2005 monitoring data, in the Caucasian coast of the Black Sea 100-160 phytoplankton species were listed that included mixotrophic and heterotrophic species and benthic diatoms: about 60 Bacillariophyceae species (including common benthic diatoms like Thalassionema nitzschioides), 78 dinophyceae species (including heterotrophs traditionally accounting within phytoplankton, e.g. Ceratium spp., Dinophysis spp., Diplopsalis spp., Protoperidinium spp., etc.), 4 species of Silicoflagellates, 1 Chrysophyceae? 5 Prymnesiophyceae, 1 Euglenophyceae, 1 Prasinophyceae, and 1 identified cyanobacterium. This number was close to the earlier data (119 species) from the same region based on one-year monitoring of microphytoplankton in Gelendjik coast (Zernova 1980).

Interior Black Sea: Long-term dynamics of phytoplankton communities in the interior basin has been studied using the phytoplankton data base, for the period from 1968 to 2007 (Mikaelyan, 2008). Stations are located in the Northern part of the Black Sea deeper than 150 m, mainly in its Northeastern area. Because of strong cross-shelf water exchanges, the key phytoplankton species in the shelf and deeper areas are usually the same and thus the data from stations shallower than 150 m were excluded from the analysis. Total number of stations and samples exceded? 1000 and 2600, respectively

Long-term changes of 5 taxonomic groups were analyzed: Dinoflagellates, Diatoms, Coccolithophorids, Silicoflagellates and Flagellates for the upper mixed layer and lower part of the euphotic zone. Annual changes were studied for 4 time periods: spring (March-April), early summer (May-June), summer (July-September) and autumn (October-November). Due to the lack of data, winter season was not taken into consideration

The most striking feature of the spring season is a decreasing trend of diatoms abundance from 60-80% of the total phytoplankton biomass in 1970-1990 to 15-25% after 1995 (Fig. 5.3). They were replaced by dinoflagellates and phytoflagellates. The early summer season (May-June) was characterized by an increase of coccolithophorids abundance from 5-15% before the mid-1980s to 20 in the 1980s and 50% after 1994 until the present. On the contrary, dinoflagellate standing stock decreased from 60-80% to 15-25% during the same period. The role of diatoms increased from 1% to 60% in the upper mixed layer in summer season of the last two decades. The same trend was not so evident for the pycnocline layer where the most noticeable change was the reduction of silicoflagellate abundance. It comprised from 10 to 90% of the total phytoplankton biomass in 1969 and only from 0 to 5% after 1970?s. For the autumn season, the role of dinoflagellates in phytoplankton biomass decreased from 60-90% to 10-40% in the upper mixed layer. An opposite trend was recorded for flagellates. Their input to the total phytoplankton biomass increased from 0-5% to 20-70%. Thus, phytoplankton species community was dominated by dinoflagellates in spring and early summer and diatoms in summer and autumn after 1994. Phytoflagellates also became a dominant component of the community with contribution more than 20% throughout the year. Coccolithophorids also became a predominant part of the community during May-June as also supported by the ocean color data (Cokacar et al., 2003).

The most remarkable changes occurred during the seasonal plankton successions in the cold climate period 1985-1994. The predominance of diatoms in spring shifted to the prevalence of dinoflagellates and phytoflagellates. Substantial increase of coccolithophorids was reported in spring-summer instead of dinoflagellates. Dinoflagellates replaced by diatoms in summer and silicoflagellates by phytoflagellates in autumn. Thus, the classical seasonal phytoplankton succession with the spring diatoms bloom followed by proliferation of dinoflagellates and then phytoplagellates was not observed any longer. They all indicated a ?regime shift? in phytoplankton community structure during the early 1990?s. This mode still prevails and the phytoplankton community structure of the deep Black Sea has not yet return to the state observed during the 1960-70s.

5.3. Long-term changes in algal blooms

Northwestern Black Sea shelf: For the 1973 ? 2005 period, 158 bloom cases were registered by 50 species and varieties of algae (see Table 5.4 in Appendix) including 25 species of diatoms, 7 of dinophytes, 11 of blue-green, 4 of green, 2 of crysophytes algae and 1 of Euglenophyceae. 53 bloom events were registered in 1973 ? 1980 over more than half of the northwestern Black Sea area (Nesterova, 2001). The most remarkable outbursts were caused by Prorocentrum cordatum, which initiated ?a red tide? at the sea surface in September 1973, (Nesterova, 1979) after a similar event that occurred? in Sevastopol Bay in 1909 (Zernov, 1913). Also ?blooming? of Cerataulina pelagica and Emiliania huxleyi was first noted in 1973-1980 (Nesterova, 2001).

From 1980 to 1990, the number of phytoplankton blooms decreased to 33. However, outbursts of rare species such as (Leptocylindrus minimus), and of new species (Microcystis pulverea, Gleocapsa minima, etc.) increased in number. Most frequent "blooms" were caused by Skeletonema costatum, Cerataulina pelagica, Prorocentrum cordatum, Chaetoceros socialis. In 2001, outbursts of dinophytes ? Gymnodinium simplex, G. sphaeroideum, Scrippsiella trochoidea and Akashiwo sanguinea were also recorded.

Massive algal outbursts were rarely observed along the Crimean coast, and their maximum abundance was always lower than in the NWS (Mashtakova and Roukhiyainen, 1979; Senichkina, 1993). For instance, Skeletonema costatum abundance along the Crimean coast reached 0.9 millon per liter (Senichkina, 1993), while it was 30.6 millon per liter in the NWS (Nesterova, 2001).

The highest values of phytoplankton biomass in the NWS were observed in 1973 ? 1980 (Fig. 5.4) and attributed to the heavy eutrophication (Nesterova, 1987). The average phytoplankton biomass increased almost 17 times -? from 0.9 g m -3 to 16.0 g m -3? as compared to the 1950-1960s (Nesterova, 1987). From 1981 to 1993 the phytoplankton biomass started to decrease gradually with a minimum biomass registered in 1991-1993. In 1994 ? 2000, the biomass was around 6.0 g m -3 and the contribution of dinophyte algae tended to decrease in contrast to more intense development of diatoms (Derezyuk et al., 2001). The proliferation of Skeletonema costatum was more intensive as an indicator of hypereutrophic waters (Nesterova, 2003). The decrease in phytoplankton biomass to around 4.0 g m-3 in 2001-2005 was accompanied by an increased role of dinophytes. In 2005, a ?red tide? dominated by Scrippsiella trochoidea and blue-green algae was documented near the Odessa coast.

Phytoplankton data for the period 1988 ? 2004 from the estuarine part of the Danube ? the main source of Black Sea eutrophication (Zaisev at al., 1989) have been analyzed for three different periods (Nesterova, 1998; Nesterova, Ivanov, 2001; Nesterova, 2005). The phytoplankton abundance did not change much during these periods and was on the average 3.6 million cells∙l-1 (Fig. 5.5a). More recent data for 2003-2008, on the other hand, show large interannual variability in the range of 0.5-15 million cells∙l-1 (Fig. 5.5b). The biomass gradually decreased from 38.0 g m -3 in the 1980s to ~5.0 g m -3 in 2000-2004, mostly due to the reduction in dinophytes (Heterocapsa triquetra) in spring and increase in diatoms (small-size species, such as Skeletonema costatum, Chaetoceros socialis). The latter average value included extreme cases such as 14.5 g m -3 in 2003 and 2 g m -3 in 2004. The biomass manifested an increasing trend after 2004 up to 8 g m -3 in 2008.? A similar decrease in phytoplankton biomass from the 1980s to the 1990s and enhanced growth of Skeletonema costatum was also observed in the Odessa area (Nesterova and Terenko, 2000) where the number of blooming species changed irregularly year-to-year (Fig. 5.5c).

Near southeastern coast of Crimea the abundance and biomass of phytoplankton have also increased in the past 50 years. Small size species of diatoms (Skeletonema costatum) and coccolithophorids (Emiliania huxleyi) dominated phytoplankton blooms (Kuzmenko at al., 2001). Dominance of coccolithophorids in the summer-autumn period was particularly prominent in the coastal zone near Sevastopol in 2001-2003 (Polikarpov at al., 2003).

To summarize, the phytoplankton structure and dynamics in the NWS have been altered not uniformly in the different areas of the shelf during the past 50 years. The phytoplankton species diversity increased and this increase was accompanied by changes in the ratio of diatoms and dinophyte algae in favour of dinophytes and declining contribution of diatoms during the 1970-1980s. In the Sevastopol area and the southeastern coast of Crimea, the species diversity of coccolithophorids increased. A reverse trend was observed after 2000 characterized by elevated diatom contribution and reduction of dinophyte abundance along with a decrease in the total phytoplankton biomass that imply a decline of? eutrophication impact and a partial recovery of the northwestern shelf ecosystem (Nesterova, 2003).

Romanian shelf area:The phytoplankton density and biomass followed the general tendency of decrease in the Romanian Black Sea waters after the 1980?s as well. Both abundance and biomass in coastal waters near Constanta underwent a significant reduction during 2001-2005 that accounted for 75% and 55% decrease relative to the 1980?s (Table 5.5 and Fig. 5.6) and approaching to values comparable to the 1960s. Algal bloom frequency and concentration declined: out of 24 blooms, only three exceeded 50 million cells/l whereas this number was 15 in the 1980s and 4 in the 1990s (Table 5.5). Besides, diminished number and intensity of algal blooms, the number of blooming species reaching density higher than 10 million cells/l was reduced from 11 in the 1990s to 9 in 2001-2005 (Fig. 5.7). Cyclotella caspia (maximum 78.6 ?106 cells/l),? dinoflagellates Prorocentrum cordatum (15.3?106 cells/l), Scrippsiella trochoidea (25.2?106 cells/l) and Heterocapsa triquetra (16.0 ?106 cells/l), cyanophytes Microcystis pulverea (16.7 ?106 cells/l), M. aeruginosa (15.0 ?106 cells/l) and M. orae (271.9 ?106 cells/l), diatoms Tabellaria sp. (maximum 17.1 ?106 cells/l) and Navicula sp. (maximum 67.5?106 cells/l) produced the most significant blooms. The last five species were alochtonous fresh-brackish water species introduced into the sea mainly by the River Danube, the blooms occurring in regions of relatively low salinity and warm water. The relatively large phytoplankton biomass in 2007 (Fig. 5.6) was due to large-size dinoflagellate bloom, but the abundance was low (Fig.5.6).?

Table 5.5. Mean phytoplankton density and biomass in the shallow waters in front of Constanta and number of blooms registered in Romanian marine waters during different periods.

Period

Density
(106 cell/l)

Biomass
(g/m3)

Number of
blooms

Number of
Blooms, density > 50·106 cell/l

1959-1965

0.887

2.00

   

1983-1990

5.870

7.14

49

15

1991-2000

2.261

5.960

29

4

2001-2005*

1.481

3.22

24

3

         

* Mean minus extreme values/atipique from August and September, 2000 and 2001.

Bulgarian shelf area: The 1980?s and the early 1990s were characterized by most intense blooms and a shift to r-strategy species (Moncheva, Krastev, 1997). A total of 31 monospecific blooms occurred, out of which seven attained densities higher than 50 mil cells.l-1 and the biomass varied between 10 and 20 g m-3. Starting by the mid-1990s, an overall decreasing trend in the density and biomass of all dominant species was observed down? to a total biomass of about 3 g m-3 after 2000 (Fig. 5.9). Along with the reduction of frequency, duration, and intensity of phytoplankton outbursts (only 3 cases of abundance exceeding 50 mil ?cells.l-1 reported in the late 1990s and?? none in the period after 2000), a decline in the extent and duration of exceptional events, especially in summer was documented. The list of bloom producing species was further diversified and several species contributed to a single bloom event (Moncheva et al., 1995, Velikova et al. 1999, Moncheva et al., 2001) ? Fig.5.7a.

After 2000, a number of controversial trends were evident in summer, such as proliferation of large diatoms (Pseudosolenia calcar avis and Cerataulina pelagica) at the level of red-tide biomass (higher than 20 g/m3 in August 2002), elevated occurrence of small heterothrophic microflagellates and large dinoflagellates (Akashiwo sanguinea and species from genus Ceratium), and almost recurrent blooms of Emiliania huxleyi (Moncheva et al., 2006). The presence of species from genus Dinophysis (D. acuta ? 4.4 x103 and D. caudata - 1.7 x103 ? Petrova and Velikova, 2003) and Pseudonitzschia cited as toxic for other areas of the world ocean all together signify perturbed phytoplankton succession and ecosystem instability.

The summer frequency distribution of EQ classes during the period 1990-2000 and 2000-2007 based on chlorophyll-a and phytoplankton biomass (Moncheva and Slabakova, 2007) revealed a reduction of ?poor/bad? conditions from more than 70% to less than 40% in the Varna Bay and to none at station 201 near Cape Kaliakra, and to about 40% at station 301, near Cape Galata (Fig. 5.10), indicating an improvement in the environment of the region. Nonetheless the "good" class frequency maintained below 50% in Varna Bay implies a continuation of eutrophic conditions of ecological concern.

Southern Black Sea: The analysis of the data collected along the Turkish coast during two different hydrological phases: stagnant period (where significant nutrient injection is possible due to deeper mixed layer in cold seasons) and non-stagnant period (shallower mixed layer; warm seasons) suggested a common trend of lower phytoplankton abundance after 1994 (Fig. 5.11), most likely related to improvement of eutrophic conditions in the southern Black Sea coastal waters. Relatively high abundance in the stagnant periods reflected mainly the contribution of the spring blooms.

Georgia shelf region: Since 1981, phytoplankton was sampled along 8-12 transects at standard depths (0, 5, 10, 25, 50, 75, 100m) and 68-70 stations along the Georgian coast from Chorokhi River up to Bzibi River. The average annual abundance and biomass during 1992, 1998, 1999 and 2005 (Fig. 5.12) indicated a rather uniform level during the 1990s (around 100-150x103 cell l-1 and 2.5 g m-3) in coastal waters between Poti and Batumi. The exceptionally high density and biomass of phytoplankton (788 x103 cell l-1 and 11.7 g m-3) were recorded in both regions during 2005 that were associated with proliferation of large Bacillariophyceae species Coscinodiscus granii, Hyalodiscus ambiguus, Pseudosolenia calcar avis, Dactyliosolen fragilissimus, Prorocentrum micans.

Interior Black Sea: Phytoplankton biomass as an average of all measurements conducted within the interior basin at stations deeper than 150 m also indicate distinct decadal changes (Fig. 5. 13). The biomass which was only about 2 g m-2 during the 1960s increased up to 10 g m-2 after the mid-1970s and then to about 20 g m-2 in the 1980s and the early 1990s, exceeding even 50 g m-2 in 1985 and 1992. By the mid-1990s, phytoplankton biomass oscillated annually between 5 g m-2 and 20 g m-2 and therefore is still comparable with the conditions of eutrophication phase.

As the spring-summer phytoplankton productivity is mainly driven by the amount of nutrients entrained into the euphotic zone by winter convection, it is expected that phytoplankton biomass should be proportional to severity of winters that is indicated in Fig. 5.13 by the winter-average SST and mean temperature of the Cold Intermediate Layer (CIL) during May-October. As shown in Fig. 5.13, phytoplankton biomass follows closely temperature variations with higher (lower) biomass during cold (warm) years. This close relation implies that a part of the biomass increase in the 1980s was imposed by climate impact, in addition to eutrophication. The recent increase in biomass after 2002 may also be attributed to the climate as there is no evidence of increase in eutrophication within the interior basin during the recent years.

5.3. Seasonal dynamics

The averaged data for the NWS during 1975-2005 suggest three particular peaks in the annual dynamics of phytoplankton biomass. The first one occurred in April, usually dominated by diatoms (Skeletonema costatum, species of the genera Thalassiosira), the second- in June-July dominated by dinoflagellates (Prorocentrum cordatum) making up 84.6 % of the total biomass, and the third and highest one in September-October due to diatoms (Cerataulina pelagica, Pseudonitzschia seriata, Ps. delicatissima, Leptocylindrus danicus) and dinophyte (Prorocentrum cordatum, Goniaulax polyedra), which contributed to biomass irregularly (Fig. 5.14). During diatoms outbursts, they build up about 70% of the biomass while dinophyte contribution decreased to 22%. Because of their small cell-size coccolithophorids contributed to only 8% of the biomass.? The most important feature was an almost one order of magnitude increase of the monthly phytoplankton biomass during 1973-2005 as compared to 1954-1974 - Fig. 5.14

During the summer outbursts the bulk of phytoplankton biomass was concentrated in the upper 0-10 m, except in shallow waters. The difference in the abundance between the surface and near bottom layers increased from spring to summer, decreasing in the autumn. The highest abundance and biomass were observed in the Danube River runoff impacted zone of the NWS, with frequent and intensive blooms, while the abundance and biomass declined sharply by several orders of magnitude beyond this zone. During spring and autumn intense diatoms outbursts were registered locally near river estuaries. In summer during permanent blooms, large areas of high phytoplankton biomass were covered between the estuaries of the Dnieper?Bug Liman and the Danube.

In the Bulgarian shelf area, during the cold years of the 1980s as well as in 1994, the annual phytoplankton biomass manifested pronounced late-winter and spring peaks, often exceeding 10 g m-3 - to more than 30 g m-3 as observed in the 1990 spring (Fig. 5.15). The biomass decreased considerably since 1995 down to less than 5 g m-3 after 2000, associated with the onset of a decade-long climatic warming phase along with the reduction of nutrients and the shift in their ratios (Moncheva et al, 2008). Contrary to the cold climate phase, there was no clear seasonal pattern, and the timing of phytoplankton intensive growth varied irregularly.

In the northeastern shelf, the phytoplankton growth started in February by proliferation of small diatoms, usually Pseudo-nitzschia pseudodelicatissima most frequently co-dominated by Skeletonema costatum, Dactyliosolen fragilissimus, Cerataulina pelagica, Hemiaulus hauckii, and Chaetoceros spp. and nanoplankton flagellates. In 2004, Thalassiosira spp. alone reached a density of 100 000 cell l-1. The spring peak of phytoplankton diversity and abundance occurred?? in April. At this time, large diatoms (e.g. Pseudosolenia calcar avis, Proboscia alata) and heterotrophic dinoflagellates dominate in the community biomass. The diversity and abundance decreased in May-June, with the exception of cases of massive proliferation of coccolithophores or a re-intensified growth of P.pseudodelicatissima and/or Thalassiosira spp., populations.

The beginning of most intensive and longest period of phytoplankton growth and maximum diversity was in July, culminating in early August, parallel to the annual maximum of surface water temperature. The phytoplankton abundance is dominated by dinoflagelates. Monospecific blooms may also occur like Cochlodinium polykrikoides bloom at Bolshoy Utrish (Krasnodar Krai) in 2001 (Vershinin et al., 2005). September-October was a time of gradual decline of phytoplankton community: total cell density and biomass decreased, and the portion of dinoflagellate species also. The intensity and duration of this annual phytoplankton succession at Caucasian coast varied from year to year, but the general pattern was maintained.

The succession cycle in the northeastern Black Sea coastal waters starts typically with the outburst of a single species of high growth rate, or less frequent, several of several species - small diatoms and/or coccolithophores. Then, they are replaced by heterotrophic dinoflagellates at temperatures higher than ~15oC. The data suggested that biotic factors (life cycle, growth rate and grazing, etc.) drive the start and evolution of each succession cycle, whereas the initiation, intensity and duration are determined mostly by water temperature.

5.4. Conclusions and recommendations

The overall analysis provided rather contrasting trends of phytoplankton assembly during the present decade. On the one hand, the increased species diversity and richness, reduced frequency and magnitude of phytoplankton blooms and thus decrease of total biomass and abundance, reduced frequency of ?bad/poor? EQ classes all point to an improvement of the ecological state of the Black Sea. On the other hand, concomitantly with still high nutrient concentrations, the increased dominance of heterotrophic dinoflagellates and elevation of abundance and biomass of ?other? species (e.g. coccolithophores and phytoflagellates) reflect features of a perturbed transitional state and an ongoing ecological instability. The seasonal species succession manifested irregular pattern and varied regionally and from year to year. A notable character of the annual phytoplankton structure is the substantial increase of coccolithophorids in May-June all over the basin.

Due to the high sensitivity of phytoplankton communities to external forcing as well as highly dynamic internal structure of the ecosystem, the frequency of sampling is critical for setting an adequate monitoring system for phytoplankton related indicators. Occasional high phytoplankton blooms observed during the present decade in many coastal waters requires a systematic monitoring. Monthly sampling is strongly recommended, while sampling during spring and summer is an imperative. Remote sensing ocean color data with an improved algorithm for coastal waters are crucial especially in spring-summer for capturing the spatial features of bloom events.


Appendix

Table 5.4. Abundance (cells/l) and biomass (mg/m3) of dominant and blooming phytoplankton species along the Bulgarian shelf in different periods.

1954-1970

2000-2005

1980-2000

Taxa

[106 cells/l]

B [g/m3]

Taxa

[106 cells/l

B [g/m3]

[106 cells/l

Winter Bacillariophyceae

Skeletonema costatum

4.2 -5.7

Skeletonema costatum

2.3- 6.4 -3.9-15.0

43.47

Detonula confervaceae

2.4 -4.4-7.3

Detonula confervaceae

4.4

Pseudonitzschia seriata

2.6-4.3

Pseudonitzschia seriata

3.1

Cerataulina pelagica

9.8

Pseudonitzschia delicatissima

Chaetoceros similis

Chaetoceros similis

0.9

7.7

Chaetoceros curvisetus

Ditylum brightwellii

Chaetoceros affinis

Dinophyceae

Glenodinium sp.

Gyrodinium lachryma

1.06

Ceratium fusus

Cyst Alexandrium

0.6

Prorocentrum cordatum

Heterocapsa triquetra

0.8

24

Prorocentrum micans

Protoperidinium divergens

0.97

Protoperidinium grannii

Ceratium furca, C. ?fusus

Akashiwo sanguinea

Microflagellates

 

Microflagellates

1954-1970

2000-2005

1980-2000

Taxa

[106 cells/l]

B [g/m3]

Taxa

[106 cells/l

B [g/m3]

[106 cells/l

Chrysophyceae

Apedinella spinifera

 1.7

Coccolithus sp.

Spring Bacillariophyceae

Cerataulina pelagica

22.9

Cerataulina pelagica

3.7

6.3

Chaetoceros curvisaetus

5.2

Chaetoceros socialis

11.8

3.5

Pseudonitzschia delicatissima

1.3

Pseudonitzschia delicatissima

3.1

Skeletonema costatum

10

Skeletonema costatum

35.8

Cyclotella caspia

Cyclotella caspia

2.3

9.9

Thalassionema nitszchioides

Chaetoceros similis

0.9

Detonula confervaceae

 Shroderella delicatula

4.8 

Pseudosolenia calcar-avis

3.6

Dinophyceae

Prorocentrum micans

Prorocentrum cordatum

3.7

3.1

30.5-96.8

Ceratium fusus

Heterocapsa triquetra

1.7-3.7

14.3

7.7-39.5

Protoperidinium crassipess

Scrippsiella trochoidea

1.8

Peridinium divergens

Ceratium fusus

4.3

Dinophysis acuta

0.66

Akashiwo sanguinea

12.24

Ceratium tripos

Chrysophyceae

Emiliania huxleyi

3.88-4.33- 4.7

3.2

Microflagellates

Microflagellates

1.1-33.0

42.8

1954-1970

2000-2005

1980-2000

Taxa

[106 cells/l]

B [g/m3]

Taxa

[106 cells/l

B [g/m3]

[106 cells/l

Summer Bacillariophyceae

Cerataulina pelagica

Cerataulina pelagica

1.8-6.4

11.3-15.3-12.0-2.5

6.8

Pseudonitzschia delicatissima

Pseudonitzschia delicatissima

1.4

Pseudosolenia calcar-avis

Pseudosolenia calcar-avis

23

1.8

Cyclotella caspia

 0.6-2.1

Cyclotella caspia

1.1

Thalassionema? nitzschioidea

Thalassionema? nitzschioidea

2.8

 Dactyliosolen fragilissimum

0.42

5.7-8.4

Nitszchia longissima

3.2-5.9

 Nitschia tenuirostris

20

Chaetoceros affinis

Chaetoceros socialis

2.7

35.5

Dinophyceae

Prorocentrum cordatum

 5.4

Prorocentrum cordatum

1.1

2.6-1.9

480

Prorocentrum micans

Heterocapsa triquetra

Ceratium fusus

Scrippsiella trochoidea

Prorocentrum micans

0.7

Peridinium crassipess

Dinophysis caudata 

Ceratium fusus

Ceratium furca

1.1

1954-1970

2000-2005

1980-2000

Taxa

[106 cells/l]

B [g/m3]

Taxa

[106 cells/l

B [g/m3]

[106 cells/l

 Gyrodinium spirale

Dinophysis acuta

Akashiwo sanguinea

12.24

Ceratium tripos

Chrysophyceae

Emiliania huxleyi

1.7-1.8-2.3-3.1

52.9

Phaeocystis pouchettii

4.4

90

Cryptophyceae

Ochromonas sp.

1.5

0.7-1.6

Microflagellates

Microflagellates

1.7

Euglenophyceae

Eutreptia lanowii

4.6

1954-1970

2000-2005

1980-2000

Taxa

[106 cells/l]

B [g/m3]

Taxa

[106 cells/l

B [g/m3]

[106 cells/l

Autumn Bacillariophyceae

Sceletonema costatum

1.6

Skeletonema costatum

1.31-2.2-2.4

57.2

Pseudosolenia delicatissima

5.7

 14.8

Pseudosolenia delicatissima

4.2

Dytilum Brightwellii

Pseudosolenia calcar-avis

Cerataulina pelagica

7.3

Pseudonitzschia seriata

2.6

Dinophyceae

Prorocentrum micans

Alexandrium monilatum

15.8

Dinophysis caudate

Dinophysis sacculus

Gymnodinium sp.

2.34

Prorocentrum cordatum

0.4

Prorocentrum cordatum

1.02-3.48

60

Goniaulax spinifera

2.9

Prorocentrum micans

Ceratium furca

2.9

1.2

Chrysophyceae

Emiliania huxleyi

2.11-4.08

4.2

Microflagellates

Table 5.5. Maximum abundance (million cells/l) of species that caused phytoplankton blooms in the northwestern Black Sea in the 1954-1960s and in 1973-2005.

Species

1954?1960s*

1973-2005

Bacillariophyceae

Melosira granulata (Her.) Ralfs

1.8

2.9

Skeletonema costatum (Grev.) Cl.

32.0

30.6

Sk. potamos (Weber) Hasle

8.4***

Sk. subsalsum (A.Cl.) Bethge

-

8.5

Thalassiosira parva и Th. subsalina Pr.-Lavr.

2.7

54.0

Cyclotella caspia Grun.

5.2

6.2

C. glomerata Bachm.

22.5***

Stephanodiscus hantzschii Grun

-

20.8

St. socialis Makar. Et Pr.-Lavr

-

4.9**

Leptocylindrus minimus Grun.

-

16.0

L. danicus Cl.

72.0

28.0

Dactyliosolen ?fragilissimus (Bergon) Hasle.

0.1

12.2**

Chaetoceros affinis Laud.

-

1.9

Ch. Insignis Pr.-Lavr.

-

1.7

Ch. karianus Grun.

-

4.0

Ch. socialis Laud.

5.4

16.7

Ch. rigidus Ostf.

-

14.0**

Cerataulina pelagica (Cl.) Perag.

0.6

37.0

Diatoma elongatum (Lyngb.) Ag.

0.7

6.7

Synedra actinastroides Lemm.

-

1.9

Asterionella formosa Hass.

-

2.3

Nitzschia tenuirostris Mer.

-

28.6

Cylindrotheca closterium (Ehr.) W.Sm.

-

16.0

Pseudo-nitzschia seriata (Cl.) H. Perag.

-

12.4

Surirella ovata var.salina (W.Sm.) Hust.

-

10.7

Dinophyceae

Prorocentrum cordatum (Ostf.) Dodge

4.3

224.0

Pr. micans Her.

-

15.4**

Gymnodinium sphaeroideum Kof.?

-

4.0

G.simplex (Lohmann) Kof. et Sw.

-

251.1

Akashiwo sanguinea (Hirasaka) G. Hans. et Moestr.

-

140.0

Heterocapsa triquetra (Her.) Stein.

-

18.0

Scrippsiella trochoidea (Stein) Balech ex Loeblich III

-

125.4

Cyanophyceae

Microcystis aeruginosa Kutz.

4.3

15.0

M. pulverea (Wood) Elenk. F. pulverea

-

94.8

Gleocapsa minor (Kutz.) Hollerb. Ampl.

-

2.6

G. minima (Keissl.) Hollerb.

-

4.4

Merismopedia glauca (Her.) Nag.

-

1.0

M. minima (Keissl.) Hollerb.

-

22.0

M. punctata Meyer

-

8.1

M. tenuissima Lemm.

44.8

8.2

Anabaena spiroides Kleb.

2.5

6.3

Aphanizomenon flos-aquae (L.) Ralfs

0.9

34.0

Oscillatoria kisselevi Anissim.

-

147.0

Chlorophyceae

Monoraphidium arcuatus Korsch.

-

1.9

Scenedesmus obliquus (Turp.) Kutz.

-

8.6

Sc. quadricauda (Turp.) Breb. Var. Quadricauda

1,4***

Micractinium pusillum Fr.

-

6.6

Chrysophyceae

Emiliania huxleyi (Lohm.) Hay & Mohler

-

9.0

Dinobryon sp.

-

4.0

Euglenophyceae

Eutreptia lanovii Steuer

-

1.7

* Ivanov (1967); ** ? Terenko, Terenko (2000); -*** Nesterova, Terenko, 2007

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