Populations of the red tide forming dinoflagellate Noctiluca scintillans (Macartney): A comparison between the Black Sea and the northern Adriatic Sea

Harmful Algae 33 (2014) 29–40

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Populations of the red tide forming dinoflagellate Noctiluca scintillans (Macartney): A comparison between the Black Sea and the northern Adriatic Sea Alexander S. Mikaelyan a,*, Alenka Malej b, Tamara A. Shiganova a, Valentina Turk b, Anastasia E. Sivkovitch a, Eteri I. Musaeva a, Tjasˇa Kogovsˇek b, Taisia A. Lukasheva c a

Institute of Oceanology RAS, Nakhimovsky prosp., 36, Moscow 117997, Russia National Institute of Biology, Marine Biological Station Piran, Fornace 41, 6330 Piran, Slovenia c Southern Branch of P.P.Shirshov Institute of Oceanology RAS, Prospornaya str. 1, Gelendzhik 353470, Russia b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 11 July 2013 Received in revised form 3 December 2013 Accepted 27 January 2014

Populations of Noctiluca scintillans (hereafter Noctiluca) were compared from two regions: the northeastern-central Black Sea and the northern Adriatic Sea. In both seas samples were collected in near-shore waters 2–3 times per month during 2004–2012. For analysis of feeding activities and seasonal dynamics additional cruise data on the open waters of the Black Sea were used. Comparison between the two populations shows similarity in size structure with two classes 401–500 mm and 501– 600 mm being the most numerous. Seasonal changes in cell abundance in both seas demonstrated a regular annual maximum with the peak period of high abundances in May–June with additional sporadic peaks in other seasons. In spring the average number of food vacuoles in the cell (1.78) and the proportion of feeding cells in populations (79%) in the Adriatic Sea were similar to those in the Black Sea (1.58 and 76%). In September–October, these parameters were lower both in the Adriatic Sea (0.69 and 49%) and in the Black Sea (1.46 and 65%) demonstrating that Noctiluca was better provided with food in spring. Among biotic parameters (wet phytoplankton biomass, chlorophyll biomass and zooplankton species) only the concentration of the eggs of Calanus euxinus was significantly positively correlated with abundance of Noctiluca. The possible effect of a high concentration of copepod eggs on the growth of Noctiluca in the peak period is discussed. An obvious negative relationship was observed between Noctiluca cell numbers in the peak period and wind velocity in both seas. The most significant negative correlation was observed between the number of windy hours per month (velocity more than 5–6 m s1) and cell concentrations in the Black Sea (r = 0.92) and in the northern Adriatic Sea (r = 0.67). On this basis, a new hypothesis has been proposed and discussed: in connection with features of the food behavior of Noctiluca, its outbursts during the peak period are controlled by the wind. An evident positive relationship was observed between the number of Noctiluca in the peak period and its quantity in the preceding months in both seas. Thus, we suggest that abundance data during early spring and weather forecasts (winds) may be used for medium-term prediction of Noctiluca outbursts and red tides. ß 2014 Elsevier B.V. All rights reserved.

Keywords: Black Sea Inter-annual changes Noctiluca scintillans Northern Adriatic Seasonal dynamics Wind

1. Introduction Noctiluca scintillans (Macartney) Kofoid & Swezy (=Noctiluca miliaris Suriray), hereafter referred to as Noctiluca, is a harmful heterotrophic and omnivorous dinoflagellate which is common in plankton communities worldwide (Harrison et al., 2011). It is widespread both in the open-shelf and in coastal waters where it

* Corresponding author. Tel.: +7 499 124 59 74; fax: +7 499 124 59 83. E-mail address: [email protected] (A.S. Mikaelyan). 1568-9883/$ – see front matter ß 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.hal.2014.01.004

frequently forms red tides. Noctiluca is one of the most eurythermal organisms among plankton species. It produces mass outburst events in cold waters at a sea surface temperature (SST) of 10 8C and in warm shelf waters at SST over 29 8C (Fonda-Umani et al., 2004; Mohanty et al., 2007). Temperature preferences of Noctiluca are so variable in different regions that the existence of multiple temperature strains is possible (Harrison et al., 2011). Field observations and experimental studies have shown a broad range of food items ingested by Noctiluca: phytoplankton, detritus, bacteria, protozoa, copepod eggs, fecal pellets, nauplii and even small Noctiluca cells (Mironov, 1954; Daan, 1987; Greze,

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1979; Kirchner et al., 1996; Petranu, 1997; Nakamura, 1998a; Nikishina et al., 2011). Such a broad food spectrum permits this dinoflagellate to be flexible in nutrition strategy and produce mass development events including red tides in many areas of the World Ocean (Malej, 1983; Elbrachter and Qi, 1998; Dela-Cruz et al., 2002; Lirdwitayaprasit et al., 2006; Mohamed and Mesaad, 2007; Harrison et al., 2011). Probably, because of such peculiarities of feeding, an obvious dependence on phytoplankton biomass is not usually observed. Generally, outbursts of Noctiluca occur more often in eutrophic waters (Kiørboe and Titelman, 1998; Harrison et al., 2011). Many investigations of the spatial and temporal distribution of Noctiluca have been done in various geographical regions, particularly in those where it forms red tides. Although these studies provide some insights into reasons for variability in abundance, there are still uncertainties regarding environmental factors governing population dynamics (Kirchner et al., 1996). In the Japan Sea, a positive relationship was observed between abundance of this dinoflagellate and the biomass of diatoms and chlorophyll (Nakamura, 1998a). In the Sagami Bay (Japan), a relationship with wind direction and rainfall was detected (Miyaguchi et al., 2006). In the South China Sea, a positive relationship was noted with average water temperature while a negative relationship was found with Noctiluca abundance during the peak season and chlorophyll concentration (Huang and Qi, 1997). In the North Sea, the summer biomass of Noctiluca was positively correlated with winter SST (Heyen et al., 1998). Based on 50-years of observations in the northeast Atlantic region, no significant correlation was established between SST and cell abundance (Hinder et al., 2012). In turn, in the Bay of Bengal the relationship with water temperature was negative (Mohanty et al., 2007). In Port Blair Bay (Indian Ocean), abundance of Noctiluca positively depended on terrigenous and allochthonous input (Dharani et al., 2007). On the southeast coast of Australia, a positive correlation was observed between an increase of nutrient stock caused by uplifting of deep water with subsequent phytoplankton blooms and Noctiluca abundance (Dela-Cruz et al., 2002). In the Red Sea, the same correlation with nutrient concentration was negative (Mohamed and Mesaad, 2007). In the Black Sea, mass development of Noctiluca was mainly related to the temperature regime or low spring SST (Bitukov, 1969; Shiganova, 2009). In the northwestern region and Bulgarian shelf waters, relatively high biomass coincided with cold SST years and vice versa for the warm years (Oguz and Velikova, 2010). In shallow

waters of the northwestern part of the sea, high numbers of Noctiluca were observed simultaneously with the high biomass of diatoms and dinoflagellates (Porumb, 1989). In the open waters, chlorophyll concentration was negatively correlated with Noctiluca in September-October (Yuneva et al., 1999). In the northern Adriatic and in the Sea of Marmara, a negative relationship was observed between mesozooplankton as a potential competitor for food resources and Noctiluca (Fonda-Umani et al., 2004; Yilmaz et al., 2005). From many studies it is evident that abiotic and biotic parameters related to spatial and temporal fluctuations may vary in space and time and differ between regions. Meanwhile, the mechanisms controlling mass development of the population are not quite clear. The idea of the current research is to apply a comparative analysis of Noctiluca populations in two quite similar environments and to reveal the common factors driving the populations in both regions. Cell size structure, feeding features, seasonal and interannual changes were compared in the northeastern part of the Black Sea and the northern Adriatic Sea. We tested the hypothesis that fluctuations in the population of Noctiluca are associated with the same drivers, but operating on a regional scale. 2. Material and methods 2.1. Studied areas The northern Black Sea and the northern Adriatic basin are located approximately at the same latitudes (Fig. 1a). This governs the similar annual temperature regimes. SST varied from a winter low 6 8C to a summer maximum around 26 8C in the northern Adriatic (Malacˇicˇ et al., 2006) and in the Black Sea (with the exception of the northwestern shallow area) from 7 8C to 27 8C (Kazmin and Zatsepin, 2007; Phiotukh et al., 2011). The most remarkable dissimilarities between the regions are the bottom depths and salinity. The northern Adriatic with the Gulf of Trieste is a very shallow area with depths mostly less than 50 m increasing gradually toward the south. The northern part of the Black Sea has a narrow shelf with a width from 5 to 12 miles. Bottom depth gradually drops to 200–300 m and then abruptly falls to a deep basin with depths of 1500–2100 m. Due to the presence of numerous mesoscale hydrological eddies along the coast, intensive water exchange between the shelf and open waters takes place during the year (Zatsepin et al., 2003). As a

Fig. 1. Areas of observation in the Black Sea and in the northern Adriatic Sea. Rectangles show the location of two monitored sites. Dots show sampling coverage in the open waters of the northeastern part of the Black Sea.

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result, species composition in the open and in the shelf waters is very similar. Salinity varied from 33 to 37 in the northern Adriatic Sea, while in the northeastern Black Sea it changed in the upper mixed layer ca from 17 to 18 (Oguz et al., 2005). Both regions have been recognized as mesotrophic ecosystems. Annual primary production is estimated as 100–115 g C m2 year1 (Vedernikov and Demidov, 2002) in the Black Sea and as 42–53 g C m2 year 1 in the northern Adriatic Sea (Fonda-Umani et al., 1992). Despite different salinity and sea depths, species composition of phytoplankton and zooplankton are quite similar. Many of the key phytoplankton species like the diatoms Skeletonema costatum, Pseudo-nitzschia pseudodelicatissima, Cylindrotheca closterium, Chaetoceros spp., Proboscia alata and the dinoflagellates Scrippsiella trochoidea, Lingulodinium polyedrum, Neoceratium fusus, Neoceratium furca, Neoceratium tripos, Prorocentrum spp. etc. are common in both seas (Fonda-Umani et al., 1992; Mozeticˇ et al., 1998; Eker-Develi and Kideys, 2003; France and Mozeticˇ, 2006; Pautova et al., 2007). Nowadays the most prominent feature of the phytoplankton community in the Black Sea is the regular springsummer bloom of coccolithophorids which is not evident in the northern Adriatic (Mikaelyan et al., 2011; Aubry et al., 2012; Mozeticˇ et al., 2012). The similarity also holds true for key zooplankton species: Acartia clausi, Paracalanus parvus, Penilia avirostris, Sagitta spp., Podon sp., Oithona spp. and gelatinous predators such as Aurelia aurita s.l. (Kamburska and Fonda-Umani, 2006; Shiganova et al., 2009; Aubry et al., 2012; Malej et al., 2012). In both seas Noctiluca plays an important role in heterotrophic plankton periodically dominating zooplankton communities. In the northeastern and central parts of the Black Sea, it comprises up to 60% of the total zooplankton biomass during periods of mass development (Kovalev et al., 2001). In the northern Adriatic, Noctiluca produced blooms and caused red tide events when it totally predominated in zooplankton biomass (Malej, 1983; Fonda-Umani et al., 2004). 2.2. Sampling and processing In the Black Sea samples were collected in the near-shore waters of the Caucasian shelf in the Blue Bay in the vicinity of the town of Gelendzhik (44834.270 , 37858.680 ) from 2002 to 2012. Sampling was carried out from the pier (150 m offshore) every 10 days (Fig. 1b). Likewise, sampling at the coastal station near the town of Piran in the northern Adriatic took place from 2004 to 2012 (Fig. 1a). Sampling was performed bi-monthly at the station approximately 3 miles offshore (45832.90 , 13833.00 ). In the Black Sea, samples were also collected in deep waters along a standard inshore-offshore 50–100 mile transect and in the northern-eastern part of the Black Sea (Fig. 1b). The total number of stations visited from 1997 to 2012 in open waters with a sea bottom depth more than 50 m is equal to 447. At the nearshore stations in the Black Sea and the northern Adriatic Sea samples were collected by vertical tows from bottom to surface (7 and 20 m, respectively) using a plankton Juday and WP2 net (178 and 200-mm mesh size, 0.25 m2 opening). Black Sea open waters were sampled with a plankton Juday net (178-mm mesh size, 0.1 m2 opening) and tows were carried out either from the sea bottom or from a depth with density 16.2 kg m3 (the upper boundary of the H2S layer, which varies from ca 70 m to 180 m in open waters). At 6 stations in May–June and at 19 in August–September multiple net tows by layers were conducted. Vertical profiles consisted of 3 layers: the upper mixed layer (UML), pycnocline (PICN) and the layer below (LBP). Samples were preserved with 2% buffered formaldehyde and were processed during 2–3 months. All Noctiluca cells in samples were counted in Bogorov’s chamber under magnification x 70 except in cases of very high

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density when subsamples were counted. Cell size and number of food vacuoles in a cell were determined seasonally: in May, June, September, October in the open waters of the Black Sea and in April–October in the northern Adriatic Sea. Cell diameter was measured assuming the cell shape as a sphere. The number of food vacuoles was counted and their size measured under 70 magnification. Only vacuoles with the evident cover membrane were taken into account, therefore we set the minimum size of counted vacuoles as 30 mm. The shape of the vacuoles was considered to be a sphere. Cells with one or more vacuoles containing food items were counted and their share in total cell numbers was calculated. In the samples from the Black Sea, zooplankton species and the number of eggs of the copepod Calanus euxinus were counted. Eggs were identified by their morphology and size range of 168–195 mm. For correlation analysis additional parameters were used. SST was measured at the monitored sites on the day of sampling. Data on phytoplankton wet biomass in the Black Sea for May-June were taken from the Black Sea phytoplankton data base (Mikaelyan et al., 2007) with the addition of recent data. Data on chlorophyll concentration were retrieved from Aqua MODIS satellite images, monthly averages, 4 km resolution (http://oceancolor.gsfc.nasa.gov). In the Adriatic Sea, chlorophyll concentration was averaged for the area in the Gulf of Trieste bounded by 458330 –458400 N latitude and 138250 –138400 E longitude. In the Black Sea, for the same purpose an area was chosen (438000 –448300 N and 368300 – 388000 E) in which the most stations were located (Fig. 1b). For the same area, data on wind velocity (10 m above the sea surface, 6 h averaging) were taken from the reanalysis dataset (http:// nomad3.ncep.noaa.gov/ncep_data). In the Adriatic Sea, wind velocity data were obtained from a moored hydrographic buoy (5 m above the sea surface, 6 measurements per day) at the location also representing the sampling site for Noctiluca. Standard statistical procedures (ANOVA, t-test and correlation analysis) were used for comparing data. Mean values in the text below are presented with standard error (SE) and number of measurements (n). 3. Results 3.1. Size structure and feeding activity Noctiluca was most abundant during spring (March–June) both in the northern Adriatic and the northeastern Black Sea, with populations having similar average cell diameter in both studied areas: 507 mm and 536 mm, respectively (Table 1). In autumn (September–October) average cell sizes were smaller (468 and 514 mm) in both studied regions. For both periods average cell diameter was significantly higher in the Black Sea. Nevertheless, both populations had similar size structure (Fig. 2) with two classes 401–500 mm and 501–600 mm being the most numerous. On average, these two size classes contributed from 60 to 70% to total cell numbers. In both seas minimum cell diameter was around 200 mm while the maximal diameter was close to 800– 1000 mm. Typically one cell contained 1 to 2 food vacuoles and the highest number of the vacuoles per cell was 10 in both seas. Different food items were identified in the vacuoles: eggs (mainly copepod eggs), nauplii, veligers, phytoplankton cells and cysts (Fig. 3). The maximum size of food vacuole in the Adriatic and Black Sea cells was 430 mm and 360 mm, respectively. In spring the average number of vacuoles in the cell in the Adriatic Sea (1.78) was similar to that in the Black Sea (1.58). In autumn, this parameter was substantially lower (0.69) in the Adriatic Sea and slightly less (1.46) in the Black Sea (Table 1). The mean food vacuole diameter was roughly similar in both seas and varied from 79 to 95 mm. In

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Table 1 Characteristics of Noctiluca scintillans in the Adriatic Sea and the Black Sea during the period of highest cell abundance (May–June) and in autumn (September– October). Period

Adriatic Sea May September–October p Black Sea 1 May–15 June September–October p

Cells

Food vacuoles

Diameter (mm)

Number per cell

Diameter (mm)

% in samples

507  7.0 (280) 468  9.1 (106) 0.003

1.78  0.14 (192) 0.69  0.09 (106) 0.003

79  2.0 (341) 94  4.4 (73) 0.01

79  6.0 (19) 49  7.0 (11) 0.03

536  5.7 (280) 514  2.5 (2152) 0.002

1.58  0.09 (280) 1.46  0.06 (1150) 0.26

Feeding cells

95  2.8 (426) 86  1.1 (1701) 0.000

76  3.2 (28) 65  2.0 (115) 0.008

Mean  SE. Number of measurements is given in brackets. p – probability of Null hypothesis for two averages given above, the bold marks significant difference of means for 95% probability level.

the Black Sea, it was higher in spring and in the Adriatic Sea in autumn. In spring the percentage of feeding cells within the populations was the same in both seas and varied from 76 to 79%. In both seas the share of cells containing food items in a population was significantly lower in autumn compared to spring.

Fig. 2. Cell size spectrum of Noctiluca in the Black and Adriatic Seas. Columns show mean proportion of six size categories in the total cell numbers. Total number of cell diameters measured equals 1212 for the Adriatic Sea and 2746 for the Black Sea.

3.2. Seasonal and interannual dynamics In both studied regions the annual dynamics of Noctiluca showed a similar pattern with the evident maximum in spring or early summer (peak period) and relatively low densities in other seasons of the year (Fig. 4). In the Black Sea, the highest cell abundance occurred in May and in the first half of June (Fig. 4a) with a similar pattern both at the nearshore site and in open waters thus showing good positive correlation (r = 0.8, p = 0.01, n = 24). In the northern Adriatic Sea, the peak period occurs in May (Fig. 4b). As a whole, the period with notable presence of Noctiluca is longer in the Adriatic Sea. Substantial cell concentrations were often

Fig. 3. Light micrographs of Noctiluca scintillans with different food items: (a) veliger, (b) nauplius, (c) copepod eggs, (d) dinoflagellate cysts.

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Fig. 4. Seasonal dynamics of Noctiluca in the Black Sea (a) and Adriatic Sea (b). Columns show all years means of number of cells (103 m3) for 15 day periods. For the Black Sea white columns show the pier data; black columns – the open waters data. Dotted curves show the sea surface temperature (SST). Vertical bars show SE.

observed from the second half of March until August. Maximal Noctiluca cell densities were observed in a similar range of temperatures from 12 8C to 22 8C in both seas (Fig. 4) however, in the northern Adriatic Sea, notable cell concentrations occurred both at low temperatures in February (9 8C) and at high temperatures in August (25 8C). In contrast to a similarity in seasonal dynamics, considerable differences were found in interannual dynamics between the two seas. In the Black Sea, the most prominent peaks in cell numbers

were observed in 2008, 2011 and 2012 (Fig. 5). Maximal abundance of Noctiluca reached 20–25  103 cells m3. Less notable cell maxima (1–5  103 cells m3) were observed in 2002 and 2003 (not shown on Fig. 5) and in 2005, 2006 and 2009. Very low maximum cell numbers (0.1–0.3  103 cells m3) were registered in 2004, 2007 and 2010. In all years, the annual maximum occurred in May and the first part of June. In the northern part of the Adriatic Sea, a large number of cells of Noctiluca was recorded in 2004, 2009 and 2012 (Fig. 5). In these

Fig. 5. Long-term changes of Noctiluca populations at two monitored sites in the Adriatic Sea and in the Black Sea. Columns show monthly averages (2–3 observations) of cell abundance (103 m3). Numbers indicate the extra maximal values.

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Fig. 6. Vertical distribution of cells of Noctiluca and eggs of Calanus euxinus in the Black Sea in May-June and in August-September. Columns show averages of cell and egg numbers for three layers: UML-the upper mixed layer, PYCN – pycnocline, LBP – layer below the pycnocline. Horizontal bars – SE. Total number of averaged vertical profiles is equal to 6 for May-June and 19 for August–September.

average depth of 15 m in August, cell density was very low (0.008  0.004  103 cells m3). Almost the entire population (98.6%) was located below the UML. Vertical distribution of the eggs of the copepod Calanus euxinus, which are the food items for Noctiluca in the Black Sea, showed the highest density (99  49 eggs m3) in the UML in May–June (Fig. 6a). Below the UML, concentration of eggs decreased to 40  11 eggs m3. About 30% of all eggs in the water column were contained in the UML. The number of eggs in the UML was 3 times lower (30  52 eggs m3) in August–September (Fig. 6b). Similar to the vertical distribution of Noctiluca cells, the highest densities of eggs (97  33 eggs m3) were observed in the pycnocline and about 25% of all eggs in the water column were contained in this layer.

years, the annual maximum of cell density reached 15– 70  103 cells m3. Low cell maxima (1–7  103 cells m3) were observed in 2008, 2010 and 2011. Noctiluca abundance was very low (0.3–0.6  103 cells m3) in 2005, 2006 and 2007. Usually one peak was observed during each year, with the exception of 2008 when two peaks occurred in May and late July. Annual maxima of cell numbers were recorded in different months from April (2004) to August (2011). In the case of mass development the annual peaks were observed in May. 3.3. Vertical distribution Vertical distribution of Noctiluca in spring showed high cell concentration in the UML and in the pycnocline in spring and early summer (Fig. 6a). Average cell densities in both layers were similar (1.6  1.1  103 cells m3 in the UML and 1.8  0.6  103 cells m3 in the pycnocline). A significant part of the population (33%) was located in the UML, which typically occupied the upper 10 m. In late summer and early autumn, the highest cell concentration (0.3  0.09  103 cells m3) occurred in the pycnocline and was several times lower than in May–June (Fig. 6b). In the UML, with its

3.4. Correlation analysis It was assumed that the factors controlling growth of Noctiluca are more obvious during the peak period. For this period, the relationships between the concentration of cells and different abiotic and biotic parameters were analyzed. It is obvious that correlation at the level of samples will not be quite correct because

Table 2 Correlation coefficients (r) between Noctiluca abundance (m3) in the peak period and abiotic/biotic parameters in the Black Sea and in the northern Adriatic Sea. Parameter

Black Sea

Northern Adriatic

Monitored site

Open waters

Eggs of Calanus euxinus, no. m3

0.09 p = 0.72, n = 11 0.18 p = 0.62, n = 8 0.45 p = 0.22, n = 9 np

Calanus euxinus, no. m3

np

0.52 p = 0.18, n = 9 0.57 p = 0.89, n = 9 0.18 p = 0.96, n = 8 0.76 p = 0.006, n = 11 0.01 p = 0.99, n = 11 0.9 p = 0.001, n = 11 S0.94 p = 0.001, n = 11 S0.92 p = 0.001, n = 11 nd

Sea surface temperature, 8C 1

Phytoplankton biomass (mean for the upper 15 m layer) mg l Chlorophyll, mg l1

Wind velocity, m s

1

Square wind velocity, m2 s2 Windy hours, per montha Noctiluca abundance in April, cell m3 Noctiluca abundance in March, cell m3

0.54 p = 0.09, n = 11 S0.72 p = 0.01, n = 11 S0.63 p = 0.043, n = 11 0.75 p = 0.02, n = 10 0.58 p = 0.1, n = 10

nd

0.27 p = 0.51, n = 8 nd 0.63 p = 0.065, n = 9 np np 0.57 p = 0.1, n = 9 0.55 p = 0.1, n = 9 S0.67 p = 0.04, n = 9 0.45 p = 0.22, n = 9 0.72 p = 0.03, n = 9

Peak period–period of annual maximal abundances (1 May–15 June for the Black Sea and May for the northern Adriatic Sea); n – number of values (averages for one year); p – probability of Null hypothesis; nd – no data; np – no parameter. a See explanations in the text. Bold indicates significant correlation with p < 0.05.

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Fig. 7. Abundance of Noctiluca versus Calanus euxinus eggs in the open waters of the Black Sea in May–June. Dots show annual averages of cell numbers (103 m3) for May–June (upper panel) and for August–September (bottom panel). Vertical bars show SE. Some bars are very small and they are masked by dots.

of the various patchiness of biological parameters and an apparent time lag with environmental changes. Because of this, averages of cell numbers for the peak period are more suitable for correlation analysis. Based on this, for the Black Sea, the mean cell densities for May and the first half of June were taken for analysis. For the northern Adriatic Sea, the average concentrations for May were used.

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As expected from observed interannual dynamics (Fig. 5) no correlation was found between average cell concentrations in the peak periods in the two seas. No relationship was observed between the SST and Noctiluca abundance (Table 2). In the Black Sea, no correlation was found between phytoplankton biomass in the upper 15 m layer and cell numbers. The same was true regarding chlorophyll concentration. In the northern Adriatic Sea, a moderate positive correlation with a rather high probability (93.5%) was revealed between chlorophyll concentration and Noctiluca abundance mainly due to data from 2009. In that year the very high values of cell numbers (70  103 cells m3) and chlorophyll concentration (4.5 mg l1) were observed. Analysis of the relationship between Noctiluca cell numbers and the abundance of the main zooplankton species revealed no significant correlation in the open waters of the Black Sea. Among all representatives of zooplankton only the number of eggs of Calanus euxinus was positively correlated with abundance of Noctiluca (Table 2). This relationship between Noctiluca and the eggs was observed in the peak period in May–June (Fig. 7a) and high cell numbers of Noctiluca occurred in years when the concentration of eggs was more than 50 per m3. In contrast, no significant correlation was found in August-September (Fig. 7b). Noctiluca abundance was not significantly related to the number of adult specimens of C. euxinus at any time. In contrast to the main biotic parameters, a significant relationship was observed between Noctiluca cell numbers and wind velocity in both seas (Table 2). In the Black Sea, average wind velocity in the peak periods varied from 3.3 to 5.5 m s1, revealing the strong negative correlation (r = 0.9) with cell densities in open waters. At the nearshore site this relationship also existed but at a lower probability level (r = 54, p = 0.09). A similar correlation (r = 57, p = 0.1) was observed in the northern Adriatic Sea, where the average wind velocity in the peak periods varied from 3.5 to 4.2 m s1. The wind has an impact on Noctiluca population by increasing turbulence of the water. The latter depends on wind stress, which is defined as square wind velocity multiplied by some coefficient (Zatsepin et al., 2008). Use of a square wind velocity in

Fig. 8. Abundance of Noctiluca versus number of windy hours in the Black Sea and in the northern Adriatic Sea in May-June and in August. Dots show annual averages. On panel (a) values are presented for the open waters (black cycles, cell numbers  10) and for pier (white cycles). The hours were defined as windy if the wind speed was more than 6 m s1 for the Black Sea and 5 m s1 for the Adriatic Sea.

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Fig. 9. Abundance of Noctiluca versus number of windy hours at the monitored sites in the Black Sea and in the Adriatic Sea in the peak period in May–June. Only years with substantial cell abundance in April are shown. Other definitions are the same as those on Fig. 8.

correlation analysis led to an essential increase in the power of the correlation for the Black Sea (Table 2). The most profound effect on the turbulence of water is created by strong winds and therefore we calculated the number of windy hours per month during the peak periods. We tested various values of wind velocity above which the wind was considered as strong. In each range of these values from 4 to 7 m s1 a significant negative correlation was observed between the number of windy hours and cell concentrations. In the Black Sea, the strongest correlation (r = 0.92) was found for the open waters when wind exceeding 6 m s1 was defined as the strong (Table 2). In the northern Adriatic Sea, the highest correlation (r = 0.67) was obtained at winds higher than 5 m s1. At the coastal sites in both seas high cell densities were observed if the number of windy hours per month was less than 170 (Fig. 8a, b). A higher value of 220 h was determined for the open waters of the Black Sea. The relationships between the abundance of Noctiluca and duration of windy hours or average wind velocity were absent in August in both seas (Fig. 8c, d). A close relationship in both seas between the number of Noctiluca in the peak period and its abundance in the preceding months was observed (Table 2). In the Black Sea, a high positive correlation (r = 0.75) was established between the cell abundance in May–June and in April. Less pronounced, but also a positive correlation was found with the number of cells in March. In the northern Adriatic Sea, a high positive correlation (r = 0.72) was revealed between the amount of cells in May and in March (Table 2). For both nearshore sites cell concentrations in April of more than 0.1  103 cells m3 can be considered as substantial. In this case Noctiluca abundance in the peak period has even more obviously depended on wind regime (Fig. 9). Both in the northern Adriatic and the Black Sea mass development of Noctiluca was observed when the number of windy hours was less than 170–180. This boundary definitely divided years with high and low cell abundance. 4. Discussion Due to the very shallow depth of 7 m at the monitored site in the Black Sea cell densities may not be fully representative for the whole area, but reflect those of the shelf waters. Observed annual peaks in the Black Sea (1–26  103 cells m3) were comparable to those in the northwestern part of the Black Sea where maxima varied from ca 5  103 cells m3 to 65–70  103 cells m3 in 2001 and 2002 (Velikova and Mihneva, 2005). In general, our values are similar to those found in previous periods (1993–1995) in the northeastern part (Shiganova, 2009) as well as in Bulgarian shelf waters in 2002–2006 (Shiganova et al., 2009). A lower interannual

range (2.5–12  103 cells m3) was reported for coastal waters near Crimea in 1960–1964 (Bitukov, 1969). In the northern Adriatic Sea, cell densities found during this study were comparable to those (2–70  103 cells m3) reported for previous periods (Fonda-Umani et al., 2004). In the open waters of the Black Sea, maximal cell densities (1–15  103 cells m3) were lower than at the nearshore monitored site. The maximal concentration (42  103 cells m3) was recorded in the pycnocline in June 2011 (Drits et al., 2013). Thus, similar ranges of cell numbers were observed in both seas while the record values were higher in the Adriatic Sea (Fig. 5). It should be noted that during nine years (2004–2012) of synchronous observations in coastal waters, the red tides caused by Noctiluca were not observed in the Black Sea and were noted on a small scale as very localized events in the Adriatic Sea. The observed seasonal dynamics of the abundance of Noctiluca (Fig. 4) is consistent with previous studies in both seas. In the northeastern part of the Black Sea, the regular annual maxima in cell density were registered in May–June (Vinogradov et al., 1992; Shiganova, 2009). Slightly different peak periods (June–July) were recorded along Romanian and Bulgarian shelf waters (Porumb, 1989; Shiganova et al., 2009). Maximal cell densities in the northwestern shelf waters also occurred in June, but additional peaks were recorded in November (Velikova and Mihneva, 2005). Along the southern coast of the Black Sea, peaks in Noctiluca abundance regularly occurred in April–May, while additional maxima were observed in July-August or December (Ustun, 2005). Near the shore of the Crimea, the annual peaks were mainly recorded in June (Zaika, 2005). In the northern Adriatic Sea, the regular annual maxima in cell numbers occurred from March to June (Malej, 1983; Fonda-Umani et al., 2004). Additional sporadic peaks of cell density were observed in November–December and February (Fonda-Umani et al., 2004). Seasonal dynamics of Noctiluca abundance are generally similar in different areas of the world showing maxima mainly in spring or early summer. In the North Sea, the maximum was recorded in June-July with a lower but pronounced peak in December–January (Daan, 1987; Uhlig and Sahling, 1990). In coastal waters of the Japan Sea, the maximum was recorded in March-June and a second peak occurred in October–December (Fung and Trott, 1973; Montani et al., 1998; Miyaguchi et al., 2006). In the Red Sea, the bloom was recorded in February (Mohamed and Mesaad, 2007). In the Gulf of Oman, the bloom occurred in June-July and a second peak was recorded in November (Al-Azri et al., 2007). In the northeastern Arabian Sea, the seasonal peak occurred in February– March (Prakash et al., 2007). In the Bay of Bengal, the bloom was observed in April (Mohanty et al., 2007). In the Gulf of Thailand, two peaks were registered, in March–June and in October (Lirdwitayaprasit et al., 2006). In Mazatlan Bay, Gulf of California, a bloom was registered in January (Rodrı´guez et al., 2005). A bloom was recorded in November–December (Australian spring) near the Andaman Islands and near the coast of Australia (Dela-Cruz et al., 2002; Dharani et al., 2004). Thus, the general pattern of seasonal changes in Noctiluca abundance in the Black Sea and in the Adriatic Sea as well as in most areas of the world demonstrates a regular annual maximum occurring in spring – early summer and additional sporadic short peaks with a lower density appearing in other seasons. Annual peaks in Noctiluca abundance were observed within a certain range of water temperatures in both seas (Fig. 4). In previous studies it was considered that the period of intensive growth of the Noctiluca population in the Black Sea is related to water temperature. The cumulative heating calculated as a sum of daily water temperatures during a period prior to outburst was considered to be a trigger for Noctiluca mass development (Bitukov, 1969). The optimum temperature range was defined as from 11 8C

A.S. Mikaelyan et al. / Harmful Algae 33 (2014) 29–40

to 14 8C. Later the optimum temperature for the Noctiluca spring peak was considered to be from 15 8C to 19 8C (Shiganova, 2009). In the present study we observed Noctiluca peaks at SST ranging from 12 8C to 22 8C in both examined areas. In the past, in the northern Adriatic the seasonal maxima were observed in April at low temperatures (10 8C) as well as in June at high temperature 22– 25 8C (Malej, 1983; Fonda-Umani et al., 2004; present study). Also, it was considered earlier that high temperatures suppress the growth of Noctiluca population. In the Black Sea, it disappears from the upper mixed layer in summer, which coincides with an increase in water temperature to 20–24 8C (Porumb, 1989; Bitukov, 1969; Vinogradov et al., 1992). In the South China Sea, Noctiluca decreased after the temperature rose to over 25 8C (Huang and Qi, 1997). In the Bay of Bengal, the optimum temperature for population bloom ranges from 26.7 8C to 30.6 8C and the temperature crucial for growth is over 31 8C (Mohanty et al., 2007). It seems that even a temperature over 24– 25 8C is not physiologically crucial for growth of so eurythermal an organism like Noctiluca. Its disappearance from the upper mixed layer in summer (Fig. 6b) may be related to changes in nutritional or other environmental conditions. Based on a wide temperature range of about 10 8C to 25 8C at which maximal cell numbers are observed in temperate waters (Harrison et al., 2011; this study), it can be assumed that the temperature itself is not a factor which controls Noctiluca blooms. This conclusion is consistent with many observations in different world regions which showed contradictory results concerning the effect of temperature on Noctiluca population dynamics. The positive relationship between winter SST and Noctiluca abundance was evidenced in the North Sea (Heyen et al., 1998) and in the Sea of Marmara (Yılmaz et al., 2005). A negative relationship between SST and cell abundance was found in the Indian Ocean (Dharani et al., 2004; Mohanty et al., 2007) and in the South China Sea (Huang and Qi, 1997). The absence of any relationship between these parameters was observed in Sagami Bay (Miyaguchi et al., 2006), in the Gulf of Trieste (Fonda-Umani et al., 2004), in the Red Sea (Mohamed and Mesaad, 2007), in the Gulf of Oman (Al-Azri et al., 2007) and in this study. The interannual variations in 2004–2012 did not match in both areas of this study. In some years, there was quite a different number of Noctiluca in the northern part of the Adriatic Sea and in the Black Sea (Fig. 5). There was no correlation in peak abundances between the two seas. Climate control of gelatinous plankton abundance has been recorded for several marine regions including the Mediterranean Sea (Molinero et al., 2008) and the Black Sea (Niermann, 2004). Observed divergence in the interannual pattern of Noctiluca abundances in the Black Sea and in the Adriatic Sea may be explained by different regional climatic forcing. The North Atlantic Oscillation index (NAO) affects the Adriatic Sea (Conversi et al., 2010), while the Black Sea regional climate is governed both by NAO and East-Atlantic–West-Russia teleconnection patterns (Oguz et al., 2006). In addition, local factors specific to each area may be more important during a particular year than more global climate alterations. One important Noctiluca population feature we studied was its cell size and we found a similarity in cell size spectra for the Black Sea and the Adriatic populations (Fig. 2). Our data from the Black Sea confirm the previous study of Zaika (2005) who reported cell diameters from 400 to 600 mm as typical for the Noctiluca population in the Black Sea. To our knowledge there was no similar study in the Adriatic Sea. The reported range is also common for the North Sea (Elbrachter and Qi, 1998). Average cell diameter changed from 380 to 660 during the year in the Sea of Japan (Nakamura, 1998a). Cell size of Noctiluca in the Black Sea and in the northern Adriatic Sea was substantially smaller than in the southeast coastal waters of Australia where the cell diameter

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typically is larger than 600 mm (Dela-Cruz et al., 2002; Mcleod et al., 2012). Seasonal changes in cell diameter are well documented for many sea areas. Average cell size was higher in the Australian spring than in other seasons (Dela-Cruz et al., 2002), which is consistent with our results (Table 1). Another pattern was observed in the coastal waters of Sagami Bay, Japan where the maximum cell volume reached a peak in winter (Miyaguchi et al., 2006). In the same region, the maximal cell size was also recorded in August (Nakamura, 1998a). Some authors believe that the prevalence of large cells points to a degradation of population (Uhlig and Sahling, 1990; Huang and Qi, 1997; Dela-Cruz et al., 2002; Al-Azri et al., 2007). The present study does not support this idea and agrees with some results of growth experiments and field observations (Nakamura, 1998a, 1998b). In both seas, the average cell diameter in the peak periods was higher than in autumn (Table 1), when the population of Noctiluca has a low cell number, indicating the descending phase. The proportion of cells containing food particles in their food vacuoles observed in both seas in spring (70.8–72.6%) was very similar to that (77.6%) observed along the southeast coast of Australia in the same season (Dela-Cruz et al., 2002). The lower share of feeding cells which were observed in autumn in the Black Sea (64.2%) and in the Adriatic Sea (48.5%) also corresponded to a lower proportion of feeding cells that occurred during the Australian autumn and winter (44.6%) (Dela-Cruz et al., 2002). The maximal number of food vacuoles in a cell that we found in both seas was equal to 10, but the typical value was much lower (1–2). Observed numbers of 2–32 (typically 4–6) were reported for Noctiluca grazing on phytoplankton cultures (Strom, 2001). Higher content of vacuoles in cells in laboratory experiments in contrast to that in our field data can be explained by high food concentration (more than 500  103 Gymnodinium cell l1) which was not observed in nature. This is consistent with findings in the Sea of Marmara where the number of food vacuoles in a cell at more eutrophic stations was higher than that at other stations (Yılmaz et al., 2005). We speculate that smaller Noctiluca cells in autumn may be related to poorer nutritional conditions. The evident decrease in the share of feeding cells and number of food vacuoles supports this suggestion (Table 1). Generally Noctiluca seems to be better provided with food in the peak period in both seas. Close ranges of cell numbers and magnitude of annual maxima indicate similar food conditions for Noctiluca in both seas. Thus, comparison between populations of Noctiluca from the two regions showed similarity in size structure, feeding activity and seasonal dynamics, while their interannual changes were different. Among all biotic parameters only the concentration of the eggs of Calanus euxinus was well positively correlated with abundance of Noctiluca (Table 2 and Fig. 7). In the Black Sea, egg diameter ranges from 168 mm to 195 mm with an average of 180 mm (Sazhina, 1987; Isinibilir et al., 2009). The mesh size used was slightly less. It is impossible to estimate the real part of the captured eggs, because there are many sources of mucus in the Black Sea, which is actually increases catchability of small objects, such as eggs. The number of eggs ranged from 500 to 20,000 m2 (8000 an average), which is very close to the values from 4000 to 12,000 m2, which were obtained using a net with a mesh size of 112 mm (Yuneva et al., 1999). It can be assumed that most of the eggs had been caught. Given that the number of eggs changed several times from year to year (Fig. 7), possible losses are not critical to the reliability of the observed positive relationship. The feeding of Noctiluca on copepod eggs has been recorded in many regions. In the inshore waters of southern California, Noctiluca preyed heavily on Acartia tonsa eggs, eliminating ca 50% of the total egg abundance (Kimor, 1979). Consumption of 70% of Acartia clausi

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eggs was estimated in the Japan Sea (Sekiguchi and Kato, 1976). A similar maximal value (70% of A. clausi eggs) was reported for the Mediterranean Sea (Quevedo et al., 1999). In the southern North Sea, the highest percentage of ingested copepod eggs was close to 75% (Daan, 1987). In the Black Sea, the grazing pressure on Calanus euxinus eggs was estimated as 15–42% in March, 16% in April and 23% in June (Nikishina et al., 2011) and much less 1–10% in late June (Drits et al., 2013). In these studies the daily consumption of A. clausi eggs was estimated as 1–7% (up to 80% in swarms) in March and 43% in June. The displayed correlation may explain sudden outbursts of Noctiluca abundance in the absence of phytoplankton mass development. The appearance of highly caloric, easily captured and conveniently sized food like eggs could be the trigger and a source for rapid population growth of Noctiluca. This assumption is in accordance with estimations of daily rations of Noctiluca, which on 3–47% (in terms of carbon) consisted of copepod eggs in spring (Nikishina et al., 2011). In addition, vertical distribution shows that substantial portions of the total amount of both Noctiluca and eggs are contained in the UML in spring (Fig. 6a), which makes their encounter possible. On the other hand, the average number of Calanus euxinus eggs per one Noctiluca cell seems to be rather low. It was equal to 0.06 for the UML in May–June, which is in the range from 0.03 to 0.4 reported for the total water column earlier (Nikishina et al., 2011). Even if all eggs would be consumed from the whole water column, only a small part of the population will be provided with eggs. It is clear that C. euxinus eggs alone cannot support the growth of Noctiluca. Also, taking into account a clearance rate on large food items of 0.4 ml day1 (Kiørboe and Titelman, 1998) it is not clear how Noctiluca encounters its prey with such low densities (100 eggs per m3). During August–September the main bulk of cells and eggs is located in the pycnocline (Fig. 6b). An average ratio between the eggs and the cells is much higher (0.3) than in spring. Nevertheless, this does not support the development of Noctiluca, whose cell numbers in this layer are much lower than in spring. It could be hypothesized that the possible dependence of Noctiluca growth on copepod egg density (including eggs of small copepods not assessed in this study) occurs only in spring and in case of high egg concentration and can act as an additional factor to generally favorable conditions. Also it is probable that this correlation is casual and can be governed by similar favorable conditions for growth of Noctiluca and copepod egg production. The importance of wind as a factor which forces the cells of Noctiluca to mechanically accumulate at physical discontinuities and forms red tides was reported by many authors (Al-Azri et al., 2007; Miyaguchi et al., 2006; Elbrachter and Qi, 1998). As observed in this study in both seas, the negative relationship between the number of cells and the effect of the wind indicates a direct impact on the abundance of Noctiluca (Table 2, Figs. 8 and 9). This relationship has not been reported previously with one exception. The negative correlation between the number of several species of dinoflagellates, including Noctiluca, and summer surface scalar wind speed has been revealed in the analysis of a 50-year (1960–2009) time series of phytoplankton abundance in the northeast Atlantic (Hinder et al., 2012). There are, however, many references in the literature to the importance of stable water conditions for Noctiluca growth. In the Sagami Bay (Japan), such meteorological factors as wind direction and rainfall affected Noctiluca growth (Miyaguchi et al., 2006). These authors also noted that that the transition from low to high water stability contributed to bloom formations. Near the southeast coast of Australia, the abundance of Noctiluca was high when the highly stratified water column and high cell number of small centric diatoms in surface water layers were observed (Dela-Cruz et al., 2002). In the upper gulf of Thailand, Noctiluca was observed all year round except during strong wind periods (Lirdwitayaprasit et al., 2006).

In littoral of northwestern shelf of the Black Sea, at an abnormal windless conditions in June and July 1986, Noctiluca reached an enormous amounts of 500,000 ind. m3, that led to a series of red tides (Porumb, 1989). Obviously, wind stirring increases turbulence in the UML. It is generally known that while low, small-scale turbulence doesn’t seriously influence division and growth of dinoflagellates (Havskum and Hansen, 2006), it negatively influences at high levels (White, 1976; Smayda, 2010). Due to peculiarities of feeding behavior, turbulence may be the particular circumstance that prevents the normal feeding of Noctiluca. As described in detail by Kiørboe and Titelman (1998), Noctiluca feeds by means of its long tentacle with a tip covered with mucus, to which the food particles attach. In stable water, mucus strings up to several millimeters long may be formed. These threads are rolled to a clump of food items which is then brought to the cytostome. Turbulence physically interferes with the feeding process preventing formation of mucus strings and curls or their ingestion. This was confirmed in experiments in which the increase in turbulence resulted in a decrease in clearance rate by several times (Kiørboe and Titelman, 1998). Another reason that turbulence may be detrimental to the feeding process is the high nutritional requirement of Noctiluca. Experimental data and field observations indicate high growth rates of Noctiluca at very high phytoplankton (500–1000 mg C l1) and chlophyll (2 mg l1) concentrations (Nakamura, 1998a; Kiørboe and Titelman, 1998). Also, Noctiluca has a very high food concentration threshold of cc 100 mg C l1 which corresponds to phytoplankton bloom conditions (Nakamura, 1998b). Based on this evidence, it is considered that Noctiluca is adapted mainly to eutrophic conditions. It is confirmed in the numerous reports of high densities of Noctiluca associated with diatom blooms (Porumb, 1989; Painting et al., 1993; Kiørboe and Titelman, 1998; Nakamura, 1998a; Dela-Cruz et al., 2002; Turkoglu, 2013). In the northern Adriatic Sea, the maximal cell number was observed in 2009 (Fig. 5) when a very high chlorophyll concentration (4.5 mg l1) occurred. At the same time, it is not clear how Noctiluca can produce mass development in mesotrophic waters. In the Black Sea, phytoplankton wet biomass in the upper 15 m in May– June varied from 200 to 1000 mg l1 (Mikaelyan et al., 2011), which is much less than Noctiluca optimal nutritional conditions even with the possible addition of other food items. One possible explanation could be the presence of microlayers with high food concentration which are located at small gradients of density and which are not detected by our sampling technique (Dekshenieks et al., 2001; Alldredge et al., 2002). Possessing a significant ascent rate of 1.5 m h1 (Kiørboe and Titelman, 1998), Noctiluca can scan the water column and find these thin layers. That way Noctiluca colonizes aggregates of marine snow or diatoms and actively feeds on them (Shanks and Walters, 1996; Tiselius and Kiørboe, 1998). Wind induced turbulence destroys these layers decreasing the available food concentration. The effect of wind on Noctiluca is revealed under certain conditions. First of all, a substantial part of the population should be contained in the UML as it takes place in the peak period (Fig. 6a). In summer and autumn this relationship does not exist because the population is almost totally located in the pycnocline (Fig. 6b). Also the wind effect may not be important in eutrophic basins or under phytoplankton bloom conditions, where the food resources for Noctiluca growth are not limited. It is important that the abundance of Noctiluca in the peak period correlates well with that in the previous months (Table 2). This may indicate that the favorable conditions for Noctiluca population growth develop from the very beginning of spring. Another explanation is the rather high cell concentration required for mass development in the peak period. Due to low specific

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growth rates of 0.2–0.3 day1 in both seas (Fonda-Umani et al., 2004; Nikishina et al., 2011; Drits et al., 2013) a relatively high seeding cell number is needed to achieve high cell densities during the short peak period. In any case, substantial cell concentrations in April and calm weather conditions in May define the mass development of Noctiluca both in the Black Sea and in the northern Adriatic Sea (Fig. 9). Thus, cell concentrations in the months preceding the peak period and the weather forecast can be used for medium-term prediction of Noctiluca outbursts and possible red tides. 5. Conclusions The populations of Noctiluca in the northern Adriatic and the northeastern part of the Black Sea have many similarities. Size structure is characterized by two classes with 401–500 mm and 501–600 mm being the most numerous. In both the Adriatic Sea and the Black Sea, the average cell diameter in the spring peak period (507 mm and 536 mm, respectively) was higher than in autumn (468 and 514 mm, respectively). The proportion of cells containing food particles in their food vacuoles observed in the two seas in spring (70.8–72.6%) was higher than those observed in autumn in the Black Sea (64.2%) and in the Adriatic Sea (48.5%). Generally Noctiluca seems to be better provided with food in the spring peak period. The general pattern of seasonal changes in Noctiluca abundance in the Black Sea and in the Adriatic Sea demonstrates a regular annual maximum occurring in spring – early summer and additional sporadic short peaks with lower density appearing in other seasons. Annual peaks in Noctiluca abundance were observed within a wide range of water temperatures from 12 8C to 22 8C in both examined areas. In contrast to a similarity in seasonal dynamics, considerable differences were found in interannual dynamics between the two seas indicating that local factors specific in each area are more important during a particular year than more global climate alterations. Among analyzed parameters in both seas the significant negative relationship between the number of cells and the wind was revealed indicating a direct impact on the abundance of Noctiluca. A possible mechanism is that the turbulence physically interferes the feeding process and can prevent the formation of microlayers with high food concentrations which are necessary for high Noctiluca feeding rates. On this basis, a new hypothesis has been proposed: Noctiluca outbursts during the spring are controlled by the wind. In addition, in the open waters of the Black Sea the concentration of the eggs of Calanus euxinus was significantly positively correlated with abundance of Noctiluca. It could be hypothesized that the possible dependence of Noctiluca growth on copepod egg density (including eggs of small copepods) occurs in spring with high egg concentrations and as an additional factor acting together with generally favorable conditions. It is important that the abundance of Noctiluca in the peak period correlates well with that in the previous months. In the case of substantial cell concentration in April and calm weather conditions in May the mass development of Noctiluca can be expected both in the Black Sea and in the northern Adriatic Sea. Thus, cell concentrations in the months preceding the peak period and the weather forecast, together, are good predictors for Noctiluca outbursts and red tide events. Acknowledgements The work was performed within the framework of Russian and Slovenian cooperation, BI-RU/10–11-014 and financially supported by Slovenian Research Agency Program P1-0237, the

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