Scholarly article on topic 'Distribution of phytoplankton community in Kotor Bay (south-eastern Adriatic Sea)'

Distribution of phytoplankton community in Kotor Bay (south-eastern Adriatic Sea) Academic research paper on "Biological sciences"

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Similar topics of scientific paper in Biological sciences , author of scholarly article — Dragana Drakulović, Branka Pestorić, Mirko Cvijan, Slađana Krivokapić, Nenad Vuksanović

Academic research paper on topic "Distribution of phytoplankton community in Kotor Bay (south-eastern Adriatic Sea)"

VERSITA

Central European Journal of Biology

Distribution of phytoplankton community in Kotor Bay (south-eastern Adriatic Sea]

Research Article

Dragana Drakulovic1*, Branka Pestoric1, Mirko Cvijan3, Sladana Krivokapic2,#,

Nenad Vuksanovic1

Institute of Marine Biology, 85 330 Kotor, Montenegro

2Department of Biology, Faculty of Natural Science and Mathematics, University of Montenegro, 81 000 Podgorica, Montenegro

3Institute of Botany and Botanical Garden "Jevremovac", Faculty of Biology, University of Belgrade, 11000 Belgrade, Serbia

Received 01 July 2011; Accepted 30 January 2012

Abstract: The goal of this paper was to explain variability of phytoplankton in a shallow coastal area in relation to physico-chemical parameters.

Temporal variability and composition of phytoplankton were investigated in the Kotor Bay, a small bay located in the south-eastern part of the Adriatic Sea. Samplings were performed weekly from February 2008 to January 2009 at one station in the inner part of the Kotor Bay, at five depths (0 m, 2 m, 5 m, 10 m, 15 m). Phosphates, nitrites and nitrates ranged from values under the level of detection to the maximum values of 1.54, 1.53 and 23.91 ^mol l-1, respectively. The phytoplankton biomass - represented by chlorophyll a concentration - ranged from 0.12 to 6.78 mg m-3, reaching a maximum in summer. Diatoms were present throughout the whole sampling period, reaching the highest abundance in March (3.42x105 cells l-1at surface). The peak of dinoflagellates in July (2.2x106 cells l-1 at surface) was due to a single species, Prorocentrum micans. The toxic dinoflagellate Dinophysis fortii occurred at a concentration of 2140 cells l-1 in May. The present results of phytoplankton assemblages and distribution provide valuable information for this part of the south-eastern Adriatic Sea where data is currently absent.

Keywords: Phytoplankton assemblages • Diatoms • Dinoflagellates © Versita Sp. z o.o.

1. Introduction

Phytoplankton are the main source of primary production in estuarine ecosystems [1]. The response of phytoplankton to physical and chemical factors in the surrounding environment, such as salinity, temperature, light, nutrients, and water dynamics, and the configuration of the water basin, to name just a few, affects the structure and function of the entire planktonic community in transitional coastal ecosystems and makes this a central topic of research [2-4].

Studies on the structure and dynamics of plankton communities in the coastal areas of the Mediterranean Sea have increased over the last few decades [5-9]. However, information is often limited to coastal areas and is generally constrained to the northern Adriatic.

The north-eastern part of the Adriatic Sea is influenced by currents and oligotrophy karstic rivers which bring waters poor in nutrients and with higher salinity [10]. In the north-eastern Adriatic Sea, diatoms such as Cerataulina pelagica, Chaetoceros socialis, and Pseudo-nitzschia spp., often dominate the plankton community, as first noticed by Vilicic et al. [11]. In one part of this region (the Zrmanja estuary), oligothrophic conditions were most common, with diatoms dominating the community in early spring and dinoflagellates dominating in summer period [4]. A similar dominance of diatoms and an increase in dinoflagellates in June-July was recorded in the coastal waters of the north-western Adriatic Sea [12]. In the middle Adriatic Sea, phytoplankton species diversity was poor and nanophytoplankton were dominant [13]. The first information on the biovolume

E-mail: *ddragana@t-com.me *sladjana69@yahoo.com

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of microphytoplankton, nanophytoplankton and total phytoplankton in the Adriatic was reported for the southern part [14,15]. In the south-eastern part of the Adriatic, diatoms were quantitatively the most significant group of microphytoplankton, and nanophytoplankton averaged 93.6% of total number of phytoplankton cells [15]. For the southern Adriatic ViliCiC et al. [16] reported a checklist of the phytoplankton community and showed presence of the phytoplankton species. In the southeastern Adriatic, Vilicic et al. [17] presented influence of Albanian rivers on the nutrients distribution and distribution of phytoplankton and showed dominance of diatoms such as Chaetoceros species (C. circinalis, C. diversus). Caroppo et al. [18] presented phytoplankton seasonality in the south-western part of the Adriatic and found that phytoplankton densities show specific oligotrophic water.

The Kotor Bay is a region that has no great influxes of fresh water from streams and submarine springs, except during periods of precipitation. Periods of heavy rain in late winter and spring contribute to the increased amounts of nutrients in the Bay and consequently to higher phytoplankton activity [19].

Several previous studies related to the Kotor Bay referred to phytoplankton biomass [19-22] and phytoplankton communities [23].

The first occurrence of shellfish poisoning by phytoplankton in the Adriatic Sea was noted in 1989 in the northern part [24,25]. Most reports of Dinophysis spp. in the Adriatic Sea are from the northern basin, with few data available for the southern coastal areas. Caroppo et al. [26] presented a study on the composition and spatio-temporal distribution of the Dinophysis population in the coastal southern Adriatic Sea.

The aims of this study were to define the phytoplankton abundance and composition and to gain more insight into the factors that influence phytoplankton composition in the Kotor Bay (the southern Adriatic Sea). This paper may provide valuable information for future investigations as literature related to the phytoplankton in this area of the south-eastern Adriatic Sea is scarce.

2. Experimental Procedures

2.1. Study area

The Boka Kotorska Bay is located in the south-eastern part of the Adriatic Sea on the most jagged coastline of the Dinar's seashore (Figure 1). Approximately 50,000 inhabitants live along its coast. The Boka Kotorska Bay consists of four small bays (Herceg Novi Bay, Tivat Bay, Risan Bay and Kotor Bay), attached and connected to each other. The Boka Kotorska Bay also has two areas.

The first one connects open sea with the Herceg Novi Bay and the second one connects the Tivat Bay and the Risan Bay with the Kotor Bay.

The Kotor Bay, the area investigated in this study, is located in the innermost part encompassing around 30% of the Boka Kotorska Bay. The inner part of the Kotor Bay, where the sampling station is located, is shallow with a maximum depth of 20 m. The climate is of the Mediterranean type but the precipitation regime is heavily influenced by mount Orjen which receives Europe's heaviest precipitation with rain occurring seasonally [27]. In the area of the Kotor Bay there are two rivers: Skurda and Ljuta. Skurda is active during the whole year while Ljuta only during the late fall, winter and early spring.

In recent years the impact of human activity on marine ecosystem has been greater and faster as a consequence of increased settlement in coastal area. However, natural eutrophication still prevails in the Kotor Bay [21]. Although industry is not developed in this area, there is a concern because works on wastewater treatment plants have not been completed yet.

Agriculture in the Kotor Bay is present but not developed on a large scale while aquaculture has a stronger presence. Regarding aquaculture, there are 16 shellfish farms cultivating mostly mussels, and 2 fish farms rearing seabass/seabream registered in the

Figure 1. Map of the Boka Kotorska Bay in the Southern Adriatic Sea showing its four small bays. The sampling station is located in the inner part of the Kotor Bay. 1 and 2 indicate the two rivers: Ljuta and Skurda.

Boka Kotorska Bay of which in the Kotor Bay is located 8 shellfish farms and 2 fish farms. A new Law on Marine Fishery and Mariculture, which entered into force during 2009, regulates aquaculture production volume limits (minimal and maximal) and includes a programme of water quality monitoring and biomonitoring on and around the farms [28]. However, it is important to emphasize that there is no law that regulates the monitoring of toxic species in the Kotor Bay.

2.2. Sample collection and data analyses

Sampling was carried out from February 2008 to January 2009 with weekly frequency at a station in the inner part of the Kotor Bay (Figure 1) - Institute of Marine Biology (1MB). Water samples were collected at five depths (0 m, 2 m, 5 m, 10 m, 15 m) using a 5 L Niskin bottle (Hydro Bios, Germany). The total number of samples collected was 204. Sampling at weekly intervals for one year would have yielded 260 samples but some samples were not collected due to poor weather.

Physical parameters such as temperature, salinity and dissolved oxygen concentration were measured in situ using a universal meter (Multiline P4; WTW, Germany). Dissolved oxygen concentrations and saturations were determined using an oxygen electrode (Oxy Guard Handy Gamma - Zeigler Bros., Gardners, USA). Turbidity was determined using a Secchi disc. Nutrient (nitrates, nitrites and phosphates) concentrations were determined using standard methods [29]. Absorbance was detected on a Perkin Elmer UV/VIS spectrophotometer (Lambda 2 - Markham, Ontario, Canada), at a different wavelength for each nutrient. Samples to determine chlorophyll a concentration were first filtered through Whatman GF/F filters 0 4.7 cm and 0.7 pm pore size, and then the pigment was extracted in 90% acetone. Finally, chlorophyll a concentrations were determined on a Perkin Elmer spectrophotometer by measuring the absorbance at four wavelengths, and calculated according to Jeffrey et al. [30].

Phytoplankton was sampled with 5 L Niskin bottles and then preserved in 250 ml bottles using a 2% neutralized formaldehyde solution. Cells were identified and enumerated using Leica DMI4000 B inverted microscope (Heerbrugg, Switzerland) in subsamples of 25 ml after 24 h of sedimentation, following Utermohl [31]. Enumeration was carried out using phase contrast and bright field illumination at magnifications of 100, 200, and 630*. At a 100* magnification, total chamber bottom was scanned for taxa larger than 30 pm, while abundant microphytoplankton (>20 pm) were counted at two transects at magnification of 200*. Nanophytoplankton cells (2-20 pm) were counted in

15 randomly selected fields with a magnifications of 630*. The keys used for phytoplankton identification were Hustedt [32], Hasle and Syvertsen [33], Round et al. [34], and Throndsen et al. [35]. Small individuals (nanophytoplankton) that could not be detected under light microscope were not included in the taxonomic list. They were classified to recognizable taxonomic category: green nanoflagellates, small dinoflagellates and small coccolithophorids.

Statistica 7, Primer 5 and Surfer software programs were used for statistical analyses and graphical presentations of physical, chemical, and biological data. A logarithmic transformation [log10 (x+1)] was used on the data prior to statistical analyses in order to obtain normal distribution. A group-average linkage cluster analysis was used to determine the grouping of months, which was applied to the Sorensen similarity matrix computed with the presence and absence of species. Also, group-average linkage cluster analysis was used to determine the grouping of species, which was applied to the Bray-Curtis similarity matrix computed on their averaged abundances. Analyses of clustering were carried out on

16 taxa comprising taxa with a frequency greater than 20% in order to avoid confusing the patterns of cluster analysis. Two-dimensional multidimensional scaling (MDS) ordination was used to illustrate the relationships between months, with superimposed bubble plots to represent the different abundances of the most frequent species.

3. Results

Isothermic conditions were detected from March to mid May. In the summer period, temperature was variable because of weather conditions and intermittent precipitation, reaching a maximum in July (28.20°C). Inverted stratification and a strong thermocline was detected from mid October to January with a minimum in December (8.60°C, Table 1, Figure 2a). Contrary to temperature, salinity showed inverted stratification during the entire research period, with the presence of a strong halocline from mid October to January and isohaline conditions from August to September. A minimum of 2.30%o was measured in March and a maximum of 36.50%o in August (Table 1, Figure 2b).

From May to August, mean oxygen saturation was high (>100%), whereas from September a gradual decrease was recorded (the lowest O2 saturation was 67% in March and April and 69% in February) (Table 1). Nutrient concentrations did not appear stratified during the investigated period. Phosphate concentrations were higher in spring with

Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan

TEMP (oC) MAX 14.4 16.1 15.1 22.9 25.8 28.2 25.5 23.9 20.8 18.9 17.6 15.1

MIN 10.4 9.1 12.9 16.1 17.8 18.6 18.5 18.1 15.8 9.5 8.6 10.5

AVG 13.01 12.74 14.19 18.78 20.98 22.85 21.51 21.05 19.15 16.16 13.85 13.14

SD 1.37 1.62 0.72 1.76 2.13 3.06 2.33 1.69 1.41 2.16 2.58 1.68

SAL. (7j MAX 35.2 34.6 35.3 35.4 34.9 36 36.5 36.4 35.8 36 33.7 32.3

MIN 4.5 2.3 4.2 6.2 15.8 24 28.3 32.1 15.2 6.8 3 5.2

AVG 27.05 26.04 26.69 28.33 30.01 33.33 34.76 35.05 31.31 27.35 25.94 24.66

SD 13.21 11.9 10.32 8.79 5.8 2.98 2.38 1.38 6.69 9.45 79 9.65

OXY SAT. (%) MAX 83 82 108 138 136 120 120 100 94 106 79 74

MIN 69 67 67 95 98 91 93 89 81 75 72 71.7

AVG 77.25 74.4 82.5 108.8 108.9 106.6 103.9 95.05 87.93 88.15 75.93 71.7

SD 4.71 3.35 13.24 9.25 8.75 7.5 6.54 2.44 3.56 8.46 1.87 2.23

PO43-(ymol/l) MAX 0.48 1.15 1.54 1.49 1.34 0.20 0.25 0.34 0.08 0.07 0.2 0.35

MIN 0.08 0.08 0.29 0.07 0.09 0.06 0.08 0 0 0.006 0.006 0.16

AVG 0.27 0.51 0.64 0.55 0.43 0.12 0.15 0.08 0.02 0.02 0.05 0.16

SD 0.16 0.39 0.37 0.57 0.51 0.04 0.04 0.12 0.02 0.02 0.07 0.14

no2- (ymol/l) MAX 0.98 1.23 1.53 0.64 1.53 0.23 0.68 0.22 0.07 0.22 0.44 0.59

MIN 0.11 0.04 0.03 0 0 0 0.04 0 0 0.004 0 0.18

AVG 0.47 0.37 0.27 0.14 0.43 0.08 0.15 0.03 0.02 0.06 0.11 0.18

SD 0.25 0.032 0.34 0.16 0.52 0.07 8.57 0.06 0.02 0.07 0.16 0.23

NO3-(ymol/l) MAX 8.21 6.78 7.17 13.99 9.93 7.47 6.22 23.91 9.93 11.32 23.25 7.43

MIN 0.74 0.53 0.08 0.32 3.5 1.94 1.23 1.19 0 1.11 0.52 3.11

AVG 3.26 2.99 1.76 3.99 6.63 5.22 3.77 10.63 4.91 5.45 9.81 3.11

SD 2.47 2.3 1.8 3.64 1.78 1.45 8.57 8.23 2.89 3.07 7.65 2.86

Table 1. Maximum (MAX), minimum (MIN), mean (AVG) values and standard deviations (SD) of temperature (TEMP), salinity (SAL), oxygen saturation (OXY SAT), and nutrient concentrations (phosphate (PO43-), nitrite (NO2-), nitrate (NO3-)) from February 2008 to January 2009.

Figure 2. Temporal variability of a) temperature, and b) salinity in the Kotor Bay from February 2008 to January 2009.

the maximum value (1.54 jmol l-1) recorded in April (Table 1). Nitrite concentration followed the changes

in phosphate levels and reached a maximum value of 1.53 |jmol l-1 in April and June. Two maxima of

nitrate concentrations were observed: in September (23.91 |jmol l-1) and in December (23.25 |jmol l-1, Table 1). In these periods phytoplankton abundance was lower, which implies nitrate is less consumed by phytoplankton. Nitrate was significantly positively correlated both with the temperature (r=0.34, P<0.05, Table 2) and with salinity (r=0.44, P<0.01, Table 2), while nitrate and phosphate concentrations were significantly negatively correlated (r=-0.32, P<0.05, Table 2).

Phytoplankton biomass (represented by chlorophyll a) showed temporal variability. Maximum concentration of chlorophyll a was recorded in November (6.53 mg m-3 at surface) and July (6.78 mg m-3 at surface) (Table 3, Figure 3a). Mean (0-20 m) chlorophyll a concentration ranged from 1.08 mg m-3 in October and 1.09 mg m-3 in December to 4.44 mg m-3 in March (Figure 3a). Chlorophyll a was significantly positively correlated with the temperature (r=0.47, P<0.01, Table 2) and salinity

TEMP SAL TRANS PO43- NO3- CHL.a PH.AB DIAT DINO COCCO

TEMP 1.00

SAL 0.79** 1.00

TRANS. 0.00 0.29 1.00

PO43- -0.11 -0.29 -0.27 1.00

NO3- 0.34* 0.44** 0.05 -0.32* 1.00

CHL.a 0.47** 0.36* -0.08 -0.06 0.09 1.00

PH.AB 0.54** 0.28 -0.09 0.29 -0.09 0.56** 1.00

DIAT 0.17 -0.07 -0.08 0.28 -0.06 -0.06 0.22 1.00

DINO 0.64** 0.41** 0.05 -0.18 0.09 0.55** 0.53** -0.03 1.00

COCCO 0.08 0.41** 0.16 -0.30 0.28 0.05 -0.19 -0.34* -0.15 1.00

SILIC 0.03 0.04 -0.11 -0.13 -0.04 -0.23 0.01 0.04 -0.24 0.00

GREEN 0.54** 0.35* -0.11 0.27 0.01 0.57** 0.89** 0.08 0.43** -0.09

SMALL DINO 0.16 0.02 -0.12 0.31* -0.14 0.32* 0.59** 0.11 0.21 -0.08

SILIC GREEN

SMALL DINO

1.00 0.08 -0.01

1.00 0.42*

Table 2. Pearson's correlation for physical, chemical and biological parameters from February 2008 to January 2009 (in the 0-15 m layer)

The analysis was performed using monthly average of data. Correlations in bold font are significant at P<0.05 (*) and P<0.01 (**). TEMP: temperature; SAL: salinity; TRANS: transparency; PO43-: phosphate concentration; NO3: nitrate concentration; CHL. a: chlorophyll a concentration; PHY.AB: phytoplankton abundance; DIAT: diatoms; DINO: dinoflagellates; COCCO: coccolithophorids; SILIC: silicoflagellates; GREEN: green nanoflagellates; SMALL DINO: small dinoflagellates.

MAX MIN AVG SD n

DIAT 3.42 x 105 0 1.9 x 104 4.8 x 104 204

DINO 2.2 x 106 0 1.6 x 104 1.6 x 105 204

COCCO 1.9 x 105 0 2.6 x 103 1.3 x 103 204

SILIC 560 0 14.12 52.87 204

GREEN NANO 4.3 x 106 4.8 x 104 4.67x 105 4.8 x 105 204

SMALL DINO 4.3 x 105 0 5.07 x 104 7.07 x 104 204

CHL. a 6.78 0.12 2.13 1.29 204

Table 3. Maximum (MAX), minimum (MIN), mean (AVG) values and standard deviations (SD) of abundances of diatoms (DIAT), dinoflagellates (DINO), coccolithophorids (COCCO), silicoflagellates (SILIC), green nanoflagellates (GREEN NANO) and small dinoflagellates (SMALL DINO) and chlorophyll a concentration

(r=0.36, P<0.05, Table 2). Chlorophyll a was in positive significant correlation with dinoflagellates (r=0.55, P<0.01, Table 2), green nanoflagellates (r=0.57, P<0.01, Table 2) and small dinoflagellates (r=0.32, P<0.05, Table 2).

Total phytoplankton abundance reached the highest value in March (4.7x106 cells l-1 at surface), while maximum mean value was in May (1.53x106 cells l-1) (Figure 3b). Phytoplankton abundance was significantly positively correlated with the temperature (r=0.54, P=0.01, Table 2) and dinoflagellates (r=0.53, P=0.01, Table 2), green nanoflagellates (r=0.89, P=0.01, Table 2) and small dinoflagellates (r=0.59, P=0.01, Table 2).

Diatoms were presented in the phytoplankton assemblages throughout almost the entire study period, reaching a maximum in April (3.42x105 cells l-1 at surface) (Figure 4a, Table 3).

Mean diatom abundance was not much higher than dinoflagellate abundance (diatoms 1.9x104 cells l-1 and dinoflagellates 1.6x104 cells l-1), but both were approximately 7 times greater than coccolithophorid abundance (Table 3).

The highest abundance of dinoflagellates was recorded in July (2.2x106 cells l-1 at surface) due to Prorocentrum micans (Table 3), while in the other months dinoflagellate abundance was low (Figure 4b). Dinoflagellates were significantly positevely correlated with temperature (r=0.64, P<0.01, Table 2) and salinity (r=0.41, P<0.01, Table 2).

Coccolithophorid abundance was higher in autumn (maximum was in October 1.9x105 cells l-1 at surface) when diatom and dinoflagellate abundance was lower (Figure 4c, Table 3). The coccolithophorids were significantly positively correlated with salinity (r=0.41, P<0.01, Table 2) while the coccolithophorids and diatoms were significantly negatively correlated (r=-0.34, P=0.05, Table 2).

Silicoflagellates were rare and present at a very low abundance, reaching at most 560 cells l-1 in May at 15m. Mean abundance reached maximum value of 64 cells/l in May (Figure 4d, Table 3).

Average abundance of nanophytoplankton (such as green nanoflagellates and small dinoflagellates) ranged from 1.63x105 cells l-1 in February to 7.93x105 cells l-1 in May for green nanoflagellates (Figure 4e) and from 1.78x103 cells l-1 in September to 1.77x105 cells l-1 in March for small dinoflagellates (Figure 4f). Green nanoflagellates were significantly positively correlated with temperature, salinity and dinoflagellates (Table 2). Small dinoflagellates were significantly positevely correlated with phosphate, chlorophyll a, phytoplankton abundance and green nanoflagellates (Table 2).

During the entire sampling period, 109 taxa were identified: 48 diatoms (43.6%), 51 dinoflagellates (46.4%), 7 prymnesiophyceans (7.3%), 3 dictyochophytes (2.7%) (Table 4). The dominant taxa had abundance greater than 104 cells l-1 and a frequency greater than 10%. In this study the dominant diatoms were Thalassionema

Figure 3. Temporal variability of a) chlorophyll a, and b) total phytoplankton abundance in the Kotor Bay from February 2008 to January 2009.

Figure 4. Temporal variability of a) diatoms, b) dinoflagellates, c) coccolithophorids, d) silicoflagellates, e) green nanoflagellates, and f) small dinoflagellates in the Kotor Bay between February 2008 to January 2009.

MAX FR % AVG SD

Diatoms

Amphora grevilleana Gregory 200 2.95 2.55 17.345

Asterionellopsis glacialis (Castr.) Round 1520 2.45 16.47 131.364

Bacteriastrum hyalinum Lauder 440 1.47 3.73 3.73

Chaetoceros spp. 7850 5.88 113.549 782.296

Chaetoceros affinis Lauder 35358 11.8 850.088 4178.56

Chaetoceros breve Schütt 160 0.98 0.98 11.53

Chaetoceros compressus Lauder 600 0.98 4.51 47.512

Chaetoceros curvisetus Cleve 30157 4.43 297.27 2523.17

Chaetoceros decipiens Cleve 160 0.98 1.373 13.969

Chaetoceros protuberans Lauder 4712 0.49 23.098 329.906

Chaetoceros diversus Cleve 480 2.95 7.255 48.649

Chaetoceros tenuissimus Meunler 80 0.49 0.392 5.601

Chaetoceros vixvisibilis Schiller 7071 0.49 35.84 495.271

Cocconeis scutellum Ehrenb. 160 1.48 1.176 11.852

Coscinodiscus spp. 320 11.33 8.039 30.595

Coscinodiscus perforatus Ehrenb. 120 0.98 0.784 8.843

Cyclotella striata (Kütz.) Grun. 4714 1.97 25.265 330.567

Cylindrotheca closterium (Ehrenb.) 2357 0.98 23.108 232.802

Reim. et Lewin

Detonula pumila (Castr.) Gran 160 1.48 1.568 14.229

Diploneis bombus Ehrenb. 320 3.45 5.299 32.215

Diploneis sp. 2356 10.84 27.054 181.094

Eucampia cornuta (Cleve) Grun. 40 0.49 0.196 2.801

Guinardia flaccida (Castr.) Perag. 120 3.45 2.157 12.682

Guinardia striata (Stolter.) Hasle 280 4.90 6.471 32.699

Leptocylindrus danicus Cleve 47144 9.80 524.876 3975.35

Licmophora spp. 2357 3.92 14.887 165.827

Lioloma pacificum (Cupp) Hasle 1280 6.37 19.412 123.175

Lithodesmium undulatum Ehrenb. 230088 7.35 165.726 1647.56

Melosira moniliformis (Müll.) Agardh 680 2.45 7.647 57.229

Melosira nummuloides Agardh 400 2.45 6.471 44.182

Melosira spp. 523 4.41 6.877 46.38

Navicula spp. 11786 34.31 219.11 1089.33

Nitzschia incerta Grun. Peragallo 80 2.45 1.569 10.386

Nitzschia spp. 2357 10.29 36.172 240.81

Nitzschia longissima (Breb.) Ralfs 2357 7.84 31.926 235.23

Odontella mobiliensis(Bailey) Grun. 2309 1.47 12.29 161.91

Paralia sulcata (Ehrenb.) Cleve. 160 0.98 1.176 12.499

Pleurosigma formosum W. Smith 80 3.43 1.961 11.056

Pleurosigma elongatum W. Smith 320 10.29 7.255 28.944

Pleurosigma spp. 320 2.45 2.353 23.03

Proboscia alata (Brightw.) Sundström 2120 13.73 36.67 174.369

Pseudo-nitzschia spp. 99002 41.67 3662.31 11755.24

Rhizosolenia imbricata Brightw. 320 5.39 7.255 37.696

Skeletonema spp. 339437 11.76 7358.56 37707.5

Synedra spp. 80 1.47 0.98 8.365

Thalassionema fraunfeldii(Grun.) Hallegr. 200 6.86 7.451 29.833

Thalassionema nitzschioides (Grun.) 156228 69.61 4266.75 18469.9

Table 4. List of phytoplankton taxa identified in the Kotor Bay, from February 2008 to January 2009.

Analyses were performed on 204 samples from February 2008 to January 2009. Samples were taken on weekly intervals (total number should be 260, but some samples were missed because of weather conditions). Abundances were expressed as cell l-1. MAX: maximum abundance; FR%: frequency of appearance; AVG: average abundance; SD: standard deviation

MAX FR % AVG SD

Meresckowsky

Thalassiosira decipiens (Grun.) Jorg. 3140 11.76 85.564 388.092

Dinoflagellates

Amphidinium spp. 4714 11.27 73.353 440.99

Amphidinium acutissimum Schiller 7849 4.41 42.59 549.69

Dinophysis acuminata Clap. et Lachm 280 1.47 2.352 21.98

Dinophysis acuta Ehrenb. 40 0.49 0.19 2.8

Dinophysis caudata Seville-Kent 120 9.31 5.88 20.16

Dinophysis fortii Pav. 2320 25.49 78.04 317.67

Diplopsalis»complex» 40 1.96 0.78 5.56

Glenodinium spp. 240 2.45 2.35 18.89

Diplopsalis lenticula Bergh 120 7.84 5.098 18.77

Goniodoma polyedricum (Pouchet) Jorg. 280 5.39 4.51 24.86

Gonyaulax spp. 13853 21.57 206.85 1248.26

Gonyaulax digitale (Pouchet) Kof. 120 1.47 1.18 10.44

Gonyaulax polygramma Stein 800 12.75 17.65 71.7

Gonyaulax spinifera (Clap et Lachm) 120 7.84 5.69 21.17

Diesing

Gonyaulax verior Sournia 160 1.96 1.57 13.07

Gymnodinium spp. 25520 50.0 736.89 2773.28

Gyrodinium spp. 2357 7.84 16.46 165.87

Gyrodinium fusiforme Kof. et Sw. 560 10.29 10.59 48.44

Neoceratium carriense Gourret 80 8.33 3.92 13.765

Neoceratium contortum (Gourret) Cleve 80 1.96 0.98 7.36

Neoceratium furca (Ehrenb.) 800 27.94 29.61 75.604

Gomez, Moreira and Lopez-Garcia

Neoceratium fusus (Ehrenb.) 200 15.69 11.57 32.49

Gomez, Moreira and Lopez-Garcia

Neoceratium horridum (Gran) 440 24.02 22.16 53.59

Gomez, Moreira and Lopez-Garcia

Neoceratium hexacantum (Gourret) 120 5.88 3.92 16.85

Gomez, Moreira and Lopez-Garcia

Neoceratium pentagonum (Gourret) 120 3.43 1.96 11.75

Gomez, Moreira and Lopez-Garcia

Neoceratium setaceum (Jörg.) 40 1.47 0.59 4.83

Gomez, Moreira and Lopez-Garcia

Neoceratium trichoceros (Ehrenb.) 80 2.45 1.18 7.85

Gomez, Moreira and Lopez-Garcia

Neoceratium tripos (Müller) 9120 18.14 70 666.93

Gomez, Moreira and Lopez-Garcia

Ornithocercus heteroporus Kof. 40 0.49 0.19 2.8

Oxytoxum adriaticum Schiller 40 0.98 0.392 3.95

Oxytoxum sceptrum (Stein) Schröder 160 9.31 5.88 20.93

Oxytoxum scolopax Stein 120 3.43 1.96 11.75

Phalacroma rotundatum (Clap. et Lachm.) 120 12.25 6.078 17.82

Kof. et Michener

Podolampas elegans Schütt 80 3.43 1.57 8.74

Prorocentrum compressum (Bailey) 120 3.43 2.55 14.36

.Table 4. List of phytoplankton taxa identified in the Kotor Bay, from February 2008 to January 2009.

Analyses were performed on 204 samples from February 2008 to January 2009. Samples were taken on weekly Intervals (total number should be 260, but some samples were missed because of weather conditions). Abundances were expressed as cell l-1. MAX: maximum abundance; FR%: frequency of appearance; AVG: average abundance; SD: standard deviation

MAX FR % AVG SD

Abé ex Dodge

Prorocentrum micans Ehrenb. 2210748 65.69 12578.02 154937.7

Prorocentrum minimum (Pavill.) Schiller 83995 10.29 880.07 7363.9

Prorocentrum scutellum Schröder 320 5.88 7.65 37.197

Prorocentrum triestinum Schiller 360 4.41 5.88 33.41

Protoperidinium spp. 10990 26.96 125.94 803.93

Protoperidinium crassipes (Kof.) Balech 320 29.41 22.55 45.97

Protoperidinium diabolum (Cleve) Balech 1600 27.94 62.55 195.24

Protoperidinium divergens (Ehrenb.) 160 7.35 5.098 20.38

Balech

Protoperidinium globulum (Stein) Balech 320 5.39 5.29 28.55

Protoperidinium pellucidum Bergh 640 2.94 8.82 65.79

ex Loeblich Jr & LoeblichlII

Protoperidinium tuba (Schiller) Balech 160 3.92 2.35 14.12

Pseliodinium vaubanii Sournia 200 5.88 7.65 37.197

Pyrocystis lunula (Schütt) Schütt 40 0.49 0.196 2.8

Pyrocystis spp. 160 4.90 3.53 17.85

Pyrophacus horologium Stein 240 6.86 4.71 21.96

Scrippsiella sp. 1570 5.88 13.38 112.81

Coccolithophorids

Calciosolenia brasiliensis (Lohmann) 4710 20.59 193.86 715.64

J.R. Young

Acanthoica quattrospina Lohmann 4714 3.92 31.63 340.04

Calciosolenia murrayi Gran 5677 8.33 97.33 526.18

Calyptosphaera oblonga Lohmann 5756 22.55 252.75 778.27

Coccolithus walichii (Lohmann) Schiller 12560 33.33 418.55 1479.88

Ophiaster hydroideus (Lohmann)Lohmanr 3140 0.98 17.96 222.69

Rhabdosphaera tignifera Schiller 200 8.33 9.61 34.06

Syracosphaera pulchra Lohmann 192149 32.35 1554.96 1371.2

Silicoflagellates

Dictyocha fibula Ehrenb. 520 11.76 12.75 50.24

Dictyocha polyactis Ehrenb. 80 0.49 0.39 5.6

Octactis octonaria (Ehrenb.) Hovasse. 40 0.98 0.39 3.95

continued

.Table 4. List of phytoplankton taxa identified in the Kotor Bay, from February 2008 to January 2009.

Analyses were performed on 204 samples from February 2008 to January 2009. Samples were taken on weekly Intervals (total number should be 260, but some samples were missed because of weather conditions). Abundances were expressed as cell l-1. MAX: maximum abundance; FR%: frequency of appearance; AVG: average abundance; SD: standard deviation

nitzschioides with a frequency of 69.61%, Pseudo-nitzschia spp. (41.67%), Chaetoceros affinis (11.8%), Skeletonema spp. (11.76%), Coscinodiscus spp. (11.33%), Navicula spp. (34.31%) and Diploneis spp. (10.84%). The dominant dinoflagellates were Prorocentrum micans, with a maximum frequency of 65.69%, Protoperidinium crassipes (29.41%), P. diabolum and Neoceratium furca (both with a frequency 27.94%), Protoperidinium spp. (26.96%), and Dinophysis fortii (25.49%). Frequent coccolithophorids (>20 |jm) were Calciosolenia brasiliensis (20.59%), Calyptosphaera oblonga (22.55%), Coccolithus walichii (33.33%) and Syracosphaera pulchra (32.25%; Table 4).

Among the dinoflagellates, six species that produce toxins were recorded: Dinophysis acuminata, D. acuta, D. caudata, D. fortii, Phalacroma rotundatum, Prorocentrum minimum. Toxic species from the genus Dinophysis were found in up to 33.3% (68 samples) of the total samples (204 samples), and Prorocentrum minimum was found in 10.3% of the samples (Table 4). Maximum abundance of Dinophysis acuminata was 280 cells l-1, D. acuta 40 cells l-1, D. caudata 120 cells l-1, D. fortii 2320 cells l-1, Phalacroma rotundata 120 cells l-1 and Prorocentrum minimum 8.4x104 cells l-1 (Table 4). Dinophysis acuminata and D. acuta were typical of the summer period, D. acuminata being present in June and

July, while D. acuta in August. D. fortii and Phalacroma rotundatum were present during the whole sampling period.

The graphical representation of clusters provided a differentiation between months and revealed two main groups, each of which includes subgroups (Figure 5). A first group included February, March, April and May, with the greatest similarity between March and April. The other months formed the second group where the greatest similarity was found between August and September. The grouping of February-May was a result of the high level of precipitation and the increased input of nutrients. The high similarity found between the months March-April, June-July and August-September

demonstrated evident seasonality in appearing of species adapted on the weather conditions (Figure 5).

The dendrogram for different taxa versus their average abundances showed two major cluster groups of which one comprised sub-clusters (Figure 6). The species Prorocentrum micans, Thalassionema nitzschioides, Gymnodinium spp., Pseudo-nitzschia spp., Coccolithus walichii and Navicula spp. formed one cluster group where the highest similarity was between Prorocentrum micans and Thalassionema nitzschioides (the frequency of these two species was similar: 65.69% and 69.61%, (Table 4) and between Coccolithus walichii and Navicula spp. Within the second cluster group, the highest similarity was found between Protoperidinium average

- September

- August

- October

- July

- June

November ±

December ^

January

February

50 60 70 80 90 100

Similarity

Figure 5. Hierarchical cluster dendrogram for the different months versus the absence or presence of species (group average of the Sorensen index of similarity).

- Proroceiitrnm nil. ins

- Thalassionema liitzscliinirfes

- Gyimiotliiiiiiin spy.

- Psendo-nitzs cilia spy

- CDCCDlithllS L lli'llli

_ Navicula spy

- Syracospliaera pulchra

- Protopeiidjimim (haliohmi

- Gonyaulax spp

- Protnperiiliiunm crassipes

- Neoc .-T itimii homchun

- I'"1.-i.i' '■i iniuiL fmca

- Protopemhimmi spp

- Calciosolenia brasiliensis

- Dinophysis foi hi

- Calyptosphaera oljlonga

Similarity

Figure 6. Hierarchical cluster dendrogram for the different species according to phytoplankton abundance. We used 16 taxa with a frequency greater than 20% (group average of the Bray-Curtis index of similarity).

crassipes and Neoceratium horridum. This pattern showed that the species grouped according to their frequency of appearance (Figure 6, Table 4).

The graphic representation of clusters on a two-dimensional MDS plot showed the presence of the most frequent species, with a frequency of appearance greater than 10%, during the months (Figure 7). In the MDS plots,

i'sctido-nitisclmi spp.

1 X Stress: 0,07

VIII VI VII

II V 1(1 ®

Navicuia spp.

1 X Stress: 0,07

>% W VIII VI VII

F v 111 ®

Thalassionetna nitzschioides

1 X Stress: 0,07

xi lx x VIII # #

Proboscis» aliita

1 X Stress: 0,07

>% * VI

<$>* ®

Neoceriitium furcii

Thalassionema nitzschioides was more abundant in the warmer period (June and July) while Pseudo-nitzschia spp. was presented in higher frequency in April (Figure 7a,). Neoceratium furca was presented in the warmer period while Neoceratium horridum was noticed in warmer and colder period. Prorocentrum micans increased in July, while Dinophysis fortii increased in May (Figure 7b).

C'occolithus walk hii

* X Stress: 0.07

@ a iiSv

Neoceratium horridum

» N Stress: 0,57

# V VII

Diuciphy.sis foitii

< X Stress: 0,07

X!tx 50 VIII VI VII

N <2> 111 IV

Prorocentrum micans

I X Stress: 0,07

wtK M VIII VI #

II V III IV

© X Stress: 0,07

>% * VIII VI VII

II V III IV

Syrachosphaera pulchra

! • Stress: 0,07

xilx XI VI

III IV

('nK'io.solruiii brasilit'iisis

♦ X Stress: 0.07

Xtx a VIII • VII

i iv V

Cidyptosphaeru oblonga

1 X Stress: 0,07

xilx M VIII VII

II ® III №

Figure 7. MDS ordinations of the sampling months based on the abundances of 12 phytoplankton taxa represented as superimposed bubbles increasing in size with the increasing abundance.

4. Discussion

The Boka Kotorska Bay is a semi-enclosed region with no strong water sources from streams or underground springs, except during the precipitation season, which is higher in the late winter and spring then in autumn. In this period, streams and springs have an influence on the physical, chemical and biological dynamics of the seawater. This region is different from the northern part of the Adriatic Sea, which receives significant freshwater inputs during all year that have a marked positive impact on productivity [36,37].

Due to the high stratification during most of the research, salinity had a high influence on phytoplankton growth. Therefore, the correlation between salinity on one side and phytoplankton abundance and dinoflagellates and green nanoflagellates on other was significantly positive.

Concentration of nutrients in the Boka Kotorska Bay was generally high during the investigated period and favorable for phytoplankton development. In the Adriatic Sea [4,10], phosphate was detected as a limiting factor all year round and nitrogen sporadically in the summer. Although NO3- is generally considered to limit primary productivity in most of the world's oceans, some studies

[38] have suggested the Mediterranean Sea may be an exception. In a study of the south-eastern Mediterranean

[39], all the PO43- was removed from the upper water column during the winter phytoplankton bloom.In the middle Adriatic Sea [40] phosphate rather than nitrate is often the limiting nutrient. Phosphate concentrations in the current study were higher than those in the Zrmanja estuary [4] and the eastern Mediterranean [7], characterized as oligothrophic areas. Phosphate concentration showed no significant correlation with salinity or temperature, suggesting that that phosphate is not from one source but instead is a product both of the decomposition of organic material in the upper reach, as well as from anthropogenic sources. Phosphate concentration and phytoplankton abundance on one side and small dinoflagellates on other was significantly positive correlated in the current study suggesting that phosphates limit productivity in the Adriatic Sea. In contrast, Polat [7] found a significantly negative correlation between these parameters. Positive significant correlation between nitrate and salinity indicates that the low content of nitrates in fresh water is being discharged into the Kotor Bay. In other eastern Adriatic estuaries, salinity and nitrates show negative correlations [4,12] and point to an influence of river runoff during periods of high precipitation. In the period of higher phytoplankton abundance the nitrates were generally lower due to the adoption of nitrate by the phytoplankton.

Phytoplankton seasonality (as indicated by chlorophyll a concentration) is generally characterized by maximum levels in winter and minimum levels in summer [21,41]. In this study, however, the maximum chlorophyll a concentration was recorded during summer (July), likely due to low river-runoff during summer. Therefore remineralization processes and sewage discharge are considered the most important nutrient sources in this system. The same was noticed in the coastal north-western Mediterranean [42]. The present result is different from the results recorded in the Zrmanja estuary [4] in the south-eastern Adriatic [19], where a chlorophyll a peak was noticed in late winter and spring when the water column is rich with regenerated nutrients and solar radiation is increasing.

The chlorophyll a values in this study were higher than those in the more saline and less nutrient-enriched waters of the north-eastern coastal Adriatic [10], the eastern Mediterranean [6], and coastal north-western Mediterranen [43].

The maximum phytoplankton abundance in this study was similar to the values found in the northeastern Adriatic Sea (Lim Bay and Zrmanja Bay) [4,44], but differ from phytoplankton abundance in the northwestern Adriatic Sea [12], which is influenced on its north-western end by two important rivers (Po and Adige). Along with the wind stress, these two rivers modify local circulation and vertical structure of the water column. Phytoplankton abundance in the current study was higher than abundance in the coastal northeastern Mediterranean [45].

Diatoms dominated throughout almost all of the investigated period and were most abundant in late winter-early spring, which has been previously recorded in the northern Adriatic Sea [11] and in the southwestern part of Adriatic [46]. Diatom domination in late winter-early spring most likely reflects their particular ability to survive relatively more turbulent conditions. For north-western Mediterranean [47] it was mentioned that diatoms dominance is typical of coastal waters. On the contrary, in offshore waters phytoplankton assemblages is dominated by coccolithophorids.

A peak of dinoflagellates appeared in summer, likely as a consequence of decreased concentration of available nutrients and the presence of reduction of the mixing of nutrients regenerated in the sediments with the warmer, upper layers of the water column. Therefore, the lower supply of available nutrients favoured dinoflagellates in summer. Similar results occurred in the middle of the Adriatic Sea [13]. However, this study differs from the eastern Mediterranean [5] where dinoflagellates were more abundant in winter and spring, whereas diatoms were dominant in summer. In this study, the most

noticeable peak of dinoflagellates was detected in July; therefore, a positive significant correlation was found between dinoflagellates' abundance and temperature. The same situation was noticed by Morton et al. [48].

The pennate diatom Thalassionema nitzschioides was the most common species in this study. T nitzschioides is common, well known species in the Adriatic Sea, especially in nutrients enriched waters [44]. The presence of pennate diatoms such as Pseudo-nitzschia spp. was frequent, as observed in the northern Adriatic Sea by Bosak et al. [44] and Totti et al. [49], in the middle Adriatic by Totti et al. [13], and the north-eastern Mediterranean Sea by Balkis [50]. The occurrence of the genus Pseudo-nitzschia was described by some authors from different parts of the Adriatic Sea (for the middle part by Buric et al. [4], for the southern part of the basin by Caroppo et al. [46], and by Totti et al. [13] for the middle part). This genus should be monitored in the future due to the potential of some species to produce domoic acid. No data concerning the domoic acid concentration in this area or any reports of toxicity events exists. Therefore it is unclear whether the high abundances of these species recorded in this study had an impact on the shellfish farming activities in this area.

The eutrophic centric diatom Skeletonema spp. was present throughout most of the year. A similar situation was recorded in the northern Adriatic [44] for Skeletonema marinoi, and in the north-eastern Mediterranean [8] for Skeletonema costatum.

The analyses of the phytoplankton assemblages showed the appearance of species that had already been noticed in the Kotor Bay [23] with some differences in the dominance of some species. Numerous species that prefer nutrient-enriched areas were observed in the current study, including Chaetoceros affinis, Guinardia striata, Leptocylindrus danicus, Skeletonema spp., Nitzschia longissima, Pseudo-nitzschia spp. and Thalassionema nitzschioides. Species that prefer nutrient-enriched water were also recorded in the northern Adriatic Sea [10,12], the eastern Adriatic [51] and the middle Adriatic [13], also with differences in their abundance and frequency of appearance.

The presence of dinoflagellates is important because some are known to produce toxins. For example, this study revealed the toxic dinoflagellate Dinophysis forti occurred at abundances as high as 2.4*103 cells l-1. This is serious because even at low concentrations of just over 1000 cells l-1 dinoflagellate Dinophysis spp. is harmful to humans [52]. A few papers reported on the occurrence of toxic dinoflagellate species in the eastern Adriatic Sea, e.g. in the Mali Stone Bay [53], and Istrian areas [54], in which shellfish breeding was analyzed concerning diarrhetic shellfish poisoning (DSP). It was

noticed that the dinoflagellates Dinophysis fortii and D. caudata were toxic. Nincevic et al. [55] also found that five Dinophysis species (D. fortii, D. rotundata, D. caudata, D. sacculus and D. tripos) were associated with toxicity events in the Croatian waters of the Adriatic Sea. Caroppo et al. [26] reported that about 12 Dinophysis species are responsible for DSP in the southern Adriatic Sea.

The presence of the potentially toxic and toxic phytoplankton species such as Pseudo-nitzschia spp. and Dinophysis species indicate the importance of monitoring and research in the case of possible occuring of algal blooms in this area where is present active shellfish farming activities.

The autumn community is also characterized by coccolithophorids. Positive correlation among coccolithophorids and salinity confirmed that coccolithophorids develop in water with higher salinity and usually in deeper layers (5-10 m). In the Krka estuary [51 ], coccolithophorids defined the winter-spring phytoplankton.

Green nanoflagellates were the most abundant nanophytoplankton fraction in this study. The second most abundant group was small dinoflagellates. Positive significant correlation between green nanoflagellates and small dinoflagellates with phytoplankton abundance shows significant contribution of these small fractions to phytoplankton density. In Krka estuary [51] nanophytoplankton was mostly comprises of small dinoflagellates.

In this study, which concerned the south-eastern Adriatic, diatom and dinoflagellate species represented 43.6% and 46.4% of the total phytoplankton species. This record is similar to the results found for the northern Adriatic Sea [56] and the north-western Mediterranean Sea [57], but it differs from the south-western Adriatic [46,47], where diatoms represented the majority of the population (44.3%) while dinoflagellates reached 10.3%. The presence of 51 diatom taxa in the Kotor Bay is significantly lower than in the northern Adriatic Sea, but the presence of dinoflagellate taxa (48) was higher [58]. When our cluster analyses are compared with the cluster analysis from Baytut et al. [59], both show a similarity between the months and taxa are grouped according to their seasonal adaptations. Our MDS presentation for the toxic dinoflagellate Dinophysis fortii shows the presence of this species in late spring, which is different to the results of Nincevic et al. [55] where these taxa was present in late summer (Figure 6). Sidari et al. [60] and Blanco et al. [61] noticed that even Dinophysis species mostly occurred during warmer periods, and that they differed in the timing of their appearance.

5. Conclusions

Phytoplankton production depends on abiotic factors such as salinity, temperature, light (influenced by turbidity), and nutrients. Due to the high variations in these factors and higher water dynamics of this ecosystem, it is very difficult to distinguish whether this growth is a result of a natural factor or an anthropogenic activity.

In this study, diatoms dominated throughout the entire research period while dinoflagellates abundance was the highest in summer period, due to an isolate event of one species, Prorocentrum micans. The high frequency of the eutrophic species Thalassionema nitzschioides [43] and peaks of phytoplankton abundance in the order of up to 106 cells l-1 in summer both suggest increased anthropogenic influences in the Kotor Bay. The most important and alarming finding is that the abundance of the toxic species Dinophysis fortii was greater than the values considered benign. The presence of diatom Pseudo-nitzschia spp. is also important due to the possibility of producing domoic acid. Thus, in the future, this region may become a eutrophic area where toxicity

events can be expected, so sustained monitoring is advisable.

The contribution of the aquaculture in the Montenegrin national economy is insignificant. Although the economic value is currently very low, the aquaculture seems to have a great potential for future development. Therefore modernisation of the sector, diversification in production, and training and education, could all provide this potential.

The present results of phytoplankton assemblages and distribution provide valuable information for this part of the south-eastern Adriatic Sea where data is currently absent. However, hopefully more research will be conducted in this area in the future, thus providing reliable data for comparison.

Acknowledgements

This study was funded by the Norwegian Cooperation Program on Research and Higher Education with the countries in the Western Balkans: Marine science and coastal management in the Adriatic, Western Balkan. An education and research network (2006-2009).

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