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Seasonal variations in the phytoplankton and nutrient dynamics in the neritic water of Büyükçekmece Bay, Sea of Marmara NESLI˙HAN BALKIS* DEPARTMENT OF BIOLOGY, FACULTY OF SCIENCE, ISTANBUL UNIVERSITY,
VEZNECILER/ISTANBUL, TURKEY
*CORRESPONDING AUTHOR:
[email protected]
The phytoplankton species and seasonal variations of the nutrients were investigated in Büyükçekmece Bay, Sea of Marmara. The samples were collected monthly from different depths at five stations in Büyükçekmece Bay, from April 1998 to March 1999. A total of 125 phytoplankton species belonging to seven classes were identified, three of which were new to Turkish seas. The maximum values of total phytoplankton occurred at 0.5 m depth (292 103 cells 1–1) in March, for it was in this month that the diatom Skeletonema costatum bloomed. Dinoflagellates were present throughout the year and represented the majority of the population (52%), followed by diatoms (40%). The highest cell concentrations of dinoflagellates were recorded in May, and those of diatoms in March. Throughout the year, the amounts of nitrate + nitrite, phosphate and silicate were 0.05–10.79 µgat N l–1, 0.16–1.06 µg-at P l–1 and 1.10–35.23 µg-at Si l–1, respectively. The highest and lowest N:P ratios were found to be 11 at 30 m in April and 0.17 just below the surface in June, respectively. N:P ratios were below the normal value of 16:1, and N was a limiting nutrient. These findings show that the region examined is oligotrophic in nature.
I N T RO D U C T I O N Büyükçekmece Bay is part of the Sea of Marmara, which is a small basin (size ~70 250 km, surface area 11 500 km2 and maximum depth 1390 m) located between the continents of Europe and Asia (Beșiktepe et al., 1995). Forming the ‘Turkish Straits System’ along with the Bosphorus and the Dardanelles (Ünlüata et al., 1990), the Sea of Marmara is a semi-enclosed basin and has been subject to considerable human use and influence for many years. It connects to the Black Sea through the Bosphorus in the north-east and to the Aegean Sea via the Dardanelles in the south-west. The basin is occupied by two distinctly different water masses throughout the year: one is the brackish waters (22–26 p.s.u.) of Black Sea origin, forming a relatively thin surface layer (10–15 m thick) with a mean residence time of ~4–5 months, and the other is the subhalocline waters of Mediterranean origin (38.5–38.6 p.s.u.) separated from the former by a sharp interface (pycnocline) ~10–20 m thick (Ünlüata et al., 1990; Tug˘ rul and Polat, 1995). Because of the large
volume of water inflow from the adjacent Black Sea (~600 km3) into the relatively small upper layer volume (~225 km3) of the Sea of Marmara, the upper layer ecosystem of the latter has been influenced to a large extent. The biochemically modified surface water of the south-western Black Sea in the Bosphorus region evolves from alongshore currents coming from the north-western coastal margin (Polat and Tug˘ rul, 1995). During recent decades, these waters have become polluted by river (mainly the Danube) and wastewater discharges (Bologa et al., 1981). The chemical oceanography of the Sea of Marmara is significantly influenced by the biochemistry of the Black Sea and the Aegean Sea. In the upper euphotic zone, concentrations of nutrients are relatively low and show seasonal fluctuations that reflect the photosynthetic activity (Baștürk et al., 1986). Since primary production is always limited to the less saline upper layer (15–20 m) of the Sea of Marmara, the subhalocline waters of Mediterranean origin are always rich in nutrients (Polat et al., 1998).
Journal of Plankton Research 25(7), © Oxford University Press; all rights reserved
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During the last three decades, dramatic changes have occurred in the Black Sea ecosystem as a result of both human and natural pressures (Bologa et al., 1995). Since the Marmara upper layer water is renewed at least twice a year by the Black Sea inflow, similar modifications have been observed in the ecosystem of the former (Kocataș et al., 1993). There are detailed studies on the hydrochemical and physical oceanography of the Sea of Marmara. However, to the authors’ knowledge, there are few on the seasonal variability of phytoplankton in this region (Uysal, 1987, 1996; Aubert et al., 1990; Öktem, 1997; Balkıs, 2000). Therefore, this study was designed to establish the seasonal variations in nutrients, to determine the composition of the phytoplankton species in this area and to report, if any, species that would be new to Turkish waters.
METHOD Büyükçekmece Bay is located in the north-east of the Sea of Marmara. It remained connected to Büyükçekmece Lake until 1985. That year, the connection was blocked by a barrier (11.4 m in height) in order to meet the need for fresh water in Istanbul (Meriç, 1986, 1992). Since then, the Büyükçekmece Dam Lake has had no effect on the dynamics of the bay. This bay has a strong and permanent salinity stratification created by the low-saline waters of Black Sea origin, flowing over the highly saline waters coming from the Mediterranean. The deepest point (40 m) of the bay is where it connects to the open sea. The physico-chemical parameters of the five stations where the study has been carried out are similar to one another; therefore, only the mean of the values obtained from these five stations is given. Water samples for phytoplankton examination and for physical and chemical analyses were collected monthly from different depths (0.5, 5.0, 10.0, 15.0, 20.0 and 30.0 m) at five stations in Büyükçekmece Bay (Figure 1). The process lasted a year, from April 1998 to March 1999. For identification of the species, horizontal and vertical samples from each sampling station were collected with a 55 µm plankton net. For physico-chemical analyses and quantitative phytoplankton analyses, a 3 l water sampler with a thermometer was used. The samples were fixed with Lugol’s iodine solution. Then, neutral formaldehyde was added until a concentration of 4% was reached. Samples were settled and the upper layer was removed by siphoning and counted in a Sedgwick–Rafter cell, using a light microscope. The results of countings were summarized as cells per litre (Semina, 1978). The samples were observed by means of an inverted phase-contrast microscope
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equipped with a microphotosystem at a magnification of 400. Small forms of doubtful taxonomic classification were not added to the list and counted. Species were identified using a range of references (Lebour, 1930; Cupp, 1943; Trégouboff and Rose, 1957; Hendey, 1964; Sournia, 1968, 1986; Steidinger and Williams, 1970; Drebes, 1974; Taylor, 1976; Rampi and Bernhard, 1978, 1980; Dodge, 1982; Ricard, 1987; Balech, 1988; Delgado and Fortuno, 1991; Hasle and Syvertsen, 1997; Steidinger and Tangen, 1997; Throndsen, 1997). The Mohr–Knudsen method (Ivanoff, 1972) was used for measuring salinity values, and the Winkler method (Winkler, 1888) for measuring dissolved oxygen (DO). In the estimation of diversity, the most stable index of Shannon–Weaver was preferred (Zar, 1984). Water samples for nutrients were put into polyethylene bottles and frozen at –20ºC for further laboratory analyses. Nitrate + nitrite concentrations were analysed using an autoanalyser. Phosphate, silicate and chlorophyll (Chl) a analyses were performed using a spectrophotometer according to the method introduced by Parsons et al. (Parsons et al., 1984).
R E S U LT S Hydrobiological data During the course of this study, the mean water temperature went through a seasonal cycle characterized by a minimum of 6.8°C ( January) and a maximum of 23.5°C ( July) (Figure 2a). The temperature measured at one station did not vary significantly from that at another. The variations in surface temperatures were caused by atmospheric conditions. It was determined that in spring and summer, sudden temperature changes took place between the depths of 15 and 30 m, and that this change was not felt much due to vertical circulation in autumn and winter. The increase in temperature at the depth of 30 m indicated that typical Mediterranean water was dominant at this point. Salinity values ranged from 19.70 ( July) to 37.34 p.s.u. (September) (Figure 2b). It was found that less saline water from the Black Sea via the Bosphorus is effective at depths that are close to the surface. Every month, salinity was noted to increase from the surface to the bottom, reaching its highest value at a depth of 30 m due to the Mediterranean current. After 20 m, a sudden increase in salinity was remarkable in spring and summer, indicating the presence of a halocline layer. In autumn and winter, it was determined that an intermediate layer did not form with respect to vertical salinity change, and that salinity showed a similar distribution at all depths. DO values varied between 2.18 (October) and 11.95
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PHYTOPLANKTON AND NUTRIENTS OF BÜYÜKÇEKMECE BAY
Fig. 1. Research stations in Büyükçekmece Bay.
mg l–1 (May) (Figure 2c). The amount of oxygen at the depth of 30 m was found to be very low. This was due to excessive oxygen consumption during the decomposition of detritus, which is produced as a consequence of primary production in the upper layer and biochemical reactions occurring in the deeper layer. On the surface, the water is usually oversaturated, due to the exchanges with the atmosphere. However, the oxygen present in the water on the surface does not usually sink down to the bottom. Because of the limited vertical exchanges among water masses, this situation becomes critical, particularly during spring and summer. Throughout the year when the research was conducted, the amounts of nitrate + nitrite, phosphate and silicate were 0.05 ( June)–10.79 µg-at N 1–1 (April), 0.16 ( July)–1.06 µg-at P l–1 (September) and 1.10 ( July)–35.23 µg-at Si l–1 (April), respectively (Figure 2d–f ). The consumption of nutrients in the upper layer was determined to be higher. The highest and lowest N:P ratios were 11 at 30 m in April and 0.17 on the surface in June. N:P ratios show an elevation in autumn and winter. Values in intermediate
layers are higher due to the interference occurring during this period. November and December are when the increase becomes remarkable. This period is also characterized by a significant decline in the abundance of total phytoplankton. According to Tug˘ rul and Polat (Tug˘ rul and Polat, 1995), low levels of inorganic nutrient salts which come from the Black Sea enter the Sea of Marmara between spring and autumn; however, in the early winter, there seems to be an increase in nutrient level, a result that is in accordance with the findings of this study. Compared with the surface, the N:P ratio is considerably higher in deep waters, and this is in reverse proportion to DO content. As proposed by Stefanson and Richards, N:P ratios at such depths are below the normal value of 16:1, and N is a limiting nutrient (Stefanson and Richards, 1963). In autumn and winter, winds cause the water to become rough. This is how stratification is broken up, and the water from the bottom comes up to the surface. Such a phenomenon is important for the transport of nutrients from the surface of sediment to the upper strata, where there is more photosynthetic activity.
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c
d
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April1998 May June July
15
15
20
20
25
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30
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August Septembe r Octobe r November Dece mber January 1999 February March
e
f
Fig. 2. (a–f) Vertical profiles of physico-chemical parameters in the sampling stations of Büyükçekmece Bay.
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Chlorophyll
PHYTOPLANKTON AND NUTRIENTS OF BÜYÜKÇEKMECE BAY
a
0 5
April 1998 May June
10 Depth(m)
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September October Nove mber
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December January1999 Februa ry
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March
30 Fig. 3. Annual variations of Chl a (µg l–1) according to depth.
In this study, phytoplankton biomass (Chl a) was between 0.05 (December) and 8.50 µg l–1 ( January) (Figure 3). The lowest values of Chl a were observed in October–December with the decline in cell number.
Phytoplankton composition and succession A total of 125 microalgae, one cyanophycean, 65 dinoflagellates, two chrysophyceans, three dictyochophyceans, 50 diatoms, one euglenophycean and three prasinophyceans were identified during the course of this study. Of these, three species [Torodinium sp., Dinobryon balticum (Schütt) Lemmermann and Gyrosigma fasciola (Ehrenberg) Cleve] were new to the Turkish seas, and so were 56 species to the Sea of Marmara. The three species new to Turkish seas are marked with one asterisk and 56 species new to the Sea of Marmara with two asterisks in Table I. There are only a few studies on the phytoplankton species in Büyükçekmece Bay. The fact that the region had remained almost untouched until this present research was performed might explain the reason for the many new finds reported here. Mean values given in this study are common to all the stations, since the number of individuals of species found at one station did not vary significantly from that at the others. Throughout the year, total phytoplankton reached its maximal values at a depth of 0.5 m (292 103 cells l–1) in March (Figure 4), followed by those at the depths of 15 m (188 103 cells l–1), 5 m (170 103 cells l–1) and 10 m (139 103 cells l–1), respectively. Skeletonema costatum and Cylindrotheca closterium played a very important role in
this increase. March was the month when S. costatum reached an individual number of 250 103 cells l–1 at 0.5 m, 111 103 cells l–1 at 5 m, 96 103 cells l–1 at 10 m, 130 103 cells l–1 at 15 m, 15 103 cells l–1 at 20 m and 9.5 103 cells l–1 at 30 m (Figure 5). Cylindrotheca closterium, another important species seen in this month, possessed a maximal abundance at 15 m (43 103 cells l–1). This is followed by the depths of 5 m (35 103 cells l–1), 10 m (27 103 cells l–1), 0.5 m (23 103 cells l–1), 20 m (18 103 cells l–1) and 30 m (3 103 cells l–1) (Figure 5). Also during this month, a significant decrease in the number of phytoplankton was noticed at a depth of 20 m (37 103 cells l–1) and 30 m (15 103 cells l–1). May was another important month in which total phytoplankton increased (Figure 4). Especially at depths of 5 m (113 103 cells l–1), 20 m (67 103 cells l–1) and 30 m (77 103 cells l–1), dramatic elevations caused by dinoflagellates were detected. Of these, Prorocentrum scutellum and Prorocentrum micans were present in large amounts at all depths, whereas Gymnodinium sanguineum was only found at 20 and 30 m. The third peak of the year was observed in September, when Eutreptiella sp. (59 103 cells l–1) and Leptocylindrus danicus (15 103 cells l–1) showed marked concentrations at 0.5 m. April was the month with the most species (70 species), and November and January were the months with the fewest (44 species). Dinoflagellates were the most copious component of the population (52%), followed by diatoms (40%). The ‘others’ (Cyano-, Chryso-, Dictyocho-, Eugleno- and Prasinophyceae) formed only 8% of the whole population. Dinophyceae were superior to the other classes in terms of diversity and abundance. The most common genera from the Dinophyceae were as follows: Ceratium Schrank, Dinophysis Ehrenberg, Diplopsalis Bergh, Gymnodinium Stein, Noctiluca Suriray, Phalacroma Stein, Prorocentrum Ehrenberg, Protoperidinium Bergh and Scrippsiella Balech ex Loeblich III. Protoperidinium, Dinophysis and Ceratium were represented as 18, 10 and 9 species, respectively. Dinophyceae were the most common in April (42 species) and the least common in January (19 species). Prorocentrum micans and P. scutellum were in abundance at all the stations during the whole period of this study. These species were followed by Ceratium furca, Ceratium fusus, Ceratium tripos, Diplopsalis lenticula, Protoperidinium divergens and Scrippsiella trochoidea. Bacillariophyceae were the second important class in terms of the distribution and abundance of species. Cerataulina H.Peragallo, Chaetoceros Ehrenberg, Coscinodiscus Ehrenberg, Cylindrotheca (Ehrenberg) Reimann & Lewin, Ditylum (T.West) Grunow in Van Heurck, Pseudonitzschia H.Peragallo in H. & M.Peragallo and Skeletonema Greville were the most common genera of this class. The
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Table I: List and frequency distribution of phytoplanktonic taxa in Büyükçekmece Bay Species
A
M
J
J
A
S
O
N
D
1998
J
F
M
–
–
1999
CYANOPHYTA CYANOPHYCEAE **Oscillatoria sp.
–
–
–
–
–
–
V
–
–
–
CHROMOPHYTA DINOPHYCEAE **Alexandrium minutum Halim
C
V
X
R
–
–
–
–
–
–
A
R
**Ceratium candelabrum (Ehrenberg) Stein
X
–
–
–
–
–
–
–
–
–
–
–
Ceratium furca (Ehrenberg) Clap.&Lach.
V
V
V
V
V
V
V
V
V
R
R
R
Ceratium fusus (Ehrenberg) Dujardin
A
V
V
V
V
V
V
V
A
A
V
V
**Ceratium longirostrum Gourret
X
–
–
X
–
–
–
–
–
–
X
–
Ceratium macroceros (Ehrenberg) Vanhöffen
–
–
–
–
X
X
X
–
–
–
–
–
Ceratium minutum Jörgensen
C
X
–
X
–
–
–
–
–
–
–
–
Ceratium pentagonum Gourret
X
–
–
–
–
–
–
–
–
–
X
–
–
–
–
–
–
C
V
V
A
–
–
–
**Ceratium trichoceros (Ehrenberg) Kofoid Ceratium tripos (O.F.Müller) Nitzsch
V
V
V
V
V
A
V
A
A
R
V
V
**Ceratocorys armata (Schütt) Kofoid
–
–
–
–
–
–
–
–
–
–
–
X
**Cladopyxis caryophyllum (Kofoid) Pavillard
R
–
–
–
–
–
–
–
–
–
–
–
Dinophysis acuminata Claparéde & Lachmann
–
C
C
R
X
–
–
–
–
–
–
–
Dinophysis acuta Ehrenberg
A
V
V
V
A
V
–
R
A
X
X
X
Dinophysis caudata Saville-Kent
–
–
X
V
V
A
C
V
A
X
–
X
X
R
–
–
–
–
–
–
–
–
X
–
**Dinophysis fortii Pavillard Dinophysis hastata Stein
V
V
V
V
X
–
X
–
–
–
X
X
Dinophysis odiosa (Pavillard) Tai & Skogsberg
X
–
X
–
–
–
–
–
–
–
X
–
–
–
–
–
–
–
–
–
–
–
X
–
R
–
–
–
–
–
–
–
–
–
–
–
**Dinophysis punctata Jorgensen
–
X
–
–
–
–
–
–
X
–
R
–
**Dinophysis sacculus Stein
X
–
C
R
C
R
–
–
–
–
–
X
**Diplopsalis lenticula Bergh
V
V
V
C
C
V
V
V
A
V
V
V
**Dinophysis ovata Claparéde & Lachmann Dinophysis ovum Schütt
**Gonyaulax grindleyi Reinecke
–
R
A
–
–
–
–
–
–
–
–
–
–
–
–
–
X
C
X
–
–
–
–
–
**Gymnodinium sanguineum Hirasaka
V
V
V
V
C
–
X
R
A
V
R
R
**Gymnodinium simplex (Loh.) Kofoid&Swezy
C
V
R
–
–
–
–
–
–
–
–
–
X
X
–
–
–
–
–
–
–
–
–
X
A
V
–
–
–
–
–
–
–
–
V
C
Gonyaulax monacantha Pavillard
Gyrodinium spirale (Bergh) Kofoid & Swezy **Heterocapsa triquetra (Ehrenberg) Stein Kofoidinium velleloides Pavillard **Lingulodinium polyedrum (Stein) Dodge Noctiluca scintillans (Macartney) Kofoid&Swezy **Ornithocercus quadratus Schütt
–
X
V
A
R
V
R
C
C
–
–
–
R
V
X
V
C
–
–
–
–
–
–
–
V
V
V
A
A
V
V
V
C
X
C
V
R
–
–
–
–
–
–
–
–
–
–
–
Oxyphysis oxytoxoides Kofoid
–
–
–
V
–
V
–
–
–
–
–
–
Oxytoxum scolopax Stein
–
–
–
–
–
R
V
C
C
–
–
–
Phalacroma rotundatum (Clap.&Lach.) Kof.&Mich. C
X
X
A
C
V
C
C
A
A
R
X
Podolampas palmipes Stein
X
–
R
X
–
R
X
–
X
X
–
–
Polykrikos schwartzii Bütschli
X
X
–
X
–
–
X
–
–
–
–
–
Prorocentrum compressum (Bailey)Abe ex Dodge R
–
V
V
V
–
V
V
V
V
R
–
**Prorocentrum cordatum (Ostenfeld) Dodge Prorocentrum micans Ehrenberg
–
–
–
–
A
V
R
–
–
–
–
–
V
V
V
V
V
V
V
V
V
V
V
V
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Table I: Continued Species
A
M
J
J
A
S
O
N
D
1998
Prorocentrum scutellum Schröder
J
F
M
1999
V
V
V
V
V
V
V
V
V
V
V
V
**Prorocentrum triestinum Schiller
C
–
–
V
V
V
V
C
V
–
–
X
**Protoperidinium bipes (Paulsen) Balech
A
V
–
–
–
–
–
–
X
V
X
A
**Protoperidinium brochi (Kofoid&Swezy) Balech
R
C
X
–
R
–
C
R
–
–
–
–
Protoperidinium claudicans (Paulsen) Balech
C
–
–
C
A
R
X
A
C
–
–
– –
**Protoperidinium conicum (Gran) Balech
X
–
–
–
–
–
X
–
–
–
–
Protoperidinium crassipes (Kofoid) Balech
R
–
A
A
X
–
X
–
–
–
X
–
Protoperidinium depressum (Bailey) Balech
V
V
V
V
R
–
X
–
C
V
V
V
Protoperidinium divergens (Ehrenberg) Balech
V
V
V
V
V
V
V
A
C
X
V
V
–
–
–
–
–
–
X
–
–
–
–
–
Protoperidinium granii (Ostenfeld in Paulsen) Balech –
–
–
X
–
–
–
–
–
–
–
–
Protoperidinium leonis (Pavillard) Balech
R
–
X
R
C
A
X
–
–
V
V
X
–
X
–
–
–
–
–
–
–
–
–
–
**Protoperidinium globulum (Stein) Balech
**Protoperidinium mediterraneum (Kofoid) Balech **Protoperidinium oceanicum (Vanhöffen) Balech
–
X
–
R
X
A
X
–
X
–
X
–
**Protoperidinium paulseni Pavillard
–
–
–
–
A
–
–
–
–
–
–
–
Protoperidinium pellucidum Bergh
V
V
V
A
C
–
–
–
–
–
V
V
Protoperidinium pentagonum (Gran) Balech
X
R
X
A
–
–
–
–
–
C
X
–
**Protoperidinium pyriforme (Paulsen) Balech
–
V
–
–
V
V
A
–
–
–
C
X
C
V
V
V
V
V
X
C
X
–
C
R
**Protoperidinium subinerme (Paulsen) Loeblich III –
Protoperidinium steinii (Jörgensen) Balech
–
X
R
–
A
–
–
–
–
–
–
Pyrophacus horologium Stein
–
–
V
R
X
V
A
X
–
–
–
–
Scaphodinium mirabile Margalef
–
–
X
–
–
–
X
–
–
–
–
–
**Scrippsiella trochoidea (Stein) Loeblich III
V
V
V
V
V
V
C
X
R
V
V
A
*Torodinium sp.
–
–
R
X
–
–
–
–
–
–
–
CHRYSOPHYCEAE **Bicosoeaca mediterranea Pavillard
–
–
–
–
R
V
–
–
–
–
–
–
*Dinobryon balticum (Schütt) Lemmermann
X
X
–
–
–
X
–
–
–
–
V
V
Dictyocha fibula Ehrenberg
–
–
–
C
A
X
–
X
V
V
–
–
Dictyocha speculum Ehrenberg
R
R
X
R
–
–
–
R
X
–
–
C
X
–
X
X
–
–
–
–
–
R
X
–
R
DICTYOCHOPHYCEAE
**Octactis octonaria (Ehrenberg) Hovasse BACILLARIOPHYCEAE **Achnanthes brevipes Agardh
–
X
–
–
–
–
–
–
–
–
–
Cerataulina pelagica (Cleve) Hendey
R
X
V
V
V
–
–
A
R
V
A
A
Chaetoceros affinis Lauder
–
–
–
C
R
X
–
–
X
–
R
C
**Chaetoceros constrictus Gran
–
–
–
A
V
X
–
C
X
–
R
R
**Chaetoceros costatus Pavillard
X
–
–
–
–
–
–
–
–
–
–
–
**Chaetoceros curvisetus Cleve
V
V
V
V
X
X
–
–
X
–
–
–
**Chaetoceros danicus Cleve
–
–
–
–
–
–
–
–
A
A
X
X
**Chaetoceros debilis Cleve
–
–
–
–
–
–
–
–
–
V
V
V
Chaetoceros decipiens Cleve
R
–
V
V
V
C
V
V
V
X
X
X
Chaetoceros diadema (Ehrenberg) Gran
–
–
–
–
–
–
–
–
–
A
V
V
Chaetoceros holsaticus Schütt
–
–
–
R
V
X
–
–
–
X
–
–
**Chaetoceros laciniosus Schütt
–
–
–
–
V
–
–
–
–
–
–
–
**Chaetoceros lorenzianus Grunow
X
–
–
–
–
–
–
V
X
–
R
A
**Chaetoceros peruvianus Brightwell
–
–
–
–
–
C
–
–
–
–
–
–
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Table I: Continued Species
A
M
J
S
O
N
D
1998
**Climacosphenia sp.
J
F
M
1999
X
X
–
X
X
R
R
–
X
–
–
–
–
–
–
–
–
–
–
–
V
C
–
–
**Coscinodiscus perforatus Ehrenberg
V
V
V
V
A
V
A
–
V
C
X
–
Coscinodiscus radiatus Ehrenberg
V
V
V
V
V
R
C
V
C
C
V
X
Cylindrotheca closterium (Ehren.) Reimann & Lewin V
V
A
V
V
R
A
V
V
V
V
V
Dactyliosolen fragilissimus (Bergon) Hasle
R
X
A
–
X
A
–
C
V
C
–
–
–
–
–
–
–
–
–
–
–
–
–
X
Ditylum brightwellii (T.West) Grunow in Van Heurck V
Coscinodiscus granii Gough
**Diploneis bombus (Ehrenberg) Cleve
X
X
X
X
R
A
V
V
X
X
–
**Grammatophora marina (Lyngbye) Kützing
X
–
–
–
–
–
–
–
–
–
–
–
**Guinardia cylindrus (Cleve) Hasle
–
–
–
–
–
–
–
–
–
–
–
X
R
A
R
–
–
R
X
X
C
V
X
–
*Gyrosigma fasciola (Ehrenberg) Cleve
X
–
–
–
–
X
X
–
–
–
–
–
**Helicotheca tamesis (Shrubsole) Ricard
–
–
–
–
C
–
–
–
–
–
–
–
Hemiaulus hauckii Grunow in Van Heurck
–
–
–
–
–
V
V
A
–
–
–
–
Lauderia annulata Cleve
–
–
–
–
–
–
–
–
–
–
–
X
Leptocylindrus danicus Cleve
R
X
A
V
V
V
–
X
X
A
–
–
Licmophora abbreviata Agardh
X
–
–
–
–
–
–
–
–
–
–
– X
Guinardia flaccida (Castracane) Peragallo
**Melosira moniliformis (Müller) Agardh
–
–
–
–
–
–
–
–
–
–
–
Navicula sp.
A
V
R
X
–
–
–
–
–
–
C
C
Nitzschia longissima (Brébisson) Ralfs
–
–
–
–
–
–
–
–
–
V
V
–
**Pleurosigma normanii Ralfs in Pritchard
–
–
–
V
A
A
V
R
X
X
–
–
Pleurosigma sp.
–
–
–
–
–
X
–
–
–
–
–
–
Proboscia alata (Brightwell) Sundstrôm
V
R
V
A
A
V
V
C
X
–
–
–
**Pseudo-nitzschia pseudodelicatissima –
–
R
V
V
X
–
–
–
–
–
–
Pseudo-nitzschia pungens (Grun. in P.T.Cleve)Hasle C
(Hasle)Hasle
C
C
C
V
R
X
–
–
C
A
R
Pseudo-nitzschia sp.
V
R
V
A
A
V
V
V
V
A
–
V
Pseudosolenia calcar- avis (Schultze) Sundstrôm
V
X
A
V
V
V
A
V
C
–
X
–
Rhizosolenia setigera Brightwell
–
–
C
–
C
R
–
R
V
V
V
V
Skeletonema costatum (Greville) Cleve
V
X
V
V
V
C
–
V
X
A
V
V
**Striatella unipunctata (Lyngbye) Agardh
R
–
R
–
–
X
X
–
–
–
–
–
Thalassionema nitzschioides (Grunow) Meresch. X **Thalassiosira allenii Takano Thalassiosira angulata (Gregory) Hasle
–
–
A
V
V
A
V
C
–
X
–
–
–
–
–
–
–
–
–
–
–
–
X
–
–
–
–
–
–
–
–
–
X
X
R
Thalassiosira anguste-lineata (Sch.) Fryxell & Hasle –
–
–
–
–
–
–
–
–
V
V
V
Thalassiosira nordenskioeldii Cleve
–
–
–
–
–
–
–
–
–
X
X
X
Thalassiosira rotula Meunier
–
–
–
–
–
–
X
X
V
–
V
–
X
–
–
X
X
V
–
–
–
–
–
R
CHLOROPHYTA EUGLENOPHYCEAE **Eutreptiella sp. PRASINOPHYCEAE **Halosphaera viridis Schmitz
–
–
–
–
–
–
X
R
V
R
X
–
**Pyramimonas grossii Parke
–
–
–
–
X
X
–
–
–
–
–
–
**Tetraselmis sp.
–
–
–
–
–
X
–
–
–
–
X
–
V, very abundant (81–100%); A, abundant (61–80%); C, common (41–60%); R, rare (21–40%); X, present sporadically (1–20%).
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5m
0.5 m 180000 300000
150000 250000
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10 m 200000
140000 175000
120000
150000
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Dinoflagellates
Diatoms
Others
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Fig. 4. Annual variations of phytoplankton groups in the sampling depths.
genera that included the most species were Chaetoceros (12 species) and Thalassiosira Cleve (five species). Bacillariophyceae were the most common in September (27 species) and the least common in the months of May and October (17 species). It was determined that, compared with diatoms, dinoflagellates were dominant between April and September.
The reproduction of phytoplankton greatly decreased between October and December, and this was when zooplankton increased in microscopic studies. Such diatoms as Chaetoceros spp., C. closterium, Rhizosolenia setigera and S. costatum were dominant in the months of January, February and March. In spring, the largest components in the population
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Fig. 5. Annual variations of the most important phytoplanktonic taxa according to depth.
were dinoflagellates (54.2%) and diatoms (41.5%). Among dinoflagellates and diatoms, the most copious were S. trochoidea (7.6 103 cells l–1 at 10 m in April), D. lenticula (7.3 103 cells l–1 at 0.5 m in April), Protoperidinium pellucidum (3.7 103 cells l–1 at 5 m in April),
P. scutellum (80 103 cells l–1 at 5 m in May), G. sanguineum (31 103 cells l–1 at 20 m in May), P. micans (18 103 cells l–1 at 0.5 m in May), Ceratium furca (5 103 cells l–1 at 5 m in May), Protoperidinium bipes (2 103 cells l–1 at 0.5 m in May), S. costatum, C. closterium (43 103 cells l–1
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at 15 m in March), Chaetoceros spp. (13 103 cells l–1 at 5 m in March) and R. setigera (2 103 cells l–1 at 5 m in March). S. costatum (250 103 cells l–1 at 0.5 m in March) showed a remarkable increase in cell number in March. The others formed 4.3% of the whole community. In the summer, the percentage ratio among taxa was essentially unvaried: dinoflagellates (59.3%) and diatoms (33.3%) dominated the community. Along with the abovementioned species, other dinoflagellates and diatoms were also observed during this season: C. fusus (19.3 103 cells l–1 at 20 m in August); Prorocentrum compressum (5.2 103 cells l–1 at 10 m in August), Prorocentrum triestinum (3.7 103 cells l–1 at 0.5 m in August), Cerataulina pelagica (3.8 103 cells l–1 at 0.5 m in August), L. danicus (2.4 103 cells l–1 at 5 m in August) and Pseudosolenia calcar-avis (2 103 cells l–1 at 10 m in July). The others formed 7.4% of the whole community. In autumn, a decrease in the number of species and individuals was noticed. Dinoflagellates were still an important component of the population (50%), followed by diatoms (38.5%). The rest of the population (11.5%) was made up of the remaining species. During this period, the diatom species typical of the last succession stage were common, namely, L. danicus (15 103 cells l–1 at 0.5 m in September), Hemiaulus hauckii (6.2 103 cells l–1 at 10 m in September) and Dactyliosolen fragilissimus (1.7 103 cells l–1 at 5 m in September). A similar increase was detected in the cell number of Eutreptiella sp. (59 103 cells l–1 at 0.5 m in September). In winter, the number of diatoms increased more than it did in the other seasons (42.8%). The predominant species of diatoms in winter were R. setigera (16 103 cells l–1 at 20 m in February), Thalassiosira anguste-lineata (6 103 cells l–1 at 5 m in February), T. rotula (2.8 103 cells
l–1 at 5 m in February) and Chaetoceros spp. (12.2 103 cells l–1 at 5 m in January). Dinoflagellates formed 49.4% of the community, followed by the others (7.8%). Figure 5 shows the changes in the cell numbers of some of the most important taxa at various depths. Despite the presence of certain dinoflagellate species (Alexandrium minutum, Dinophysis acuta, Dinophysis acuminata, Dinophysis fortii, Heterocapsa triquetra, Lingulodinium polyedrum, Noctiluca scintillans, Phalacroma rotundatum, Prorocentrum micans, P. triestinum, S. trochoidea) that are known to be responsible for red tides and other noxious algal blooms in other geographical areas, red tides were not recorded during the sampling period. The results of the diversity index of Shannon–Weaver (Figure 6), employing the monthly estimation of species and cell numbers at chosen depths, revealed that the diversity index of phytoplankton decreased in the bloom periods of the species. The highest diversity index (H) was obtained in August at 0.5 m (H = 3.69), and the lowest in April at 30.0 m (H = 0) and in March at 0.5 m (H = 0.88). The lower values of the diversity index during the months of March, April and May may be explained by the following: the increase in the cell number of Prorocentrum micans and P. scutellum in May, and that of S. costatum and C. closterium in March, and the absence of species at a depth of 30 m in April.
DISCUSSION This study has made it possible to determine a number of phytoplanktonic members of algae from seven classes, namely, Cyanophyceae, Dinophyceae, Chrysophyceae, Dictyochophyceae, Bacillariophyceae, Euglenophyceae and Prasinophyceae. Of these, the dominant ones during
Index of Shannon-Weaver
(m)
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1 0.5 0 A '98
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M
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S
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Fig. 6. Annual variations of the Shannon–Weaver index (H) according to depth.
J '99
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the research period were the Dinophyceae and Bacillariophyceae. It was observed that the number of species and cells of Dinophyceae increased especially in late spring and during the whole period of summer, and that Bacillariophyceae dominated more in winter and early spring. It has been reported that, during summer, the phytoplankton community is dominated by diatoms in eutrophic and semi-enclosed areas (Caroppo and Cardellicchio, 1995). According to Azov, the diatoms were dominant species in the neritic region of the oligotrophic waters of the Levant Basin, and the most abundant diatoms belonged to the genera Chaetoceros, Coscinodiscus and Rhizosolenia (Azov, 1986). So far, a total of 106 species have been identified from the Sea of Marmara. Uysal (Uysal, 1987, 1996) reported 42 species, Aubert et al. (Aubert et al., 1990) 19 species, Öktem (Öktem, 1997) 62 species and Balkıs (Balkıs, 2000) five species new to Turkish coastal waters from the Sea of Marmara. Seven of the 125 taxa determined in this study could not be identified, and were thus classified to genus. Of these seven genera, Torodinium is new to Turkish coastal waters. Trégouboff and Rose reported both Torodinium teredo and Torodinium robustum from the Mediterranean Sea (Trégouboff and Rose, 1957). Gyrosigma fasciola was identified in the Black Sea (Zaitsev and Alexandrov, 1998), and so was Dinobryon balticum, which was also reported to exist in the Baltic, Atlantic, Arctic and Black Sea (Throndsen, 1997; Zaitsev and Alexandrov, 1998). Most of the species identified in Büyükçekmece Bay were neritic, temperate and subtropical in nature. Therefore, it may be considered that the microalgal communities inhabiting this bay are similar to the Levantine Sea and the Aegean Sea. Along with some benthic species belonging to such genera as Pleurosigma, Grammatophora, Navicula and Licmophora, which have adapted to plankton life, marine species (Proboscia alata, Thalassionema nitzschioides, C. fusus), brackish species (Prorocentrum micans, C. closterium) and typical species (S. costatum, Lingulodinium polyedrum) pertaining to the eutrophic areas have also been found in this bay. The shallowness of the basin and suspension of the sediment resulting from the hydrodynamism of this bay most probably account for the existence of these species. Of the spring and autumn peaks noted in the bay, those belonging to the former period occurred in March and May, and that belonging to the latter period was observed in September. It was in confirmation of this finding that the Chl a value was higher during these periods. Over the year, the amount of Chl a varied between 0.05 and 8.50 µg 1–1, decreasing in proportion to the decline of cell numbers between October and December. Ignatiades observed a diatom bloom which
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lasted from October to May, reaching its maximum abundance in February and March in Saronicos Bay (Ignatiades, 1969). A similar diatom bloom was observed in February and March during the course of this study. Uysal reported a maximum abundance of diatoms in January, in the Bosphorus junction of the Sea of Marmara (Uysal, 1996). It was found in this research that the values of temperature, salinity and DO changed according to the months and depths; however, the variations between the five stations were not very significant. At depths between 0.5 and 20 m, the Sea of Marmara is known to be affected by the brackish water coming from the Black Sea via the Bosphorus (Yüce and Türker, 1991). In this study, a similar effect was also observed at these depths and water of Mediterranean origin was detected at a depth of 30 m. It was obvious that vertical mixing was responsible for the slight increase in salinity between the depths of 15 and 20 m. Beșiktepe et al. reported that, during winter and spring, the salinity of the surface water in the Sea of Marmara was slightly higher due to both the circulation caused by the winds and the decline in water coming from the Black Sea (Beșiktepe et al., 1995). In this study, it was determined that the surface water of Büyükçekmece Bay, which is in direct contact with the atmosphere, constantly involved higher DO than did deep water. Quite lower values of DO were observed at lower layers throughout the year, especially between April and December. Of note, the amount of DO at such depths was higher in cold seasons. The DO content of the Mediterranean water decreases as it gets closer to the Sea of Marmara (Yüce and Türker, 1991). The DO content of this water diminishes significantly (2–3 mg 1–1) during its residence period of 6–7 years in the Sea of Marmara. At a depth of 30 m, characterized by lower DO, there were fewer species with low cell numbers. Vertical stratification in spring and summer does not allow the surface water to mix with the deep water (see nutrient distribution in Figure 2d–f ). The effects of eutrophication caused by increased light availability and vertical stability are evident during late spring and summer. This is when peaks of phytoplankton abundance and production have been recorded in many Mediterranean coastal regions. Red tides are also more frequent in these periods of the year (Zingone et al., 1990). During this study, none of the species reached a level of a million per litre, and no red tide was encountered in the area. Koray et al. reported 22 species causing coloration of sea water by reproducing excessively (Koray et al., 1992). Of these, 16 were found during this research, but none of them reached a level high enough to cause coloration. The only species that increased their cell number more than the others were Eutreptiella spp. in
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September, S. costatum and C. closterium in March. However, red tide was observed in the studies carried out in Izmit Bay, part of the Sea of Marmara (Öktem, 1997; Morkoç et al., 2001; Okay et al., 2001). Similar to Büyükçekmece, this bay is a semi-closed, stagnant water body taking excessive wastewater input from sewer systems and nutrients from manure used for agricultural purposes. In another study performed in Izmir Bay, fish deaths were encountered in the period of Alexandrium minutum dominance (Koray, 1994). Of the nutrient elements detected in Büyükçekmece Bay, nitrate + nitrite, phosphate and silicate increased slightly towards the winter months. However, there was not a significant difference between the amounts of those nutrients with respect to the stations and time of year. It was found that deep waters originating from the Mediterranean Sea possessed higher values of nutrients compared with upper waters and that, throughout the year, the amounts of nitrate + nitrite, phosphate and silicate were 0.05–10.79 µg-at N l–1, 0.16–1.06 µg-at P l–1 and 1.10–35.23 µg-at Si l–1, respectively. The very low levels of nutrients in the upper and near-surface waters are a result of the rapid consumption and usage of the upper waters. These waters of Black Sea origin are rich in nutrient elements and in primary production. Coming from the North-east Aegean and entering the deep layer of the Sea of Marmara, the salty waters of the Mediterranean Sea undergo important alterations during their residence of 6–7 years (Polat and Tug˘ rul, 1995; Polat et al., 1998). On passing through the Dardanelles, the waters of Mediterranean origin, poor in nutrients, become rich in nitrate and orthophosphate as a result of the decomposition of particulate organic material in the depths. Mediterranean waters then reach the Bosphorus, where they lose 70–80% of their oxygen. It is in accordance with the above information that, in this study, large amounts of nutrients were recorded in the deep waters of the Sea of Marmara, which come from the Mediterranean. It was also noticed that consumption takes place more slowly in these deep waters compared with the upper layers. It is because of the decomposition of organic material that there are low levels of oxygen in these deep waters rich in nutrients. The biochemical characteristics of the productive upper layer waters of the Sea of Marmara are affected by inputs from the Black Sea. The inputs originating from the city of Istanbul play a secondary role in contributing to the nutrient and organic carbon pool of the Sea of Marmara. Likewise, terrestrial pollutants result in disruption and alteration of the ecological composition only in semi-closed bays where water turnover is limited (Tug˘ rul and Polat, 1995). Nutrient availability, which in open waters is mainly
controlled by water column structure, is in coastal waters strongly influenced by terrestrial inputs (Zingone et al., 1990). Consequently, anthropic factors may play an important role in determining the trophic and structural characteristics of phytoplankton communities in coastal areas. According to Uslu and Saner, the phosphate concentration is 2.25 µg l–1 in coastal waters with initial eutrophication, and can rise to 4.5 µg l–1 in highly eutrophic systems (Uslu and Saner, 1998). An increase in pollutants in this bay may be a factor that will elevate future eutrophication. The findings of this study do not imply eutrophication in Büyükçekmece Bay; therefore, the upper layer of the Sea of Marmara is considered as oligotrophic, as was stated in the study of Akça et al. (Akça et al., 1998). This study has shown that a number of phytoplankton species live in the Sea of Marmara, and they contribute to the biological diversity of the Turkish seas. By determining the distribution of the species according to the seasons, the study has further attempted to find out the relationship between these species and ecological factors.
AC K N O W L E D G E M E N T S The author is grateful to Professor Dr N. Meriç from Istanbul University, Faculty of Science, for all his time and efforts during the course of this study, to Professor Dr T. Koray from Ege University, Faculty of Fisheries, and to Associate Professor Dr E. Okuș from Istanbul University, Institute of Marine Science and Management, for their valuable assistance in confirming the species and in providing related literature. This work was supported by the Research Fund of Istanbul University, project number T-494/180398.
REFERENCES Akça, L., Öztürk, I. and Aydın, A. F. (1998) Istanbul Bog˘azı ve Marmara Denizi alıcı ortam modelleme çalıșmaları. Büyükșehirlerde atıksu yönetimi ve deniz kirlenmesi kontrolu sempozyumu. ISKI, 47–56. Aubert, M., Revillon, P., Aubert, J., Leger, G., Drai, C., Arnoux, A. and Diana, C. (1990) Transfert de Polluants entre La Mer Noire, La Mer De Marmara et La Mer Egee. Mers D’Europe. Etudes Hydrobiol. Chim. Biol., 3, 47 pp. Azov, Y. (1986) Seasonal patterns of phytoplankton productivity and abundance in nearshore oligotrophic waters of the Levant Basin (Mediterranean). J. Plankton Res., 8, 41–53. Balech, E. (1988) Los dinoflagelados del Atlantico sudoccidental. Publ. Espec. Inst. Esp. Oceanogr., 1, 223–310. Balkıs, N. (2000) Five dinoflagellate species new to Turkish seas. Oebalia, XXVI, 97–108. Baștürk, Ö., Saydam, A. C., Salihog˘ lu, I. and Yılmaz, A. (1986) Oceanography of the Turkish Straits. III, Health of Turkish Straits, II: Chemical and Environmental Aspects of the Sea of Marmara. METU, Erdemli-Içel, 86 pp.
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Received on July 1, 2001; accepted on March 28, 2003
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