Estuarine, Coastal and Shelf Science 68 (2006) 593e599www.elsevier.com/locate/ecss

The blooms of a cyanobacterium, Microcystis cf. aeruginosain a severely polluted estuary, the Golden Horn, Turkey

Seyfettin Tasx*, Erdogan Okusx, Aslı Aslan-Yılmaz

Institute of Marine Sciences and Management University Istanbul, Muskule Sk.1, 34470 Vefa-Istanbul, Turkey

Received 1 June 2004; accepted 27 February 2006

Available online 22 May 2006

Abstract

The distribution of toxic cyanobacterium Microcystis cf. aeruginosa in the severely polluted Golden Horn Estuary was studied from 1998to 2000. Microcystis persisted at the upper estuary where the water circulation was poor and values ranged between 2.9� 104 and2.7� 106 cells ml�1 throughout the study. Simultaneously measured physical (salinity, temperature, rainfall and secchi disc) and chemical pa-rameters (nutrients and dissolved oxygen) were evaluated together with Microcystis data. Although the Microcystis blooms generally occur insummer due to the increase in temperature, the blooms were recorded in winter in the present study. The abundance of Microcystis depended onthe variations in salinity and both blooms were recorded below S¼ 2. A moderate partial correlation between Microcystis abundance and salinitywas detected in the presence of temperature, dissolved oxygen and precipitation data (r¼�0.561, p¼ 0.002). The M. cf. aeruginosa abundancewas low in the summer when the salinity was higher than winter. A remarkable increase in the eukaryotic phytoplankton abundance followingthe improvements in the water quality of the estuary occurred, whilst the Microcystis abundance remained below bloom level.� 2006 Elsevier Ltd. All rights reserved.

Keywords: Microcystis aeruginosa; bloom; phytoplankton; estuary; Golden Horn

1. Introduction

The cyanobacteria are found frequently in marine, brackishand freshwater. Similar to marine algal blooms, such as red-tides, cyanobacteria abundance might remarkably increaseand causes blooms. It has been noted that these cyanobacterialblooms may occur due to high nutrient inputs (Carmichael andFalconer, 1993; Rapala et al., 1997). Cyanobacterial toxinsmainly occurring in freshwater are potential risks for publichealth (Eriksson et al., 1990) since these waters are used fordrinking and recreation (Carmichael and Falconer, 1993).The blooms of the cyanobacteria may cause social, economi-cal and environmental problems such as deterioration of thewater quality, toxicity and decrease in aesthetic value ofthe affected water (Carmichael et al., 1985; Angeline et al.,

* Corresponding author.

E-mail address: stas@istanbul.edu.tr (S. Tasx).

0272-7714/$ - see front matter � 2006 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2006.02.025

1994; Watanabe et al., 1996). Most of the Microcystis speciesdominates in the eutrophic waters such as estuaries and occa-sionally form blooms (Yunes et al., 1996). Microcystis hashepatotoxin which are particularly toxic to the liver due toselective transport mechanisms (Repavich et al., 1990; Elderet al., 1993; Humpage and Falconer, 1999). Sommer (1996)reported that the hepatotoxic microcystin produced byMicrocystis aeruginosa is toxic to herbivore zooplankton.

The Golden Horn Estuary is close to the BosphoruseMarmara Sea junction, extending in northwestesoutheastdirection (28 � 970 E longitude, 41 � 020 N latitude) with ap-proximately 7.5 km length and 700 m width and 25� 106 m2

area (Fig. 1). The maximum depth is 40 m at the lower estuaryand the depth decreases towards the upper part. Although thetwo small streams carry freshwater to the estuary, the amountof the flow decreased remarkably by the end of 1990s to3� 105 m3 year�1 (Ozturk et al., 1998). Therefore, the mainsource of the freshwater flowing into the Golden Horn wasrainfall (Sur et al., 2002).

594 S. Tasx et al. / Estuarine, Coastal and Shelf Science 68 (2006) 593e599

STRAIT OF ISTANBUL

(BOSPHORUS)

AlibeyStream

Ka ıthaneStream

Bridge

Bridge

Bridge

Bridge

Semi-openedafter June 2000.

41.25

41.20

41.15

41.10

41.05

41.00

28.90 28.95 29.00 29.05 29.10 29.15 29.20

GOLDEN HORN

500 10000N

SCALE (m)

Fig. 1. The study area and sampling stations.

The pollution had been severely increased by the rise in theindustry and urban development in the Golden Horn Estuarysince 1950s. By the end of 1990s, the estuary became anoxictowards the upper parts. The quality and quantity of the phy-toplankton community decreased towards the upper parts ofthe Golden Horn (Tasx and Okusx, 2003).

By the end of 1990s, the Golden Horn Rehabilitation Pro-ject was initiated. According to this project, all of the surfacedischarges were controlled, the 4� 106 m3 anoxic sediment atthe upper part was removed and the bridge floating on pon-toons was partially opened.

In this study, the abundance of Microcystis cf. aeruginosa andthe relationship of cyanobacterium with the physicochemical

properties and eukaryotic phytoplankton were evaluated at theGolden Horn Estuary during rehabilitation project.

2. Materials and methods

2.1. Study area and sampling procedure

Samples were collected from five stations in the GoldenHorn Estuary. H1 and H2 were located at the lower estuary re-ceiving salty waters of the Bosphorus upper layer H3 was lo-cated at the mid-estuary. H4 was close to the semi-openedbridge and H5 was the station close to the streams (Fig. 1).

M J J A S N D F M A M J J A S O N D J F M A M J J A S O N D0

1000

2000

3000

Abun

danc

e (1

03 ce

lls m

l-1)

5

10

15

20

25

30

Tem

pera

ture

(°C

)

0

5

10

15

20

25

Salin

itiy Microcystis

Temperature

Salinitiy

1998 1999 2000

H5

Fig. 2. The abundance of Microcystis cf. aeruginosa and temperature and salinity in the upper estuary.

595S. Tasx et al. / Estuarine, Coastal and Shelf Science 68 (2006) 593e599

M J J A S N D F M A M J J A S O N D J F M A M J J A S O N D0

1000

2000

3000

Abun

danc

e (1

03 ce

lls m

l-1)

H5

0

20

40

60

80

100

Rai

n (m

m)

1998 1999 2000

Microcystis

Rain

Fig. 3. The abundance of Microcystis cf. aeruginosa and rainfall (the total of 5 days including the last day as the survey date) in the upper estuary.

Samples were collected monthly from May 1998 to Decem-ber 2000 (no data were available in October 1998 and January1999). Temperature and salinity measurements were per-formed by SBE 25 Sealogger CTD probe system. The rainfalldata were provided from Kandilli Meteorological Station.Samples were collected by 5 L Niskin bottles. Dissolved oxy-gen was measured according to Winkler titration method(APHA, 1999). Subsamples for nutrient analysis were prefil-tered by 45 mm syringe filters (Sartorius Mini Sart 17594-Q),transferred into acid washed polyethylene bottles and storedat �20 �C until the analysis. NO3

�þNO2�-N analysis was

performed by Skalar autoanalyser. PO4�3-P and SiO2-Si were

performed according to Parsons et al. (1984).Subsamples for phytoplankton analysis were transferred

into 1 L polyethylene bottles and fixed immediately with bo-rax buffered 40% formaldehyde solution (0.4% final concen-tration) (Throndsen, 1978). The subsamples were left at darkfor 24 h in the laboratory for precipitation (Utermohl, 1958).The supernatant was gently removed using a glass pipette(55 mm plankton net was fitted) and concentrated up to100 ml. Then the concentrated samples were transferred intodark glass bottles with addition of 2 ml 40% formaldehydefor preservation during storage (Throndsen, 1978).

2.2. Identification and cell counts

For the identification of species, 1e2 drops of sample wereput on a slide, covered with a cover glass and examined underlight microscope. Samples (5 ml) were transferred to glass tubes

and the Microcystis colonies were disintegrated by ultrasonifica-tion (50e60 Hz, 60 s) (Oudra, et al., 1997; Manage et al., 2001).Cells were counted by using a haemocytometer (Neubauer,0.1 mm depth) under a light microscope with 400� magnifica-tion. The eukaryotic phytoplankton cell counts were performedon Sedgewick-Rafter Counting Slide (Guillard, 1978).

2.3. Statistical analysis

Partial correlations were used to compare the relations be-tween Microcystis abundance and environmental parameters.All data were transformed to natural logarithms (loge xþ 1)prior to analyses (Zar, 1984) to fit normal distribution.

3. Results

Microcystis cf. aeruginosa existed at the upper estuarythroughout the study and the abundance ranged between2.7� 106 and 2.9� 104 cells ml�1 (Fig. 2). Two bloomswere recorded in December 1998 and February 1999, respec-tively (Figs. 2e3). The highest abundance was detected at H4(1.4� 106 cells ml�1) in December 1998 and at H5(2.7� 106 cell ml�1) in February 1999 (Fig. 4). The bloommight last through December to February but lack of Januarydata inhibited such prediction. Lowest values were detected inH1, at the lower estuary both in December 1998 and February1999.

The surface temperature ranged between 6.2 and 27.8 �C atthe upper estuary. Unlike the general trend, both December

H1 H2 H3 H4 H5Sampling stations

0

1000

2000

3000

Abun

danc

e (1

03 ce

lls m

l-1)

Dec. 1998

Feb. 1999

Fig. 4. The spatial distribution of the Microcystis cf. aeruginosa in the Golden Horn Estuary.

596 S. Tasx et al. / Estuarine, Coastal and Shelf Science 68 (2006) 593e599

Table 1

The abundance of Microcystis cf. aeruginosa and physical parameters of stations during December 1998 and February 1999 blooms

Parameters Secchi disc

(m)

Salinity

(S )

Temperature

( �C)

Microcystis

(103 cells ml�1)

Stations Depth

(m)

Dec. 98 Feb. 99 Dec. 98 Feb. 99 Dec. 98 Feb. 99 Dec. 98 Feb. 99

H1 40 0.9 0.8 13.9 9.9 7.1 6.1 312 975

H4 5 0.3 0.2 3.9 1.8 6.2 6.1 1425 2280

H5 5 0.3 0.2 3.7 1.8 6.3 7.1 942 2720

1998 and February 1999 blooms occurred in winter, when thesurface temperature was below 8 �C (Fig. 2). According to thedata obtained, there is no correlation between Microcystisabundance and temperature.

The surface salinity (S ) ranged between 1.8 and 18.2throughout the study and greatest decline always detected inwinter. Microcystis abundance was the highest while the salin-ity was the lowest (Fig. 2). According to the data obtained dur-ing the study, there is a moderate negative partial correlation(r¼�0.561, p¼ 0.002) between salinity and Microcystisabundance controlled by temperature, dissolved oxygen andnutrients (Table 2).

The increasing amounts of stream discharge due to heavyrainfall sharply decreased the surface salinity throughout theestuary in December 1998 and February 1999 (Table 1). Theprecipitation amounts 44.4 and 58.5 mm, respectively, werethe second and third highest precipitation values detectedthroughout the study. Although the highest rainfall was de-tected in October 2000, surface salinity was higher than thatin December 1998 and February 1999.

The high amounts of stream flow due to rainfall decreased thesecchi disc depth significantly. The secchi disc value decreasedfrom 0.6 to 0.3 m at the upper estuary, and from 1.6 to 0.9 m atthe lower estuary between November and December 1998(Table 1). During the February 1999 bloom, the value was alsobelow 1 m at the upper estuary. As the water quality improved,the secchi disc depth increased throughout the estuary. However,there was still a remarkable decrease in the secchi disc depthfrom the lower estuary towards the upper part (Table 1).

The dissolved oxygen concentration at the lower estuarywas below nitrification level (0.3 mg L�1) until May 2000(Kıratlı and Balkıs, 2001). However, two extraordinary peaksof dissolved oxygen were detected during Microcystis bloomsin December 1998 and February 1999 and values reached to6.83 mg L�1 and 7.17 mg L�1, respectively, at the lowerestuary.

The nitrateþ nitrite values were ranged between 0.2and 328 mM, ortho-phosphate 0.3e135 mM and silicate1.86e821.7 mM throughout the study. The nutrient

concentrations elevated mainly in winter when the freshwaterinflow increased due to rainfall (Okusx et al., 2001). FollowingMay 2000, the nutrient concentrations remarkably decreased.During the Microcystis blooms, the nitrateþ nitrite concentra-tions were high and ortho-phosphate concentrations were low(Fig. 5). Partial correlation between Microcystis concentrationand silicate, controlling for the effects of salinity, temperature,dissolved oxygen and precipitation pointed out a moderatecorrelation (r¼ 0.581, p¼ 0.002).

The eukaryotic phytoplankton group diversity was low dur-ing Microcystis cf. aeruginosa blooms and only five specieswere identified during December 1998 bloom throughout the es-tuary. The species diversity increased at the lower estuary andreached maximum in November 1999 with 42 species. The spe-cies distribution was dominated by dinoflagellates during Mi-crocystis blooms but distribution of diatoms increased afterJune 2000 (Fig. 6). Although no other cyanobacterial bloomswere detected following the rehabilitation of Golden Horn Estu-ary, several other eukaryotic phytoplankton blooms were re-corded. The high abundance of diatom Skeletonema costatum(Greville) Cleve (June 2000), dinoflagellate Prorocentrum min-imum Schiller (July 2000) and euglenophyte Eutreptiella sp.(October 2000) were examples for such blooms (Fig. 7).

4. Discussion

The water quality in the Golden Horn Estuary had been af-fected by large amounts of domestic discharges as well as in-dustrial inputs for decades. Heavy loads carried by streamsand little circulation resulted in higher bacteriological pollu-tion at the upper estuary than the lower estuary. The bacterio-logical indicators of pollution at the surface waters of theestuary were above 106 CFU/100 ml at the inner part (Aslan-Yılmaz et al., 2004).

Microcystis species can form blooms in nutrient-rich waterbodies (Rheinheimer, 1994). Microcystis blooms generally oc-cur during the summer months due to increasing temperaturein lake ecosystems. The abundance of six Microcystis speciesincreased in the summer and reached the maximum abundance

Table 2

Partial correlation coefficients between environmental parameters and abundance of Microcystis in the Golden Horn Estuary (Pearson correlation coefficient (r);

probability ( p))

Parameters Salinity

(m)

Temperature

( �C)

Dissolved oxygen

(mg L�1)

Nitrateþ nitrite

(mM)

Phosphate

(mM)

Silicate

(mM)

r �0.561 �0.062 �0.447 �0.242 0.357 0.581

p 0.002 0.760 0.019 0.233 0.074 0.002

597S. Tasx et al. / Estuarine, Coastal and Shelf Science 68 (2006) 593e599

M J J A S N D F M A M J J A S O N D J F M A M J J A S O N D0

1000

2000

3000Ab

unda

nce

(103

cells

ml-1

)

0

100

200

300

400

Nitr

ate+

nitri

te (µ

M)

0

50

100

150

Phos

phat

e (µ

M)

0

200

400

600

800

Silic

ate

(µM

)

821

1998 1999 2000

Microcystis

Nitrate+nitrite

Phosphate

Silicate

H5

Fig. 5. The nutrient concentrations and Microcystis cf. aeruginosa abundance in the upper estuary.

(6.7� 105 cells ml�1) in September in Suwa Lake (Park et al.,1996). The growth of Microcystis aeruginosa was limited withthe brackish region and negatively correlated by the salinity inPatos Lagoon (Yunes et al., 1997). In this present study, twoblooms were recorded in winter where the salinity was thelowest (S¼<5). The freshwater inflow increased in winterand carried high amounts of nutrients and Microcystis bloomsoccurred at the upper estuary where the water circulation wasrather stable.

In February 2000, the SwaneCanning estuary in WesternAustralia experienced a bloom of the toxic cyanobacteria Micro-cystis aeruginosa. The freshwater from the SwaneAvon Riverswith it high levels of nutrients, stimulated the algae growth. Theextent of the bloom depends largely on the availability of nitro-gen and phosphorus and the salinity of the water (Atkins et al.,2001). According to Robson and Hamilton (2003), M. aerugi-nosa grew optimally at salinities up to 4, above which growthrate declined to zero at salinity w25 in the laboratory ex-periments. Orr et al. (2004) reported that the salt tolerance ofM. aeruginosa in laboratory cultures was as high as 9.8 g L�1

and reduction in the total cell concentration in the first 23 hwas only observed in the highest salt treatment.

The concentrations of phosphate, nitrate and dissolved sil-icon are characteristically higher in river waters than in sur-face seawater of the shelf regions and this leads to a generalenhancement of nutrients in estuaries and coastal waters influ-enced by land drainage (Raymont, 1980). In this present study,

the moderate positive partial correlation between salinity andMicrocystis abundance indicated the influence of the terrestrialinput on the water quality of the estuary.

According to Reynolds (1984), the phytoplankton growthrates decreased as the cell or colony size of Microcystis aeru-ginosa increased. It is established that there was a sharp de-crease in the population of Dinophyceae and Chlorophyceaeduring the cyanobacterial bloom (M. aeruginosa and Phormi-dium mucicola) on an eutrophic lake in Tunisia (Oudra et al.,1997). The ratio of M. aeruginosa over the total phytoplanktonwas 45e85% in eutrophic conditions and 75e100% in hyper-eutrophic conditions in Latvian Lake (Druvietis, 1997). Thespecies distribution of the phytoplankton community of theGolden Horn Estuary was generally low due to heavy pollu-tion before June 2000 (Okusx et al., 2001). The phytoplanktoncommunity structure was poor especially at the upper estuaryduring the M. cf. aeruginosa bloom periods, as the develop-ment of other phytoplankton groups was surpassed by thecyanobacterium.

The abundance of Microcystis decreased towards the lowerestuary where the eukaryotic phytoplankton abundance in-creased. Following rehabilitation the abundance of Microcystisdecreased significantly, however, algal bloom risks still re-mained since domestic and industrial wastewater intrusionsinfluenced the estuarine water quality. Following rehabilita-tion, an euglenophyte bloom instead of Microcystis was re-corded in October 2000. Although the second and third

M J J A S N D F M A M J J A S O N D J F M A M J J A S O N D0

10

20

30

40

50

Num

ber o

f spe

cies

1

10

100

1000

10000

Abun

danc

e (1

03 ce

lls l-1

)

Diatom

Dinoflagellate

Other groups

Microcystis

20001998 1999

Fig. 6. The variations in the abundance Microcystis cf. aeruginosa and the number of phytoplankton species in the upper estuary.

598 S. Tasx et al. / Estuarine, Coastal and Shelf Science 68 (2006) 593e599

1

10

100

1000

10000M

icro

cyst

is (1

03 ce

lls m

l-1)

0

2000

4000

6000

8000

Tota

l phy

topl

ankt

on (1

03 ce

lls l-1

)

H4

M J J A S N D F M A M J J A S O N D J F M A M J J A S O N D1

10

100

1000

10000

Mic

rocy

stis

(103

cells

ml-1

)

0

2000

4000

6000

8000

Tota

l phy

topl

ankt

on (1

03 ce

lls l-1

)

1998 1999 2000

Microcystis

Total phytoplankton

H5

Fig. 7. The variations in Microcystis cf. aeruginosa and the total phytoplankton abundance in the upper estuary.

highest precipitation amounts resulted in Microcystis blooms,the highest rainfall resulted in a eukaryotic phytoplanktonbloom.

5. Conclusion

Microcystis blooms are generally recorded in lakes orbrackish waters such as estuarine ecosystems in summer. Con-trary to these findings, the blooms were recorded in GoldenHorn Estuary in winter. The blooms of the cyanobacteriumMicrocystis cf. aeruginosa were mainly related with the poorwater quality. The decrease in the salinity and increase inthe nutrient concentrations shifted the cyanobacterial blooms.Following rehabilitation, the abundance of eukaryotic phyto-plankton versus Microcystis increased remarkably. A healthywater circulation and limited intrusions from the terrestrial en-vironment should be the primary goals for a sustainable devel-opment in the Golden Horn Estuary.

Acknowledgements

Authors would like to thank Mr. Bryan C. Mayes for cor-recting the English text during the preparation of the manu-script. This study was conducted as a part of ongoing WaterQuality Monitoring Project funded by General Directorate ofIstanbul Water and Sewerage Administration.

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