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Morphological, genetic, chemical and ecophysiological characterisation of two Microcystis aeruginosa isolates from the Vistula Lagoon, southern Baltic

Mazur-Marzec H., Browarczyk-Matusiak G., Forycka K., Kobos J., Pliński M.

Oceanologia

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2010

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No. 52 (1)

127-146

EN

The Vistula Lagoon (southern Baltic Sea) is a shallow and highly eutrophic water body, with frequent blooms of cyanobacteria dominated by Microcystis and Anabaena species. Two Microcystis strains, MK10.10 and MAKR0205, isolated from the lagoon were characterised in this work. The morphology of the isolates differed significantly with respect to cell size and their ability to form aggregates. Based on the 16S rRNA sequence and 16S-23S internal transcribed spacer (ITS) sequence, both isolates were classified as Microcystis aeruginosa. However, only one isolate, MK10.10, possessed the mcy genes responsible for microcystin biosynthesis and only this strain produced microcystins. The effects of environmental factors, such as light, temperature and salinity, on toxin production turned out to be minor. Under the culture conditions used in the experiments, the biomass of the toxic MK10.10 was always lower. Hybrid quadrupole-time-of-flight liquid chromatography/tandem mass spectrometry (QTOF-LC/MS/MS) was used to elucidate the structure of the microcystin (MC) variants produced by MK10.10. Based on molecular ion and fragmentation spectra, the toxins were identified as MC-LR, MC-VR and MC-HIlR. Our study confirmed that some morphological criteria could be useful in preliminarily assessing the potential toxicity of a Microcystis bloom.

2

Do toxic cyanobacteria blooms pose a threat to the Baltic ecosystem?

Mazur-Marzec H., Pliński M.

Oceanologia

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2009

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No. 51 (3)

293-319

EN

Cyanobacteria, otherwise known as blue-green algae, are oxygenic, photosynthetic prokaryotes. They occur naturally in many fresh, marine and brackish waters worldwide and play an important role in global carbon and nitrogen cycles. In their long history, cyanobacteria have developed structures and mechanisms that enable them to survive and proliferate under different environmental conditions. In the Baltic Sea, the mass development of cyanobacteria is compounded by a high level of eutrophication. The dominant species in the Baltic, the filamentous Aphanizomenon flos-aquae and Nodularia spumigena, can fix dissolved atmospheric N2, as a result of which they can outcompete other phytoplankton organisms. Heterocystous, filamentous cyanobacteria also make a significant contribution to the internal nutrient loading in the Baltic. The blooms of N. spumigena are of particular concern, as this cyanobacterium produces nodularin (NOD), a hepatotoxic peptide. The concentration of the toxin in the sea is regulated mainly by dilution with uncontaminated water, photolysis, sorption to sediments and microbial degradation. The transfer of the toxin in the Baltic trophic chain through zooplankton, mussels, fish and birds has been reported, but biodilution rather than bioconcentration has been observed. Cyanobacterial blooms are thought to pose a serious threat to the ecosystem. Their harmful effects are related to the occurrence of a high biomass, oxygen depletion, a reduction in biodiversity, and the production of toxic metabolites.

3

Cyanobacterial hepatotoxins, microcystins and nodularins, in fresh and brackish waters of the Pomeranian Province, Northern Poland

Mazur-Marzec H., Spoof L., Kobos J., Pliński M., Meriluoto J.

Oceanological and Hydrobiological Studies

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2008

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Vol. 37, No.4

3-21

EN

Microcystins (MCs) and structurally related nodularins (NODs) are hepatotoxic cyclic peptides produced by bloom-forming cyanobacteria. These toxins have been implicated in the deaths of wild and domestic animals as well as in incidents of human illness. Cyanobacterial toxins occurring in the fresh and brackish waters of the Pomeranian Province, northern Poland were characterized in this study. Water samples collected from seven lakes in August and September 2005 were analysed by high performance liquid chromatography (HPLC), enzyme linked immunosorbent assay (ELISA) and protein phosphatase inhibition assay (PPIA). Cyanobacterial toxins present in field samples and in an isolated strain of Planktothrix agardhii were also characterized by liquid chromatography electrospray ionization tandem mass spectrometry (LC-ESI-MS/MS). In most of the fresh water samples MC-LR, MC-RR and MC-YR dominated. In the lakes where P. agardhii was most abundant demethylated microcystin variants tentatively identified as [D-Asp3]MC-LR, [D-Asp3]MC-YR and [D-Asp3]MC-RR, were found. Total concentrations of the toxins measured by HPLC ranged from 0.1 žg l-1 to 305.4 žg l-1. Nodularia spumigena bloom samples were collected from brackish waters of the Gulf of Gdańsk, southern Baltic, and LC-ISP-MS/MS of extract from these revealed the presence of two geometrical isomers of linear nodularin and nodularin variant with aspartic acid methyl ester [MeAsp1(OMe)]NOD.

4

Cyanobacterial blooms in the Gulf of Gdańsk (southern Baltic): the main effect of eutrophication

Jóźwiak T., Mazur-Marzec H., Pliński M.

Oceanological and Hydrobiological Studies

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2008

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Vol. 37, No.4

115-121

EN

The most striking aspect of eutrophication in the Baltic are the summer blooms of cyanobacteria. Some of the blooms are toxic to marine organisms and poisonous to people. Our studies, conducted over the last three decades, report on mass occurrences of Aphanizomenon flos-aquae (L.) Ralphs and Nodularia spumigena Mertens. It is generally assumed that cyanobacterial blooms in the Baltic Sea are stimulated by the low ratio of N:P and initiated by high water temperatures. The mean annual value of this ratio in the Gulf of Gdańsk, since 1981, is 7:1-8:1, with the lowest values, of about 4, being seen in July when the cyanobacterial blooms begin. During three years of observations (1992-1994) the smallest number of recorded taxa was reported in 1993, concurrent with the lowest water temperature (16°C in summer). In August 1994, when the temperature increased to 22°C, a huge bloom was seen. Nodularia spumigena was very abundant in that bloom, and nodularin concentration of 2.59 mg toxin per g dry weight of bloom sample was recorded. A similar situation has also been observed in the years 2003-2006.

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The potential causes of cyanobacterial blooms in Baltic Sea estuaries

Pliński M., Mazur-Marzec H., Jóźwiak T., Kobos J.

Oceanological and Hydrobiological Studies

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2007

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Vol. 36, No.1

125-137

EN

Nodularia spumigena Mertens, Aphanizomenon flos-aquae (L.) Ralfs and some species of the genus Anabaena are the dominant cyanobacterial taxa occurring in the Gulf of Gdańsk. The heterocystous cyanobacteria use dissolved molecular N2 as an additional nitrogen source, and this allows them to bloom during the summer when growth of other phytoplankton species is normally nitrogen-limited. Although cyanobacterial blooms have been reported in the Baltic Sea since the mid-19th century, the extent and intensity of blooms have recently increased due to anthropogenic sources of eutrophication. Increased river phosphorus input and changes in the phosphorus to nitrogen ratio are implicated as causal factors. After us the initial cause of the cyanobacterial bloom is a low N:P ratio, which indicates phosphorus excess, i.e. favourable nutrient conditions for nitrogen-fixing algae. An N:P ratio of 10 has been considered an approximate value for the N:P requirements of Baltic phytoplankton. For several years this ratio has been lower than 10. The mean annual value of the N:P ratio for the water of the Gulf of Gdańsk ranged from 3 to 7. Differences in the intensity of blooms observed in different years could be linked to temperature. During hot summers, when the seawater temperature increased to 20°C, large blooms were noted. For the cyanobacterial blooms in the Baltic Sea, the low N:P ratio is the primary factor and high temperature is a starting point.

6

Toxic Nodularia spumigena blooms in the coastal waters of the Gulf of Gdańsk: a ten-year survey

Mazur-Marzec H., Krężel A., Kobos J., Pliński M.

Oceanologia

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2006

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No. 48 (2)

255-273

EN

In the Baltic Sea, summer blooms of the filamentous, nitrogen-fixing cyanobacterium Nodularia spumigena are favoured by high P concentrations at low N:P ratios and a salinity range of 5-13 PSU. The blooms are initiated by calm and sunny weather, an elevated surface water temperature and thermal stratification. The mass occurrence of N. spumigena in coastal waters is a matter of special concern, as the cyanobacterium produces nodularin, a potent pentapeptide hepatotoxin. In the Gulf of Gdansk, the large-scale occurrence of N. spumigena was recorded for the first time in 1994. Blooms of a similar intensity occurred in 2001, 2003 and 2004. Nodularin concentrations in freeze-dried bloom samples varied from 0.01 to 4.01 mg g-1 d.w. In the coastal waters of the Gulf of Gdańsk, cell-bound nodularin concentrations in 2004 and 2005 attained maxima of 25852 š 107 žg dm-3 and 3964 š 125 žg dm-3, respectively. Microscopic analysis revealed the presence of diverse N. spumigena forms, with the dominance of curved filaments in bloom samples. The results of in situ studies and remote sensing measurements indicate a high frequency and intensity of cyanobacterial blooms in the Gulf of Gdańsk in the last ten years.

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The occurrence of Dinoflagellates in the phytoplankton of the Gulf of Gdańsk coastal zone in 1994-1997

Witek B., Pliński M.

Oceanological and Hydrobiological Studies

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2005

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Vol. 34, No.2

63--70

EN

Observations of the development of Dinoflagellatae in the 1994-1997 period indicate that three species dominated in the coastal zone of the gulf of Gdańsk - Peridiniella catenata, Heterocapsa triquetra, and Prorocentrum minimum. The last two species are new elements in the phytoplankton structure, and their mass development is evidence that this group of phytoplankton is changing.

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The distribution of water vegetation on the Polish coast of the Baltic Sea in 1996-2000

Pliński M., Jóźwiak T.

Oceanological and Hydrobiological Studies

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2004

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Vol. 33, No. 2

29--40

EN

Qualitative analysis of vegetation along the Polish coast was conducted. Thirty-six species were noted - 16 of green, 5 of brown and 7 of red algae and 8 of vascular plants. In the 1996-2000 period, the share of green algae was always more than 50% of the floral composition. Only a few species were present throughout the period of investigations, as follows: green algae - Entero-morpha ahlneriana, E. intestinalis, Cladophora albida, Cl. glomerata, Cl. rupestris, Cl. sericea, Cl. vagabunda; brown algae - Pilayella litoralis, Fucus vesiculosus; red algae - Polysiphonia violacea, Ceramium diaphanum; vascular plants - Zostera marina. Some general conclusions can be drawn with reference to the geographical distribution of the species. Enteromorpha intestinalis was the only species that occurred at every station in almost every year. Three species of the genus Cladophora (Cladophora albida, Cl. rupestris, Cl. sericea) and Pilayella litoralis were also very common. Zostera marina was nearly absent from the central part of the Polish coast. Other species occurred rarely and accidentally.

9

Predictional model of biocenotic changes in offshore baltic plankton due to temperature increase

Pliński M., Żmijewska M. I., Sapota M., Witek B., Mudrak S.

Oceanological and Hydrobiological Studies

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2003

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Vol. 32, No. 3

29-41

EN

Over the last 20 years, more and more reliable data concerning global climate change, mainly climate warming, have become available in the literature. Change such as this has also been documented in the Gulf of Gdańsk. Climate change has an influence on aquatic ecosystems and especially their biocoenoses, and plankton is one of its most sensitive ecological fractions. Positive and negative statistical correlation in the exclusive relationship between the quantity of plankton groups and water temperature has been observed. When time was applied as a factor, only the annual increments of the blue-green algae correlation were statistically significant, and the regression equation calculated in this paper was applied to predict a rise in the population number of this algae in response to increasing temperature. It was not possible to perform this calculation with the other plankton components.

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Cyanobacterial toxins in fresh and brackish waters of Pomorskie Province (northern Poland)

Mazur H., Lewandowska J., Błaszczyka A., Kot A., Pliński M.

Oceanological and Hydrobiological Studies

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2003

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Vol. 32, No. 1

15-26

EN

Hepatotoxic cyclic peptides and neurotoxic alkaloids are the most common groups of cyanobacterial toxins. They pose a serious threat to human and animal health; each year they are responsible for several cases of animal fatalities (mammals, fish and birds). In Polish water bodies toxic blooms of cyanobacteria are also frequently observed. In this work, a procedure for anatoxin-a analysis has been modified to obtain a sensitive and selective method for routine studies of bloom samples. The presence of cyanobacterial neuro and hepatotoxins in fresh and brackish waters of Pomorskie Province was examined. Hepatotoxins, microcystins or nodularin, were detected in all phytoplankton samples dominated by the cyanobacteria of Microcystis and Anabaena genera or by Nodularia spumigena. HPLC-PDA analysis showed the presence of anatoxin-a only in one sample collected in coastal waters of the Gulf of Gdańsk and dominated by Anabaena.

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Nodularia spumigena blooms and the occurrence of hepatotoxin in the Gulf of Gdańsk

Mazur H., Pliński M.

Oceanologia

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2003

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No. 45 (2)

305-316

EN

Nodularia spumigena forms extensive summer blooms in the Baltic Sea. The occurrence of the blooms is determined by water temperature, light intensity and nutrient concentration; levels of nitrogen and phosphorus in particular are critical. The time of the seasonal maximum and intensity of the Nodularia bloom in the Gulf of Gdansk vary significantly from year to year. In 2001 a rapid and massive proliferation of N. spumigena was observed in late June - early July. The concentration of nodularin in water ranged from 90 to 18135 žg dm-3 and in lyophilised phytoplankton samples from 3000 to 3520 žg g-1 d.w. (dry weight). Such a high concentration of toxin in the recreational waters of the Gulf of Gdansk constitutes a health risk for users of bathing areas. In 2002, the N. spumigena bloom was less dense, but lasted longer, with a maximum in late July - early August. In 2002 the concentration of nodularin did not exceed 12.6 žg dm-3 in water and 919 žg g-1 d.w. in lyophilised phytoplankton samples. Other cyanobacterial toxins - microcystins and anatoxin-a - were also detected in the coastal waters of the Gulf of Gdansk.

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Effect of salinity, temperature and light on growth of Anabaena flos-aquae and Nostoc sp. div. (cyanobacteria, blue-green algae)

Pliński M., Dziopa M.

Oceanological Studies

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2001

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Vol. 30, No. 1-2

13-19

EN

Two species of blue-green algae have been studied under laboratory conditions in several combinations of salinity (0, 8, 16, 24 PSU), light (20, 70, 120, 170 μE m^-2 s^-1) and temperature (20, 25, 30, 35 °C). Temperature within the range of 30-35 °C and light intensity of 170 μE m^-2 s^-1 were the optimum to achieve a maximum growth effect in the two species examined. Salinity as an environmental factor showed that these two tested species are fresh water in origin with some tolerance to increased salinity concentration. The best growth rate for Anabaena flos-aquae was stated in 0 PSU medium for all temperature and light conditions. For Nostoc sp. div. medium with 8 PSU was the optimum one.

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Stability of cyanotoxins, microcystin-LR, microcystin-RR and nodularin in seawater and BG-11 medium of different salinity

Mazur H., Pliński M.

Oceanologia

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2001

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No. 43 (3)

329-339

EN

Microcystins and nodularin are potent hepatotoxins produced by fresh and seawater cyanobacteria. The persistence of three hepatotoxins - microcystin-LR, microcystin-RR and nodularin - was investigated in sterile BG-11 medium of different salinity and in water collected from the Gulf of Gdansk. After 21 days of incubation at 17 š 1oC and constant illumination of about 40 žmol photon m-2 s-1 the concentration of toxins decreased by about 30-37%. No significant changes in toxin concentration in the BG-11 media of different salinity were observed. When toxins were incubated in non-sterile seawater, their concentrations decreased markedly. It is likely that some strains of bacteria are responsible for the breakdown of the toxins. Nodularin turned out to be more resistant to biodegradation than the two microcystins. The influence of certain components of cyanobacteria cells on the accelerated rate of toxin degradation was also considered.

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The first recorded bloom of Prorocentrum minimum (Pavillard) Schiller in the coastal zone of the Gulf of Gdańsk

Witek B., Pliński M.

Oceanologia

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2000

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No. 42 (1)

29-36

EN

Prorocentrum minimum (Pavillard) Schiller has occurred in the Gulf of Gdansk in low abundance for several years. However, in summer 1997 a significant increase in the numbers of cells was noted. In the same year a P. minimum bloom was recorded for the first time in one of the harbour basins in Gdynia, giving rise to a brown-red coloration of the water.

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The distribution, species composition and abundance of Enteromorpha spp. in the Gulf of Gdańsk

Haroon A. M., Szaniawska A., Pliński M.

Oceanological Studies

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1999

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Vol. 28, No. 1-2

31-39

EN

The variations in distribution, species composition, biomass and water content of Entero-morpha spp. in the Gulf of Gdansk in relation to sampling stations and season are discussed. Only four Entero-morpha species were identified in the samples collected, the most frequent being E. intestinalis (L.) Link. The species composition was found to vary in relation to sampling stations and seasons. The abundance of Enteromorpha spp. varied at different stations with a maximum at Puck variations in biomass were observed. Although Enteromorpha spp. were characterised by a high water content (96.56?0.40% of WW), no statistically significant variations in the water contents of these species with respect to sampling stations could be detected. Although there was a tendency towards seasonal changes, these occurred within a narrow range.

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The composition, abundance and distribution of dinoflagellates in the Gulf of Gdańsk in the years 1992-1994

Pliński M., Dobron K.

Oceanological Studies

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1999

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Vol. 28, No. 1-2

41-49

EN

The quantitative and qualitative analysis of dinoflagellates from samples taken in the years from 1992 to 1994 in the Gulf of Gdansk has been done. The following species was identified: Hetero-capsa triquetra, Dinophysis norvegica, D. acuminata, Peridinium balticum, P. aciculiferum, P. pellucidum, P. curvipes, P. brevipes, Peridiniella catenata, Gonyaulax triacanta, Prorocentrum micans. The highest quantity of dinoflagellates was observed in May 1994.

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Temperature and N:P ratio as factors causing blooms of blue-green algae in the Gulf of Gdańsk

Pliński M., Jóźwiak T.

Oceanologia

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1999

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No. 41 (1)

73-80

EN

The bloom dynamics of two planktonic, nitrogen-fixing species of blue-green algae Aphanizomenon flos-aquae (L.) Ralfs and Nodularia spumigena Mertens in the Gulf of Gdansk were studied. The Gulf of Gdansk is a shallow part of the Baltic Sea where the water has a mean salinity of ca 8 PSU. Increased riverine nutrient input and/or changes in the N:P ratio are indicated as factors causing blue-green algae blooms. A low N:P ratio appears to trigger blooms. The mean annual value of N:P in the Gulf of Gdansk since 1981 is 6.5 with a minimum of ca 3. There could be a link between temperature and the year-to-year differences in bloom intensities. A huge bloom of toxic N. spumigena was reported in July 1994 when the water temperature rose to 22oC.

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Occurrence of blue-green algae in the phytoplankton of the Gulf of Gdansk in the years 1994-1997

Witek B., Pliński M.

Oceanological Studies

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1998

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Vol. 27, No. 3

77-82

EN

The development of the blue-green algae in the Gulf of Gdansk begins in May and lasts till October. To the stable compo-nents of the filamentous forms belong Aphanizomenon-flos aquae, Nodularia spumigena, Planktolynbya limnetica, Pseudanabaena limnetica and Planktothrix sp. The coccoid forms are represented by Snowella septentrionalis, S. lacustris, Merismopedia punctata, M. tenuissima, Woronichinia compacta, Rabdogloea linearis, Cyanodictyon imper,fectum, C.planctonicum. In the years 1992 and 1993 the openwater area of the Gulf of Gdansk was characterised by the summer (July) domination of two species of blue-green algae: Microcystis aeruginosa and Aphanizomenon flos-aquae. The presence of Nodularia spumigena was also noticed. In 1994, the extremely dense bloom of Nodularia spumigena occurred with the biomass increase to 130 mgŠCŠ m^3. The intensity of this bloom could be linked to temperature which in summer 1994 was very high and reached over 22?C. In the years 1996 and 1997, temperature did not attained so high values and the intensity of blooms was lower.

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Blue-green algae blooms in the Gulf of Gdańsk and surrounding area

Pliński M., Musiał A., Ostrowski B.

Oceanological Studies

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1998

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Vol. 27, No. 1

39-44

EN

The phenomenon of blue-green algae blooms in the Baltic and the surrounding freshwater bodies has been known since several years. Recently these blooms have increased. The negative effects of this phenomenon concern not only environ-ment but also pose epidemiological threats because some blue-green algae produce toxins. The presence of potential toxic blue-green algae species in the Gulf of Gdaąsk as well in the whole southern Baltic has been noticed for almost hundred years. In the recent years, when water temperature reached more than 18?C, the rapid growth of Nodularia spumigena has been observed. In the year 1994, the huge bloom with toxic features of this species has been noticed. With less intensity such a bloom appeared also in 1996. Since several years Anabaena flos-aquae blooms in the Vistula Lagoon and Microcystis flos-aquae in many lakes in the Kashubian Lakeland.

20

Coastal and inland cyanobacterial blooms (blue-green algae) – hazards to human and animal health [commun.]

Pliński M., Codd G. A.

Oceanologia

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1998

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No. 40 (4)

399-403

EN

The aim of this communication is to increase the awareness about the hazards presented to animal and human health by cyanobacterial toxins, signs of poisoning by the toxins, samples to be taken for analysis and of sources of information on therapy. Heightened awareness is advocated in view of the increasing occurrence of cyanobacterial blooms and scums in Polish waters and of reports of animal intoxications attributed to cyanobacterial toxins in neighbouring and other countries around the Baltic Sea.