On the effect of cyanobacterial blooms on the flounder stock in the Gulf of Finland. Tenno Drevs, Andres Jaanus, and Ele Vahtmäe

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1 ICES CM 3/S:1 Marine Ecosystem Change Ecosystem Consequences of Cyanobacteria in the Baltic Sea (Session S) On the effect of cyanobacterial blooms on the flounder stock in the Gulf of Finland Tenno Drevs, Andres Jaanus, and Ele Vahtmäe Experimental catches as well as reports of fishers were analyzed to reveal the effect of harmful algal blooms in summer on the abundance indices of flounder. Flounder is one of the most common commercial species in Estonian coastal waters in summer and therefore it is more useful for investigations. An extensive cyanobacterial bloom in the southern Gulf of Finland was observed from the end of June to the midst of July with subsequent decaying phase of algae during -3 week after the bloom collapse. At the first stage of cyanobacterial bloom Aphanizomenon flos-aquae was the predominating species. Potentially toxic cyanobacterial species Nodularia spumigena and Anabaena spp. were determined near the Estonian north coast in the second phase of the bloom and bathing was not recommended during this period. Therefore it could be mostly a dead mass of algae driven by wind towards to the beaches in the second part of July. After the very extensive algal bloom in coastal waters near the Estonian north coast in the summer 1-year old flounder disappeared in experimental catches while during experimental catches in 1999,, and 1 1-year-old flounder was caught. Last allows to assume the connection between toxic algal blooms and natural mortality of the young flounder. During the bloom statistically significant negative trend in flounder catch per unit of effort was found in several national fishing rectangles near Tallinn, but after the bloom the flounder abundance indices restored. Key words: cyanobacteria, natural mortality, behaviour, flounder Tenno Drevs: Tallinn Pedagogical University, Narva mnt., 11 Tallinn, Estonia,(tel , e.mail: haugas@ness.sea.ee ). Andres Jaanus: Estonian Marine Institute, Marja d 1617, Estonia, (tel , andres@phys.sea.ee ). Ele Vahtmäe: Tallinn Pedagogical University, ( elkin@hot.ee). Introduction In recent years harmful algal blooms have become an increasing problem in coastal waters. Abundance of Aphanizomenon flos-aquae as well as Nodularia spumigena has increased in the period in relation of the period in the Baltic Sea (Finni et al., 1). Phytoplankton primary production, biomass, and the number of potentially toxic taxa all increase considerably from the Bothnian Bay to the northern Baltic Sea proper and are generally higher in open sea than in coastal waters (Hajdu, ). This pattern reflects increasing salinity, an increased nutrient availability, and prolongation of productive season from north to south (Hajdu, ). Nodularia spumigena, Aphanizomenon sp. (cyanobacteria), Dinophysis acuminata, D. norvegica, Prorocentrum minimum (dinoflagellates), and Chrysochromulina spp. (prymnesiophycean flagellates) are potentially toxic taxa that may reach high abundance in the northern Baltic, where salinity is above PSU (Hajdu, ).

2 In the open Baltic Sea Aphanizomenon and Nodularia annually form mass populations in late July early August (Anon., 1998). The cyanobacterial bloom initiation always coincides with the increase of the surface water temperature over 1-16 C in the Gulf of Finland (Kanoshina, ; Jaanus & Pellikka, 3). In the coastal areas freshwater species, such as Microcystis, Anabaena, Gomphosphaeria, and Oscillatoria/Planktothrix can form regional blooms (Anon., 1998). Nodularia spumigena has been found responsible for toxicity of the blooms in the Baltic Sea and the toxin involved has been nodularin, a hepatotoxic cyclic pentapeptide (Anon., 1998). Very warm summer in was unusual for the Estonian northern coast. Resulted in the phytoplankton bloom, which maximum was recorded in the end of June and beginning of the July, dead and alive phytoplankton mass was driven by northwestern wind into the beaches around the Tallinn. Therefore the bathing was not recommended between 16(th) and 3 (th) July in several beaches (Anon., 3). In the first week of July the absolute maximum of abundance of cyanobacteria was found in central and southern Gulf of Finland while the Aphanizomenon flos-aquae was mainly responsible for the bloom. Abundance of Nodularia spumigena was not very high during the bloom peak. By Central Laboratory of Microbiology of the Health Protection Inspectorate potentially toxic species Nodularia spumigena and Anabaena lemmermanii were detected at the beaches of Pirita, Kakumäe, and Stroomi (Anon., 3). The main mass of phytoplankton could be dead mass, which decomposition takes nearly -3 weeks after the bloom. Decomposition can produce the most quantities of the toxic substances into the water. Phytoplankton blooms can affect the different stages of fish by different ways. By clogging of the fish gills and by resulting the oxygen depletion, they can influence natural mortality of fish also without production of the toxic substances (Edler, Kononen, Kuosa, 1996; Fogg, ). On the other hand, micro-algae play the outstanding role of primary producers in aquatic habitats (Fogg, ). Phytoplankton as a food for zooplankton and zoobenthos influences their abundance and the feeding conditions for young fish. The toxic substances can also distribute by food web. Cyanobacterial toxins are found in the liver of flounder in August in the western Gulf of Finland, but in relatively low concentrations, while flesh was not found toxic (Sipiä, 1).In case of flounder all the above mentioned ways were under consideration. Flounder distribution by different depths depends on size, age of flounder, and season. Smaller and younger individuals (1-year-old and younger) feed mainly in coastal area in the depths between some cm to m (Mikelsaar, 198) and also in river mouths. Last makes them sensitive to the situation like in summer near Estonian north coast. Therefore dependence of natural mortality of young flounder on the algal blooms could be a point of interest. Behaviour of older flounder depends on season and sometimes they are also situated in coastal areas. Estonian commercial fishery of flounder is now concentrated in coastal area in the depth below m in the Gulf of Finland and flounder seems to avoid the areas of algal blooms.

3 Purpose of current work is to investigate the effect of summer toxic algal blooms on the natural mortality of young flounder as well as changes of distribution of older ones. Material and methods The studied area (national fishing rectangles 11-1) is situated between and E along the northern Estonian coast (Fig.1). The area covered by algal bloom was studied using satellite images (Fig.). Analyzes of the Central Laboratory of Microbiology of the Health Protection Inspectorate were used to determine the period of the most possible effect of algal bloom in coastal area of northern Estonia, which was between 16 (th) and 3 (th) July, at the beaches of Pirita, Kakumäe, and Stroomi, and also the potentially toxic cyanobacteria species (Anon., 3). In experimental catches in the Muuga Bay in SE from the Port of Muuga the monitoring gill nets with different mesh sizes were used for estimating the relative abundance of different age groups of flounder including the relative abundance of 1-year-old flounder. Age was determined using otoliths. Relative abundance dynamics by different years and months by different age groups were analyzed in relation of the algal bloom in. The nets with length 3 m were used. Catches were done mainly in August and September, but also in April, May, June, and October. The nets with mesh size 3 and mm allow to catch also the 1-year old flounder, which is point of interest in relation of algal blooms in coastal area. Experimental catches in Muuga Bay in NW from the Port of Muuga as well as analysis of fisher s reports from the northern coast of Estonia in were used to investigate relative abundance of flounder with mainly legal size for fishing. At the station NW from Muuga Port in Muuga Bay the nets with length 6 m and mesh size 9-1 mm were used to reveal the relative abundance of flounder with mainly legal size for fishing. In current work the catches in July and August were under consideration. Catch per unit of effort dynamics in conditions of algal bloom in relation of the years when algal situation was different, was studied. 1. Total number of net hauls in experimental catches in Muuga Bay was as follows in Table Table1. Total number of net hauls at two different stations in Muuga Bay: NW from the Muuga Port in July and August; SE from the Muuga Port Year NW SE The quantity of analyzed net hauls in fisher's reports is presented in the Table.

4 Table. Number of net hauls per different national fishing rectangles in July and August according fisher's reports. Rectangle Total July August The fisher s reports as well as experimental catches were used to reveal the significance of trends in the catch per unit of effort (CPUE) dynamics by correlation and regression analysis. Results and discussion According the data of Central Laboratory of Microbiology of the Health Protection Inspectorate there have not been before the algal mass in coastal areas like during the second part of July in near the northern coastal area of Estonia (Anon., 3). An extensive bloom was also in 1997 and 1999, but too few data from coastal areas are available. The data on the cyanobacterial blooms and surface accumulations in are presented between Tallinn and Helsinki (Jaanus & Pellikka, 3), but information on the situation along the Estonian northern coast is lacking. Only the public beaches are studied a little in. Disappearing of the 1-year-old flounder in experimental catches in Muuga Bay after the algal bloom in summer could be a result of increase of the natural mortality (Fig.3). Experimental catches were done in the end of August and in September in after the cyanobacterial bloom, but 1-year-old flounder did not appear this year. 1-year -old flounder was not found also in 3 (Fig.3). It is possible that the year-class 1 as well as the year class were both affected. Therefore algae monitoring can be useful for flounder yearclass strength estimations. Summer algal blooms interaction with winds, which can drive the algal mass into the coastal areas can affect seriously young flounder, which feeds mainly in the shallow waters. By estimating the total area, duration, and intensity of algal blooms in coastal waters, the natural mortality of young flounder can be better estimated. The effect of algal blooms in consideration with oil pollution is not weaker. For example, in, 1 days after the oil pollution in Muuga Bay, the 1-year -old flounder was caught, but condition index Fulton coefficient of flounder was significantly decreased. Decrease of CPUE values in several national rectangles of Northern Estonian coast (rectangles 13, 1, and 18) according experimental catches in the Muuga Bay (national fishing rectangle 13) and fisher s reports between 16(th) and 3(th) July, were statistically significant (Fig. 1, a-7b). CPUE was restored after the disappearance of algal mass, which leads to the opinion that the bloom affects mainly the behaviour of the flounder of legal size for fishing. Experimental catches in the Muuga Bay (national fishing rectangle 13) between in July and August in did not show clear negative trend in CPUE values in the second part of July except in 1999, when stronger as usual cyanobacterial bloom existed in the Gulf of Finland. In 1997 and 1999 in conditions of algae blooms higher than usual (Kanoshina,; Anon., ) the dynamics of CPUE values during experimental catches in the Muuga Bay in July and August were different than in years of less abundance of cyanobacteria as in 1998 and. In 1 the stronger cyanobacterial bloom was registered in Finnish waters and near northeastern Estonian coast, where the flounder is relatively rare (Anon., ). In 1997 the CPUE values in July were relatively low and in August started to increase rapidly. In 1999 clear negative trend in the second part of July can

5 be seen and higher values in August. In the years of less abundance of cyanobacteria the CPUE dynamics is highly dispersed but without clear trends, except in 1 when in the second part of July increased trend was seen in the Bay of Muuga. Salinity in deeper areas is important factor, which is positively correlated with flounder catches and CPUE in the Gulf of Finland (Drevs, 1999, ). Fluctuations of salinity are not measured every day and therefore this factor cannot be considered in case of cyanobacterial bloom in. The absolute values of CPUE in different years are not compared, only the trends because salinity dynamics in deeper areas in different years remarkably effects the abundance of flounder also in coastal areas. Flounder with legal size for fishing usually avoids higher temperatures of the water ( C and more) while the young flounder does not. Cyanobacteria bloom coincidents with higher water temperature. In the water temperature in August was not lower than in the second part of July. In August the CPUE values increased in national fishing rectangles 13, 11, and 18. Therefore the temperature could not be the reason of the decrease of CPUE in the second part of July. Catch intensity is also important. In the national fishing rectangle 18 a slight negative (r = -.19), but not statistically significant trend in the number of total net hauls per day between the 16 (th) and 3 (th) July, was found. In rectangles 13 and 1 slight positive trend (r=. and r=.3 correspondingly) was found, which was statistically not significant. In the rectangle 1 total number of net hauls increased twice in August. In rectangles 13 and 18 it did not change remarkably. The relationship between CPUE and catch intensity supports the opinion that catch intensity probably could not be the reason of decrease of the CPUE in the second part of July in the three national rectangles. The CPUE values of flounder in national rectangles 13, 1, and 18 were fluctuating in July-August so, that in the second part of July the CPUE values were not lower than the minimum values during first part of July and August. Therefore it is obvious that besides cyanobacterial bloom other factors are also important (Fig. a, a, 6a, 7a). Algae, especially Cladophora, make the gill nets more visible for fish and therefore can decrease catch ability of the fishing gear. Usually in the nets which are more filled by algae less fish are found in comparison of the cleaner nets of the same fleet and at the same time. In case of cyanobacterial blooms the gill nets become, too, more visible for fish and their catch ability probably decreases a little, but the Cladophora is much more essential in decrease of the catch ability. Therefore the differences in CPUE values in current study reflect mainly abundance of flounder and in lesser extent decrease of the catch ability of gill nets. Conclusion Cyanobacterial blooms seem to increase significantly the mortality of young flounder in case when the temperature of water is relatively high and the algal mass is driven by wind into shallow coastal waters. The last seems to be the most important way how the blooms can affect the abundance of flounder. The blooms can also change the behaviour of older flounder (mainly with legal size for fishing). They leave the areas with unfavorable algal situation, and the last cannot be explained by changes of temperature or catch intensity, but the effect is temporary.

6 On the other hand, the algae make gill nets more visible for the fish. In case of cyanobacteria accumulations the differences in catch ability of gill nets are probably not significant. Aknowledgements We wish to thank prof. A. Järvik as a leader of Port of Muuga Monitoring Pr oject, which allowed to do experimental catches in the Muuga Bay, and also Mrs. L.Järv. References Anon Harmful algal blooms in European marine and brackish waters.(granely, E., Codd, G.A., Dale, B., Lipiatou, E., Maestrini, S.Y., Rosenthal, H., ed.-s).european Commission, Belgium. Anon.. Rannikumere eutrofeerumine. In Eesti keskkonnaseire (Roose, A. ed.), Tartu Ülikooli Kirjastus, Tartu. Anon. 3. Tervisekaitseserver. http: (visited and 6 March, 3). Drevs,T Population dynamics of flounder (Platichthys flesus) in Estonian waters. Proc. Estonian Acad. Sci. Biol. Ecol., 8,, Drevs, T.. On the flounder yield and spawning stock medium-term forecasts in Estonian waters. ICES CM/V:. Edler,L., Kononen,K., Kuosa, H Harmful algae. In Third Periodic Assessment of the State of Marine Environment of the Baltic Sea, ; Background document Balt.Sea Envir. Proc. No. 6B. Finni, T., Kokonen, K., Olsonen, R., Wallström, K. 1. The History of Cyanobacterial Blooms in the Baltic Sea. Ambio, Vol 3 No -, Fogg, G.E.. Harmful algae- a perspective. Harmful Algae, Vol.1 No1, 1-. Fütoplankton. (visited..3). Hajdu, S.. Phytoplankton of Baltic Environmental Gradients: Observations on Potentially Toxic Species. Doctoral Thesis, Department of Systems Ecology Stockholm University. Jaanus, A., Pellikka, K. 3. Does increasing phosphorus necessarily cause increasing biomass of diazotrophic cyanobacteria? Proc.Est.Acad.Sci.Ecol.,3, 3, -17. Kanoshina,I.. The influence of meteorological conditions and hydrophysical processes to the spatio-temporal variation of the summer phytoplankton bloom development in the Gulf of Finland, Baltic Sea. Thesis submitted for the degree of master of science. University of Tartu, Tartu. Mikelsaar,N Flounder of the Eastern Baltic Sea. Doctoral Thesis. Academy of Sciences of Estonian SSR, Tartu (in Russian). Sipiä,V. 1. Accumulation of cyanobacterial hepatotoxins and okadaic acid in mussel and fish tissues from the Baltic Sea. Academic dissertation. Finnish Institute of Marine Research, Helsinki.

7 ESTONIA Figure 1. South (Estonian) coast of the Gulf of Finland; Estonian national fishing rectangles 13, 1, and 18.

8 Figure. Satellite image (NASA EOS Terra/MODIS, modified by A.Reinart) indicating cyanobacterial bloom (green area) on the1 (th) July, in the Baltic Sea.

9 Number of individuals per net and night //1999 1/6/ /8/ /9/1999 3/9/ /9/ 6/9/ 1// 3/1/.1.1. //1 31//1 Figure 3. Abundance of 1-year-old flounder in the Muuga Bay (rectangle 13) 1. 6/6/1 9/8/1 /9/1 9/8/ 9/11/ 6/9/ //3 8//3

10 Number of flounders per hours and net /1/ 7/8/ 7/1/ 7// 7/9/ 8// 8/1/ 8/19/ 8/6/ Figure a. Abundance of flounder in the Muuga Bay according experimental catches in July and August Number of flounders per hours and net /16/ 7/18/ 7// 7// 7// 7/6/ y = -,996x R =,3761 p=. 7/8/ 7/3/ 8/1/ Figure b. Abundance of flounder in the second part of July according experimental catches in the Muuga Bay, rectangle 13

11 Catch per haul of net, kg 3 1 7/1/ 7/8/ 7/1/ 7// 7/9/ 8// 8/1/ 8/19/ 8/6/ Figure a. Catch of flounder per haul of net according fisher s reports in Muuga Bay (rectangle 13) in July and August Cathc per haul of net, kg y = -,1378x + 16 R =,71 p=. 7/16/ 7/18/ 7// 7// 7// 7/6/ 7/8/ 7/3/ Figure b. Flounder catch per haul of net in the Muuga Bay (rectangle 13) between 16 (th) and 3 (th) July,

12 Catch per haul of net, kg /1/ 7/8/ 7/1/ 7// 7/9/ 8// 8/1/ 8/19/ 8/6/ Figure 6a. Catch per haul of net according fisher s reports at rectangle 1 in July and August Catch per haul of net, kg y = -,381x + 89,7 R =,777 p=. 7/16/ 7/17/ 7/18/ 7/19/ 7// 7/1/ 7// 7/3/ 7// 7// 7/6/ 7/7/ 7/8/ 7/9/ 7/3/ Figure 6b. Flounder catch per haul of net at the rectangle 1 between 16 (th) and 3 (th) July,

13 Catch per haul of net, kg /1/ 7/8/ 7/1/ 7// 7/9/ 8// 8/1/ 8/19/ 8/6/ Figure7a. Catch per haul of net according fisher s reports at rectangle 18 in July and August Catch per haul of net, kg y = -,88x + 33, R =,71 p=. 7/16/ 7/18/ 7// 7// 7// 7/6/ 7/8/ 7/3/ Figure 7b. Flounder catch per haul of net at rectangle 18 between 16 (th) and 3 (th) July,