Introduction. Marcina C. P. Gemelgo 1, Célia L. Sant Anna 2,3, Andréa Tucci 2 e Heloiza R. Barbosa 1 - PDF

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Hoehnea 35(2): , 2 tab., 7 fig., Population dynamics of Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju, a Cyanobacteria toxic species, in water supply reservoirs in

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Hoehnea 35(2): , 2 tab., 7 fig., Population dynamics of Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju, a Cyanobacteria toxic species, in water supply reservoirs in São Paulo, Brazil Marcina C. P. Gemelgo 1, Célia L. Sant Anna 2,3, Andréa Tucci 2 e Heloiza R. Barbosa 1 Received: ; accepted: ABSTRACT - (Population dynamics of Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju, a Cyanobacteria toxic species, in water supply reservoirs in São Paulo, Brazil). The Guarapiranga and Billings reservoirs are main sources of public water supply to millions of people in the city of São Paulo, Brazil. They have been under intense antropic action as a result of domestic, industrial, farm and livestock waste being dumped in the reservoirs. Cyanobacteria develop very well in such an environment, producing blooms that are most often toxic. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju is a toxic species which is rapidly spreading all over the world and is abundant in the studied reservoirs. The goal of the study was to follow the year-round variation of the C. raciborskii population density and to correlate it with selected environmental factors. Samples were collected monthly on the surface of the water column and studied under a binocular optic microscope, whereas quantitative studies were carried out under an inverted microscope, according to the Utermöhl method. Among the phytoplankton community, organisms of the Cyanobacteria Class were represented by the greatest population density (cells ml -1 ). Cylindrospermopsis raciborskii was one of the abundant species in the Billings reservoir, both in the dry and rainy season. The principal environmental factors that influenced C. raciborskii population dynamics were water temperature, high ph values and low euphotic zone values. Key words: bloom, Cylindrospermopsis raciborskii, eutrophic reservoirs, phytoplankton RESUMO - (Dinâmica populacional de Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju, uma espécie tóxica de Cyanobacteria em reservatórios de abastecimento, SP, Brasil). Os Reservatórios Guarapiranga e Billings integram uma das principais fontes de abastecimento público da cidade de São Paulo, suprindo água para milhões de pessoas. Esses reservatórios estão sofrendo intensa ação antrópica devido a despejos domésticos, industriais e agropecuários. Em tais ambientes, Cyanobacteria desenvolvem-se intensamente, formam florações que, na maioria das vezes são tóxicas. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju é uma espécie tóxica e em expansão em todo o planeta, sendo uma das espécies abundantes nos reservatórios estudados. O objetivo do trabalho foi acompanhar a variação da densidade da população de C. raciborskii ao longo do ano, relacionando com os fatores ambientais estudados. As coletas mensais, realizadas na superfície da coluna d água, foram analisadas ao microscópio óptico binocular e a análise quantitativa foi feita ao microscópio invertido, conforme método de Utermöhl. A maior densidade (cel ml -1 ) da comunidade fitoplanctônica observada, foi representada por organismos da classe Cyanobacteria, em ambos os reservatórios. Cylindrospermopsis raciborskii foi uma das espécies abundantes no Reservatório Billings, nas estações seca e chuvosa. Os principais fatores ambientais que influenciaram na dinâmica de C. raciborskii foram: temperatura da água e ph elevados, assim como baixos valores da zona eufótica. Palavras-chave: Cylindrospermopsis raciborskii, fitoplâncton, florações, reservatórios eutróficos Introduction The Guarapiranga and Billings reservoirs are components of one of the main sources of public water supply in the metropolitan area of the city of São Paulo, providing water to millions of people and hundreds of industrial plants. Those reservoirs, like all reservoirs located near large urban centers, suffer intense antropic action due mostly to the discharge of household and industrial waste water and fertilizer, and to deforestation of surrounding areas. According to Zagatto et al. (1997), high nutrient concentration, mostly phosphates and nitrogen compounds, added to light intensity, water temperature 1. Universidade de São Paulo, Instituto de Ciências Biomédicas, Departamento de Microbiologia, ICB II, Av. Prof. Lineu Prestes, 1374, São Paulo, SP, Brasil 2. Instituto de Botânica, Caixa Postal 3005, São Paulo, SP, Brasil 3. Corresponding author: 298 Hoehnea 35(2): , 2 tab., 7 fig., 2008 (between 15 and 30 C) and ph values between 6 and 9, together favor the multiplication of phytoplankton species, leading to blooming. Cyanobacteria blooms have several environmental, social and economic consequences on continental waters around the globe and their ability to produce toxins also causes important losses to the public health sector. The competitive success of Cyanobacteria is based on their adaptive strategies, both physiologic and ecologic, which enable them to remain in the euphotic zone and to regulate their position within the water column in order to take greater advantage of light and nutrients (Klemer 1991). Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju, in particular, has been widely studied (Isvánovics et al. 2000, Padisák 1997, Padisák et al. 2003, Sant Anna et al. 2006) because it to produces blooms that interfere with water utilization and contains hepatotoxins (cyclic guanidinic alkaloid) and neurotoxins (carbamate-type alkaloids). The cylindrospermopsin-type hepatotoxin inhibits protein synthesis, thus damaging the structure and leading to necrosis of the liver, as well as of the kidneys, heart, lungs and gastric mucosa. The saxitoxin-type neurotoxin (known as Paralytic Shellfish Poison or PSP in short) blocks sodium channels in nerve cells, leading to paralysis, hypotension and respiratory failure (Kuiper-Goodman et al. 1999, Sant Anna et al. 2006). Padisák (1997) analyzed data about the occurrence, ecology, migratory patterns and distribution of Cylindrospermopsis raciborskii on four continents, and observed its dominance in different environments, resulting from its many abilities to compete and to resist herbivore organisms. According to Padisák (1997), the ecologic success of C. raciborskii is attributed to different factors such as floatability, tolerance to low light levels and high capacity to assimilate ammonium and phosphate. The occurrence and migratory patterns of C. raciborskii suggest that its wide distribution through tropical, subtropical and temperate zones is due to its great ability to disperse through water bodies and through birds and to its resistant akinetes. In view of the above and of the environmental and public health problems C. raciborskii has been causing, Komárek & Komárková (2003) emphasize the importance of carrying out detailed studies of the autoecology of this species. Several studies show Cylindrospermopsis raciborskii is widely distributed in Brazil but studies of its population dynamics are lacking. Among them it can be found the researches of Branco & Senna (1991, 1994), which studied taxonomic aspects of Cylindrospermopsis raciborskii in Paranoá Lake (center-west region of Brazil), Bouvy et al. (1999), which registered the dynamics of this species in an eutrophic reservoir in Pernambuco (northeast of Brazil), Komárková et al. (1999) which studied its morphology in a south Brazil coastal lagoon, and finally, Tucci & Sant Anna (2003) which studied C. raciborskii weekly variation in an eutrophic reservoir in São Paulo. Regarding the reservoirs analyzed in the course of this study there are even fewer studies on C. raciborskii dynamics and the only existing work is that of Souza et al. (1998). In that study the phytoplankton of a branch of the Billings reservoir was analyzed and the authors observed that C. raciborskii was the dominant species throughout the period studied. Thus, in view of the problems caused by this species and the importance of the reservoirs as sources of water provision to millions of people, the goal of this study was to analyze the population dynamics of C. raciborskii during a full seasonal cycle in two tropical water supply reservoirs, and to determine its relationship to the environmental factors that influenced the development of the organism. Material and methods The Guarapiranga and Billings reservoirs are part of the High Tietê basin and are located in the São Paulo, SP metropolitan area, in Brazil (table 1). Samples of material were collected on the surface of the water, every month, from February 2002 to January A specific sampling point was selected for each reservoir, at the location where water is captured for supplying to the consumer public. The following measurements were made: water temperature, transparency (Secchi Disk), euphotyc zone (Cole 1994), turbidity (Turbiditymeter), dissolved oxygen (Oxymeter OXI-197 TWT), conductivity (Conductivitymeter) and ph. The collected material was analyzed as follows: ammonium - NBR 10560, ABNT (1988); nitrate NO - 3, APHA (1998); nitrite NO - 2, APHA (1998); total phosphorus 4500P, APHA (1998) and chlorophyll a (CETESB 1990). Samples used for qualitative analysis of the phytoplankton were collected by means of a plankton net with a 20 µm mesh size, and fixed in 4% formaldehyde. Analysis of the material was made M.C.P. Gemelgo et al.: Cylindrospermopsis raciborski in water supply reservoirs 299 Table 1. General characteristics of the Guarapiranga and Billings Reservoirs (municipality of São Paulo). Guarapiranga Billings Coordinates 23º43 S and 46º32 W 23º47 S and 46º40 W Area 33 Km Km 2 Maximum profundity 13 m 18 m Water retention time 185 days 720 days under a binocular microscope whose optical train was fitted with a light chamber, a measuring eyepiece and an epifluorescence device. The following classification systems were used: Komárek & Anagnostidis (1989, 1999, 2005) for Cyanobacteria, Van den Hoek et al. (1995) for Chlorophyceae and Bourrelly (1985) for the remaining classes. Samples gathered for quantitative analysis of the phytoplankton were collected by means of a Van Dorn bottle and preserved in a 1% acetic lugol solution. Cell counts were established according to the method described by Utermöhl (1958), using an inverted Carl Zeiss microscope, under 400 Í magnification. Sedimentation time of the samples was three hours for each centimeter of height of the chamber, according to the criterion proposed by Lund et al. (1958). The sedimentation chamber used was a 2 ml one. Counting was carried out by means of horizontal and vertical transects and the minimum number of counted fields per sedimentation chamber followed the stabilization curve of the number of species, which was obtained based on new species added to each counted field. The dominant species were considered with superior densities to 50% of the total density of the sample.the abundant species were those with superior densities to the medium density of each sample (Lobo & Leighton 1986). Statistical analysis of results was made by multivaried analysis of data. Principal Components Analysis (PCA) was used in order to determine the variability of environmental data, in relation to the months studied (McCune & Mefford 1997). Results Abiotic variables - Data on physical and chemical variables are shown in figure 1 and 2 for the Guarapiranga and Billings reservoirs, respectively. They are transparency, euphotic zone, rainfall, water temperature, dissolved oxygen, ph, conductivity, turbidity, ammonium, nitrates, nitrites and total phosphorus. The Principal Components Analysis (PCA), applied to both reservoirs studieds herein, showed the two aquatic environments as two different units, grouping 68% of the total variability in the two first axes (it represents table 2, figure 3). Axis 1 summarized the variability for both systems, separating the reservoirs, Table 2. Pearson and Kendall correlation between environmental variables on the two first axes of the PCA ordination, as observed in the two reservoirs, Guarapiranga and Billings, during the period covered by the study (n = 24). Environmental variables Abbreviations Principal Components Axis 1 Axis 2 Water temperature WT Euphotic zone Euphz Turbidity Turb Conductivity Cond ph ph Dissolved oxygen DO Ammonium + NH Nitrate - NO Total phosphorus TP Chlorophyll a Chlo a 300 Hoehnea 35(2): , 2 tab., 7 fig., 2008 according to the environmental variables, as well as in gradient seasonal tracking the axis 2: on the positive side of Axis 1 (53% of explained variance) the sampling units of June, July, August and October were ordered, associated to the high values of nitrite and euphotic zone, in the Guarapiranga reservoir. On the negative side of Axis 1 the sampling units of February, June, August, October, November, December and January, during which the highest of conductivity, turbidity, dissolved oxygen, total phosphorus and ph values, in the Billings reservoir. On the negative side of Axis 2 (15% of explained variance) the sampling units of March, April and January associated to the high values of temperature of the water, in both reservoirs. Phytoplankton community - Quantitative A B C D E Figure 1. Monthly variation of physical and chemical parameters of Guarapiranga reservoir: euphotic zone (m, - -); precipitation (mm, - -) and water temperature ( o C, - -); dissolved oxygen (mg L -1, - -) and ph (- -); conductivity (µs cm -1, - -) and turbidity (UNT, - -) in A, B, C and D; nutrient concentrations (- - ammonium, - - nitrate, nitrite, - - phosphorus total) in E. Months are represented from February (F) through December (D) 2002 and January (J) 2003. M.C.P. Gemelgo et al.: Cylindrospermopsis raciborski in water supply reservoirs 301 analyses of samples from the Guarapiranga reservoir yielded 178 taxa distributed among nine classes. In the Billings reservoir 142 taxa were identified, distributed among eight classes. Chlorophyceae was the class qualitatively best represented in both Reservoirs, with 88 taxa (49%) in the Guarapiranga Reservoir and with 61 taxa (42%) in the Billings Reservoir. Cyanobacteria was the second best represented class in each of the Reservoirs, with 34 taxa (20%) in the Guarapiranga and 35 taxa (26%) in the Billings reservoir. Bacillariophyceae was represented by 10% of the identified taxa in each of the reservoirs. Xanthophyceae was present only in the Guarapiranga Reservoir. From the quantitative standpoint, Cyanobacteria is the class presenting the greatest annual density in cells ml -1 in both reservoirs. Figure 4 show the percentage of phytoplankton classes in relationship to chlorophyll a in the studied reservoirs. A B C D E Figure 2. Monthly variation of physical and chemical parameters of Billings reservoir: euphotic zone (m; - -); precipitation (mm; - -) and water temperature ( o C, - -); dissolved oxygen (mg L -1, - -) and ph (- -); conductivity (µs cm -1, - -) and turbidity (UNT, - -) in A, B, C and D; nutrient concentrations (- - ammonium, - - nitrate, nitrite, - - phosphorus total) in E. Months are represented from February (F) through December (D) 2002 and January (J) 2003. 302 Hoehnea 35(2): , 2 tab., 7 fig., 2008 Figure 3. Biplot ordination resulting from the PCA applied to the sampling units with the physical, chemical and biological variables, in the Billings and Guarapiranga reservoirs. Months are represented from B02=February, B03=March, B04=April, B05=May, B06=June, B07=July, B08=August, B09=September, B10=October, B11=November, B12=December of 2002 and B01=January of 2003; G02=February, G03=March, G04=April, G05=May, G06=June, G07=July, G08=August, G09=September, G10=October, G11=November, G12=December of 2002 and G01=January of Abbreviations for environmental variables are presented in table 2. Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju (figure 5) is characterized by single, straight or curved trichomas, cells with aerotopes, terminal heterocytes and cylindrical, subterminal akinetes. When comparing the density of C. raciborskii (figure 6) with densities of other Cyanobacteria in the Guarapiranga reservoir, C. raciborskii occurred in February, May, November, December 2002 and January 2003 and was one of the abundant species in February, reaching 20% of the total density of all Cyanobacteria. In the Billings reservoir it occurred during the entire period of the study and was abundant in the dry (May, June and August 2002) and rainy (November and December 2002, and January 2003) seasons (figure 6). The figure 6 show a comparison of C. raciborskii density with that of other Cyanobacteria species and of clorophyll a, for both reservoirs. In figure 7, the annual densities of phytoplankton classes are compared to the density of C. raciborskii, the latter being larger than the density of all other phytoplankton classes. Discussion The composition of the phytoplankton community in the two reservoirs, Guarapiranga and Billings, revealed that the Chlorophyceae class, mostly represented by the Chlorococcales order, was the one with the largest number of taxa. These results seem to apply to other eutrophized reservoirs in Brazilian tropical regions and are consistent with those from several other authors: Beyruth (1996), Bouvy et al. (1999), Matsuzaki (2004), Sant Anna M.C.P. Gemelgo et al.: Cylindrospermopsis raciborski in water supply reservoirs 303 A B Figure 5. Photomicrograph of Cylindrospermopsis raciborskii with terminal heterocyte. Figure 4. Contribution of phytoplankton classes to total density and cloroplyll a in the Guarapiranga (A) and Billings (B) reservoirs. Months are represented from February (F) through December (D) 2002 and January (J) et al. (1989, 1997), Silva (1999) and Tucci & Sant Anna (2003). The Principal Component Analysis (PCA) showed that the physical and chemical variables that interfered in the temporal reservoirs dynamics were: water temperature, euphotic zone, turbidity, conductivity, ph and dissolved oxygen. Moreover, high nitrate and total phosphorus were available, allowing ideal conditions to phytoplankton blooms on both reservoirs. The PCA has also confirmed the difference between the reservoirs, showed by their separation through axis 1, also by a seasonal gradient through axis 2. Moreover, the observed high availability of total phosphorus, ammonium, nitrate and nitrite, help create ideal conditions for the formation of blooms by Cyanobacteria. Similar results were obtained by Huszar et al. (2000) in eight tropical lakes situated in different tropical regions of Brazil. The results of the present study confirm the high population density of the phytoplankton community in the Guarapiranga reservoir, the same observation having been made by Beyruth et al. (1997), who attributed the problem to the eutrophication of the water body. In our study, values upwards of 10 6 cells ml -1 were detected, mainly for Cyanobacteria. Important results obtained in the present study show that, starting in 2002, the density of Cylindrospermopsis raciborskii (Wolosz.) Seen. & Subba Raju, was high. This species had not been found in this reservoir before 2000 (C. L. Sant Anna, unpublished data). The present research also shows an increase in the number of taxa of the Cyanobacteria class in relation to the number found by Beyruth (1996), who identified 14 taxa of that class. This present study shows that the number of taxa have risen to 34 and including the presence of Cylindrospermopsis raciborskii. This fact is probably due to urban human settlements in the reservoir area, a phenomenon that has been growing in the last years and leads to eutrophication (Beyruth et al. 1997). Urbanization, as well as other human activities, when carried out improperly or in the absence of adequate planning, cause sometimes irreversible damage to the capacity of water
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