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Acta Limnologica Brasiliensia, 2014, vol. 26, no. 4, p. 442-456 http://dx.doi.org/10.1590/S2179-975X2014000400011 Limnological characterisation and seasonal variation in a subtropical shallow (Guaiba Lake, Brazil): a long-term study Caracterização limnológica e variação sazonal do fitoplâncton em um lago raso subtropical (Lago Guaíba, Brasil): estudo de longa duração Rodrigo da Rocha Andrade1 and Danilo Giroldo2

1Laboratório de Biologia Aquática e Ecotoxicologia, Departamento Municipal de Água e Esgotos – DMAE, Rua Barão do Cerro Largo, 600, CEP 90850-110, Porto Alegre, RS, Brazil e-mail: [email protected] 2Programa de Pós-Graduação em Biologia de Ambientes Aquáticos Continentais, Instituto de Ciências Biológicas – ICB, Universidade Federal do Rio Grande – FURG, CEP 96201-900, Rio Grande, RS, Brazil e-mail: [email protected]

Abstract: Aim: to provide a long-term limnological characterisation of a subtropical shallow lake in addition to verifying seasonal differences, including phytoplankton variation. Methods: monthly sampling at sites IP, SJ and MD from 2000 to 2009 to

analyse temperature - T; depth - Z; the depth of the euphotic zone - Zeu; Zeu/Z (%); total suspended solids – TSS; dissolved oxygen – DO; pH; electrical conductivity - EC;

N-NH3, N-NO2, N-NO3; soluble reactive - SRP; chlorophyll a - Chl-a

and phytoplankton. Results: low values of Z and Zeu characterised the shallow and turbid conditions of lake and corresponded to the contribution of nano-microflagellates (Chlamydomonas sp., Spermatozopsis sp., Cryptomonas sp. and Rhodomonas sp ) and diatoms

(Aulacoseira granulata). Zeu/Z (%), SRP and Chl-a were significantly different at site IP (meso-eutrophic) compared to sites SJ and MD (eutrophic). Phytoplankton density was also significantly higher at sites SJ and MD, and the largest relative contribution of Actinastrum sp., Dictyosphaerium sp., Micractinium sp., Monoraphidium sp., Scenedesmus/ Desmodesmus sp. and Euglena sp. corresponded to the most polluted at site SJ. The significantly higher T (°C) in corresponded to significantly higher Chl-a as well as a greater richness and density of phytoplankton. Cocconeis sp., Gomphonema sp. and Pinnularia sp. (pennated diatoms) were negatively correlated with temperature and were therefore more representative at the three sites in . Asterionella formosa was correlated with SRP and vernal blooms were recorded (2000-2001). Planktothrix isothrix and Planktothricoides raciborskii were expressive in the summer/late summer (2004-2005), and were significantly correlated with Chl-a and low SRP in column. Conclusions: The study corroborated the sensitivity of phytoplankton in characterising different stages of at different sites and corresponding watersheds as well as in characterising different seasons in a shallow lake in the subtropical zone of Brazil. Keywords: freshwater, , cyanobacteria, eutrofication.

Resumo: Objetivo: prover caracterização limnológica de longa duração e verificar as variações sazonais associadas ao fitoplâncton em um lago raso subtropical no sul do Brasil. Métodos: coletas mensais em três locais (IP, SJ e MD), de 2000 a 2009, para as seguintes

análises: temperatura - T; profundidade - Z; profundidade da zona eufótica - Zeu/Z (%); sólidos suspensos – TSS; oxigênio dissolvido – DO; pH; condutividade - EC;

N-NH3, N-NO2, N-NO3; fósforo solúvel - SRP; clorofila-a - Chl-a e fitoplâncton.

Resultados: baixos valores de Z e Zeu caracterizaram a condição túrbida e rasa do lago e corresponderam à contribuição de Aulacoseira granulata e de flagelados nano- microplanctônicos dos gêneros Chlamydomonas sp., Spermatozopsis sp., Cryptomonas sp.

e Rhodomonas sp dos grupos X2 e Y. Zeu/Z (%), SRP e Chl-a foram significativamente menores no ponto IP (meso-eutrófico) comparado aos pontos SJ e MD (eutróficos) onde a densidade do fitoplâncton foi significativamente maior. A maior contribuição relativa de gêneros Actinastrum sp., Dictyosphaerium sp., Micractinium sp., Monoraphidium sp., Scenedesmus/Desmodesmus sp. e Euglena sp. ocorreu nas águas mais poluídas do ponto SJ. T média significativamente maior no verão correspondeu aos maiores valores médios de Chl-a e às maiores riqueza e densidade do fitoplâncton. Diatomáceas penadas (Cocconeis 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 443

sp., Gomphonema sp., Pinnularia sp.) foram negativamente correlacionadas à T e foram mais representativas no ponto IP, provavelmente em função da maior vazão do rio Jacuí. Asterionella formosa foi correlacionada ao SRP e florações vernais foram registradas entre 2000 e 2001. Planktothrix isothrix e Planktothricoides raciborskii foram expressivas no verão dos anos de 2004 e 2005 e foram significativamente correlacionadas à Chl-a e associadas à períodos de baixos valores de SRP na coluna d’água. Conclusões: o estudo confirmou a sensibilidade do fitoplâncton em caracterizar diferentes estágios de eutrofização, bem como, caracterizar diferentes estações do ano em um lago raso subtropical do Brasil. Palavras-chave: água doce, algas, cianobactérias, eutrofização.

1. Introduction due to the marked seasonality in these regions (Huszar et al., 2005). Several long-term studies The artificial enrichment of inland waters with have been performed to establish not only patterns , mainly N and P, results from sewage of phytoplankton fluctuations but also to verify from urban, industrial and agricultural alterations in these patterns over the years due regions (Huszar et al., 2005). This process, to hydrological, nutritional and climatic changes referred to as eutrophication, has worldwide (Elliott, 1990; Anneville et al., 2004). negative repercussions, causing serious damage In tropical zones, temperature is not a to water supplies, notably during treatment for human consumption (Tundisi et al., 2006; limiting factor for phytoplanktonic development. McGowan et al., 2012), and changes in aquatic , the morphometry of water bodies, the and related biological communities, use and occupation of watersheds and the frequency, mainly phytoplankton (Istvánovics, 2009). distribution and amount of rain, in addition to Phytoplankton represents an important food the velocity and direction of winds are the most source for consumers in the of inland important factors for explaining the occurrence, waters and is important when assessing water structure and variation of phytoplankton (Huszar, quality (Demir and Atay, 2002), as it acts as a 1996). refined sensor of environmental conditions and Brazil is a continental country located an accurate indicator of environmental changes between the tropical and subtropical zones, (Alvarez-Cobelas et al., 1998). Phytoplankton and its inland waters are mainly represented communities are generally grouped into classes by , , dams and shallow coastal for taxonomic description and for summarising and . A study conducted across the ecological status of aquatic environments. Brazil showed that the conditions in most of its More recently, phytoplankton functional groups inland water bodies ranged from mesotrophic to or assemblages, which are groupings of species eutrophic (Abe et al., 2006) due to population and genera based on similar sensitivities and and economic growth in their corresponding tolerances, have been proposed to improve watersheds, which has compromised the quality analyses of ecological status and water quality of water supplies and of water for other uses, (Reynolds et al., 2002; Reynolds, 2006; mainly due to the occurrence of cyanobacterial Padisák et al., 2006, 2009). blooms (Sant’Anna et al., 2008). Despite its Because the growth of planktonic algae and significance for predicting events and the cyanobacteria is associated with the availability identification of environmental changes, of light and nutrients (Reynolds, 2006), such as those related to climate, hydrology, characterisation of phytoplankton is important eutrophication and oligotrophication (Barbosa in describing trophic states and in limnological and Padisák, 2004; Valdes-Weaver et al., 2006), characterisation (Bellinger and Sigee, 2010), as there long-term limnological studies in inland waters is a direct relationship between planktonic dynamics are scarce in Brazil (Seeliger et al., 2002). and nutritional levels associated with rivers, dams The aim of this study was to provide a long- and lakes (Wetzel, 1983). term limnological characterisation of a subtropical Phytoplankton varies in time and space at shallow lake from southern Brazil (Guaiba Lake), in different scales (Abreu et al., 2010). Models have addition to verifying seasonal differences, including related phytoplankton variability to the influence of quali-quantitative phytoplankton concentrations in inland waters of temperate zones variation. 444 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia

2. Material and Methods In the region of the lake, the climate is humid subtropical (soft mesothermal), categorised as Cfa in 2.1. Study area Köppen classification (Köppen, 1948). The average minimum and maximum air temperature values Guaiba Lake (29°55’-30°24’ S; 51°01’-51°20’ range from 14.8 °C (winter) to 24.2 °C (summer), W) is located in the Central Depression of Rio and the annual average accumulated Grande do Sul State, Brazil. It extends from the ranges from 1,324 mm (Livi, 1998) to 1,366 mm north, in the region of the mouths of rivers that (Vieira and Rangel, 1988). form the Jacuí Delta, to the south, in the Itapua Guaiba Lake is an important water supply tip, where it flows into Patos (Figure 1). source for the surrounding cities as well as The length of the lake is approximately 50.0 km, supporting other uses related to economic and and its width ranges from 0.9 to 19.0 km. The commercial activities (Bendati et al., 2003). The surface area of the lake is approximately 496 km2 most frequent perturbations in this (Nicolodi et al., 2010), and its depth is highly are caused by agriculture processes, urbanisation variable, averaging two meters (Bendati et al., 2003). and domestic and industrial sewage discharges The rivers that form the Jacuí Delta contribute (Terra et al., 2009). Five water intake facilities are 3 –1 an average flow of 2,193 m .s , with 84.6% of the operated by the Departamento Municipal de Água volume being attributed to the Jacuí , 7.5% e Esgotos – DMAE (water and wastewater public to the dos Sinos River, 5.2% to the Caí River and works) of Porto Alegre city, three of which have not 2.7% to the Gravataí River. As carriers of sediment, changed the location of water intake and have been the rivers lose competence toward the broad monitored by DMAE since the 1970s. This database depositional basin, and the rates of constitutes a potential data source for long-term –1 coarse material range from 3.5 to 8.3 mm.year . limnological studies and production of information Guaiba Lake stores a volume of approximately (Andrade and Giroldo, 2010). 1.5 billion m3 of water. The river output, water level fluctuations in Patos Lagoon and the direction and 2.2. Sampling and analysis intensity of winds are the main factors controlling Sampling was carried out monthly between the flow dynamics in this area. Thus, the lake is January 2000 and December 2009. The samples not only an extension of the rivers but represents a were collected just below surface, in the water type of tank that is closely linked to Patos Lagoon column at three sites (n = 360): Ilha da Pintada - IP; (Nicolodi et al., 2010). São João/Navegantes – SJ; and Menino Deus - MD

Figure 1. Study area and the IP, SJ and MD sampling sites in Guaiba Lake, Rio Grande do Sul State, Brazil. 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 445

(Figure 1). The field analysis included the genera that, on average, represented 0.1% or more measurements of the following parameters: water of the total density of the samples were considered temperature (°C) – T, using an alcohol thermometer; to represent descriptive taxa (Bicudo et al., 2006). depth (m) – Z, using a graduated weighted rope and Descriptive and inferential statistics were transparency (m), using a Secchi disk. The depth determined using the Kruskal-Wallis (K-W) test of the euphotic zone - Zeu (m) was calculated as at a significance level of at least 95% (p < 0.05) three times the Secchi disk extinction depth (Cole, for the set of limnological variables and the data 1994). In the laboratory, the following limnological on the richness and density of phytoplankton (log variables were analysed: total suspended matter transformation), and all data were grouped into (mg.L–1) – TSS, via a gravimetric method (ABNT, sites and seasons. The data were framed by season 1989); dissolved oxygen (mg.L–1) – DO, using according the official calendar of the U.S. Naval the Winkler volumetric method (ABNT, 1988); Observatory (USNO) for the southern hemisphere, –1 pH and electrical conductivity (µS.cm ) – EC, where the summer conventionally starts on with an electrometric method (ABNT, 1999a, December 21, on March 21, winter on 1999b); and – N-NH3, – N-NO2, June 21 and on September 23. - N-NO3 and soluble reactive phosphorus To summarise the obtained data, a matrix –1 (µg.L ) – SRP, via ion chromatography (USEPA, of the standardised means (z scores) of the –1 1986, 1993). Chlorophyll-a - Chl-a (µg.L ) limnological variables and phytoplankton richness determination was carried out following 90% and density data for each season at each site was acetone extraction through spectrophotometric used to perform a principal component analysis analysis (APHA, 1998). (PCA). Pearson’s correlations were provided to For phytoplankton analyzes the samples were investigate the relationships between the densities collected by direct passage of bottles in the sub- of descriptive taxa with limnological variables surface of the . During transport at p < 0.05 significance level. All descriptive, (up to 2 hours), the samples remained chilled (8 inferential and multivariate statistics were obtained °C) to its preservation in the laboratory. Non- using Paleontological statistics software package preserved aliquots were analysed qualitatively under for education and data analysis - PAST freeware a microscope to survey algae genera, which were (Hammer et al., 2001). identified mainly according Bicudo and Bicudo (1970), Bicudo and Menezes (2005) and Bourrelly 3. Results (1970, 1972, 1981). Some previously identified species were recorded in this study. Aliquots 3.1. Limnological characterisation were preserved with 0.5% acetic Lugol solution (Vollenweider, 1974) Due to the large number The water temperature varied from 10.4 °C at of samples collected and analyses performed, the SJ site to 29.5 °C at both the SJ and MD sites several Brazilian sanitation companies adopt ( 1). IP was the shallowest site, although the quick protocols for phytoplankton identification average Zeu values were not significantly different and quantification in order to standardize results. between the sites. However, the Zeu/Z ratio (%) was Tests between laboratories have shown similar significantly higher at IP in relation to the other and satisfactory results obtained using counting sites, while that at MD was significantly lower in chambers (Sedgwick-Rafter) compared to the relation to the SJ site. The MD and SJ sites were traditional sedimentation method with Utermöhl significantly different from site IP in terms of higher chambers (Müller et al., 2010). Thus phytoplankton values of Z, N-NO2, SRP and Chl-a and lower was quantified in Sedgwick-Rafter chambers values of pH and DO. The SJ and MD sites were (length: 50 mm; width: 20 mm; height: 1 mm, significantly different in that a higher value of Z volume: 1 mL) with the aid of a Whipple reticule was observed at the MD site, while higher values coupled to the ocular of a light microscope. The of the Zeu/Z ratio (%), TSS, EC and N-NH3 were genera were quantified in random fields or bands, found at the SJ site. On the other hand, the highest and whenever possible, one hundred individuals of concentration of N-NO3 was detected at the MD a predominant genus were quantified as described site, which was not significantly higher at the IP and in APHA (1998). SJ sites, while the Chl-a values were significantly The genera were grouped into taxonomic classes lower at site IP, by almost two times, in relation to according to Van den Hoek et al. (1995). The algae sites SJ and MD. 446 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia <0.001 <0.001 <0.001 <0.001 <0.001 <0.05 >0.05 <0.001 <0.05 <0.05 <0.001 <0.05 <0.05 <0.05 <0.05 <0.001 <0.001 <0.001 <0.05 <0.001 <0.05 <0.05 >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 <0.05 >0.05 >0.05 >0.05 >0.05 <0.001 <0.001 <0.001 p -value (season) 2.5 2.5 2.5 0.6 0.9 1.0 0.5 0.4 0.4 16.5 14,957 5.5 22.2 17.6 1.3 0.7 1.0 0.7 0.3 0.3 0.3 7.1 17.1 14.0 195.1 402.4 403.9 2.3 11.5 11.3 228.3 243.0 248.8 38.4 51.3 55.1 2.7 2.4 2.2 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± c c d d b b b b a b b b b b b d a b b b a a a a a a a a a a a a a d b b Spring a,b a,b a,b,c 1.0 4.1 6.8 1.1 1.1 7.3 5.7 7.2 7.0 4.7 2.8 3.6 2.8 11.1 7.1 15.4 21.6 21.9 22.2 10.0 28.5 26.7 27.6 23.6 50.9 81.4 76.6 24.0 23.6 41.3 77.8 85.2 5.6 197.3 769.7 759.1 488.5 520.1 503.6 2.0 2.0 1.6 0.5 0.5 1.0 0.5 0.3 0.4 12.1 5.3 5.4 23.4 10.7 1.5 0.4 1.0 0.8 0.2 0.2 0.4 5.2 19.0 15.5 129.3 331.1 508.5 3.0 12.7 8.7 301.3 324.2 369.7 39.5 56.2 53.1 0.8 2.8 4.6 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± c c c c c c c b b b a b b b b b b b b b b b a a a a a a a a a b a a a a b Winter b,c b,c 8.9 6.8 1.0 2.4 4.2 6.8 1.1 1.2 6.6 7.1 6.9 6.9 4.7 2.6 1.1 11.6 15.9 15.9 16.0 10.1 25.6 26.5 25.4 24.0 51.0 84.5 79.7 18.8 20.1 32.8 71.8 70.3 15.7 156.0 802.6 876.6 524.9 613.2 609.9 3.5 3.5 3.2 0.5 0.5 0.7 1.7 0.5 0.6 4.6 8.4 6.9 16.4 10.4 8.8 0.9 1.1 0.8 0.3 0.2 0.2 10.3 23.3 14.7 106.9 592.8 398.1 4.8 13.7 244.6 324.5 356.8 372.6 35.6 59.1 24.3 1.3 3.2 16.7 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± b b b b b b a a a b a b b a b b a a a a a a a a a a a a a a b b b Autumn a,b a,b a,b a,b a,b a,b 4.0 6.7 9.8 1.9 1.5 8.1 6.0 6.1 7.2 7.0 5.6 1.5 3.0 7.5 1.4 7.1 19.3 19.3 20.7 50.5 20.3 15.2 55.6 92.9 83.2 24.3 69.6 32.3 77.2 113.4 19.2 20.4 17.1 143.0 877.5 737.6 464.4 507.3 502.3 1.4 1.2 1.5 0.4 0.5 0.9 0.5 0.4 0.4 2.8 7.7 5.7 8.2 7.7 7.6 0.6 0.9 0.8 0.3 0.2 0.3 4.9 15.1 10.4 73.1 406.1 264.8 5.6 16.0 75.8 174.1 186.8 176.3 34.4 54.6 38.1 0.4 7.3 6.2 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a a Summer 3.6 6.2 9.5 1.1 1.5 1.5 7.0 5.4 5.7 7.4 7.2 7.2 5.4 3.5 7.5 7.6 26.8 27.4 43.9 23.5 12.8 17.9 54.8 88.6 26.0 28.9 65.3 26.9 15.7 16.0 76.3 38.0 48.9 911.0 141.7 375.2 382.6 628.2 406.4 >0.05 >0.05 <0.05 >0.05 (sites) <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 p -value 4.6 4.8 4.5 0.6 0.7 0.9 1.1 0.5 0.5 30.5 7.7 5.9 19.1 12.9 12.1 1.0 1.1 0.9 0.3 0.3 0.3 7.5 19.1 13.9 136.9 448.7 448.7 4.1 13.6 38.0 263.3 289.8 299.5 36.8 54.8 53.5 3.7 4.8 9.2 ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± c c c a a a a b a a a a b a b a a b b a b b a a a b b a b b a a a a b b a b b 9.8 1.3 6.1 7.1 5.0 4.0 6.6 1.2 5.9 7.2 7.1 4.2 7.8 5.1 1.5 2.7 Site 13.3 78.9 21.2 34.1 21.4 20.3 26.3 69.2 21.4 18.7 22.9 86.8 23.5 73.2 53.1 38.8 21.4 160.9 853.6 506.0 853.6 495.8 461.4 IP IP IP IP IP IP IP IP IP IP IP IP IP SJ SJ SJ SJ SJ SJ SJ SJ SJ SJ SJ SJ SJ MD MD MD MD MD MD MD MD MD MD MD MD MD ) ) ) ) ) –1 –1 ) –1 ) ) –1 –1 –1 –1 –1 (µg.L (µg.L (µg.L 2 3 3 Variable (m) /Z(%) eu eu T (°C) T Z (m) Z Z TSS (mg.L DO (mg.L pH EC (µS.cm N-NH N-NO N-NO (µg.L SRP Chl- a (µg.L test results (p-values); different letters: significant differences of values at p < 0.05. of letters: significant differences different (p-values); Lake and K-W test results in Guaiba and seasonal mean ± sd of variables Sites Table 1. 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 447

With respect to seasonal limnological variation contribution of Bacillariophyceae was higher at (Table 1), there were significant differences between SJ in relation to the IP and MD sites. When the the average temperatures detected in the four average sampled richness was considered, rather seasons at site IP. The autumn and spring average than the cumulative results of the inventory, it was T values were significantly different on the sites IP found to be significantly higher at the SJ and MD and SJ. On the other hand, the average value of sites than at site IP (p < 0.001). For all samples, the Z was significantly lower in summer for the three average density at site IP was 354 ind.mL–1, which sites. The euZ /Z ratio (%) was not significantly was significantly lower than the average density different between summer and autumn for the at SJ (732 ind.mL–1) and MD (609 ind.mL–1). IP and MD sites. Similar to the seasonal average The inferential tests confirmed that the average temperatures at site IP, DO showed values that were phytoplanktonic richness at site IP was significantly significantly higher in winter than summer. At the higher in summer compared to the other seasons SJ site, the average dissolved oxygen in spring was (Figure 2). At the SJ site, the average richness in not significantly different from that in the other autumn and winter was significantly lower than seasons, whereas at the MD site, the average DO the richness in spring and summer, while at the was significantly higher only in winter. The average MD site, it was only possible to confirm that the pH values were substantially and significantly richness in autumn was significantly lower than the higher in summer for the three sites, whereas the richness in summer. In turn, the average summer variables EC, N-NH3, N-NO2, N-NO3 and SRP densities at the IP and SJ sites were significantly showed almost no significant differences in terms higher compared to the other seasons, while at site of the average seasonal variations, except that EC MD, it was only possible to conclude that the winter was significantly lower in summer at the IP site, densities were significantly lower than the densities and N-NO3 was significantly lower in summer in the other seasons. compared to winter at the SJ site. The average The most representative taxa belonged to seven values of Chl-a presented a directly proportional taxonomic classes (Table 2). The IP site stood out correspondence to temperature and an inversely due to the major contributions of Bacillariophyceae proportional correspondence to DO at site IP, genera (Aulacoseira sp., Cocconeis sp., Gomphonema whereas at the SJ and MD sites, only the summer sp., Pinnularia sp., unidentified diatoms), in the average values of Chl-a were significantly higher in density of phytoflagellates from the Cryptophyceae relation to other seasons. (Cryptomonas sp.) and Euglenophyceae (Euglena sp., Strombomonas sp., Trachelomonas sp.) classes and based 3.2. Phytoplankton on the higher density of phytoflagellates from class Two hundred and fourteen taxa of planktonic Chlorophyceae, such as Eudorina sp., Spermatozopsis algae and cyanobacteria were inventoried, with sp. (Spermatozopsis exsultans Korshikov) and one hundred ninety-eight being identified to the colourless flagellates of class Chrysophyceae genus level and the others to the suprageneric (Cladomonas sp., Rhipidodendron sp.). level (7.4%). The most representative taxonomic The SJ and MD sites stood out in showing classes in terms of richness were Chlorophyceae the lowest relative contribution among the (30.8%) and Bacillariophyceae (24.8%), followed identified genera of Bacillariophyceae, except for by Cyanophyceae (13.6%), Chrysophyceae (9.3%), Asterionella sp. (Asterionella formosa Hassal), in Euglenophyceae (7.0%) and Zygnematophyceae the higher relative contribution of Chlorophyceae (6.5%). Cryptophyceae represented 2.3% of (Actinastrum sp., Dictyosphaerium sp., Micractinium the observed richness, while the other classes sp, Monoraphidium sp., Scenedesmus /Desmodesmus each contributed 1.4% of the richness sp.) and due to the higher density of Cryptophyceae (Dinophyceae, Prasinophyceae, Raphidophyceae and Euglenophyceae. The genera Cyclotella sp. and Xanthophyceae). The survey quantified one and Nitzschia sp. as well as phytoflagellates of hundred eighty-four taxa for site IP, one hundred different classes, such Peridiniales NI, Bicosoeca seventy-nine for site MD and one hundred sixty- sp., Chromulina sp. Synura sp. and Rhodomonas five taxa for site SJ (Figure 2). The richness of sp. (Rhodomonas minuta v. nannoplanctica Skuja), class Chlorophyceae was slightly higher at the IP were more expressive at the MD site in relation to and MD sites in relation to the SJ site. On the SJ and IP sites. other hand, the absolute and relative contribution The highest phytoplankton density (Figure 3) of Chrysophyceae was lower, while the relative generally occurred in January (summer), while 448 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia

Figure 2. Absolute and relative contributions of taxonomic classes and sites and seasonal variations of richness and density of phytoplankton in Guaiba Lake; different letters indicate significant differences of values at p < 0.05. the lowest density occurred in July (winter) than the annual summer increases, were observed within the annual cycles. Almost all of the most in spring at all sites. In 2000, a considerable representative taxonomic classes experienced an contribution of Bacillariophyceae at site SJ it was increase in density towards summer in the annual observed in late winter (September), when the cycles, whereas the most representative groups in density of diatoms was 1,863 ind.mL–1, mainly winter were Bacillariophyceae and Cryptophyceae. contributed by Asterionella sp., and there were low Some density increments, which were generally less increments of density between winter and spring. 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 449

Figure 3. Temporal profile of density classes of phytoplankton in Guaiba Lake.

In that year, Asterionella sp. represented 70% of In January 2007, cyanobacteria also contributed the phytoplanktonic density (283 ind.mL–1) at the to the phytoplankton densities at the three sites, and MD site. in 2008, the contribution of cyanobacteria persisted In the summer months and early fall of 2004, until early autumn at the MD and SJ sites. there was a greater contribution of cyanobacteria 3.3. Relationship between phytoplankton and belonging to the taxa Planktothrix/Planktothricoides limnological variables , i.e., P. isothrix (Skuja) Komárek & Komárková and P. agardhii (Gomont) Anagnostidis & Komárek as The PCA accounted for 85.5% of the variation well as Planktotricoides raciborskii (Woloszynska) in the analysed system (Figure 4). The first axis Suda & Watanabe at sites SJ and MD, and in 2005, (56.9%) represented the longitudinal distribution a similar situation was observed at sites IP and SJ. of sites, and it was positively and significantly related 450 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia

Figure 4. Biplot of seasonal units at the IP, SJ and MD sites and variable vectors on the first two PCA axes; su – sum- mer; sp – spring; wi – winter; au- autumn; in box: underlined numbers p <0.05, bold numbers p < 0.001.

to EC, N-NH3, N-NO2 and SRP, with higher among these genera, Asterionella sp. was associated concentrations of Chl-a being associated with a with higher levels of SRP (r = 0.427), which were higher density and richness of phytoplankton at observed at the MD and SJ sites compared to site the SJ and MD sites, regardless of the season. On IP (Table 2). Centric diatoms (Aulacoseira sp., the negative side, the first axis was correlated with r = 0.441; Cyclotella sp., r = 0.367) and stellate shallower and more transparent waters, together filaments of Nitzschia sp. (Nitzschia fruticosa with lower DO and Chl-a concentrations as well a Hustedt; r = 0.309) were associated with elevated lower richness and density of phytoplankton at site temperatures. Among the observed phytoflagellates, IP. The second axis (28.6%) represented the seasonal the genera Trachelomonas sp. and Euglena sp. variation in limnological variables and the density (Euglenophyceae) were correlated with the deeper and richness of phytoplankton. The temperature waters (r = 0.246 and 0.306), rich in N-NH3 increase toward the negative side of axis 1 was (r = 0.342 and 0.381), with high EC (r = 0.295 associated with increased pH and Chl-a values as and 0.395) and low DO levels (r = –0.472 and well as the density and richness of phytoplankton –0.398). Between green flagellates, Chlamydomonas towards the summer months for the three sites sp. (r = 0.350), Eudorina sp. (r = 0.365) and considered. At the three sites, the winter season Pandorina sp. (r = 0.367) were positively associated was mainly characterised by low temperatures and with temperature. However, only Chlamydomonas higher levels of TSS and DO. sp. were more associated with Zeu (r = 0.265) and Regarding the composition of genera, it was found higher EC (r = 0.302) and Chl-a values (r = 0.336). that pennated diatoms of the genera Asterionella Spermatozopsis exsultans was most strongly associated sp.(r = –0.166), Encyonema sp (r = –0.116)., Eunotia with a greater Zeu (r = 0.582).The most representative sp. (r = –0.130), Gomphonema sp. (r = –0.187) genera in terms of (Chl-a) were Aulacoseira and Pinnularia sp. (r = –0.161) were significantly sp. (r = 0.256) and Cyclotella sp. (r = 0.250), correlated (p < 0.05) with low temperatures, and Monoraphidium sp. (r = 0.204), Chlamydomonas sp. 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 451

Table 2. Average relative contribution (%) of descriptive (r = 0.336), Mallomonas sp. (r = 0.281), Cryptomonas taxa to the total density of phytoplankton at the IP, SJ sp. (r = 0.341) and dinoflagellates - PeridNI and MD sites in Guaiba Lake; NI – unidentified. (r = 0.290). The higher correlation of Planktothrix/ BACILLARIOPHYCEAE IP SJ MD Planktothricoides (Planktothrix isothrix and Asterionella sp. <0.1 3.1 0.8 Planktothricoides raciborskii) with Chl-a (r = 0.509) Aulacoseira sp. 7.8 4.0 5.7 Cocconeis sp. 0.3 0.2 0.1 was influenced by summer peaks, mainly in 2004 Cyclotella sp. 3.9 3.2 5.4 (MD and SJ) and 2005 (IP and SJ). Encyonema sp. 0.1 0.1 0.1 Pennate diatom NI 1.3 0.6 0.8 4. Discussion Eunotia sp. 0.1 0.1 0.1 The trophic status of a water body can roughly Gomphonema sp. 1.0 0.5 0.6 be assessed based on information regarding the Melosira sp. 0.6 0.3 0.4 concentration of the limiting nutrient, chlorophyll-a Navicula sp. 1.0 0.8 1.0 and transparency, which indicate algal biomass, Nitzschia sp. 5.8 5.5 6.0 Pinnularia sp. 0.3 0.2 0.2 sediment resuspension and penetration of light into CHLOROPHYCEAE the water. The most widely accepted limits of these Actinastrum sp. 0.1 0.5 0.4 variables have been suggested by OECD (1982) to Ankistrodesmus sp. 0.3 0.6 0.3 characterise the trophic categories (oligotrophic, Chlamydomonas sp. 7.6 8.1 7.1 mesotrophic and eutrophic) of inland waters Crucigenia sp. 0.4 0.4 0.6 (Istvánovics, 2009). In this study, the ranges of the Dictyosphaerium sp. 0.2 0.8 0.6 mean to maximum values of Chl-a at the IP, SJ and Eudorina sp. 0.4 0.2 0.2 MD sites were found to be 2.7-26.0, 4.2‑37.6 and Golenkinia sp. 0.2 0.1 0.1 5.0-88.9 µg.L–1, respectively. According to OECD Micractinium sp. 0.2 1.3 1.1 –1 Monoraphidium sp. 2.6 3.4 3.2 (1982), average values between 2.5 and 8.0 µg.L Oocystis sp. <0.1 0.2 0.2 characterise mesotrophic waters, while maximum –1 Pandorina sp. 0.2 0.3 0.2 values above 25.0 µg.L characterise eutrophic Pedinopera sp. 1.0 0.7 0.5 waters. The average SRP values were also higher Scenedesmus/Desmodesmus sp. 1.6 2.5 1.8 than the limit of 35.0 µg.L–1 of total phosphorus Spermatozopsis sp. 17.9 4.6 3.5 for mesotrophic waters at the SJ and MD sites, DINOPHYCEAE characterising these sites as eutrophic. Additionally, Peridiniales NI 2.1 2.3 2.5 the average Secchi disk values (Zeu/3) obtained CHRYSOPHYCEAE IP SJ MD at the three sites were less than 3.0 m, typical of Bicosoeca sp. 2.2 1.9 2.3 Chromulina sp. 0.2 0.2 0.4 eutrophic waters. Chrysococcus sp. 0.1 0.3 0.2 The lowest average SRP value obtained at the –1 Cladomonas sp. 0.4 0.1 <0,1 IP site (34.1 µg.L ) was coincident with the lowest –1 Codosiga sp. 0.4 0.1 0.4 average values recorded for EC (53.1 µS.cm ), Dinobryon sp. 0.1 0.1 0.1 dissolved inorganic (mainly in the form Mallomonas sp. 0.7 0.8 0.8 –1 –1 of N-NH3; 160.9 µg.L ), Chl-a (2.7 µg.L ) and Rhipidodendron sp. 0.3 <0.1 <0.1 the total phytoplankton density (354 ind.mL–1). Synura sp. 0.1 0.4 1.7 This set of parameter values characterised this site CRYPTOPHYCEAE as “less eutrophic” in relation to SJ and MD, which Chroomonas sp. 0.7 0.3 0.7 was also corroborated by the higher average DO Cryptomonas sp. 27.4 38.3 37.0 –1 Rhodomonas sp. 9.3 8.6 13.1 (7,8 mg.L ) and Zeu/Z (38.8%) values observed CYANOPHYCEAE at the IP site in relation to sites SJ and MD. These Anabaena sp. 0.8 0.4 0.3 data and the limits established by the OECD Merismopedia sp. 0.8 1.4 0.9 suggest meso-eutrophic conditions for site IP and Planktothrix/Planktothricoides sp. 3.3 2.2 2.8 truly eutrophic conditions for sites SJ and MD in Pseudanabaena sp. 0.3 0.5 0.5 Guaiba Lake. EUGLENOPHYCEAE The trophic statuses of the three sites investigated Euglena sp. 0.5 1.9 1.7 in this study were associated with their locations in Phacus sp. 0.1 0.1 0.1 different watersheds. The IP site is influenced by Strombomonas sp. 0.2 0.3 0.3 Trachelomonas sp. 1.8 3.1 3.3 the flow of the Jacuí River, which is the largest to the lake, approximately 1,850 m3.s–1, and whose basin is predominantly occupied by 452 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia agricultural activities (Noronha, 1998; Faria and (853.6 µg.L–1) values, the SJ site showed no Lersch, 2001). The trophic statuses determined at significantly different values regarding Chl-a or the the MD and SJ sites corresponded to the higher richness and density of phytoplankton in relation to occupancy of these basins in terms of population. the MD site. The SJ site is located downstream from Thus, the water quality at the latter two sites has the mouth of the Gravataí River, which is a tributary become more eutrophic, whether due to higher presenting a lowest flow rate (approximately 59 concentrations of nutrients and chlorophyll-a or m–3.s–1), highest human population density and the greater density of phytoplankton. This finding highest concentrations of pollutants in the region corroborates the idea that the structure and (Noronha, 1998). The apparently most polluted development of phytoplankton are influenced by condition observed at the SJ site in relation to the the hydrology and the use and occupation of the MD and IP sites coincided with the greatest relative corresponding watershed, as observed in the inland contribution of Chlorophyceae genera such as waters in tropical zones of Brazil (Huszar, 1996). Actinastrum sp., Ankistrodesmus sp., Dictyosphaerium In this study different taxonomic classes sp., Micractinium sp., Monoraphidium sp., and of phytoplanktonic algae had significantly Scenedesmus/Desmodesmus sp. and the greater relative higher density in eutrophic points (MD and SJ) contribution of phytoflagellate genera belonging compared to meso-eutrophic point, as well as, it to class Cryptophyceae (Cryptomonas sp.) and had significantly higher density in the summer Euglenophyceae (Euglena sp.) to the density of compared to other seasons. This finding revealed phytoplankton. Unicellular and coenobial/colonial that the traditional classification of phytoplankton green algae belonging the F, X1 and J functional taxonomic may be a limited tool in limnological groups are associated with shallow eutrophic systems assessment of lakes and rivers. Reynolds et al. (2002) (Padisák et al., 2009), while cryptomonads (X and has proposed of a functional classification scheme 2 Y groups) are linked to the availability of nutrients for the phytoplankton species that has been tested (Klaveness, 1988) and euglenoids (W group) to and it is considered as an important predictive tool. 1 the availability of (Tell et al., 2005). This classification scheme brings species with similar The increasing values of Chl-a, phytoplankton morphology, physiology, and together into density, EC, and some forms of nutrients at the IP, functional groups named using alphanumerical MD and SJ sites coincided with the water quality characters. Since then, tests using phytoplankton index (WQI) values observed over time in a long- have been constantly improved to qualify the term study (2000-2009) by Andrade et al. (2012), environments (Padisák et al., 2006). Regarding the composition of phytoplankton, in which the mean scores (and ranges) were found diatom genera, such as Cocconeis sp., Gomphonema to be 69.8 (regular), 51.3 (regular/bad) and 49.2 sp., Pinnularia sp. and unidentified diatoms, (bad) for these sites, respectively. This comparison referred to as DiaPenNI, showed a higher relative confirmed the sensitivity of the composition and contribution at the IP site in relation to the others. density of phytoplankton in indicating different According to Padisák et al. (2009), some pennated trophic conditions as well as the different water diatoms belonging to the MP functional group quality conditions observed at the sites investigated are indicators of river flows, which agrees with the in the present study. hydrodynamic characterisation of site IP, which is For the three sites, there were higher influenced by the greatest river flow. In contrast, relative densities of the genera Aulacoseira sp., the genus Asterionella sp. showed a higher mean Chlamydomonas sp., Spermatozopsis sp., Cryptomonas density at sites SJ and MD. This exception agrees sp. and Rhodomonas sp. According to Reynolds with studies showing that blooms of A. formosa (2006), Aulacoseira species (P group, Aulacoseira are associated with higher phosphorus availability granulata v. angustissima (O. Müller) Simonsen) are in certain periods of seasonal variation, especially meroplanktonic (spending one phase of life in the the vernal period in temperate zones of the Earth sediment and another in the pelagic zone) and can (Sommer, 1988). A. formosa belongs to the C be significant in shallow lakes under meso-eutrophic functional group, indicating eutrophic small and conditions when exposed to wind and wave action, medium-sized lakes that are sensitive to the onset as occurs in the investigated lake (Nicolodi et al., of stratification (Padisák et al., 2009). 2010). Nano-microplanktonic flagellates (X2 and Despite exhibiting significantly higher average Y groups) belonging to the genera mentioned –1 –1 TSS (22.9 mg L ), EC (86.8 µS.cm ) and N-NH3 above are collectively common and constitute 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 453 representative assemblages in shallow lakes whose season showing the lowest values of accumulated main strategy is rapid growth. precipitation and depth. The high diversity of Chlorophyceae and In contrast to what has been demonstrated in Bacillariophyceae at the three sites was in accord subtropical (Rodrigues et al., 2005), the with the findings of a short-term study showing development of phytoplankton in Guaiba Lake in that say these groups are more representative of summer was not followed by an increase in TSS, the diversity observed at the mouths of the rivers but by increased transparency. Similar behaviour has that form the delta of the Jacuí River, upstream of been observed in subtropical Brazilian rivers, where Guaiba Lake (Rodrigues et al., 2007). abiogenic during rainy periods in winter Long-term studies have been performed to and spring overcomes the biogenic turbidity caused establish seasonal patterns in phytoplankton by the development of phytoplankton in summer and to verify variations over the years due to (Devercelli, 2006). hydrological, nutritional and climatic changes The temporal profile of the phytoplanktonic (Anneville et al., 2004). In this study, the long-term density by class shows that the peak densities of data obtained were useful for verifying significant Chlorophyceae, Bacillariophyceae (centric diatoms: seasonal patterns in limnological conditions as Aulacoseira sp., Cyclotella sp.) and Cryptophyceae in well as phytoplankton richness and density. If the summer were most likely associated with low water temperature in the tropical zone is not a limiting levels subjected to turbulence caused by winds, as factor for the development of phytoplankton usually occurs in the lake (Nicolodi et al., 2010). (Huszar, 1996), the same cannot be said for Guaiba The expressive contribution of cyanobacteria, Lake, which is situated in the subtropical zone of especially in 2004 (MD and SJ sites) and 2005 Brazil, considering that the average density in winter (IP and SJ sites), characterised by development of Planktothrix isothrix and Planktothricoides raciborskii recorded in this long-term study was significantly were associated with anomalies in precipitation lower than the average density in summer. (La Niña) and high values of chlorophyll-a The significantly higher temperatures in (r = 0.509, p < 0.01) according to Andrade and summer coincided with significantly higher values Giroldo (2010) as well as high transparency and of Chl-a, pH, phytoplankton density and Z /Z eu temperatures (Maizonave et al., 2009). According (%), and significantly lower values of Z, TTS and to Padisák et al. (2009) P. isothrix (referred to as P. DO. The increased water temperature in summer mougeotii ) belongs to R codon. Such assemblages is related to the more intense solar radiation that are associated with stratification and occur in the occurs in the subtropical region of Brazil in this metalimnion or upper of oligo- season (Mendonça and Danni-Oliveira, 2007) mesotrophic lakes. Because lower phosphorus levels because the variation in irradiance is cyclical and occur in the summer and the main source of this is inversely proportional to latitude. This pattern element during periods of high hydraulic retention characterises temperature as a determining factor (due to low rainfall in anomalous periods) should in the seasonal abundance and the distribution and be the sediment, it is likely that these species (P. geographic variation of phytoplankton (Reynolds, isothrix and Planktothricoides raciborskii) explore 1988). Because light availability is crucial to the the bottom to assimilate and store phosphorus development of phytoplankton, some classes of (Paerl, 1988). In fact, short term study conducted algae experienced a density increase in summer in by Ribeiro et al. (2012) in a south bay of Guaiba Guaiba Lake, and only seven genera were negatively Lake, between spring 2011 and summer 2012 has correlated with water temperature, five of which suggested that changes in rainfall patterns due to were pennated diatoms (Asterionella sp. Encyonema La Niña can influence the environment, increasing sp. Eunotia sp. Gomphonema sp. Pinnularia sp.), and transparency and recruiting cyanobacterial inocula two were colonial flagellates of class Chrysophyceae deposited in layers more enriched. The study also (Cladomonas sp. Synura sp.). pointed out that there was thermal stratification Regarding the reduced Z in the lake in summer, prior to the beginning of summer Planktotricoides the long-term study by Andrade and Giroldo (2010) raciborskii bloom. revealed a significant correlation of Z with the The antagonic conditions in winter confirmed volume of rain. The authors stated that the thermal/ that low temperatures and high turbidity (high climatic seasonality of Guaiba Lake is accompanied TSS) inhibit the development of phytoplankton in by hydrological seasonality and that summer is the Guaiba Lake, which confirms that there are seasonal 454 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia limnological conditions in this lake, associated with American Public Health Association – APHA. 1998. variations in phytoplankton. Standard methods for the examination of water and The results of this study show the potential of wastewater. Washington. phytoplankton regarding differentiating between ANDRADE, RR. and GIROLDO, D. 2010. trophic state conditions and, thus, for assisting in Considerações sobre a variação temporal do fitoplâncton em um ponto amostral do lago Guaiba: the limnological characterisation of inland waters. estudo de longa duração. Ecos Técnica, no. 3, p. 5-13. The composition and density of phytoplankton ANDRADE, RR., COLARES, ERC., KRIGGER, should also be helpful in diagnosing the quality SS., MAIZONAVE, CRM. and MORANDI, IC. of waters that are subject to eutrophication and 2012. Lago Guaiba (RS): índice de qualidade da the development of cyanobacteria, as occurs in água – IQA, 2000 a 2009. Ecos Técnica, no. 4, p. 5-14. many lakes and rivers in Brazil (Abe et al., 2006; ANNEVILLE, O., SOUISSI, S., GAMMETER, S. Sant’anna et al., 2008). The subtropical inland and STRAILE, D. 2004. Seasonal and inter-annual waters in the subtropical region of Brazil suffer scales of variability in phytoplankton assemblages: abnormal rain fluctuations related to the El Niño comparison of phytoplankton dynamics in three southern oscillation (Abreu et al., 2010; Andrade peri-alpine lakes over a period of 28 years. Freshwater , vol. 49, no. 1, p. 98-115. http://dx.doi. and Giroldo, 2010). The occurrence of this type org/10.1046/j.1365-2426.2003.01167.x of pattern alters the seasonal fluctuations of Associação Brasileira de Normas Técnicas – ABNT. 1988. phytoplankton, corroborating the significance NBR 10559: Águas – Determinação de oxigênio of long-term studies to better characterise and dissolvido – Método idométrico de Winkler e suas understand phytoplankton ecology. modificações. Rio de Janeiro: ABNT. Associação Brasileira de Normas Técnicas – ABNT. 1989. Acknowledgements NBR 10664: Água – Determinação de resíduos The authors are indebted to professors Paulo C. (sólidos) – Método gravimétrico. ABNT, Rio de Abreu from the Universidade Federal do Rio Grande Janeiro. (FURG), Lezilda C. Torgan from the Fundação Associação Brasileira de Normas Técnicas – ABNT. Zoobotânica do Rio Grande do Sul (FZB/RS) and 1999a. NBR 14339: Água – Determinação de pH – Método eletrométrico. Rio de Janeiro: ABNT. referees of Acta Limnologica Brasiliensia for the useful suggestions provided throughout the original Associação Brasileira de Normas Técnicas – ABNT. 1999b. NBR 14340: Água – Determinação da manuscript. condutividade e da resistividade elétrica. Rio de Janeiro: ABNT. References BARBOSA, FAR. and PADISÁK, J. 2004. Considerações ABE, DS., TUNDISI, JG., MATSUMURA-TUNDISI, sobre desenho amostral para estudos de longa T., TUNDISI, JEM., GALLI, CS., TEIXEIRA- duração. In BICUDO, CEM. and BICUDO, DC., SILVA, V., AFONSO, GF., VON HAEHLING, orgs. Amostragem em Limnologia. São Carlos: Rima. PHA., MOSS, G. and MOSS, M. 2006. Monitoring p. 343-351. of inland quality and trophic potential BELLINGER, EG. and SIGEE, DC. 2010. Freshwater in a continental-scale in Brazil by hydroplane. In algae: identification and use as bioindicators. Willey- TUNDISI, JG., TUNDISI, TM. and GALLI, Chichester: Blackwell. CS., orgs. Eutrophication in South America: causes, BENDATI, MM., SCHWARZBACH, MSR., consequences and technologies for management MAIZONAVE, CRM., ALMEIDA, LB. and and control. São Carlos: International Institute of BRINGHENTI, ML. 2003. Avaliação da qualidade Ecology. p. 225-239. da água do Lago Guaiba: subsídios para a gestão da ABREU, PC., BERGESCH, M., PROENÇA, LA., bacia hidrográfica. Ecos Pesquisa, vol. 4, no. 7, p. 34. GARCIA, CAE. and ODEBRECHT, C. 2010. BICUDO, CEM. and BICUDO, RMT. 1970. Algas Short- and long-term chlorophyll-a variability in the de águas continentais do Brasil: chave ilustrada para shallow microtidal Patos Lagoon , Southern identificação de gêneros. São Paulo: Fundação Brazil. and Coasts, vol. 33, no. 2, p. 554- Brasileira para o Desenvolvimento do Ensino de 569. http://dx.doi.org/10.1007/s12237-009-9181-9 Ciências/EDUSP. ALVAREZ-COBELAS, M., REYNOLDS, CS., BICUDO, CEM. and MENEZES, M. 2005. Gêneros de SANCHEZ-CASTILLO, P. and KRISTIANSEN, J. algas continentais do Brasil: chave para identificação e 1998. Phytoplankton and trophic gradients. Dordrecht: descrições. São Carlos: Rima. Kluwer Academic Publishers. (Developments in BICUDO, DC., FERRAGUT, C., CROSSETTI, LO. , no. 129). and BICUDO, CEM. 2006. Efeitos do represamento 2014, vol. 26, no. 4, p. 442-456 Limnological characterisation and phytoplankton seasonal variation… 455

sobre a estrutura da comunidade fitoplanctônica do KLAVENESS, D. 1988. Ecology of the Cryptomonadida: reservatório de Rosana, baixo rio Paranapanema, a first review. In SANDGREN, CD., ed. Growth and Estado de São Paulo. In NOGUEIRA, MG., reproductive strategies of freshwater phytoplankton. HENRY, R. and JORCIN, A., orgs. Ecologia de Cambridge: Cambridge University Press. p. 105-133. reservatórios: impactos potenciais, ações de manejo e KÖPPEN, W. 1948. Climatología: um studio de los sistemas em cascata. São Carlos: Rima. p. 349-377. climas de la tierra. Mexico: Fondo de Cultura BOURRELLY, P. 1970. Les algues d’eau douce: initiation a Economica del Mexico. la systematique. Tome III: Les algues bleues et rouges, LIVI, P. 1998. Elementos do clima: o contraste dos Les Euglenins, Peridiniens et Cryptomonadines. tempos frios e quentes. In MENEGAT, R., PORTO, Paris: Boubee Ed. and Cie Paris. ML., CARRARO, CC. and FERNANDES, LAD., BOURRELLY, P. 1972. Les algues d’eau douce: initiation ed. Atlas Ambiental de Porto Alegre. Porto Alegre: Ed. a la systematique. Tome I: Les algues vertes. Paris: da UFRGS. p. 73-78. Boubee Ed. and Cie Paris. MAIZONAVE, CRM., ANDRADE, RR., THEWES, BOURRELLY, P. 1981. Les algues d’eau douce: initiation a MR. and SCHERER, KD. 2009. Florações de algas la systematique. Tome II: Les algues jaunes et brunes. e cianobactérias no lago Guaiba: série histórica do Chrysophycees, Phaeophycees, Xanthophycees et Dmae de Porto Alegre, RS. Ecos Técnica, no. 2, Diatomees. Paris: Boubee Ed. and Cie Paris. p. 5-14. Textbook of Lymnology COLE, GA. 1994. . Illinois: MCGOWAN, S., BARKER, P., HAWORTH, EY., Waveland Press. LEAVITT, PR., MABERLY, SC. and PATES, J. DEMIR, N. and ATAY, D. 2002. The treatment 2012. Humans and climates as drivers of algal efficiency of in the Ivedik drinking water community change in since 1850. treatment plant, Ankara. Turkish Journal of Biology, , vol. 57, no. 2, p. 260-277. http:// vol. 26, no. 4, p. 229-234. dx.doi.org/10.1111/j.1365-2427.2011.02689.x DEVERCELLI, M. 2006. Phytoplankton of middle MENDONÇA, F. and DANNI-OLIVEIRA, IM. 2007. Paraná river during an anomalous hydrological Climatologia: noções básicas e climas no Brasil. São period: a morphological and functional approach. Paulo: Oficinas de Textos. , vol. 563, p. 465-478. http://dx.doi. org/10.1007/s10750-006-0036-0 MÜLLER, CC., RAYA-RODRIGUEZ, MT. and CYBIS, LF. 2010. Diagnóstico da qualidade analítica na ELLIOTT, JM. 1990. The need for long-term quantificação de cianobactérias. Engenharia Sanitária investigation in ecology and the contribution of e Ambiental, vol. 15, no. 3, p. 283-290. http://dx.doi. the Freshwater Biological Association. Freshwater org/10.1590/S1413-41522010000300012 Biology, vol. 23, no. 1, p. 1-5. http://dx.doi. org/10.1111/j.1365-2427.1990.tb00250.x NICOLODI, JL., TOLDO JÚNIOR, EE. and FARINA, L. 2010. Dinâmica e ressuspensão por ondas no FARIA, CM. and LERSCH, EC. 2001. Monitoramento Lago Guaiba (RS, Brasil) e implicações nos locais das águas do Delta e foz dos rios formadores do de captação de água para abastecimento humano. Guaíba. Ecos Pesquisa, no. 5, p. 1-63. Pesquisas em Geociências, vol. 37, no. 1, p. 25-39. HAMMER, Ø., HARPER, DAT. and RYAN, PD. Baía de todas as águas 2001. Past: paleontological statistics software package NORONHA, LC. 1998. : for education and data analysis. Palaeontologia preservação e gerenciamento ambiental na bacia Electronica, vol. 4, no. 1, p. 1-9. hidrográfica do Guaiba. Porto Alegre: Secretaria Executiva do Pró-Guaíba. HUSZAR, VLM. 1996. Floristic composition and biogeographical aspects of the phytoplankton of an Organisation for Economic Cooperation and amazonian -plain lake (lake Batata, Pará, Brazil). Development – OECD. 1982. Eutrophication of Acta Limnologica Brasiliensia, vol. 8, p. 127-136. waters: monitoring, assessment and control. Paris: OECD. HUSZAR, VLM., BICUDO, DC., GIANI, A., FERRAGUT, C., MARTINELLI, LA. and PADISÁK, J., BÓRICS, G., GRIGORSZKY, I. HENRY, R. 2005. Subsídios para a compreensão and SORÓCZKI-PINTÉR, É. 2006. Use of sobre a limitação de nutrientes ao crescimento phytoplankton assemblagles for monitoring ecological do fitoplâncton e do perifíton em ecossistemas status of lakes within the water framework directive: continentais lênticos do Brasil. In ROLAND, F., the assemblage index. Hydrobiologia, vol. 553, no. 1, CESAR, D. and MARINHO, M., orgs. Lições de p. 1-14. http://dx.doi.org/10.1007/s10750-005- Limnologia. São Carlos: Rima. p. 243-260. 1393-9 ISTVÁNOVICS, V. 2009. Eutrophication of lakes and PADISÁK, J., CROSSETTI, LO. and NASELLI- reservoirs. In LIKENS, GE., ed. Plankton of Inland FLORES, L. 2009. Use and misuse in the application Waters: a derivative of Encyclopedia of Inland Waters. of the phytoplankton functional classification: a San Diego: Elsevier. p. 316-324. critical review with updates. Hydrobiologia, vol. 621, 456 Andrade, RR. and Giroldo, D. Acta Limnologica Brasiliensia

no. 1, p.1-19. http://dx.doi.org/10.1007/s10750- SOMMER, U. 1988. Growth and survival strategies 008-9645-0 of planktonic diatoms. In SANDGREN, CD., PAERL, HW. 1988. Growth and reproductive strategies ed. Growth and reproductive strategies of freshwater of freshwater blue-green algae (cyanobacteria). In phytoplankton. Cambridge: Cambridge University SANDGREN, CD., ed. Growth and reproductive Press. p. 227-260. strategies of freshwater phytoplankton. Cambridge: TELL, G., O’FARRELL, I. and LOMBARDO, RJ. Cambridge University Press. p. 261-315. 2005. Euglenoid morphospecies replacement along a REYNOLDS, CS. 1988. Functional morphology and hydraulic gradient of Lower Paraná Basin (Argentina). the adaptative strategies of freshwater phytoplankton. Freshwater Biology, vol. 50, no. 4, p. 616-626. http:// In SANDGREN, CD., ed. Growth and reproductive dx.doi.org/10.1111/j.1365-2427.2005.01347.x strategies of freshwater phytoplankton. Cambridge: TERRA, NR., FEIDEN, IR. and FACHEL, JMG. Cambridge University Press. p. 388-433. 2009. Monitoring of a swamp river contaminated by REYNOLDS, CS., HUSZAR, V., KRUK, C., multiple waste. Acta Limnologica Brasiliensia, vol. 21, NASELLI-FLORES, L. and MELO, S. 2002. no. 1, p. 79-88. Towards a functional classification of the freshwater TUNDISI, JG., TUNDISI, TM. and GALLI, CS. 2006. phytoplankton. Journal of Plankton Research, vol. 24, Eutrophication in South America: causes, consequences no. 5, p. 417-428. http://dx.doi.org/10.1093/ plankt/24.5.417 and technologies for management and control. São Carlos: International Institute of Ecology. REYNOLDS, CS. 2006. Ecology of Phytoplankton. Cambridge: Cambridge University Press. United States Environmental Protection Agency – USEPA. 1986. Method 300.7: Dissolved RIBEIRO, GF., ANDRADE, RR., MAIZONAVE, sodium, ammnonium, potassium, magnesium and CRM. and CROSSETTI, LO. 2012. Effects of calcium in wet by chemically suppressed cyanobacterial summer bloom on the phytoplankton ion chromatography. Atlanta: USEPA. structure in an urban shallow lake, Guaiba Lake, southern Brazil. Neotropical Biology and Conservation, United States Environmental Protection Agency – USEPA. vol. 7, no. 2, p. 78-87. 1993. Method 300.0: Determination of inorganic RODRIGUES, LC., TRAIN, S., PIVATO, BM., BOVO, anions by ion chromatography. Atlanta: USEPA. VM., BORGES, PAF. and JATI, S. 2005. Assembléias VALDES-WEAVER, LM., PIEHLER, MF., PINCKNEY, fitoplanctônicas de trinta reservatórios do estado JL., HOWE, KE., ROSSIGNOL, K. and PAERL, do Paraná. In RODRIGUES, L., THOMAZ, HW. 2006. Long-term temporal and spatial trends SM., AGOSTINHO, AA. and GOMES, LC., in phytoplankton biomass and class-level taxonomic eds. Biocenoses em reservatórios: padrões espaciais e composition in the hydrologically variable Neuse- temporais. São Carlos: Rima. p. 57-72. Pamlico estuarine continuum, North Carolina, RODRIGUES, SC., TORGAN, L. and U.S.A. and , vol. 51, SCHWARZBOLD, A. 2007. Composição e variação no. 3, p. 1410-1420. http://dx.doi.org/10.4319/ sazonal do fitoplâncton na foz dos rios do Delta do lo.2006.51.3.1410 Jacuí, RS, Brasil. Acta Botanica Brasílica, vol. 21, VAN DEN HOEK, C., MANN, DG. and JAHNS, no. 3, p. 707-721. http://dx.doi.org/10.1590/S0102- HM. 1995. Algae: An introduction to phycology. 33062007000300017 Cambridge: Cambridge University Press. SANT’ANNA, CL., AZEVEDO, MTP., WERNER, VIEIRA, EF. and RANGEL, SRS. 1988. Planície costeira VR., DOGO, CR., RIOS, FR. and CARVALHO, do Rio Grande do Sul: geografia física, vegetação e LR. 2008. Review of toxic species of Cyanobacteria in dinâmica sócio-demográfica. Porto Alegre: Sagra. Brazil. Algological studies, vol. 126, p. 251-265. http:// dx.doi.org/10.1127/1864-1318/2008/0126-0251 VOLLENWEIDER, RA. 1974. A manual on methods for measuring in aquatic environments. SEELIGER, U., CORDAZZO, CE. and BARBOSA, Oxford: Blackwell Science Publications. FAR. 2002. Os sites e o programa brasileiro de pesquisas ecológicas de longa duração. Belo Horizonte: FUFRS/ WETZEL, RG. 1983. Limnologia. Lisboa: Fundação UFMG. Calouste Gulbenkian.

Received: 19 September 2013 Accepted: 02 December 2014