P R I M A R Y R E S E A R C H P A P E R
Spatial and temporal variations of Dinophyceae
in subtropical reservoirs in southern Brazil
Luciana de Souza Cardoso •PaulaBraga Fagundes•Vanessa Becker
Received: 15 September 2009 / Revised: 21 June 2010 / Accepted: 18 July 2010 / Published online: 8 August 2010 Ó Springer Science+Business Media B.V. 2010
Abstract Knowledge of dinoflagellate diversity in Brazilian reservoirs is limited, especially in subtrop-ical environments. We investigated as to how nutri-ents and other environmental variables influenced the biomass of Dinophyceae species in three subtropical ecosystems. The reservoirs Samuara, Faxinal, and Sa˜o Miguel were sampled fortnightly from 2002 to 2006, and eight dinoflagellate taxa were identified. High temperature was a determining factor for the occurrence of Peridinium africanum Lemmermann. Peridinium umbonatum Stein and P. willei Huitfeld-Kass required high concentrations of nutrients. P. willei was inversely related to temperature and directly related to nutrients. P. umbonatum Stein var.
umbonatum Stein showed the largest range of toler-ance toward resources. Durinskia baltica Carty & Cox and Peridinium gatunense Nygaard could be opportunistic, since they did not show any spatial or temporal pattern.
Keywords Dinoflagellates Freshwater Seasonality Ecology Temperate climate
Introduction
The apparent benefits of the particular organization of dinoflagellate cells include (1) ability to migrate vertically; (2) low self-shading; (3) potential for low specific phosphorus requirements; (4) ability for ‘‘luxury consumption’’ of phosphorus, and (5) low rates of cell loss due to sinking and grazing (Pollingher,
1988). The abundance of dinoflagellates is related to both bottom-up (factors promoting growth) and top-down (factors causing loss) processes (Carty,2003).
Dinoflagellates can form blooms in various types of freshwater ecosystems. This can be explained by ecophysiological characteristics and by reproductive strategies, which enable them to develop and survive in conditions that are unfavorable to other algae (Pollingher,
1988). The best-known dinoflagellate that forms fresh-water blooms is Ceratium hirundinella, has been studied in many lakes and reservoirs of the United States, Canada, Europe, Africa, and Japan (Carty,2003). Handling editor: Judit Padisak
L. de Souza Cardoso (&)
Instituto de Biocieˆncias, Departamento de Botaˆnica, UFRGS, Av. Bento Gonc¸alves, 9500, Pre´dio 43433, Bairro Agronomia, Porto Alegre, RS CEP 91501-970, Brazil
e-mail: luciana.cardoso@ufrgs.br P. B. Fagundes
Curso de Graduac¸a˜o em Cieˆncias Biolo´gicas, UFRGS, Bolsista de Iniciac¸a˜o Cientı´fica FAURGS projeto 2624-7, Porto Alegre, Brazil
V. Becker
UFRN, Programa de Po´s-Graducao em Engenharia Sanitaria, Centro de Tecnologia, Av. Senador Salgado Filho, 3000, Campus Universita´rio, Natal, RN CEP 59078-970, Brazil
In subtropical regions, blooms of Peridinium gatunense are common in Lake Kinneret (Pollingher & Serruya,1976; Hickel & Pollingher,1988; Yacobi et al.,1996; Viner-Mozzini et al.,2003; Roelke et al.,
2007), the best-known subtropical environment in the world. In a subtropical Australian reservoir, Ceratium hirundinella was investigated in relation to a P-limited bloom (Baldwin et al., 2003) and vertical migration (Whittington et al.,2000). In a reservoir in Argentina, the contribution of C. hirundinella to phytoplankton biomass occurred during high outflow periods (Mac Donagh et al., 2005,2009). However, until this study, C. hirundinella had not been recorded in Brazilian waters (Cardoso & Torgan, 2007). In Japan and other Asian countries (Kawabata & Ohta,
1989; Kawabata & Hirano,1995; Wu & Chou,1998; Kim et al.,2007), members of the genus Peridinium are the most common dinoflagellates.
In spite of the importance of the Dinophyceae in many freshwater systems, few regional surveys of this group have been carried out. In Ohio, USA, water samples from ponds, lakes, and reservoirs were collected from over 100 sites, and 24 taxa were identified (Carty, 1993). A first appraisal of the taxonomy and distribution of 24 taxa of dinoflagel-lates was done in Tasmania (Australia), where 92 lakes were chosen to cover a broad limnological and ecological spectrum (Ling et al., 1989). In Hungary, 23 taxa of dinoflagellates from 86 shallow water bodies were analyzed, and temperature and organic-matter content proved to be the most important factors controlling their occurrence (Grigorszky et al.,
2003). The dinoflagellate flora of 27 temperate lakes in Trentino Province, Italy, representing all lake types, was recently studied, and 34 taxa were reported (Hansen & Flaim, 2007).
Little is known about the factors that influence the occurrence of Dinophyceae (Grigorszky et al.,2003). Therefore, investigations in different regions of the world could be very important to enhance knowledge of the ecology of Dinophyceae on a broad scale. Lack of ecological knowledge of dinoflagellates in reser-voirs in general, and in subtropical systems in particular, prompted this investigation to assess the temporal and spatial distribution of the Dinophyceae in these Brazilian subtropical reservoirs, and to suggest possible reasons for the lack of blooms of this group. This study is a pioneer investigation for this region of Brazil.
Materials and methods
Study sites
The city of Caxias do Sul (29°0500000S; 51°0303000W)
is located in northeastern Rio Grande do Sul, in southern Brazil. This subtropical region has a temperate climate, without a dry season (type Cfa; Ko¨ppen,1936), with an annual mean temperature of 16°C, and a total annual precipitation between 1,800 and 2,200 mm (Becker et al.,2008,2009a,b).
SAMAE (Servic¸o Autoˆnomo Municipal de A´ gua e Esgoto) is the water company responsible for water supply and wastewater treatment in Caxias do Sul, with four reservoirs: Faxinal, Samuara, Sa˜o Miguel, and Maestra. Only the main reservoir Faxinal has been studied limnologically, and is meso-eutrophic. It provides 64% of the water supply, with an area of 3.1 km2and zmax of 30 m. It is a warm monomictic reservoir (winter overturn), with a metalimnion between 5- and 8-m depth and a well-defined thermal gradient. The behavior of Faxinal is lakelike because of its high retention time (191 days) and low river input, with long stratification periods (Becker,2008; Becker et al., 2008, 2009a, b). The other three reservoirs are smaller: (Samuara 17 ha and zmax6 m, Sa˜o Miguel 47 ha and zmax15 m, and Maestra 54 ha and zmax 20 m). Samuara is mesotrophic, while Sa˜o Miguel and Maestra are eutrophic systems (SAMAE, personal communication).
Sampling and data analysis
For all the four reservoirs, samples were collected near the water intake, from the surface layer (between 0 and 0.5 m), weekly or biweekly (February 2002– February 2006), and were preserved with neutral Lugol’s iodine solution. The samples were deposited in a herbarium after being donated by the water company. Physical and chemical parameters were sampled at the same point (temperature, turbidity, ammonium, nitrate, nitrite, phosphate, iron, and manganese). Analytical methods are detailed in Becker et al. (2008,2009a,b).
The species of Dinophyceae were identified according to Popovsky & Pfiester (1986, 1990), Popovsky (1970,1983), and Thompson (1950).
Phytoplankton was quantified by sedimentation; at least 100 specimens of the most frequent taxa were counted (Lund et al., 1958). Only samples where
dinoflagellates were abundant ([10% of total phyto-plankton density) were considered, for a total of 26 samples (nine from Samuara, three from Faxinal, and 14 from Sa˜o Miguel). In Maestra Reservoir and during 2004 for the other reservoirs, dinoflagellates were not abundant, and therefore, these samples were excluded from this study.
From each of these 26 samples, one aliquot (1 ml) was re-examined with an inverted microscope (Olympus IX70), and the dinoflagellates were counted and identified. The biomass was estimated volumetri-cally (Edler, 1979) assuming a specific gravity of 1 mm3l-1= 1 mg l-1(Wetzel & Likens,2000).
The structure of the dinoflagellate populations was evaluated for richness and biomass. The Shannon– Wiener function was used to measure the diversity (Shannon & Weaver, 1949 apud Krebs,1978) based on the biomass data.
Pearson’s r correlation analyses (P \ 0.05) were used to determine relationships among biotic and limnological data matrices, with StatisticaÒsoftware (Statsoft Inc., 1996). Multivariate analyses were used to establish relationships among environmental fac-tors and sampling units (Principal Components Analysis—PCA) or the species contribution (Canon-ical Correspondence Analysis—CCA) to spatial and/or temporal patterns, with PC-ORDÒ software (MacCune & Mefford, 1995). Biomass data were transformed using log10(x ? 1) to normalize the variances (Ter Braak,1986).
Results
Eight Dinophyceae taxa were identified: Durinskia baltica Carty & Cox, Gymnodinium sp., Peridiniopsis penardiforme Bourrely, Peridinium africanum Lemmermann, Peridinium gatunense Nygaard, P. um-bonatum Stein, P. umum-bonatum Stein var. umum-bonatum Stein, and P. willei Huitfeld-Kass.
A synthesis of environmental data for each dinofla-gellate taxon in the reservoirs (Sa˜o Miguel, Faxinal, and Samuara) is presented in Table1. The maximum values of turbidity and all nutrients were recorded in Sa˜o Miguel Reservoir, whereas the maxima for temperature and pH were found in Samuara Reservoir.
Species richness ranged from two to five species per sample (mean 3.4), with the maximum value recorded in Sa˜o Miguel Reservoir during the winter Table
1 Range of abiotic variables for each Dinophyceae taxon (SA = Samuara, FA = Faxinal, SM = Sa ˜o Miguel) Reservoir Temperature (°C) Turbidity (NTU) pH NH 4 (l gl -1 ) NO 3 (l gl -1 ) NO 2 (l gl -1 ) PO 4 (l gl -1 ) Fe (lgl -1 ) Mn (l gl -1 ) Durinskia baltica Carty & Cox SA, SM 13.8–26.9 1.05–26.6 6.5–9.0 \ 1–250 \ 10–4,400 \ 1–68 \ 1–120 0.16–0.82 \ 0.001–0.17 Gymnodinium sp. SA 20.6 7.7 6.5 \ 1 2,300 32 20 0.30 0.04 Peridiniopsis penardiforme Bourrely SA 22.9–24.4 2.8–3.3 7.2–7.3 23–32 100–1,800 \ 1–23 10-30 0.39–0.43 0.02–0.03 Peridinium africanum Lemmermann SA, FA, SM 20.3–26.9 3.8–9.0 6.6–9.0 \ 1–60 \ 10–3,030 \ 1–19 \ 1–70 0.35–0.53 \ 0.001–0.15 Peridinium gatunense Nygaard SA, FA, SM 13.8–26.9 2.8–26.6 6.4–9.0 \ 1–250 \ 10–5,900 \ 1–760 \ 1–120 0.16–0.82 \ 0.001–0.17 Peridinium umbonatum Stein var. umbonatum Stein SA, FA, SM 13.8–24.4 1.05–26.6 6.4–8.4 \ 1–250 \ 10–5,900 \ 1–77 \ 1–120 0.10–0.82 \ 0.001–0.17 Peridinium umbonatum Stein SA, FA, SM 13.5–24 1.05–10.4 6.8–8.0 \ 1–250 \ 10–5,900 \ 1–77 10–120 0.1–0.46 \ 0.001–0.17 Peridinium willei Huitfeld-Kass FA, SM 13.8–23.3 3.17–10.4 6.8–8.0 10–250 \ 10–5,900 3–77 30–120 0.1–0.46 \ 0.001–0.17
2005, and the minimum values recorded in Sa˜o Miguel (autumn 2002) and in Samuara (summers 2002 and 2003).
The diversity (biomass data) ranged from 0.13 to 2.13 bits mg-1 (mean 1.23 bits mg-1), with the maximum value recorded in Sa˜o Miguel Reservoir (winter 2005), and the minimum value in Samuara (summer 2002) (Fig.1).
Higher richness and diversity (2.13 bits mg-1) occurred in the same sampling unit (Fig. 1), charac-terized by colder temperatures (13.8–15.1°C) and higher concentrations of nutrients (2,600–4,400 lg NO3–N l-1; 36–68 lg NO2–N l-1; 50–120 lg PO4– P l-1).
The biomass ranged from 0.033 to 1.912 mg l-1 (mean 0.553 mg l-1), with the maximum value
Fig. 1 Biomass values (% and mg l-1) and diversity (bits mg-1) of Dinophyceae taxa in three reservoirs (SA = Samuara, FA = Faxinal, SM = Sa˜o Miguel; Durin = Durinskia baltica, Gymno = Gymnodinium sp., Ppenar = Peridiniopsis penardiforme, Pafri = Peridinium africanum, Pgatu = Peridinium gatunense, Pumbo = Peridinium umbonatum var. umbonatum, Pumbo2 = Peridinium umbonatum,
recorded in Samuara Reservoir (spring 2002), and the minimum value in Faxinal Reservoir (summer 2006) (Fig.1). The biomass peak occurred when the temperature (20.6°C) and nitrogen (2,300 lg NO3– N l-1; 32 lg NO2–N l
-1
) were higher than the mean, pH slightly acid (6.51), and phosphate (20 lg PO4– P l-1) lower than the mean.
Of all the reservoirs, Samuara showed maximum biomass while Sa˜o Miguel showed maximum rich-ness and diversity. The correlation analysis showed that the abiotic variables were inversely correlated with the Dinophyceae data, except for Peridinium umbonatum var. umbonatum (Table 2).
The PCA ordination explained 97.4% of data variability on axis 1 and 2 (Fig.2), whereas in the CCA, only axis 1 contributed significantly (P \ 0.05) to the variance of the data (27.1%) (Fig.3). The seasonality and trophic gradients were the main factors responsible for the ordination of samples and/or species in these analyses. No spatial gradient pattern was observed, only a seasonal gradient (Figs.2,3).
In CCA (Fig.3), the summer units of three reservoirs and the spring units of Samuara Reservoir were well separated from the rest, being strongly correlated with temperature (r = 0.72). The iron concentration (r = 0.68) was higher in Samuara Reservoir (0.30–0.82 mg l-1) than in the others, contributing to its ordination.
The correlations between species and environmen-tal variables were significant (P = 0.004) on CCA axis 1. Peridinium africanum (r = 0.84) was more
abundant during summer in all the reservoirs. Almost all the sampling units from Sa˜o Miguel Reservoir, especially in winter, and from Faxinal Reservoir were correlated with nutrients (r = -0.54 to r = -0.74) and manganese (r = -0.47 and r = -0.58), where the biomasses of P. umbonatum (r = -0.65) and P. willei (r = -0.78) were higher. P. umbonatum var. umbonatum (r = 0.76) was plotted near the center of the graph (Fig.3), since its biomass contribution was practically constant among all the sampling units. Table 2 Correlation matrix (r-Pearson, P \ 0.05) between abiotic variables and Dinophyceae data (for definitions of abbreviations see caption of Fig.1)
Temperature Turbidity NH4 NO3 NO2 Fe Richness Biomass Diversity
Richness -0.53 -0.41 1.00 Biomass -0.38 -0.39 -0.38 1.00 Diversity -0.58 -0.42 -0.45 0.88 1.00 Gymno Pafri -0.40 -0.54 Ppenar Pgatu 0.70 Pumbo 0.45 0.54 Pumbo2 0.38 0.41 Durin 0.37 Pwill -0.63 -0.45 0.68 0.62 Temp NH4 NO3 NO2 PO4 Mn 0 50 80 40 52 54 56 Axis 1 - 93.1% Axis 2 - 4.3% Reservoir Samuara Faxinal São Miguel
Fig. 2 PCA ordination diagram for environmental variables and sampling units from the reservoirs (temp = water temperature)
Discussion
The richness in these reservoirs was low in compar-ison to other surveys, where 23–34 taxa of dinoflag-ellates were recorded (Ling et al.,1989; Carty,1993; Grigorszky et al., 2003; Hansen & Flaim, 2007). However, in these surveys, the number of water bodies sampled was larger than in this study (only three reservoirs). In six tropical Brazilian lakes (Rio Doce Valley), nine species of the Dinophyta were registered, where their contribution to total biomass were 6.3% in Lake Dom Helve´cio (Borics et al.,
2005). In shallow lakes (eight) and wetlands (four) in the subtropical part of Brazil, 11 taxa were identified (Cardoso & Torgan, 2007). Researches focused on strategies involved in bloom formation such as life cycle characteristics and production of secondary metabolites as conducted by Flaim et al. (2010), where experiments were combined with a monitoring program. This could point to specific environmental (physical and chemical, hydrological, and land use) and/or biotic factors driving the distribution of dinoflagellates. Besides that, in our study, these factors are not clear due to the water company monitoring being carried only in the water intake, on the surface, and few physical and chemical variables
being analyzed in accordance with the law of the Ministry of Health (Brasil, 2004) for cyanobacterial control in Brazilian reservoirs. We are aware of the limitations in our findings; however, the preliminary approaches to dinoflagellates in subtropical reservoirs presented here are important to drive future researches in Brazil in the fields of ecology as well as taxonomy.
For the best-known lake of a subtropical region, Lake Kinneret, it was necessary to analyze a 34-year data set to show that the system was characterized by a hysteresis (Roelke et al., 2007). The analyses of Lake Kinneret data from 1969 through 1993 (a period characterized by large spring blooms dominated by Peridinium gatunense) using conventional statistics (correlation and principal components analyses, and non-metric multidimensional scaling) failed to reveal which physicochemical and biological factors influ-enced the Peridinium gatunense blooms. When Roelke and coworkers focused only on the 1994–2001 period; however, correlative relationships were apparent, and they involved physicochemical parameters and zoo-plankton taxa where linkages between biota and the physicochemical environment, and food-web interac-tions, could be envisaged. In other words, it was necessary for Roelke et al. (2007) to experiment within the framework of the alternative-states model to eluci-date potential triggering mechanisms, which were a function of wintertime physical and chemical conditions and the structure of the zooplankton assemblage, and zooplankton biomass and body size.
In addition, Lake Tovel (a small and oligotrophic mountain lake) is famous for its blood-red summer blooms (up to 1964) in the SW Red Bay (Flaim et al.,
2003) caused by Glenodinium sanguineum Marche-soni. During 2003–2005, a large multidisciplinary project was initiated, which focused on the causes of the disappearance of the reddening of Lake Tovel (Hansen & Flaim, 2007), almost 40 years after the ending of blooms. Detailed taxonomic studies of the dinoflagellates had never been made in this region before, and it turned out to represent at least three different species which in the past promoted blooms mistakenly attributed to G. sanguineum (Moestrup et al.,
2006; Hansen & Flaim,2007; Flaim et al.,2010). The dinoflagellates provide excellent examples of species adapted to thrive and persist under low concentrations of nutrients, and may also be well adapted to low turbulence. Their life strategies may
Temp NH4 NO3 NO2 PO4 Fe Mn 0 0 80 40 40 80 Axis 1 - 27.1% r 0.86 p 0.004 Axis 2 Reservoir Samuara Faxinal São Miguel
Fig. 3 CCA ordination diagrams for biomass data of Dino-phyceae taxa in reservoirs according to environmental vari-ables (for definitions of abbreviations see caption of Fig.1)
correlate with a certain degree of heterotrophy and the development of defense mechanisms against grazers or predators (Margalef, 1978). Mixotrophy is a common strategy in oligotrophic environments, and in Lake Tovel, some dinoflagellates also have phagotrophic mixotrophic feeding mechanisms rep-resenting an ecological advantage by integrating photo-autotrophic growth (Flaim et al., 2010). Fur-thermore, the lake has low dissolved organic carbon (DOC) concentrations (\1 mg l-1), and any addi-tional organic input could be an important factor for growth. In the presence of organic nitrogen sources, blooms occurring in rainy springs supported the hypothesis that organic nitrogen triggered bloom formation (Flaim et al., 2010). Indeed, the diversity and biomass found in this study were inversely correlated to turbidity and nitrogen, respectively, but P. umbonatum var. umbonatum was directly corre-lated to turbidity. This behavior was quite unex-pected, except that the turbidity was very low (1.05–26.6 NTU) in this study. Mixotrophy could be a major strategy used here by dinoflagellates to enhance biomass during high temperatures, when input of nutrients was low.
The abundance of dinoflagellates has been inves-tigated around the world from many ecological and physiological aspects, but the effect of temperature is the most diverse depending on the species. In our study, low temperature was related to richness, diversity, and Peridinium willei. However, in tem-perate lakes of Trentino, P. willei seemed to be restricted to spring/summer, with wide distribution among lake types (Hansen & Flaim, 2007). This shows that the same species can have distinct responses to the same variable if climate conditions are different (temperate and subtropical).
The development of the vegetative cells and their blooms occurred in similar environmental conditions in Lake Kinneret and in temperate zones, where the unfavorable conditions for the dinoflagellates occurred in summer in the subtropical lake, and in winter in temperate water bodies (Pollingher & Hickel, 1991). High temperature was the most important variable affecting blooms of dinoflagellates, in lakes (Tempon-eras et al., 2000; Gligora et al., 2003) as well as in reservoirs (Kawabata & Kagawa, 1988). However, some species prefer low temperature and this cold-water preference can favor bloom formation in cold waters by reduced competition and grazing due to low
temperatures (Flaim et al., 2010). Our correlation results (Table2) showed that cold water can favor increase in diversity and richness of dinoflagellates as well as biomass of Peridinium willei.
Indeed, temperature did not as a rule drive the abundance of all the dinoflagellate species in our study. Neither was it the only factor governing the spatial and temporal distribution of dinoflagellates (Flaim et al.,2010). Although only P. willei showed a correlation with low temperatures, the CCA ordina-tion showed that high temperature was an important factor for the distribution of P. africanum and Peridiniopsis penardiforme in these subtropical res-ervoirs. Indeed, to both species, the temperature range of their distribution was very narrow (Table1). In temperate lakes of Trentino, P. penardiforme [transferred to Glochidinium penardiforme (Lemmer-mann) Boltovskoy] appeared to be a warm-water species too but was never very abundant (Hansen & Flaim,2007). High temperatures and P-depletion led to an increase in cell volume; Flaim et al. (2010) suggested that this might be related to the inhibition of cell division leading to larger cells. It was mainly true of P. africanum where the increase of biomass happened during summer, in Samuara reservoir, when phosphorous and nitrogen levels were below the detection limits (Fig.1; Table1).
In subtropical shallow lakes and wetlands in Rio Grande do Sul (Cardoso & Torgan,2005,2007), the populations of Dinophyceae were analyzed only in relation to habitat and hydroperiod, where Peridinium gatunense was an indicator species associated with high water level (high precipitation and depth, low temperature, and Secchi transparency) and P. um-bonatum was an indicator species associated with non-connected lakes (specificity of habitat) which means very small and shallow lakes. In the reservoirs in Caxias do Sul, the biomass of Peridinium gatun-ense and P. umbonatum var. umbonatum was max-imal during spring where the nutrients were not limiting variables (2,300 lg NO3–N l-1 and 80 lg PO4–P l-1, respectively).
According to Reynolds (1999), the hydrological mechanisms in shallow lakes are very different from reservoirs. However, the selective mechanisms by phytoplankton did not differ between reservoirs and natural lakes in response to fluctuations in available resources. In shallow lakes (Cardoso & Torgan,
periods with high precipitation/water level; while high density was related to high temperature. In subtropical Rio Grande do Sul, high and constant precipitation periods (high water level) are common in winter, and also occur in autumn during some years (Cardoso & Torgan, 2007). In other words, temperature linked to hydrological aspects could explain much more about the spatial and temporal distribution of dinoflagellates in these reservoirs. Unfortunately, hydrological data were not collected by the water company (SAMAE) for all the reser-voirs, only for Faxinal Reservoir as mentioned above. In terms of the limitation of nutrients for phyto-plankton (Reynolds, 2006), the algal requirements based on half-saturations for growth can be consid-ered as limited by SRP at 3.1 lg l-1 and by DIN concentrations lower than 98 lg l-1. The reservoirs in Caxias do Sul were not limited by DIN, but sometimes they were limited by P, except in Samuara Reservoir, where P. africanum found conditions during summer (2002 and 2003) favorable enough to become the dominant species, where the biomass peak occurred when the temperature was above the mean (21.0°C) and with DIN concentrations below the mean (\1 lg NH4–N l-1; \10 lg NO3–N l-1; 16 lg NO2–N l-1). The opposite pattern for uptake limitation was established for dinoflagellates in relation to DIN (close to 140 lg NO3–N l
-1
) by Huszar & Caraco (1998). In Lake Kinneret (Roelke et al.,2007), high NO3–N loading enhanced the development of Peridinium gatunense blooms. However, in our study, P. africanum behaved differently from other dinoflag-ellates with regard to nutrient limitation.
In our reservoirs, the temporal abundance of dinoflagellates was short-lived and limited to less than one week, indicating opportunistic behavior. Monitoring in the Caxias do Sul reservoirs (Frizzo et al.,2004) showed that cyanobacteria are a resident group in these ecosystems, occasionally forming blooms. Indeed, in spring 2002, in Samuara Reser-voir, the density recorded for Anabaena planctonica was as high as 5,000 cells ml-1; while in Sa˜o Miguel Reservoir, the density of Microcystis aeruginosa was 70,000 cells ml-1 in autumn 2002, and 10,000 cells ml-1 in summer 2003 (Frizzo et al., 2004). The data suggest that the phytoplankton species co-occurring on these occasions were competing for some resource (light or nutrients), where these cyanobacteria species were successful. This is related
to their rapid growth rates coupled with the efficiency of this group, especially in high phosphate concen-trations (Huszar & Caraco, 1998). This probably contributed to the relatively low abundance of dinoflagellates in successive temporal samples during these 4 years.
Based on a culture experiment, Sukenik et al. (2002) showed that allelopathic substances excreted by Microcystis caused inhibition of Peridinium growth. This result was fundamental to prove the authors’ hypothesis that allelopathy could control bloom succession of Peridinium gatunense in Lake Kinneret. However, our results pointed to nutrient limitation as the most probable cause of the phyto-plankton competition. During the study at Faxinal Reservoir in 2004 (Becker et al., 2009b), the water-column stability, higher phosphate concentrations, and lower DIN favored Anabaena crassa during summer. In spring, when the reservoir was P-limited and also had lower DIN concentrations, and a mixing epilimnion, diatoms (Asterionella formosa) domi-nated the system. The dinoflagellates, represented by Peridinium species, showed increased biomass during the end of summer and spring, when the water stability was increased, with lower DIN concentra-tions (Becker et al.,2009b). However, this increase of Peridinium species in Faxinal was not sufficient for it to become abundant in the phytoplankton commu-nity, probably due to low DIN concentration.
Our study contributed to increasing knowledge of the ecological requirements of dinoflagellates, par-ticularly with regard to temperature and nutrients. In general, studies of phytoplankton communities, species of Peridinium are combined and assumed to have the same resource requirements. We, however, distinguished each species, thus providing species-specific information. In short, in these subtropical reservoirs, P. willei and P. umbonatum require high concentrations of nutrients to be more competitive (with a preference for more eutrophic conditions). P. umbonatum var. umbonatum was found over a large range of nutrient and metal concentrations, as well as temperature and pH. P. africanum occurred at the measured extremes of the physical and chemical variables, except temperature, where higher temper-atures were a determining factor for its occurrence (20.3–26.9°C). Durinskia baltica and Peridinium gatunense showed opportunistic behavior, not evi-dencing any spatial or temporal patterns in relation to
environmental variables. However, Peridiniopsis pe-nardiforme proved to have a narrower tolerance limit, since it was only recorded during spring 2005 in Samuara Reservoir.
Soft waters (Pollingher, 1988; Ling et al., 1989) and allelopathic inhibition by cyanobacteria (Sukenik et al.,2002) could be possible causes for the lack of blooms in these Brazilian subtropical reservoirs. How-ever, according to findings in Faxinal Reservoir (Becker et al.,2008,2009a,b), which could be extrapolated to Sa˜o Miguel and Samuara reservoirs, the most probable cause of the lack of dinoflagellates blooms in these reservoirs was related to limitation of nutrients and the consequent competition by phytoplankton.
Seasonality gradients were basically driven by nutrients and temperature, and reflected the contri-bution of dinoflagellates species in these reservoirs. This investigation was important to improve knowl-edge of Dinophyceae ecology in subtropical Brazilian reservoirs. Unfortunately, the lack of hydrological data and of more physical and chemical variables analyzed in this study does not permit further interpretation of the ecology requirements of dino-flagellates. However, studies combining laboratory and field data must be improved to understand the autoecology of dinoflagellates as described by Flaim et al. (2010), so that a theoretical model of the species’ life cycle in a determined environment can be proposed and compared to a different environment order to define the tolerance limits of each species.
Acknowledgments We are grateful to SAMAE of Caxias do Sul for providing physical and chemical water data, and, especially, to their chemical engineer Fernanda B. Spiandorello; to Graziela P. Monc¸ani, Rovana Sussella, and Renivo Girardi, technicians of SAMAE, for their technical support and the donation of samples deposited in the ICN-UFRGS Herbarium; and to Dr. Sandra Maria Alves da Silva, curator of the HAS, for permission to access the samples deposited in the herbarium. We thank Luciane Crossetti for her suggestions that improved the quality of this manuscript, and finally Dr. Janet W. Reid (JWR Associates) for the revision of the English text.
References
Baldwin, D. S., J. Whittington & R. Oliver, 2003. Temporal variability of dissolved P speciation in a eutrophic reser-voir – implications for predicating algal growth. Water Research 37: 4595–4598.
Becker, V., 2008. A importaˆncia do regime de mistura sobre a dinaˆmica fitoplanctoˆnica em reservato´rios monomı´ticos:
uma abordagem em diferentes escalas temporais. Tese (Doctoral in Biological Sciences – Botany), Universidade Federal do Rio de Janeiro. Museu Nacional, Rio de Janeiro.
Becker, V., V. L. M. Huszar, L. Naselli-Flores & J. Padisa´k, 2008. Phytoplankton equilibrium phases during thermal stratification in a deep subtropical reservoir. Freshwater Biology 53: 952–963.
Becker, V., L. de S. Cardoso & V. L. M. Huszar, 2009a. Diel variation of phytoplankton functional groups in a sub-tropical reservoir in southern Brazil, during an autumnal stratification period. Aquatic Ecology 43: 285–293. Becker, V., V. L. M. Huszar & L. O. Crossetti, 2009b.
Responses of phytoplankton functional groups to the mixing regime in a deep subtropical reservoir. Hydrobi-ologia 628: 137–151.
Borics, G., I. Grigroszky, J. Padisa´k, F. A. R. Barbosa & Z. Z. Doma, 2005. Dinoflagellates from tropical Brazilian lakes with description of Peridinium brasiliense sp. nova. Algological Studies 118: 47–61.
Brasil, 2004. Portaria nr. 518/2004. Ministe´rio da Sau´de. Cardoso, L. de S. & L. C. Torgan, 2005. Distribuic¸a˜o e
den-sidade de Peridinium gatunense e P. umbonatum (Dino-phyceae) em ecossistemas da zona costeira no sul do Brasil. In Anais da X Reunia˜o Brasileira de Ficologia, Salvador 2004. Museu Nacional, Rio de Janeiro: 517–526. Cardoso, L. de S. & L. C. Torgan, 2007. Dinoflagelados em diversos habitats e hidroperı´odos na zona costeira do sul do Brasil. Acta Botaˆnica Brası´lica 21: 411–419. Carty, S., 1993. Contribution to the dinoflagellate flora of Ohio.
Ohio Journal of Science 5: 140–146.
Carty, S., 2003. Dinoflagellates. In Wehr, J. D. & R. G. Sheath (eds), Freshwater Algae of North America. Elsevier Science, USA: 685–714.
Edler, L., 1979. Recommendations on methods for marine biological studies in the Baltic Sea: phytoplankton and chlorophyll. The Baltic Marine Biologists, UNESCO, Paris. Flaim, G., E. Rott, F. Corradini, G. Toller & B. Borghi, 2003. Long-term trends in species composition and diurnal migration of dinoflagellates in Lake Trovel (Trentino, Italy). Hydrobiologia 502: 357–366.
Flaim, G., E. Rott, R. Frassanito, G. Guella & U. Obertegger, 2010. Eco-fingerprinting of the dinoflagellate Borghiella dodgei: experimental evidence of a specific environmental niche. Hydrobiologia 639: 85–98.
Frizzo, E. E., V. Becker, F. B. Spiandorello, R. Girardi & J. S. Yunes, 2004. Implantac¸a˜o do monitoramento fit-oplanctoˆnico, com eˆnfase em cianobacte´rias e cianotox-inas nos mananciais de abastecimento do municı´pio de Caxias do Sul-RS. In Anais VIII Exposic¸a˜o de Experi-eˆncias Municipais em Saneamento-34aAssemble´ia Nac-ional da Associac¸a˜o NacNac-ional dos Servidores Municipais de Saneamento. ASSEMAE, Caxias do Sul: 421–424. Gligora, M., A. Plenkovic-Moraj & I. Ternjej, 2003. Seasonal
distribution and morphological changes of Ceratium hirundinella in two Mediterranean shallow lakes. Hydro-biologia 506–509: 213–220.
Grigorszky, I., G. Borics, J. Padisa´k, B. To´tme´re´sz, G. Vasas, S. Nagy & G. Borbe´ly, 2003. Factors controlling the occurrence of Dinophyta species in Hungary. Hydrobio-logia 506–509: 203–207.
Hansen, G. & G. Flaim, 2007. Dinoflagellates of the Trentino Province, Italy. Journal of Limnology 66: 107–141. Hickel, B. & U. Pollingher, 1988. Identification of the
bloom-forming Peridinium from Lake Kinneret (Israel) as Peridinium gatunense (Dinophyceae). British Phycologi-cal Journal 23: 115–119.
Huszar, V. L. de & N. F. Caraco, 1998. The relationship between phytoplankton composition and physical-chemi-cal variables: a comparison of taxonomic and morpho-logical-functional descriptors in six temperate lakes. Freshwater Biology 40: 679–696.
Kawabata, Z. & Y. Hirano, 1995. Growth pattern and cellular nitrogen and phosphorus contents of the dinoflagellate Peridinium penardii (Lemm) Lemm causing a freshwater red tide in a reservoir. Hydrobiologia 312: 115–120. Kawabata, Z. & H. Kagawa, 1988. Distribution pattern of the
dinoflagellate Ceratium hirundinella (Muller, O. F.) Bergh in a reservoir. Hydrobiologia 169: 319–325. Kawabata, Z. & M. Ohta, 1989. Cyst distribution and excystment
conditions for the dinoflagellate Peridinium penardii (Lemm.) Lemm. in a reservoir. Freshwater Biology 21: 437–444. Kim, B. H., M. H. Park & S. J. Hwang, 2007. Excystment
patterns of the freshwater dinoflagellate Peridinium bipes (Dinophyceae) in Juam Reservoir, Korea. Aquatic Microbial Ecology 47: 213–221.
Ko¨ppen, W., 1936. Das geographische System der Klimate – Handbuch der Klimatologie, v. 1, Part C, Gebr. Borntra¨-ger Verlag, Berlin.
Krebs, C. J., 1978. Ecology: The Experimental Analysis of Distribution and Abundance, 2nd edn. Harper & Row, New York.
Ling, H. U., R. L. Croome & P. A. Tyler, 1989. Freshwater dinoflagellates of Tasmania, a survey of taxonomy and distribution. British Phycological Journal 24: 111–129. Lund, J. W. G., C. Kipling & E. D. Lecren, 1958. The inverted
microscope method of estimating algal number and the statistical basis of estimating by counting. Hydrobiologia 11: 143–170.
MacCune, B. & M. J. Mefford, 1995. PC-ORD. Multivariate Analysis of Ecological Data, Version 2.0. MJM Software Design, Gleneden Beach, OR.
Mac Donagh, M. E., M. A. Casco & M. C. Claps, 2005. Col-onization of a neotropical reservoir (Cordoba, Argentina) by Ceratium hirundinella (O. F. Muller) Bergh. Annales de Limnologie. Internacional Journal of Limnology 41: 291–299. Mac Donagh, M. E., M. A. Casco & M. C. Claps, 2009. Plankton relationships under small water level fluctuations in a subtropical reservoir. Aquatic Ecology 43: 371–381. Margalef, R., 1978. Life forms of phytoplankton as survival alternatives in an unstable environment. Acta Oceano-logica 1: 493–509.
Moestrup, Ø., G. Hansen, N. Daugbjerg, G. Flaim & M. D’Andrea, 2006. Studies on woloszynskioid flagellates II: on Tovellia sanguinea sp. nov., the dino-flagellates responsible for the reddening of Lake Tovel, N. Italy. European Journal of Phycology 41: 47–65. Pollingher, U., 1988. Freshwater armored dinoflagellates:
growth, reproduction strategies, and population dynamics. In Sandgren, C. D. (ed.), Growth and Reproductive Strategies of Freshwater Phytoplankton. Cambridge University, Cambridge: 134–174.
Pollingher, U. & B. Hickel, 1991. Dinoflagellate associations in a subtropical lake (Lake Kinneret, Israel). Archive fur Hydrobiologie 120: 267–285.
Pollingher, U. & C. Serruya, 1976. Phased division of Peridinium cinctum f westii (Dinophyceae) and development of Lake Kinneret (Israel) bloom. Journal of Phycology 12: 162–170. Popovsky, J., 1970. Some thecate dinoflagellates from Cuba.
Archiv fur Protistenkunde 112: 252–258.
Popovsky, J., 1983. Problems in the determination of fresh-water dinoflagellates (Dinophyceae). Schweizerische Zeitschrift Fur Hydrologie 45: 365–372.
Popovsky, J. & L. A. Pfiester, 1986. A taxonomical note to the section umbonatum of the genus Peridinium Ehrenberg, 1932 (Dinophyceae). Archiv fur Protistenkunde 132: 73–77. Popovsky, J. & L. A. Pfiester, 1990. Dinophyceae (Dinoflag-ellida). In Ettl, H., J. Gerloff, H. Heynig & D. Mollen-hauer (eds), Su¨bwasserflora von Mitteleuropa, 6. Gustav Fischer Verlag, Sttugart.
Reynolds, C. S., 1999. Phytoplankton assemblages in Reser-voirs. In Tundisi, J. G. & M. Strasˇkraba (eds), Theoretical Reservoir Ecology and Its Applications. International Institute of Ecology, Brazilian Academy of Sciences and Backhuys Publishers, Sa˜o Carlos: 439–456.
Reynolds, C. S., 2006. The Ecology of Phytoplankton (Ecol-ogy, Biodiversity and Conservation). Cambridge Univer-sity Press, Cambridge.
Roelke, D. L., T. Zohary, K. D. Hambright & J. V. Montoya, 2007. Alternative states in the phytoplankton of Lake Kinneret, Israel (Sea of Galilee). Freshwater Biology 52: 399–411. Sukenik, A., R. Eshkol, A. Livne, O. Hadas, M. Rom, D.
Tchernov, A. Vardi & A. Kaplan, 2002. Inhibition of growth and photosynthesis of the dinoflagellate Peridinium gatun-ense by Microcystis sp. (cyanobacteria): a novel allelopathic mechanism. Limnology and Oceanography 47: 1656–1663. Temponeras, M., J. Kristiansen & M. A. Moustaka-Gouni, 2000. New Ceratium species (Dinophyceae) from Lake Doirani, Macedonia, Greece. Hydrobiologia 424: 101–108. Ter Braak, C. J. F., 1986. Canonical correspondence analysis: a
new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179.
Thompson, R. H., 1950. New genus and new records of fresh-water Pyrrophyta in the Desmokontae and Dinophyceae. Lloydia 13: 277–299.
Viner-Mozzini, Y., T. Zohary & A. Gasith, 2003. Dinoflagel-late bloom development and collapse in Lake Kinneret: a sediment trap study. Journal of Plankton Research 25: 591–602.
Wetzel, R. G. & G. E. Likens, 2000. Limnological Analyses, 3rd ed. Springer-Verlag, New York.
Whittington, J., B. Sherman & D. Green, 2000. Growth of Ceratium hirundinella in a subtropical Australian reser-voir: the role of vertical migration. Journal of Plankton Research 22: 1025–1045.
Wu, J. T. & J. W. Chou, 1998. Dinoflagellate associations in Feitsui Reservoir, Taiwan. Botanical Bulletin of Acade-mia Sinica 39: 137–145.
Yacobi, Y. Z., U. Pollingher & Y. Gonen, 1996. HPLC analysis of phytoplankton pigments from Lake Kinneret with special reference to the bloom-forming dinoflagellate Peridinium gatunense (Dinophyceae) and chlorophyll degradation products. Journal of Plankton Research 18: 1781–1796.
