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Dynamics of phytoplankton associations in three reservoirs in northeastern Brazil
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assessed using Reynolds’ theory
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Ênio Wocyli Dantas1,2, Maria do Carmo Bittencourt-Oliveira3, Ariadne do Nascimento
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Moura2
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Aplicadas – CCBSA, R. Monsenhor Walfredo Leal, nº 487, Tambiá, CEP 58020-540, João Pessoa,
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Paraíba, Brazil; Phone: +55 83 3238 9236, E-mail: eniowocyli@yahoo.com.br
Universidade Estadual da Paraíba - UEPB - Campus V, Centro de Ciências Biológicas e Sociais
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Manoel de Medeiros, S/N, Dois Irmãos, CEP 52171-030, Recife, Pernambuco, Brazil; Phone: +55 81
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3320 6350.
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de São Paulo, Av. Pádua Dias 11, Piracicaba, SP, CEP 13418-900, Brazil; Phone: +5519-3429-4128.
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Fax: +5519-3434-8295.
Universidade Federal Rural de Pernambuco, Departamento de Biologia, Área de Botânica, R. D.
Departamento de Ciências Biológicas, Escola Superior de Agricultura Luiz de Queiroz, Universidade
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Running title: Phytoplankton associations in Brazilian reservoirs
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Abstract: The aim of the present study was to evaluate the influence of seasonality on the
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behavior of phytoplankton associations in eutrophic reservoirs with different depths in
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northeastern Brazil. Five collections were carried out at each of the reservoirs at two depths
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(0.1 m and near the sediment) at three-month intervals in each season (dry and rainy). The
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phytoplankton samples were preserved in Lugol’s solution and quantified under an inverted
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microscope for the determination of density values, which were subsequently converted to
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biomass values based on cellular biovolume and classified in phytoplankton associations. The
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following abiotic variables were analyzed: water temperature, dissolved oxygen, pH,
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turbidity, water transparency, total phosphorus, total dissolved phosphorus, orthophosphate
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and total nitrogen. The data were investigated using canonical correspondence analysis. The
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influence of seasonality on the dynamics of the phytoplankton community was lesser in the
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deeper reservoirs. Depth affected the behavior of the algal associations. Variation in light
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availability was a determinant of changes in the phytoplankton structure. Urosolenia and
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Anabaena associations were more abundant in shallow ecosystems with a larger eutrophic
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zone, whereas the Microcystis association was more related to deep ecosystems with adequate
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availability of nutrients. The distribution of Cyclotella, Geitlerinema, Planktothrix,
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Pseudanabaena and Cylindrospermopsis associations was different from that seen in
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subtropical regions and the substitution of these associations was related to a reduction in the
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eutrophic zone rather than the mixture zone.
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Keywords: eutrophic reservoir; functional groups; planktonic algae; seasonal dynamics;
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water supply
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1. Introduction
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The composition and biomass of phytoplankton species in reservoirs depends on a complex
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combination of factors, such as temperature, light, availability of nutrients and zooplankton
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community. Reynolds et al. (2002) used these factors for the establishment of a functional
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classification of algae capable of reflecting the ecology of the species.
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Unlike what is found in temperate regions, tropical ecosystems exhibit a succession of
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associations of cyanobacteria that often dominate an entire seasonal cycle (Marinho and
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Huszar, 2002). According to Nabout et al. (2006), diatoms associations succeed those of
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cyanobacteria during the time interval in which winds and rains cause instability in the
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system. Soon afterward, filamentous cyanobacteria begin to co-dominate and, when the water
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column is stabilized, coccoid cyanobacteria dominate. The different associations of diatoms
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are related to the trophic state of the system, with algae related to oligotrophic (A),
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mesotrophic (B and N) and eutrophic (C, D and P) ecosystems (Reynolds et al., 2002).
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The majority of invasive algae that develop under conditions of abundant underwater
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luminosity and nutrient availability are generally single-celled chlorophytes (X1) (Melo and
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Huszar, 2000). In northeastern Brazil, there are reports of the predominance of chlorophytes
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in the phytoplankton community under oligo-mesotrophic conditions (Dellamano-Oliveira et
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al., 2003; Chellappa et al., 2008), especially functional groups X1 and J.
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In subtropical regions, the considerable variation in temperature and other
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environmental variables produces predictable changes in the composition of phytoplankton in
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aquatic systems (Grover and Chrzanowski, 2006). In contrast, tropical regions exhibit little
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annual temperature variation and successional changes in the algal community are the result
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of seasonal rainfall patterns, with different algal structuring in the rainy and dry seasons
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(Ibañez, 1998). In northeastern Brazil, the structure of the phytoplankton is formed by a single
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group of taxa, for which only the biomass values oscillate throughout the year (Huszar et al.,
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2000; Moura et al., 2007a, b; Dantas et al., 2008).
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Environmental conditions in tropical reservoirs are influenced by precipitation events,
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which alter the volume and level of the ecosystem and are especially important to the
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dynamics of the phytoplankton community. Greater algal biomasses occur when reservoir
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levels are low and these algae are favored by thermal circulation and the re-suspension of
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nutrients (Arfi, 2005).
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Rainfall is an important factor to raising the level of aquatic systems and reducing
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light availability and algal biomass. This consequently leads to changes in the composition of
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different associations of algae in tropical systems (Chellappa et al., 2008; Dantas et al., 2008).
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The aim of the present study was to investigate the seasonal and spatial variation in
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phytoplankton associations in three reservoirs of different depths in northeastern Brazil,
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relating these associations to abiotic variables. This study tests the following hypotheses: a) a
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reservoir has vertical thermal patterns in function of depth that alter with the seasons; these
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patterns are less variable in both shallow and deep reservoirs, whereas well-defined seasonal
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patterns are expected in reservoirs of intermediate depth, with greater fluctuations in algal
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biomass values and the structure of the phytoplankton associations; b) the availability of light
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and nutrients varies in relation to depth and seasonality and is reflected in the succession of
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the phytoplankton community; a greater limitation of light is expected in shallow reservoirs
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and greater limitation of nutrients is expected in deep reservoirs, with different algal
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associations in each ecosystem.
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Materials and Methods
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Study area
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Three reservoirs were studied – Duas Unas and Tapacurá, located in the coastal zone, and
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Jucazinho, located in the semi-arid hinterland of the state of Pernambuco, Brazil (Figure 1).
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Table 1 displays the morphometric data and information on the use of the reservoirs. The
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climate of the region has Köppen classification A (warm, wet pseudotropical) and is strongly
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influenced by precipitation, with well-defined rainy (March to August) and dry (September to
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February) seasons (Almeida et al., 2009). During the study period (March 2007 to May 2008),
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atypical rainfall occurred in September 2007 and March 2008 and the rainy season had
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generally southerly winds of lesser intensity (Figure 2).
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Abiotic and biotic analyses
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Sampling was carried out at three-month intervals over the course of one year (March
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2007 to May 2008) at each reservoir. At the Duas Unas reservoir, the sampling site was
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located at 8°04’58” S and 35°02’56” W and depth ranged from 5.2 to 9.1 m. At the Tapacurá
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reservoir, the sampling site was located at 8°02’40” S and 35°11’22” W and the depth ranged
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from 11.0 to 15.9 m. At the Jucazinho reservoir, the sampling was located at 7°58’53” S and
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35°48’32” W and the depth ranged from 11.0 to 22.0 m.
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Water samples for nutrient analysis and the investigation of the phytoplankton
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community were collected with a 5-L vertical Van Dorn bottle (7.0-cm opening) from the
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subsurface and approximately 1 m above the bottom (no light). Abiotic variables were
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determined in situ and included water temperature and dissolved oxygen (Schott Glaswerke
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Mainz, handylab OX1), turbidity (Hanna Instruments, HI 93703), pH (Digimed, DMPH-2),
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water transparency (Secchi disc, 25 cm in diameter) and maximal depth (echo bathymeter).
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The euphotic zone (Zeu) was determined based on Margalef (1983). The mixture zone (Zmix)
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was estimated based on water column temperature and was considered equal to maximal
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depth (Zmax) when there was no thermal gradient with a minimal difference of 0.5 °C.m-1.
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For the determination of dissolved and total nutrients, water aliquots were placed in 300-
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ml polyethylene flasks and kept refrigerated until analysis. Samples were filtered through 47-
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mm AP20 glass multi-pore filters for the determination of orthophosphate and total dissolved
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phosphorus. Non-filtered aliquots were used for the determination of total nitrogen and total
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phosphorus. Analysis for the determination of concentrations of total nitrogen (μg.TN.L-1)
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followed procedures described by Valderrama (1981). Total phosphorus (μg.TP.L-1) and total
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dissolved phosphorus (μg.TDP.L-1) were determined following Valderrama (1981).
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Orthophosphate (μg.P-PO4.L-1) was determined following Strickland and Parsons (1965).
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The Carlson Trophic State Index adapted by Toledo Jr. et al. (1983) for tropical
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regions was used for the trophic characterization of the ecosystems. Calculations were based
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on Secchi disk values, total phosphorus and orthophosphate. Ultra-oligotrophic (≤ 20),
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oligotrophic (21 to 40), mesotrophic (41 to 50), eutrophic (51 to 60) and hypertrophic ( 61)
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conditions were then determined (Kratzer and Brezonik, 1981). Atomic total N/total P ratios
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were calculated.
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Samples were preserved in Lugol’s solution for taxonomic analysis. Identification was
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performed down to species level using an optical microscope (Zeiss/ Axioskope) or to the
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greatest possible taxonomic resolution using the relevant literature (Prescott and Vinyard,
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1982; Komárek and Fott, 1983; Komárek and Anagnostidis, 1989, 1999, 2005; Popovský and
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Pfiester, 1990; Krammer and Lange-Bertalot, 1991a, 1991b; Komárek and Cronberg, 2001;
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John et al., 2002).
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Aliquots of the samples collected with the Van Dorn bottle were stored in 200-mL
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flasks and immediately preserved in Lugol’s solution for the subsequent phytoplankton count.
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Counts were performed using an inverted microscope (Zeiss/ Axiovert) following the method
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described by Utermöhl (1958). The biovolume of the species was calculated by the number of
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cells and mean cell volume, which were determined using geometric models (Hillebrand et
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al., 1999). Functional groups were established using the criteria proposed by Reynolds et al.
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(2002) and Padisák et al. (2009).
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Statistical methods
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Analysis of variance (ANOVA) was used to determine seasonal and vertical
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differences in abiotic and biotic variables (p < 0.05) using the BioEstat 5.0 program (Belém,
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PA, Brazil). Canonical correspondence analysis (CCA) was performed to assess the
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relationships between algal associations and environmental variables. In the multivariate
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analysis, the matrix with biotic data was constructed with phytoplankton associations that
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accounted for more than 5% of the total biomass per season and the abiotic variables were
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log-transformed (x) and progressively reduced using the stepwise forward procedure available
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on the Canoco 4.5 program (license number CAN6346) (ter Braak and Smilauer, 2002). The
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significance of the variables that explained the variance in biotic data (p < 0.05) was
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determined using the Monte Carlo test, with 999 unrestricted permutations.
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Results
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Physiochemical characteristics
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Throughout the study, the reservoirs analyzed were warm (above 25° C) and eutrophic to
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hypertrophic, with low N:P ratios (Figure 3).
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The Duas Unas reservoir exhibited few vertical thermal differences (< 1 ºC) and
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significantly more acidic (F=5.32, p<0.05) and turbid (F=18.69, p<0.01) waters in the rainy
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season. There was a high concentration of total phosphorus (F=16.91, p<0.01) and dissolved
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phosphorus (F=12.58, p<0.01) in the dry season, in which the euphotic zone was greater
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(Figures 3 and 4).
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The Tapacurá reservoir exhibited thermal mixture in the rainy season, when the water
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column was oxygenated and turbid (F=9.73, p<0.05). Thermal stratification occurred in both
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seasons and was accompanied by reductions in oxygen concentration in the hypolimnion as
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well as an increase in phosphorus content, especially in the dry season (Figure 3).
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At the Jucazinho reservoir, the water had neutral to alkaline pH and thermal
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stratification occurred throughout the entire study. Hypoxia and anoxia occurred only at the
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end of the dry season and beginning of the rainy season. Concentrations of total nitrogen
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(F=8.11, p<0.05) were greater in the rainy season (Figure 3).
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Phytoplankton community
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The Duas Unas reservoir exhibited seasonal differences in biomass values (F=6.24, p<0.05),
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whereas no seasonal variation occurred in the Tapacurá and Jucazinho reservoirs (Figure 4).
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In the Duas Unas reservoir, the taxa with high relative biomasses were Anabaena sp. (H1),
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Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju (Sn), Cyclotella
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meneghiniana Kützing (C), Urosolenia eriensis (H.L. Smith) F.E. Round and R.M. Crawford
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(A) and Synedra acus Kützing (D) in the dry season and Aulacoseira granulata (Ehrenberg)
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Simonsen (P), Melosira varians C. Agardh (P), U. eriensis (A), Anabaena sp. (H1),
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Cryptomonas ovata Ehrenberg (Y) and Cryptomonas sp. (Y) in the rainy season. However,
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seasonal differences occurred in the D (F=34.53, p<0.001) and Sn (F=8.24, p<0.05)
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associations, which had higher values in the dry season (Table 2).
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In the Tapacurá reservoir, Microcystis aeruginosa (Kützing) Kützing (M), C.
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raciborskii (Sn) and Woronichinia botrys (Skuja) Komárek and Hindák (Lo) had the greatest
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biomasses throughout the entire study. Seasonal differences were marked by the greater
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relative biomass of Microcystis flos-aquae (Wittrock) Kirchner (M) in the rainy season and
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greater relative biomass of Anabaena spiroides Klebahn (H1), Geitlerinema amphibium (C.
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agardhii) Anagnostidis (S1), A. granulata (P) and Synedra acus Kützing (D) in the dry season
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(Table 2).
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The phytoplankton community in the Jucazinho reservoir was composed of
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filamentous cyanobacteria (Sn, S1 and H1 associations) and centric diatoms (C association).
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These associations exhibited greater relative biomass in the dry season. Blooms of M.
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aeruginosa and M. flos-aquae, both of which belong to the M association, occurred only in
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one month of rainy season.
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Canonical correspondence analysis
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The Monte Carlo test revealed significant relations (p<0.05) between abiotic and biotic
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variables. The CCA results reveal that depth, orthophosphate and total nitrogen were the main
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determinants in the separation of samples on Axis 1. These variables differentiated the
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reservoir with the least depth from the deeper reservoirs. A, C, D and H1 associations
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exhibited a relation with samples from lesser depths and were abundant in the Duas Unas
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reservoir. Lo and M associations were more abundant in the Tapacurá and Jucazinho
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reservoirs (Figure 5, Table 3).
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Mixture zone, turbidity and light availability were more related to Axis 2, contributing
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toward the variation in temporal patterns. A and P associations exhibited a relation with
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mixture and turbidity. C, D, S1 and Sn associations were more abundant with greater light
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availability in the epilimnion (Figure 5).
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Discussion
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The phytoplankton biomass in the shallow Duas Unas reservoir demonstrated a relation with
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seasonality, with higher values in the dry season. However, biomass values were lower than
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those reported for shallow, eutrophic, subtropical lakes (Rücker et al., 1997; Honti et al.,
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2007) and other shallow tropical reservoirs with the same trophic state (Huszar et al., 2000;
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Crossetti and Bicudo, 2008).
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Low biomass values have been recorded in the shallow, eutrophic Juturnaíba reservoir
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in southeastern Brazil (Marinho and Huszar, 2002). However, the greatest biomasses occurred
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in the rainy season, when M, H1 and Sn cyanobacterial associations were abundant. Except
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for M, these associations contributed most to the biomass during the dry season in the Duas
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Unas reservoir. The lowest biomass values in this ecosystem occurred in the rainy season and
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characterized by the presence of the diatoms A. granulata (P), M. varians (P) and U. eriensis
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(A), the cyanobacteria Anabaena sp. (H1) and the phytoflagellates Cryptomonas sp. (Y) and
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C. ovata (Y). All these associations have the ability to develop in shallow, mixed ecosystems,
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such as the Duas Unas reservoir.
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In the Jucazinho reservoir, which is a deep system, there was thermal stratification in
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both the dry and rainy seasons. A large standard deviation was found in the biomass, with the
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algal dynamics related to the variation in depth and the euphotic layer. The increase in depth
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is explained by the input of water from rainfall, which was insufficient to produce thermal
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circulation, but certainly contributed toward the input of nutrients, which were used by the
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organisms. Thermal stratification affects the optic and nutrient behavior in an ecosystem and
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favors the cyanobacteria better adapted to these conditions (Pennard et al., 2008) or small
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diatoms (Winder et al., 2009).
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The phytoplankton structure in the Jucazinho reservoir remained formed by S1 (G.
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amphibium and P. agardhii), Sn (C. raciborskii) and H1 (A. constricta) cyanobacteria and a
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C diatom (C. meneghiniana). In May 2008 (rainy season), when there was a change in the
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Zeu/Zmix ratio, with limited light in the epilimnion, these associations were replaced by M.
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aeruginosa (M), which had the greatest biomass values of the seasonal cycle (>70 mm3.L-1).
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The greatest phosphorus concentrations (mean value between 670.0 μg.L-1 and 3522.0 μg.L-1)
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were recorded in May 2008, coinciding with the smallest euphotic zone (1.05 m); this was the
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only month in which the euphotic zone was smaller than the mixture zone.
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The conditions in the Jucazinho reservoir contrast those found in the literature, which
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justify the occurrence of S1 associations. In deep lakes, the occurrence of S1 filamentous
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cyanobacteria, such as P. agardhii, is typical of mixed, turbid layers with considerably
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deficient light and these organisms are often accompanied by C. raciborskii (Sn) and
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Aphanizomenon gracile (Lemmermann) Lemmermann (H1). P. agardhii is more successful in
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shallow, mixed ecosystems (Nixdorf et al. 2003). The behavior of the S1 association is
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reported by a number of authors, who attribute its success to a smaller euphotic zone than
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mixture zone (Melo and Huszar, 2000; Burford and O’Donohue, 2006; Babanazarova and
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Lyashenko, 2007; Naselli-Flores and Barone, 2007). In the present study, the epilimnion was
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small and the euphotic zone was larger than the mixture zone during the months in which the
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S1 association exhibited high relative abundance.
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A number of studies on subtropical and tropical ecosystems agree with the positioning
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of the species C. raciborskii, which Padisák and Reynolds (1998) include in the Sn
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association due to its ecological similarity with Oscillatoriales. The Sn association is found in
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warm, mixed layers and is commonly cited for shallow ecosystems (Bouvy et al., 2000;
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Huszar et al., 2000; Mischke, 2003; Stoyneva, 2003; Vardaka et al., 2005; Burford and
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O’Donohue, 2006; Moura et al., 2007a). On the other hand, in studies on tropical and
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subtropical Australian reservoirs, McGregor and Fabbro (2000) found that the greatest
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abundance of C. raciborskii occurred in strongly stratified, deep ecosystems (>15 m);
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according to the authors, this species commonly forms associations with Oscillatoriales,
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especially Pseudanabaenaceae, in conditions of stratification.
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The C diatom (C. meneghiniana) was well adapted to the conditions found in the
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Jucazinho reservoir. However, the size class of this species is intermediate (15 μm and 40 μm)
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and, according to Winder et al. (2009), is not correlated with stratification.
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In a shallow lake in Germany, Wilhelm and Adrian (2008) observed the C association
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in the onset of stratification and Babanazarova and Lyashenko (2007) report this association
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together with filamentous cyanobacteria (S1).
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The M association has been reported to be abundant in shallow lakes and eutrophic
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reservoirs in Europe, occurring in periods of warm water temperature and small euphotic
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layer (Naselli-Flores and Barone, 2003; Babanazarova and Lyashenko, 2007; Çelik and
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Ongun, 2008). In shallow tropical reservoirs in Brazil, stratification, reduced transparency,
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oxygen concentrations in the hypolimnion and an increase in pH are reported to be indicators
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of an increase in the biomass of species of this association (Marinho and Huszar, 2002;
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Crossetti and Bicudo, 2008; Fonseca and Bicudo, 2008). Although occurring in ecosystems
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with greater depths in the present study, the environmental conditions are similar to those
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found in other regions, which confirms the positioning of this association in tropical
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reservoirs.
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In the Tapacurá reservoir, which has an intermediate depth, there was thermal
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variation throughout the year, with periods of stratification and mixture. However, this did not
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contribute toward seasonal variation in the structure and behavior of the phytoplankton
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biomass and Lo, M and Sn cyanobacterial associations predominated throughout the entire
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year. The light deficiency in the epilimnion throughout the entire seasonal cycle certainly
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contributed toward the success of these algae. Seasonality influenced the increase in biomass
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and relative abundance of the M association in the rainy season. Lo and M associations,
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formed by colonial species enveloped in mucilage, are capable of regulating their buoyancy
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during phases of stratification and mixture (Fonseca and Bicudo, 2008), whereas the Sn
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association is adapted to limited light conditions (Padisák and Reynolds, 1998). This certainly
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contributed toward the vertical difference found throughout the study in the Tapacurá
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reservoir. The conditions in this ecosystem are in agreement with the literature regarding the
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occurrence of the Sn association (Padisák et al., 2009) and depth is certainly a limiting factor
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for the consolidation of this association in tropical reservoirs.
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The dynamics of algal associations is influenced by aspects of the food chain,
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especially zooplankton (Reynolds et al., 2000; 2002). While some associations, such as those
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formed by phytoflagellates, are more susceptible to this type of influence, associations of
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filamentous and colonial cyanobacteria are favored. Phytoflagellate associations are
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successful in the littoral region of reservoirs or in shallower ecosystems, in which the top-
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down influence is lesser due to more frequent mixture events (Moura et al., 2007a). On the
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other hand, the relative unpalatability of filamentous and colonial cyanobacteria may favor the
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selection of other algae on the part of zooplankton, thereby maintaining the dominance of
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cyanobacteria (Gragnani et al., 1999). However, the quantification of zooplankton could not
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be performed in the present study, which hinders greater detailing of the top-down influence
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in the algal associations.
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From the results of the present study, the functional classification model appears to
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function very well in shallow, tropical ecosystems, in which the effects of seasonality are
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evident in the behavior of the algal biomass and structural changes in the phytoplankton.
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Although determined by seasonality, the change in thermal behavior in the ecosystem with an
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intermediate depth did not affect the biomass or restructuring patterns of the phytoplankton
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community. Seasonality did not affect the phytoplankton dynamics in the deep reservoir and
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divergences occurred in the use of algal associations. The depth of an ecosystem appears to
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have a strong influence over the behavior of phytoplankton associations in tropical, eutrophic
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reservoirs, whereas seasonality especially affects shallow lakes. Variations in the behavior of
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the euphotic layer cause changes in the phytoplankton structure in the reservoirs of the state of
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Pernambuco.
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A and H1 associations were more abundant in the shallow reservoir with a greater
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euphotic zone, whereas the M association was more related to the deep reservoir with an
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adequate availability of nutrients. C, S1 and Sn exhibited different behavior in the shallow
317
and deep ecosystems. C and Sn associations occurred in the shallow ecosystem with thermal
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mixture and exhibited seasonal variation in months with higher water temperatures. These
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associations also occurred in the deep, stratified ecosystem, with no particular seasonal
320
variation. The S1 association was more related to the deep ecosystem, occurring under
321
conditions of stratification and adequate light availability in the epilimnion. The Tapacurá
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reservoir united characteristics that favor the occurrence of the Sn association, which is in
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agreement with the literature. The conditions in the Jucazinho reservoir may reflect a
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distribution pattern of C, S1 and Sn associations in deep tropical ecosystems, in which
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replacement may be related to the reduction in the euphotic layer rather than the mixture zone,
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unlike what occurs in subtropical systems. The present study confirms the importance of
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phytoplankton associations as indicators of the environmental conditions of tropical reservoirs
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of different depths.
329
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Figure Captions
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Figure 1: Map and location of Duas Unas, Tapacurá and Jucazinho reservoirs, state of
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Pernambuco, Brazil
477
Figure 2: Precipitation, wind intensity and direction in three reservoirs in state of
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Pernambuco (Brazil) between March 2007 and May 2008; Legends: NE = northeast, E = east,
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S = south, SE = southeast
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Figure 3: Mean (columns), minimum and maximum values for (a) water temperature, (b)
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dissolved oxygen (diss. O2), (c) pH, (d) turbidity, (e) total phosphorus (TP), (f) total dissolved
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phosphorus (TDP), (g) orthophosphate (PO4), (h) total nitrogen (TN), (i) N:P ratio and (j) Trophic
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State Index (TSI) in Duas Unas, Tapacurá and Jucazinho reservoirs, state of Pernambuco (Brazil) in
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rainy (R) and dry (D) season
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Figure 4: Euphotic zone (Zeu), Mixture zone (Zmix), maximal depth (Zmax) and variation in
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phytoplankton biomass (mm3.L-1) in Duas Unas (A), Tapacurá (B) and Jucazinho (C)
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reservoirs, state of Pernambuco (Brazil) between March 2007 and May 2008
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Figure 5: CCA ordination among main algal association and significant abiotic variables in
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three reservoirs in state of Pernambuco (Brazil); Abbreviations: TN = total nitrogen; PO4 =
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orthophosphate; Turb = turbidity; ZeuZmix = euphotic zone/mixture zone ratio; Zmax =
491
maximal depth; Zmix = mixture zone; samples are identified with depth (S = surface; B =
492
bottom) and season in which collection was performed (R = rainy season, D = dry season)