Phytoplankton community of Reis lake in the Brazilian Amazon

Reis Lake is located in the municipality of Caracaraí, state of Roraima (Brazil) and is subject to fl uctuations in water level. The aim of this study was to analyze the structure of the phytoplankton community on the nictemeral and seasonal scales and determined the infl uence of limnological variables. Sampling was performed in the rainy season (June/2006) and dry season (November/2006), considering two nictemeral cycles. The phytoplankton community was assessed with regard to composition and density, abiotic variables were analyzed simultaneously. The lake had low concentrations of oxygen, clinograde profi le and water stratifi ed during the day and homogenous at night, with low concentrations of nutrients and waters ranging from slightly acidic to alkaline. The phytoplankton was represented by 43 taxa, 35 species in the dry season and 29 species in the rainy season. Low densities of phytoplankton occurred in both nictemeral cycles, with accentuated vertical gradient. The highest densities were recorded in the dry season. Reis Lake exhibits characteristics that classify it as a polymythic and oligotrophic environment. The variability in the data was more important seasonally than on the nictemeral scale, supporting the hypothesis of the infl uence of the hydrological cycle on the dynamics of phytoplankton communities in fl oodplain lakes.


INTRODUCTION
Brazilian Amazon has a hydrographic basin with a large variety of aquatic systems distinguished by their combination of physical, chemical and biological characteristics.Some lakes located in depressions of the Boa Vista Formation are generally small and isolated from large and medium-sized rivers (Silva et al. 2010).In these areas, lakes generally have clear waters that may be either occupied by different species of aquatic macrophytes and fi lamentous algae or deprived of vegetation (Filho et al. 1997).
The area drained by the Branco River basin creates numerous lakes that are characterized by remaining connected to the river during the fl ood period and becoming isolated in the dry season.These lakes are used by the surrounding population, mainly for fi shing or for recreation.Although the importance of studies in fl oodplain lakes is recognized for understanding the ecology 649-663 ISE G. SILVA, ARIADNE N. MOURA and ENIO W. DANTAS of these environments and the river systems to which they are linked, surveys in fl oodplain lakes in the Brazilian Amazon are still punctual (Melo andHuszar 2000, Melo et al. 2004).Hydrographic and hydrological characteristics are suggested as being the factors that determine the behavior of the phytoplankton of these lakes.
The effects of water-level fl uctuations as a major factor in the composition and dynamics of phytoplankton communities in fl oodplain lakes have been discussed by several authors (Ganf 1974, Ibañez 1998, Barbieri et al. 1989, Nabout et al. 2006).
Precipitation, wind and water-level fl uctuations may be much more relevant than light and temperature on seasonal patterns of phytoplankton in tropical lakes.In the Albuquerque Lake (Pantanal Matogrossense) the highest phytoplankton densities were observed in low water periods and lower densities were observed during high waters, as a consequence of the availability of nutrients and light that are also infl uenced by variation in water level (Espíndola et al. 1996).
The algal community is considered a good indicator of the changes that occur in an aquatic environment due to its rapid response to short time intervals, especially regarding reproductive processes.Thus, knowledge of the structure and functioning of these biological communities, as well as their interaction with the physical environment become essential for understanding the behavior of these environments, aiming to achieve the sustainable use of resources and access to future generations.
Based on the hypothesis that spatial and temporal patterns of phytoplankton in fl oodplain lakes are infl uenced by fl uctuations in abiotic variables as a result of variation in the water level in these environments, this study aimed to characterize a lake ecosystem of the fl oodplain of the Branco River, in the Brazilian Amazon, with regard to the composition and dynamics of the phytoplankton community and the infl uence of environmental variables on this community during the period of high waters (rainy) and low waters (dry).

MATERIALS AND METHODS
Reis Lake (01°30'59,1" N e 61°15'50,4" W) is located on the right bank of the Branco River, in Caracaraí, southern region of the state of Roraima, in the Brazilian Amazon.It has an area of approximately 19.2 ha and, since it is connected to the Branco River, it exhibits high water-level fl uctuation, reaching a maximum depth of about 8 m during high waters and a minimum depth of 1.5 m during low waters.The lake has slightly dark waters and its margins are well-preserved.
Based on the Köppen-Geiger classifi cation, the state of Roraima pertains to the climatic group A (humid tropical).The rainfall pattern is represented by two rather distinct periods: a rainy season (April to September) and a dry season (October to March) (Silva et al. 2010).
Water samples for nutrient analysis and the investigation of the phytoplankton community (taxonomic and density studies) were collected at the same time and with two repetitions with a vertical Van Dorn bottle with a 3L of capacity at a central station in the lake over 24-hour sampling periods from the subsurface, middle of the water column and approximately 30 cm above the bottom.Samples (n = 2) were taken at four-hour intervals for a total of seven collections per period (Noon,4 p.m.,8 p.m.,12 a.m.,4 a.m.,8 a.m. and midnight).Sampling was performed in the rainy season (June 2006) and dry season (November 2006).
Samples for taxonomic and density analyzes (n =2) were preserved in acetic Lugol's solution.Morphometric features of the reproductive and vegetative phases were analyzed under a Zeiss microscope (model Axioskop) equipped with a light chamber, photographic camera and ocular with a measurement grid.Those specimens for which identifi cation was not possible were considered phytofl agellates.The samples were added to the collection at the Professor Vasconcelos Sobrinho Herbarium of the Universidade Federal Rural de Pernambuco.
Densities (individuals per microliter) were estimated based on the method described by Utermöhl (1958), using an inverted microscope (Zeiss, Axiovert).Organism counts were carried out with two repetitions for each depth sampled; the values are presented as the mean of the repetitions.The calculations were carried out based on the method described by Villafaiñe and Reid (1995).Dominant and abundant species were determined based on the concepts described by Lobo and Leighton (1986), for which a dominant species is that which surpasses 50% of the total phytoplankton density and an abundant species is that with a density value greater than the mean value of the community.The values are presented as the mean of the repetitions.
Analysis of variance (ANOVA) was used with a 5% level of signifi cance to determine the degree of temporal variation (time of day, season), seasonal period and spatial variation (depth).Tukey's multiple comparison test was used to identify where differences were expressed in time and space.Analyses were performed using the Statistica 2004 software program (StatSoft, Inc., Tulsa, OK, USA).The Shannon-Wiener diversity index (H', bits/ind) was calculated (Shannon and Weaver 1948); Evenness was assessed based on the H' of the Shannon-Wiener index.Canonical correspondence analysis (CCA) was used to determine correlations between biotic and abiotic variables.In the multivariate analysis, the matrix with biotic data was constructed with abundant and dominant species and the abiotic variables were log-transformed (x).The CANOCO 4.5 program (license number CAN6346) was used for the statistical analysis.

RESULTS
The thermal structure of the water of Reis Lake during the dry period is characterized by a system with stratifi ed surface layers during the day (thermal variation from 1.1 to 3.5°C) and homogenization at night until the early hours of the morning.During the rainy period the water column is completely unstratifi ed at all sampled hours (Table I).ISE G. SILVA, ARIADNE N. MOURA and ENIO W. DANTAS The highest concentrations of dissolved oxygen were observed in the dry season (F = 129.602,p < 0.001), characterized by a clinograde profi le in most of the sampled hours.The water column was homogeneous with low dissolved oxygen concentrations during the rainy season.
The pH values were stable (6.90) in the rainy season and showed a low amplitude in the dry season with values close to neutral and slightly alkaline.Electrical conductivity (F = 57.08,p <0.01) and turbidity (F = 2,378.85,p < 0.01) were more pronounced during the rainy season, where turbid waters were observed in the subsurface (F = 100.07,p < 0.01) (Table I).Water transparency was low during the two nictemeral cycles, ranging between 0.7 m and 1.0 m.The minimum value was found during the dry season (Z max 1.8 m) and the maximum value occurred during the rainy season (Z max 8.0 m).The euphotic zone ranged from 2.1 m to 3.0 m in depth and comprised the entire water column during the dry season.
The Reis Lake was characterized by low nutrient concentrations.Total nitrogen, nitrate and nitrite showed similar nictemeral variation patterns, with slightly larger values toward the bottom (Tukey p < 0.05) in both seasons and irregular oscillations over the hours, especially during the dry season (p < 0.05) (Table I).
The concentrations of total phosphorus and total dissolved phosphorus were higher in deeper layers (Tukey p < 0.05) in both seasons and in most of the sampled hours.Although no signifi cant vertical differences were observed, concentration of orthophosphate showed a similar trend.The lowest concentrations of phosphorus elements in the rainy season (F TP = 78.42 and F TDP = 16.636,p < 0.01) signifi cantly contributed to an increase in the TN:TP atomic ratio and a reduction in trophism.The ecosystem is characterized as limited by nitrogen (NT:PT < 12 ratio), oligotrophic (IET < 41) during the rainy season and generally mesotrophic in the dry season (Table I).
The seasonal analysis showed the presence of 35 species in the dry season and 29 species in the rainy season.Chlorophyta and Bacillariophyta had the largest number of species in the dry season (17 spp and 6 spp, respectively) (Table II).
Of the taxa surveyed, 14 were abundant during the two nictemeral cycles.Chlorophyta contributed with four species, Bacillariophyta with four, Cyanophyta with three, and Chrysophyta and Euglenophyta with one species.The species Tabellaria sp.(Bacillariophyta) and Phormidium sp.(Cyanophyta) as well as the phytofl agellates were dominant throughout the study (Table III).
The pattern of distribution of phytoplanktonic density was characterized by the formation of well-defi ned vertical gradients, with higher values at the subsurface and lower ones in the deeper layers of the lake.Regarding seasonal variation, the rainy season was characterized by having low densities, while the highest densities occurred in the dry season.
Bacillariophyta contributed with 57.3% of the total density, and Tabellaria sp was primarily responsible for this contribution.This species was present only during the period of low waters and its distribution in the water column showed small variations, with higher densities occurring usually at the subsurface.The pattern of distribution of Bacillariophyta was the inverse to other groups, in which the highest densities occurred in the deeper layers.
Chlorophyta    The phytofl agellates were the third most important group, quantitatively, accounting for 15.3% of the total density.
The specifi c diversity was variable between hours and depths, with low, medium and high values.The equitability values in the Reis Lake were mostly below 0.5, characterizing a nonuniform distribution of the species (Fig. 2).
The results of the CCA analysis are summarized in Table IV and Figure    In axis 2, water temperature and total nitrogen were the most important variables in the intra-set correlations, related to the axis in positive and negative ways, respectively.The sampling units ordered by this axis showed vertical variation, the samples being collected at the subsurface on the positive side and at the bottom in the opposite direction.Lepocinclis ovum (Ehrenberg) Lemmermann was the taxon most closely related to this axis, occurring especially in the dry season and in the superficial layers of the lake.

DISCUSSION
The fl ood pulse is the main force responsible for nutrient dynamics, changes in the structure of aquatic communities, as well as the way in which humans occupy and exploit the fl oodplains (Junk et al. 1989).
According to Forsberg et al. (1988) the lakes of the Amazon fl oodplain receive water and nutrients primarily from two sources: the local watershed and the main river, and the seasonal variations in water level can cause large changes in the area and depth of these lakes.
The water level fl uctuation of the Branco River caused by seasonal variation is a main factor in determining the ecological processes of the Reis Lake.Large oscillations in the volume and depth of the lake directly infl uence the dynamics of the limnological variables and biota.The thermal stability of the water column during the low water period was probably responsible for the distribution pattern of dissolved oxygen that exhibited a clinograde profi le.These conditions also infl uenced the dynamics of nutrients, contributing to accumulation events in the deeper layers.These events can lead to limitations in nitrogen and high phosphorus concentrations, confi rmed by the low NT:PT ratio found in the lake.
The environmental characteristics observed in the Reis Lake corroborate Tundisi et al. (1984) who associated the depletion of dissolved oxygen and nutrient accumulation in the deeper layers of two Amazonian lakes to their thermal stratifi cation.In the same way, the behavior of the abiotic conditions of the Reis Lake confi rms the fi ndings by Esteves et al. (1994) for Batata and Mussurá Lakes, two fl oodplain lakes of the Trombetas River basin (state of Pará), where the thermal behavior was responsible for the homogeneous vertical distribution of pH, conductivity and dissolved oxygen.
The distribution of phytoplankton in the water column is strongly infl uenced by the physicalchemical conditions of the water, such as light availability, temperature, turbulence, concentration of dissolved oxygen, and nutrients (Esteves and Suzuki 2011) that in turn exhibit signifi cant temporal variations as a consequence of the fl ood pulse (Nabout et al. 2006).The temporal dynamics of the phytoplankton community in Reis Lake displayed fl uctuations as a function of the hydrological pulse.The highest densities occurred in the dry season (low water) and the lowest in the rainy season (high water); factors such as turbidity and nutrient availability, were certainly responsible for these variations.This confi rms the fi ndings by Espíndola et al. (1996) who observed higher phytoplankton densities in the low water period and lower densities during high waters, sustaining that these differences were due to variations of light and nutrients, which were infl uenced by water level fl uctuations.High densities in the low water period were also observed by Huszar (2000) for Batata Lake and by Pinilla (2006) for Boa Lake (Colombian Amazon).In Batata Lake, the incorporation of nutrients and frequent mixing of the water column during low waters infl uenced the increase in density.Other authors also discuss the infl uence of the fl ood pulse on the structure and composition of the phytoplankton community (Melo and Huszar 2000, Domitrovic 2003, Melo et al. 2004).
The high diatom densities observed in the deeper layers of the Reis Lake during the low water period are explained by their sedimentation ability, confi rming the statement made by Esteves (1988).
The phytoplankton composition of the Reis Lake is similar to that found in other Amazonian lakes (Ibañez 1998, Huszar 1996, Melo and Huszar 2000, Echenique et al. 2004, Nabout et al. 2006, Souza et al. 2007) with Chlorophyta being the predominant group in most studies.
The canonical correspondence analysis showed that the variability of the data was more important seasonally than on the nictemeral scale, reinforcing the hypothesis that the hydrological cycle infl uences  the dynamics of phytoplankton communities in fl oodplain lakes.In the rainy season, turbidity was responsible for the dynamics of the phytoplankton community, when the lowest densities were recorded.In the dry period, the variables dissolved oxygen, pH, nitrate and phosphate infl uenced the temporal pattern of the community.High densities of Aucoloseira granulata, Melosira varians, Tabellaria sp.(Bacillariophyta) and Phormidium sp.(Cyanophyta) as well as the phytofl agellates, were observed during the study.

CONCLUSION
The hydrological pulse was the determining factor in the dynamics of the phytoplankton community, particularly because it regulated the low values of turbidity and nutrient availability, and infl uenced the changes in the phytoplankton densities.
The highest densities were recorded in the dry season and the lowest densities were recorded in the rainy season.Reis Lake exhibited characteristics that classify it as a polymythic, oligotrophic environment.The analysis demonstrated that the variability in the data was more important seasonally than on the nictemeral scale, supporting the hypothesis that the hydrological cycle infl uences the dynamics of phytoplankton communities in fl oodplain lakes.Palavras-chave: fi toplâncton, nictemeral, lagos de várzea, sazonal, estado de Roraima.

TABLE I Physical-chemical variables and Trophic Index State, over 24-hour sampling periods, at the subsurface, middle and bottom of the Reis lake, state of Roraima, Brazil, during rainy and dry seasons of 2006
. ISE G. SILVA, ARIADNE N. MOURA and ENIO W. DANTAS

TABLE II Phytoplanktonic species registered at Reis Lake, State of Roraima, during rainy and dry seasons of 2006. (R: Rainy season; D: Dry season).
ISE G. SILVA, ARIADNE N. MOURA and ENIO W. DANTAS 3. The CCA indicated that the eigenvalues of axes 1 and 2 explained

TABLE III Abundant species over 24-hour sampling periods. at the subsurface. middle and bottom of the Reis Lake. state of Roraima. Brazil. during rainy and dry seasons of 2006
. PHYTOPLANKTON COMMUNITY OF FLOODPLAIN LAKE Scenedesmus quadricauda Chodat and Tabellaria sp.

TABLE IV Statistical summary and correlation coeffi cients for phytoplankton species and abiotic variables on the fi rst two CCA axes for the Reis Lake, state of Roraima, Brazil
. ISE G. SILVA, ARIADNE N. MOURA and ENIO W. DANTAS