Spatial and temporal variations in phytoplankton communities in continental waters have received attention from limnologists, since they are differently influenced by many physico-chemical and biological factors. This study was undertaken with the aim to identify the environmental variables that influence the temporal and spatial dynamics of the phytoplankton near a fish farm in ]]>
H1, MP, S1 and Sn associations was recorded in most of the months studied, except August 2008, when there was a substitution of the
S1 association (Planktothrix agardhii) by the P association (Aulacoseira granulata). Water temperature, precipitation and pH were the parameters with the greatest influence over the temporal variation in phytoplankton, whereas the vertical distribution of the phytoplankton biomass was directly related to the availability of light in the wáter column. There were no spatial or temporal differences in water quality, likely due to the ]]>
Resumen ]]>
Las variaciones espaciales y temporales en las comunidades de fitoplancton en las aguas continentales han recibido la atención de limnólogos, ya que están influenciados de manera diferente por muchos factores físico-químicos y biológicos. El objetivo del presente trabajo fue identificar las variables ambientales que ejercieron influencia sobre la dinámica temporal y espacial de ]]>
las estaciones y profundidades de recolecta. La co-dominancia de cianobacterias pertenecientes a las ]]>
H1, MP, S1 y Sn, fue registrada durante la mayor parte del periodo de estudio, excepto en ago/2008, cuando ocurrió una sustitución de la asociación S1 (Planktothrix agardhii) por P (Aulacoseira granulata) en la ]]>
fetch del agua.
Palabras clave: disponibilidad de luz, Brasil, variaciones climatológicas, represa Jucazinho, asociaciones del fitoplancton.
Spatial and temporal variations in the phytoplankton community have received attention from limnologists worldwide for many years. A number of studies on this community have ]]>
et al. 2007, Borges et al. 2008, Caputo et al. 2008, Dejenie et al. 2008, Lohrenz et al. 2008, Sarmento et al. 2008). ]]>
et al. 1999, Zanata & Espíndola 2002). Others also show the importance of regional climate, hydrological patterns and geo-morphology to the temporal dynamics of phytoplankton, which can cause changes in the availability of nutrients, water flow ]]>
Morpho-physiological factors and buoyancy strategies among species are directly related to spatial variation in phytoplankton, especially vertical variation. Reynolds (1984) recognizes three distinct groups of algae: 1) non-mobile algae, with negative buoyancy and considerable sinking velocity; 2) algae with ]]>
According to Tundisi and Matsumura-Tundisi (2008), studies on the variation and spatial distribution of phytoplankton are important to determine the spatial variability of ]]>
et al. 1999).
According to Diaz et al. (2001), the amount of dissolved nutrients (especially phosphorus and ammonium), ]]>
Anabaena, Microcystis and Oscillatoria. However, ]]>
The demand of potable water in Northeastern Brazil is huge, especially in semi-arid regions. A number ]]>
Jucazinho has considerable importance among the different reservoirs in Northeastern Brazil. It is the largest drinking-water reservoir in the state of Pernambuco, ]]>
Oreochromis niloticus Linnaeus, 1758), which is an important activity for income generation to the surrounding communities and the diversification of the economy. Nonetheless, intensive fish farming may accelerate the deterioration of wáter quality by increasing the nutrient content, overnourishing the water and causing changes to the composition and dominance of species of phytoplankton (Diaz et al. ]]>
et al. 2002, Lazzaro et al. 2003, Panosso et al. 2007).
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While the ecology of reservoirs has been well studied throughout the world (Scheffer 1998), the majority of investigations have been addressed to temperate environments (Moss 1998), whereas studies on reservoirs in semiarid regions are relatively scarce (Naselli-Flores 2003). The aim of the present study was to test the hypothesis that spatial and temporal variation occurs in the dynamics of the phytoplankton community in an eutrophicated tropical ecosystem.
Materials and methods
Study area: The Jucazinho reservoir (Fig.1) (07º57’50’’ S - 35º44’27’’ W) is located at 300m ]]>
Caatinga biome between the municipalities of Cumaru, Riacho das Almas and Surubim in the state of Pernambuco (Northeastern Brazil). The region has a warm, semi-arid, low-latitude climate (BSHs’), with a mean annual temperature of 25º C, mean annual precipitation of 599mm, irregularly distributed rains throughout the year (Albuquerque & Andrade 2002) and a mean wind speed of 5.0m/s.
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Jucazinho is the largest reservoir in the state of Pernambuco, with a volume of 327 million m3, providing water for approximately 800 000 inhabitants. Its maximal depth is 40m and the theoretical residence time is 2 103 days. Constructed over granitic rock and litholytic soil, Jucazinho reservoir is currently hypertrophic (Melo-Júnior et al. 2007). Areas of native Caatinga and farmlands surround this ecosystem, on which the main activities are subsistence farming and cattle breeding. In 2006, the Brazilian National Water Agency (ANA, Brazil), allowed the installation of six intensive fish farms to raise the Nile tilapia (Oreochromis niloticus Linnaeus, 1758) in tank-net systems in this ecosystem. Each farm has a volume of 1 800m3, totaling 10 800m3. Thus, the farms occupy less than 1% of the total volume of the reservoir. Dantas (2010) carried out a study between May 2007 and May 2008 in this same reservoir near the collection sites used in the present study and found that the occurrence of stratification (Zmix<3m) was common throughout the year and that thermal variation between the surface and bottom was more than 1ºC (Fig. 2).
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Sampling and analyses: Water samples for nutrient analysis and the investigation of the phytoplankton community (taxonomic and density studies), were collected at the same time with two repetitions (n=2) using a vertical van Dorn bottle with a capacity of 3L. The samples were collected from three sampling stations (Fig. 1) at two depths (subsurface and ~0.5m from the bottom) in the dry (Oct, Nov and Dec 2008) and rainy (Aug 2008, Feb and Mar 2009) seasons. ]]>
The sampling stations were established near the fish farming tanks in the reservoir. Site 1 (S1) was located 600m upstream from the tanks (S1: 07º59’00.1’’ S - 35º49’03.9’’W); this site has a minimal and maximal depth of 17.5m and 23.9m, respectively. Site 2 (S2) was established 100m downstream from the tanks (07º58’57.5’’ S - 35º48’39.3’’ W), and has a minimal ]]>
Air temperature (ºC), precipitation (mm), wind direction (º) and wind speed (m/s) were obtained from the Brazilian National Meteorology Institute. The following variables were determined in the field: water temperature ]]>
Samples for taxonomic and density analyses (n=2) were preserved in acetic Lugol´s solution. Morphometric features of the reproductive and vegetative phases were analyzed under a Zeis microscope (model Axioskop), equipped with a photographic camera and ocular with a measurement grid and identified down to the lowest possible taxonomic level using specific literature, such as Prescott & Vinyard (1982), Komárek & Fott ]]>
et al. (2002) and Komárek & Anagnostidis (2005).
The Utermöhl method (Utermöhl 1958), with an inverted Zeiss microscope (model Axiovert ]]>
et al. (1999) and Sun & Liu (2003), converted to biomass assuming a specific gravity of 1mg/mm3 (Wetzel & Likens 2000) and expressed as mg/L. The species were categorized in the functional groups proposed by Reynolds (1997); Reynolds et al. ]]>
et al. (2009). Species diversity was calculated from biomass data using the índices proposed by Shannon & Weaver (1963) and Pielou (1966), respectively. Abundance and dominance were determined using the criteria proposed by Lobo & Leighton (1986).
Analysis of variance (ANOVA) was ]]>
Results
Abiotic variables: Absolute and mean air temperature values were lowest in August 2008 and the highest ]]>
Fig.3). There was a significant difference in precipitation between seasons (F=13.16), with mean monthly rainfall of 93.93±42.80mm in the rainy season and 3.53±4.16mm in the dry season (ANOVA, p<0.05). Wind speed was =5.9±0.59 m/s in the dry season and
=4.2±0.45m/s in the rainy season. The predominant wind direction in the region was West to East, except in August 2008, when it was Northeast to Southeast. Mean thermal differences between the surface and bottom were greater than 1ºC, except in August 2008, when the mean difference was 0.5ºC, demonstrating the occurrence of a mixture phenomenon in the water column at this time. The variations in the other hydrological parameters between the surface and bottom are displayed in Figure 4.
No significant differences were found in spatial variation regarding the majority of abiotic variables, with the exception of wáter temperature (F=14.94) and dissolved oxygen (F=29.04) (ANOVA, p<0.05). Higher values occurred in the rainy season for mean water temperature ( =27.7 ± 1.70º C), dissolved oxygen (7.25±3.99mg/L), electrical conductivity ( =1648.78±168.31μS/cm), turbidity (
=50.19±32.45UNT), water transparency ( =0.99±0.14m) and limit of the euphotic zone (
=2.66±0.37m), whereas mean pH ( =7.99±0.44) was higher in the dry season. Throughout the study, water temperature, dissolved oxygen and pH were higher at the subsurface at all sampling sites. Electrical conductivity was generally greater at the bottom of the reservoir (Fig. 4a-f). ]]>
The concentrations of nutrients were always high. The highest total phosphorus content occurred in the rainy season (=343.48±116.26μg/L). There were significant ]]>
Fig. 4g). However, no significant differences were found between sampling sites (ANOVA,p<0.01). There were no spatial or temporal differences in total nitrogen content, thereby demonstrating no distribution pattern for this variable. Total nitrogen was slightly higher in the dry season (
=48.00±36.07μg/L) (Fig.4h). The TN:TP ratio was very low throughout the study, with values above 1.0 only recorded at the subsurface at Site 1 in November and December and at the bottom at Site 2 in November.
Spatial-temporal variation in ]]>
The phytoplankton was made up of 53 species and one variety: Chlorophyta (45.28%), Cyanophyta (30.19%), Bacillariophyta (15.09%), Euglenophyta (3.77%), Cryptophyta (3.77%) and Chrysophyta (1.89%). No significant differences were found in the number of species of Bacillariophyta, Chlorophyta and Cyanophyta between rainy and dry seasons.
Spatially, there ]]>
Fig. 5a) were recorded throughout the study ( =35.28±28.66mg/L in the rainy season and =39.18±23.92mg/L in the dry season), with no significant seasonal differences. However, there were significant vertical differences (F=33.42), with the biomass values at the subsurface ( =55.32±22.86mg/L) on average threefold higher than those at the bottom (=19.15±13.64mg/L) (ANOVA, p<0.01).
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Among sampling sites, there were no significant differences in biomass values at the subsurface in either rainy and dry seasons, whereas significant differences were found at the bottom of the reservoir between Sites 1 and 3 in the rainy season (F=3.51) and between Sites 2 and 3 in the dry season (F=13.62) (ANOVA, p<0.05).
Cyanobacteria and diatoms ]]>
Planktothrix agardhii (Gomont) Anagnostidis and Komárek, Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju, Pseudanabaena catenata Lauterborn and Aulacoseira granulata (Ehrenberg) Simonsen accounting for more than 85.0% of the total biomass, on average. However, the relative contribution of these species varied throughout ]]>
Three taxa were dominant: Anabaena sp. (58.7%) at the subsurface of S1 in the dry season (Dec 2008); A. granulata (56.8%) at the bottom of S1 in the rainy season (Aug 2008); and P. agardhii ]]>
P. agardhii was dominant, the Jucazinho reservoir was characterized by the co-dominance of P. catenata (=17.92±5.80%), C.raciborskii (=22.38±10.25%) and P. agardhii ( =29.08±7.73%) in the dry season at all sampling sites and both ]]>
P. catenata (=14.15±6.19%), P. agardhii (=15.92±15.92%), A. granulata (=23.59±24.78%) and C. raciborskii (=23.80±5.77%) occurred at all sampling sites and both depths.
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Due to the dominance of few species throughout the study, there was low diversity (=2.38±0.57bit/mg). There were no significant differences in species diversity between sampling sites at either depth. However, significant differences were found between seasons (F=16.92) at both the subsurface (F=5.42) and bottom (F=13.26) (ANOVA, p<0.05). Diversity values were generally higher in the dry season at both the subsurface ( =2.75±0.38bit/mg), and bottom ( ]]>
Fig. 5b).
Nineteen functional groups were recorded, with a predominance of groups adapted to conditions of eutrophication. Throughout practically the entire study, there was co-dominance of the S1 ]]>
P. agardhii and Geitlerinema amphibium (Agardh) Anagnostidis), Sn (represented by C. raciborskii), MP (represented by P. catenata) and H1 (represented by Anabaena sp. and Aphanizomenon sp.) ]]>
P association (represented by A. granulata) replaced the S1 group (Fig. 6a and b).
No significant differences were found in the vertical or horizontal distribution of the main ]]>
H1, MP, S1 and Sn were generally greater at the subsurface, whereas the P association had greater biomasses at the bottom. In the dry season, there were significant differences in the biomass of the H1, MP, S1 and
SN associations between the subsurface and bottom (F=6.71) as well as between sampling sites at the bottom of the reservoir (F=5.28) (ANOVA, p<0.05). The S1 association generally contributed most to the total phytoplankton biomass at all sampling sites and both depths in the rainy and dry seasons (Fig. 6a and b).
CCA confirmed the ]]>
Table 1).
The CCA results ]]>
H1, S1 and Sn cyanobacteria occurred throughout the dry season, whereas P diatoms and
MP cyanobacteria occurred in the rainy season (especially in August 2008). The August 2008 sampling units were positively related to Axis 1. This month exhibited a high abundance of P diatoms as well as the lowest water temperature, pH and electrical conductivity values recorded throughout the study. Dissolved oxygen and total phosphorus were related to Axis 2 and differentiated the sampling carried out at the subsurface and bottom, respectively. This analysis also revealed the predominance of H1, ]]>
Sn and MP associations at the subsurface, the P association at both the subsurface and bottom and S1 at the bottom (Fig. 7).
The similarity analysis revealed no significant differences between sampling sites with regard to ]]>
Fig. 8a). At the bottom S2 differed significantly from the other sites (Fig. 8b). Seasonal differences were found only at the subsurface, with August and February (rainy season) separated from the other months (Fig. 8a). But, the clear separation of August in the grouping for both the subsurface (Fig. 8a) and bottom (Fig. 8b) was related to ]]>
P diatoms in this month.
Other environmental peculiarities that occurred in this period were thermal mixture (Fig. 2), the lowest water temperature (Fig. 4a), electrical conductivity (Fig. 4e) and pH ]]>
Fig. 4f) values and a change in wind direction from east to southeast.
Discussion
In the Jucazinho reservoir, the ]]>
Previous studies carried out on relatively small reservoirs located in semi-arid regions in Brazil with volume and water retention time similar to those found at Jucazinho, also report longitudinal homogeneity as well as vertical and seasonal heterogeneity in the abiotic limnological conditions (Chellappa & Costa 2003, Moura et al. ]]>
et al. 2008). In contrast, heterogeneity in the abiotic conditions are reported for the Salto Grande reservoir, which holds a larger volume of water and is located in a wet subtropical region (Zanata & Espíndola 2002), and Lake Caçó, located in a tropical region of Brazil (Dellamano-Oliveira et al. 2003). According to Armengol et al. (1999) and Tundisi & Matsumura-Tundisi (2008), the homogeneity of ]]>
The composition of phytoplankton species in the Jucazinho reservoir reveals an accelerated process of eutrophication, with a predominance of cyanobacteria and Chlorophyceae. Studies carried out in other reservoirs of northeastern Brazil ]]>
et al. 2007a, b, Chellappa et al. 2008, Dantas et al. 2008, Lira et al. 2009). According to Huszar (2000), Chlorococcales is the order with the greatest species richness in freshwater environments in Brazil. Similar results are reported by ]]>
The phytoplankton biomass in the Jucazinho reservoir did not demonstrate a clear relationship with seasonality. However, the biomasses were significantly different between depths, with threefold higher values at the subsurface than at the bottom. While the values recorded for Jucazinho are high, considering the mean biomass obtained for both the subsurface and ]]>
et al. 2010, Sun et al. 2010). Though, considering only the biomass recorded for the subsurface of the Jucazinho reservoir, the value is higher than those recorded for the Chapéu, Pão de Açúcar and Ingazeiras reservoirs in northeastern Brazil (Huszar 2000). High biomass values in aquatic environments may be explained by the large availability of nutrients in both temperate and ]]>
et al. 1990, Sarmento et al. 2008), as well as optimal temperature conditions (Moisan et al. 2002, Oberhaus et al. 2007), and long water retention time (Borges et al. 2008). All these conditions occur in Jucazinho, which explains the high values recorded throughout the entire study.
Reservoirs located in tropical ecosystems generally have limited nitrogen (Ryding & Rast 1989), and the greater availability of this resource may result in an increase in algal density. Some species of cyanobacteria, which was the predominant group in Jucazinho, are endowed with specialized structures for the fixation ]]>
et al. (2008), even with the increase in the density of cyanobacteria related to the limited nitrogen, the dominance of this group may be the result of an increase in phosphorus. In the present ]]>
et al. 2008).
Diversity is considered an ]]>
et al. 2001, Dellamano-Oliveira et al. 2003, Moura
et al. 2007a).
The vertical dynamic of the phytoplankton was mainly related to the depth of the sampling site, with the availability of light a limiting factor to the increase in phytoplankton biomass at the bottom of the reservoir. According to Padisák et al. (2003), cylindrical phytoplankton species have ]]>
According to Reynolds et al. (2002) and Padisák et al. (2009), the dominance of filamentous ]]>
H1, MP, S1 and Sn associations is common in stratified eutrophic environments, whereas organisms belonging to the P association develop better in mixed environments. The dominance of the P association, formed by Aulacoseira granulata var. granulata,
A. granulata var. angustissima (O.F. Müller) Simonsen, Fragilaria capucina Desmazières and Closteriopsis acicularis (Chodat) Belcher and Swale, was associated to high nutrient values (especially total itrogen), lower temperatures and the complete mixture of the water column. Complete mixture was determined by a difference of less than 1ºC between the subsurface and bottom of the water column in August (rainy season), and was related to a change in wind ]]>
The dominance of the S1 association, represented by Planktothrix agardhii and Geitlerinema amphibium, was associated to the high nutrient, temperature, pH, ]]>
P. agardhii is a quite common species in lakes and reservoirs throughout the world and can form persistent blooms in shallow environments for several consecutive years (Chorus & Bartram 1999, Poulí ková et al. 2004). According to Oberhaus et al. (2007), P. agardhii exhibits optimal growth at ]]>
et al. 2002). Its cylindrical shape and numerous gas vesicles give it adaptive advantages, allowing it to float near the surface of the water even under conditions of intense water flow generated by variations in wind speed and direction.
H1, MP and Sn associations were dominant in the dry season, when there were higher nutrient concentrations, a greater concentration of dissolved oxygen and greater wind speed, as these associations generally occur at the subsurface. The H1 association was represented by Anabaena sp. and Aphanizomenon sp. According to Reynolds et al. ]]>
MP association, represented by Pseudanabaena catenata, is formed by periphytic species that ]]>
et al. 2006, Moura et al. 2007a, Padisák et al. 2009).
Although a nitrogen-fixing filamentous cyanobacterium, such as representatives from
H1 and H2 associations, Cylindrospermopsis raciborskii was grouped by Reynolds et al. (2002) in the Sn association due to its environmental preferences similar to organisms pertaining to the S1 and S2 associations, which are formed by non-nitrogen-fixing filamentous organisms. ]]>
Cylindrospermopsis raciborskii biomass was high throughout the study period, thereby reflecting the eutrophic conditions of the Jucazinho reservoir, which has warm, turbid waters throughout the year. According to Padisák & Reynolds (1998) and Reynolds et al. (2002), C. raciborskii is well adapted to warm, mixed environments and has considerable tolerance ]]>
et al. 2006).
The co-dominance and high biomasses throughout the study of potentially toxin-producing cyanobacteria belonging to the S1 (P.agardhii and
G. amphibium), Sn (C. raciborskii), MP (P. catenata) and H1 (Anabaena sp. and Aphanizomenon sp.), associations are troublesome as the toxins produced by these algae can cause mass mortality in fish, birds, crustaceans and cattle and affect human health through skin, hepatic and neurological intoxication that ]]>
P. agardhii and G. amphibium produce microcystins and a neurotoxin (ß-N-methylamino-L-alanine). C. raciborskii produces anatoxin-a(s), cylindrospermopsin, homoanatoxin and saxitoxins. Anabaena sp. and Aphanizomenon sp. produce anatoxin-a and a(s) and saxitoxins (Funari & Testai 2008).
The absence of a longitudinal gradient in the Jucazinho reservoir demonstrates the advanced process of eutrophication in this environment, which is homogeneous with regard to physiochemical conditions. Despite the low nitrogen values, there was no nitrogen limitation for the phytoplankton community. Thus, the availability of light in the water column is certainly the factor that exerts the greatest influence over the spatial and temporal dynamics of ]]>
]]>
The results of the present study also demonstrate that the temporal change in algal structure is explained by changes in the physical conditions of the water between the subsurface and bottom caused by a change in wind direction and consequent change in the fetch of the water. This event only occurred because the reservoir is very long and relatively narrow. In ecosystems with a more regular morphology, this factor may not exert an influence over the phytoplankton community. ]]>
Acknowledgments
The authors are grateful to the Brazilian fostering agency Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the grant and funding for the study (Process 471121/2007-0).
References
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*Correspondencia a:Ariadne do Nascimento Moura & Emanuel Cardoso do Nascimento: Universidade Federal Rural de Pernambuco - UFRPE, Departamento de Biologia, Área de Botânica, R. Dom Manoel de Medeiros, s/n, Dois Irmãos, 52171-030, Recife, Pernambuco, Brazil; ariadne@db.ufrpe.br Ênio Wocyli Dantas: Universidade Estadual da Paraíba - UEPB, Campus V, Centro de Ciências Biológicas e Sociais Aplicadas- CCBSA. R. Monsenhor Walfredo, nº 487, Tambiá, 58020-540, João Pessoa, Paraíba, Brazil. 1. Universidade Federal Rural de Pernambuco - UFRPE, Departamento de Biologia, Área de Botânica, R. Dom Manoel de Medeiros, s/n, Dois Irmãos, 52171-030, Recife, Pernambuco, Brazil; ariadne@db.ufrpe.br 2. Universidade Estadual da Paraíba - UEPB, Campus V, Centro de Ciências Biológicas e Sociais Aplicadas- CCBSA. R. Monsenhor Walfredo, nº 487, Tambiá, 58020-540, João Pessoa, Paraíba, Brazil.
Received 24-I-2011. Corrected 10-II-2011. Accepted 18-III-2011.
=5.9±0.59 m/s in the dry season and