Phytoplankton in Coqueiro Lake ( Pantanal de Poconé , Mato Grosso , Brazil )

Studies on loristic composition are key to understand qualiquantitative changes on phytoplankton assemblages over the year. Spatial-temporal variation in composition, richness, frequency of occurrence, and abundance (semi-quantitative) of the phytoplankton community was analyzed monthly (from April 2002 to May 2003), at 3 stations, in Coqueiro Lake (Pantanal, Mato Grosso, Brazil). We registered 256 taxa, mainly represented by Zygnematophyceae (36%), Chlorophyceae (21%), and Euglenophyceae (14%). The highest average abundance occurred at the limnetic station (2), but Bacillariophyceae, Cyanophyceae, Chlorophyceae, and Zygnematophyceae prevailed at the 3 stations. The highest average richness was obtained at the littoral station (3), but this station showed a signiicantly lower abundance (p < 0.05) than the 2 limnetic stations. The system Biotemas, 28 (2): 9-25, junho de 2015 ISSNe 2175-7925 http://dx.doi.org/10.5007/2175-7925.2015v28n2p9


Introduction
In environments subject to seasonal floods, oscillations in water level are regarded as the driving force in plankton community dynamics (HUSZAR; REYNOLDS, 1997;HUSZAR et al., 1998;TRAIN;RODRIGUES, 1998;CARDOSO et al., 2012), where a set of synergistic environmental and spatial factors respond to these hydrologic variations and lead to changes in communities (LOVERDE-OLIVEIRA et al., 2012).Thus, phytoplankton population cycles are constantly changing, and this causes qualitative and quantitative responses by assemblages over the year (REYNOLDS, 1984).Therefore, knowing the loristic composition of a phytoplankton community is key to understand variations in biomass and density, describe functional groups, trophic status, and dynamics of an aquatic ecosystem (HUSZAR et al., 1998;NABOUT;NOGUEIRA, 2007).
Studies about algal communities in tropical regions are scarce and incipient (LOVERDE-OLIVEIRA et al., 2012), but it has been shown that quantitative and qualitative variations are related to the climatic and hydrologic regime (PAYNE, 1986;DIAS JR., 1990;ESPÍNDOLA et al., 1996;LOVERDE-OLIVEIRA;HUSZAR, 2007), and that phytoplankton dynamics is controlled by a combination of several hydrodynamic processes acting on different spatial and temporal scales (CALIJURI, 1988).
Along with loristic knowledge, there is a growing need to investigate phytoplankton ecology in the Pantanal (LOVERDE-OLIVEIRA et al., 2012), since this is a peculiar, wide, and complex system (BOZELLI; HUSZAR, 2003).Knowledge on qualitative and quantitative composition and phytoplankton productivity is crucial for better using these ecosystems (DIAS JR., 1990), as studying plankton organisms from marginal lakes may provide primordial information to develop ecological theories.
It is worth emphasizing that the current knowledge on epicontinental algae, with higher concentration of studies in the Brazilian South and Southeast regions and lower concentration in the North and Central-West regions (BICUDO; MENEZES, 2010), is very heterogeneous, not only when the geographic region is taken into account, but also when the taxonomic group is considered.Therefore, studies based on ecological compositional and diversity attributes are needed to boost applied and experimental research on Phytoplankton in Coqueiro Lake, Pantanal phytoplankton.Thus, this study aimed to analyze the composition, species richness, frequency of occurrence, and abundance (semi-quantitative) of phytoplankton species at three sampling stations in Coqueiro Lake, at the different phases of the hydrological cycle in the Pantanal.

Study area
Coqueiro Lake (Figure 1) is located in the municipality of Nossa Senhora do Livramento (16º15'12"S; 56º22'12"W), within the sub-region Pantanal de Poconé, in the state of Mato Grosso, Brazil.It is a loodplain permanent lake, with elongated shape, 4 km long and 1 km wide (total area: < 2.5 km 2 ); it is shallow (maximum depth: 2.3 m) (LOVERDE-OLIVEIRA et al., 2007).During the drought, this lake remains isolated from the other water bodies and during the lood it is connected to Piraim river, a tributary on the right bank of Cuiabá river.The region climate (Köppen) is Aw type, warm and wet, with rainfalls in summer and low water in winter.Total annual rainfall (1,259 mm) and the annual average air temperature (27ºC) are within the climatological patterns within the region, when compared to the historical means (800-1,600 mm and 26ºC, respectively) (LOVERDE-OLIVEIRA et al., 2007).

Sampling and data analysis
Data on rainfall in the region was provided by the 9 th Weather Forecast District of the National Institute of Meteorology (INMET), Cuiabá, Mato Grosso, Brazil.
Phytoplankton samples (n = 39) were taken monthly, from April 2002 to May 2003 using plankton net (25 mm) and they were preserved with Transeau (1:1).Samplings were accomplished through 10 vertical hauling on the water column at three sampling stations: site 1-on the limnetic region under lotic inluence during the lood; site 2-on the deepest part from the limnetic region in the lake; and site 3-located on the littoral region close to aquatic macrophytes (Eichhornia azurea (SW.)Kunth, E. crassipes (Mart) Solms-Laubach, Salvinia sp.Weevil).
In order to determine the abundance and frequency of occurrence, samples were previously homogenized, and we used 0.5 mL by glass slide.The number of slides was previously determined through the curve speciesarea, totaling 15 slides/sample.Thus, the phytoplankton community was characterized qualitatively and semi-  For the qualitative analysis, the material was oxidized, according to Simonsen (1979), modiied by Moreira-Filho and Valente-Moreira (1981).We adopted the classiication system provided by Van den Hoek et al. (1997).
The species were regarded as abundant and dominant according to the criteria provided by Lobo and Leighton (1986).The frequency of occurrence (F) was expressed as the relationship between the occurrence of different species and the total number of samples.The species were classiied as constant when F > 60%; common: 20% < F < 60%; and rare: F < 20% (GOMES, 1989).
Based on the results of rainfall and water level, 4 periods were established: period I-falling or decrease in water level (April to July 2002); period II-low water (August to November 2003); period III-rising or increase in water level (December 2002 andJanuary 2003); and period IV-high water (February to May 2003).
Through the numerical abundance within seasonal periods and at the sampling stations, we conducted a Cluster Analysis (Systat 12) and a Friedman Analysis of Variance (a=0.05;BioEstat 5.0).

Variations in rainfall and water level
The lower rainfall values within the Cuiabá region occurred during the falling (period I) and the higher ones, from October, with a maximum (297 mm) in January 2003, within period III.At this time, there was a lood in the Cuiabá river loodplain, with a consequent increase in water level in Coqueiro Lake.The period of high water (IV) was characterized by decrease in rainfall and higher values in average depth on the water column (Figure 2).
There was higher similarity in the variation of phytoplankton abundance between the sites E1 and E2, and E3 was the most distinct in comparison to the other two.Between the periods from the hydrological cycle, periods I and IV were more similar, as well as periods II and III (Figure 6).Concerning spatial variation in species classified as abundant and dominant, we observed maximum values of A. granulata var.granulata in August 2002 (50%) and September 2002 (79%), both at the limnetic site (1) and that of Chlorophyceae C. reticulatum (87%) in July 2002 also at the site (1) (Appendix 2).In July 2002, C. reticulatum also contributed with 92% to abundance at the limnetic site (2) and Aphanothece smithii Komárková-Legnerová & Cronberg., represented 68% from the total of the community abundance in February 2003, at this site.In relation to the littoral site, there was no abundant and dominant species, but A. ambigua contributed with around 40% to abundance in October 2002, and Lepocinclis ovum (Ehrenberg) Lemmermann, A. ambigua and E. fottii were constant throughout the seasonal cycle at this site (Figure 5).Furthermore, we registered species constancy and dominance of Aulacoseira spp.throughout the hydrological cycle.

Frequency of occurrence
When considering the frequency of occurrence, at the irst limnetic site, 58% of the species were considered as rare, 34% as common, and 8% as constant.At the site (2), 69% of the species were classiied as rare, 27% as common and 4% as constant.The littoral site (3) consisted in 42% of rare species, 48% common, and 10% constant (Figure 7).
Out of the total number of species identiied (256 taxa), 111 were rare, 45 were common, and 7 species were registered as constant for the 3 sites.Most of the rare species belong to the Zygnematophyceae class, such as

Discussion
Coqueiro Lake has a loristic composition similar to the other aquatic systems in the Pantanal, but different from the other rising lakes (LIMA, 1996;DE-LAMONICA-FREIRE;HECKMAN, 1996), due to the high values of species richness and abundance.
Great contributions by Zygnematophyceae, in the high water period, are related to the high number of representatives from the periphytic community [Gonatozygon monotaenium, Hyalotheca dissiliens, Bambusina borreri, Staurodesmus clepsydra Teiling and Teilingia wallichi], also described by Camargo et al. (2009).The occurrence of these species on plankton may be related to water turbulence, which causes the detachment of these organisms from the substrate, contributing to the increased species richness on phytoplankton.According to Train (1998), interrelations between phytoplankton and periphyton, with several species regularly occurring in both biotopes, are frequently observed in shallow lakes colonized by aquatic macrophytes.42% of rare species, 48% common constant (Figure 7).The great contribution by Chlorophyceae to species richness, after the rising period, may have occurred due to the higher availability of light on the water column, since Coqueiro Lake, during the high water in the hydrological cycle, has a deep euphotic zone (LOVERDE-OLIVEIRA, 2005).Euglenophyceae were beneited by the increased availability of organic matter within the rising period, where there is a great input of allochthonous material in the lakes of Pantanal, coming from adjacent lotic systems (NOGUEIRA, 1989) and the loodplain.The higher contribution by Euglenophyceae was registered under conditions of low hydrometrical level and reduced water transparency (RODRIGUES et al., 2002).In the Paraguay river and Tamengo Channel in the Pantanal of Mato Grosso do Sul, a greater species richness of this group was observed during the rising, with contributions by Trachelomonas volvocina Ehernberg and Trachelomonas volvocinopsis (SILVA et al., 2000).
Greater richness in the dry season and lowest richness in the rising and high water also have been reported by Loverde-Oliveira (2005) and Loverde-Oliveira and Figueiredo (2009).The greater abundance in loodplain lakes during the low water are due to the reduced depths and wind action that, among other factors, are determinant of conditions involving high turbulence, turbidity, and high availability of nutrients (LOVERDE-OLIVEIRA, 1999;TRAIN et al., 2001).The lood is responsible for decreased phytoplankton abundance, primarily due to the dilution effect, which determines a decrease in planktonic populations (LOVERDE-OLIVEIRA; HUSZAR, 2007), along with a increase in the number of taxa and diversity (TRAIN et al., 2001).
Abundance was represented by few species (Aulacoseira spp., Coelastrum reticulatum, Planktolyngbya sp., Anabaena spp.and Eutetramorus fottii).This finding was expected, because the communities consist of a small number of species with many individuals or, sometimes, by only one species that prevails along with several species with lower representativeness (MARGALEF, 1983).The temporal distribution pattern shown by abundance accompanies the hydrometric luctuation generated by the lood pulse, with periods in the hydrological cycle signiicantly different, whose maximum lies on the low waters and the minimum on the high waters.
Among the centric diatoms registered in the Coqueiro Lake, Aulacoseira granulata has shown high abundance values regardless of the period in the seasonal cycle, however, the conditions found in the low water are key for the establishment and reproductive success of these algae (REYNOLDS, 1984), as they are characterized by dominance in environments with constant movements in the water column, facilitating permanence in the euphotic zone, besides nutrient availability (MOURA, 1997).The dominance of Aulacoseira granulata and its varieties were registered in Sá Mariana Lake (LOVERDE-OLIVEIRA, 1999) and Recreio (LIMA, 1996), in the Pantanal; Patos Lake, in the Upper Paraná river loodplain (RODRIGUES et al., 2002), and also in Paraguay river (SILVA et al., 2000).
The higher inluence of a river at the limnetic sites may explain the lower species richness on phytoplankton when compared to the littoral site with lower current flow and close to aquatic macrophyte stands.The greater number of rare species may have occurred due to the connectivity with to lotic systems that increase the low of individuals coming from other niches.The inlow of the river to the marginal lakes causes changes in the physical and chemical characteristics of the water in the lakes, and thus changing the distribution, the composition and abundance of phytoplankton (DIAS JR., 1990).
The greater number of common species and species richness, mainly consisting in Zygnematophyceae and Phytoplankton in Coqueiro Lake, Pantanal Euglenophyceae, were registered at the littoral site and this inding is associated with closeness to aquatic macrophytes that provide a constant supply of species detached from the periphyton and occurring on plankton, as the loristic composition of plankton from lentic and shallow biotopes, with or without connection to rivers or secondary channels, has phytoplankton complexity and similarity between diversity in the littoral and limnetic zones.The similarity between some biotopes with higher species richness in the littoral zone, when compared to the limnetic zone, is due to addition to the plankton of metaphytic and periphytic algae, mainly desmidiales and diatom (TRAIN et al., 2001).Thus, corroborating Loverde-Oliveira et al. ( 2012), the composition of phytoplankton community in marginal lagoons has a strong relation to habitat quality and it relects the availability of niches in the aquatic ecosystem.
In general, the lood pulse was key to the variation in phytoplankton abundance in the Coqueiro Lake.The frequency of occurrence of rare, constant, and common species is also associated with oscillations in water level, corroborating the information that, in shallow lakes, seasonal variations in structure and abundance of plankton communities are generally combined to hydrometrical changes (LIMA, 1996).
The groups of phytoplankton algae had their abundance inluenced by the hydrological cycle, with decrease during the high water and increase during the low water, probably responding to factors such as lotic inluence, close to stands of aquatic macrophytes, among other physical and chemical factors of water.Variations in abundance, species richness, and frequency of occurrence evidenced that the dynamics of this community tends to be similar to other rising lakes driven by the lood pulse, but they keep peculiar characteristics of each aquatic system.Based on our results, it was possible to verify a high richness of species of phytoplankton algae in the Coqueiro Lake.The composition and number of phytoplankton species in the lagoon proved to be inluenced by closeness of macrophytes, promoting a interrelationships between phytoplankton and periphyton, and also by increased hydrological stability within the drought period.Just as underlined by the literature, the limnetic region shows a higher abundance of phytoplankton algae.The number of individuals (numerical abundance) was directly related to seasonal hydrological variations of the system, with its apex within the dry period, reasserting the lood pulse as the deining factor of the temporal and spatial distribution of richness and abundance.Some authors (ALHO, 2011;ALHO, et al., 2011) have conirmed the importance of the increasing number of studies addressing loristic composition and spatialtemporal variations, which are key to improve knowledge on biodiversity in the Pantanal, a system requiring further investigation, as it has been increasingly threatened by anthropogenic pressures.

FIGURE 1 :
FIGURE 1: Location of Coqueiro Lake within Pantanal de Poconé and the samplings sites.
12S.F. Marçal e S. M. Loverde-Oliveira quantitatively by counting of taxa and importance (numerical abundance) of each taxon in the samples, respectively.

FIGURE 2 :
FIGURE 2: Variation in rainfall and mean depth in Coqueiro Lake from April 2002 to May 2003.(Periods: I-falling; II-low water; IIIrising; IV-high water and beginning of the falling).

FIGURE 3 :
FIGURE 3: Relative contribution of taxonomic classes to the phytoplankton from Coqueiro Lake.

FIGURE 4 :FIGURE 5 :
FIGURE 4: Variation in numerical abundance and taxa richness at sites E1, E2, and E3; periods: I-falling; II-low water; III-rising; IVhigh water and beginning of the falling.

FIGURE
FIGURE 5: Relative abundance of taxonomic classes and E3; periods: falling; FIGURE 6: Dendrograms of Sorensen similarity for numerical abundance among the sites (E1, E2, and E3) and between the periods (PI, PII, PIII, and PIV).

FIGURE 7 :
FIGURE 7: Frequency of occurrence of species rare, common and constant, at the 3 sites from April 2002 to May 2003.