Brazilian Journal of Biology https://doi.org/10.1590/1519-6984.

222607
ISSN 1519-6984 (Print)
Original Article
ISSN 1678-4375 (Online)

Structure and dynamics of the protoplankton community in an

environmentally protected urban stream
M. A. M. Lipperta , F. M. Lansac-Tôhab , B. R. Meirab , L. F. M. Velhob,c  and
F. A. Lansac-Tohab* 
a
Programa de Pós-graduação em Biologia Comparada, Universidade Estadual de Maringá – UEM,
Av. Colombo, 5790, CEP 87020-900, Maringá, PR, Brasil
b
Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura – NUPELIA, Programa de Pós-graduação em Ecologia de
Ambientes Aquáticos Continentais, Universidade Estadual de Maringá – UEM,
Av. Colombo, 5790, CEP 87020-900, Maringá, PR, Brasil
c
Instituto Cesumar de Ciência, Tecnologia e Inovação – ICETI, Centro Universitário Cesumar – Unicesumar,
Av. Guedner, 1610, CEP 87050-900, Maringá, PR, Brasil
*e-mail: [email protected]

Received: April 12, 2019 – Accepted: July 31, 2019 – Distributed: November 30, 2020
(With 10 figures)

Abstract
We aimed to investigate spatial and temporal scales, abundance, and factors that structure the communities of protozoans
in a tropical urban stream. Methods: Samples of water for analysis of biological communities (testate amoebae, ciliates
and bacteria) and limnological variables were taken in the Mandacaru stream located in the Conservation Unit of
Parque do Cinquentenário, in the city of Maringá, Paraná State, Brazil, in two hydrological periods (dry and rainy).
We calculated the Water Quality Index (WQI) composed by nine parameters of water quality (dissolved oxygen,
thermotolerant coliforms, pH, BOD, water temperature, total nitrogen, total phosphorous, turbidity, and total solids),
Trophic State Index (TSI) for phosphorous and we used a Redundancy Analysis (RDA) to verify the influence of
environmental variables in the protozoan community. Results: The WQI showed that water quality was considered good
in some points and considered bad in other points. The TSI for phosphorus classified the stream as mesotrophic in the
majority of sampled sites points (mean between 53.09 and 58.35). We identified 19 taxa of testate amoebae, belonging
to six families, being Difflugiidae, Centropyxidae, and Arcellidae those with more species and 71 infrageneric taxa of
ciliates, distributed in 12 orders being Peniculida the most representative order, followed by Euplotida. According to
RDA analysis, samples of the dry period were characterized by higher values of bacteria density and concentrations of
chlorophyll-a, total phosphorous, and total nitrogen. Ciliates and testate amoebae presented higher abundance values in
some of the months characterized by higher precipitation and in conditions of higher system productivity. Conclusion: we
may conclude that the Mandacaru stream, although strongly influenced by anthropic action, still presents an acceptable
water quality. Lastly, we emphasize that protists abundance was strongly influenced by system productivity. This was
evidenced by elevated protozoan densities where there was higher primary and bacterial productivity. Thus, these
organisms must be considered in studies that aim at the identification of organisms that may indicate anthropic impacts
and environmental quality.
Keywords: protist, plankton, water quality, testate amoebae, ciliates.

Estrutura e dinâmica da comunidade de protoplâncton em um córrego

urbano ambientalmente protegido

Resumo
O objetivo foi investigar, em escalas espacial e temporal, a abundância das comunidades de protozoários bem como os
fatores intervenientes na estruturação das mesmas em um córrego urbano. Métodos: Amostras de água para análise de
comunidades biológicas (amebas testáceas, ciliados e bactérias) e para análise de variáveis limnológicas foram tomadas
no córrego Mandacaru localizado na Unidade de Conservação do Parque do Cinquentenário, na cidade de Maringá,
Paraná State, Brasil, em dois períodos hidrológicos (seco e chuvoso). Calculamos o Índice de Qualidade de Água
(IQA), o Índice de Estado Trófico (ETI) para fósforo e utilizamos uma Análise de Redundância (RDA) para verificar
a influência de variáveis ambientais na comunidade de protozoários. Resultados: O IQA mostrou que a qualidade da
água foi considerada boa em alguns pontos e considerada ruim em outros pontos, e o ETI para o fósforo classificou
o córrego como mesotrófico na maioria dos locais amostrados (média entre 53,09 e 58,35). Foram identificados
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 Protoplankton in an urban stream

19 táxons de amebas testáceas, pertencentes a seis famílias, sendo Difflugiidae, Centropyxidae e Arcellidae as mais
especiosas, e 71 táxons de ciliados, distribuídos em 12 ordens, sendo Peniculida a ordem mais representativa, seguida
por Euplotida. De acordo com a análise RDA, amostras do período seco foram caracterizadas por maiores valores de
densidade bacteriana e concentrações de clorofila-a, fósforo total e nitrogênio total. As amebas testáceas e os ciliados
apresentaram valores de abundância maiores em alguns dos meses caracterizados por maior precipitação e em condições
de maior produtividade do sistema. Podemos concluir que o córrego Mandacaru, embora fortemente influenciado pela
ação antrópica, ainda apresenta uma qualidade de água aceitável. Por fim, enfatizamos que a abundância de protistas foi
fortemente influenciada pela produtividade do sistema. Isto foi evidenciado pelas elevadas densidades de protozoários
onde houve maior produtividade primária e bacteriana. Assim, esses protistas devem ser considerados em estudos que
visem à identificação de organismos que possam indicar impactos antrópicos e qualidade ambiental.
Palavras-chave: protozoários, plâncton, qualidade da água, amebas testáceas, ciliados.

1. Introduction initial levels of the trophic nets acting in matter and energy
transfer, these are fundamental organisms for the dynamics
City growth in the last decades has been responsible
of aquatic ecosystems (Fenchel, 1987; Rossi et al., 2016).
for increased pressure of anthropic activities on natural
Particularly, the small size, high metabolic rates,
resources (Lopes et al., 2015; Martínez-Fernández et al.,
and short life cycle allow the protists to respond rapidly
2019). Changes in habitat structure and in processes that
to changes in environmental characteristics (Xu et al.,
control patterns of composition, species diversity and
2002; Segovia et al., 2016). These organisms are good
abundance, including specific interactions, microclimate,
indicators of stream health (Dias et al., 2008; Segovia et al.,
and resource availability, are widely reported in scientific
2016). Studies on species richness of these organisms are
literature as recurrent phenomena in urban landscapes
practically non-existent due to difficulties still existent in
(Shochat et al., 2006).
the taxonomic identification of the species (Auer and Arndt,
Water quality in the planet has been intensely degraded
2001; Debastiani et al., 2016). According to Debastiani et al.
(Rebouças et al., 2002; Andrietti et al., 2016), generating
(2016), there are few studies on the longitudinal variation
loss of aquatic biodiversity due to physical and chemical
of protist species richness and density in urban streams.
restructuring of the environment and alteration of the natural
We aimed to investigate spatial and temporal scales,
dynamics of biological communities. Efforts to evaluate and
abundance, and factors that structure the communities
manage urban aquatic resources exist in scientific, political,
of protozoans in a tropical urban stream. Furthermore,
and social spheres (Alberti, 2009). Even if incipient, these
we characterized the limnology of this stream, providing
actions seek, through the development of research that
information on water quality through the evaluation of
contemplates quantitative and qualitative aspects of the
Indexes of Water Quality and Trophic State.
resources, to evaluate the integrity of these ecosystems
and subsidize management actions. Rapid urban growth
2. Material and Methods
together with previous anthropogenic impacts promote
environmental changes in small time lapses, reducing 2.1. Study area
the ability of ecosystems to keep the balance driven by Samples were taken in the Conservation Unit of Parque
the action of environmental factors combined in different do Cinquentenário (23° 22’ S; 51° 56’ W), in the city of
spatial scales (Moerke and Lamberti, 2006). Maringá, Paraná State, Brazil, which possesses an area
Recent studies describe the effects of urbanization on of 18.38 ha. The park comprises part of the medium and
urban streams, including hydrographic changes, increase low slopes of the Mandacaru stream, belonging to the
in nutrient and contaminant concentrations, and alterations Pirapó River watershed, comprising a larger area on its
in the morphology and stability of the canal (Paul and right margin and extending to the bottom of the stream
Meyer, 2001; Cunico et al., 2012; Harfuch et al., 2019). valley. On the left margin, the park comprises only the
To better understand the water quality of a river, physical, valley bottom (Figure 1). This stream suffers the impacts
chemical, and biological characteristics must be considered caused by domestic and industrial effluents, especially
(Lobo et al., 2004). in the Point 4.
Physical variables are mainly estimates of temperature, The park presents no eroded sites. However, erosion is
watercolor and turbidity. Chemical quality is measured present in its surroundings, due to the absence of riparian
by the identification, through specific methodologies, of forest. Anthropic action around the park is pronounced,
water components as concentrations of dissolved oxygen, with the presence of great quantity of construction debris
biochemical and chemical oxygen demands, pH, and and solid residuals (Paula and Ferreira, 2005).
conductivity.
Biological communities may be good indicators of the 2.2. Field sampling
influence of human expansion on the environment, and are Due to the stream extension, we established six
important for the evaluation of water quality (Munn et al., equidistant sampling points along the longitudinal axis
2002). Protoplankton is an aquatic community that represents of the stream, with approximately 100 meters between

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 Lippert, M.A.M. et al.

Figure 1. Parque Cinquentenário, anthropized forest fragment located in the city of Maringá, PR. The arrow indicates water
flow direction; the rectangle indicates the direct sewage discharge in the stream.

each point. Sampling was conducted bimonthly, between column. For the testate amoebae, we used a graduated
April 2012 and April 2013. We calculated precipitation bucket to filter 200 liters of water by sample with a
for each sampling period as the mean precipitation of the plankton net of 68 µm of mash opening. Bacteria samples
five days preceding the sample. The Main Climatologic were fixed with a solution composed of formaldehyde,
Station of Maringá provided rainfall data. alkaline lugol and thiosulfate (Sherr and Sherr, 1993).
We sampled ciliate (4 liters) and bacteria (100 mL) Testate amoebae were preserved in formaldehyde at 4%
passing a polyethylene flask at the subsurface of the water buffered with calcium carbonate. Ciliate samples were

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 Protoplankton in an urban stream

kept alive to avoid cellular deformations resulting from Effluents of any nature may only be discharged into the
the fixation process. inland or coastal waters, surface or underground, when
We used samples in sterile glass flasks kept under they meet the values stipulated by these decrees.
refrigeration to microbiological tests. We used the Concentrations of coliforms, COD, BOD, total
multiple‑tube method to determine thermotolerant coliforms phosphorous, total nitrogen, and total solids were determined
(APHA, 1985). by the Labsam laboratory – Laboratory of Environmental
We measured electric conductivity (S.cm-1), dissolved Quality, according to APHA (2006). Concentrations of
oxygen (mg.L-1), pH, depth, and water temperature (°C) in chlorophyll-a (µg.L-1) were determined by the Laboratory
the field, with portable devices. Water samples were taken of Basic Limnology of Nupelia/UEM, according to
through the immersion of polyethylene flasks 30 cm under Golterman et al. (1978).
the water surface. These samples were used to analyze the 2.4. Data analysis
following variables: Chemical Oxygen Demand (COD)
We summarized data from physical and chemical water
(mg.L-1), Biochemical Oxigen Demand (BOD) (mg.L-1),
variables as water temperature (ºC), dissolved oxygen
chlorophyll-a (µg.L-1), total phosphorous (mg.L-1), total
(mg.L-1), pH, electric conductivity (S.cm-1), turbidity
nitrogen (mg.L-1), turbidity (NTU), and total solids (mg.L-1). (NTU), phosphorous (mg.L-1), nitrogen (mg.L-1), total
2.3. Laboratory analyses solids (mg.L-1), Biochemical Oxygen Demand (mg.L-1),
and Chemical Oxygen Demand (mg.L-1) in an Analysis of
We stained samples with Rose Bengal and counted only
Principal Components (PCA). We used the Broken-Stick
the organisms that presented a colored protoplasm, assuming
criterion (Jackson, 1993) to select the significant PCA axes.
they were alive at the sampling moment. We withdrew
Before the analysis, variables were ln (x + 1) transformed,
six subsequent subsamples with a Hensen-Stempel pipete
except for pH. This analysis was realized in the software
of 2.5 mL and analyzed in Sedgwick-Rafter chamber to
PC-ORD, version 4.01 (McCune and Mefford, 1999).
make a quantitative analysis of samples. Individuals were
Calculation of the Water Quality Index (WQI), composed
withdrew from each sample and were assembled in slides by nine parameters of water quality (dissolved oxygen,
with glycerin for posterior identification. We analyzed thermotolerant coliforms, pH, BOD, water temperature,
all samples with an optic microscope (Olympus). For the total nitrogen, total phosphorous, turbidity, and total solids),
qualitative analysis, we assembled 10 slides to verify the was made according to the Formula 1 (ANA, 2004),
occurrence of new species in each sample. Taxonomic
n
identification of species was based on the following WQI = ∑ qi wi (1)
literature: Ogden and Hedley (1980), Velho et al. (1996), i =1
Velho and Lansac-Tôha (1996) and Lansac-Tôha et al.
(2008, 2014). Taxonomic framework of testate amoebae where: WQI = Water Quality Index, varying between
was based on that proposed by Adl et al. (2005). Thus, 0 and 100; qi = quality of the i-th parameter, varying
organisms were grouped in Arcellinida Kent, 1880 between 0 and 100, obtained from the respective quality
(Amoebozoa, Testacealobosia). graphic, in function of its concentration or measurement
Ciliate density was estimated in vivo in an optic microscope (result of the analysis); wi = weight correspondent to the
i-th parameter fixed in function of its importance for the
Olympus CX41, within six hours of sampling, in increases
global quality importance, that is, a number between 0 and 1,
of 100x and 400x. We counted 10 slides per sample, and
so that: being n the number of parameters considered in
expressed total density in individuals.L-1. Identification
the WQI calculation.
was based on specialized literature (Foissner and Berger,
WQI calculation required a normalization, where each
1996; Foissner et al., 1999). Taxonomic classification was
parameter was transformed in a scale between 0 and 100%,
performed according to Lynn (2008).
with 100% representing the best water quality. Then, we
To determine the density of bacterioplankton, we applied weights to each parameter according to their
filtered subsamples of 1 mL of water in a black filter importance (Table 1) (Pesce and Wunderlin, 2000).
Nucleopore/Watchman with 0.2 μm of pore opening stained with We classified water from each sampled point in
1 mL of DAPI fluorochrome (4.6-diamidin-2- phenylindole) the stream with WQI according to CETESB (2008)
at 0.1% during five minutes in the dark. We quantified in: Very good (WQI between 80 and 100), Good
bacteria in an increase of 1000x in epifluorescent microscope (WQI between 52 and 79), Regular (WQI between 37 and 51),
(Bjørnsen, 1986). Total density was expressed in cells.mL-1. Bad (WQI between 20 and 36), and Very bad (WQI
We determined thermotolerant coliforms according to between 0 and 19).
methods specified in “Standard Method for the Examination We also calculated the Trophic State Index for phosphorous
of Water and Wastewater”, edited by the “American Public – TSI (TP) (modified by Lamparelli, 2004), established for
Health Association” (APHA, 2006). Values obtained from lotic environments, according to the Equation 2:
the analysis were compared with values recommended by
the CONAMA Resolution 357/2005 (Article 34) (Brasil, ( ( ))
TSI (TP ) = 10x 6 − ( 0, 42 − 0, 36 x ( ln TP ) ) / ln 2 − 20 (2)
2005) and by the São Paulo State Decree Nº 8.468/1976
(Article 18), with the aim of verifying if the parameters are where: TP = total phosphorous concentration measured at
within patterns acceptable by the mentioned legislations. water surface, in mg.L-1; ln = natural logarithm.

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 Lippert, M.A.M. et al.

To interpret the results, sampled points were classified and biochemical oxygen demand), total chlorophyll, and
according to limits established to the different trophic bacterioplankton density. Biotic and abiotic data were
classes in rivers, according to Lamparelli (2004). previously logarithmized, except for pH. These analysis
Species composition was considered only for the were realized in software R, version 3.0.1 (R Core Team,
communities of testate amoebae and ciliates. Testate 2013), with the package vegan.
protozoans were grouped by Family and ciliates by Order.
We calculated frequency of occurrence of each species 3. Results
(Constancy Index) through the percentage of samples in
3.1. Pluviometric precipitation
which the species occurred, according to the expression:
c = n x 100/N, where n is the number of samples in which To evaluate mean precipitation during the study period
the species occurred and N is the total number of samples. we considered data obtained in the five days prior to
Species were classified as to occurrence in constant (present sampling date. Thus, We considered samples realized in
in more than 50% of samples), accessory (between 25% April, July, and December 2012 as dry period, and samples
and 50% of samples), and rare (occurring in less than 25% made in September 2012 and February and April 2013 as
of samples) (Dajoz, 1973). rain period (Figure 2).
Furthermore, we calculated species richness (for 3.2. Limnological variables
testate amoebae and ciliates) and mean density (for the Results of the Principal Component Analysis (PCA)
three protoplankton groups) for each sample point and evidenced a higher temporal than spatial segregation
hydrological period and compared density among groups. in sampling units. The first and second PCA axes were
To evidence statistical differences among richness and significant (p < 0.05). Thus, samples in the rainy period
density data, we realized variance analyses (ANOVA) with were negatively correlated to the first PCA axis, and were
the software Statistica 7.1 (Statsoft, 2005), considering as characterized by turbidity, COD, BOD, oxygen, and pH.
significant p values larger than 0.05. Samples in the dry period were positively correlated to
We characterized species dominance for testate amoebae this axis, presenting higher values of nitrogen, total solids,
and ciliates according to Lobo and Leighton (1986): conductivity, and temperature (Figure 3).
a) dominant species those that occurred in densities 3.3. Water Quality Index (WQI)
superior to 50% of total sample density; We evaluated water quality index (WQI) mainly as
b) abundant species those that occurred in densities acceptable during the entire study period in the majority
superior to mean sample density. of sampled points (mean between 37.79 and 50.73).
Water quality was considered good in some points
We used a Redundancy Analysis (RDA) to verify (mean between 58.17 and 66.51), and considered bad
the influence of environmental variables, bacteria, and in points 4 and 6 during the first and fourth sampling
chlorophyll in the protozoan community (testate amoebae campaigns (mean between 30.55 and 32.57).
and ciliates). This method combines Linear Regression Results obtained for each parameter composing WQI
and Principal Component Analysis (PCA), and is an are presented in Table 2.
extension of Regression Analysis to model multivariate 3.4. Trophic State Index (TSI)
data (Legendre and Legendre, 1998). For this, we used a
matrix with density values of the distinct protozoan groups We classified the trophic state of streams according
and a matrix with abiotic variables (water temperature, to CETESB, 2004 (Table 3). In most of the sampled
points the streams were considered mesotrophic (mean
pH, electric conductivity, dissolved oxygen, total
phosphorous, total nitrogen, chemical oxygen demand,

Table 1. Relative weight of each limnological variable used

in WQI calculation.
Relative
Variables
weight (wi)
Thermotolerant coliforms (TC) 0.16
Biochemical oxygen demand (BOD) 0.11
Total phosphorous (TP) 0.10
Total nitrogen (TN) 0.10
Dissolved oxygen (DO) 0.17
Potential Hydrogenion (pH) 0.11
Total solids (TS) 0.7
Turbidity (Turb) 0.08
Figure 2. Precipitation mean during the five days prior to
Water temperature (Temp) 0.10 each sampling date.

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 Protoplankton in an urban stream

Table 2. Minimum (Min), maximum (Max), and mean values of limnological variables used for the WQI calculation.
Rainy Dry
Variables Unit
Mean Min Max Mean Min Max
Water temperature °C 21.7 18.2 25 22.4 19.3 24.4
Dissolved oxygen mg.L-1 6.44 5.41 7.04 6.87 4.52 9.53
BOD mg.L-1 5.99 3.25 8.81 5.0 1.1 23.6
pH 6.88 4.75 7.4 6.75 5.15 8.36
Thermotolerant coliforms UFC.100mL-1 1.87 x 104 4 x 102 27 x 104 9.68 x 104 4 x 102 9 x 104
Total solids mg.L-1 199 164 234 347.4 138 628
Total nitrogen mg.L-1 3.02 2.09 3.6 5.13 2.96 11.35
Total phosphorous μg.L-1 0.05 0.01 0.1 0.25 0.02 1.2
Turbidity NTU 9.25 4.23 15.8 2.34 1 4.34

Table 3. Classification of trophic state used for lotic Although Difflugiidae is the family with most species,
environments. all taxa in this family were classified as rare by frequency of
Total phosphorous occurrence of each species (Constancy Index). Centropyxidae
Trophic state and Arcellidae were the only families that presented constant
(mg.m-3)
Ultraoligotrophic P ≤ 13 species in most of the sampled points, highlighting Arcella
discoides and Centropyxis aculeata (Table 4).
Oligotrophic 13 P ≤ 35
We identified 71 infrageneric taxa of ciliates, distributed
Mesotrophic 35 P ≤ 137 in 12 orders. Peniculida was the most representative order
Eutrophic 137 P ≤ 296 (19 taxa), followed by Euplotida (12 taxa). Among ciliates,
Supereutrophic 296 P ≤ 640 we did not identify any constant taxa, and most of them
Hypereutrophic 640 P were classified as rare. Only in Peniculida, Euplotida,
Source: CETESB (2004). Peritrichida, Pleurostomatida, Philasterida, and Haptorida
we registered accessory species (Table 4).
3.6. Species richness
Of the total protozoan richness (90 taxa), 71 were
ciliates and 19 testate amoebae (Figure 4; Table 4). Total
richness was higher in the rainy period. Ciliates presented
a higher number of taxa in both studied periods (dry and
rainy). However, ciliate richness was significantly higher
in the rainy period (F = 11.54; p = 0.001). Testate richness
presented no significant difference between periods
(F = 4.11; p = 0.0503).
Ciliate richness was, in general, proportionately
higher than testate richness in sampled points (Figure 5).
Considering each group, testate amoebae presented higher
richness in points 1, 3 and 5, and ciliates in points 1, 5, and 6
(Figure 5).
Figure 3. Dispersion of the scores of sampling points along Testate density was significantly higher in dry periods
the first two PCA axes (Turb: turbidity; COD = chemical (April, July, and December 2012) (F = 4.35; p = 0.04),
oxygen demand; BOD = biochemical oxygen demand; with higher values registered in April. The smallest density
Temp = temperature; Cond. = electric conductivity; was registered in February 2013, rainy period (Figure 6).
TSS = total solids; TN = total nitrogen; TP = total Considering sampling points, we observed the same
phosphorous; DO = dissolved oxygen). pattern as to the studied periods (higher values during
dry periods). Higher values were found in point 5, during
drought. In the rainy period, values were not higher than
between 53.09 and 58.35). During the second sampling, 200 ind.m-3, except in point 3 (Figure 7).
two points were classified as eutrophic (points 1 and 6) Contrary to the observed for testate amoebae, higher
with values varying between 59.96 and 60.61. Moreover, ciliate density was observed during the rainy season,
point 4 was considered supereutrophic during the fourth especially in the third campaign (Figure 8). This difference
sampling (64.05) and as hipereutrophic in the second in ciliate density between periods was considered significant
sampling (70.76). (F = 8.7; p = 0.005).
There was a representative difference in ciliate density
3.5. Species composition
during the rainy period in comparison with the dry period,
We identified 19 taxa of testate amoebae, belonging to six when evaluating the distribution of this attribute among
families, being Difflugiidae (six taxa), Centropyxidae (five sampling points (Figure  9). The dry period was kept
taxa), and Arcellidae (four taxa) those with more species. uniform and with lower densities in the sampling points.

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 Lippert, M.A.M. et al.

Table 4. List of testate amoebae species (grouped by family) and ciliate species (grouped by order) and frequencies of
occurrence in each sampling point, according to the Dajoz index (xxx = constant; xx = accessory; x = rare) and according to
the dominance index (light grey = abundant; dark grey = dominant).
SAMPLING POINTS
TESTATE AMOEBAE
1 2 3 4 5 6
ARCELLIDAE Ehrenberg, 1830
Arcella discoides Ehrenberg, 1843 xxx xx xxx xx xxx xxx
Arcella hemisphaerica Perty, 1852 xx x x xx xx x
Arcella megastoma Pénard, 1902 xx x - - xx -
Arcella vulgaris Ehrenberg, 1830 x - x - x x
CENTROPYXIDAE Deflandre, 1953
Centropyxis aculeata (Ehrenberg, 1838) xxx xxx xxx xxx xxx xxx
Centropyxis constricta (Ehrenberg, 1838) x - x - - -
Centropyxis discoides (Pénard, 1890) xxx xx xxx xx - xx
Centropyxis ecornis (Ehrenberg, 1841) xx xxx xxx xx xx xx
Centropyxis hirsuta Deflandre, 1929 xx x xx x xx -
DIFLLUGIIDAE Awerintzew, 1906
Mediolus corona (Wallich, 1854) - x - - - -
Difflugia gramen Pénard, 1902 - - x - - -
Difflugia lithophila Pénard, 1902 - - - - x -
Difflugia lobostoma Leidy, 1879 - - x - - -
Difflugia oblonga Ehrenberg, 1838 - x - - - -
Difflugia stellastoma Vucetich, 1989 - x - - - -
TRIGONOPYXIDAE Loeblich and Tappan, 1964
Cyclopyxis impressa (Daday, 1905) - - x - - -
Cyclopyxis kahli Deflandre, 1929 x xx xx xx xx -
LESQUEREUSIIDAE Jung, 1942
Lesquereusia spirallis (Ehrenberg, 1840) x - - - - -
PLAGIOPYXIDAE Bonnet & Thomas 1960
Plagiopyxis callida Pénard, 1910 - - x - - -
SAMPLING POINTS
CILIATES
1 2 3 4 5 6
COLPODIDA
Colpoda magna Gruber, 1880 - x - - x x
Colpoda steinii Maupas, 1883 - x - - - -
Colpoda sp. - x x - - -
Cyrtolophosis mucicola Stokes, 1885 - - - - - x
CHLAMYDODONTIDA
Chilodonella uncinata (Ehrenberg, 1838) - - - x - -
Trithigmostoma sp. - - - x - x
HETEROTRICHIDA
Blepharisma sp. - - - x x x
Stentor sp. - - x - x -
PENICULIDA
Colpidium colpoda Gannerr & Foissner, 1989 - x - x - -
Dexiotricha granulosa Foissner, Berger & Kohmann, 1994 - - - x - -
Disematostoma tetraedricum Kalh, 1931 - - - x - -
Disematostoma sp. - - - - x -
Epenardia myriophylli Corliss, 1971 x x - - x -
Frontonia leucas Ehrenberg, 1838 x - - - - -
Glaucoma reniforme (Schewiakoff, 1892) x x x x x -
Glaucoma scintillans (Ehrenberg, 1830) - - xx x - -
Glaucoma sp. - - - - - x
Lembadium bullinum (Perty, 1852) - - x - - x

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 Protoplankton in an urban stream

Table 4. Continued...
SAMPLING POINTS
CILIATES
1 2 3 4 5 6
Lembadium lucens (Maskell, 1887) x - - - - x
Ophyryoglena sp. - x - - - -
Paramecium aurelia complex. x x - x x x
Paramecium bursaria (Ehrenberg, 1831) x - x x - x
Paramecium caudatum Ehrenberg, 1834 - x x - x x
Stokesia vernalis Wenrich, 1929 - - x - x -
Tetrahymena pyriformis (Ehrenberg, 1830) x xx xx - x x
Tetrahymena sp. - - x x - -
Urocentrum turbo (Mueller, 1786) xx - x x xx x
EUPLOTIDA
Aspidisca cicada (Mueller, 1786) - xx x - x xx
Aspidisca lynceus (Mueller, 1773) x x xx - x -
Euplotes aediculatus Pierson, 1943 - xx xx x - x
Euplotes eurystomus (Wrzesniowski, 1870) - xx - x xx xx
Euplotes moebiusi Kahl, 1932 x - - - - x
Hypotrichida sp. - - - xx - x
Hypotrichium sp. - - x - - x
Holosticha sp. - - - - - x
Oxytricha saprobia Kahl, 1932 x - - - - -
Oxytricha similis Engelmann, 1862 x - - - - -
Oxytricha sp. x - - x x -
Stichotricha secunda Perty, 1849 - - x - - -
OLIGOTRICHIDA
Halteria grandinella (Mueller, 1773) x x - - x x
Limnostrombidium sp. x x x x - -
PERITRICHIDA
Carchesium polypinum Linnaeus, 1758 - x - - - x
Epistyllis hentcheli Kahl, 1935 - x - - - -
Epistyllis sp. xx - - - xx x

Vorticella aquadulcis complex xx x x x xx xx

Vorticella campanula Ehrenberg, 1831 - xx x x xx x
Vorticella convallaria complex xx - - xx xx x
Vorticella mayeri Faure-Fremiet, 1920 - x x - - -
Vorticella sp. - - x x - -
PLEUROSTOMATIDA
Acineria uncinata Tucolesco, 1962 - - - x x -
Amphileptus pleurosigma (Stokes, 1884) - x - - - xx
Amphileptus procerus (Penard, 1922) x - x - - -
Litonotus alpestris Foissner, 1978 x - - - x x
Litonotus crystallinus (Vuxanovici, 1960) - x - - x -
Litonotus lamella (Mueller, 1773) x - - - - -
PRORODONTIDA
Balaniom planctonicum (Foissner et al., 1990) - - x - - -
Coleps spetai Foissner, 1984 - - x - - -
Holophrya discolor Ehrenberg, 1833 - - - - x -
PHILASTERIDA
Cinetochilum margaritaceum (Ehrenberg, 1831) xx x xx - x xx
Cyclidium glaucoma Mueller, 1773 xx xx xx xx x x
Cyclidium SP x - - x xx x

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 Lippert, M.A.M. et al.

Table 4. Continued...
SAMPLING POINTS
CILIATES
1 2 3 4 5 6
Dexiotrichides centralis (Stokes, 1885) x - - - - -
Sathophilus muscorum (Kahl, 1931) x - - - - -
SUCTORIDA
Podaphyra sp. - - - - x -
HAPTORIDA
Balantidium pellucidum Eberhard, 1862 - - - - x x
Campanella sp. x x - - - -
Cyclotrichium viride Gajewskaja, 1933 - - - - x -
Dexiostoma campylum (Stokes, 1885) x - x - x x
Philasterides armatus Kahl, 1931 - - x - x xx
Monodinium balbiani Fabre-Domergue, 1888 - - x - x xx
Platynematum sociale (Penard, 1922) - - - - - x

Figure 4. Total species richness estimated for testate Figure 6. Mean and standard error of testate amoebae
amoebae and ciliates in sampled points during dry and rainy density in different hydrological periods.
periods.

Figure 5. Average of the species richness of testate amoebae Figure 7. Mean and standard error of testate density in each
and ciliates in sampling sites. hydrological period and sampling point.

3.7. Species dominance For ciliates, we registered no dominant species. However,

For testate amoebae, Arcella discoides was considered many taxa were classified as abundant, highlighting species
abundant in all sampling points, and Centropyxis aculeata of orders Peritrichida, especially Vorticella aquadulcis
was classified as dominant in points 2 and 3 and abundant and V. convalaria, and Philasterida, especially Cyclidium
in all the other points (Table 4). glaucoma (Table 4).

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 Protoplankton in an urban stream

3.8. Effect of environmental heterogeneity on protozoan

communities
According to the RDA, environmental variables
explained 41% of variability in abundance data of the three
protozoan groups, and an ANOVA evidenced significance
in both axes (axis 1 = 0.005; axis 2 = 0.04).
Results of the RDA showed, in general, the same
pattern of distribution of the sampling units as described
in the PCA. Thus, we observed also in this analysis a
higher temporal (between hydrological periods) than
spatial segregation (among sampling points) (Figure 10).
According to this analysis, samples of the dry period
were characterized by higher values of bacteria density
and concentrations of total phosphorous, and total nitrogen
Figure 8. Mean and standard error of ciliate density in (Figure 10). On the other hand, ciliates presented higher
different hydrological periods. abundance values in some of the months characterized
by higher precipitation and where higher values of BOD
and COD were found (Figure 10). Testate amoebae also
presented higher abundances in conditions of higher system
productivity (higher nutrient concentration, bacteria,
BOD, and COD), although higher density values were
not observed in the rainy season (Figure 10).

4. Discussion
4.1. Limnological variables, WQI and TSI
According to parameters established by CETESB
(2008), WQI results must be interpreted in relation to
the individual behavior of each of the parameters that
compose it. This is important especially when one or
more of them is distorting the WQI results, due to their
concentration and dynamics in the water body. This index
Figure 9. Mean and standard error of ciliate density in each may mask relevant information on the parameters due to
hydrological period and sampling point. its reductionist character. This evaluation is important,
as it allows a more realistic diagnostic of water quality.
The huge amount of waste that is generated in cities can
reach streams and rivers when carried by rainwater and
thus carry large amounts of inorganic and dissolved organic
matter, which can make the water unsuitable for direct
and indirect use (Ntengwe, 2006; Harfuch et al., 2019).
A large part of the obtained BOD values surpass the
limit of 5 mg.L-1 established by the CONAMA resolution
357/05 (Brasil, 2005) for class 2 freshwater. The mean
varied between 5.23 and 23.6 mg.L-1, with higher values
found in points located near wastewater discharge made
directly in the stream. The increase in BOD in water bodies
may be a consequence of sewage discharge, which causes
an increase in organic matter and, consequently, decrease
dissolved oxygen through oxidation (CETESB, 2009).
The discharge of organic matter into the stream is
generally higher in rainy periods, due to leakage. Although
Figure 10. Ordination diagram for the first two axes
in these periods there is also a higher dilution of organic
of the Redundancy Analysis, with scores of the stream
according to abiotic variables (Cond = electric conductivity;
matter due to larger water volume, the organic matter
Temp = temperature; Turb = turbidity; DO = dissolved discharge results in BOD increase. Accordingly, our
oxygen; TN = Total Nitrogen; TP = Total Phosphorous; PCA indicated a positive correlation between BOD and
BOD = Biochemical Oxygen Demand; COD = Chemical the rainy period.
Oxygen Demand), biotic (Bact = bacterioplankton), and For turbidity, there was no difference between sampled
protozoan (TA = testate amoebae; CIL = ciliates). points, and all of them were in accordance to the CONAMA

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 Lippert, M.A.M. et al.

resolution (Brasil, 2005) that establishes 100 UNT as the arrival and transport of matter from acid soils adjacent
maximum limit to type 2 freshwater. However, we highlight to the water bodies (Marotta et al., 2008).
that the higher values were obtained in the rainy period, The minimum limit of dissolved oxygen according
as evidenced by the positive correlation between turbidity to Brasil (2005) is of 5 mg.L-1. At the Mandacaru stream,
and this hydrological period. Othes studies also have concentrations were in general above this limit, with the
pointed that turbidity tends to increase when there is flow value 4.52 mg.L-1 in only one sampling unit. Reduction in
increase (Fritzsons et al., 2003; Harfuch et al., 2019). With dissolved oxygen is one of the indicators of water pollution,
precipitation, erosion and leaching become common around due to its consumption by the decomposition of organic
rivers and streams, favoring the dispersion of suspended compounds (CETESB, 2010).
particles in the water. The chlorophyll-a limit established by the resolution
The maximum value of total solids is of 500 mg.L-1 is of 30 μg.L-1 (Brasil, 2005), with values above this limit
according to the CONAMA resolution (Brasil, 2005). indicating eutrophication of the aquatic system. At the
Most of our sampled points presented values lower than Mandacaru stream, all values were below this limit.
this limit, except for the first sample, in which we verified We  highlight that, in lotic environments, flow velocity
values ranging from 503 to 628 mg.L-1. The quantity of constitutes a limiting factor to the development of typical
total solids in rivers, lakes, and streams indicates their planktonic populations, resulting in low primary productivity
degree of pollution so that the higher the concentration, and, consequently, in low chlorophyll concentrations
the higher is the pollution (Almeida and Schwarzbold, (Reynolds and Descy, 1996).
2003). Total solids may be from natural sources, sewage A limit of 1,000 thermotolerant coliforms.100 mL-1 of water
discharges, urban outlets or industrial waste discharges is allowed according to Brasil (2005). At the Mandacaru stream,
(Ntengwe, 2006). this limit was surpassed in almost all sampled points, with
The highest value of total phosphorous allowed by values varying between 1,500 and 270,000 coliforms.100 mL-1
the resolution to lotic environments is of 0.1 mg.L-1 in the rainy period and dry period, respectively. In only
(Brasil, 2005). At the Mandacaru stream, concentration one sample the values were below the established limit
of this variable in general surpasses this limit, with means (between 400 and 800 coliforms.100 mL-1 of water).
ranging from 0.1 to 1.2 mg.L-1. We found the highest These results differ from those obtained in streams of the
value of phosphorous at the point where there is sewage Pirapó River basin, Paraná State (Harfuch et al., 2019).
discharge at the stream (point 4 during the dry period). The presence of thermotolerant coliform bacteria is an
In  turn, Harfuch et al. (2019) in studies carried out in indicator of pollution by sanitary wastewater and animal
other streams of the Pirapó River basin, Paraná State, did waste (CETESB, 2010).
not find values of this variable above that stipulated by There was practically no variation in temperature
the resolution of Brasil (2005). between sampled points in the studied period. This is
Phosphorous is considered the main responsible for probably because all samples were taken during the
eutrophication in aquatic ecosystems (Sperling, 2007). morning period.
Naturally, it comes from rocks, decomposition and superficial The TSI was developed for reservoirs, but has been
rainwater leakage. Artificially, it comes from particles in applied to rivers. It is however necessary to make a critical
the atmosphere, fertilizers, and domestic and industrial review of its application in lotic systems (Lamparelli, 2004).
wastewater (Wetzel, 2001). According to Lamparelli This same author, when comparing TSI classifications
(2004), mean nutrient concentrations, especially total obtained through phosphorous with chlorophyll-a values,
phosphorous, are higher in lotic than in lentic systems. verified great inconsistency between them when applying
The highest total nitrogen value allowed by Brasil this index in lotic systems.
(2005) in class 2 waters is 10 mg.L-1. However, nitrate Contrary to what is frequently registered for reservoirs,
concentrations above 5 mg.L-1 indicate inadequate sanitary trophy classifications in rivers were little coherent in São
conditions. A value surpassing this limits was observed Paulo State, using the conjugated index that includes total
only at the point were there is sewage direct discharge at phosphorous and chlorophyll-a (Lamparelli, 2004). Thus,
the stream (Point 4 in the dry period). in rivers, where chlorophyll concentration is generally low
One of the established criteria for water potability (Reynolds and Descy, 1996), using indexes that include this
is pH. According to the resolution (Brasil, 2005), pH variable seems little efficient. For this reason, we decided
values may vary between 6.0 and 9.0. In our study, most not to include this variable in the TSI calculations in this
of the pH values were within the established limits. Only study. On the other hand, in urban lotic systems, subjected
in some periods, at the points influenced by sewage to anthropic action, phosphorous concentrations tend to
discharge, we registered values under 6.0. pH may be be high (Lamparelli, 2004).
influenced by organic matter quantity in the water. In acid The mesotrophic conditions tending to eutrophy/hypertrophy
organic compounds and at the decomposition of organic found in the Mandacaru stream have been found in other
matter, there is carbon dioxide liberation, which makes lotic systems (Zanini et al., 2010). This increase in trophy
the water acid (Marotta et al., 2008). Similar results were verified in some sampling points and periods may be due
found in streams of the Pirapó River basin, Paraná State to the discharge of domestic wastewater directly into the
(Harfuch et al., 2019). Low pH values are often related to stream.

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 Protoplankton in an urban stream

4.2. Composition and richness of testate amoebae and frequently found at the pelagic zone of aquatic systems
ciliates (Velho et al., 2013).
The most representative families of testate amoebae Studies on ciliate species richness in lotic systems
in this study, Difflugiidae, Centropyxidae, and Arcellidae, have shown a variation from 20 to 200 registered species
are also the most representative in other studies realized in (Madoni, 2005; Madoni and Braghiroli, 2007; Dias et al.,
Brazilian freshwater systems (Lansac-Tôha et al., 2007, 2008; Debastiani et al., 2016). Thus, species richness in
2008, 2014; Alves et al., 2012; Mansano et al., 2013, our study (71 taxa) may be considered as relatively high,
among others). as samples were taken in only one stream. A study realized
However, there are few studies with these protozoans in only one urban stream at southeast Brazil identified
in urban streams. Among these, we highlight the one 22  taxa (Dias et al., 2008).
developed in the region northwest of the State of São Although no ciliate species have been identified as
Paulo, where 21 taxa have been identified (Fulone et al., constant, some of them were considered accessories,
2005). These authors attributed the low species number from which we highlight Cinetochilum margaritaceum
to the eutrophication process in the studied streams. and Cyclidium glaucoma, who have been registered as
Lippert (2013) realized a taxonomic survey, description, frequent and abundant taxa in many rivers and streams
and illustration of testate protozoans in three anthropized (Madoni and Braghiroli, 2007; Bagatini et al., 2013;
first order streams in the State of Paraná. In this study, Segovia et al., 2016). These species, belonging to the
22 taxa were identified, and the author concluded that the order Philasterida, are registered mainly in mesotrophic
low species richness was associated to negative impacts and eutrophic environments (Beaver and Crisman, 1989),
of anthropic intervention on this community. Thus, the which are the predominant conditions of the Mandacaru
small number of species in the Mandacaru stream (19 taxa) stream. On the other hand, some groups as Oligotrichida
corroborates with results of the authors cited above. This present low species richness in the studied stream, which
evidences the anthropic effect on these urban ecosystems, may be associated to the fact that species from this order
considering the sampling points presented, in general, TSI are mainly found in oligotrophic environments and are
varying between mesotrophic and hipereutrophic. adapted to the plankton habit (Beaver and Crisman, 1989).
Many studies realized in freshwater environments have The larger species richness of ciliates and testate
registered a close association between testate amoebae amoebae found in the rainy periods may be due to the
and aquatic macrophytes (Alves et al., 2012). Thus, the carriage of species from the benthonic compartment and
absence of these plants may also explain the low species littoral region to the water column, due to increase in
richness in the stream. water flow caused by rains (Lampert and Sommer, 2007).
According to Margalef (1963), systems with strong In this sense, the water column may act as a collector of
environmental fluctuations remain in a low maturity state. protozoa from all the stream compartments, mainly those
In these systems, species with higher potential growth small and shallow (Velho et al., 2013; Lansac-Tôha et al.,
rates become frequent, reducing diversity and hindering 2014). Similar results have been found by Fulone et al.
an efficient mechanism of ecosystem homeostasis. (2005) in streams from the southeast region of Brazil.
According to this tendency, the evaluated stream presented,
4.3. Density of testate amoebae and ciliates
as highlighted above, a low specific richness of testate
amoebae, with an elevated representativeness of only Among testate amoebae, Arcella discoides (Arcellidae)
three species, who were constant in almost all sampled and Centropyxis aculeata (Centropyxidae) were the only
points. Thus, Centropyxis aculeate, C. ecornis, and Arcella species abundant in all sampled points. Centropyxis
discoides, evidenced in this study, are among those with aculeata, besides being abundant, was the only dominating
larger geographic distribution in Brazil. They have been species. The family Centropyxidae contains opportunistic
registered in different freshwater systems, in samplings species found in impacted fluvial systems (Patterson and
of plankton, sediment, and macrophyte associated fauna Kumar, 2000). According to Patterson and Kumar, (2000),
(Velho et al., 2003; Lansac-Tôha et al., 2014). C. aculeata tolerates environments contaminated by industrial
According to Velho et al. (2003), the occurrence of effluents. In one of our sampled points where this species
testate amoebae is associated to the shape of their theca. is dominant (P3), there is direct discharge of domestic
Thus, the above-mentioned taxa are well distributed in wastewater. The  numeric dominance of this species among
the Mandacaru stream probably due to their flattened testate amoebae has also been verified in other aquatic
shape, common in most Arcellidae and Centropyxidae systems in Brazil (Lippert, 2013; Lansac‑Tôha et al.,
taxa. The flattened theca brings adaptive advantages to the 2014, among others).
organisms that inhabit lotic environments, as this shape Various studies have evidenced that the presence of
makes individuals less susceptible to carriage by water flow. disturbances and the dominance of tolerant species to the
Among ciliates, the orders with higher species richness detriment of more sensible species markedly change the
in our study (Peniculida, Euplotida, and Peritrichida) have structure and distribution of fish fauna (Jackson et al., 2001).
been registered as representative in rivers and streams Cunico et al. (2012) evidenced that environmental changes
(Madoni and Braghiroli, 2007). Species in these orders related to pollutants have influenced fish assemblage in
are considered, in general, as interstitial benthonic, but are urban streams, including the Mandacaru. These authors

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 Lippert, M.A.M. et al.

verified that variation on the fish community structure Berger, 1996; Segovia et al., 2016). The high abundance
was related to the entrance of organic nutrients in these of bacterivore ciliates seems to be widespread among
environments. We emphasize that these urban streams streams (Segovia et al., 2016).
present an elevated pollution degree due to urban occupation Moreover, many studies have demonstrated the
(allotments and industries) and to the reception of diverse effect of organic pollution on trophic relationships, as
effluents as non-treated domestic sewage. Such conditions in ciliate protozoan communities in freshwater systems
may explain the fact that only one testate species was (Primc-Habdija et al., 1998; Madoni, 2005; Madoni and
dominant in the Mandacaru stream. Braghiroli, 2007; Segovia et al., 2016). Thus, studies show
The family Difflugiidae presented the highest number a dominance of bacterivore ciliates with increasing organic
of species among testate amoebae, but was not abundant load (Madoni and Braghiroli, 2007; Segovia et al., 2016).
in our study. This family is the most diversified among Organic pollutants provoke an increase in phosphate and
testate amoebae (Lansac-Tôha et al., 2014), presenting other nutrients, altering the structure of bacteria communities,
a high variety of shapes. However, its predominantly inducing changes in the protists, which have bacteria as
globed or elongated shape limits the development of one of their main food sources (Pace, 1982). Therefore,
large populations in systems with elevated flow velocity elevated values of phosphorous and other nutrients may
(Velho et al., 2003). promote a higher availability of resources for ciliates.
No ciliate species was considered dominant in the In  this sense, ciliate and testate amoebae abundances
different sampled points of the stream. However, species were, in general, associated to larger values of BOD and
in some Orders, especially Peniculida and Peritrichida, COD, suggesting a positive relationship between organic
presented abundant species. These ciliate groups have pollution and protozoan abundance.
been frequently registered as abundant in lotic systems
(Kiss et al., 2009). 5. Conclusion
The higher ciliate densities found in the rainy period
From the results obtained in this study, we may conclude
diverge from results of other studies that found higher
that the Mandacaru stream, although strongly influenced
densities of these protozoans in the dry period (Velho et al.,
by anthropic action due to its location at the metropolitan
2005, 2013) due to the dilution effect on these individuals
region of a medium sized city, still presents an acceptable
during the rainy period. The pluvial regime, mainly in
water quality, according to WQI. Furthermore, the TSI
lotic systems, is an important factor that changes ciliate
evidenced the prevalence of mesotrophic conditions in
protists abundances, as demonstrated in other studies
most of the sampled points and periods.
(Primc-Habdija et al., 1998). The ciliate community was
Lastly, we emphasize that protists abundance was
composed in great part of species not truly planktonic in
strongly influenced by system productivity. This was
both hydrological periods. Thus, it is likely that, in the
evidenced by elevated protozoan densities where there
rainy period, a great quantity of individuals from species
was higher primary and bacterial productivity. Thus, these
that inhabit the sediment and littoral vegetation, and even
organisms must be considered in studies that aim at the
the inundated soil, is carried to the water column. In this
identification of organisms that may indicate anthropic
sense, some non-planktonic species as Vorticella aquadulcis,
impacts and environmental quality.
Cyclidium glaucoma, V. convallaria, Glaucoma reniformis,
and Cinetochilum margaritaceum reached their higher
densities in the rainy period. Acknowledgements

4.4. Effect of environmental heterogeneity on protozoan We would like to thank Nupélia/PEA/PGB/UEM for
communities logistical support. We would like to thank CAPES and
We found higher abundance values of both protozoan CNPq for fellowships. We also thank Geziele Mucio
groups related to system productivity. This was shown Alves, Leilane Schwind, Diogo Castanho Amaral, Maria
by larger abundance values associated to sample units do Carmo Roberto, Carlos Eduardo Aguiar Soares and
with elevated nutrient concentrations and higher primary Lisiane Hoff for their assistance in field surveys, biological
(chlorophyll) and bacterial productivity, as evidenced by material analyzes and laboratory procedures as well as for
the RDA. valuable suggestions.
Food availability is an important abiotic factor
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