Environmental variables likely influence the periphytic diatom community in a subtropical lotic environment

Journal Pre-proof Environmental variables likely influence the periphytic diatom community in a subtropical lotic environment Gabriela Medeiros, Andre´ Andrian Padial, Mailor Wellinton Wedig Amaral, Thelma Alvim Veiga Ludwig, Norma Catarina Bueno

PII:

S0075-9511(18)30140-3

DOI:

https://doi.org/10.1016/j.limno.2019.125718

Reference:

LIMNO 125718

To appear in:

Limnologica

Received Date:

11 August 2018

Revised Date:

9 July 2019

Accepted Date:

9 July 2019

Please cite this article as: Medeiros G, Andrian Padial A, Wedig Amaral MW, Ludwig TAV, Bueno NC, Environmental variables likely influence the periphytic diatom community in a subtropical lotic environment, Limnologica (2019), doi: https://doi.org/10.1016/j.limno.2019.125718

This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier.

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Environmental variables likely influence the periphytic diatom community in a subtropical lotic environment Gabriela Medeiros*a, André Andrian Padialb, Mailor Wellinton Wedig Amaralc, Thelma Alvim Veiga Ludwigd, Norma Catarina Buenoe *ace

Universidade Estadual do Oeste do Paraná, Centro de Ciências Biológicas e Saúde, Rua Universitária, 2019, Jardim Universitário, 85819-110, Cascavel, Paraná, Brasil bd Universidade Federal do Paraná, UFPR, Departamento de Botânica, Setor de Ciências Biológicas, C. Postal 19031, CEP 81531-990, Curitiba, PR, Brasil * corresponding autor

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E-mail adresses: a [email protected] ; b [email protected] ; c [email protected] d [email protected] ; e [email protected] All authors have contributed substantially to this work

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Abstract – We evaluated the response of diatom community relative to environmental changes with the aim of characterizing and comparing, along a linear gradient, three environments across the Cascavel River microbasin with distinct land-uses. In June 2016, 10 substrates were collected for periphyton extraction in locations with different land-uses (conservation, urban, and agriculture respectively). One-hundred and nine infrageneric taxa and 30 genera were found. Eunotia and Gomphonema presented elevated and representative taxa richness at all stations, with totals of 14 and 11 respectively. Pinnularia and Navicula (12 and 8 taxa respectively) were significant indicators at the more upstream points; while Encyonema, Achnanthidium and Navicula (5, 5, and 6 taxa respectively) occurred primarily downstream. The sampling stations were quite distinct in their densities, species richness, and physical, chemical, and biological characteristics. The tests showed a significant difference among the stations based on the species abundance matrix. Upstream points, within the conservation area, revealed high Eunotia density, high nitrate concentrations and low pH. The urbanized area was characterized by greater exposure to light associated with elevated electrical conductivity and high ammoniacal nitrogen concentration, favoring the cosmopolitan species development such as Gomphonema lagenula, Gomphonema exilissimum and Fragilaria gracilis. The agricultural area exhibited elevated flow, a factor limiting the colonization of species and favoring the development of Achnanthidium and Fragilaria species. The distribution of the community across the microbasin were related to flow, dissolved oxygen, electrical conductivity, nitrate, ammonia, and total coliforms, confirming the distinctiveness among the environments. Except for spatial autocorrelation, there wasn’t a single environmental filtering explanation for the diatom community variation. The abiotic variables differentiated the environment in conjunction with the spatial variation. Along the river, physical characteristics such as depth, water volume, flow, solar incidence, concentration of solids, and temperature varied, directly interfer with the periphytic community’s primary production. Keywords: Bacillariophyceae, land-uses impact, environmental gradient, spatial structure.

2 1.

Introduction Lotic systems experience various changes from headwater to mouth (Vannote et al.,

1980) such as in water speed, depth, and light availability (Wetzel, 2001). Going downstream, the riverbed usually expand, allowing for a greater incidence of sunlight on its substrate, temperature elevation, and increases in periphytic algae and other primary products (Vannote et al., 1980; Huston, 1999). Diversity studies in lotic environments with distinct anthropogenic impacts along their courses can reveal, based on the continuous river theory, how the naturally expected alterations can be influenced by the impacts. Simultaneous variations in factors, such as nutrient concentrations indicate that changes in the composition of the landscape may impact

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the waters biogeochemistry (Krusche et al., 2005). In general, agricultural activities increase the transport of contaminants, such as total coliforms, to the riverbed (Gonçalves et al., 2005). Sliva and Williams (2001) found that

urban land use also positively influences the concentration of coliforms, suggesting that soil

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occupation in urban regions constitutes a substantial predictor of water quality. Furthermore, strong correlations between pollution-indication diatoms and total coliforms were verified by

contamination of water resources.

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Dere et al. (2006), highlighting the agricultural use of the soil as a contributor to the

Among the periphytic communities, diatoms (Bacillariophyta) represent a significant

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portion, possessing adaptations which favor substrate attachment (Wehr and Sheath, 2003). Various negative effects on aquatic ecosystems due to accelerated nutrient enrichment stemming from urbanization or from large agricultural areas can be reflected in the

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distribution of diatoms (Jeppesen et al., 2000; Davidson and Jeppesen, 2013). Studies that involve diatom ecology in lotic environments, including the factors

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controlling their distribution, are common in temperate regions, for example in China (Dong et al., 2016; Liu et al., 2016) and France (Bottin et al., 2014; Jamoneau et al., 2018), and boreal regions, in Finland (Soininen and Weckström, 2009; Virtanen and Soininen, 2012,

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2016). In Brazil we can cite some studies that evaluate controlling factors for the composition, distribution, and abundance of diatoms. Raupp et al. (2009) analyzed the variation in the phytoplanktonic diatom community relative to inundation pulses in Cutiuaú Lake, Manaus, in flood plain environments. Wetzel et al. (2012), in the same hydrographic basin (Negro River, Amazon basin), evaluated the change in the community relative to geographic distance, comparing the distance-decay relationships between taxa with similar ecological requirements, but with different forms of growth. Burliga et al. (2014), in Itajaí-Mirim River

3 (southern Brazil), studied altitude as the driver for dispersion for the periphytic diatom community. Zorzal-Almeida et al. (2017) investigated the main factors controlling the biodiversity and distribution of planktonic diatoms and surface sediment in connected dams of different trophic states, focusing on the Piracicaba River basin and the Cantareira System. Studies in subtropical lotic environments including controlling factors for diatom distribution are still incipient. The present work seeks to characterize and compare three lotic environments with distinct landscapes and physical characteristics along the Cascavel River microbasin by surveying the periphytic diatoms and by characterizing the environment. The following hypotheses were tested: a) the periphytic diatom assembly composition is correlated to landscape factors; b) there is observational evidence for selection of adapted

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species due to environmental changes in the river water caused by urbanization.

Material and methods

2.1. Study area

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The municipality of Cascavel (24º57’21'’ S, 53º27’19'’ W) is located in western

Paraná, a subtropical region with an average annual temperature of 21 °C (Alvares et al.,

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2013). Most of the headwaters of the Cascavel River (24º 32’, 25º 17’ S and 53º 05’, 53º 50’ W) are within the urban perimeter and the main channel of the river presents in its

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development a 17.5 km extension (FUNDETEC, 1995). According to Cembranel et al. (2017) land use in the Cascavel River drainage region consists of urban areas (33.84%), where the main river headsprings are located, as well as agricultural areas (36.84%) and forest and

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reservoirs (29.34%). 2.2. Sample design

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The collection of biological material was done in June 2016. The sampled period presented an average minimum temperature of 9 °C and average maximum of 19 °C and

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average precipitation of 1.67 mm. During the 15 days before the collection there was no precipitation, the average humidity was 79.14%, average windspeed was 3.47 m/s (daily data furnished by the Paraná Meteorological System (SIMEPAR). The sampling period was chosen for its low precipitation, making it easier to evaluate the sampling stations without interference from non-local pollutants. Three sampling stations were selected along the microbasin of the Cascavel River (Fig. 1):

4  Station 1: located in a conservation district within the urban are, close to the border with the Paulo Gorski Ecological Park. The park features 111.26 ha of native forest and 38 ha of water surface with approximately 4,060,000 m3 of water volume (Cembranel et al., 2017). The land use is divided into urban area (76%) and preservation area (24%) (see more in Remor et al., 2018). A stretch with characteristics of a stream (presence of many stones and reduced depth). Average depth of 0.06 m, average width of 3.6 m, and average flow of 0.12 m3 s-1.  Station 2: located in the urban area, lacking ciliary vegetation, a stretch of the river with semi-lotic characteristics. Average depth 0.21 m, average width 3.73 m, and average flow 0.50 m3 s-1.

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 Station 3: located in a rural area, with ciliary vegetation, a length of river with semilotic conditions. Average depth of 0.17 m, average width of 5.88 m, and average flow of 0.64 m3 s-1.

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In order to improve sampling, five separate transects were delineated separated by 3 meters, making a total distance of 12 meters between the first and last transect (Fig. 2). The

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physical, chemical, and biological data were evaluated at the center of each transect, with a total of 5 analyses per sampling station. Samples of the water, biotic community, and the

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periphytic substrate were taken from all transects.

Samples of the water and the periphytic substrate were taken from all transects. To evaluate the periphytic diatom community, substrate (stones) was collected from each transect

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at both banks (left and right) of the river, totalizing 10 stones per station. The stones were abundant at all of the sample points and readily collected. For each transect, the geographic

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coordinates were obtained via GPS (see Table in Appendix A). 2.3. Field sampling

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In order to estimate the relative abundance of the taxa, a standardized scraping of the

stones was done (area of 3 cm2) from the downstream face of each substrate sample, using a toothbrush. The remaining surface of the substrate was scraped in a non-standardized way to better sample the whole periphytic community. Sixty samples (30 relative abundances and 30 non-standardized) were packaged in flasks of 250 mL duly identified. The non-standardized samples were preserved in a 1:1 solution of Transeau and the relative abundance samples in a 1% solution of acetic Lugol (Bicudo and Menezes, 2006). The material was placed in the

5 Herbário da Universidade Estadual do Oeste do Paraná, the Western Paraná State University Herbarium (UNOP-Algae 1036–1074, 1222–1241 and 1361). For identification and counting of the taxa, subsamples of 10 mL were oxidized according to the technique proposed by Simonsen (1974), modified by Moreira-Filho and Valente-Moreira (1981). Permanent slides were prepared with a known volume (1.5 mL) using Naphrax® resin (I.R. = 1.74) for mounting. The observations and illustrations of the specimens were done using an Olympus BX60 binocular optical microscope with a DP 71 capture camera attached. The taxonomic framework followed Round et al. (1990) and Cox (2015). Species identifications were based on specialized literature, such as Hustedt (1930), Patrick and Reimer (1975), Krammer and Lange-Bertalot (1986, 1991), Metzeltin and Lange-

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Bertalot (1998, 2002), Rumrich et al. (2000), Levkov et al. (2016), Costa et al. (2017) among other works and periodicals. 2.4. Environmental variables

Physical and chemical data for the sampling sites such as temperature (Temp; °C),

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electrical conductivity (Ec; mS cm-1), dissolved oxygen (DO; mg L‑1), pH, and turbidity (Turb; NTU) were measured in situ using a HORIBA U-5000 multiparameter probe.

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The analyses in laboratory were carried out by GERPEL (Grupo de Pesquisas em Recursos Pesqueiros e Limnologia – Fishery Resources and Limnology Research Group),

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Unioeste-Campus Toledo. Physico-chemical variables mensured were: oxygen consumption analyses as a function of chemical oxidation (COD; mg L‑1) and of organic material (BOD; mg L‑1), concentrations of total Kjeldahl nitrogen (TKN; mg L‑1), nitrate (NO3;

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mg L‑1), ammonia (NH4; mg L‑1), total dissolved phosphorus (TP; mg L‑1), orthophosphate (PO4-; mg L‑1), total solids (TS; mg L‑1), dissolved solids (DS; mg L‑1) and suspended solids

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(SS; mg L‑1). We also measured three biological variables: chlorophyll a (CLa; mg L‑1), total coliforms (TC; mg L‑1) and Escherichia coli (E. coli; NMP/100 mL). All analyses were

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performed using standard methods (APHA, 2012). Chemical variables were measured after collection by means of sub-surface immersion of polyethylene flasks, properly refrigerated and kept in darkness until their destination. All analyses were done for each transect delimited as described in the sample design

above.

6 2.5.

Response variables

Individual diatoms were identified and counted to a minimum of 600 valves as recommended by Kobayasi and Mayama (1982) with 95% efficiency (Pappas and Stoermer, 1996). Diatom valves were counted in an optical microscope (1000 X), as oxidation tended to separate frustules (Moro and Bicudo, 2002), – including at least 50% of their full size broken ones. Cells in pleural view were identified when possible. For the quantitative analysis we calculated the density per cm2 according to Battarbee (1986) and Lobo et al. (1995). Abundant (valve density exceeds the average density for the sample) and dominant species (valve density is over 50% of the total density) were

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determined according to Lobo and Leighton (1986). 2.6. Data analysis

Considering the strong influence of the different land-uses, observed at sampling stations, on the periphytic diatom community, all the biotic and abiotic variables were

analyzed using descriptive statistics (average and coefficient of variation) according to their

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nature. For comparing potential statistical differences in species’ relative abundance and

observed richness between stations, single factor variance analysis (one-way ANOVA) was

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used with the post-hoc Tukey’s test, when significant.

The variation of environmental factors and periphytic diatom communities between

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stations was verified via a non-parametric permutational multivariate analysis (PERMANOVA), applied to the Bray-Curtis similarity matrix with 9,999 permutations. Environmental variables were submitted to principal component analysis (PCA) with

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the aim of characterize the stations and identify the variables that best differentiate them (Wiegleb, 1980).

To identify the environmental variables most related to species composition, a forward

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selection methodology was adopted. Thus, a Redundancy Analysis (RDA) was performed aiming to evaluate the ordering of the sampling stations in relation to the selected

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environmental variables and the diatom composition (Rao, 1964; Borcard and Legendre, 2002).

The matrix is composed of spatial variables (distances between transects and sampling

stations) that were generated to represent probable dispersion routes. For this purpose, we used a watercourse distance matrix. As a result, spatial filters were generated by eigenvalue analysis, a Principal Coordinates of Neighbor Matrices (PCNM, Borcard and Legendre, 2002). The truncation value used was the maximum geographic distance, which allows all the

7 communities to be linked in the connectivity matrix (Borcard and Legendre, 2002). The principal coordinates generated were also selected using forward selection, with the goal of highlighting those most related to species composition. Finally, the principle coordinates and the environmental variables most related to species composition selected, derived from positive eigenvalues, were utilized as exploratory variables in the partial RDA (Borcard and Legendre, 2002). The biotic abundance data was passed through Hellinger’s transformation and the environmental variables were standardized so that they would have the same weight in the analyses (Borcard et al., 2011). All the analyses were done using the statistical computation language R and its environment (R CORE TEAM, 2010) together with the vegan package

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(Oksanen et al., 2011).

3. Results

One-hundred and nine taxa distributed in 30 genera were found. Eunotia and

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Gomphonema presented the greatest richness at all stations with a total of 14 and 11 taxa

respectively. Also, at station 1, the genera Pinnularia and Navicula presented higher richness than others (12 and 8 taxa respectively) and at station 3, Encyonema, Achnanthidium, and

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Navicula (5, 5, and 6 taxa respectively), as illustrated in Fig. 3.

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The valve density was significantly different among stations (Df = 29, F = 31.29, p = 9.31 x 10-9), higher in station 2 (post hoc Tukey’s test). The species richness was also significantly distinct (Df = 29, F = 39.98, p = 8.5 x 10-9), with higher richness in station 1

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(post hoc Tukey’s test) (Table 2).

Among the taxa identified, 58 occurred with a relative abundance of 2% or higher (see

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Table in Appendix B). Gomphonema lagenula Kützing was the only taxon dominant – in 20% of the samples from station 2. The PERMANOVA test showed significant differences

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between stations based on the species abundance matrix (Df = 29, F = 5.04), R2 = 0.15, p = 0.001), thereby revealing the difference between the sample station communities. The PERMANOVA test showed significant difference between the stations based on

the environmental variable measured (see Table in Appendix B; F = 27.25, Df = 14, R2 = 0.68, p = 0.002). Principal component analysis (PCA) accounts for 51.85% of the total variability in the data in the first two axes (Fig. 4). The spread of the scores from the sampled locations in these axes exposed a spatial gradient with a clear separation in the collection

8 station map (Fig. 4). The first axis of the PCA explains the variability primary related to pH (correlation value: 0.33) and DO (0.4), both positively, and BOD (‑ 0.32) and nitrate (‑ 0.35), negatively. In this axis the separation between stations 1 and the others is clear (Fig. 4). The second axis is positively related with total coliforms (0.407) and Escherichia coli (0.47), and negatively with dissolved solids (‑ 0.37), total solids (‑ 0.35), and flow (‑ 0.33), This axis clearly differentiates station 2 from station 3 (Fig. 4).

The environmental selected variables most related to species composition were flow, dissolved oxygen, electrical conductivity, nitrate, ammonia, and total coliforms. Then, the

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detrended redundancy analysis (RDA) resulted in an explanatory power of 37.62%, showing that the species composition is significantly related to the selected variables as seen in the graph in Fig. 5 (F = 3.6501, p = 0.001).

The RDA defined two main ordination axes. The first (RDA1) with 20.52%

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explicability (eigenvalue = 0.085), presented more representative positive scores and

indicated the greater contribution of the variables ammonia (0.75), dissolved oxygen (0.44), and electrical conductivity (0.32). The species associated with positive values in these

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conditions were Discostella stelligera, Gomphonema lagenula and Fragilaria gracilis. Nupela pardinhoensis presented a negative relationship with the same conditions.

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The second ordination axis (RDA2), with 17.10% explicability (eigenvalue = 0.071) was associated positively by the flow variable (0.96). Achnanthidium minutissimum, Gomphonema pumilum and Gomphonema saprophilum were associated with positive values

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in these conditions. The negative scores for this axis showed greater contribution for the variables nitrate (‑ 0.77) and total coliforms (‑ 0.83) and were related with the presence of

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Sellaphora saugerresii and Eunotia botulitropica.

The variation partitioning method for quantifying the contribution of spatial and

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environment predictors for the diatom composition resulted in a variation 35.19% explained. In the partitioning, the pure environment effect contributed 0.22% while the spatial contributed 1,64%. Consequently, the greater part of the explanation for the community comes from the spatially structured environmental component (See more in Appendix D, fig. Da). Upon analyzing pure environment, an RDA show a diffuse grouping of the samples analyzed between stations (See more in Appendix D, Fig. Db), highlighting the positive

9 relationship of axis 1 with the variable DO. For axis two, the electrical conductivity variable showed a negative relationship and ammonia a negative. However, this analysis did not offer a significant explanation for the distribution of species between points (F = 1.0154, p = 0.423). Upon analyzing pure spatial, an RDA show a diffuse grouping of the samples analyzed between stations (See more in Appendix D, Fig. Dc), highlighting the negative relationship of axis 1 with the spatial variable PCNM 11 and PCNM 12. For axis two, the spatial variable PCNM 1 showed a positive relationship. However, this analysis also did not offer a significant explanation for the distribution of species between points (F = 1.1997, p = 0.164). As such, removing the spatial autocorrelation made it impossible to find a single

variables are spatially constrained in a linear gradient. 4.

Discussion

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environmental filtering explanation for the community variation as all environmental

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As expected, the species composition of the diatom communities presented great

differences between the sampling stations. Given the locations’ proximity, there is strong

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evidence that anthropic alterations are the cause of the changes instead of a natural alteration, as expected along a continuous river. The influence of environmental variables on the

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structure of the periphytic diatom assembly can also be observed throughout the data analysis. The sample design along a linear gradient exposes a spatial dependence model of environmental variables. This resulted in no evidence of a single explanation about

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environmental variables in the removal of spatial autocorrelation. In any case, anthropic impact is clear, as shown by the environmental differences among stations. The analyzed environments are clearly distinct regarding all the physical,

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chemical, and biological conditions analyzed. Studies involving periphytic diatom assemblies have reported the influence of different trophic environments on the structure and distribution

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of the species (Virtanen and Soininen, 2012; Burliga et al., 2014; Jamoneau et al., 2018). In the present study, the PCA grouped the majority of the transects according to sampling station, reflecting the differences in their structures. The relationship among the samples from the conservation area with nitrate

concentrations and BOD may be a response to the anthropic impact from the visitation and the advancement of urbanization, even in the presence of ciliary vegetation (see more in Remor et al., 2018). The station located in the urban area, more impacted and without ciliary vegetation,

10 responds to higher temperatures and turbidity. As the incidence of light on a body of water has a great effect on the development of periphytic diatoms (Tuji, 2000; Liess et al., 2009; Algarte et al., 2017), the extent of ciliary vegetation and depth of the body of water could have influenced its development. This aspect explains the higher richness in places with ciliary vegetation and higher density in the more impacted places, which are located in urban areas with a low proportion of ciliary vegetation (see also Dunck et al., 2013). The genera with high species richness for all the sampling stations are commonly periphytic groups, because they possess a variety of mucilaginous structures enabling them to attach to the substrate surface (Hoagland et al., 1982; Silver et al., 2006). Eunotia is cited in the literature as the most diverse genus in acidic environments, reflection of the water pH

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(Silver et al., 2006; Costa et al., 2017). Gomphonema is usually well-represented regarding richness, due to its form of attachment, with mucilage stalks, and because it includes many cosmopolitan species (Krammer and Lange-Bertalot, 1986; Levkov et al., 2016).

In stations with agricultural impacts Eunotia botulitropica, E. veneris and E. fallax

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stood out, indicating low total nitrogen concentration and electrical conductivity (Soininen et al., 2004; Costa et al., 2017). The presence of Sellaphora saugerresii in the same samples may be related not only to the nutrient conditions, but to low turbidity as well (Marra et al.,

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2016).

The relationship of the samples from station 2 with elevated levels of fecal coliforms

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and E. coli may reflect the influence of the area’s urbanization as well as the presence of an unofficial domestic trash dump. All variables indicate impoverishment of the ciliary vegetation and urban impact in station 2. This features favored the development of

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cosmopolitan diatoms such as Gomphonema lagenula, Gomphonema exilissimum, Discostella stelligera and Fragilaria gracilis, but nevertheless limited the development of more sensitive

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species (Soininen et al., 2004; Lange-Bertalot and Ulrich, 2014; Domingues et al., 2015; Lobo et al., 2015). Those taxa are commonly registered as tolerant of pollution and occurring in elevated nutrients and light availability conditions (Jüttner et al., 2013; Lobo et al., 2015;

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Faustino et al., 2016; Marra et al., 2016). In regions of high populational density, effluents coming from residences and

commercial establishments are the main reason for augmentation of fecal coliforms and nutrients in rivers and streams as well as for elevated turbidity, causing an imbalance in aquatic ecosystems (Von Sperling, 2014). Thus, elevated coliform values are an indication of strong interference from urbanization. Virtanen and Soininen (2012) suggest that those factors are important for the community diatom composition, as this group is strongly influenced by

11 specific environmental factors (Soininen, 2007; Bottin et al., 2014). In this, our results agree with previous studies, as there is a clear distinction in the composition of species between the sampled areas. Furthermore, in the location with the highest anthropic impact, the species present are clearly those tolerant of pollution (Van Dam et al., 1994; Tuji and Williams, 2007; Levkov et al., 2016). The distinction cited above is reflected in the shape of the species cells. In all areas, occurred species with “centric” shape. Generally considered predominant among planktonic river organisms (Round, 1990), the centric diatoms registered in the Cascavel River have already been reported in mesotrophic and eutrophic environments and are characterized in a broad way as tolerant of environments impacted by elevated nutrients load (see also in Silva

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et al., 2010; Lobo et al., 2015; Bicudo et al., 2016). We suggested that in small gradients, the effect of nutrients was low to detect the effect on the Aulacoseira. Possibly this occurs by the planktonic habit, characteristic of the genus, which facilitate the dispersion of the species for the other stations.

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In fact, autocorrelation is observed along the linear gradient of the river, because physical characteristics such as depth, water volume, flow, solar incidence, solid

concentrations, and temperature are altered, interfering directly in the primary production of

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the periphytic community (Vannote et al., 1980). Thus, the environmental variables do not explain in isolation the distribution of the community, because they are spatially structured in

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response to the sample design.

The agricultural area was characterized by high flow and dissolved oxygen concentration, factors directly interfering on diatom density as well as on species richness.

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Several studies highlight the importance of stream speed for the diatom community (Soininen, 2004; Michels et al., 2006; Virtanen and Soininen, 2012). According to Soininen (2004),

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under high velocity, the species richness tends to decrease because the community establishment is difficult in the environment. A few diatoms, as Achnanthidium and Fragilaria, are more resistant to high current velocity stream (Virtanen and Soininen, 2012),

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due to the fixation strategy that allows frustule to remain adhered to substrata by raphe or mucilaginous pads (Hoagland et al., 1982). That being the case, the presence of species such as Achnanthidium minutissimum can be explained by the strategy of resistance to turbulence, making the species better positioned in the biofilm (Wang et al., 2014). Our results clearly indicate the dynamics of the distribution of community adaptation. Small species such as Achnanthidium minutissimum, Gomphonema pumilum and Nupela pardinhoensis presented better development in station 3, which had lower nutrient load (Lobo

12 et al., 2015; Levkov et al., 2016), and higher flow (Wang et al., 2014). On the other hand, higher nutrient concentrations (Virtanen and Soininen, 2012; Lange-Bertalot and Ulrich, 2014; Lobo et al., 2015) and lower flow (see also Costa-Böddeker et al., 2012) were associated to stations with larger species, such as the mobile species of Frustulia and Pinnularia genera, and species such as Gomphonema naviculoides, Fragilaria pectinalis and Fragilaria gracilis, adhering by mucilage stalks or pads. We stress that the representation of the environmental variables was performed in a complete manner, generating a high percentage of explanation from the biological community, which is not commonly seen in the literature (see also Valente-Neto et al., 2017). The inclusion of microbiological factors in this study was particularly relevant, as it helped to

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improve the understanding of the relationship of the diatom community with microbiological indicators in tropical flows. The coliform concentration, an indicative of organic

contamination, was fundamental in determining that the changes along the basin occured as a consequence of soil usage and were not solely due to the system dynamic (Beltrami et al.,

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2012). Furthermore, in our study, nitrogen concentrations were more representative than the phosphorus as a representative of the trophic conditions of the environment in that analysis. Detecting human impact in a fluvial system is challenging due to several components

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requiring analysis (Krusche et al., 2005). Despite its local scale, our study has clearly demonstrated the impact of urbanization and agricultural areas in the composition and

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diversity of diatom communities in a microbasin, corroborating previous studies (e.g. Marra et al., 2018). By representing the environmental variables in a complete manner, we show the universal effect of the spatial autocorrelation (see also Heino et al., 2015). Only a complete

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analysis of the taxa (and its biological characteristics) with multivariate analysis standards can

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indicate how anthropic impacts affect the natural communities.

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Acknowledgements

Authors acknowledge CAPES and Fundação Araucária for continuous support

considering both student and researcher scholarships, and other financial resources. We are also grateful for two anonymous reviewers and the editor Michael Hupfer for valuable suggestions to improve the manuscript.

13 References

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-p

ro of

Abarca, N., Jahn, R., Zimmermann, J., Enke, N., 2014. Does the cosmopolitan diatom Gomphonema parvulum (Kützing) Kützing have a biogeography? PLoS One 9, e86885. https://doi.org/ doi:10.1371/journal.pone.0086885. Algarte, V.M., Siqueira, T., Landeiro, V.L., Rodrigues, L., Bonecker, C.C., Rodrigues, L.C., Santana, N.F., Thomaz, S.M., Bini, L.M., 2017. Main predictors of periphyton species richness depend on adherence strategy and cell size. PLoS One 12, 1–14. https://doi.org/10.1371/journal.pone.0181720. Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonc, L.D.M., Sparovek, G., 2013. Köppen’s climate classification map for Brazil Clayton. Meteorol. Zeitschrift 22, 711–728. https://doi.org/10.1127/0941-2948/2013/0507. APHA, A.P.H.A., 2012. Standard Methods for the Examination of Water and Wastewater, 22nd ed., Standard Methods. Copyright, Washington. Battarbee, R.W., 1986. Diatom analysis, in: Berglund, B.E., Ralska-Jasiewiczowa, M. (Eds.), Handbook of Holocene Palaeoecology and Palaeohydrology. J. Wiley & Sons, Chichester, pp. 527–570. Beltrami, M.E., Ciutti, F., Cappelletti, C., Lösch, B., Alber, R., Ector, L., 2012. Diatoms from Alto Adige/Südtirol (Northern Italy): Characterization of assemblages and their application for biological quality assessment in the context of the Water Framework Directive. Hydrobiologia 695, 153–170. https://doi.org/10.1007/s10750-012-1194-x. Bertolli, L.M., Tremarin, P.I., Ludwig, T.A.V., 2010. Diatomáceas perifíticas em Polygonum hydropiperoides Michaux, reservatório do Passaúna, Região Metropolitana de Curitiba, Paraná, Brasil. Acta Bot. Brasilica 24, 1065–1081. https://doi.org/10.1590/S010233062010000400022. Bes, D., Ector, L., Torgan, L.C., Lobo, E.A., 2012. Composition of the epilithic diatom flora from a subtropical river, Southern Brazil. Iheringia - Ser. Bot. 67, 93–125. Bicudo, C.E. de M., Menezes, M., 2006. Gêneros de Algas de Águas Continentais do Brasil, segunda ed. RiMa, São Carlos - SP. Bicudo, D.C., Tremarin, P.I., Almeida, P.D., Zorzal-, S., Wengrat, S., Faustino, S.B., Costa, L.F., Elaine, C.R., Rocha, A.C.R., Bicudo, C.E.M., Morales, E.A., Wengrat, S., Faustino, S.B., Costa, L.F., Bartozek, E.C.R., Rocha, C.R., Bicudo, C.E.M., Morales, E.A., 2016. Ecology and distribution of Aulacoseira species (Bacillariophyta) in tropical reservoirs from Brazil. Diatom Res. 8347, 1–17. https://doi.org/10.1080/0269249X.2016.1227376. Borcard, D., Gillet, F., Legendre, P., 2011. Use R!, Springer. Springer US, New York. https://doi.org/10.1007/978-0-387-78171-6. Borcard, D., Legendre, P., 2002. All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol. Modell. 153, 51–68. https://doi.org/10.1016/S0304-3800(01)00501-4. Bottin, M., Soininen, J., Ferrol, M., Tison-Rosebery, J., 2014. Do spatial patterns of benthic diatom assemblages vary across regions and years? Freshw. Sci. 33, 402–416. https://doi.org/10.1086/675726. Burliga, A.L., Torgan, L.C., De Andrade, E.A.N., Sutil, C., Beaumord, A.C., Laux, M., Kociolek, J.P., 2014. Changes in diatom associations with altitudinal gradient and land use in Itajaí-Mirim River, Southern Brazil. Iheringia - Ser. Bot. 69, 451–464. Cembranel, A.S., Sampaio, S.C., Remor, M.B., Gotardo, J.T., Rosa, P.M.D., 2017. Geochemical background in an oxisol. Eng. Agrícola 37, 565–573. https://doi.org/http://dx.doi.org/10.1590/1809-4430-Eng.Agric.v37n3p565-573/2017. Costa-Böddeker, S., Bennion, H., Jesus, T.A. de, Albuquerque, A.L.S., Figueira, R.C.L.,

14

Jo

ur

na

lP

re

-p

ro of

Bicudo, D. de C., 2012. Paleolimnologically inferred eutrophication of a shallow, tropical, urban reservoir in southeast Brazil. J. Paleolimnol. 48, 751–766. https://doi.org/10.1007/s10933-012-9642-1. Costa, L.F., Wetzel, C.E., Lange-Bertalot, H., Ector, L., Bicudo, D.C., 2017. Taxonomy and ecology of Eunotia species (Bacillariophyta) in southeastern Brazilian reservoirs. Cramer, Stuttgart, Germany. Cox, E.J., 2015. Diatoms (Diatomeae, Bacillariophyceae s.l.), in: Frey, E.W. (Ed.), Syllabus of Plant Families - A. Engler’s Syllabus Der Pflanzenfamilien Part 2/1: Photoautotrophic Eukaryotic Algae. Schweizerbart Science Publishers, Stuttgart, Germany, pp. 64–103. Davidson, T.A., Jeppesen, E., 2013. The role of palaeolimnology in assessing eutrophication and its impact on lakes. J. Paleolimnol. 49, 391–410. https://doi.org/10.1007/s10933012-9651-0. Dere, S., Dalkiran, N., Karacaoglu, D., Elmaci, A., Dülger, B., Sentürk, E., 2006. Relationship among epipelic diatom taxa, bacterial abundances and water quality in a highly polluted stream catchment, Bursa – Turkey. Environ. Monit. Assess. 112, 1–22. https://doi.org/10.1007/s10661-006-0213-7. Domingues, R.B., Guerra, C.C., Barbosa, A.B., Galvão, H.M., 2015. Are nutrients and light limiting summer phytoplankton in a temperate coastal lagoon? Aquat. Ecol. 49, 127– 146. https://doi.org/10.1007/s10452-015-9512-9. Dong, X., Li, B., He, F., Gu, Y., Sun, M., Zhang, H., Tan, L., Xiao, W., Liu, S., Cai, Q., 2016. Flow directionality, mountain barriers and functional traits determine diatom metacommunity structuring of high mountain streams. Sci. Rep. 6, 1–11. https://doi.org/10.1038/srep24711. Dunck, B., Nogueira, I., Felisberto, S., 2013. Distribution of periphytic algae in wetlands (Palm swamps, Cerrado), Brazil. Brazilian J. Biol. 73, 331–346. https://doi.org/10.1590/S1519-69842013000200013. Faustino, S.B., Fontana, L., Bartozek, E.C.R., Bicudo, C.E de M., Bicudo, D. de C., 2016. Composition and distribution of diatom assemblages from core and surface sediments of a water supply reservoir in Southeastern Brazil. Biota Neotrop. 16, 1–23. https://doi.org/http://dx.doi.org/10.1590/1676-0611-BN-2015-0129. FUNDETEC - Fundação para o desenvolvimento científico e tecnológico. 1995. Bacia Hidrográfica do Rio Cascavel – Proposta para recuperação ambiental. FUNDETEC, Cascavel. 164p. Gonçalves, C.S., Rheinheimer, D. dos S., Pellegrini, J.B.R., Kist, S.L., 2005. Qualidade da água numa microbacia hidrográfica de cabeceira situada em região produtora de fumo. Rev. Bras. Eng. Agric. Ambient. 9, 391–399. Heino, J., Melo, A.S., Siqueira, T., Soininen, J., Valanko, S., Bini, L.M., 2015. Metacommunity organisation, spatial extent and dispersal in aquatic systems: Patterns, processes and prospects. Freshw. Biol. 60, 845–869. https://doi.org/10.1111/fwb.12533. Hoagland, K.D., Roemer, S.C., Rosowski, J.R., 1982. Colonization and community structure of two periphyton assemblages, with emphasis on the diatoms (Bacillariophyceae). Am. J. Bot. 69, 188–213. https://doi.org/10.1002/j.1537-2197.1982.tb13249.x. Hofmann, G., 1994. Aufwuchs-Diatomeen in Seen und ihre Eignung als Indikatoren der Trophie. Cramer, Stuttgart, Germany. Houk, V., Klee, R., 2004. The stelligeroid taxa of the genus Cyclotella (Kützing) Brébisson (Bacillariophyceae) and their transfer into the new genus Discostella gen. nov. Diatom Res. 19, 203–228. https://doi.org/10.1080/0269249X.2004.9705871. Hustedt, F., 1930. Bacillariophyta (Diatomeae), in: Pascher, A. (Ed.). Die Süsswasser-Flora Miteleuropas. Gustav Fischer, Jena, pp. 1–466. Huston, M.A, 1999. Local process and regional patterns: appropiate scales for understanding

15

Jo

ur

na

lP

re

-p

ro of

variation in the diversity of plants and animals. Oikos 86, 393–401. Jamoneau, A., Passy, S.I., Soininen, J., Leboucher, T., Tison-Rosebery, J., 2018. Beta diversity of diatom species and ecological guilds: response to environmental and spatial mechanisms along the stream watercourse, in: Freshwater Biology. https://doi.org/10.1111/fwb.12980. Jeppesen, E., Jensen, J.P., SØndergaard, M., Lauridsen, T., Landkildehus, F., 2000. Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw. Biol. 45, 201–218. https://doi.org/10.1046/j.1365-2427.2000.00675.x. Jüttner, I., Ector, L., Reichardt, E., Van De Vijver, B., Jarlman, A., Krokowski, J., Cox, E.J., 2013. Gomphonema varioreduncum sp. nov., a new species from northern and western Europe and a re-examination of Gomphonema exilissimum. Diatom Res. 28, 303–316. https://doi.org/10.1080/0269249X.2013.797924. Kobayasi, H., Mayama, S., 1982. Most pollution-tolerant diatoms of severely polluted rivers in the vicinity of Tokyo. Japanese J. Phycol. 30, 188–196. Krammer, K., 1997. Die cymbelloiden Diatomeen: eine Monographie der weltweit bekannten taxa. II Encyonema Part., Teil 2., Encyonopsis and Cymbellopsis. Bibl. Diatomol., J. Cramer, Stuttgart. Krammer, K., Lange-Bertalot, H., 1986. Bacillariophyceae. 1. Teil: Naviculaceae., Süβwasserflora von Mitteleuropa. Gustav Fischer Verlag, Stuttgart - New York. Krammer, K., Lange-Bertalot, H., 1988. Bacillariophyceae: Bacillariaceae, Epithemiaceae, Surirellaceae, in: Ettl, H., Gerloff, J., Heynig, H. & Mollenhauer, D. (Eds.), Süßwasserflora von Mitteleuropa. Gustav Fisher, Jena, Stuttgart, pp. 1–596. Krammer, K., Lange-Bertalot, H., 1991. Bacillariophyceae 4. Teil: Achnanthaceae, Kritische Erganzungen zu Navicula (Lineolatae) und Gomphonema, in: Ettl, H., Gerloff, J., Heynig, H. & Mollenhauer, D. (Eds.), Süßwasserflora von Mitteleuropa. Gustav Fischer, Stuttgart, pp. 1–576. Krusche, A.V., Victoria, M., Ballester, R., Victoria, R.L., Correa, M., Leite, N.K., Hanada, L., Victoria, D.D.C., Marcondes, A., Ometto, J.P., Moreira, M.Z., Gomes, B.M., Alexandre, M., Neto, S.G., Bonelli, N., Deegan, L., Neill, C., Aufdenkampe, A.K., Richey, J.E., 2005. Efeitos das mudanças do uso da terra na biogeoquímica dos corpos d’água da bacia do rio Ji-Paraná, Rondônia. Acta Amaz. 35, 197–205. https://doi.org/10.1590/S004459672005000200009. Lange-Bertalot, H., 2001. Diatoms of Europe, Volume 2: Navicula Sensu Stricto, 10 Genera Separated from Navicula Sensu Lato, Frustulia. Gantner Publishers, Stuttgart, Germany. Lange-Bertalot, H., Bak, M., Witkowski, A., 2011. Eunotia and some related genera. Diatoms of Europe, Gantner Verlag Kommanditgesellschaft, Ruggell. Lange-Bertalot, H., Moser, G., 1994. Brachysira, Monographie der Gattung. Bibl. Diatomol., Stuttgart, Berlin. Lange-Bertalot, H., Ulrich, S., 2014. Contributions to the taxonomy of needle-shaped Fragilaria and Ulnaria species. Lauterbornia 78, 1–73. Lepskaya, E. V., Jewson, D.H., Usoltseva, M. V., 2010. Aulacoseira subarctica in kurilskoye lake, kamchatka: A deep, oligotrophic lake and important pacific salmon nursery. Diatom Res. 25, 323–335. https://doi.org/10.1080/0269249X.2010.9705853. Levkov, Z., Krstić, S., Metzeltin, D., Nakov, T. 2007. Diatoms of Lakes Prespa and Ohrid. About 500 taxa from ancient lake system, in: Lange-Bertalot, H. (Ed.), Iconogr. Diatomol. Annotated Diatom Monographs. Gantner Verlag, Ruggell, pp. 1–613. Levkov, Z., Metzeltin, D., Pavlov, A. 2013. Luticola and Luticopsis, in: Lange-Bertalot, H. (Ed.), Diatoms of Europe. Diatoms of the European inland waters and comparable habitats. Koeltz Scientific Books, Königstein, pp. 1–697. Levkov, Z., Mitić-Kopanja, D., Reichardt, E., 2016. The diatom genus Gomphonema from the

16

Jo

ur

na

lP

re

-p

ro of

Republic of Macedonia, in: Lange-Bertalot, H. (Ed.), Diatoms of Europe, Koeltz Botanical Books, pp. 1–552. Liess, A., Lange, K., Schulz, F., Piggott, J.J., Matthaei, C.D., Townsend, C.R., 2009. Light, nutrients and grazing interact to determine diatom species richness via changes to productivity, nutrient state and grazer activity. J. Ecol. 97, 326–336. https://doi.org/10.1111/j.1365-2745.2008.01463.x. Liu, S., Xie, G., Wang, L., Cottenie, K., Liu, D., Wang, B., 2016. Different roles of environmental variables and spatial factors in structuring stream benthic diatom and macroinvertebrate in Yangtze River Delta, China. Ecol. Indic. 61, 602–611. https://doi.org/10.1016/j.ecolind.2015.10.011. Liu, Y., Wang, Q., Fu, C., 2011. Taxonomy and distribution of diatoms in the genus Eunotia from the Da’erbin Lake and Surrounding Bogs in the Great Xing’an Mountains, China. Nov. Hedwigia 92, 205–232. https://doi.org/10.1127/0029-5035/2011/0092-0205. Lobo, E., Leighton, G., 1986. Estructuras comunitarias de las fitocenosis planctonicas de los sistemas de desembocaduras de rios y esteros de la zona central de chile. Rev. Biol. Mar. 22, 1–29. Lobo, E.A., Katoh, K., Aruga, Y., 1995. Response of epilithic diatom assemblages to water pollution in rivers located in the Tokyo Metropolitan area, japan. Freshw. Biol. 34, 191– 204. Lobo, E.A., Schuch, M., Heinrich, C.G., Ben, A., Düpont, A., Wetzel, C.E., Ector, L., 2015. Development of the Trophic Water Quality Index (TWQI) for subtropical temperate Brazilian lotic systems. https://doi.org/10.1007/s10661-015-4586-3. Lowe, R.L., Kociolek, P., Johansen, J.R.; Van de Vijver, B., Lange-Bertalot, H., Kopalová, K. 2014. Humidophila gen. nov., a new genus for a group of diatoms (Bacillariophyta) formerly within the genus Diadesmis: species from Hawai'i, including one new species. Diatom Res. 29, 351–360. http://dx.doi.org/10.1080/0269249X.2014.889039. Mann, D.G., Mcdonald, S.M., Bayer, M.M., Droop, S.J.M., Chepurnov, V.A., Loke, R.E., Ciobanu, A., Du Buf, J.M.H., 2004. The Sellaphora pupula species complex (Bacillariophyceae): morphometric analysis, ultrastructure and mating data provide evidence for five new species. Phycol. 43, 459–482. Marra, R.C., Algarte, V.M., Ludwig, T.A.V., Padial, A.A., 2018. Diatom diversity at multiple scales in urban reservoirs in Southern Brazil reveals the likely role of trophic state. Limnol. 70, 49–57. https://doi.org/10.1016/j.limno.2018.04.001. Marra, R.C., Tremarin, P.I., Algarte, V.M., Ludwig, T.A.V., 2016. Epiphytic diatoms (Diatomeae) from Piraquara II urban reservoir, Paraná state. Biota Neotrop. 16, 1–19. https://doi.org/http://dx.doi.org/10.1590/1676-0611-BN-2016-0200. Metzeltin, D., Lange-Bertalot, H., 1998. Iconog. Diatomol., Volume 5: Diversity, Taxonomy and Geobotany: Tropical Diatoms of South America I: About 700 predominantly rarely known or new taxa representative of the neotropical flora, Iconogr. Diatomol.. A.R.G. Gantner Verlag, California. Metzeltin, D., Lange-Bertalot, H., 2002. Iconogr. Diatomol., Volume 11: Tropical Diatoms of South America, II: Special Remarks on Biogeographic Disjunction. A.R.G. Gantner Verlag, California. Metzeltin, D., Lange-Bertalot, H., 2007. Tropical diatoms of South America II. Special remarks on biogeographic disjunction, in: Lange-Bertalot, H. (Ed.), Iconogr. Diatomol., Volume 18, A.R.G. Gantner Verlag, Ruggell, pp. 1–877. Metzeltin, D., Lange-Bertalot, H., García-Rodríguez, F., 2005. Diatoms of Uruguay. Compared with other taxa from South America and elsewhere, in: Lange-Bertalot, H. (Ed.), Iconogr. Diatomol., volume 15, A.R.G. Gantner Verlag, Ruggell, pp. 1–736. Michels, A., Umaña, G., Raeder, U., 2006. Epilithic diatom assemblages in rivers draining

17

Jo

ur

na

lP

re

-p

ro of

into Golfo Dulce (Costa Rica) and their relationship to water chemistry, habitat characteristics and land use. Arch. für Hydrobiol. 165, 167–190. https://doi.org/10.1127/0003-9136/2006/0165-0167. Morales, E.A., Ector, L., Fernández, E., Novais, M.H., Hlúbiková, D., Hamilton, P.B., Blanco, S., Vis, M.L., Kociolek, P., 2011. The genus Achnanthidium Kütz. (Achnanthales, Bacillariophyceae) in Bolivian streams: a report of taxa found in recent investigations. Algol. Stud. 136/137, 89–130. https://doi.org/10.1127/18641318/2011/0136-0089. Moreira-Filho, H., Valente-Moreira, I., 1981. Avaliação taxonômica e ecológica das diatomáceas (Bacillariophyceae) epifitas em algas pluricelulares obtidas nos litorais dos Estados do Paraná, Santa Catarina e São Paulo. Bol. do Mus. Bot. Munic. (Brazil). 1, 1– 17. Moro, R.S., Bicudo, C.E.M., 2002. Estimativa da densidade valvar de diatomáceas em lâminas permanentes e em câmaras de sedimentação: qual método utilizar? Acta Limnol. Brasiliensia. 14, 53–57. Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., O ’hara, R.B., Simpson, G.L., Stevens, M.H.H., Wagner, H., 2011. Vegan: Community Ecology Package Version 1. Pappas, J.L., Stoermer, E.F., 1996. Quantitative method for determining a representative algal sample count. J. Phycol. 32, 693–696. https://doi.org/10.1111/j.0022-3646.1996.00693.x. Patrick, R., Reimer, C.W., 1966. The Diatoms of United States: exclusive of Alaska and Hawaii. The Academy of Natural Sciences of Philadelphia, Philadelphia. Patrick, R., Reimer, C.W., 1975. The diatoms of the United States : Exclusive of Alaska and Hawaii. The Academy of Natural Sciences of Philadelphia, Philadelphia. Potapova, M., Hamilton, P.B., 2007. Morphological and ecological variation within Achnanthidium minutissimum (Bacillariophyceae) species complex. J. Phycol. 43, 561– 571. https://doi.org/ 10.1111/j.1529-8817.2007.00332.x. R Core Team, 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0. URL. http://www.R-project.org/. Rao, C.R., 1964. The Use and Interpretation of Principal Component Analysis in Applied Research. Sankhya -Indian J. Stat. Ser. A 26, 329–358. Raupp, S. V., Torgan, L.C., Melo, S., 2009. Planktonic diatom composition and abundance in the Amazonian floodplain Cutiuaú Lake are driven by the flood pulse. Biol. Limnol. 21, 227–234. Reichardt, E., 1997. Taxonomische Revision dês Artenkomplexes um Gomphonema pumilum (Bacillariophyceae). Nov. Hewigia 65, 114-115. Reichardt, E., 1999. Zur Revision der Gattung Gomphonema. Die Arten um G. affine/insigne, G. angustatum/micropus, G. acuminatum sowie gomphonemoide Diatomeen aus dem Oberoligozän in Böhmen, in: Lange-Bertalot, H. (Ed.), Iconogr. Diatomol. 8. A.R.G. Gantner Verlag K.G., Rugell, Germany, pp. 1–206. Reichardt, E., 2015. Gomphonema gracile Ehrenberg sensu stricto et sensu auct. (Bacillariophyceae): A taxonomic revision. Nova Hedwigia. 101, 367–393. https://doi.org/ 10.1127/nova_hedwigia/2015/0275. Remor, M.B., Sampaio, S.C., Rijk, S. De, Boas, M.A.C., Gotardo, J.T., Pinto, E.T., Schardong, F.A., 2018. Sediment geochemistry of the urban Lake Paulo Gorski. Int. J. Sediment Res. 33, 406–414. https://doi.org/10.1016/j.ijsrc.2018.04.009. Round, F.E., 1990. Diatom Communities their Response to Changes in Acidity. Philos. Trans. R. Soc. B Biol. Sci. 327, 243–249. https://doi.org/10.1098/rstb.1990.0059. Round, F.E., Crawford, R.M., Mann, D.G., 1990. The diatoms: Biology and morphology of the genera. Cambridge University Press, Cambridge.

18

Jo

ur

na

lP

re

-p

ro of

Rumrich, U., Lange-Bertalot, H., Rumrich, M., 2000. Diatomeen der Anden : von Venezuela bis Patagonien/Feuerland: und zwei weitere Beiträge = Diatoms of the Andes : from Venezuela to Patagonia/Tierra del Fuego: and two additional contributions. A.R.G. Gantner Verlag, Königstein, Germany. Silva, A.M. da, Ludwig, T.A.V., Tremarin, P.I., Vercellino, I.S., 2010. Diatomáceas perifíticas em um sistema eutrófico brasileiro (Reservatório do Iraí, estado do Paraná). Acta Bot. Brasilica 24, 997–1016. Silver, P.A., Hamilton, P.B., Morales, E., 2006. Two new planktic species of Eunotia (Bacillariophyceae) from freshwater waterbodies in North. Arch. Hydrobiol. Suppl. Algol. Stud. 119, 1–16. https://doi.org/10.1127/1864-1318/2006/0119-0001. Simonsen, R., 1974. The diatom plankton of the Indian Ocean expedition of R/V Meteor, 1964-1965. Meteor Forschungsergebnisse, Reibe D19. pp. 1 –107. Siver, P.A., Hamilton, P.B., 2011. Diatoms of North America: The Freshwater Flora of Waterbodies on the Atlantic Coastal Plain, in: Lange-Bertalot, H. (Ed.) Iconogr. Diatomol., A.R.G. Gantner Verlag, Rugell, pp. 1-923. Sliva, L., Williams, D.D., 2001. Buffer zone versus whole catchment approaches to studying land use impact on river water quality. Wat. Res. 35, 3462–3472. Soininen, J., 2004. Assessing the current related heterogeneity and diversity patterns of benthic diatom communities in a turbid and a clear water river. Aquat. Ecol. 38, 495– 501. https://doi.org/10.1007/s10452-005-4089-3. Soininen, J., 2007. Environmental and spatial control of freshwater diatoms—a review. Diatom Res. 22, 473–490. https://doi.org/http://dx.doi.org/10.1080/0269249X.2007.9705724. Soininen, J., Paavola, R., Muotka, T., 2004. Benthic diatom communities in boreal streams: community structure in relation to environmental and spatial gradients. Ecography (Cop.). 27, 330–342. https://doi.org/10.1111/j.0906-7590.2004.03749.x. Soininen, J., Weckström, J., 2009. Diatom community structure along environmental and spatial gradients in lakes and streams. Fundam. Appl. Limnol. 174, 205–213. https://doi.org/10.1127/1863-9135/2009/0174-0205. Taylor, J.C., Harding, W.R., Archibald, C.G.M., 2007. An Illustrated Guide to Some Common Diatom Species from South Africa An Illustrated Guide to Some Common Diatom Species from South Africa. WRC Report TT 282/07, Pretoria. Tremarin, P.I., Ludwig, T.V., Torgan, L.C., 2013. Morphological variation and distribution of the freshwater diatom Aulacoseira ambigua (Grunow) Simonsen in Brazilian continental environments. Iheringia - Ser. Bot. 68, 139–157. Trobajo, R., Rovira, L., Ector, L., Wetzel, C.E., Kelly, M., Mann, D.G., 2013. Morphology and identity of some ecologically important small Nitzschia species. Diatom Res. 28, 37– 59. http://dx.doi.org/10.1080/0269249X.2012.734531. Tuji, A., 2000. Note the Effect of Irradiance on the Growth of Different Forms of Freshwater Diatoms: Implications for Succession in Attached Diatom Communities 661, 659–661. Tuji, A., Houki, A., 2004. Taxonomy, Ultrastructure, and Biogeography of the Aulacoseira subartica Species Complex. Natl. Sci. Museum 30, 35–54. Tuji, A., Williams, D.M., 2007. Type Examination of Japanese Diatoms Described by Friedrich Meister (1913) from Lake Suwa. Natl. Sci. Museum 33, 69–79. Tuji, A., Williams, D.M., 2008. Typification and type examination of Synedra familiaris Klitz. and related taxa. Diatom Res. 24, 25–29. Valente-Neto, F., Durães, L., Siqueira, T., Roque, F.O., 2017. Metacommunity detectives: Confronting models based on niche and stochastic assembly scenarios with empirical data from a tropical stream network. Freshw. Biol. 63, 86–99. https://doi.org/10.1111/fwb.13050.

19

Jo

ur

na

lP

re

-p

ro of

Van Dam, H., Mertens, A., Sinkeldam, J., 1994. A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands. Netherlands J. Aquat. Ecol. 28, 117–133. https://doi.org/10.1007/BF02334251. Vannote, R.L., Minshall, G.W., Cummins, K.W., Sedell, J.R., Cushing, C.E., 1980. The River Continuum Concept. Can. J. Fish. Aquat. Sci. 37, 130–137. https://doi.org/10.1139/f80017. Virtanen, L., Soininen, J., 2012. The roles of environment and space in shaping stream diatom communities. Eur. J. Phycol. 47, 160–168. https://doi.org/10.1080/09670262.2012.682610. Virtanen, L.K., Soininen, J., 2016. Temporal variation in community-environment relationships and stream classifications in benthic diatoms: Implications for bioassessment. Limnologica 58, 11–19. https://doi.org/10.1016/j.limno.2016.01.003. Von Sperling, M., 2014. Introdução à Qualidade das Águas e ao Tratamento de Esgotos Volume 1. Coleção Princípios do Tratamento Biológico de Água, fourth ed. UFMG, Belo Horizonte. Vouilloud, A.A., Sala, S.E., Avellaneda, M.N., Duque, S.R., 2010. Diatoms from the Colombian and Peruvian Amazon: the Genera Encyonema, Encyonopsis and Gomphonema (Cymbellales: Bacillariophyceae). Rev. Biol. Trop. 58, 45–62. Wang, Q., Hamilton, P.B., Kang, F., 2014. Observations on attachment strategies of periphytic diatoms in changing lotic systems (Ottawa, Canada). Nov. Hedwigia 99, 239– 253. https://doi.org/10.1127/0029-5035/2014/0171. Wehr, J.D., Sheath, R.G., 2003. Freshwater habitats of algae, in: Freshwater Algae of North America. Elsevier, pp. 11–57. https://doi.org/10.1016/B978-012741550-5/50003-9. Wetzel, C.E., Bicudo, D. de C., Ector, L., Lobo, E.A., Soininen, J., Landeiro, V.L., Bini, L.M., 2012. Distance Decay of Similarity in Neotropical Diatom Communities. PLoS One 7, e45071. https://doi.org/10.1371/journal.pone.0045071. Wetzel, C.E., Ector, L., 2015. Taxonomy and Ecology of Fragilaria microvaucheriae sp. nov. and Comparison with the Type Materials of F. uliginosa and F. vaucheriae. Cryptogam. Algol. 36, 271–289. https://doi.org/10.7872/crya/v36.iss3.2015.271. Wetzel, C.E., Ector, L., Van De Vijver, B. V.D., Compère, P., Mann, D.G., 2015. Morphology, typification and critical analysis of some ecologically important small naviculoid species (Bacillariophyta). Fottea 15, 203–234. https://doi.org/10.5507/fot.2015.020. Wetzel, C.E., Lobo, E.A., Oliveira, M.A., Bes, D., 2002. Diatomáceas epilíticas relacionadas a fatores ambientais em diferentes trechos dos rios Pardo e Pardinho, Bacia Hidrográfica do Rio Pardo, RS, Brasil: resultados preliminares. Cad. Pesqui. série Biol. (ISSN 16775600) 14, 17–38. Wetzel, R.G., 2001. Limnology: lake and river ecosystems. Academic Press, San Diego. Wiegleb, G., 1980. Some applications of principal components analysis in vegetation: ecological research of aquatic communities, in: Maarel, E. Van Der (Org.), Vegetation: Ecological research of aquatic communities. Vegetatio, Oldenburg, pp. 67–73. https://doi.org/10.1007/978-94-009-9197-2. Wojtal, A., 2003. Diatoms of the genus Gomphonema Ehr. (Bacillariophyceae) from a karstic stream in the Krakowsko-Częstochowska Upland. Acta. Soc. Bot. Pol. 72, 213–220. Wojtal, A.Z., Ector, L., Van de Vijver, B., Morales, E.A., Blanco, S., Piatek, J., Smieja, A., 2011. The Achnanthidium minutissimum complex (Bacillariophyceae) in southern Poland. Algol. Stud. 136, 211–238. https://doi.org/10.1127/1864-1318/2011/0136-0211. Yang, J.R., Dickman, M., 1993. Diatoms as indicators of lake trophic status in central Ontário, Canada. Diatom Res. 8, 179–193. https://doi.org/10.1080/0269249x.1993.9705249.

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Zorzal-Almeida, S., Soininen, J., Bini, L.M., Bicudo, D.C., 2017. Local environment and connectivity are the main drivers of diatom species composition and trait variation in a set of tropical reservoirs. Freshw. Biol. 62, 1551–1563. https://doi.org 10.1111/fwb.12966.

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Fig 1. Locations of the three sampling stations along the Cascavel River, municipality of Cascavel, PR, Brazil.

Fig 2. Delimitation schema for the collection transects at each sampling station evaluated in the Cascavel River microbasin, municipality of Cascavel, PR, Brazil. T: transect, LB: left bank of the river, RB: right bank.

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Fig. 3. Species richness by genus present at the Cascavel River sample stations (S: sampling station).

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Fig. 4. Analysis of the principal components for the physical, chemical, and biological data at the three sampling stations of the Cascavel River, PR, Brazil. Legend: Temp: temperature, Ec: electrical conductivity, DO: dissolved oxygen, Turb: turbidity, Flo: flow, COD: chemical oxidation demand, BOD: biochemical oxygen demand, TN: total Kjeldahl nitrogen, NO3-: nitrate, NH4+: ammonia, TP: total dissolved phosphorus, PO43-: orthophosphate, CLa: chlorophyll a, TS: total solids, DS: dissolved solids, SS: suspended solids, CT: total coliforms, E. coli: Escherichia coli.

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Fig. 5. Detrended redundancy analysis (RDA) diagram done with the species abundance matrix the measured variables matrix, selected by forward selection. (Ec: electrical conductivity, DO: dissolved oxygen, Flo: flow, NO3-: nitrate, NH4+: ammonia, TC: total coliforms.). See species codes in Appendix B.

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Table 2 Minimum, maximum, and average values and coefficients of variation for diatom valve density per cm 2 and species richness in the Cascavel River sampling stations (n = 10). (S: sampling station, CV: coefficient of variation). Minimum Maximum Average CV S1 1.33 2.05 1.63 0,127 Density (valves/cm²) x106 S2 7.30 26.55 12.06 0,462 S3 1.38 2.27 1.66 0,150 S1 30 37 34 0,069 Species richness S2 21 28 24 0,103 S3 15 31 21 0,227

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Appendix D

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Fig. D. (a) Partition of the diatom community variation between measured environmental variables selected via forward selection (X1) and spatial ones (X2) for species abundance between the transects of the sampling stations. Res = residuals. (b) Diagram of the detrended partial redundancy analysis (partial RDA) resulting from the partition done with the species abundance matrix of the measured variables, selected via forward selection. (c) Diagram of the detrended partial redundancy analysis (partial RDA) resulting from the partition done with the species abundance matrix of the watercourse distance matrix, selected via forward selection. (Ec: electrical conductivity, DO: dissolved oxygen, Flo: flow, NO 3-: nitrate, NH4+: ammonia, TC: total coliforms).