https://orcid.org/0000-0002-5280-3185
Figures
Abstract
In order to access environmental conditions, the use of bioindicators that have a close relationship with environmental stressors is a largely common practice, but when evaluating environmental inferences, the individual dominant taxa need to be interpreted. Humid regions such as the marshlands are fragile ecosystems and sustain communities of microalgae, often used as bioindicators, of which diatoms are a good example. Although they provide an excellent response to chemical and physical changes in water, diatom studies in surface sediments in wetlands are scarce worldwide. To determine whether diatom species have the potential to provide unambiguous inferences in the influence of environmental factors, we have evaluated diatom abundance in surface sediment, from three Pantanal lakes, against a set of environmental gradients: pH, dissolved oxygen, turbidity, conductivity, total dissolved solids, water temperature, index of trophic water status, total phosphorus and total nitrogen. The Ferradura lake presented an oligotrophic state and both Burro and Caracará lakes presented mesotrophic state. Diatoms were more abundant in the a mesotrophic conditions, but with higher species richness in the oligotrophic conditions. Depending on the N:P ratio, the nutrients nitrogen and phosphorus can also play the role of pollutants and may have negative and unpredictable effects in the environment, such as biotic homogenization. Despite the spatial variation in species, there was a greater richness of Eunotia Ehrenberg species, with the highest relative density of Eunotia formica Ehrenberg and E. pantropica Glushchenko, Kulikovskiy & Kociolek, due to the environmental acidic conditions, a determining characteristic of this genus. It was also observed that a small increase in the level of phosphorus generated an increase in the abundance of Aulacoseira Thwaites with the highest relative density of A. pusilla (Meister) Tuji & Houki and A. veraluciae Tremarin, Torgan & T.Ludwig. However, A. italica dominated in the moderately acidic environment. The results can help with decisions in impacted areas to solve socioeconomic problems, environmental management and biodiversity.
Citation: Nardelli MS, Bicudo DC, Sampaio SC, Cordovil CMdS (2021) Structure and species composition of diatom community during the wet season in three floodplain lakes of Brazilian Pantanal. PLoS ONE 16(5): e0251063. https://doi.org/10.1371/journal.pone.0251063
Editor: George Swann, University of Nottingham, UNITED KINGDOM
Received: January 6, 2021; Accepted: April 19, 2021; Published: May 5, 2021
Copyright: © 2021 Nardelli et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript.
Funding: - M.S.N.:This work was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES - Finance Code 001/PDSE process number 88881.134251/2016-01) - C.M.d.S.C.: This work was funded by the NitroPortugal (H2020-TWINN-2015, EU support action n. 692331 for funding, 1Jan 2016-31 Dez 2018), and by the Forest Research Centre, a research unit funded by Fundação para a Ciência e a Tecnologia I.P. (FCT - Portugal - UIDB/00239/2020). -The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Aquatic environments have frequently been affected by different anthropic activities, resulting in negative impacts to river basins in developed [1–6] and wild regions [7–9], such as Pantanal of Mato Grosso, the largest continuous floodplain in South America, located in Brazil. Compared to the six Brazilian continental biomes, the Pantanal Biome accounts for only 1.76% of the country territory. However, it is of outstanding importance due to the complexity of habitats and high diversity of plant and animal species, and therefore is considered a World Natural Heritage and Biosphere Reserves by Unesco [10].
Moreover, it is well known for its annual flood pulse, a river-plain interaction which affects the entire biota of the system [11]. For example, the natural eutrophication phenomenon locally called Decoada, which occurs during the beginning of the flood phase, causes a series of changes in water quality that are of great importance to the processes of decomposition and chemosynthesis [12].
Another important impact is the anthropogenic eutrophication, aggravated in wetlands by the annual floods [13,14], which harms the structure and dynamics of the communities of aquatic organisms [12]. The increase in nutrient concentration during the eutrophication process, drastically changes the microorganism biomass populations [15]. Robust conclusion of environmental condition may be drawn from the presence of bioindicators that have intense relationships with stressors, such as the diatoms [16]. Nevertheless, the interpretation of individual dominant taxa, needs to be addressed when making environmental inferences [17–19].
Diatoms are a group of silicified microalgae, considered as one of the most sensitive groups to environmental changes [20]. In the last decades, the study of diatom assemblages, linked to any single substratum, has received increasing attention [21–26], because it provides relevant information about the ecosystem stratification, allowing a correlation of ecological information with time and space [27–29], as well as the assessment of the ecological status of rivers, streams and lakes in temperate zones [30–32]. However, there is still an urgent need to expand the information to the wetland regions of the globe, where studies of diatom community are scarce [33,34]. So far, in South America, namely in Brazil, studies have focused on the planktonic and epilithic diatoms in rivers and streams, mainly related to the evaluation of water quality [35–37] and periphytic diatoms in floodplain [38]. Recent studies have focused on the role of eutrophication in environmental reorganization, with diatom assemblages and land-use records used as a tool to infer the trophic state history of the water body [39,40] as well as a record of biotic homogenization of diatom diversity in sedimentary samples [41]. Furthermore, some advances were also made in the auto-ecology of tropical species, the influence of environmental and spatial factors on diatom biodiversity, and its distribution [42,43].
In spite of these advances, there are a lack of studies on diatoms in surface sediment. Taxonomic studies contribute to the knowledge of biodiversity and provide the basis for the advancement of other approaches such as bioindication, environmental reconstruction, research on conservation and definition of priority areas such as the Pantanal, among many others. The more relevant works in the region are on the distribution of two species of diatoms and their association with the historical variation in water levels in the Paraná River [44]; the diatom flora in the Pantanal of Mato Grosso do Sul [45]; the history of the salinity in the southern Pantanal [46] and records of flood pulse dynamics [47]. Other studies, not related to diatoms, refer to the wetland carbon storage [48] and the influence that hydroclimatic variables exert on limnogeological processes [49]. However, the diatom biodiversity of this region remains understudied. This may be due to the difficulty of sampling in flooded areas as a result of a lack of suitable transportation through the wetland, as well as people specialized in diving in these areas. Thus, to better understand the biodiversity of diatoms in sediments of tropical wetland areas, the present study aimed to evaluate the influence of environmental factors on the distribution of these organisms in surface sediments in three different lakes of the Brazilian Pantanal (wetland) of Mato Grosso State. Our approach merges an assessment of diatom species with presence/absence and relative abundance data.
This study brings a contribution to the understanding of flooded tropical regions and intends to increase the knowledge of diatom biodiversity in Pantanal, using the structure and composition of species as a limnological bioindicator in tropical wetlands that are still poorly explored. Furthermore, the results of this study in the current context of the environmental destruction of Pantanal (fire/forest 2020) and the influence that it may have had on limnological processes, currently and also in the future, are extremely relevant to raise new comparative studies for the area, to help with decisions that may be of socioeconomic reasons, environmental management and also of biodiversity issues.
Materials and methods
Ethics statement
The Surface sediment and water samples were taken from public water bodies, no location was on protected or private land. No permits were required for the described study. The field sampling was done in accordance with Brazil national and regional regulations and permission was not necessary to collect the data. The field studies involved neither endangered nor protected species.
Study area
In this study, the surface sediments of three permanent lakes of the Pantanal of Mato Grosso were collected in 10 sites per lake (Table 1) and analysed for the diatom species present, as a bioindicator of the state of water quality.
The Pantanal is located on a 140,000 km2 plain in the tropical southwest of Brazil, bordering Bolivia and Paraguay, with coordinates 15° to 22° S and 55° to 58° W [50]. The flooded area, to the North and Northeast, is the source of the large rivers Paraguai, São Lourenço and Cuiabá, which are responsible for the flooding of the Pantanal North and for conditioning the floods along the North-South axis of the Paraguai river [12]. The predominant conditions in Pantanal determine a period of intense summer rain (November to March) with periods of high water and flooding, and other season the of dry (April to October) [51]. The average annual atmosphere temperature is around 25° C, ranging from a maximum of 34° C to a minimum of 15° C [52]. Average annual rainfall is 1400 mm, with a variation between 800 and 1600 mm, with 70% during the rainy season, November to March [53].
Characterization of the experimental sites
The three lakes studied were:
- Ferradura Lake (FP), located at 16°31’24” S and 56°23’40” W, with an average width of 300 m, an approximate extension of 1200 m, depth of 270–650 cm and connected to the Cuiabá river. Rainfall data (accumulated monthly) from five months prior to collection in the Ferradura lake region, weather station code: 1656002, see Table 2 [54].
- Burro Lake (BP), located at 17°45’46” S and 57°23’44” O, with an average width of 1000 m, an approximate extension of 5000 m, depth of 140–280 cm and connected to the São Lourenço river. Rainfall data (accumulated monthly) from five months prior to collection in the Burro lake region, weather station code: 1655001, see Table 2 [54].
- Caracará Lake (CP) located at 17°50’33” S and 57°27’52” O, has an average width of 3000 m with approximate extension of 3600 m, depth of 120–290 cm and connected to the Paraguai river. Rainfall data (accumulated monthly) from five months prior to collection in the Caracará lake region, weather station code: 1757001, see Table 2 [54].
In the literature it is found that the Cuiabá river is influenced by the discharge of sewage as well as by pisciculture that release their effluents containing high total N levels. Both São Lourenço and Paraguai rivers are influenced by agricultural, livestock activities as well as by heavy metals mainly by mercury, due to gold mining activities [12].
Sampling method and analysis of samples
Collection of superficial sediment (SS) was performed in February 2015. This month is considered to be representative due to high water from the flooding characteristic of summer rains. For the analysis of diatoms taxa ten samples of SS were collected with an Ekman dredger in the first 5.0 cm at the bottom of each lake, in the inflow, at the outflow, in the middle and in the marginal zone. Water samples were collected in polyethylene bottles on the sub-surface water of the lakes from the same 10 points for physical and chemical analysis. Both sample sets were kept under refrigeration for three days (2±0.5 °C).
Each sediment sample (0.5 g) was oxidized according to the standard method [55] using 35% H2O2 and 37% HCl. After the cleaning process, the slides (1 ml of the oxidized) were prepared with NAPHRAX, for qualitative and quantitative analysis of the different diatom taxa found. For the registration of the species (qualitative analysis) an image capture microscope (Zeiss Axioskop 2 plus), equipped with a digital camera (DC500) of high resolution, with a magnification of up to 1000 × was used.
For the identification of the species, at the lowest possible taxonomic level, classical ecological floras and new published data were used [56–63]. Counting of slides of 400 diatom valves (quantitative analysis) was performed to verify the relative density [28]. Diatom analysis was performed on species that achieved relative abundances ≥5% on at least one sampling station. Diatom species codes were assigned according to the Omnidia software [64].
Water temperature, pH, dissolved oxygen, turbidity (TU), conductivity, total dissolved solids (TDS), and depth were obtained with multiparameter probe (Horiba U50). Water total P and total N were determined according to Valderrama [65] and chlorophyll-a analysis followed Marker [66] method.
The water trophic state index was established according to Lamparelli [67], adopting values of trophic classification for lentic environment for chlorophyll-a and total P. Analysis of the TSI (Trophic State Index) is a measure of the potential of eutrophication, with P being the nutrient considered to be the causative agent.
N:P “Redfield ratio” was also determined. It is an important indicator in water bodies, indicating which nutrient is probably limiting productivity. Thus, the nutrient that will limit the growth of phytoplankton is the nutrient that reaches a minimum value before the other nutrients [68].
Statistical analysis
Differences between means were verified by ANOVA and the f-test, for both abiotic (physical-chemical) and biotic parameters (species frequency). Pearson’s linear analysis was also performed with species that presented abundance greater than 5%, as well as Pearson analysis to verify the correlation between its abiotic variables. Principal Component Analysis (PCA) was performed with the abiotic and also with biotic variables, the PCA allows you to identify patterns in the data and express them in such a way that their similarities and differences are highlighted.
In order to deal with multiple factors, biological (diatom distribution), chemical and physical variables, a multivariate statistical analysis was performed using canonical correspondence analysis (CCA). For the CCA analysis, only the biotic variables with abundances ≥5% and that showed autocorrelation (p <0.05, Pearson) were selected. For the abiotic variables, the conductivity and total dissolved solids variables were extracted, which are variables related to turbidity. The analysis was performed using the program XLstat 2018.1.01.
Results
Abiotic variables
Chemical and physical characterization of the lakes is presented in Table 3.
The three lakes showed high total N concentrations, according to CONAMA resolution for the protection of aquatic communities, with the maximum level in Ferradura lake. The high N concentrations in the water, compared to P, increased the N:P ratio at all points, with high mean values (Ferradura: 79:1, Burro: 63:1 and Caracará: 94:1), with the maximum value observed in Caracará (217:1), as evidenced by the low concentrations of total P (FP = 2.05; BP = 6.14; CP = 3.41 ug/L-1) and by the low chlorophyll-a concentration.
Pearson analysis showed that depth had a negative correlation with water temperature, pH, DO % and TSI, and the TU positive with the water temperature with the pH and DO % (Table 4).
PCA analysis using only the significant abiotic variables (Pearson), explained a total of 61.95% of the total variation in the two first axes.
The first axis (F1) recorded an explicability of 41.24%, with emphasis on total N and depth, with higher contributions of their negative scores, and greater positive contributions to the level of DO %, T °C, pH and TU. These contributions distinguished the Caracará and Ferradura lakes. In the Caracará lake, the higher water temperature were observed together with the higher values of the variables TU, DO % and pH, and concomitantly with the lower depth. In Ferradura lake the higher the depth and total N, the lower the values of TU, DO %, pH, and water temperature (Fig 1).
Depth collects; water temperature (T °C); hydrogenation potential (pH); Dissolved oxygen (DO%); Total Nitrogen for water (TN); Total phosphorus for water (TP) and Trophic State Index (TSI), Ferradura (FP) Burro (BP) and Caracará (CP).
The second axis (F2) recorded an explicability of 20.72%, with higher contributions of total P and higher trophic state, separating BP from the other two lakes. The Burro lake is shallow in depth, with the highest level of total P and consequently higher trophic level (Fig 1).
Index of Trophic Status
Index of Trophic Status was evaluated by the determination of chlorophyll-a, considered to be the response of the water body to the causative agent [69]. Therefore, the Ferradura lake presented an oligotrophic state and both the lakes, Burro and Caracará, presented a mesotrophic state, according to the Cetesb-TSI classification [69]. The three lakes did not present enrichment due to excess nutrients and they are between low and medium values of the acceptable parameters of the trophic state index (Fig 2).
Ferradura lake (FP) oligotrophic (47≤ TSI ≤ 52) minimum trophic level, Burro lake (BP) and Caracará lake (CP), both mesotrophic (52 ≤ TSI ≤ 59), medium trophic level.
Biotic variables
In the surface sediments of the three lakes, we found 119 taxa belonging to 31 genera, with greater richness of the genus Eunotia Ehrenberg (40 taxa) and greater abundance of Aulacoseira Thwaites. Moreover, 26 taxa were common to the three lakes. The Ferradura lake presented the greatest richness, with a total of 82 taxa, Caracará lake with 77 taxa and the Burro lake with 71 taxa. None of the taxa was dominant (+50%) and 25 showed abundance greater than 5% according to the relative density analysis (Table 5).
The values of the descriptive analysis of the 25 species of the lakes, FP, BP and CP are presented in Table 6, illustration in Fig 3. The greatest abundance in the Ferradura lake was for Aulacoseira italica (AITA). In the Burro lake, the species Eunotia transfuga (ETRA), Aulacoseira pusilla (AUPU) and A. veraluciae (AUVE), and in the Caracará lake, Eunotia desmogonioides (EDMG).
AEXG: Achnanthes exiguum; AAMB: Aulacoseira ambigua; AUGR: A. granulata; AUIT: A. italica; AUPU: A. pusilla; ASIM: A. simoniae; AUMI: A.minuscula; AUVE: A. veraluciae; ECUT: E. curtiraphe; EDID: E. didyma; EDMG: E. desmogonioides; EFOR: E. formica; ELGC: Eunotia longicamelus; EMET: E. metamonodon; EMON: E. monodon; EFLX: E. flexuosa; EPAP: E. papilio; EGUI: E. guianense; EPAN: E. pantropica; ETRA: E. transfuga; FBRA: Fragilariforma brasiliensis; PSYM: Placoneis symmetrica; SLCR: Staurosirella crassa; SLDB: S. dubia; SGOU: Synedra goulardii.
Of the most abundant species (> 5%), 21 presented significant correlation p <0.05, by Pearson correlation matrix (Table 7). Aulacoseira italica, A. granulata and A. veraluciae were the species with highest correlation with biotic variables. Among the species with significant correlation, 35% species had strong interactions, 46% species weak interactions and 15% moderate interactions, regarding the classification by Hinkle et al. [69].
PCA using only the significant biotic variables (Pearson) showed an explicability of 38.58% considering the first and second axes: The first axis (F1) registered an explicability of 23.45%, with emphasis for six mero-planktonic species of the Aulacoseira genus (AUVE, AUGR, AAMB, ASIM, AUMI, AUPU) and three periphytic species (EPAP, ETRA, FBRA) with higher contributions of their positive scores, and greater negative contributions for four periphytic species, three of the Eunotia genus (ECUT, EDMG, EPAN) and one Synedra (SGOU).
The second axis (F2) recorded an explicability of 15.13%, with emphasis for three periphytic species (EFLX, EMET, EMON) and one mero-planktonic species (AUIT), with higher contributions of their negative scores, and greater positive contributions to four periphytic species (AEXG, SLCR, SLDB, PSYM).
The positive scores of the first axis are driven primarily by planktonic species of the Aulacoseira genus, and the second axis is driven by periphytic species. The Burro lake presented greater richness of Aulacoseira species and Caracará and Ferradura lakes a richness of Eunotia species. The diatom sample scores of Principal Component Analysis (PCA) are shown in Fig 4.
Biotic and abiotic correlations
Chemical and physical variables analyzed in the lakes had no significant differences (p <0.05). However, some variables showed different patterns, which allowed distinguishing the three lakes. Pearson’s correlation between biotic and abiotic variables resulted in 14 species presenting statistical significance (p <0.05) to perform analysis by CCA (Table 8).
CCA presented an explicability of 86.13% considering the first two ordination axes. The species matrix was linearly related to the abiotic variables (pseudo-F = 2.37) (p = 0.05) (Fig 5).
Depth; water temperature (T °C); hydrogenation potential (pH); dissolved oxygen (DO%); total nitrogen (TN); total phosphorus (TP); trophic state index (TSI), Ferradura (FP) Burro (BP) and Caracará (CP).
The first axis (F1) recorded an explicability of 53.03% (auto-value = 0.479), with higher contribution of N and depth for their negative scores, and higher positive contributions to the level of TSI and phosphorus.
In the Burro lake, three species of Aulacoseira Thwaites (AAMB, AUGR, AUVE) and two Eunotia Ehrenberg species (EPAP, ETRA) were present in high abundances when the level of trophic state and phosphorus were also high, and the depth was low. However, on the other side of the axis, for Ferradura lake, the higher the concentration of N in the water, the greater the depth, and with lower level of trophic state, the higher was the contribution of diatom species AUIT, EFLX, EMET, EDID and EMON. Eunotia longicamelus occurred in the three lakes, but in greater abundance in places with lower phosphorus level (Fig 5 and species codes in Table 5).
The second axis (F2) recorded an explicability of 33.10% (auto-value = 0.318). The variables that contributed most to the positive scores for this axis were the higher water temperature, higher availability of DO % and pH around 7.
The combinations of levels of these abiotic variables differentiated the Caracará lake from the other two lakes, with the highest abiotic values for pH, water temperature and DO % and a higher development of the three periphytic species (EPAN, EDMG, SGOU).
Discussion
In terms of trophic conditions, the Ferradura lake is oligotrophic, while the lakes Burro and Caracará are mesotrophic, indicated by the highest concentration of phosphorus in both downstream lakes. Note that ours results, compared with data found in the literature to characterize the sites [12], seem not to support that the Cuiabá river is influenced by the discharge of sewage as well as by pisciculture that release their effluents.
However, according to studies by Yang et al. [70] available nutrients such as N and P seem to be the key point to control eutrophication and, under limiting conditions of one of the nutrients N or P, no significant increase in algae will occur in the water bodies. Some authors state that if the N:P ratio is greater than 10:1 [71] or 16:1 [72] P is acting as the limiting factor [73]. In the three lakes this was observed low total-P and also low chlorophyll-a concentration, but high concentration of N, in this case the P may be acting as a limiting factor. The higher level of N in the Ferradura lake, may be keeping the oligotrophy state for N:P ratio. The high N concentration in this lake comes from the discharge of effluent from fish farming tanks in the Cuiabá River [74].
The Burro lake presented the highest level of trophic conditions among the three lakes, but it is a lake with a lower depth, which receives greater discharge from the São Lourenço, a river impacted by gold mining activities [12]. This activity can compromise the quality and conservation of natural resources (water, soil, air) and affect the environment, primarily by using non-renewable resources and by altering the ecological balance. Analysed by Zeilhofer et al. [74] that studied the Northern Pantanal during the drought and flood phases and observed different phosphorus daily variation (1–4 t/day respectively) with higher P concentration in the São Lourenço river (0–5 t/day).
The three lakes did not present species dominance but, in general, Aulacoseira species had the greatest abundance and the Eunotia genus the greatest richness. Among the species with significant correlation, 35% of them had strong interactions and 46% had weak interactions regarding the classification by Hinkle et al. [75]. Poulin et al. [76] suggests that the difference in abundance between species is greater in communities characterized by weak interactions, while strong interactions may lead to greater evenness in the abundance of species. This was true for the three lakes that had a low uniformity and a higher percentage of weak interactions.
The Burro lake showed a greater richness of Aulacoseira species. These species can live part of their life cycle in benthic environments and with water turbulence, they re-suspend and increase their colonization capacity in the plankton [77,78]. Several studies have reported that Aulacoseira species excel in environments with a higher trophic level [33,79], occurring in the surface sediment with the highest abundance in eutrophic conditions [80] and increase their abundance in oligotrophic environments to mesotrophic [81].
Although the Aulacoseira has most of its species with a preference for a high concentration of total P, this characteristic may not be a general rule of the Aulacoseira genus. In this study Aulacoseira italica (Ehrenberg) Simonsen (AITA) presented a statistically significant relation for most of the abiotic variables, being negative for TSI and pH. Aulacoseira italica was found preferably in oligotrophic environments, cleaner or less turbid waters, or zones of low pollution. According to studies by Nakamoto et al. [82] Aulacoseira italica is more adapted to medium depth (maximum 12.0 m—mean 3.0 m), mild temperatures and scarce nutrients concentration. The species also has the characteristic to form spores and remains at rest in the sediment, like the other species of its genus [77,78] and returns to the surface if any event stimulates its growth [82]. Previous studies done in lake Broa, Brazil with similar environment characteristics to our study, the dominant species was Melosira italica (Ehrenberg) Kützing (= Aulacoseira italica (Ehr) Sim.) in the rainy summer period [82]. The identification consisted of spherical filaments typical of a resting cell (spore of resistance) as also verified in our study.
According to our studies the greater abundance of spores of A. italica was apparently due to rain events (Pantanal flooding) that increased nutrients dilution prior to sampling. With the conclusion of the rain period and in still waters, the spores may have increased in the sediment for the next event where the species resurfaces again. Pantanal is strongly related to the flood pulse, when autochthonous processes are a result of resuspension tactics in which sediments containing diatoms are made available in the pelagic environment [83]. Most of its records (A. italica spores) are still more common in fossil materials [84,85] and sites with some type of disturbance [86]. Siver and Kling [87] examined samples from 60 US and Canadian lakes for phytoplankton, surface sediment, and sediment from lower sections of gravity cores, and A. italica was more common in older sediment remains. Houk [88] and Genkal [89] report that Aulacoseira italica is a rare species in lakes and streams, but did not record the chemical parameters of the environment. However, in a study of plankton samples performed in the Iguaçu River, Brazil, Aulacoseira italica was an occasional taxon, occurring in only 1 out of 24 samples analysed during one year [90].
Although Aulacoseira italica occurred in the three lakes, the highest abundance (49.6) occurred in the Ferradura lake which presented the most acidic pH. The other two lakes presented much lower abundances (BP: 15.0 and CP: 11.8) and less acidic pH. Greater abundances of Aulacoseira italica was also observed in slightly acidic waters in other studies [83,91], and is reported to be a very rare species in alkaline waters [90]. The diatom flora associated with A. italica is also distinctive. The most commonly found genera include Eunotia, species essentially benthic and characteristic of a very different environment from the open water plankton of A. ambigua and A. granulata [77,92–94]. Ecology studies recorded in the "Catalogue of the main ecologic parameters of non-marine diatoms (in Portuguese)" [95], present a very extensive range of optimal developmental characteristics for the Aulacoseira italica, but some of these contradict current observations. This may be due to misidentification of Aulacoseira italica (AITA) with Aulacoseira valida (Grunow) Krammer (AVAL). When correctly identified A. italica is a valuable environmental indicator because it greatly differs from the habitat of other Aulacoseira taxa such as AUGR. The ecology of A. italica is not well known but clearly differs from the planktonic species [77].
Ferradura lake is oligotrophic and presented the greatest species richness, particularly of the Eunotia genus, due to higher acidity, depth and total N concentration. Studies carried out in the Amazon, Brazil, a variety of Eunotia species were found at pH values between 4.4 and 5.3, proving evidence that acid pH provides environmental conditions to develop a very particular diatom community dominated by specimens of Eunotiaceae [96]. Liu et al. [94] observed a great decrease of the number of Eunotia species between pH of 4.3 to 10.2 and temperature of 11°C to 22°C. The highest number of Eunotiaceae were found in a marsh with a pH of 4.3 to 6.5, with EPAP a rare species found only at pH 4.8. Compared to the low diversity of Eunotia (2 species) found by Santos et al. [45] for lakes in the Pantanal, with the majority of the lakes studied having alkaline waters, we can highlight that the highest occurrence of the genus in this study is actually due to more acidic environment.
It was observed that in wetland of the Pantanal of Mato Grosso, due to flooding and Decoada process, natural allochthonous and autochthonous material are deposited at the bottom of the lakes and this produces more acidic waters [12] that creates a friendly environment for Eunotia genus. The genus Eunotia prefers acidic environments so, both EPAP and ETRA are species usually found in wetlands, with an optimum pH development below seven. They live in still water, shallow lakes and high water temperatures (>30 °C) [95].
In sediment analysis by [97], it was reported that EMET and EMON species occurred together under oligotrophic conditions. The EFLX is also considered a rare species, but may present better development in swampy habitats, during summer, with pH-values ranging from 4,5 to 6,5 (acidophilus), being this its better characteristic [94,98].
The combinations of the higher water temperature, higher availability of % DO, pH around 7 and lower depth, separated the Caracará lake from the other two lakes and with higher development of three periphytic species (EPAN, EDMG, SGOU). Most species of the genus Eunotia are described as acidophilic with development in acidic water [99]. Eunotia pantropica Glushchenko, Kulikovskiy & Kociolek (EPAN = E. rabenhorstiana var elongate (R.M.Patrick) Metzeltin & Lange-Bertalot) is a species that develops at pH < 7, with its optimum below pH 5.5, as well as in water rich in humic substances and temperatures above 30 °C [92].
Although in the Caracará lake the pH variation was between 5.9–6.8, the highest development of this species (EPAN) occurred in this lake in a site with pH variation between 6.4–6.8. Probably the low depth, high light availability and high water temperature of Caracará lake favoured the higher abundance of the species (59%) compared to the other two lakes (BP: 20.63% and FP: 20.34%). Besides the higher water temperature, the Caracará lake presented higher concentration of humic substances, and higher DO concentration. Eunotia desmogonioides (EDMG) is also a species that equals the ecology of EPAN, described above. In sediment studies by Faustino et al. [97] the same was observed in 23% of the samples under oligotrophic conditions. In other studies, the same occurred in oligo-mesotrophic waters, slightly acidic to neutral, characterizing the bio-indication of this species [100].
The third species with the greatest development in Caracará lake is Synedra goulardii (SGOU), an alkaliphilic epileptic species with an optimum development at pH around 7 [101]. In studies conducted by Nardelli et al. [102] this species also occurred at pH around 7 and in an environment of greater transparency and high availability of DO. It could be characterized that this species has a better development in waters with high concentration of DO.
Diatoms seemed to be a good bioindicator to evaluate the quality of water in the lakes studied. Diatom communities have been recommended by researchers in many countries as appropriate to the evaluation of water quality [103–108]. Several studies present a broad discussion about the use of diatoms, considering sensitivity especially to pH, conductivity, nutrient concentration, organic matter and dissolved oxygen [32,35–37,109–113]. Complementing, surface sediment diatoms are robust indicators of environmental conditions, strongly associated with environmental factors, probably because they integrate information in space and time [114].
In summary the three lakes showed a high diatom diversity, with numerous populations of Eunotia and Aulacoseira genera. The wetlands often presented low pH which provides environmental conditions to develop the Eunotia genus. This was true in the Ferradura lake with more acidic environment. However, Aulacoseira genus, with three species (AAMB, AUGR, AUVE), characterised the environment towards trophic level increase. This was observed in the Burro and Caracará lakes that had a mesotrophic environment and with the mentioned species above as the most abundant. These species were a good indicator of trophic levels. On the other hand, A. italica was the most important species under oligotrophic environment in the lake Ferradura, with more acidic environment.
Despite the greater abundance of Eunotia and Aulacoseira, in different situations, there were no dominance species in the three lakes. This means that optimal conditions for the development of these species were not present, although favourable conditions promoted an increase in their populations. Lakes characteristics, slightly acidic water and oligotrophic to mesotrophic conditions, justified the diversity of diatom species group found in the sediments analysed (Eunotia—slightly acidic water and Aulacoseira—trophic condition), showing that diatoms are a good bioindicator, due to their sensitivity to physical and chemical variations in the environment. The species group have shown to be dependent on the concentration but also on the combination of physical and chemical parameters, that determine variations in the size of their populations.
Although the analysis of the average physical and chemical parameters in the water did not show significant differences among the three lakes, the combination of these parameters determined biotic differences in the lakes. Due to the richness found and the fact that we did not find teratological frustules, it can be inferred that the anthropogenic disturbances were still small in these three lakes. We hypothesize that the material accumulated downstream of the rivers also accumulated in the lakes and the diversity decreases due to mesotrophic conditions, however the differences between the lakes were still not extreme, as seen by biotic and abiotic conditions. Thus, the set of this information indicates that the studied environments of the Pantanal presented good ecological conditions from a naturally oligotrophic to mesotrophic environment. However, the results of this study in the context of the environmental destruction that the Pantanal underwent (fire/forest 2020) and the influence that it may have had on limnological processes, is of extremely relevance to raise new comparative studies for the area.
Acknowledgments
We thank the Gerpel/Unioeste (Grupo de Pesquisas em Recursos Pesqueiros e Limnologia) for providing us with the Chlorophyll-a and total P chemical analysis of water samples. We thank the divers, 6th Naval District of the Brazilian Navy, for the logistic support in the accomplishment of the collection of sediment, and Dr. Marcelo Bevilacqua Remor for supporting the sampling the water.
References
- 1. Brönmark C, Hansson L-A. Environmental issues in lakes and ponds: current state and perspectives. Environmental Conservation. 2002;29: 290–306.
- 2. Smol JP, Wolfe AP, Birks HJB, Douglas MS V., Jones VJ, Korhola A, et al. Climate-driven regime shifts in the biological communities of arctic lakes. Proceedings of the National Academy of Sciences. 2005;102: 4397–4402. pmid:15738395
- 3. Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, et al. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews. 2006;81: 163. pmid:16336747
- 4. Bozelli RL, Caliman A, Guariento RD, Carneiro LS, Santangelo JM, Figueiredo-Barros MP, et al. Interactive effects of environmental variability and human impacts on the long-term dynamics of an Amazonian floodplain lake and a South Atlantic coastal lagoon. Limnologica. 2009;39: 306–313.
- 5. Battarbee RW, Anderson NJ, Bennion H, Simpson GL. Combining limnological and palaeolimnological data to disentangle the effects of nutrient pollution and climate change on lake ecosystems: Problems and potential. Freshwater Biology. 2012.
- 6. Barinova S. On the Classification of Water Quality from an Ecological Point of View. International Journal of Environmental Sciences & Natural Resources. 2017;2: 1–8.
- 7. Anderson D, Glibert P, Burkholder J. Harmful algal blooms and eutrophication: nutrient sources, compositions, and consequences. Estuaries. 2002;25: 704–726. pmid:19956363
- 8. Schindler DE, Scheuerell MD. Habitat coupling in lake ecosystems. Oikos. 2002;98: 177–189.
- 9. Preston SD, Alexander RB, Schwarz GE, Crawford CG. Factors Affecting Stream Nutrient Loads: A Synthesis of Regional SPARROW Model Results for the Continental United States. Journal of the American Water Resources Association. 2011;47: 891–915. pmid:22457574
- 10.
Embrapa P. Programação de Pesquisa da Embrapa Pantanal 2006/2007. Corumbá, MS: Embrapa Pantanal; 2007 p. 57.
- 11.
Pantanal MT. Bacia do Alto Paraguai Cobertura Vegetal: Monitoramento das alterações da cobertura vegetal e uso do solo na Bacia do Alto Paraguai. Periodo de análise: 2002 a 2008. 2002nd–200 8th ed. Geralda Magela (WWF-Brasil) Mirella Domenich (CI-Brasil), editor. Brasil: Baita Desing; 2009. http://d3nehc6yl9qzo4.cloudfront.net/downloads/monitoramento_bap_2010_2012.pdf.
- 12.
Tabarelli M, Rocha CFD da, Romanowski HP, Rocha O, Lacerda LD de. PELD–CNPq Dez Anos do Programa de Pesquisas Ecológicas de Longa Duração no Brasil: Achados, Lições e Perspectivas. Tabarelli M, Rocha CFD da, Romanowski HP, Rocha O, Lacerda LD de, editors. Editora Universitária UFPE. 2013.
- 13. Hupp CR. Hydrology, geomorphology and vegetation of costal plain rivers in the south-eastern USA. Hydrological Processes. 2000;14: 2991–3010.
- 14.
Souza CA de, Souza JB de. Pantanal Mato-Grossense: Origem, Evolução e as Características Atuais. Revista Eletrônica da Associação dos Geógrafos Brasileiros. 2010; 34–54.
- 15. Dodds WK. Eutrophication and trophic state in rivers and streams. Limnology and Oceanography. 2006;51: 671–680.
- 16. Göthe E, Angeler DG, Gottschalk S, Löfgren S, Sandin L. The Influence of Environmental, Biotic and Spatial Factors on Diatom Metacommunity Structure in Swedish Headwater Streams. PLoS ONE. 2013;8: 1–9. pmid:23967290
- 17. Reavie ED, Cai M. Consideration of species-specific diatom indicators of anthropogenic stress in the Great Lakes. PLoS ONE. 2019;14: 1–15. pmid:31048847
- 18. Algarte VM, Siqueira T, Landeiro VL, Rodrigues L, Bonecker CC, Rodrigues LC, et al. Main predictors of periphyton species richness depend on adherence strategy and cell size. PLoS ONE. 2017;12: 1–14. pmid:28742122
- 19. Wetzel CE, Bicudo DC, Ector L, Lobo EA, Soininen J, Landeiro VL, et al. Distance Decay of Similarity in Neotropical Diatom Communities. PLoS ONE. 2012;7: 10–11. pmid:23028767
- 20.
Smol JP, Stoermer EF. The Diatoms: Applications for the Environmental and Earth Sciences. 2nd ed. Smol JP, Stoermer EF, editors. Cambridge, UK: University Press Cambridge; 2010.
- 21. Bennion H, Appleby PG, Phillips GL. Reconstructing nutrient histories in the Norfolk Broads, UK: implications for the role of diatom-total phosphorus transfer functions in shallow lake management. Journal of Paleolimnology. 2001;26: 181–204.
- 22. Bradbury JP, Colman SM, Reynolds RL. The history of recent limnological changes and human impact on Upper Klamath Lake, Oregon. Journal of Paleolimnology. 2004;31.
- 23. Della Bella V, Puccinelli C, Marcheggiani S, Mancini L. Benthic diatom communities and their relationship to water chemistry in wetlands of central Italy. Ann Limnol. 2007;43: 89–99.
- 24. Reid M. Diatom-based models for reconstructing past water quality and productivity in New Zealand lakes. Journal of Paleolimnology. 2005;33: 13–38.
- 25. Perez L, Brugnoli E, Muniz P, Sunesen I, Sar EA, Crisci C, et al. Diatom assemblages from surface sediments of the Río de la Plata estuary, Uruguay. New Zealand Journal of Marine and Freshwater Research. 2017;8330: 1–15.
- 26. Riato L, Della Bella V, Leira M, Taylor JC, Oberholster PJ. A diatom functional-based approach to assess changing environmental conditions in temporary depressional wetlands. Ecological Indicators. 2017;78: 205–213.
- 27. Bennion H. Surface-sediment diatom assemblages in shallow, artificial, enriched ponds, and implications for reconstructing trophic status. Diatom Research. 1995;10: 1–19.
- 28.
Smol JP. Pollution of lakes and rivers: a paleoenvironmental perspective. 2nd ed. Smol J, editor. Blackwell Publishing. Hong Kong: Blackwell Publishing; 2008.
- 29. Gregory-Eaves I, Beisner BE. Palaeolimnological insights for biodiversity science: An emerging field. Freshwater Biology. 2011;56: 2653–2661.
- 30. Soininen J, Paavola R, Muotka T. Benthic diatom communities in boreal streams: Community structure in relation to environmental and spatial gradients. Ecography. 2004;27: 330–342.
- 31. Potapova M, Charles DF. Diatom metrics for monitoring eutrophication in rivers of the United States. Ecological Indicators. 2007;7: 48–70.
- 32. Blanco S, Cejudo-Figueiras C, Álvarez-Blanco I, van Donk E, Gross EM, Hansson LA, et al. Epiphytic diatoms along environmental gradients in Western European shallow lakes. Clean—Soil, Air, Water. 2014;42: 229–235.
- 33. Dong X, Bennion H, Battarbee R, Yang X, Yang H, Liu E. Tracking eutrophication in Taihu Lake using the diatom record: Potential and problems. Journal of Paleolimnology. 2008;40: 413–429.
- 34. Stoof-Leichsenring KR, Junginger A, Olaka LA, Tiedemann R, Trauth MH. Environmental variability in Lake Naivasha, Kenya, over the last two centuries. Journal of Paleolimnology. 2011;45: 353–367.
- 35. Lobo EA, Callegaro V, Hermany G, Bes D, Wetzel C, Oliveira MA. Use of epilithic diatoms as bioindicators from lotic systems in southern Brazil, with special emphasis on eutrophication. Limnology. 2004;16: 25–40.
- 36. Salomoni SE, Rocha O, Callegaro VL, Lobo EA. Epilithic diatoms as indicators of water quality in the Gravataí river, Rio Grande do Sul, Brazil. Hydrobiologia. 2006;559: 233–246.
- 37. Bere T, Tundisi JG. The effects of substrate type on diatom-based multivariate water quality assessment in a tropical river (Monjolinho), São Carlos, SP, Brazil. Water, Air, and Soil Pollution. 2011;216: 391–409.
- 38. Ruwer DT, Rodrigues L. Subfossil and periphytic diatoms from the upper Paraná river, Brazil: last ~ 1000 years of a transition period 1. 2018;45: 1–19.
- 39. Costa-Böddeker S, Bennion H, de Jesus TA, Albuquerque ALS, Figueira RCL, de C. Bicudo D. Paleolimnologically inferred eutrophication of a shallow, tropical, urban reservoir in southeast Brazil. Journal of Paleolimnology. 2012;48: 751–766.
- 40. Fontana L, Albuquerque ALS, Brenner M, Bonotto DM, Sabaris TPP, Pires MAF, et al. The eutrophication history of a tropical water supply reservoir in Brazil. Journal of Paleolimnology. 2014;51: 29–43.
- 41. Wengrat S, Padial AA, Jeppesen E, Davidson TA, Fontana L, Costa-Böddeker S, et al. Paleolimnological records reveal biotic homogenization driven by eutrophication in tropical reservoirs. Journal of Paleolimnology. 2017; 1–11.
- 42. Zorzal-Almeida S, Soininen J, Bini LM, Bicudo DC. Local environment and connectivity are the main drivers of diatom species composition and trait variation in a set of tropical reservoirs. Freshwater Biology. 2017;62: 1551–1563.
- 43. Zorzal-Almeida S, Bini LM, Bicudo DC. Beta diversity of diatoms is driven by environmental heterogeneity, spatial extent and productivity. Hydrobiologia. 2017;800: 7–16.
- 44. Ruwer DT, Rodrigues L. Abundance of Diadesmis confervacea Kützing and Eunotia camelus Ehrenberg indicates the historical water level variation in a marsh. Brazilian Journal of Botany. 2018;4.
- 45. de S Santos KR, da Rocha ACR, Sant’Anna CL. Diatoms From Shallow Lakes in the Pantanal of Nhecolândia, Brazilian Wetland. Oecologia Australis. 2012;16: 756–769.
- 46. Guerreiro RL, McGlue MM, Stone JR, Bergier I, Parolin M, da Silva Caminha SAF, et al. Paleoecology explains Holocene chemical changes in lakes of the Nhecolândia (Pantanal-Brazil). Hydrobiologia. 2018;815.
- 47. McGlue MM, Silva A, Zani H, Corradini FA, Parolin M, Abel EJ, et al. Lacustrine records of Holocene flood pulse dynamics in the Upper Paraguay River watershed (Pantanal wetlands, Brazil). Quaternary Research (United States). 2012;78: 285–294.
- 48. Rasbold GG, McGlue MM, Stevaux JC, Parolin M, Silva A, Bergier I. Enhanced middle Holocene organic carbon burial in tropical floodplain lakes of the Pantanal (South America). Journal of Paleolimnology. 2021;65: 181–199.
- 49. McGlue MM, Silva A, Corradini FA, Zani H, Trees MA, Ellis GS, et al. Limnogeology in Brazil’s “forgotten wilderness”: A synthesis from the large floodplain lakes of the Pantanal. Journal of Paleolimnology. 2011;46: 273–289.
- 50. Cunha CN da Junk WJ. Year-to-year changes in water level drive the invasion of Vochysia divergens in Pantanal grasslands. Applied Vegetation Science. 2004;7: 103–110.
- 51. Clarke RT, Tucci CEM, Collischonn W. Variabilidade Temporal no Regime Hidrológico da Bacia do Rio Paraguai. Revista Brasileira de Recursos Hídricos. 2003;8: 201–211.
- 52. Viana DR, Alvalá RC dos S. Vegetation Index Performance for the Pantanal Region During Both Dry and Rainy Seasons. Geografia. 2011;36: 143–158.
- 53. Andrade RG, Sediyama GC, da Paz AR, Lima E de P, Facco AG. Geotecnologias aplicadas á avaliação de parǎmetros biofísicos do Pantanal. Pesquisa Agropecuaria Brasileira. 2012;47: 1227–1234.
- 54.
ANA. Agência Nacional das águas. 2017.
- 55.
Battarbee RW, Jones VJ, Birks HJB, Last WM. Diatom. 3rd ed. In: Smol J. P., Birks HJB, Last W., editors. Rastreando Mudança Ambiental Usando Sedimentos Lake. 3rd ed. Dordrecht: Kluwer Academic Publishers; 2001. pp. 155–202.
- 56.
Hustedt F. Bacillariophyta (Diatomeae). 10th ed. Pascher A, editor. Jena: Verlag von Gustav Fischer; 1930.
- 57.
Krammer K, Lange-Bertalot H. Bacillariophyceae: Centrales, Fragilariaceae, Eunotiaceae. In: Süsswasser-Flora von Mitteleuropa. 3rd ed. Ettl H, Gerlloff I, Heynig H, Mollenhauer D, editors. Stuttgart: Jena, G. Fischer; 1991. http://www.scielo.br/scielo.php?script=sci_nlinks&ref=000254&pid=S0102-3306201000040001500034&lng=en.
- 58.
Metzeltin D, Lange-Bertalot H. Tropical Diatoms of South America I Tropische Diatomeen in Südamerika I. 700 überwiegend wenig bekannte oder neue Taxa repräsentativ als Elemente der neotropischen Flora. 5th ed. Metzeltin D, Lange-Bertalot H, editors. Iconographia Diatomologica 5. Germany: Lubrecht & Cramer Ltd; 1998.
- 59.
Krammer K. The genus Pinnularia Diatoms of Inland Waters and Comparable Habitats. 1st ed. Krammer K, editor. Europa: Diatoms of Europa; 2000. http://www.scielo.br/scielo.php?script=sci_nlinks&ref=000242&pid=S0102-3306201000040001500028&lng=en.
- 60.
Rumrich U, Lange-Bertalot H, Rumrich M. Diatomeen der Anden. Von Venezuela bis Patagonien/Feuerland. Iconographia Diatomologica, Vol. 9. 2000.
- 61.
Metzeltin D, Lange-Bertalot H, García-Rodríguez F. of Uruguay compared with other taxa from South America and elsewhere. In Iconographia Diatomologica, Annotated Diatom Monographs. 1st ed. Lange-Bertalot H, editor. Iconographia Diatomologica 15. Berlin: Gantner Verlag K.G.; 2005.
- 62.
Lange-Bertalot H, Bak M, Witkowski A. Eunotia and some related genera. 6th ed. Lange-Bertalot H, editor. Diatoms of Europe. Diatoms of the European Inland Waters and Comparable Habitats. Germany: Königstein, Koeltz Scientific Books; 2011.
- 63.
Costa LF, Wetzel CE, Lange-Bertalot H, Ector L, Bicudo DC. Taxonomy and Ecology of Eunotia Species (Bacillariophyta) in Southeastern Brazilian Reservoirs. Bibliothec. Costa LF, Wetzel CE, Lange-Bertalot H, Ector L, Bicudo DC, editors. Schweizerbart Science Publishers; 2017.
- 64. Lecointe C, Coste M, Prygiel J. “Omnidia”: software for taxonomy, calculation of diatom indices and inventories management. Hydrobiologia. 1993;269–270: 509–513.
- 65. Valderrama JC. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry. 1981;10: 109–122.
- 66.
Marker AFH. Chlorophyll a SCA Method Revision. 1st ed. Bristol: National Rivers Authority; 1994.
- 67.
Lamparelli MC. “Graus de trofia em corpos d’água do estado de São Paulo: avaliação dos métodos de monitoramento.” Universidade de São Paulo. 2004.
- 68.
Chapra SC. Surface Water-Quality Modeling. 1st ed. Chapra SC, editor. Long Grove, Illinois: Waveland Press, INC.; 1997.
- 69.
Cetesb. Qualidade das Águas Interiores no Estado de Sao Paulo 2016. São Paulo: Cetesb; 2017.
- 70. Yang X, Wu X, Hao H, He Z. Mechanisms and assessment of water eutrophication. Journal of Zhejiang University SCIENCE B. 2008;9: 197–209. pmid:18357622
- 71. Kratzer CR, Brezonik PL. Carlson-Type Trophic State Index for Nitrogen in Florida Lakes. Journal of the American Water Resources Association. 1981;17: 713–715.
- 72.
Redfield AC, Ketchum BH, Richards FA. The Influence of Organisms on the Composition of Sea Water. 1st ed. The sea: ideas and observations on progress in the study of the seas. Washington; 1963.
- 73. Hodgkiss IJ, Lu S. The effects of nutrients and their ratios on phytoplankton abundance in Junk Bay, Hong Kong. Hydrobiologia. 2004;512: 215–229.
- 74. Zeilhofer P, Lima EBNR, Lima GAR. Spatial patterns of water quality in the cuiabá River Basin, Central Brazil. Environmental Monitoring and Assessment. 2006;123: 41–62. pmid:17089078
- 75.
Hinkle DE, Wiersma W, Jurs SG. Rule of Thumb for Interpreting the Size of a Correlation Coefficient. 5th ed. Applied Statistics for the Behavioral Sciences. Boston; 2003.
- 76. Poulin R, Luque JL, Guilhaumon F, Mouillot D. Species abundance distributions and numerical dominance in gastrointestinal helminth communities of fish hosts. Journal of Helminthology. 2008;82: 193–202. pmid:18544177
- 77. Crawford RM, Likhoshway YV, Jahn R. Morphology and Identity of Aulacoseira Italica and Typification of Aulacoseira (Bacillariophyta). Diatom Research. 2003;18: 1–1.
- 78. Becker V, Motta-Marques D. Water dynamics, phytoplankton biomass and size structure of a shallow freshwater subtropical lake (Itapeva lake, south of Brazil). Acta Limnol Bras. 2004;16: 163–174.
- 79. Taylor D, Dalton C, Leira M, Jordan P, Chen G, León-Vintró L, et al. Recent histories of six productive lakes in the Irish Ecoregion based on multiproxy palaeolimnological evidence. Hydrobiologia. 2006;571: 237–259.
- 80. Bartozek ECR, Zorzal-Almeida S, Bicudo DC. Surface sediment and phytoplankton diatoms across a trophic gradient in tropical reservoirs: new records for Brazil and São Paulo State. Hoehnea. 2018;45: 69–92.
- 81. Nardelli MS, Bueno NC, Ludwig TAV, Guimarães ATB. Structure and dynamics of the planktonic diatom community in the Iguassu River, Paraná State, Brazil. Brazilian Journal of Biology. 2016;76. pmid:26934158
- 82. Nakamoto N, Marins MA, Tundisi JG. Synchronous growth of a freshwater diatom Melosira italica under natural environment. Oecologia. 1976;23: 179–184. pmid:28308924
- 83. Loverde-Oliveira SM, Huszar VLM. Phytoplankton ecological responses to the flood pulse in a Pantanal lake, Central Brazil. Acta Limnologica Brasiliensia. 2007;19: 117–130. Available: http://ablimno.org.br/acta/pdf/acta19_vol2_01.pdf.
- 84. Yang J-R, Dickman M. Diatoms as Indicators of Lake Trophic Status in Central Ontario, Canada. Diatom Research. 1993;8: 179–193.
- 85. Eberle ME. Recent Diatoms Reported from the Central United States: Register of Taxa and Synonyms. Biology Faculty Papers. 2016;5: 1–91.
- 86.
Potapova BM, Carlisle DM. Development and application of indices to assess the condition of benthic algal communities in U.S. streams and riverss: U.S. Geological Survey Open File Report 2011–1126. US Geological Survey. 2011.
- 87. Siver PA, Kling H. Morphological observations of Aulacoseira using scanning electron microscopy. Canadian Journal of Botany—Revue Canadienne de Botanique. 1997;75: 1807–1835.
- 88.
Houk V. Atlas of freshwater centric diatoms with a brief key and descriptions. Part I. Melosiraceae, Orthoseiraceae, Paraliaceae and Aulacoseiraceae. 1st ed. Poulícková A, editor. Czech Republic: Olomouc; 2003.
- 89. Genkal SI. Aulacoseira italica, A. valida, A. subarctica and A. volgensis Sp. nov. (Bacillariophyta) in the waters of Russia. Bot Xyph. 2017;84: 40–49.
- 90. Nardelli MS, Bueno NC, Ludwig TAV, Tremarin PI, Bartozek ECR. Coscinodiscophyceae and Fragilariophyceae (Diatomeae) in the Iguaçu River, Paraná, Brazil. Acta Botanica Brasilica. 2014;28: 127–140.
- 91. Rodrigues L. Contribuição ao Connhecimento das Diatómaceas, Do Rio Tubarão—Santa Catarina—Brasil. ÍNSULA. 1984;14: 47–120.
- 92. Whitmore TJ. Florida diatom assemblages as indicators of trophic state and pH. Limnology and Oceanography. 1989;34: 882–895.
- 93. Van Dam H, Mertens A, Sinkeldam J. A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands. Netherlands Journal of Aquatic Ecology. 1994;28: 117–133.
- 94. Liu Y, Wang Q, Fu C. Taxonomy and distribution of diatoms in the genus Eunotia from the Da’erbin Lake and Surrounding Bogs in the Great Xing’an Mountains, China. Nova Hedwigia. 2011;92: 205–232.
- 95.
Moro RS, Furstenberger CB. Catálogo dos principais parâmetros ecológicos de diatomáceas não-marinhas. II. Moro RS, Furstenberger CB, editors. Ponta Grossa, PR, BR: UEPG-Universidade Estadual de Ponta Grossa; 1997.
- 96. Ferrari F, Procopiak LK, Alencar YB, Ludwig TAV. Eunotiaceae (Bacillariophyceae) em igarapés da Amazônia Central, Manaus e Presidente Figueiredo, Brasil. Acta Amazonica. 2007;37: 1–16.
- 97. Faustino SB, Fontana L, Bartozek ECR, Bicudo MCE, Bicudo DC. Composition and distribution of diatom assemblages from core and surface sediments of a water supply reservoir in Southeastern Brazil. Biota Neotropica. 2016;16: 1–23.
- 98. Kim YS, Choi JS, Kim HS. Epiphytic diatom communities from two mountain bogs in South Korea. Nova Hedwigia. 2007;84: 363–379.
- 99.
Round FE, Crawford RM, Mann DG. The diatoms. 4th ed. Round FE, Crawford RM, Mann DG, editors. Cambridge, UK: Cambridge University Press; 2007.
- 100. Marra RC, Tremarin PI, Algarte VM, Ludwig TV. Epiphytic diatoms (Diatomeae) from Piraquara II urban reservoir, Paraná state. Biota Neotropica. 2016;16: 1–20.
- 101. Sumita M, Watanabe T. New General Estimation Community of River Pollution Using New Diatom as Biological Indicators Based on Index (NDCI) Specific Composition of Epilithic Diatoms Communities, Applied to Asano-gawa and Sai-gawa Rivers in at each station were shown in Tables. Jap J Limnology. 1983;44: 329–340.
- 102. Nardelli MS, Bueno NC, Ludwig TAV, Guimarães ATB. Structure and dynamics of the planktonic diatom community in the Iguassu River, Paraná State, Brazil. Braz J Biol. 2016;76: 374–386. pmid:26934158
- 103.
Magurran AE. Ecological Diversity and Its Measurement. Princeton University Press. Dordrecht: Springer Netherlands; 1988.
- 104. Kazuhiro K. Spatial and Seasonal Variation oi Diatom Assemblages Composition in a Partly Polluted River. Japanese Journal of Limnology (Rikusuigaku Zasshi). 1991;52: 229–239.
- 105. Lobo EA, Callegaro VLM, Wetzel CE, Hermany G, Bes D. Water quality study of the Condor and Capivara streams, Porto Alegre municipal district, RS, Brazil, using epilithic diatom biocenoses as bioindicators. Oceanological and Hydrobiological Studies. 2004;33: 77–93.
- 106. Beyene A, Addis T, Kifle D, Legesse W, Kloos H, Triest L. Comparative study of diatoms and macroinvertebrates as indicators of severe water pollution: Case study of the Kebena and Akaki rivers in Addis Ababa, Ethiopia. Ecological Indicators. 2009;9: 381–392.
- 107. La Hée JM, Gaiser EE. Benthic diatom assemblages as indicators of water quality in the Everglades and three tropical karstic wetlands. Freshwater Science. 2012;31: 205–221.
- 108.
Lobo EA. O Perifíton como Indicador da Qualidade da Água. 1st ed. In: A , Schwarzbold A, Burliga AL, Torgan LC, editors. Ecologia do Perifíton. 1st ed. São Carlos, SP: Rima; 2013. pp. 205–235.
- 109. Eloranta P, Soininen J. Ecological status of some Finnish rivers evaluated using benthic diatom communities. Journal of Applied Phycology. 2002;14: 1–7.
- 110. Levkov Z, Blanco S, Krstic S, Nakov T, Ector L. Ecology of benthic diatoms from Lake Macro Prespa (Macedonia). Algological Studies. 2007;124: 71–83.
- 111. Faria DM De Tremarin PI, Alvim T, Ludwig V, Alegre P. Diatomáceas perifíticas da represa Itaqui, São José dos Pinhais, Paraná: Fragilariales, Eunotiales, Achnanthales e Gomphonema Ehrenberg Introdução Resultados e Discussão. Biota Neotropica. 2010;10: 415–427. Available: http://www.biotaneotropica.org.br/v10n3/pt/abstract?inventory+bn04110032010.
- 112. Canani LGDC, Menezes M, Torgan LC. Diatomáceas Epilíticas de Águas Oligotróificas e Ácidas do Sudeste do Brasil. Acta Botanica Brasilica. 2011;25: 130–140.
- 113. Bes D, Ector L, Torgan LLC, Lobo EEA. Composition of the epilithic diatom flora from a subtropical river, southern Brazil. IHERINGIA, Sér Bot, Porto Alegre. 2012;67: 93–125. Available: http://www.vliz.be/imis/imis.php?module=ref&refid=218278.
- 114. Bartozek ECR, Silva-lehmkuhl AM, Gregory-eaves I, Bicudo DC. Environmental and spatial drivers of diatom assemblages in the water column and surface sediment of tropical reservoirs. Journal of Paleolimnology. 2019;3: 1–14.