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All issues Volume 58 (2022) Int. J. Lim., 58 (2022) 6 Full HTML
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Issue
Int. J. Lim.
Volume 58, 2022
Article Number 6
Number of page(s) 10
DOI https://doi.org/10.1051/limn/2022006
Published online 03 June 2022

© EDP Sciences, 2022

1 Introduction

Understanding the distribution and abundance of species, how they vary on spatial and temporal scales and the factors that control them are central points in ecological research (Langenheder et al., 2012). Therefore, studies of diversity in aquatic environments help to understand the functioning of the system, considering that this ecological knowledge covers the interaction of aquatic organisms with the physical and chemical environment (Callisto et al., 2001; Hodkinson and Jackson, 2005; Moretto et al., 2013).

Beta diversity (β) is one of the most widely used means of evaluating species changes in an environmental gradient (β-spatial) or the same environment over time (β-temporal) (Magurran, 2004), and it provides an interesting perspective with regard to knowledge of areas to be preserved (Ward et al., 1999). In the case of β-temporal diversity, it can be defined as the change in identities and/or the abundance of named taxa in a specified community at two or more points in time (Magurran et al., 2019). It has been widely used to track changes attributed to the composition of species and, most of the time, efficiently reflects the ecological processes and ecosystem functions that are involved (Magurran et al., 2019), especially where intense anthropic pressures are currently causing consistent damage to natural ecosystems (Bonecker et al., 2013).

In recent years, the middle Iguaçu region has gone through a very intense process of occupation of floodplains and areas with springs, causing a number of impacts. Occupation affects water supply systems, sewage treatment and urban drainage systems, which do not keep up with the striking growth of cities (Suderhsa, 2000), negatively affecting the environment and the quality of life of people (Bueno-Krawczyk et al., 2015). Many studies have been carried out in this region, taking into consideration pollution gradients and how these affect aquatic communities (Bueno-Krawczyk et al., 2015; Melo-Silva et al., 2018; Lehun et al., 2020, 2021). Research has demonstrated that, in addition to organic pollution, high levels of pollution from heavy metals (Melo-Silva et al., 2018) phenols (Lehun et al., 2020) and caffeine (Bueno-Krawczyk et al., 2015) are present in this region.

Several living organisms have been used in the biomonitoring of polluted environments, because they respond effectively to environmental changes (Alba-Tercedor, 1996) and provide important information on the health of aquatic ecosystems (Bunzel et al., 2013). Among these, the community of benthic invertebrates is the most widespread (Hellawell, 1986), because they respond quickly to changes in the biological quality and ecological status of the environments in which they live or are released (Bunzel et al., 2013). They are even used in the evaluation of contamination by pesticides coming from agricultural regions and wastewater treatment stations (Bunzel et al., 2013; Burdon et al., 2019).

The community of benthic invertebrates is represented mainly by the phyla Arthropoda, Mollusca, Nematoda, Platyhelminthes and Annelida (Hauer and Resh, 1996; Ribeiro and Uieda, 2005), the last of which constitutes the largest part of total biota in lentic and lotic systems. Of these, Oligochaeta is the subclass with the most abundant and representative species in diversity inventories (Martin et al., 2008; Krawczyk et al., 2013; Abubakr et al., 2018).

Oligochaeta inhabit a variety of aquatic environments, such as wetlands, rivers, reservoirs, canals and lakes (Righi, 2002; Girolli et al., 2021; Pires et al., 2021). These organisms have benthic habits, crawl on the substrate or build galleries in the sediment, but are also found associated with other organisms such as bryophytes and aquatic macrophytes (Alves and Gorni, 2007; Sanches et al., 2016), sponges (Gorni and Alves, 2008); mollusks (Martins and Alves, 2008) and amphibians (Oda et al., 2015). The group of aquatic oligochaetes presents a reduced size (from 1 mm to a few centimeters in length), greater mobility and more elaborate sensory organs when compared to terrestrial species (Rocha, 2003; Hickman, 2004) and is directly influenced by local variation in environments (Moretto et al., 2013).

Like most aquatic invertebrates, these individuals are considered excellent bioindicators of environmental change (Cortelezzi et al., 2012; Abubakr et al., 2018). They are frequently used as bioindicators to study organic pollution in rivers (Lin and Yo, 2008), with some species found in high densities in polluted environments (Pamplim et al., 2005) and, due to low dispersion, are considered indicators of specific habitats (Verdonschot, 2001). In addition, they play an important role in sediment structuring, nutrient cycling and the energy flow of ecosystems (Gorni & Alves, 2008; Ragonha et al., 2013). Approximately 1100 species of aquatic oligochaetes are described in freshwater environments (Martin et al., 2008), and in Brazil about 70 species have been catalogued (Righi, 2002). Despite their importance, the scarcity of studies on these organisms in Brazilian aquatic ecosystems is evident, due to their complex identification process (Rocha, 2003), needing more revisions and studies for a more accurate species survey close to the real situation. There is also a need for further studies that address the ecological aspects of the group.

The Iguaçu River is the second most polluted river in Brazil and in the Middle Iguaçu region this river is used for the public water supply (Brazilian Institute of Geography and Statistics (IBGE, 2012). Efforts to understand the dynamics and conservation of this river are necessary, since this region has a lack of studies. Here, we investigate changes in the β-temporal diversity and species composition of aquatic Oligochaeta in an impacted urban river stretch over a three-year period. We predicted that changes in abiotic conditions might cause differences in species composition between years, leading to a reduction in β-temporal diversity.

2 Material and methods

2.1 Study area

The Iguaçu River is located in the Atlantic Forest biome, and it forms the frontier between the states of Paraná and Santa Catarina, Brazil. It is an important tributary of the Paraná River and is considered the main river in the state of Paraná (Dalla-Corte et al., 2015). Covering a total area of 54,820.4 km2, the Iguaçu River is formed by the confluence of the Irai and Atuba Rivers, to the east of the city of Curitiba, and it follows a course of 1320 km, crossing the three plateaus of the state of Paraná until it flows into the Paraná River. This basin is divided into Water Resources Management Hydrographic Units, in accordance with Resolution Nº 49/2006/CERH/PR: namely, the Lower Iguaçu, Middle Iguaçu and Upper Iguaçu (Sema, 2010). The Iguaçu River is the second most polluted river in Brazil, due to anthropogenic effects arising from the increase in population, such as the dumping of untreated sewage, use of soil, the removal of riparian forest and the increase in the dosage of chemical products by treatment stations, altering the quality of the water (Zarpelon, 2008; Freire et al., 2015; Lehun et al., 2021).

The sampling points are located in the Middle Iguaçu in the region of União da Vitória 26° 1345.0912″ S; 51° 4′46.9488″ W (Fig. 1; Tab. S1). The landscape is composed of plains, mountains, valleys and large floodplain areas (Rocha, 2013). The region has a humid subtropical climate, type cfb (Köppen) mesothermal (Turismo Porto União da Vitória, 2012). Rains occur in all months, with no defined dry season. However, this stretch of the river near the region of União da Vitória has little infrastructure for sewage drainage, and there is thus a potential contamination, with organic pollution due to the discharge of sewage (Sema, 2010).

thumbnail Fig. 1.

Location of Middle Iguaçu River, Paraná, Brazil. Dashed lines represent the sampled section.

2.2 Sample collection

To analyse the composition of the Oligochaeta species, we collected sediment samples along a stretch of the Iguaçu River, approximately 10 km in lenght, using an Ekman-Birge grab (15×15 cm). Sampling was carried out in August and November 2012 at 4 points on the river, in November 2013 and February 2014 at 3 points and in December 2014 at 5 points. For each point, 3 to 4 sediment subsamples were collected, totaling 75 subsamples, which were stored separately in plastic bags, preserved in situ with 10% formalin and taken to the laboratory. However, for temporal analyses of the aquatic community of Oligochaeta, the sub-samples from each point were grouped into a composite sample, in order to standardize the sample number between years, totaling 19 biological samples.

After that, the samples were washed in a set of sieves with 2.0 mm, 1 mm and 0.2 mm mesh. The Oligochaeta retained in the sieves were added to glass vials (10 ml) and fixed/preserved in 70% ethanol. In addition to biological samples, we also collected sediment for further analysis of the organic matter content.

After each sample, all individuals were organized on slides in Amman’s Lactophenol solution for the clarification of the organisms (Brinkhurst and Marchese, 1991) and later identified at the lowest possible taxonomic level using an optic microscope and the specialized identification manual of Righi (1984), Brinkhurst and Marchese (1991) and Gaviria (1993). Specimens were deposited in the Zoology Laboratory of the Biology Laboratory of the State University of Paraná (UNESPAR), Campus União da Vitória.

2.3 Abiotic variables

During the sampling, we measured the abiotic variables considered important to the aquatic Oligochaeta communities, such as water temperature (°C), dissolved oxygen (mg L–1), electrical conductivity (μS cm–1), pH, organic matter (Amo et al., 2017), aluminum (Al) and lead (Pb).

Electrical conductivity, pH, temperature and dissolved oxygen were measured using test kits and a YSI oximeter 550A, respectively. Organic matter in the sediment was obtained from 10 g dry sediment by incineration at 560°C for four hours in a muffle furnace (Moretto et al., 2013). The difference between the initial and final weight of the sediment indicates the amount of organic matter present in the sediment.

For metal analysis, we collected surface water from the Iguaçu River and stored it in 500 mL polyethylene bottles. The sample was centrifuged and examined by inductively coupled plasma optical emission (ICP OES) for large and selected oligoelements. The spectrophotometry was done by atomic absorption according to the American Public Health Association (APHA, 2012) guidelines. In this study, we only used the metals aluminum (Al) and lead (Pb), which had values above those established by the Brazilian legislation (CONAMA, 2005).

2.4 Data analysis

To test the changes in the abiotic variables over the years, we performed a Multivariate Permutational Variance Analysis (PERMANOVA) (Anderson, 2006). We considered the abiotic variables as predictor variables and used the Euclidean distance. A total of 999 permutations were carried out to assess significance. We also used a pairwise PERMANOVA to assess significant differences between years.

To investigate the variability in the abiotic variables (environmental heterogeneity) between years, we used the multivariate homogeneity of group dispersion (PERMDISP; Anderson, 2006), considering the mean distances in the abiotic variables (Euclidean dissimilarity matrix) from each sample in relation to its centroid groups (years, 2012, 2013 and 2014) in a multidimensional space of Principal Coordinate Analysis (PCoA). The significance value (p value) of the mean distances (PERMDISP) was verified using a test with 999 permutations and analysis of variance (ANOVA).

The (dis)similarity in Oligochaeta species composition over the years was visualized by a PCoA (Legendre and Legendre, 1998) using a presence/absence matrix and the Jaccard distance. A PERMANOVA was performed to evaluate changes in the Oligochaeta species composition over the years (Anderson, 2006). A total of 999 permutations were performed to assess significance. We also used a pairwise PERMANOVA to assess significant differences between years.

The variability of Oligochaeta species composition (beta diversity) over the years was evaluated by a PERMDISP (Anderson, 2006), using a presence/absence matrix and the Jaccard distance, considering the mean distances of Oligochaeta species composition of each sample in relation to its centroid groups (years, 2012, 2013 and 2014) in a multidimensional space of Principal Coordinate Analysis (PCoA). The significance value (p value) of the mean distances (PERMDISP) was verified using a test with 999 permutations and analysis of variance (ANOVA). We also used a pairwise PERMDISP to assess significant differences between years.

Multiple regression analyses were carried out to test the influence of the abiotic variables (water temperature, dissolved oxygen, electrical conductivity, pH and organic matter) on Oligochaeta species composition using both axes of the PCoA. The collinearity amongst the predictors was checked by the variance inflation factor (VIF < 5). Thus, we removed temperature from the model because it showed high inflation values (VIF > 5).

Analyses were performed with the program R 3.3.1 (R Development Core Team, 2019). PCoA used the vegan (Oksanen et al., 2019), permute (Simpson, 2019) and lattice (Sarkar, 2008) packages, and PERMANOVA was performed according to the function “ADONIS” of the vegan package.

3 Results

We identified a total of 35 species of Oligochaeta during the sampling years (Tab. 1). We recorded 32 species in 2012, 14 species in 2013 and the same number of species in 2014. The result of the Principal Coordinates Analysis (PCoA) showed differences in species composition between the years (Fig. 2), indicating a temporal change in the species composition, which was confirmed by PERMANOVA (F = 2.59; p = 0.002). The pairwise PERMANOVA showed significant differences between 2012 and 2013, and between 2012 and 2014 (Tab. 2).

We corroborated our prediction because we observed lower beta diversity over the years. The variability of the Oligochaeta species composition (beta diversity) was also different between the sampling years (F = 12.228; p = 0.002), with a decrease in the beta diversity over the years (Fig. 3). Based on PERMDISP pairwise comparisons, beta diversity values were significantly different between 2012 and 2013, 2014 (Tab. 3).

Table 1

Oligochaeta occurrence from the Middle Iguaçu River over the years (2012–2014).

thumbnail Fig. 2.

Principal coordinate analysis showing the variability in the Oligochaeta species composition over the years in the Iguaçu River.
Table 2

Pairwise PERMANOVA of the Oligochaete species composition over time in the Iguaçu River. Significant values in bold.

thumbnail Fig. 3.

Oligochaeta beta diversity in the Iguaçu River during the years.
Table 3

Pairwise comparisons of the homogeneity of multivariate dispersions of the Oligochaeta species composition over time in the Iguaçu River. Significant values in bold.

3.1 Abiotic variables

The means of environmental variables (water temperature, dissolved oxygen, electrical conductivity, organic matter, Aluminum and Lead) for the years 2012, 2013 and 2014, as well as the standard deviation, are presented in Table 4.

The multiple regression analyses using all variables (global model) were significant between species composition and abiotic variables on axis 1 (Model, R2 = 0.686; p = 0.014) and axis 2 (Model, R2 = 0.628, p = 0.034). Considering each variable, the species composition was significantly related, to electrical conductivity and aluminum on axis 1, and to electrical conductivity and organic matter on axis 2 (Tab. 5).

Significant differences were also observed in the abiotic variables in the Iguaçu River between the sampling years (F: 5.09; p = 0.001; Fig. 4). A pairwise PERMANOVA showed changes in abiotic variables between 2014 and 2012, 2013, respectively (Tab. 6).

With regard to the variability of abiotic variables (environmental heterogeneity), no significant differences were observed between sampling years (F: 3.111; p = 0.059; Fig. 5).

Table 4

Mean values and standard deviation (SD) for each abiotic variable. Water temperature (WT), dissolved oxygen (DO), electrical conductivity (EC), organic matter (OM), Aluminum (Al) and Lead (Pb).

Table 5

Results of multiple regression between Oligochaeta species composition and abiotic variables in the Iguaçu River, Brazil. Water temperature (WT), dissolved oxygen (DO), electrical conductivity (EC), organic matter (OM), Aluminum (Al) and Lead (Pb). Significant values in bold.

thumbnail Fig. 4.

Principal Coordinate Analysis (PCoA) derived from the abiotic variables of the Iguaçu River over the years.
Table 6

Pairwise PERMANOVA of the abiotic variables composition over time in the Iguaçu River. Significant values in bold.

thumbnail Fig. 5.

PERMDISP values derived from the abiotic variables of the Iguaçu River over the years.

4 Discussion

Our results corroborate our prediction because we observed that changes in abiotic variables caused changes in Oligochaeta species composition and beta diversity over the years. The abiotic variables electrical conductivity, organic matter in the sediment and aluminum were related negatively with the composition of species, indicating an influence on the structure of the community. Limnological variables have a higher influence on the Oligochaeta communities compared to habitat components (heterogeneity, e.g. particle size composition) (Amo et al., 2017). Of the abiotic variables evaluated in this study, only dissolved oxygen, pH and lead were not related to the composition of Oligochaeta species.

The relationship of multiple variables with species composition can be explained by the fact that many Oligochaeta species are sensitive to chemical changes in the environment, such as variations in electrical conductivity, for example (Bechara, 1996). The negative relationship between species composition and electrical conductivity has been previously found in other studies (Ragonha et al., 2013; Rosa et al., 2014). High values of electrical conductivity can biologically affect Oligochaeta individuals because they promote high osmotic pressure in the environment (high concentrations of ions) that can cause physiological changes, negatively affecting the survival of these organisms (Frouz et al., 2005). In an urban area, high conductivity values are indirect measures of the concentration of pollutants in the water, derived from ions from effluents and decomposition of organic matter (Esteves, 1998; Rosa et al., 2014).

Changes and oscillations in abiotic variables over the years in aquatic ecosystems can result from oscillations in the fluviometric level, seasonal variations, human activities and especially increased pollution (Barletta et al., 2019). The pollution of aquatic environments can affect important limnological variables that structure aquatic communities. For example, organic pollution increases the values of electrical conductivity (Esteves, 1998).

An increase in human activities and aquatic pollution contributes to changes in abiotic variables over time (Martins et al., 2017) and, consequently, promotes changes in the composition of species. Oligochaeta communities are considered a good bioindicator for predicting environmental changes in rivers (Cortelezzi et al., 2012; Abubakr et al., 2018), although in some cases it is not possible to clearly distinguish between the effects of natural factors and anthropogenic disturbances (Behrend et al., 2012). The study area has only 109 km of sewage collection system (IBGE, 2017), where human activities contribute to the input of organic matter in this stretch of the river (Freire et al., 2015). Benthic invertebrates, like most species of Oligochaeta, have detritivorous habits, using organic matter from sediment as a food resource (Brinkhurst and Austin, 1979). Thus, urbanization and human pollution may have increased the input of food resources by increasing organic matter, promoting optimal conditions for Oligochaeta and contributing to the establishment of this community in this region (Behrend et al., 2012; Rosa et al., 2014). In our study, however, we observed a negative correlation between Oligochaeta species composition and the amount of organic matter; the increase in organic matter derived mainly from human activities (domestic and industrial sewage) may favor the establishment of only a few generalist and tolerant species, thus explaining the negative correlation with this attribute.

The species recorded in all sampling years, especially from the subfamily Tubificinae, found in regions polluted by urban effluent (Uzunov et al., 1988; Abubakr et al., 2018), are probably tolerant of environmental variations and pollution. These include Limnodrilus hoffmeisteri, a species related to high levels of mud that can be found in polluted sites with high levels of organic matter and low dissolved oxygen concentration (Dumnicka and Pasternak, 1978; Abubakr et al., 2018), conditions similar to the study area, especially in relation to the last sampling in 2014.

The reduction in beta diversity, combined with changes in temporal species composition, may be due to aquatic pollution. The stretch of river studied has a high organic pollution level, which is reflected in our results, where species of the family Tubificidae (Brinkhurst and Gelder, 1991) and genus Dero (Martin, 1996) were recorded. These are taxa that are good indicators of environmental conditions related to organic pollution and low levels of oxygen concentration in lakes and rivers (Lin and Yo, 2008; Behrend et al., 2012; Rosa et al., 2014). However, other variables that were not evaluated in this study (e.g. seasonality and biotic interaction) may also be responsible for decreasing Oligochaeta's beta diversity. For example, the water flow velocity affects species composition and decreases the beta diversity of this community (Petsch et al., 2020).

In addition to organic pollution, this stretch is polluted by heavy metals (e.g. lead and aluminum) (Melo-Silva et al., 2018) and other contaminants (e.g. caffeine, phenol) (Bueno-Krawczyk et al., 2015; Lehun et al., 2020; 2021), which can influence the individuals and the composition of benthic invertebrate communities (Beghelli et al., 2020). The negative relationship found between aluminum concentrations and the composition of Oligochaeta species may be related to the toxicity that this metal can present to many species of aquatic invertebrates, causing mortality and sublethal effects, such as respiratory disorders and dysfunction in osmoregulation (Herrmann, 2001), since these organisms tend to accumulate aluminum on ion-regulatory surfaces (Gensemer and Playle, 1999). Furthermore, aluminum toxicity has been directly related to reduced survival and/or impaired reproduction in many aquatic communities, including aquatic invertebrates (Sparling and Lowe, 1996).

Other studies have observed the effects of high concentrations of heavy metals on aquatic organisms (Beghelli et al., 2020). Melo-Silva et al. (2018) found high concentrations of lead and aluminum in the middle Iguaçu River region and, consequently, cellular alterations and nuclear abnormalities in fish (Astyanax bifasciatus) in this region. Lehun et al. (2021, in press) observed a low parasitic diversity (nematodes) in fish (Geophagus brasiliensis) in polluted sites of the Iguaçu River, suggesting that the pollution gradient of the river was responsible for the change in the composition of the parasitic fish fauna. Thus, we direct attention to the Oligochaeta group, since they are often generalized as organisms that are tolerant of pollution. However, in this group there are species sensitive to environmental variation. For example, it was recently observed that Limnodrilus hoffmeisteri, which is considered pollution-tolerant, is a taxon sensitive to chromium metal concentrations (Beghelli et al., 2020). The sensitivity is different among species, although the identification of these organisms is generally neglected in tropical regions (Christoffersen, 2010), keeping only the taxonomic level of the group, which can lead to incorrect interpretations.

We also do not exclude the possibility that intrinsic community factors such as competition, predation, and population dynamics explain the temporal variation in species composition and the reduction in beta diversity. Regarding competition and predation, these factors can decrease abundance of some species; on the other hand in the absence of predators and competitors some species can become abundant, such as Tubifex and Limnodrilus (Dornfeld et al., 2006). For example, some predators like crayfish reduce the abundance of Oligochaeta in the environment influencing other community attributes (e.g. species composition) (Weber and Traunspurger, 2017).

We recognize some limitations in our study, but they do not invalidate our results. One of the limitations may be the absence of some variables that are pollution indicators, such as nitrogen and phosphorus, and particle size composition, which has been shown to be important in the structure of the Oligochaeta communities, since it can increase the percentage of explanation of the inter-annual variation of species composition and the reduction in beta diversity. However, we added variables considered pollution indicators, such as heavy metals, conductivity and organic matter in sediment. The second limitation is the fact that the lower sampling effort in 2013 may influence the results of species composition and beta diversity. However, the same replication number is not always possible in ecological studies, and this different sample number does not have strong ecological influence, since in 2014 the sampling effort was similar to that of 2012, but even so the beta diversity was lower. The last limitation is that seasonality, especially temperature and precipitation can influence Oligochaeta community attributes (Paoletti and Sambugar, 1984; Behrend et al., 2008). Although, we prioritized sampling in warmer months (spring and summer), one sampling was conducted in the cold period. In our study, the effect of seasonality on our data was minor, because the Middle Iguaçu region has no distinction between dry and flood periods, and only one sampling was performed in winter.

5 Conclusion

We concluded that the region of the middle Iguaçu presents evident interannual variation in the species composition of Oligochaeta, with a tendency for the beta diversity to decrease, due to the changes and oscillations in abiotic variables. We suggest that basic preservation and sanitation measures be considered not only in this stretch studied, but also in other urban rivers that suffer from anthropic pressures related to pollution, to avoid the loss of diversity of aquatic Oligochaeta species. Otherwise, changes in the composition of and reduction in diversity may imply changes in other environmental functions related to sediment aeration, consumption of organic matter and transfer of matter and energy.

Finally, our results support the idea that these species are indicators of environmental variations. In addition, we highlight the possible biotic homogenization of Oligochaeta communities over time, due to the reduction in beta diversity. Temporal analysis draws attention because the environmental conditions observed are of a river which is used for the public water supply, and thus efforts to understand the dynamics and conservation of the river are particularly necessary.

Author contributions

Rosa, Oliveira and Bueno-Krawczyk designed the research. Rosa, Oliveira, Pereira and Silva contributed to the sampling, sorting and identification of Oligochaeta. Rosa and Oliveira wrote the first draft of the manuscript. All authors significantly contributed to further manuscript revisions and gave final approval for publication.

Supplementary Material

Table S1. Sampling sites and geographic co-ordinates of the six sampling sites, located at the Middle Iguaçu in the region of União da Vitória, Brazil. Access here

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Cite this article as: Rosa J, de Oliveira FR, Fátima Pereira L, de Melo Silva M, Bueno-Krawczyk ACD. 2022. Temporal variation in Oligochaeta species composition in an anthropized stretch of a Neotropical urban river. Int. J. Lim. 58: 6

All Tables

Table 1

Oligochaeta occurrence from the Middle Iguaçu River over the years (2012–2014).

In the text
Table 2

Pairwise PERMANOVA of the Oligochaete species composition over time in the Iguaçu River. Significant values in bold.

In the text
Table 3

Pairwise comparisons of the homogeneity of multivariate dispersions of the Oligochaeta species composition over time in the Iguaçu River. Significant values in bold.

In the text
Table 4

Mean values and standard deviation (SD) for each abiotic variable. Water temperature (WT), dissolved oxygen (DO), electrical conductivity (EC), organic matter (OM), Aluminum (Al) and Lead (Pb).

In the text
Table 5

Results of multiple regression between Oligochaeta species composition and abiotic variables in the Iguaçu River, Brazil. Water temperature (WT), dissolved oxygen (DO), electrical conductivity (EC), organic matter (OM), Aluminum (Al) and Lead (Pb). Significant values in bold.

In the text
Table 6

Pairwise PERMANOVA of the abiotic variables composition over time in the Iguaçu River. Significant values in bold.

In the text

All Figures

thumbnail Fig. 1.

Location of Middle Iguaçu River, Paraná, Brazil. Dashed lines represent the sampled section.
In the text
thumbnail Fig. 2.

Principal coordinate analysis showing the variability in the Oligochaeta species composition over the years in the Iguaçu River.
In the text
thumbnail Fig. 3.

Oligochaeta beta diversity in the Iguaçu River during the years.
In the text
thumbnail Fig. 4.

Principal Coordinate Analysis (PCoA) derived from the abiotic variables of the Iguaçu River over the years.
In the text
thumbnail Fig. 5.

PERMDISP values derived from the abiotic variables of the Iguaçu River over the years.
In the text

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