Free Access
Ann. Limnol. - Int. J. Lim.
Volume 56, 2020
Article Number 9
Number of page(s) 9
Published online 30 April 2020

© EDP Sciences, 2020

1 Introduction

Understanding the mechanisms that drive the distribution of organisms in space and time is still one of the central goals of ecology (Sutherland et al., 2013), which seeks to identify, describe, and explain the general patterns that are the major driving forces of community structure (Hubbell 2001; Leibold et al., 2004). The metapopulation theory formulated by Levins in 1969 is one of the theories designed to understand these community organization patterns. Levins proposed that populations of the same species might be structured in different ways, due to local extinction mechanisms and colonization by migrating individuals, derived from more stable populations (e.g., sites with more resources and genetic variability) (Hansky et al., 1996; Hansky and Simberloff 1997). Therefore, even sites with low amounts of resources or environmental conditions outside the range for species requirements might maintain biodiversity at a certain level due to source habitats, which would provide constant migration of species.

In order to quantify this spatial dynamics and the variation in species composition in communities, diversity can be divided into three scales, alpha (α) diversity, which is defined as the local diversity, or diversity within the habitat; gamma (γ) diversity, which is the total diversity of a region including several habitats; and beta (β) diversity (Buschini and Woiski 2008), which is the variation in species composition between sites or different habitats (Whittaker 1972). Alfa-diversity is traditionally called species richness and is one of the most frequently used measures to evaluate diversity patterns (Arrhenius 1921; MacArthur and Wilson 1967; Wright 1983), despite its limitation to equate all species. This problem is minimized in beta-diversity due to its potential to measure variation in species composition, which thus renders it a robust tool both to detect diversity patterns (Koleff et al., 2003; Harrison et al., 1992; Peixoto et al., 2017; Juen and De Marco 2011; Brasil et al., 2018) and to measure environmental impacts on biotic diversity (Quintana et al., 2017; Altermatt and Holyoak 2012; Ferreira et al., 2017). Beta-diversity is considered an important measure, providing a connection between alpha-diversity (local) and gamma-diversity (regional) (Vellend 2010).

The major hypotheses that explain differences in diversity use local, geographical, and/or historical environmental factors (Nekola and White 1999). Due to higher variation in environmental conditions, there is an increase in dissimilarity of species composition (beta-diversity) (Heino et al., 2015), which might in turn provide higher variation, in environmental conditions contemplating species with different environmental requirements. Thus, sites that are environmentally more heterogeneous would have higher beta-diversity values (Anderson et al., 2006). Considering spatial factors, sites that are farther from each other are expected to have higher dissimilarity in species composition (beta-diversity) (Legendre 1993). This is because the closer the areas are, the higher is the probability of migration within the landscape (Alahuhta and Heino 2013). However, under this spatial perspective, autoecological factors such as species dispersal ability and biogeographical factors, such as the presence of geo-graphical barriers, might limit dispersal and limit species diversity patterns across the landscape (Juen and De Marco 2012; Dambros et al., 2017; Brasil et al., 2018).

The constant conversion of natural landscape for anthropic purposes, e.g. agro-systems, urbanization, and/or industrialization (Brando et al., 2013; Gardner et al., 2013) is one of the great bottlenecks in maintaining biodiversity since it generally results in a simplification of environmental conditions, leading to habitat homogenization. Therefore, understanding how these environmental changes affect species, environmental conditions, and ecosystem services has become an increasingly pressing issue (Nessimian et al., 2008; Laurance et al., 2017). In this setting, evaluating variations in beta-diversity across environmental gradients with different environmental change levels is an important tool for biomonitoring (Ligeiro et al., 2013) as the local extinction of more specialist species is more frequent due to environmental impacts, because they tolerate few environmental changes. On the other hand, it is not rare for generalist species to enter these habitats, since they have more ability to disperse and tolerate higher variation in environmental conditions (Oliveira-Junior et al., 2015; 2019a). Therefore, this variation is not detected by alpha-diversity, as alpha-diversity is practically constant or might even increase. These characteristics indicate that evaluating changes in species composition across environmental gradients provide more robust results than traditional alpha-diversity measures (species richness) for the analyses of environmental impact on species distribution at a community level (Miguel et al., 2017)

In aquatic environments, aquatic insects are considered good models to evaluate how environmental changes affect environmental quality (Resh and Rosenberg, 1993). Among these organisms, Heteroptera stands out since they have a high dispersal ability and great potential as pioneer species in colonizing new water bodies (Bachmann 1998). Heteroptera are strongly dependent on riparian vegetation and are therefore good indicators of physical disturbances in streams (Dias-Silva et al., 2010; Cunha et al., 2015). Additionally, the removal of riparian vegetation leads to a disruption in physical characteristics of streams, increasing silting and destabilizing margins, affecting width, depth, and stream flow, which are very important metrics for the structuring of aquatic communities in streams.

In this scenario of environmental change, our aim was to evaluate the effect of environmental change on beta-diversity of aquatic and semi-aquatic Heteroptera in streams of the Cerrado, testing the following hypotheses: (1) preserved environments have higher beta-diversity than environments with lower preservation values; (2) beta-diversity shall be more sensitive than species richness in detecting changes in community related to environmental integrity gradients.

2 Material and methods

2.1 Study area

The sampling of aquatic and semi-aquatic Heteroptera was conducted in the Pindaíba River basin, a tributary of the right margin of the middle Rio das Mortes River, located in the eastern region of Mato Grosso, with an area of approximately 10,323 km2, in the Cerrado Biome. Its sources are located in the Acantilados Plateau, in the municipality of Barra do Garças.

1st and 4th-order stretches were sampled (Strahler, 1957) from 5 streams (Córrego da Mata (CRM), Córrego Caveira (CRCV), Taquaral (CRT), Cachoeirinha (CRC), and Papagaio (CRP)), totaling 20 sampling points (Fig. 1). The samples were realized in the month of September 2009, end of the dry season and beginning of the rainy season, so that samples from intermittent streams due to drought were not collected and the rainy season was avoided due to the filling of streams and the carrying of Gerromorpha by the water. The focus on a single seasonal period also reduces sampling “noise” in the analyses and results (Heino 2014). These streams have relatively similar features regarding the region of their sources. However, they differ in the conservation state of other stretches due to extensive cattle breeding and agricultural activities in the areas of Cachoeirinha and Caveira streams, whereas the riparian forests in Mata, Taquaral, and Papagaio streams were preserved.

Climate in the region is Aw type according to Koppen's classification, with mean annual temperature ranging from ±20 to ±26 °C and mean rainfall ranging from 1500 to 1600 mm, with two well-defined seasons; winter, less hot and dry (May to September) and a rainy summer (November to March).

thumbnail Fig. 1

Location of the 1st to 4th-order streams where the samplings of aquatic and semi-aquatic Heteroptera were conducted in 2008.

2.2 Heteroptera sampling and identification

Samplings were conducted in fixed 100-m transects, divided in segments with five meters each (100/20 = 5). With the help of a net with 18 cm diameter (32 mm mesh size), three samples were collected in each segment in the water column (Cabette et al., 2010). Heteroptera were screened in the field, conserved in alcohol (85%) and identified in the laboratory with the help of dichotomous keys (Nieser and Melo 1997; Ribeiro 2005). Witness material is deposited at the Zoobotanical Collection “James Alexander Ratter” of UNEMAT, Nova Xavantina Campus.

2.3 Environmental conditions of streams

Environmental integrity was measured using the Habitat Integrity Index (HII) proposed by Nessimian et al. (2008). This index is comprised of 12 items that evaluate the structure of water bodies regarding riparian vegetation status, land use pattern beyond this range, retention devices, and types of substrate, aquatic vegetation, and detritus. HII has been widely used quite effectively as predictor of environmental conditions of streams about distribution of aquatic communities (Brasil et al., 2017; Vieira et al., 2015), and more specifically, for Heteroptera (Dias-Silva et al., 2010; Cunha and Juen 2017; Giehl et al., 2019).

Each of the 12 items in the HII is scored from 1 (very altered) to 4 or 5 (very preserved). This is because some items have 4 and other items have 5 response alternatives. For each item, in each stream the score obtained by the researcher is divided by the total number of options (4 or 5). This gives a partial score (12 points per stream). The final index is given by the sum of all partial scores divided by 12 (total number of items). In order to separate groups derived from sites considered either preserved or altered, streams with HII ≤ 0.6 were considered “altered” and sites with HII higher than that limit value were considered “preserved” (Brasil et al., 2017). Previous studies have already shown that these categories are efficient for classifying lotic environments according to their conservation category (Pereira et al., 2012; Oliveira-Junior et al., 2015; 2019b). In addition, the classification was also validated with observation by researchers in the field, where streams classified as altered due to heavy agricultural mechanization, the gallery forest at margins of these streams are highly deforested, replaced by pastures or soy monoculture, cattle raising. Other processes, such as erosion and silting are also observed. Since stream margins are exposed, the river channel lacks retention mechanisms and consequently little deposited organic material. On the other hand, for places characterized as preserved the predominant characteristics were: more than 50 m in width of gallery forest, continuously with the adjacent forest, retention mechanisms strongly fixed, lack of banks, little or no accumulation of sediments, riverbed, with stones grouped together, mosses and algae patches, and leaf detritus and woody material without sediment (Pereira et al 2012).

The physical-chemical variables were measured in the field and at the time of collection. Air temperature and water temperature were obtained with a digital thermometer (Multidigital) (Incoterm®), pH, turbidity, electrical conductivity, oxygen dissolved (OD) were obtained with a portable multi-parameter probe (Horiba®). For the analysis of phosphate, nitrate, nitrite and ammoniacal nitrogen we used a portable spectrophotometer (Hach®), and for the total hardness, calcium and magnesium we used the titulometric method with EDTA at 0.0002 M. Width measurements were obtained with a measuring tape (Leica DISTO TM®), the depth measurement was made using a depth meter (Sonar Echotest II®) and for the current speed we used a current meter (Geopacks MJP®). Flow data were calculated using the formula: Q = A × V, which represents the relationship between the area (A) of the channel cross section (width x average depth) and the speed of the current (V), being expressed as Q = L × P × V, where Q = flow, L = average width, P = average depth and V = average speed (Cunha and Guerra, 1996). All the variables mentioned above were measured at three points in each stream and the average values were used in the analyses.

2.4 Data analysis

The relationship of Heteroptera with environmental integrity gradients is idiosyncratic considering its infraorders Gerromorpha and Nepomorpha. Conditions concerning the physical part of the stream are mostly related to Gerromorpha and chemical conditions are mostly related with Nepomorpha; therefore, we analyzed both communities as a whole and its infraorders (Gerromorpha and Nepomorpha) separately in all tests (Dias-Silva et al., 2010). Additionally, the group of taxa selected for all analyses in each stream was considered a sampling unit.

Species richness was obtained based on the non-parametric estimator, first-order Jackknife, using the EstimateS Win 7.5 software (Colwell 2000). Beta-diversity was calculated using Sorensen's index modified by Chao et al., (2005). This index was chosen because it considers species abundance along with an estimate of species that have not been sampled (Chao et al., 2005). Moreover, it is considered relatively independent of species richness and more accurate even with small samples (Soininen et al., 2007). The higher the Sorensen's value, the higher the difference in species composition between two given communities. In order to find a beta-diversity value for each community, a mean value of comparisons (Sorensen's index) is calculated for the focal community with all the others in the background (Dambros et al., 2017; Brasil et al., 2018).

We performed simple linear regressions to test the hypothesis that there is a positive re-lationship between beta-diversity and environmental integrity, as well as the hypothesis that beta-diversity will be more effective than species richness in detecting changes in community regarding this environmental integrity gradient. Complementarily, we tested if there were differences between communities of preserved and degraded sites using a permutational analysis of dispersion homogeneity PERMANOVA (Permutational Multivariate Analyses of Variance) among the sampled sites using the “adonis” function (R vegan package) and PERMDISP (Permutational Analysis of Multivariate Dispersions) with the “betadisper” function (R vegan package) (Anderson et al., 2006). This test was performed based on the mean distances between points in a group of samples and the centroid of their multivariate space.

3 Results

3.1 Environmental conditions

Environmental integrity of streams varied between HII 0.52 and 0.96 (Tab. 2). Considering the integrity threshold value of HII = 0.6, eight streams were considered altered and twelve streams were considered preserved (Fig. 2a). Checking the environmental water conditions, we observed that streams considered to be preserved were more heterogeneous than the altered ones (Fig. 2b). The ordination of environmental conditions explained 57% of environmental variation in the first two axes and separated preserved streams from altered streams in the first axis (Fig. 2b). The most important environmental variables for this separation were pH, conductivity, hardness, Ca, and Mg, negatively related to the first axis, water and air temperature positively related to the second axis (Fig. 2c). Of the variables mentioned above, the highest differences occurred in water temperature, air temperature, both with higher values in degraded streams, and pH with the highest values in preserved streams (Fig. 2c-f).

Table 1

Tests of difference (PERMANOVA) and homogeneity (PERMIDISP) in species composition of Heteroptera communities in preserved and altered streams in the Brazilian Cerrado.

Table 2

Mean values of environmental variables in Mata Stream (MS), Cachoeirinha Stream (CS), Taquaral Stream (TS), Papagaio Stream (PS) and Caveira Stream (CVS). pH, conductivity eletrical (Eletrical. C.), turbidity (T.), Water Temperature (W.T.), Air Temperature (Air.T.), oxygen dissolved (O.D.), phosphate (P), hardness total (H), calcium (C), magnesium (Mg), nitrate (N), nitrite (Ni), Mean Width (M.W.), Mean depth (M. D.), flow (F) and HII for each streams and order sampled this study of Bioma Cerrado, Brazil.

thumbnail Fig. 2

Environmental variations in streams. Variations in HII values of preserved and altered streams (a), environmental heterogeneity in preserved and altered streams (b), ordination of environmental variables (c), variation in air temperature (d), water temperature (e) of preserved and altered streams, and variation in water pH of preserved and altered streams (f).

3.2 Description of communities

A total of 2817 individuals were collected, distributed in 10 families, 32 genera, 13 species and 56 morphospecies. Most of the organisms were specimens of Gerromorpha, with 2294 individuals (81%), four families, 17 genera, and 31 morphospecies, and Nepomorpha, with 523 specimens (19%), six families, 13 genera, and 36 morphospecies/species (Tab. 3).

Table 3

Species list and abundance of the individuals from Heteroptera in Cerrado Stream.

3.3 Environmental integrity and Heteroptera communities

Heteroptera richness (considering both infraorders together) was not affected by the environmental integrity gradient (r 2 = 0.139; p = 0.106) (Fig. 3d), and the same result was found for the infraorder Nepomorpha (r 2 = 0.00; p = 0.928) (Fig. 3f). However, Gerromorpha species richness had a significant positive relationship with environmental integrity gradient (r 2 = 0.227; p = 0.034) (Fig. 3b). Considering beta-diversity as a response variable, beta-diversity of both Heteroptera and Gerromorpha infraorder had a significant and positive relationship with the environmental integrity gradient (r 2 = 0.34; p = 0.007, and r 2 = 0.570; p < 0.001, respectively) (Fig. 3a and c). However, Nepomorpha beta-diversity had no relationship with the environmental integrity gradient (r 2 = 0.066; p = 0.274) (Fig. 3f).

Once streams were classified as either preserved (HII ≤ 0.6) or altered (HII > 0.6), there was no difference in species composition both of Heteroptera (Gerromorpha and Nepomorpha combined) and of Gerromorpha (PERMANOVA: pseudo-F = 2.136, R 2 = 0.106, p = 0.107 and pseudo-F = 2.100, R 2= 0.104, p = 0.098, respectively) between preserved and altered streams. However, there was difference in Nepomorpha species composition (PERMANOVA: pseudo-F = 3.225, R 2 = 0.151, p = 0.001) (Tab. 1). When we checked whether there was difference in the multivariate homogeneity of species composition in preserved and altered streams, both Heteroptera (Gerromorpha and Nepomorpha combined) and Gerromorpha had the most homogeneous communities at altered sites (PERMDISP: F = 5.875, p = 0.029 e F = 4.928, p = 0.039, respectively) (Tab. 1). The results of the multivariate homogeneity analysis are complementary evidence of the relative relationship between beta-diversity and HII (Fig. 3a and b), and both emphasize on community homogenization in streams that are environmentally more altered.

thumbnail Fig. 3

Effect of environmental integrity gradient measured by the Habitat Integrity Index (HII) on Gerromorpha beta-diversity (A) and Gerromorpha estimated species richness (B), Heteroptera beta-diversity (C) and estimated species richness (D) considering both infraorders together, and Nepomorpha beta-diversity (E) and Nepomorpha estimated species richness (F).

4 Discussion

Overall, Heteroptera communities underwent changes due to loss of environmental integrity of streams. Beta-diversity was more sensitive to environmental integrity gradient than species richness. This positive relationship of beta-diversity with environmental integrity shows that pristine sites have a more dissimilar species composition than the background analyzed (all sites). This occurs because there are more rare species and/or species more sensitive to environmental changes at more preserved sites. On the other hand, community is more homogeneous at more altered sites, with predominant occurrence of more generalist species (Brasil et al., 2017). This causes species composition of the most altered site in the integrity gradient to be more similar to the background and this is reflected in its low beta-diversity values.

Sites that are environmentally more heterogeneous are expected to have more species, and this occurs because environmental heterogeneity provides more niche partitioning, which allows for a higher number of species with different environmental requirements to live sparingly, occupying complementary spaces in the environment (Tilman 1982; Cunha and Juen 2017). The lack of relationship of species richness with environmental integrity might occur when species change across the gradient of environmental conditions, especially with local extinction of more sensitive species and the intrusion of more generalist species (Dias-Silva et al., 2010; Cunha et al., 2015). This change cannot always be detected by species richness measures, as they are not sensitive to changes in species composition. However, changes can be detected by beta-diversity values (Carvalho and Gomes 2012), as we observed in the present study.

The positive effect of the Habitat Integrity Index on Heteroptera and Gerromorpha beta-diversity indicates that sites with higher integrity values harbor a higher diversity of these organisms and that these groups are related to habitat structure. Different impact intensities affect beta-diversity, and this can be caused by different mechanisms (Gutiérrez-Cánovas et al., 2013). One of the many factors associated with diversity studies is environmental heterogeneity (Death and Winterbourn 1995; Vieira et al., 2015; Alahuhta et al., 2017). In heterogeneous environments, species with different tolerance ranges tend to have differential spatial distribution patterns (Mykrä et al., 2007). Gerromorpha is a group that depends on the physical structure of streams, such as shading, channel retention material forming pools, or sites such as rapids. Therefore, when this structure is changed, this group responds more rapidly to these changes (Dias-Silva et al., 2010). So far, Nepomorpha has not shown to be sensitive to the physical changes that occurred in the studies we have evaluated, showing to be more sensitive to limnological variables. However, this response pattern cannot always be detected (Dias-Silva et al., 2010; Cunha et al., 2015), which leads us to believe that this group has a wide range of environmental plasticity.

For environmental monitoring, it is necessary to take some precautions when interpreting beta-diversity (Heino et al., 2015). Beta-diversity occurs due to turnover (exchange in species composition among sampling units) or nestedness (species richness gradient) (Baselga, 2010). Therefore, it is common to increase beta-diversity at large spatial scales due to species turnover related to biogeography (Alves-Martins et al., 2019; Brasil et al., 2018). This is not related to gradients of alteration of anthropic origin. On the other hand, in smaller spatial scales, beta-diversity reflects the nestedness nesting caused by loss of species sensitive to environmental changes (Heino et al., 2015). This creates a gradient of species richness. Therefore, the concomitant relationship between environmental integrity and species richness and beta-diversity in Gerromorpha and Heteroptera in our work demonstrates that there is a loss of species that causes the change in beta-diversity.

We have evidence that beta-diversity is more related to stream physical structure than species richness, and this is due to changes in species composition across the environmental gradient. Moreover, corroborating previous studies (Dias-Silva et al., 2010; Vieira et al., 2015), we emphasize that Gerromorpha are more sensitive to changes in environmental gradients and can therefore be used for these purposes. Overall, we indicated that the most altered sites located in pasture and/or agricultural areas are environmentally more homogeneous and have the lowest beta-diversity values. These results reinforce that changes in soil use without respecting riparian vegetation boundaries cause changes in environmental conditions, biodiversity, and might be changing the ecosystem services related to these communities.


We are grateful to Laboratório de Insetos Aquáticos de Nova Xavantina, FAPE-MAT, Proc. n° 098/2004 and 0907/2006. LJ received continuous research support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) productivity grants (Process 304710/2019-9). LSB thanks CAPES for the scholarship of the Programa Nacional de Pós-Doutorado (PNPD) linked to the Programa de Pós-Graduação em Zoologia da Universidade Federal do Pará (UFPA).


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Cite this article as: Dias-Silva K, Brasil LS, Veloso GKO, Cabette HSR, Juen L. 2020. Land use change causes environmental homogeneity and low beta-diversity in Heteroptera of streams. Ann. Limnol. - Int. J. Lim. 56: 9

All Tables

Table 1

Tests of difference (PERMANOVA) and homogeneity (PERMIDISP) in species composition of Heteroptera communities in preserved and altered streams in the Brazilian Cerrado.

Table 2

Mean values of environmental variables in Mata Stream (MS), Cachoeirinha Stream (CS), Taquaral Stream (TS), Papagaio Stream (PS) and Caveira Stream (CVS). pH, conductivity eletrical (Eletrical. C.), turbidity (T.), Water Temperature (W.T.), Air Temperature (Air.T.), oxygen dissolved (O.D.), phosphate (P), hardness total (H), calcium (C), magnesium (Mg), nitrate (N), nitrite (Ni), Mean Width (M.W.), Mean depth (M. D.), flow (F) and HII for each streams and order sampled this study of Bioma Cerrado, Brazil.

Table 3

Species list and abundance of the individuals from Heteroptera in Cerrado Stream.

All Figures

thumbnail Fig. 1

Location of the 1st to 4th-order streams where the samplings of aquatic and semi-aquatic Heteroptera were conducted in 2008.

In the text
thumbnail Fig. 2

Environmental variations in streams. Variations in HII values of preserved and altered streams (a), environmental heterogeneity in preserved and altered streams (b), ordination of environmental variables (c), variation in air temperature (d), water temperature (e) of preserved and altered streams, and variation in water pH of preserved and altered streams (f).

In the text
thumbnail Fig. 3

Effect of environmental integrity gradient measured by the Habitat Integrity Index (HII) on Gerromorpha beta-diversity (A) and Gerromorpha estimated species richness (B), Heteroptera beta-diversity (C) and estimated species richness (D) considering both infraorders together, and Nepomorpha beta-diversity (E) and Nepomorpha estimated species richness (F).

In the text

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