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Silva-Santos Et Al 2023

This study assessed the physical habitat and biological condition of streams in eastern Amazonia using different biotic indices based on Ephemeroptera, Plecoptera, and Trichoptera (EPT) aquatic insects. 32 stream sites were sampled along a land use gradient from primary forest to areas with conventional logging to sites with multiple land uses including agriculture, pasture, and mining. The study found that metrics like EPT taxon richness, abundance, and diversity were responsive to anthropogenic impacts on streams, but EPT taxon richness was the most sensitive indicator. The Biological Monitoring Working Party and Average Score Per Taxon indices, which use EPT insects, were also effective in detecting environmental changes in stream biota caused by different land use

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0% found this document useful (0 votes)
111 views9 pages

Silva-Santos Et Al 2023

This study assessed the physical habitat and biological condition of streams in eastern Amazonia using different biotic indices based on Ephemeroptera, Plecoptera, and Trichoptera (EPT) aquatic insects. 32 stream sites were sampled along a land use gradient from primary forest to areas with conventional logging to sites with multiple land uses including agriculture, pasture, and mining. The study found that metrics like EPT taxon richness, abundance, and diversity were responsive to anthropogenic impacts on streams, but EPT taxon richness was the most sensitive indicator. The Biological Monitoring Working Party and Average Score Per Taxon indices, which use EPT insects, were also effective in detecting environmental changes in stream biota caused by different land use

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Water Biology and Security 2 (2023) 100132

Contents lists available at ScienceDirect

Water Biology and Security


journal homepage: www.keaipublishing.com/en/journals/water-biology-and-security

Original article

Assessing physical habitat structure and biological condition in eastern


Amazonia stream sites
Jady Vivia Almeida da Silva Santos a, Myllena Lima c, *, Josinete Sampaio Monteles d,
Daiany Larissa Ribeiro Carrera b, Ana Paula Justino de Faria e, Leandro Schlemmer Brasil f,
Leandro Juen a, b, c, d
a
Faculdades de Ci^encias Biol ogicas, Instituto de Ci^encias Biologicas, Universidade Federal do Par
a/Rua Augusto Correia, Nº 1, Bairro Guama, CEP, 66075-110, Belem,
Par a, Brazil
b
Laboratorio de Ecologia e Conservaç~ ao, Universidade Federal do Par a/ Rua Augusto Correia, Nº 1, Bairro Guama, CEP, 66075-110, Belem, Para, Brazil
c
Programa de P os-graduaç~ao em Zoologia, Universidade Federal do Par a/Museu Paraense Emílio Goeldi, Rua Augusto Correia, Nº 1, Bairro Guam a, CEP, 66075-110,
Belem, Par a, Brazil
d
Programa de P os-graduaç~ ao em Ecologia, Universidade Federal do Par a e Embrapa Amaz^onia Oriental, Rua Augusto Correia, Nº 1, Bairro Guam a, CEP, 66075-110,
Belem, Par a, Brazil
e
Programa de P os-Graduaç~ ao em Agricultura e Ambiente, Laboratorio de Ci^encias Ambientais e Biodiversidade, Universidade Estadual do Maranh~ ao, S~
ao Luís, Brazil
f
Instituto de Ci^encias Biol
ogicas e Saúde, Universidade Federal do Mato Grosso, Campus Araguaia, Pontal do Araguaia, Mato Grosso, Brazil

A R T I C L E I N F O A B S T R A C T

Keywords: The advance of agricultural frontiers and industrialization in Amazonia has increased natural resource deterio-
Land use ration, resulting in degraded physical habitat structure and reduced local aquatic biodiversity. We evaluated the
Aquatic insects relative sensitivities of the Biological Monitoring Working Party (BMWP) and Average Score Per Taxon (ASPT)
Biotic index
biotic indexes based on EPT (Ephemeroptera, Plecoptera, Trichoptera) versus EPT taxa richness, EPT abundance,
Environmental monitoring
and Shannon-Wiener EPT diversity for evaluating anthropogenic impacts on Amazonian streams. We expected
that EPT-BMWP and EPT-ASPT would be more sensitive in detecting environmental changes on stream biota than
the other measures. We sampled 32 stream sites in eastern Amazonia distributed along an environmental gradient
resulting from different land use intensities. All the biological metrics except EPT-ASPT were significantly
responsive to anthropogenic pressures; however, EPT taxa richness was slightly more responsive.

1. Introduction These modifications are easily perceived by the impoverishment of


aquatic communities and are associated with decreases in abundance or
The expansion of socioeconomic activities, the growth of the human local extirpation of species sensitive to impacts on the environment
population and the global demand for food have become a major chal- (Oliveira-Junior et al., 2015; Miguel et al., 2017; Monteles et al., 2021).
lenge for sustainable development in recent years (FAO, 2020). In The main way to assess or detect its loss is through its biotic condition.
Amazonia, since the 1970s, the advance of agricultural frontiers and However, because of its complex characteristics, this evaluation is not an
industrialization have increased the deterioration of natural resources easy task, contributing to the development of multiple methodologies
(Gardner et al., 2013; Moreira and Ribeiro, 2020), especially aquatic and indices. These indices try to reflect the multivariate nature of bio-
ecosystems exploited for diverse purposes (Lima et al., 2022). Among the logical systems using parameters that assess the conditions of individuals,
changes observed in these ecosystems are modifications in the physical populations, assemblages, and the surrounding landscape (Karr, 1981).
and chemical characteristics of water (Faria et al., 2021; Cruz et al., Among the groups most affected by anthropogenic changes are
2022) and the physical structure of streams, which affect local aquatic aquatic insects, with special emphasis on the Ephemeroptera, Plecoptera
biodiversity (Dala-Corte et al., 2016; Juen et al., 2016; Dala-Corte et al., and Trichoptera (EPT) because of their close relationships with envi-
2020). ronmental conditions (Abílio et al., 2007; Brasil et al., 2014; Faria et al.,

* Corresponding author.
E-mail addresses: [email protected] (M. Lima), [email protected] (A.P.J. Faria), [email protected] (L.S. Brasil), leandrojuen@
ufpa.br (L. Juen).

https://doi.org/10.1016/j.watbs.2022.100132
Received 9 August 2022; Received in revised form 28 November 2022; Accepted 15 December 2022
Available online 23 December 2022
2772-7351/© 2022 The Authors. Publishing services by Elsevier B.V. on behalf of KeAi Communications Co. Ltd. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

2017). The observed variations in taxonomic richness and composition of watershed of the Rio Capim, municipality of Paragominas, state of Para,
EPT insects, as well as their sensitivity to environmental disturbances Brazil, in June 2015 and September 2017 (Fig. 1). The annual rainfall
(Compin and Cer eghino, 2003; Faria et al., 2017) have made them average in the region is 2000 mm (Albuquerque et al., 2010), with a
important bioindicators of environmental quality for use in bio- well-defined dry season from June to November and a rainy season from
monitoring (Wong et al., 2020). This is because these organisms provide December to May (Menezes et al., 2015). The annual temperature
different biological responses and have distinct levels of tolerance to average is 26.3  C and the relative humidity is 81% (Alvares et al., 2013).
changing environmental conditions (Rosenberg, 1993; Roque et al., The municipality of Paragominas is considered one of the largest
2014), in addition to being cosmopolitan, abundant, and diverse in agro-industrial hubs in Para, influencing the regional socio-economic
freshwater ecosystems (Goulart and Callisto, 2003). development through mining, livestock pasturing, logging and farming
The biotic condition of the aquatic ecosystem can be assessed using (Lima et al., 2022). The intensification of these activities in the munici-
diversity metrics, such as taxonomic richness, abundance, and taxa di- pality has degraded water quality and physical habitat structure in recent
versity (García-Criado et al., 1999; Couceiro et al., 2012). These metrics decades (Gardner et al., 2013; Faria et al., 2021; Cruz et al., 2022). Thus,
can also be used to calculate biotic indexes that use pre-established scores we selected sites distributed in three treatments: multiple land-uses (12
of sensitivity and tolerance assigned to taxa relative to water body quality sites), conventional logging (8 sites) and native forests (reference, 12
(Resh and Jackson, 1993; Roche et al., 2010). Despite being less used in sites). Conventional logging includes illegal logging (e.g., Cardoso et al.,
Brazil than in other countries, the Biological Monitoring Working Party 2018), including in the riparian zone. The reference sites were located
(BMWP) has been adapted and employed in some Brazilian biomes with inside a dense primary forest fragment, representing the most preserved
excellent results in monitoring the condition of lotic and lentic ecosys- environmental condition in the region. Multiple land use sites were
tems (Cota et al., 2002; Oliveira and Callisto, 2010; Rezende et al., 2012; characterized by the occurrence of pasture, agriculture and mining sur-
Silva et al., 2016). It is based on family-level taxonomy and the relative rounding the site.
sensitivity of those taxa to water quality, traditionally organic wastes
(Hawkes, 1997). The Average Score per Taxon (ASPT) is also an index 2.2. Habitat Integrity Index (HII)
that uses BMWP scores to assess water quality (Walley and Hawkes,
1997). These indexes have the advantage of using a family-level taxo- An anthropogenic impact gradient on the sites was based on Habitat
nomic resolution of aquatic macroinvertebrates, which considerably Integrity Index (HII) scores (Nessimian et al., 2008). This index has
decreases application costs (Junqueira et al., 2000; Silva et al., 2016). proven to be a very efficient metric for assessing anthropogenic changes
In this context, our goal was to compare the sensitivity of the EPT- in aquatic ecosystems and their effects on aquatic insect communities
BMWP, EPT-ASPT, Shannon-Wiener EPT diversity, EPT taxa richness, (Brasil et al., 2020). The HII is used to visually assesses 12 types of
and EPT taxa abundance for assessing anthropogenic impacts on environmental variables within streams and their surroundings. Vari-
Amazonian streams. We expected that the EPT-BMWP and EPT-ASPT ables include types of land use in riparian zones, as well as their width
would be more sensitive in detecting environmental changes on and degree of preservation, sediment deposition in channels and reten-
streams than the other measures. tion mechanisms, bank structure, substrate types, flow, aquatic vegeta-
tion, and debris. This index scores sites from 0 to 1; scores near 0 indicate
2. Materials and methods a higher degree of degradation, whereas scores near 1 indicate more
preserved environments (Nessimian et al., 2008).
2.1. Study area

We sampled 32 stream sites from first to third order located in the

Fig. 1. Distribution of the land uses and the 32 sites sampled in the Capim River basin, Para, Brazil. The map was constructed using data from Project MapBio-
mas (2022).

2
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

2.3. Aquatic insect sampling Models using the "hnp" function (Moral et al., 2017). All analyses were
processed in R software (R Core Team, 2018) using the "car", "hnp",
A site of 150 m was delimited in each stream, divided into 10 equi- "vegan" and graphic "ggplot2" packages (Wickham, 2016; Moral et al.,
distant longitudinal sections of 15 m each. Subsequently, each section 2017; Fox and Weisberg, 2019; Oksanen et al., 2019).
was subdivided into three segments of 5 m, in which we collected EPT in
the first 10 m (first two segments) of each section by using a dip net (18 3. Results
cm diameter, 0.05 mm mesh). All 20 of the sub-samples were combined
into a single composite sample for each of the 32 sites, looking to collect 3.1. Description of aquatic insect assemblages
the widest possible variety of substrates (submerged leaves, sand, wood
debris, roots, vegetated banks and other fine sediment) and maximize A total of 4385 EPT specimens were collected, represented in 17
community variation. families, and distributed in 39 genera (Appendix A). Among the
This method has been successfully used in other studies for Ephem- Ephemeroptera, the most abundant families were the Leptophlebiidae (n
eroptera, Plecoptera and Trichoptera (EPT) collection in the Amazon ¼ 1722), Polymitarcyidae (n ¼ 751), Baetidae (n ¼ 80), Caenidae (n ¼
(Shimano and Juen, 2016; Shimano et al., 2018; Faria et al., 2017). The 39) and Euthyplociidae (n ¼ 35); the least abundant were the Lep-
organisms collected were separated in the field and fixed in 85% alcohol. tohyphidae (n ¼ 11). We found only one Plecoptera family, Perlidae (n ¼
The individuals were identified to the lowest possible taxonomic reso- 181). The most abundant Trichoptera families were the Hydropsychidae
lution (genus) using dichotomous keys (Hamada and Silva, 2014; Salles (n ¼ 747), Calamoceratidae (240), Leptoceridae (n ¼ 219), Poly-
et al., 2014; Pes et al., 2014). The collected specimens are deposited in centropodidae (n ¼ 188) and Glossossomatidae (n ¼ 105). The least
the Entomological Collection of Aquatic Insects of the Laboratory of abundant families were the Philopotamidae (n ¼ 50), Odontoceridae (n
Ecology and Conservation at the Federal University of Para (UFPA), ¼ 11), Ecnomidae (n ¼ 4) and Hidroptilidae (n ¼ 2).
Brazil.
3.2. Biological indicators versus land uses
2.4. Biological indexes
The EPT-BMWP classified more reference and conventional logging
The EPT-BMWP was calculated based on the values obtained by sites as having good water quality than multiple land-use sites (Table 1).
summing the number of EPT families found in each site with scores For example, 83.33% of the reference sites were classified as excellent
assigned to each family (1–10) according to their degree of resilience to and 16.67% as good. In conventional logging, 75% of the sites were
environmental disturbances. Scores close to 1 indicate the most tolerant classified as having excellent water quality, 12.5% as good, and 12.5% as
families to environmental disturbance, whereas values close to 10 the regular. In multiple land use areas, 50% of the sites were classified with
most sensitive families (Junqueira et al., 2000). The final scores for each excellent water quality, 16.66% good, 25% poor and 8.33% bad. For the
site correspond to biological water body categories. The higher the EPT-ASPT index, 100% of the sites in reference and conventional logging
EPT-BMWP score, the more preserved the site (Walley and Hawkes, areas were classified as clean water. Over 90% of the sites with multiple
1996, 1997; Buss et al., 2003; Junqueira et al., 2000). The scores ob- land use influences were classified as having clean water and only 8.33%
tained in the EPT-BMWP index classify water body quality into five as poor (Table 2).
categories: Category I (>81) classifies water quality as excellent, cate- The EPT-BMWP, Shannon-Wiener EPT index, EPT richness and EPT
gory II (80–61) as good, category III (60–41) as fair, category IV (40–26) abundance were significantly different among treatments (Fð2;29Þ ¼ 7.00;
as bad, and category V (<25) is poor. p ¼ 0.02; Fð2;29Þ ¼ 15.25; p  0.001; Fð2;29Þ ¼ 15.37; p  0.001 and Fð2;29Þ
The EPT-ASPT is calculated by dividing the EPT-BMWP score by the ¼ 11.41; p  0.001, respectively; Fig. 2). On the other hand, the EPT-
number of EPT families collected from the site (Walley and Hawkes, ASPT index showed no difference among treatments (Fð2;29Þ ¼ 0.20; p
1997). The EPT-ASPT score is divided into four classes: clean water (>6), ¼ 0.07) (Fig. 2). Of the 39 EPT genera collected, 19 were shared among
doubtful quality (5–6), moderate pollution (4–5), and severe pollution the three treatments; five were shared only between the multiple land use
(<4) (Gonçalves and Menezes, 2011; Silva et al., 2016). and reference areas, and five between conventional logging and refer-
We used the Shannon-Wiener index (H0 ) to estimate EPT diversity as a ence. Within each treatment, nine genera were exclusive, with three from
function of the uniformity and richness of EPT genera collected from a multiple land uses and six from reference sites (Fig. 3).
site. EPT taxa richness is simply the number of EPT genera and EPT taxa For both the EPT-BMWP and the Shannon-Wiener EPT index, sites
abundance is the number of EPT individuals. from reference and conventional logging areas were more similar (p ¼
0.075; p ¼ 0.082, respectively), but both differed from sites within the
2.5. Data analysis multiple land use mosaic (p  0.001; p < 0.001, respectively). For EPT
richness the reference sites differed from those in both conventional
To assess the effectiveness of EPT richness, EPT abundance, Shannon- logging and multiple land uses (p  0.001; p  0.001, respectively;
Wiener EPT diversity, EPT-BMWP and EPT-ASPT metrics among treat- Fig. 3). However, streams in conventional logging areas and multiple
ments we performed a Variance Analysis (ANOVA, one-way) followed by land uses were similar (p ¼ 0.31) (Fig. 2). Reference sites had ten more
Tukey's post hoc test. For the ANOVA, we tested the assumptions of ho- genera than conventional logging sites and 13 more than multiple land
moscedasticity and normality of the residuals (Legendre and Legendre, use sites.
1998).
To assess if the EPT-BMWP and EPT-ASPT were more sensitive in 3.3. Relationships between HII scores and biotic indicators
detecting environmental changes in sites than other diversity measures
we used Generalized Linear Models (GLM). In the model, EPT richness, EPT richness (t ¼ 4.506; p < 0.001; r2 ¼ 0.44), EPT abundance (z ¼
EPT abundance, Shannon-Wiener EPT index, EPT-BMWP and EPT-ASPT 2.920; p ¼ 0.003; r2 ¼ 0.29), Shannon-Wiener EPT diversity (t ¼ 4.365; p
index scores were the response variables and the HII scores were the < 0.001; r2 ¼ 0.38) and EPT-BMWP index (t ¼ 3.225; p ¼ 0.003; r2 ¼
predictor variables. We used the appropriate distribution family for each 0.25) were positively related to HII scores (Table 1; Fig. 4). However,
GLM model: (i) Quasi Poisson distribution family for EPT richness; (ii) EPT-ASPT showed no significant relationship with HII (t ¼ 0.456; p ¼
Negative binomial for EPT abundance, and (iii) Gaussian distribution 0.668).
family for the EPT-BMWP, EPT-ASPT, and Shannon-Wiener EPT index.
The generated models were validated through Simulated Envelope

3
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

Table 1
Generalized Linear Model (GLM) results showin the relationships between EPT taxa richness, EPT abundance, EPT Shannon-Wiener diversity, EPT-BMWP, and EPT-
ASPT with the anthropogenic disturbance gradient represented by the Habitat Integrity Index (HII). Values in bold correspond to significant results at a P < 0.003.
METRICS Estimate (β) Std. Error t-value r2 Pr(>|t|)

EPT Richness Intercept 0.8851 0.3802 2.328 0.44 0.0269


HII 2.2707 0.5039 4.506 <0.001*
Estimate (β) Std. Error z-value Pr(>|z|)
EPT Abundance Intercept 3.321 0.540 6.147 0.29 7.91010**
HII 2.269 0.777 2.920 0.003*
Estimate (β) Std. Error t-value P(>|t|)
Shannon-Wiener EPT diversity Intercept 0.00482 0.37254 0.013 0.38 0.9897
HII 2.34184 0.53650 4.365 <0.001*
Estimate (β) Std. Error t-value P(>|t|)
EPT BMWP Intercept 35.37 15.92 2.222 0.25 0.0340
HII 73.96 22.93 3.225 0.003*
Estimate (β) Std. Error t-value P(>|t|)
EPT ASPT Intercept 7.3244 0.4367 16.774 – 2e-16
HII 0.2866 0.6288 0.456 0.652

4. Discussion taxonomic refinement (Metcalfe, 1989; Cairns and Pratt, 1993; Eriksen
et al., 2021). Even if it is possible to calculate diversity indices with
EPT richness, EPT abundance, Shannon-Wiener EPT diversity and identification at the family level, the precision and accuracy are greater
EPT-BMWP were sensitive to a gradient in physical habitat structure as when the taxonomic resolution is more refined using identification at the
reflected by HII scores. However, the EPT-ASPT showed no difference genus or species level.
among the three land use treatments and was not significantly related to Widely used in stream water quality monitoring in Europe, the BMWP
the HII. Furthermore, Shannon-Wiener EPT-diversity and the EPT-BMWP biotic index has proven to be an excellent tool in environmental moni-
showed the same response pattern for reference and conventional log- toring of benthic macroinvertebrates, especially aquatic insects (Romero
ging sites, although both distinguished the reference from multiple land et al., 2017; Magall on et al., 2021). An important advantage of the
use sites, The multiple land use sites, which had the lowest biotic index EPT-BMWP is that by employing family-level binary taxonomic data, one
scores, are related to the widespread agricultural, pasture, and mining can classify site water body quality with reduced time and money
activities carried out in the region. Such activities compact the soil, (Walley and Hawkes, 1996; Cota et al., 2002). Of course, the same could
intensify erosion (Tanaka et al., 2015), degrade riparian forests, and lead be said of family-level EPT richness (Oliveira et al., 2011; Silva et al.,
to eutrophication (Hepp et al., 2010; Attanasio et al., 2012), compro- 2017). The basis of this evaluation is the existing relationship between
mising site water quality and physical habitat structure (Calv~ao et al., the biological assemblage and the environment, the more balanced and
2018). These changes directly affect biotic condition by reducing integrated the assemblage is, the better the condition of the environment,
microhabitat availability, and food resources (Shimano et al., 2012; Lima and vice versa (Karr and Dudley, 1981).
et al., 2022). Multimetric indices and richness and tolerance metrics have been
In our results, sites located in a multi-use area showed the lowest EPT- commonly used in Latin American nations (70% of applications), with
BMWP scores, corroborating with the results of studies conducted in the BMWP/ASPT being the most frequently used (Eriksen et al., 2021). But
southeastern region of Brazil (Cota et al., 2002; Rezende et al., 2012). see Ruaro et al. (2020) regarding multimetric indices. Often, the
The similarity in EPT-BMWP scores and in reference and conventional BMWP/ASPT has been able to robustly measure the impacts arising from
logging areas may be related to the presence of riparian forests. In a wide variety of anthropogenic activities in different types of rivers,
contrast, sites in multiple use areas had no or highly altered riparian habitats, and ecoregions (García-Criado et al., 1999; Oliveira and
forest, thus yielding low scores. Nevertheless, the results reinforce the Callisto, 2010; Romero et al., 2017; Magall on et al., 2021). In Brazil, the
importance of maintaining riparian forests in protecting the ecological adaptations made by Junqueira and Campos (1998) and Junqueira et al.
and biotic condition of small Amazonian streams (Leal et al., 2020). (2000), facilitated use of the BMWP for tropical streams (Cota et al.,
EPT richness was the only indicator that significantly differentiated 2002; Roche et al., 2010; Silva et al., 2016) demonstrating the efficiency
reference sites from both conventional logging and multiple land use of this index in assessing changes in different biomes and under different
sites, but not between multiple land use sites and conventional logging types of impacts related to deforestation, siltation, agricultural uses, and
sites. For EPT richness, the taxonomic resolution employed was genus, mining (Eriksen et al., 2021). However, in some index applications, the
which clearly differentiated this metric from the EPT-BMWP index. EPT BMWP failed to separate sites based on a pollution gradient, attributable
richness requires a more refined taxonomic resolution so that the sensi- to biogeographical differences (Ochieng et al., 2020). One of the reasons
tivity of the index is not lost as a result of the wide variation in tolerance for the inefficiency of BMWP in some situations is its need to be cali-
that exists between individuals belonging to the families Baetidae, Cae- brated to the natural environmental gradients of each region (García--
nidae and Hydropsychidae (Minaya et al., 2013; Mbaka et al., 2014; Criado et al., 1999; Cota et al., 2002). Also, because it uses binary data
Lakew and Moog, 2015; Kabore et al., 2016; Masese et al., 2017). and is based on family-level taxonomy, the scores given to families
Although EPT richness is an excellent metric for assessing biotic condi- should consider which genera occur in the region studied and their
tion, it requires more refined taxonomic resolution, thus more time and relative tolerances so that the scores given to families are consistent with
financial resources to score (Shimano et al., 2018). Its application, the BMWP conceptual model (Walley and Hawkes, 1996; Ochieng et al.,
therefore, may be advised when aiming for a more accurate and precise 2020). But this is a potential problem for all tolerance-based indicators,
environmental assessment (Stoddard et al., 2008). indicating the need to quantitatively analyze large data sets along a
The Shannon-Wiener EPT diversity index and the EPT-BMWP had multivariate disturbance gradient to determine more consistent family-
similar responses to environmental condition. When applied to envi- and genus-level tolerance values (Whittier and Van Sickle, 2010).
ronmental assessment, both indices circumvented some recurrent diffi- Other authors have developed predictive multimetric indices to in-
culties in saprobic and biotic indexes (Metcalfe, 1989; Cairns and Pratt, crease the reliability of their results (e.g., Moya et al., 2011; Macedo
1993; Eriksen et al., 2021). However, diversity indices end up being less et al., 2016; Chen et al., 2017; Silva et al., 2017). However, these also
indicated when looking for quick answers because they need greater have limitations because of their greater mathematical complexity

4
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

Table 2
EPT-BMWP and EPT-ASPT index scores and condition classifications.
Treatments Sites Category Color BMWP Quality ASPT Quality

MULTIPLE LAND
USES

CONVENTIONAL
LOGGING

REFERENCE

(Mugnai et al., 2011), specific reference values (Dedieu et al., 2015; based on the Petersen protocol (1992) to visually assess the environ-
Zagarola et al., 2017), the need for sufficiently large datasets (Blakely mental conditions of stream sites considering land use relationships, ri-
et al., 2014), and sufficient environmental data, and the greater technical parian zone, bed characteristics, channel morphology, and flow. Similar
expertise needed for model development (Eriksen et al., 2021). Thus, the qualitative visual estimators of stream anthropogenic disturbance have
BMWP remains an important assessment tool when time and financial been employed for assessing physical habitat quality of USA streams
resources are limited, especially in developing countries like Brazil, (Hughes et al., 2010; Kaufmann et al., 2022b). Despite being a simple
where biology is not part of the water quality assessment system, even protocol composed of 12 parameters, it has great power to represent the
though legislation recommends its use (Brasil, 2005). environmental conditions and separate dissimilar streams in statistical
We observed that the EPT-ASPT was less able than the EPT-BMWP to analyses. Even though it is a physical habitat index, its capacity for
detect differences in water body condition as estimated by the HII. This assessing anthropogenic pressures on stream sites is often greater than
result occurs because ASPT is simply an average (BMWP/number of those of the biotic indices used in our study. Kaufmann et al. (2022a) also
families), meaning that it reduces the range in BMWP scores to a simple reported that indicators of streambed stability, riparian vegetation cover,
mean. and instream habitat heterogeneity had higher precision than commonly
EPT diversity metrics and the EPT-BMWP index were positively used macroinvertebrate metrics in the USA (Stoddard et al., 2008) as well
related to the HII. The HII was developed by Nessimian et al. (2008) as highly significant levels of responsiveness to various types of

5
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

Fig. 2. Boxplots showing the effects of multiple land uses, conventional logging and reference on site biological indicators. Letters indicate statistically significant
differences in the ANOVA test with Tukey's post-hoc test.

results, the HII, EPT diversity metrics, and the EPT-BWMP index when
evaluated together are excellent for assessing the environmental condi-
tion of sites influenced by different land uses.
Forested aquatic systems had higher indicator scores because they
contribute to greater riparian vegetation cover, channel canopy cover,
bed stability, environmental heterogeneity, dissolved oxygen levels, and
allochthonous energy inputs (Allan, 2004; Luiza-Andrade et al., 2017;
Alvarenga et al., 2021). All those factors are favorable to the maintenance
of stream EPT assemblages (Allan, 2004; Shimano et al., 2012; Brasil
et al., 2014) and functional diversity (Alvarenga et al., 2021; Lima et al.,
2022).

5. Conclusion

Although the richness and diversity indices performed slightly better,


the EPT-BMWP biotic index is feasible as a fast, practical, and responsive
tool in stream biological monitoring programs in Amazonia. However,
we suggest that future applications of the BMWP index be adapted to the
conditions of the Amazon biome, such as the inclusion of local taxa to
obtain more robust and reliable results and better adequacy of the ASPT
index. Furthermore, our results reinforce the efficiency and importance
of using aquatic insects in assessing environmental quality in streams
Fig. 3. Shared and exclusive genera of the treatments.
subjected to different anthropogenic activities. Lastly, it shows the
importance of proposing mitigating actions for conserving aquatic
anthropogenic disturbances (Kaufmann et al., 2022b). The HII is ecosystem biodiversity.
commonly used in environmental assessment programs to measure
anthropogenic impacts on tropical aquatic ecosystems and their influ- CRediT authorship contribution statement
ence on aquatic biodiversity (Cunha and Juen, 2017; De Paiva et al.,
2017). Brasil et al. (2020) showed that HII is a good predictor for aquatic Jady Vivia Almeida da Silva Santos: Conceptualization, Method-
organisms, especially insects, in different land uses and regions of Brazil. ology, Data curation, Formal analysis, Writing – original draft. Myllena
Its success as a predictor is because the index relates site biotic condition Lima: Conceptualization, Methodology, Data curation, Formal analysis,
to the dependence of organisms on environmental heterogeneity (Nes- Writing – original draft. Josinete Sampaio Monteles: Conceptualiza-
simian et al., 2008; Oliveira-Junior et al., 2015). Thus, based on our tion, Writing – original draft. Daiany Larissa Ribeiro Carrera: Visual-
ization, Writing – review & editing. Ana Paula Justino de Faria:

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J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

Fig. 4. Relationship of EPT richness (A), EPT abundance (B), Shannon-Wiener EPT diversity (C) and EPT-Biotic Biological Monitoring Party (BMPW) (D) along an
anthropogenic disturbance gradient represented by the Habitat Integrity Index (HII). Higher HII scores indicate better physical habitat quality.

Visualization, Writing – review & editing. Leandro Schlemmer Brasil: Albuquerque, M.F., Souza, E.B., Oliveira, M.C.F., Souza-Junior, J.A., 2010. Precipitaç~ao
nas mesorregi~ oes do Estado do Para: climatologia, variabilidade e tend^encias nas
Visualization, Writing – review & editing. Leandro Juen: Conceptuali-
últimas decadas (1978-2008). Revista Brasileira de Climatologia 6 (6), 151–168.
zation, Funding acquisition, Visualization, Writing – review & editing, Allan, J.D., 2004. Landscapes, and riverscapes, the influence of land use on stream
Supervision. ecosystems. Annu. Rev. Ecol. Evol. Syst. 35 (1), 257–284.
Alvarenga, L.R.P., Pompeu, P.S., Leal, C.G., Hughes, R.M., Leitao, R.P., 2021. Land-use
changes affect the functional structure of stream ichthyofauna in the Brazilian
Declaration of competing interest Savanna. Neotrop. Ichthyol. 19 (3), e210035.
Alvares, C.A., Stape, J.L., Sentelhas, P.C., Goncalves, J.L.M., Sparovek, G., 2013. Koppen's
climate classification map for Brazil. Meteorol. Z. 22 (6), 711–728.
The authors of the manuscript declare that they have no conflict of Attanasio, C.M., Gandolfi, S., Zakia, M.J.B., Veniziani Junior, J.C.T., Lima, W.P.A., 2012.
interest. A import^ancia das areas riparias para a sustentabilidade hidrol ogica do uso da terra
em microbacias hidrol ogicas. Bragatina 71 (4), 403–501.
Blakely, T.J., Eikaas, H.S., Harding, J.S., 2014. The Singscore: a macroinvertebrate biotic
Funding index for assessing the health of Singapore's streams and canals. Raffles Bull. Zool. 62.
Brasil. Resolution CONAMA 357, 2005. Conselho nacional de Meio ambiente. Available
in. www.mma.gov.br/port/conama/res/res05/res35705.pdfgt;. Acesso em: 22 mar.
We thank Cikel LTDA, 33 Forest, Instituto de Floresta Tropical (IFT), 2022.
Biodiversity Research Consortium (BRC) and Hydro Paragominas Com- Brasil, L.S., Juen, L., Batista, J.D., Pavan, M.G., Cabette, H.S.R., 2014. Longitudianl
pany for financing and logistical support; the National Council for Sci- distribuition of the funcional feeding groups of aquatic insects in streams of the
Brazilian cerrado savanna. Neotrop. Entomol. 43 (5), 421–428.
entific and Technological Development (CNPq) for financing (process no. Brasil, L.S., Lima, E.L., Spigoloni, Z.A., Ribeiro-Brasil, D.R.G., Juen, L., 2020. The Habitat
449315/2014–2 and process no. 481015/2011–6); Coordenaç~ao de Integrity Index and aquatic insect communities in tropical streams: a meta-analysis.
Aperfeiçoamento de Pessoal de Nível Superior (CAPES, process no. Ecol. Indicat. 116 (1–7), 106495, 11.
Buss, D.F., Baptista, D., Nessimian, J.L., 2003. Bases conceituais para aplicaç~ao de
88887.615447/2021–00) to ML; the National Council for Scientific and biomonitoramento em programas de avaliaç~ao da qualidade da agua de rios. Cad.
Technological Development (CNPq) for the Scientific Initiation Fellow- Saúde Pública 19 (2), 465–473.
ship for JVASS and the productivity fellowship in research to LJ (process Cairns, J., Pratt, J.R., 1993. A history of biological monitoring using benthic
macroinvertebrates. Freshwater biomonitoring and benthic macroinvertebrates
nº. 304710/2019–9) and to LSB (process nº. 305929/2022–4). This paper
10–27.
is number BRC0024 in the publication series of the BRC. Calvao, L.B., Juen, L., Oliveira-Junior, J.M.B., Batista, J.D., De Marco, P., 2018. Land use
modifies Odonata diversity in streams of the Brazilian Cerrado. J. Insect Conserv. 22,
675–685.
Appendix A. Supplementary data Cardoso, M.N., Calv~ao, L.B., Montag, L.F.A., Godoy, B.S., Juen, L., 2018. Reducing the
deleterious effects of logging on Ephemeroptera communities through reduced
Supplementary data to this article can be found online at https:// impact management. Hydrobiologia 823, 191–203.
Chen, K., Hughes, R.M., Brito, J.G., Leal, C.G., Leitao, R.P., Oliveira-Junior, J.M.B.,
doi.org/10.1016/j.watbs.2022.100132. Oliveira, V.C., Dias-Silva, K., Ferraz, S.F.B., Ferreira, J., Hamada, N., Juen, L.,
Nessimian, J.L., Pompeu, P.S., Zuanon, J., 2017. A multi-assemblage, multi-metric
References biological condition index for eastern Amazon streams. Ecol. Indicat. 78, 48–61.
Compin, A., Cereghino, R., 2003. Sensitivity of aquatic insect species richness to
disturbance in the Adour–Garonne stream system (France). Ecol. Indicat. 3 (2),
Abilio, F.J.P., Ruffo, T.L.M., Souza, A.H.F.F., Florentino, H.S., Oliveira-Junior, E.T., 135–142.
Meireles, B.N., Santana, A.C.D., 2007. Macroinvertebrados bent^ onicos como
bioindicadores de qualidade Ambiental de corpos Aquaticos da Caatinga. Oecologia
Brasiliensis 11 (3), 397–409.

7
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

Cota, L., Goulart, M., Callisto, M., 2002. Rapid assessment of river water quality using an Lakew, A., Moog, O., 2015. A multimetric index based on benthic macroinvertebrates for
adapted BMWP index: a practical tool to evaluate ecosystem health. Annu. Rev. assessing the ecological status of streams and rivers in central and southeast
Entomol. 28, 1–4. highlands of Ethiopia. Hydrobiologia 751 (1), 229–242.
Couceiro, S.R.M., Hamada, N., Forsberg, B.R., Pimentel, T.P., Luz, S.L.B., 2012. Leal, C.G., Lennox, G.D., Ferraz, S.F., Ferreira, J., Gardner, T.A., Thomson, J.R.,
A macroinvertebrate multimetric index to evaluate the biological condition of Barlow, J., 2020. Integrated terrestrial-freshwater planning doubles conservation of
streams in the Central Amazon region of Brazil. Ecol. Indicat. 18, 118–125. tropical aquatic species. Science 370 (6512), 117–121.
Cruz, G.M., Faria, A.P.J., Juen, L., 2022. Patterns and Metacommunity Structure of Legendre, P., Legendre, L., 1998. Numerical Ecology. Elsevier, p. 1006.
Aquatic Insects (Trichoptera) in Amazonian Streams Depend on the Environmental Lima, M., Firmino, V.C., Paiva, C.K.S., Juen, L., Brasil, L.S., 2022. Land use changes
Conditions. Hydrobiologia, pp. 1–13. disrupt streams and affect the functional feeding groups of aquatic insects in the
Cunha, E.J., Juen, L., 2017. Impacts of oil palm plantations on changes in environmental Amazon. J. Insect Conserv. 1–12.
heterogeneity and Heteroptera (Gerromorpha and Nepomorpha) diversity. J. Insect Luiza-Andrade, A., Brasil, L.S., Benone, N.L., Shimano, Y., Farias, A.P.J., Montag, L.F.A.,
Conserv. 21 (1), 111–119. Juen, L., 2017. Influence of oil palm monoculture on the taxonomic and functional
Dala-Corte, R.B., Giam, X., Olden, J.D., Becker, F.G., Guimaraes, T.D.F., Melo, A.S., 2016. composition of aquatic insect communities in eastern Brazilian Amazonia. Ecol.
Revealing the pathways by which agricultural land-use affects stream fish Indicat. 82, 478–483.
communities in South Brazilian grasslands. Freshw. Biol. 61 (11), 1921–1934. Macedo, D.R., Hughes, R.M., Ferreira, W.R., Firmiano, K.R., Silva, D.R.O., Ligeiro, R.,
Dala-Corte, R.B., Melo, A.S., Siqueira, T., Bini, L.M., Martins, R.T., Cunico, A.M., et al., Kaufmann, P.R., Callisto, M., 2016. Development of a benthic macroinvertebrate
2020. Thresholds of freshwater biodiversity in response to riparian vegetation loss in multimetric index (MMI) for neotropical savanna headwater streams. Ecol. Indicat.
the Neotropical region. J. Appl. Ecol. 57 (7), 1391–1402. 54, 132–141.
De Paiva, C.K.S., Faria, A.P.J., Calvao, L.B., Juen, L., 2017. Effect of oil palm on the Magallon, O., Guillermo, C.E.G., Lopez-Lopez, E., Jacinto Sedeno-Diaz, J.E.,
Plecoptera and Trichoptera (Insecta) assemblages in streams of castern Amazon. Hernandez, M.L., Arroyo-Damian, M., Moncayo-Estrada, R., 2021. Water quality
Environ. Monit. Assess. 189 (8), 393. analysis in a subtropical river with an adapted biomonitoring working party (BMWP)
Dedieu, N., Clavier, S., Regis, V., Cerdan, P., Cereghino, R., 2015. A Multimetric index. Diversity 11, 606.
Macroinvertebrate Index for the Implementation of the European Water Framework Masese, F.O., Raburu, P.O., 2017. Improving the performance of the EPT Index to
Directive in French Guiana, East Amazonia. River Res. Appl. 32 (3), 1–15. accommodate multiple stressors in Afrotropical streams. Afr. J. Aquat. Sci. 42 (3),
Eriksen, T., Brittain, J.E., Soli, G., Jacobsen, D., Goethals, P., Friberg, N., 2021. A global 219–233.
perspective on the application of riverine macroinvertebrates as biological indicators Mbaka, J.G., M'Erimba, C.M., Thiongo, H.K., Mathooko, J.M., 2014. Water and habitat
Africa, South-Central America, Mexico and Southern Asia. Ecol. Indicat. 126, quality assessment in the Honi and Naro Moru rivers, Kenya, using benthic
107–609. macroinvertebrate assemblages and qualitative habitat scores. Afr. J. Aquat. Sci. 39
Faria, A.P.J.E., Ligeiro, R., Callisto, M., Juen, L., 2017. Response of aquatic insecta (4), 361–368.
assemblages to the activities of traditional populations in eastern Amazonia. Menezes, F.P., Fernandes, L.L., Rocha, E.J., 2015. O uso da estatística para regionalizaç~ao
Hydrobiologia 802 (1), 39–51. da precipitaç~ao no Estado do Para, Brasil. Revista Brasileira de Climatologia 16,
Faria, A.P.J., Paiva, C.K.S., Calvao, L.B., Cruz, G.M., Juen, L., 2021. Response of aquatic 64–71, 0.
insects to an environmental gradient in Amazonian streams. Environ. Monit. Assess. Metcalfe, J.L., 1989. Biological water quality assessment of running waters based on
193, 763. macroinvertebrate communities: history and present status in Europe. Environ.
Fox, J., Weisberg, S., 2019. An {R} Companion to Applied Regression, p. 447. Thousand Pollut. 60 (1–2), 101–139.
Oak CA. Miguel, T.B., Oliveira-Junior, J.M.B., Ligeiro, R., Juen, L., 2017. Odonata (Insecta) as a
Garcia-Criado, F., Tome, A., Vega, F.J., Antolin, C., 1999. Performance of some diversity tool for the biomonitoring of environmental quality. Ecol. Indicat. 81 (2017),
and biotic indices in rivers affected by coal mining in northwestern Spain. 555–566.
Hydrobiologia 394, 209–217. Minaya, V., McClain, M.E., Moog, O., Omengo, F., Singer, G.A., 2013. Scale-dependent
Gardner, T.A., Ferreira, J., Barlow, J., Lees, A.C., Parry, L., Vieira, I.C.G., Zuanon, J., effects of rural activities on benthic macroinvertebrates and physico-chemical
2013. A social and ecological assessment of tropical land uses at multiple scales: the characteristics in headwater streams of the Mara River, Kenya. Ecol. Indicat. 32,
Sustainable Amazon Network. Phil. Trans. Biol. Sci. 368 (1619), 20120166. 116–122.
Goncalves, F.B., Menezes, M.S., 2011. Uma analise comparativa de índices bi oticos que Monteles, J.S., Gerhard, P., Ferreira, A., Sonoda, K.C., 2021. Agriculture impacts benthic
utilizam Macroinvertebrados avaliar a qualidade da agua em um rio costeiro do insects on multiple scales in the Eastern Amazon. Biol. Conserv. 255, 108–998.
estado do Paran a, sul do Brasil. Biota Neotropica 11 (4), 27–36. Moral, R.A., Hinde, J., Demetrio, C.G.B., 2017. Half- normal plots and overdispersed
Goulart, M.D., Callisto, M., 2003. Bioindicadores de qualidade de agua como ferramenta models in R: the hnp package. J. Stat. Software 8 (10), 1–23.
em estudos de impacto ambiental. Revista da FAPAM 2 (1), 156–164. Moya, N., Hughes, R.M., Dominguez, E., Gibon, F.M., Goita, E., Oberdorff, T., 2011.
Hamada, N., Silva, J.O., 2014. Ordem Plecoptera. In: Hamada, N., Nessimian, J.L., Macroinvertebrate-based multimetric predictive models for measuring the biotic
Querino, R.B. (Eds.), Insetos aquaticos na Amaz^ onia Brasileira: taxonomia, biologia e condition of Bolivian streams. Ecol. Indicat. 11, 840–847.
ecologia. Instituto Nacional de Pesquisas da Amaz^ onia, Manaus, Amaz^ onia, Mugnai, R., Buss, D.F., Oliveira, R.B., Sanfins, C., Carvalho, A.D.L., Baptista, D.F., 2011.
pp. 283–288. Application of the biotic index IBE-IOC for water quality assessment in wadeable
Hawkes, H.A., 1997. Origin and development of the biological monitoring working party streams in south-east Brazil. Acta Limnol. Bras. 23, 74–85.
score system. Water Res. 32, 964–968. https://doi.org/10.1016/S0043-1354(97) Nessimian, J.L., Venticinque, E., Zuanon, J., De Marco, P., Gordo, M., Fidelis, L.,
00275-3. Batista, J.D., Juen, L., 2008. Land use, habitat integrity, and aquatic insect
Hepp, L.U., Milesi, S.V., Biasi, C., Restello, R.M., 2010. Effects of agricultural and urban assemblages in Central Amazonian streams. Hydrobiologia 614 (1), 117–137.
impacts on macroinvertebrate assemblages in streams (Rio Grande do Sul, Brazil). Ochieng, H., Odong, R., Okot-Okumu, J., 2020. Comparison of temperate and tropical
Zool. 27 (1), 106–113. versions of biological monitoring working party (BMWP) index for assessing water
Hughes, R.M., Herlihy, A.T., Kaufmann, P.R., 2010. An evaluation of qualitative indexes quality of river aturukuku in eastern Uganda. Global Ecology and Conservation 23,
of physical habitat applied to agricultural streams in ten U.S. states. J. Am. Water e01183. https://doi.org/10.1016/j.gecco.2020.e01183.
Resour. Assoc. 46, 792–806. Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D.,
Juen, L., Cunha, E.J., Carvalho, F.G., Ferreira, M.C., Begot, T.O., Luiza-Andrade, A., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H.H., Szoecs, E.,
Shimano, Y., Leao, H., Pompeu, P.S., Montag, L.F.A., 2016. Effects of oil palm Wagner, H., 2019. Vegan: community Ecology package. R package version 2.5-6. http
plantations on the habital structure and biota of streams in Eastern Amazon. River s://CRAN.R-project.org/package¼vegan.
Res. Appl. 32 (10), 2081–2094. Oliveira, A., Callisto, M., 2010. Benthic macroinvertebrates as bioindicators of water
Junqueira, V.M., Campos, S.C.M., 1998. Adaptation of the “BMWP” method for water quality in an Atlantic Forest fragment. Iheringia. Serie Zool. 100, 291–300.
quality evaluation to Rio das Velhas watershed (Minas Gerais, Brazil). Acta Limnol. Oliveira, R.B.S., Baptista, D.F., Mugnai, R., Castro, C.M., Hughes, R.M., 2011. Towards
Bras. 10 (2), 125–135. rapid bioassessment of wadeable streams in Brazil: development of the Guapiaçu-
Junqueira, M.V., Amarante, M.C., Dias, C.F.S., Franca, E.S., 2000. Biomonitoramento da Macau Multimetric Index (GMMI) based on benthic macroinvertebrates. Ecol.
qualidade das  aguas da Bacia do Alto Rio das Velhas (MG/Brasil) atraves de Indicat. 11, 1584–1593.
macroinvertebrados. Acta Limnol. Bras. 12 (1), 73–87. Oliveira-Junior, J.M.B., Shimano, Y., Gardner, T.A., Hughes, R.M., De Marco, P., Juen, L.,
Kabore, I., Moog, O., Alp, M., Guenda, W., Koblinger, T., Mano, K., Melcher, A.H., 2016. 2015. Neotropical dragonflies (Insecta: odonata) as indicators of ecological condition
Using macroinvertebrates for ecosystem health assessment in semi-arid streams of of small streams in the eastern Amazon. Austral Ecol. 40 (6), 733–744.
Burkina Faso. Hydrobiologia 766 (1), 57–74. Pes, A.M., Santos, A.P.M., Silva, P.B., De Camargos, L.M., 2014. Ordem Trichoptera. In:
Karr, J.R., 1981. Assessment of biotic integrity using fish communities. Fisheries 6 (6), Hamada, N., Nessimian, J., Querino, R.B. (Eds.), Insetos aquaticos na Amaz^ onia
21–27. brasileira:taxonomia, biologia e ecologia. Instituto Nacional de Pesquisas da
Karr, J., Dudley, D.R., 1981. Ecological perspective on water quality goals. Environ. Amaz^ onia, Manaus, Amazonas, pp. 129–140.
Manag. 5 (1), 55–68. Project MapBiomas - collection 6 of Brazilian land cover & use map series. accessed on
Kaufmann, P.R., Hughes, R.M., Paulsen, S.G., Peck, D.V., Seeliger, C.W., Weber, M., October 19th, through the link: https://mapbiomas.org/download.
Mitchell, R.M., 2022a. Physical habitat in conterminous US streams and rivers, part 1: Resh, V.H., Jackson, J.K., 1993. In: Rosenberg, D.M., Resh, V.H. (Eds.), Rapid Assessment
geoclimatic controls and anthropogenic alteration. Ecol. Indicat. https://doi.org/ Approaches to Biomonitoring Using Benthic Macroinvertebrates, Freshwater
10.1016/j.ecolind.2022.109046. Biomonitoring and Benthic Macroinvertebrates. Chapman and Hall, New York,
Kaufmann, P.R., Hughes, R.M., Paulsen, S.G., Peck, D.V., Seeliger, C., Kincaid, T., pp. 195–233.
Mitchell, R.M., 2022b. Physical habitat in conterminous US streams and rivers, part Rezende, R.S., Dos Santos, M.A., Goncalves Junior, J.F., 2012. Avaliaç~ao ambiental do rio
2: quantitative assessment of condition. Ecol. Indicat. https://doi.org/10.1016/ Pandeiros utilizando macroinvertebrados como indicadores de qualidade da agua.
j.ecolind.2022.109047. Ecol. Austral 22 (3), 159–169.

8
J.V.A.S. Santos et al. Water Biology and Security 2 (2023) 100132

Roche, K.F., Queiroz, E.P., Righi, K.O., de Souza, G.M., 2010. Use of the BMWP and ASPT Silva, K.W.D.S., Everton, N.D.S., Melo, M.A.D.D., 2016. Aplicaç~ao dos índices biol ogicos
indexes for monitoring environmental quality in a neotropical stream. Acta Limnol. Biological Monitoring Working Party e Average Score per Taxon para avaliar a
Bras. 22 (1), 105–108. qualidade de agua do rio Ouricuri no Município de Capanema, Estado do Para, Brasil.
Romero, K.C., Del Rio, J.P., Villarreal, K.C., Anillo, J.C.C., Zarate, Z.P., Gutierrez, L.C., Revista Pan-Amaz^ onica de Saúde 7 (3), 13–22.
Valencia, J.W.A., 2017. Lentic water quality characterization using Silva, D.R.O., Herlihy, A.T., Hughes, R.M., Callisto, M., 2017. An improved
macroinvertebrates as bioindicators: an adapted BMWP index. Ecol. Indicat. 72, macroinvertebrate multimetric index for the assessment of wadeable streams in the
53–66. neotropical savanna, Brazil. Ecol. Indicat. 81, 514–525.
Roque, F.O., Buss, D.F., Abes, S.S., Stefanes, M., Juen, L., Siqueira, T., 2014. Insetos Stoddard, J.L., Herlihy, A.T., Peck, D.V., Hughes, R.M., Whittier, T.R., Tarquinio, E., 2008.
aquaticos no ambito de instrumentos de gest~ao ambiental caminhos ainda pouco A process for creating multi-metric indices for large-scale aquatic surveys. J. North
explorados. In: Hamada, N., Nessimian, J.L., Querino, R.B. (Eds.), Insetos aquaticos Am. Benthol. Soc. 27, 878–891.
na Amaz^ onia brasileira: taxonomia, biologia e ecologia. Instituto Nacional de Tanaka, M.S., Souza, A.L.T., Oliveira, A.K., Moschini, L.E., 2015. Redund^ancia entre
Pesquisas da Amaz^ onia, Manaus, Amazonas, pp. 129–140. metricas da qualidade ambiental de riachos em paisagem agrícola. Revista Ambiente
Rosenberg, D.M., 1993. Introduction to Freshwater Biomonitoring and Benthic & agua 10 (4), 833–845.
Macroinvertebrates in Freshwater Biomonitoring and Benthic Macroinvertebrates. Walley, W.J., Hawkes, H.A., 1996. A computer-based reappraisal of the biological
Chapman and Hall, New York, 1993. monitoring working part scores using data from the 1990. River quality survey of
Ruaro, R., Gubiani, E.A., Hughes, R.M., Mormul, R.P., 2020. Global trends and challenges england and wales. Water Res. 30 (9), 2086–2094.
in multimetric indices of ecological condition. Ecol. Indicat. 110. https://doi.org/ Walley, W.J., Hawkes, H.A., 1997. A computer-based development of the Biological
10.1016/j.ecolind.2019.105862. Monitoring Working Party score system incorporating abundance rating, site type
Salles, F.F., Nascimento, J.M.C., Cruz, P.V., Boldrini, R., Belmont, E.L.L., 2014. Ordem and indicator value. Water Res. 31 (2), 201–210.
Ephemeroptera. In: Hamada, N., Nessimian, J.L., Querino, R.B. (Eds.), Insetos FAO, IFAD, UNICEF, WFP, WHO, 2020. The State of Food Security and Nutrition in the
aquaticos na Amaz^ onia brasileira: taxonomia, biologia e ecologia. Instituto Nacional World 2020. Transforming Food Systems for Affordable Healthy Diets. FAO, Rome.
de Pesquisas da Amaz^ onia, Manaus, Amazonas, pp. 193–216. Whittier, T.R., Van Sickle, J., 2010. Macroinvertebrate tolerance values and an
Shimano, Y., Juen, L., 2016. How oil palm cultivation is affecting mayfly assemblages in assemblage tolerance index (ATI) for western USA streams and rivers. J. North Am.
Amazon streams. Int. J. Limnol. 52 (2016), 35–45. Benthol. Soc. 29, 852–866.
Shimano, Y., Salles, F.F., Faria, L.R.R., Cabette, H.S., Nogueira, D.S., 2012. Distribuiç~ao Wickham, H., 2016. Ggplot2: Elegant Graphics for Data. Analysis. Springer-Verlag, New
espacial das guildas troficas e estruturaç~ao da comunidade de Ephemeroptera York, p. 215p.
(Insecta) em corregos do Cerrado de Mato Grosso, Brasil. Iheringia Ser. Zool. 102 (2), Wong, A.B., Chaw, V., Fikri, A.H., 2020. Land use effects on Ephemeroptera, Plecoptera,
187–196. and Trichoptera (EPT) communities in ranau-beluran district, sabah, Malaysia.
Shimano, Y., Cardoso, M., Juen, L., 2018. Ecological studies of mayflies (Insecta, Aquaculture, Aquarium, Conservation & Legislation 13 (4), 1812–1819.
Ephemeroptera): can sampling effort be reduced without losing essential taxonomic Zagarola, Jean-Paul A., Martinez, P., Guillermo, L., Maria, Eugenia,
and ecological. Acta Amazonica 48 (2), 137–145. Anderson, Christopher B., 2017. Assessing the effects of urbanization on streams in
Tierra del Fuego. Ecol. Austral 27 (1), 45–54.

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