© The Authors, 2022, Published by the Universidad del Zulia
*Corresponding author: jurdanigo@uteq.edu.ec
Juan Pablo Urdánigo Zambrano
1
*
Karla Micaela Pérez Anchundia
1
Elian Briohildo Intriago Giler
1
Gabriela Jazmín Arriaga Loor
1
Solange Anabeth Zambrano Ganchozo
2
Oscar Oswaldo Prieto Benavides
1
Rev. Fac. Agron. (LUZ). 2022, 39(4): e223952
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v39.n4.07
Environment
Associate editor: Dr. Jorge Vilchez-Perozo
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
Keywords:
Aquatic macroinvertebrates
Land use
Biological indices
Bioindicators of water quality with different riparian cover in the Guapara micro watershed,
Ecuador
Bioindicadores de calidad hídrica con diferente cobertura ribereña en la microcuenca Guapara,
Ecuador
Bioindicadores da qualidade da água em riachos com diferentes coberturas ripícolas na microbacia
hidrográca de Guapara, Equador
1
Universidad Técnica Estatal de Quevedo. Av. Quito km 1.5
vía Santo Domingo de los Tsáchilas. Quevedo, Ecuador.
2
Gobierno Autónomo Descentralizado de San Francisco de
Puebloviejo. San Francisco de Puebloviejo, Ecuador.
Received: 09
-08-2022
Accepted: 27-09-2022
Published: 24-11-2022
Abstract
Agricultural activities produce changes in the margins of the stream banks,
causing disturbances in water quality, and in the assemblage of aquatic insect
communities. The objective of this research is to evaluate the changes in the
structure and composition of the aquatic macroinvertebrate community, and
physicochemical variables in relation to the land use of the Guapara river,
Cotopaxi province, Ecuador. Samplings were conducted during the rainy
season (December to February 2018-2019) in three streams with different
riparian cover: agricultural, native forest, and forest plantations, where
samples of aquatic insects and physicochemical parameters were collected in
situ. A total of 461 aquatic insects corresponding to 7 orders and 25 families
were collected. In general, the highest abundance in order and family was
presented by Ephemeroptera with 34 %, and Leptophlebiidae with 21 %
respectively. According to the Ephemeroptera, Plecoptera Trichoptera (EPT)
index, the highest ecological condition was found in streams with native
forest cover, and forest plantations respectively, and decreased in the stream
with agricultural cover; while BMWP-Cr indicated water contamination in
the three streams. Hydrobiosidae (Trichoptera) were associated with high
turbidity values; while Gerridae (Hemiptera) were associated with high
dissolved oxygen concentrations; in addition, Ptilodactylidae (Coleoptera)
preferred the Q1-CA, and Q3-CF conditions, while Leptophlebiidae
(Ephemeroptera) were associated with the stream of native forest. A negative
inuence of agricultural activity on the physicochemical parameters of the
water and on the structure of the aquatic insect community assemblage was
evidenced.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2022, 39(4): e223952. October-December. ISSN 2477-9407.2-5 |
Resumen
Las actividades agrícolas producen cambios en los márgenes de
las riberas de las quebradas ocasionando perturbaciones en la calidad
hídrica y en el ensamble de las comunidades de insectos acuáticos. El
objetivo de la investigación es evaluar los cambios en la estructura
y composición de la comunidad de macroinvertebrados acuáticos
y variables sicoquímicas en relación con los usos de suelo del río
Guapara, provincia Cotopaxi, Ecuador. Se realizaron muestreos en la
temporada lluviosa (diciembre a febrero, 2018-2019) en tres quebradas
con diferente cobertura riparia: agrícola, bosque nativo y plantaciones
forestales, en las que se recolectaron muestras de insectos acuáticos
y parámetros sicoquímicos in situ. Se recolectaron 461 insectos
acuáticos correspondientes a 7 órdenes y 25 familias. En general la
mayor abundancia en orden y familia lo presentaron Ephemeroptera
con 34 % y Leptophlebiidae con 21 % respectivamente. Según
el índice Ephemeroptera, Plecoptera Trichoptera (EPT) la mayor
condición ecológica la presentaron las quebradas con cobertura de
bosque nativo y plantaciones forestales respectivamente y disminuyó
en la quebrada con cobertura agrícola; mientras, BMWP-Cr indicó
contaminación del agua en las tres quebradas. Hydrobiosidae
(Trichoptera) se asoció con valores altos de turbidez; mientras,
Gerridae (Hemiptera) con concentraciones altas de oxígeno disuelto;
además, Ptilodactylidae (Coleoptera) se prerió las condiciones de
Q1-CA y Q3-CF, mientras Leptophlebiidae (Ephemeroptera) con la
quebrada de bosque nativo. Se evidencio una inuencia negativa de
la actividad agrícola en los parámetros sicoquímicos del agua y en la
estructura del ensamble de comunidades de insectos acuáticos.
Palabras clave: macroinvertebrados acuáticos, usos de suelo, índices
biológicos.
Resumo
As actividades agrícolas produzem alterações nas margens dos
bancos de riachos causando perturbações na qualidade da água e
no conjunto das comunidades de insectos aquáticos. O objectivo
da investigação é avaliar mudanças na estrutura e composição da
comunidade de macroinvertebrados aquáticos e variáveis físico-
químicas em relação ao uso do solo no rio Guapara, província de
Cotopaxi, Equador. A amostragem foi realizada durante a estação
chuvosa (Dezembro a Fevereiro de 2018-2019) em três riachos
com diferentes coberturas ripícolas: agricultura, oresta nativa e
plantações orestais, onde foram recolhidas in situ amostras de
insectos aquáticos e parâmetros físico-químicos. Foram recolhidos
um total de 461 insectos aquáticos correspondentes a 7 encomendas
e 25 famílias. Em geral, a maior abundância em ordem e família foi
encontrada em Efeméroptera com 34 % e Leptophlebiidae com 21 %
respectivamente. De acordo com o índice Ephemeroptera, Plecoptera
Trichoptera (EPT), a condição ecológica mais elevada foi encontrada
nos riachos com cobertura orestal nativa e plantações orestais
respectivamente e diminuiu no riacho com cobertura agrícola;
enquanto que a BMWP-Cr indicou a poluição da água nos três
riachos. Hydrobiosidae (Trichoptera) foram associados a altos valores
de turbidez; enquanto Gerridae (Hemiptera) com altas concentrações
de oxigénio dissolvido; além disso, Ptilodactylidae (Coleoptera)
preferiu as condições Q1-CA e Q3-CF, enquanto Leptophlebiidae
(Ephemeroptera) com o riacho da oresta nativa. Uma inuência
negativa da actividade agrícola sobre os parâmetros físico-químicos
da água e sobre a estrutura do conjunto da comunidade de insectos
aquáticos foi evidente.
Palavras-chave: macroinvertebrados aquáticos, uso da terra, índices
biológicos.
Introduction
The increase in human activities represented by land use and
cover affects the quality of multiple hydrographic networks around
the world (Damanik-Ambarita et al., 2016). Agricultural activity is
one of the main productive activities. It is estimated that agriculture
constitutes 70 % and 90 % of the annual labor demand (Gozlan et al.,
2019), and in South America, approximately 50 % of the population is
dedicated to this activity (Pimentel and Burgess, 2013); consequently,
poor agricultural practices generate contamination in surface water
resources due to poor agrochemical management (Stehle and Schulz,
2015), deteriorating the quality of sh, and aquatic invertebrate
communities (Malaj et al., 2014).
Ecuador is a country with high agricultural production, and
poor agricultural practices. Multiple relatively current studies have
documented the inuence of human activities on surface water
bodies in Ecuador (Capparelli et al., 2021; Deknock et al., 2019).
Currently, in the province of Cotopaxi, the ecological quality of
surface water resources has decreased considerably due to untreated
industrial, agricultural, and petroleum wastewater discharges, being
poor agricultural practices one of the main sources of contamination
(Zapata et al., 2021).
To evaluate the impacts of anthropogenic activities on aquatic
ecosystems, biological indicators are used to provide information
on the ecological status of water bodies. In this sense, aquatic
macroinvertebrate assemblages are excellent indicators of water
quality because biota responds to stress factors from multiple spatial
or temporal scales (He et al., 2020). In addition, using aquatic
organisms in ecological studies has proven to be more effective than
using environmental variables (Bonada et al., 2006). Numerous
studies indicate that changes in land use and riparian vegetation
in streams produce effects on the assemblages of aquatic insects,
on their taxonomic composition, and consequently a decrease in
diversity in relation to pasture covers for agricultural activities, and
forest plantations (Guerrero et al., 2017).
The objective of the research is to evaluate the use of bioindicators
of water quality with different riparian cover in the Guapara micro
watershed, in Ecuador. The information from the study will serve
as an ecological basis for future water quality studies with aquatic
macroinvertebrates as biological indicators, in addition, it will
provide information on the responses of the aquatic macroinvertebrate
assemblage to change in land use, useful for the formulation of
conservation, restoration, and management strategies for streams, and
water bodies.
Materials and methods
Location and sampling points
The research was carried out in three streams of the Guapara
River, province of Cotopaxi, Ecuador, with different vegetation
covers, based on the following criteria: agricultural cover (Q1-CA);
native forest cover (Q2-CN); forest plantation cover (Q3-CF). The
altitudinal range of the sampling stations varied between 182.5 and
213.6 m.a.m.s.l., belonging to the tropical premontane forest zone
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Urdánigo et al. Rev. Fac. Agron. (LUZ). 2022, 39(4): e2239523-5 |
(Bh-PM), with temperatures ranging between 20 and 28 ºC, according
to Holdridge Life Zones classication system (1978).
Sampling Station 1 (Q1-CA) (X = 693318 E and Y = 9876708
S, 213.6 m.a.m.s.l.) has agricultural plantation cover, mainly cocoa
(Theobroma cacao L.) and banana (Musa paradisiaca L.) crops.
Sampling Station 2 (Q2-CN) (X = 692374 E and Y = 9877600 S,
182.5 m.a.m.s.l.) corresponds to a zone with forest plantations; crops
of teak (Tectona grandis L.f.), balsa tree (Ochroma pyramidale (Cav.
ex Lam. Urb.) and pachaco (Schizolobium parahyba (Vell.) S.F.
Blake) predominate here, with trees about 10 m high belonging to the
timber company PLANTABAL S.A.
Sampling Station 3 (Q3-CF) (X = 693088 E and Y = 9876920
S, 207 mamsl) is a zone of native plantations with species such as
laurel (Laurus nobilis L.), Spanish cedar (Cedrela odorata L.), and
guarumo (Cecropia peltata L.).
Physicochemical and hydrological variables
The following basic physicochemical water parameters were
measured in situ: pH, oxidation-reduction potential (POR), electrical
conductivity (C.E., μS.cm
-1
), total dissolved solids (STD, mg.L
-1
),
dissolved oxygen (OD, %), and turbidity (NTU) with a Hanna HI-
98194 multiparameter meter. The height and depth of the water
column were determined with a exometer, and a rod graduated in
units of length (cm). The ow rate (Q, m
3
.s
-1
) was delimited through
the oating object method as described by Urdanigo et al., (2019b).
Collection and analysis of aquatic macroinvertebrates
The collection of aquatic macroinvertebrates was conducted in
a hydrological period (rainy season) from December to February
2018-2019. Four samplings were conducted with an interval of 45
days between each sampling. The aquatic macroinvertebrates were
collected using a 405 cm
2
D-net with 500 µm mesh located in the
opposite direction of the water ow and were labeled and stored in
containers with 70 % alcohol (Roldán, 2003). The taxonomic location
of the species was done up to the family level, using a stereoscope and
specialized taxonomic keys (Domínguez and Fernández, 2009), the
backup specimens were analyzed and deposited in the Microbiology
and Entomology laboratory of the Technical University of Quevedo,
Quevedo, Ecuador.
Biological indices
The Shannon-Weaver index and Simpson’s index of proportional
abundance of ecological diversity were used to estimate diversity; in
addition, the Ephemeroptera, Plecoptera, Trichoptera index (EPT),
and the Biological Monitoring Working Party index (BMWP/Costa
Rica) (MINAE, 2007) were used to determine water quality at each
sampling station.
Statistical analysis
The statistical differences between the streams studied in relation
to the physicochemical variables, and abundance of orders, were
analyzed with a one-way ANOVA, after validating the assumptions of
normality (Kolmogórov-Smirnov) and homoscedasticity (Levene’s
test) and Tukey’s test to determine comparisons. The Shannon-
Weaver, Simpson, EPT, and BMWP Costa Rica diversity indices
were analyzed with the Kruskal–Wallis one-way analysis of variance,
and Dunn’s post-hoc test. All inferential tests were performed with a
statistical signicance level of p = 0.05.
The environmental variables and the abundance of aquatic
macroinvertebrate families were correlated with a Redundancy
Analysis (RDA), for this, rare species < 10% of the total frequency
were eliminated (Hill and Gauch, 1980), then the Hellinger
transformation was applied to the values of the families. In addition,
collinear water quality variables based on the ination variance factor
(VIF) 10 were removed. Finally, RDA was applied with a step-
forward selection (Blanchet et al., 2008). All multivariate analyses
were performed using the “Vegan” package (Oksanen et al., 2015) of
the R software platform (R Core Team, 2015).
Results and discussion
Physicochemical and hydrological variables
The physicochemical and hydrological variables measured at the
three sampling stations showed signicant differences in relation
to water depth, height, and ow (p < 0.05). The greatest height and
average ow were found in stream 1 (18.0 ± 1 m) and (31.88 ± 0.78
m
3
.s
-1
) respectively; while the greatest average depth was recorded in
stream 2 (0.613 ± 0.10 m), the differences in depth and width directly
inuence the ow, as they are variables used to calculate the cross-
sectional area of each sampled section (Urdanigo et al., 2019a). The
rest of the variables did not show signicant differences between the
streams studied (table 1).
Table 1. Physicochemical and hydrological parameters of the
Guapara river sampling streams, Ecuador.
Q1-CA Q2-CN Q3-CF
pH 8.82 ± 0.53 8.69 ± 0.77 8.64 ± 0.4
Oxide reduction
potential (%)
153.8 ± 12.68 146.14 ± 32.01 158.45 ± 29.89
Conductivity (μS.cm
-1
) 49.03 ± 10.74 39.93 ± 5.63 55.54 ± 17.32
Total dissolved solids
(mg.L
-1
)
24.39 ± 5.51 20.04 ± 2.85 27.78 ± 8.69
Dissolved oxygen (%) 50.62 ± 18.93 50.04 ± 14.38 49.93 ± 14.76
Turbidity (NTU) 30.55 ± 20.47 31.11 ± 38.76 27.99 ± 19.64
Depth (m) 0.44 ± 0.04 b 0.613 ± 0.10 a 0.38 ± 0.09 b
Height (m) 18.0 ± 1 a 10.0 ± 1.5 c 14.0 ± 1 b
Speed (m.s
-1
) 3.73 ± 0.25 3.16 ± 0.64 2.86 ± 0.65
Flow (m
3
.s
-1
) 31.88 ± 0.78 a 20.03 ± 3.27 b 15.86 ± 2.57 b
Q1-CA: agricultural cover. Q2-CN native forest cover. Q3-CF: forest plantation
cover. Different letters between sampling stations denote signicant differences
(Tukey, p < 0.05).
Taxonomic variability of aquatic macroinvertebrates between
streams
A total of 461 aquatic macroinvertebrates belonging to 7 orders
and 25 families were collected in the water bodies evaluated. The
most abundant order was Ephemeroptera with 34 %, followed by
Trichoptera with 21 %, and Coleoptera with 19 %; while Hemiptera,
Odonata, Diptera, and Tricladida represented 26 % of the remaining
orders. The Ephemeroptera order had a higher abundance in the
streams with native forest cover, and forest plantation cover with 41
% and 38 % respectively, being lower in the stream with agricultural
cover with 25 %. This is similar to that reported by Morelli and Verdi
(2014), who detected the order Ephemeroptera as the most abundant
in sampling areas with high forest inuence. The order Coleoptera
recorded the highest abundance in the stream with native forest cover
with 25 %, followed by the stream with agricultural cover with 21
% respectively, having inuence in both streams by the presence of
organic matter, and allochthonous material due to the abundance of
detritus from leaf litter (Bojsen and Jacobsen, 2003).
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2022, 39(4): e223952. October-December. ISSN 2477-9407.4-5 |
cover because this family is not found in waters of low ecological
quality inuenced by the use of agricultural chemicals, industrial
discharges, and domestic waters (Forio et al., 2016; Jandry et al.,
2014) (gure 1).
Figure 1. Redundancy analysis based on the abundance of
macroinvertebrate families, and environmental
variables in three streams with different riparian
cover in the Guapara River, Ecuador. Q1-CA ,
agricultural cover; Q2-CN, native forest cover; Q3-
CF, forest plantation cover; S.D.T., Total Dissolved
Solids; OD, Dissolved oxygen; Hds, Hydrobiosidae; Gr,
Gerridae; Ptd, Ptilodactylidae; Lep, Leptophlebiidae.
Biological indices
The Ephemeroptera, Plecoptera, Trichoptera (EPT) index did
not present signicant differences (p > 0.05); however, regular
water quality was recorded for the stream with agricultural cover
(41.75 ± 11.79), and good quality for the streams with native
forest 62.05 ± 18.67), and forest plantation cover (62.43 ± 19.65),
similar to that described by Alomía et al. (2017) who noted that
the EPT index presented regular water quality in both seasons,
especially in station two, which is characterized as a stream with
agricultural plantations. Finally, the number of EPT taxa was
higher in the stream with native forest cover (9), in relation to the
streams with agricultural cover and forest plantations with 8 taxa
each respectively; no signicant differences were found between
streams. These results are related to those described by Galeano-
Rendón and Mancera-Rodríguez (2018b), who pointed out that EPT
taxa are sensitive to anthropic disturbances, thus proving the good
ecological quality of riparian vegetation cover.
On the other hand, in the three study streams, values between
29 - 62 (px > 0.05) of the BMWP-Cr index were recorded,
demonstrating water contamination in the three sampling stations.
Gutiérrez-Fonseca and Lorion (2014) indicated that the BMWP-Cr
index showed a low correspondence in water quality between the
three types of sites (forested, grasslands with a buffer zone, and
grasslands without a buffer zone).
In relation to the biodiversity analyses, the Shannon index was
higher (2.5) for the stream with native forest cover, although, without
signicant differences compared to the values presented in the
streams with forest plantation cover (2.432), and agricultural cover
(2.162), respectively, similar to the study conducted by Morelli and
Verdi (2014), whose streams with forest plantation cover, obtained
values of the Shannon index between 1.06 and 2.55. Simpson’s
index did not show signicant differences between streams either;
however, this index showed lower dominance in streams with native
forest cover (0.115), and forest plantation cover (0.116), compared
to a slight increase in the stream with agricultural plantations cover
with 0.168. These results differ from what was recorded by Rosado
et al. (2017) where Simpson’s dominance index was higher in
Although the order Coleoptera is relatively abundant in streams
with forest cover (Meza et al., 2012), it is also detected in areas
inuenced by native forest. Pérez-Rodríguez et al. (2021) reported
this order as the most abundant in a study of ve streams in the
protected area of native species in the Serranía de la Macuira,
Colombia; similarly, Urdanigo et al. (2019) reported that this
order was the most abundant in the stream with secondary native
forest. The order Hemiptera was the most abundant in the stream
with agricultural cover with 32 %; however, in coffee crop cover
in Colombia, abundance levels of 2.6 % of the order Hemiptera
were observed due to the low prevalence of the species Pontoscolex
corethrurus (Annelida: Oligochaeta), which prevents further growth
of the taxonomic group (Rojas-Múnera et al., 2021).
The order Tricladida obtained the lowest abundance among
streams, in the stream with agricultural cover the order presented the
lowest abundance with 1 %; while, in the streams with native forest
and forest plantation cover 2 % and 4 % respectively. Likewise, the
Diptera order had the lowest abundance in the stream with native
forest cover (1 %), followed by 3 % in the stream with agricultural
cover, and 5 % in the stream with forest plantation cover. In a
study conducted by Murillo et al. (2018), Tricladida and Diptera
were not abundant orders either, presenting higher abundances in
a stream of a conserved area for the order Diptera, and in a stream
with agricultural cover for Tricladida. Finally, the order Odonata
presented similar abundances between streams ~ 4 %, Tampo et al.
(2021) indicate that the tolerance of the order Odonata allows it to
inhabit contaminated habitats. There were no signicant statistical
differences in the abundance of orders between streams (p > 0.05).
Redundancy analysis (RA) between families of aquatic
macroinvertebrates, and environmental variables
The most abundant families in the studied streams were
Leptophlebiidae (21 %), followed by Gerridae (16 %),
Hydrobiosidae (13 %), and Ptilodactylidae (12 %); while the families
Megapodagrionidae, Helicopsychidae, and Glossosomatidae
recorded less than 1% abundance each respectively. In the study, the
environmental predictor variables of the AR model associated with
aquatic macroinvertebrate communities were: Dissolved Oxygen
and Turbidity (p < 0.01), with two canonical axes explaining 23 %
of the total variance by Monte Carlo permutation test, this is similar
to that reported by Mosquera-Restrepo and Peña-Salamanca (2019),
who determined that Dissolved Oxygen and Turbidity contribute
signicantly as predictor variables of the aquatic insect assemblage
in the Jordan River subwatershed, Colombia. The results showed
that Hydrobiosidae was positively correlated with turbidity, and
was associated with the stream of native forest cover (Q2-CN) due
to the high ecological conditions of the habitat since it is usually
found in good water quality conditions (Mena-Rivera et al., 2018;
Stark, 1998); however, Gerridae was inuenced by low values of
Dissolved Oxygen due to its tolerance with moderately polluted
environments low in dissolved Oxygen (Nuñez and Fragoso-
Castilla, 2019).
In addition, Ptilodactylidae presented afnity with the stream
of forest plantation cover (Q3-CF), this relationship agrees with
that described by Galeano-Rendón and Mancera-Rodríguez
(2018) who found that this family of Coleoptera is associated
with streams of forest and native cover, due to the abundance of
detritus from the litter (Bojsen and Jacobsen, 2003), in contrast to
streams with deforestation processes due to agricultural activities.
Leptophlebiidae was associated with the stream of native forest
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Urdánigo et al. Rev. Fac. Agron. (LUZ). 2022, 39(4): e2239525-5 |
streams with an anthropic disturbance with 0.78, while the streams
with agricultural cover showed the lowest dominance of 0.58.
Conclusions
These results reveal that in the Guapara micro watershed there
is an alteration in water quality, and in the structure of aquatic insect
assemblages due to poor agricultural practices, and changes in land
use on the banks of the streams. The streams with native forest
cover and forest plantation presented the highest ecological quality
according to the EPT index, which recorded the highest response on
water quality at the sampling stations.
Literature cited
Alomía, J., Iannacone, J. A., Alvariño, L., & Ventura, K. (2017). Macroinvertebrados
Bentónicos Para Evaluar La Calidad De Las Aguas De La Cuenca Alta Del
Río Huallaga, Perú. The Biologist, 1(2), 65–84. https://doi.org/10.24039/
rtb2017151144
Blanchet, F. G., Legendre, P., & Borcard, D. (2008). Forward selection
of explanatory variables. Ecology, 89(9), 2623–2632. https://doi.
org/10.1890/07-0986.1
Bojsen, B. H., and Jacobsen, D. (2003). Effects of deforestation on macroinvertebrate
diversity and assemblage structure in Ecuadorian Amazon streams. Archiv
Fur Hydrobiologie, 158(3), 317–342.
Bonada, N., Prat, N., Resh, V. H., & Statzner, B. (2006). Developments in aquatic
insect biomonitoring: a comparative analysis of recent approaches. Annu.
Rev. Entomol., 51, 495–523.
Capparelli, M. V., Molinero, J., Moulatlet, G. M., Barrado, M., Prado-Alcívar,
S., Cabrera, M., Gimiliani, G., Ñacato, C., Pinos-Velez, V., & Cipriani-
Avila, I. (2021). Microplastics in rivers and coastal waters of the province
of Esmeraldas, Ecuador. Marine Pollution Bulletin, 173. https://doi.
org/10.1016/j.marpolbul.2021.113067
Damanik-Ambarita, M. N., Lock, K., Boets, P., Everaert, G., Nguyen, T. H.
T., Forio, M. A. E., Musonge, P. L. S., Suhareva, N., Bennetsen, E.,
Landuyt, D., Dominguez-Granda, L., & Goethals, P. L. M. (2016).
Ecological water quality analysis of the Guayas river basin (Ecuador)
based on macroinvertebrates indices. Limnologica, 57, 27–59. https://doi.
org/10.1016/j.limno.2016.01.001
Deknock, A., De Troyer, N., Houbraken, M., Dominguez-Granda, L., Nolivos, I.,
Van Echelpoel, W., Forio, M. A. E., Spanoghe, P., & Goethals, P. (2019).
Distribution of agricultural pesticides in the freshwater environment of
the Guayas river basin (Ecuador). Science of The Total Environment, 646,
996–1008. https://doi.org/10.1016/j.scitotenv.2018.07.185
Domínguez, E., and Fernández, H. R. (2009). Macroinvertebrados bentónicos
sudamericanos Sistemática y biología. Fundación Miguel Lillo.
Forio, M. A. E., Van Echelpoel, W., Dominguez-Granda, L., Mereta, S. T.,
Ambelu, A., Hoang, T. H., Boets, P., & Goethals, P. L. M. (2016).
Analysing the effects of water quality on the occurrence of freshwater
macroinvertebrate taxa among tropical river basins from different
continents. Ai Communications, 29(6), 665–685.
Galeano-Rendón, E., and Mancera-Rodríguez, N. J. (2018). Efectos de la
deforestación sobre la diversidad y la estructura del ensamblaje de
macroinvertebrados en cuatro quebradas Andinas en Colombia. Revista
de Biología Tropical, 66(4), 1721–1740.
Gozlan, R. E., Karimov, B. K., Zadereev, E., Kuznetsova, D., & Brucet, S. (2019).
Status, trends, and future dynamics of freshwater ecosystems in Europe
and Central Asia. Inland Waters, 9(1), 78–94. https://doi.org/10.1080/20
442041.2018.1510271
Guerrero, N., Díaz, M., Urdánigo, J., Tayhing, C., Guerrero, V., & Yepez, Á. (2017).
Uso de suelo y su inuencia en la calidad del agua de la microcuenca El
Sapanal, Ecuador. Revista Cubana de Ciencias Biológicas, 5(2), 1–11.
http://www.rccb.uh.cu/index.php/RCCB/article/view/156/265
Gutiérrez-Fonseca, P. E., and Lorion, C. M. (2014). Application of the BMWP-
Costa Rica biotic index in aquatic biomonitoring: Sensitivity to collection
method and sampling intensity. Revista de Biologia Tropical, 62(April),
275–289. https://doi.org/10.15517/rbt.v62i0.15792
He, S., Soininen, J., Chen, K., & Wang, B. (2020). Environmental factors override
dispersal-related factors in shaping diatom and macroinvertebrate
communities within stream networks in China. Frontiers in Ecology and
Evolution, 8, 141.
Hill, M. O., and Gauch, H. G. (1980). Detrended correspondence analysis: An
improved ordination technique. Vegetatio, 42(1), 47–58. https://doi.
org/10.1007/BF00048870
Holdridge, L. (1978). Ecología basada en zonas de vida. Instituto Interamericano de
Ciencias Agrícolas (IICA). http://repositorio.iica.int/handle/11324/7936
Jandry, J., Brulin, M., Parinet, B., & Grandjean, F. (2014). Ephemeroptera
communities as bioindicators of the suitability of headwater streams
for restocking with white-clawed craysh, Austropotamobius pallipes.
Ecological Indicators, 46, 560–565.
Malaj, E., Von Der Ohe, P. C., Grote, M., Kühne, R., Mondy, C. P., Usseglio-
Polatera, P., Brack, W., & Schäfer, R. B. (2014). Organic chemicals
jeopardize the health of freshwater ecosystems on the continental scale.
Proceedings of the National Academy of Sciences of the United States of
America, 111(26), 9549–9554. https://doi.org/10.1073/pnas.1321082111
Mena-Rivera, L., Vásquez-Bolaños, O., Gómez-Castro, C., Fonseca-Sánchez, A.,
Rodríguez-Rodríguez, A., & Sánchez-Gutiérrez, R. (2018). Ecosystemic
assessment of surface water quality in the Virilla river: towards sanitation
processes in Costa Rica. Water, 10(7), 845.
Meza, M., Rubio, J., Días, A., & Walteros, L. (2012). Calidad de agua y
composición de macroinvertebrados acuáticos en la subcuenca alta del río
Chinchiná. Water quality and composition of aquatic macroinvertebrates
in the subwatershed of river Chinchiná. Caldasia. Caldasia, 34(2), 443–
456. http://www.icn.unal.edu.co/
MINAE. (2007). Reglamento para la Evaluación y Clasicación de la Calidad
de los Cuerpos de Aguas Superciales. 178. www.cimar.ucr.ac.cr/PDFS/
Reglamento Evaluacion y Clasica-cion_Calidad_Agua_Supercial.pdf
Morelli, E., and Verdi, A. (2014). Diversidad de macroinvertebrados acuáticos en
cursos de agua dulce con vegetación ribereña nativa de Uruguay. Revista
Mexicana de Biodiversidad, 85(4), 1160–1170. https://doi.org/10.7550/
rmb.45419
Mosquera-Restrepo, D., and Peña-Salamanca, E. J. (2019). “Ensamblaje” de
macroinvertebrados acuáticos y su relación con variables sicoquímicas
en un río de montaña en Colombia. Revista de Biología Tropical, 67(6),
1235–1246.
Murillo, S. A., Mendoza, A., Restrepo, E. S., & Rodríguez, M. Á. (2018).
Utilización de macroinvertebrados acuáticos como herramienta para
determinar la calidad del agua en la quebrada Santo Tomás, municipio de
Pensilvania, Colombia. Revista de La Academia Colombiana de Ciencias
Exactas, Físicas y Naturales, 42(164), 212–220. https://doi.org/10.18257/
raccefyn.655
Nuñez, J. C., and Fragoso-Castilla, P. J. (2019). Uso de macroinvertebrados
acuáticos como bioindicadores de contaminación del agua de la Ciénaga
Mata de Palma (Colombia). Información Tecnológica, 30(5), 319–330.
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D.,
Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H.
H., Szoecs, E., & Wagner, H. (2015). Vegan: Community Ecology Package
(R package version 2. 3-0). https://cran.r-project.org/package=vegan
Pérez-Rodríguez, C., Manjarres-Pinzón, G., & Tamaris-Turizo, C. . (2021).
Insectos acuáticos asociados a arroyos de la Serranía de La Macuira -
La Guajira, Colombia. Revista U.D.C.A Actualidad & Divulgación
Cientíca, 24(1). https://doi.org/10.31910/rudca.v24.n1.2021.1941
Pimentel, D., and Burgess, M. (2013). Soil erosion threatens food production.
Agriculture (Switzerland), 3(3), 443–463. https://doi.org/10.3390/
agriculture3030443
R Core Team. (2015). A language and environment for statistical computing. R
Foundation for Statistical Computing.
Rojas-Múnera, D. M., Feijoo-Martínez, A., Molina-Rico, L. J., Zúñiga, M. C.,
& Quintero, H. (2021). Differential impact of altitude and a plantain
cultivation system on soil macroinvertebrates in the Colombian Coffee
Region. Applied Soil Ecology, 164, 103931. https://doi.org/https://doi.
org/10.1016/j.apsoil.2021.103931
Roldán, G. (2003). Bioindicación de la calidad del agua en Colombia: propuesta
para el uso del método BMWP Col (Universidad de Antioquia (ed.)).
Editorial Universidad de Antioquia. https://books.google.com.ec/
books?id=ZEjgIKZTF2UC
Rosado Yépez, Á., Bolívar Yépez, Á., Urdánigo Zambrano, J., Morales Cabezas,
D. C., Guerrero Chuez, N. M., and Tayhing Cajas, C. C. (2017).
Macroinvertebrados acuáticos como indicadores de calidad hídrica en
áreas de descargas residuales al río Quevedo, Ecuador. Ciencias Tecn
UTEQ, 10(1), 27–34.
Stark, J. D. (1998). SQMCI: A biotic index for freshwater macroinvertebrate
codedabundance data. New Zealand Journal of Marine and Freshwater
Research, 32(1), 55–66.
Stehle, S., and Schulz, R. (2015). Agricultural insecticides threaten surface waters
at the global scale. Proceedings of the National Academy of Sciences of the
United States of America, 112(18), 5750–5755. https://doi.org/10.1073/
pnas.1500232112
Tampo, L., Kaboré, I., Alhassan, E. H., Ouéda, A., Bawa, L. M., & Djaneye-
Boundjou, G. (2021). Benthic macroinvertebrates as ecological indicators:
their sensitivity to the water quality and human disturbances in a tropical
river. Frontiers in Water, 3, 662765.
Urdanigo, J. P., Díaz Ponce, M., Tay-Hing Cajas, C., Sánchez Fonseca, C.,
Yong Benitez, R., Armijo Albán, K., Guerrero Chúez, N., & Mancera-
Rodríguez, N. J. (2019a). Diversidad de macroinvertebrados acuáticos
en quebradas con diferente cobertura ribereña en del bosque Protector
Murocomba, cantón Valencia, Ecuador. Revista de Biología Tropical,
67(4), 861–878. https://doi.org/10.15517/rbt.v67i4.35190
Urdanigo, J. P., Díaz Ponce, M., Tay-Hing Cajas, C., Sánchez Fonseca, C.,
Yong Benitez, R., Armijo Albán, K., Guerrero Chúez, N., & Mancera-
Rodríguez, N. J. (2019b). Diversidad de macroinvertebrados acuáticos
en quebradas con diferente cobertura ribereña en del bosque Protector
Murocomba, cantón Valencia, Ecuador. Revista de Biología Tropical,
67(4), 861–878. https://doi.org/10.15517/rbt.v67i4.35190
Zapata, D., Oleas, N. H., Páez-Vacas, M., & Tobes, I. (2021). Water Quality
Assessment of the Cutuchi River Basin (Ecuador): A Review of Technical
Documents. IOP Conference Series: Earth and Environmental Science,
690(1), 12058. https://doi.org/10.1088/1755-1315/690/1/012058