836 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 836–852, e49975, enero-diciembre 2022 (Publicado Dic. 07, 2022)

Effect of environmental characteristics on the diversity of aquatic

macroinvertebrates in Andean rivers regulated for hydroelectric generation

María Isabel Ríos-Pulgarín1; https://orcid.org/0000-0002-4543-6989

Carlos Eduardo Giraldo-Sánchez2*; https://orcid.org/0000-0001-6651-3819

Samir Julián Calvo-Cardona3; https://orcid.org/0000-0003-3400-5208

James Londoño Valencia4; https://orcid.org/0000-0003-3387-1665

1. Grupo de Limnología y recursos hídricos, Universidad Católica de Oriente, Rionegro, Antioquia, Colombia;

mariaisabel.rios536@gmail.com

2. Grupo de Investigación de Sanidad Vegetal, Universidad Católica de Oriente, Rionegro, Antioquia, Colombia;

cegiral0@gmail.com (*Correspondence)

3. Grupo de Investigación de Agronomía y Zootecnia, Universidad Católica de Oriente, Rionegro-Antioquia, Colombia;

samirjulian@gmail.com

4. Grupo de Limnología y recursos hídricos, Universidad Católica de Oriente, Rionegro, Antioquia, Colombia;

jlondono@uco.edu.co

Received 02-II-2022. Corrected 13-IX-2022. Accepted 28-XI-2022.

ABSTRACT

Introduction: The Andes are characterized by an abundance of water resources and flows are frequently regu-

lated by reservoirs for the generation of energy. The effects of regulation on aquatic macroinvertebrate communi-

ties are not well known in Colombia.

Objective: To test the hypothesis that regulated currents have less macroinvertebrate diversity.

Methods: We collected water and organism samples before, and after, the regulation of the Tafetanes, Calderas

and Arenosa rivers, in Antioquia, Colombia, during various hydrological cycles (rain, transition and drought) and

climatic phenomena (ENSO/El Niño Phenomenon) between 2016 and 2018.

Results: We collected 53 214 individuals, from 165 taxa, mostly from the orders Ephemeroptera, Plecoptera,

Trichoptera and Diptera (90 % of captures). Changes in diversity responded to spatial differences rather than to

physicochemical variables: diversity was higher in non-regulated sites, regardless of the hydrological period or

associated ENSO. Most species were found in all sampling sites, but abundance was higher in the site with the

best habitat conservation status.

Conclusion: The results support the hypothesis that physical barriers have effects on macroinvertebrate diversity

at the local scale, however, the condition of adjacent habitats also seems to play an important role in preserv-

ing richness and abundance. The conservation of forest adjacent to the riverbed could mitigate the impacts of

regulation.

Key words: river flow; basin; ENSO/El Niño phenomena; Colombia.

https://doi.org/10.15517/rev.biol.trop..v70i1.49975

AQUATIC ECOLOGY

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INTRODUCTION

Aquatic macroinvertebrates (thereafter

AM) are one of the most diverse communities

in lotic ecosystems and contribute signifi-

cantly to energy flow in the ecosystem because

they belong to multiple trophic groups (Cum-

mins, 2008). Additionally, they are important

food items for ichthyofauna, especially in the

tropical rivers of medium and high eleva-

tion (Gutiérrez-Garaviz et al., 2016). Due to

their small size, the mobility of the AM is

restricted; and thus, the presence or dominance

of some genera in rivers can reflect local

conditions of water chemical quality, which

makes them important indicators of ecologi-

cal quality of the system (Forero et al., 2014;

Lozano-Ortiz, 2005; Roldán-Pérez & Ramírez-

Restrepo, 2008). Both, the structure of the

physical habitat and its temporal variability,

can affect the presence and diversity of AM

(Ríos-Pulgarín et al., 2016).

Macroinvertebrates are highly dependent

on the hydrological regime because the flow

of water determines the stability of the riv-

erbed, dispersion processes and the supply

of allochthonous organic matter, according

to the coverage of the riverbank and runoff

processes during the rainy season (Dudgeon,

2011; Rodríguez-Barrios et al., 2011; Wang et

al., 2013), but the response to this variability is

also modulated by the local habitat (Tomanova

& Usseglio-Polatera, 2007). For example, the

order of the river and the type of substrate are

related to the richness and taxonomic com-

position (Melo & Froehlich, 2001) and rivers

with dense riparian vegetation covers offer

greater substrate stability against hydrological

disturbances and faster recovery of communi-

ties (Longo et al., 2010). Since the habitat of

macroinvertebrates is the result of interaction

among the river substratum, the hydrology and

the surrounding terrestrial ecosystem, under

different habitat conditions, there would be dif-

ferent responses (e.g. richness or abundance)

of the macroinvertebrate assemblage against

hydrological alterations.

Several studies suggest that the structure

and dynamics of aquatic communities, par-

ticularly AM, respond simultaneously to habitat

heterogeneity and temporal variability, as sug-

gested by theoretical models of Habitat Templet

or Hydrological Disturbance (Ríos-Pulgarín

et al., 2016; Tomanova & Usseglio-Polatera,

2007; Townsend & Hildrew, 1994; Winemi-

ller et al., 2010). This model, representing the

RESUMEN

Efecto de características ambientales en la diversidad de macroinvertebrados acuáticos

en ríos andinos regulados para generación hidroeléctrica

Introducción: Los Andes se caracterizan por tener gran abundancia de recursos hídricos y las corrientes son

frecuentemente reguladas por embalses para la generación de energía. Los efectos de la regulación en las comu-

nidades de macroinvertebrados acuáticos no se conocen bien en Colombia.

Objetivo: Probar la hipótesis de que las corrientes reguladas presentan menor diversidad de macroinvertebrados.

Métodos: Recolectamos muestras de agua y organismos, antes y después de la regulación de los ríos Tafetanes,

Calderas y La Arenosa, en Antioquia, Colombia, durante varios ciclos hidrológicos (lluvia, transición y sequía)

y fenómenos climáticos (ENSO/Fenómeno de El Niño) entre 2016 y 2018.

Resultados: Recolectamos 53 214 individuos, de 165 táxones, en su mayoría de los órdenes Ephemeroptera,

Plecoptera, Trichoptera y Diptera (90 % de las capturas). Los cambios en la diversidad respondieron a las

diferencias espaciales más que a las variables fisicoquímicas: la diversidad fue mayor en sitios no regulados,

independientemente del periodo hidrológico o del ENSO. La mayoría de las especies se encontraron en todos

los sitios de muestreo, pero su abundancia fue mayor en el sitio de mejor estado de conservación del hábitat.

Conclusiones: Los resultados apoyan la hipótesis de que las barreras físicas tienen efectos sobre la diversidad

de macroinvertebrados a escala local, sin embargo, el estado de los hábitats adyacentes también parece jugar un

papel importante en la preservación de la riqueza y abundancia. La conservación del bosque adyacente podría

mitigar los impactos generados por la regulación.

Palabras clave: caudal; cuenca; fenómenos ENSO/El Niño; Colombia.

838 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 836–852, e49975, enero-diciembre 2022 (Publicado Dic. 07, 2022)

effects of habitat and the hydrological cycle on

aquatic communities, are applied to the AMs

that are recurrently eliminated by the dragging

of floods that clear out the riverbed, selectively

eliminating the organisms that later recolonize,

as expected in rivers whose flow rates vary

seasonally. However, it is not clear how com-

munities change in regulated systems, where

both connectivity and seasonality of flows are

reduced. Hence the interest in evaluating the

responses of the AM community to the hydro-

logical variability of Andean rivers, which

face an increasing pressure for their regulation

for purposes of energy generation. In fact, in

these systems important effects of the reduc-

tion of seasonality on benthic fauna have been

documented, during prolonged conditions of

low or high flows, such as those that occur dur-

ing the El Niño phenomenon, which is highly

prevalent in the tropical Andes (Blanco, 2003;

García et al., 2012; Longo et al., 2010; Ríos-

Pulgarín et al., 2016).

In terms of connectivity, the discontinu-

ity in rivers would divide them into discrete

regions (Stanford & Ward, 2001), whose bio-

logical structure, should respond differently

to seasonality (Terra & Araújo, 2011). This

would imply that in regulated systems, habitat

conditions would be of greater importance,

as it has been documented in other communi-

ties such as ichthyofauna (Leite et al., 2015).

These changes in connectivity and seasonality

can have important effects on the composition

and abundance of AM. Thus, elucidating their

effect on the AM communities generate infor-

mation of interest to management models of the

Andean tropical basins.

Among the most frequent hydrological

alterations in the Andean rivers are the res-

ervoirs for hydroelectric generation, whose

construction and operation implies the regula-

tion of the flows of the intervened currents.

Upstream of the reservoir, the river flow is

maintained but downstream the flow is signifi-

cantly reduced or increased, by regulation, and

the effect of hydrological seasonality may dis-

appear, because the new regime depends main-

ly on the generation rule, that is, on how much

water is required to generate power. Under

these regulation conditions, three determining

processes for the presence and abundance of

aquatic organisms are affected, the connectiv-

ity of the system (including flows of nutrients,

sediments and organisms, etc.), the seasonal

variability (rain / dry) and habitat availability.

Eastern Antioquia is one of the regions

with the greatest abundance of water resources

in Colombia and generates 30 % of the coun-

try’s production in approximately 13 500 ha

of reservoirs that regulate numerous rivers

(Ríos-Ocampo & Vélez-Gómez, 2015). There

is located the Tafetanes-Calderas system, a

complex of consecutive reservoirs and diver-

sions that regulates the flow of three rivers.

In this scenario, we studied the composition,

richness, and abundance of AM, with the aim

of evaluating the effect of regulation on their

diversity, based on the hypothesis that the river

sections after regulation present fewer diversity

than non-regulated ones, due to a potential loss

of seasonality of the system. In this scenario,

we studied the composition, richness, and

abundance of AM, with the aim of evaluating

the effect of regulation on their diversity, based

on the hypothesis that, due to a potential loss of

seasonality of the system, firstly, the sites after

regulation are expected to have less values of

alpha diversity (Q0, Q1 and Q2 values). Sec-

ondly, groups of AM exhibit different tolerance

to water quality (Ephemeroptera, Plecoptera,

Trichoptera, hereafter EPT, other arthropods

and non-arthropods), should display different

patterns of affectation. Finally, because of the

regulation, the ENSO phenomena should have

less effects in the sites downstream of the dams.

MATERIALS AND METHODS

Study area: The Tafetanes-Calderas sys-

tem is a complex of consecutive reservoirs and

diversions that regulates three rivers located

in the East of the department of Antioquia-

Colombia (Fig. 1), western of the Magdalena

basin, recognized as the world’s most diverse

diversity hotspot (International Conservation,

2020). The region includes pre-mountain and

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low mountain rain forest life zones (Holdridge,

1967), with rainfall between 3 850 and 5 552

mm/year and an average annual temperature

of 18 °C (IDEAM, 2020a). The sampling

sites were located consecutively before and

after each reservoir as follows: S1 and S2

correspond to the Tafetanes river sites before

(1 780 masl) and after the Tafetanes reservoir

(1 740 masl), S3 and S4 to the Calderas river

sites before (1 340 masl) and after the Calderas

reservoir (1 324 masl), and S5 and S6 to La

Arenosa creek sites before (1 142 masl) and

after the discharge of turbine waters from the

Calderas Reservoir (1 097 masl) (Fig. 1).

The ArcGIS 10.7.1 (ESRI, 2019) software

was used to establish the vegetation covers; a

SENTINEL 2019 satellite image, with reso-

lution 1:10 000 of the study area, which was

processed in four bands and later classified

with five cover types: forests and semi-natural

areas, agricultural territories, clouds, water, and

wet areas and artificial areas, using a buffer

area of 1 km both sides along each riverside.

The riverbank in the three rivers present mainly

semi-natural forest cover, with percentages

above 80 %. The Calderas and Tafetanes rivers

have a greater slope, depth and size of rocks

in the substratum than La Arenosa, but this

last present better conservation in the water

catchment area.

Sampling design: Each river was sampled

four times a year for three years, both sites by

river, up and downstream the regulation (six

sites), in different moments of the hydrologi-

cal cycle: rain, drought and transition (waters

Fig. 1. Study area. A. location; B. flow diagram, reservoirs and drains of the Calderas system; C. location of sampling sites

and coverage map of the Calderas, Tafetanes and La Arenosa rivers.

840 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 836–852, e49975, enero-diciembre 2022 (Publicado Dic. 07, 2022)

rising or falling). In order to evaluate the envi-

ronmental variability, in each period and sam-

pling site, the in situ values of dissolved oxygen

(DO), conductivity, pH, and water temperature

were recorded at 9:00 h, just before AM col-

lection, using Hach brand cells. Additionally,

water samples were taken for turbidity, total

dissolved solids (TDS) and total suspended

solids (TSS) in Analtec laboratories. All in situ

measurements and in the laboratory were made

according to the criteria of the Standard Meth-

ods (APHA, 2017). The sampling periods were

categorized in relation to El Niño phenom-

enon according to NOAA (2020) and IDEAM

(2020b), considering each period as Niño, Niña

or Neutral (without alteration of the ENSO/ El

Niño phenomenon).

Biological sampling: For the collection

of AM, a screen network (kicking net) was

used in the center of the river and a 405 cm2

D-net net with 500 µm mesh on the banks.

For every site sampling was performed in a

transect of 100 m x 1 m and was standardized

by time of 30 minutes. Likewise, manual col-

lection of AM was made in all possible habitats

such as vegetation, submerged wood remains,

rocks, deposition areas, among others; for

which 10 substrata were randomly selected

at each site, according to the methodology

described by Roldán (1996) and Roldán-Pérez

and Ramírez-Restrepo (2008). The obtained

specimens were packed in plastic bags with

96 % ethanol and transported to the Limnol-

ogy Laboratory of the “Universidad Católica

de Oriente” for subsequent identification. The

samples were identified at maximum taxo-

nomic resolution using specialized taxonomic

keys (Archangelsky et al., 2009; Aristizábal,

2002; Bedoya & Roldán, 1984; Manzo & Arch-

angelsky, 2008; Manzo, 2005; Merritt et al.,

2008; Posada-García & Roldán-Pérez, 2003;

Roldán, 1996; Spangler & Santiago-Fragoso,

1992). All the specimens were identified at

the genus level, except for an unidentified

morphospecies of the sub-family Orthocla-

diinae, and another of the family Chironomidae

(hereinafter Chironomidae mf1). The identified

specimens were cured and deposited in the

Aquatic Macroinvertebrate Collection of the

Limnology Laboratory of the “Universidad

Católica de Oriente” (CAM-UCO).

Data analysis: The variability of the phys-

icochemical and biological data at each of the

sites was visually inspected using box and

whisker graphs. To reduce the numbers of

physical-chemical variables was performed a

Principal Component Analysis (PCA) based

on a correlation matrix, with 100 Bootstrap

pseudo-copies. Then, those variables were used

to explore their effects on the AM diversity.

To evaluate the diversity of the AM com-

munity, the following aspects were considered:

the taxon composition, abundance, and diver-

sity aspects; based on the number of effective

species Q0, Q1 and Q2 (Moreno et al., 2011),

respectably, for each site and sampling period.

Thus, the diversity Q of order zero (Q0) refers

to the species richness, regardless of their rela-

tive abundance; the diversity of order one (Q1)

considers the relative abundance of each of the

species in the community; finally, diversity of

order two (Q2), refers to the diversity of the

most abundant or dominant species (common

species) (Jost, 2006).

To establish the differences in the taxo-

nomic composition between samples, cluster

analysis was used, where the composition by

order was considered an attribute of the sample

and the groups were identified by calorography.

The similarity matrix was obtained with the

Bry-Curtis index, using the R-Wizard software

(Guisande et al., 2014). This similarity analysis

was also performed at the minimum taxonomic

level, to corroborate the results.

To establish the differences in taxon com-

position among samples, percentage similarity

measures were used, where the taxon composi-

tion was considered an attribute of the sample,

and the clusters were identified using clusters

graphs. The similarity matrix was obtained

with the Bry-Curtis index, using PAST v 4.11

(Hammer et al., 2001).

To identify spatial (sampling sites, regula-

tion condition) and temporal patterns (ENSO

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phenomenon) in the composition of the AM

community in relation to environmental vari-

ables, Canonical Discriminant Analysis (DCA)

was conducted. The analysis included the bio-

logical variables: total abundance, diversity

(Q0, Q1, Q2) and abundance of the groups:

non-arthropods (genera of the classes Gastrop-

oda, Bivalvia, Clitellata and Rhabditophora),

ETP (Ephemeroptera, Plecoptera, Trichoptera),

Diptera (12 genera) and other arthropods (gen-

era of the orders Trombidiforme, Hemiptera,

Lepidoptera, Megaloptera, Coleoptera, Odo-

nata and Decapoda). This grouping represents

species according to their tolerance and bioin-

dication of environmental quality, considering

that ETP genera are indicators of good water

quality, non-arthropods and Diptera are indi-

cators of poor quality, and other arthropods

include groups with variable tolerance, but in

intermediate ranges. The contributions of the

different biological groups and environmental

variables in the discriminant analyzes by factor

were represented graphically as vectors whose

length is proportional to the contribution of

each variable to the explanation of the variance.

Subsequently, a non-metric multidimensional

scaling (NMDS) was performed using a matrix

of distances, considering the species (mor-

phospecies), based on the Bray-Curtis index

in PAST v 4.11 (Hammer et al., 2001). The

stress value reflects how well the ordination

summarizes the observed distances among the

samples. To reduce the stress, a three-dimen-

sional (3D) ordination space was performed

of which two axes were shown. Stress values

below 0.15 were considered a good indicator

of configuration or fit (Kruskal, 1964). Also,

an analysis of similarities (ANOSIM) was used

to test the overall AM communities for signifi-

cant differences in taxon composition between

sampling sites (Bray-Curtis similarity, 9 999

permutations, pairwise comparison by Bonfer-

roni corrected P-values).

Finally, to evaluate the effect of environ-

mental conditions (temperature and conduc-

tivity) and regulation factors and ENSO on

biological variables, the following generalized

linear model (GLM) was used, where;

(1)

Biological variables (Abundance, Q0, Q1

and Q2 index), were used as response or

exogenous variables yjklmn are the biological

variables (Abundance, Q0, Q1 and Q2 index),

and regulation (Regulated, unregulated) and

ENSO were used as endogenous variables or

factors. Temperature and electrical conductiv-

ity were integrated as covariates to the GLM;

In addition, the error associated with each

measurement was taken as random. β0 is the

intercept, αj is the effect of the j-th regulation

factor (Regulated, unregulated), ϑk is the effect

of the k-th ENSO, β1 is the linear regressor for

the covariate temperature (T), β2 is the linear

regressor for the covariate conductivity (C).

εijklmn, is the random error associated with

each measurement.

Seven generalized linear models were

compared with different probability families

(Gaussian, Poisson and Gamma) and with

different link functions; this, to identify the

model that best fit the type of data analyzed.

The best models were selected regarding the

lowest value of the Akaike (AIC) and Bayesian

(BIC) information criterion and in relation to

the real behavior of the variable in the field.

Only factors with a significant effect perceived

in previous analyzes were included in the GLM

analysis, this in order not to include bias in the

final model. These analyzes were carried out

using the specialized R-project software, ver-

sion 3.6.3 (R Core Team, 2020) and R-Wizard

4.1 software (Guisande et al., 2014).

RESULTS

Environmental variability: The param-

eters measured in the field, such as water

temperature, pH and dissolved oxygen, pre-

sented little spatial or temporal variability, with

temperature averages of 18.4 °C for Tafetanes,

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19.6 °C for Calderas, and 21.7 °C for La

Arenosa; while the dissolved oxygen aver-

ages for the three sources were between 7.5

and 7.7 mg/l; and the pH average was kept

in neutral ranges, with averages between 7.3

and 7.4 pH units. The variability of electrical

conductivity was between 11.1 µS/cm and 54

µS/cm. Other parameters were analyzed in

the laboratory (Total Suspended Solids TSS,

Total Dissolved Solids TDS, Total Solids TS

and Chemical Oxygen Demand COD), equally

low values were found for the three rivers. In

the case of TSS, averages of 41.4 mg/l were

found in Tafetanes, 13.5 mg/l in Calderas, and

10.7 mg/l in La Arenosa; the average TDS

concentrations for the three rivers were very

similar with values between 38.1 mg/l and 44.1

mg/l. The organic matter that could be oxidized,

biodegradable or not, represented in the COD,

presented averages concentrations of 25.8 mg/l

in Tafetanes, 22.04 mg/l in Calderas, and 21.9

mg/l in La Arenosa. The measured parameters

showed low concentrations, typical of surface

sources anthropically little intervened and with

good physicochemical water quality according

to Chapman. After the PCA, just five variables

were selected for the NMDS (data not shown).

The variability of both physicochemical and

biological parameters is presented in Fig. 2.

Structure of macroinvertebrates com-

munity: In total, 53 214 individuals from 165

taxa were collected, and most of them were

from the orders Ephemeroptera (23.8 %), Tri-

choptera (23 %), Coleoptera (21.76 %) and

Diptera (18.47 %), totaling about 90 % of

catches. These orders were important at all sites

and sampling periods, but their abundances

were higher at non-regulated sites, especially at

site 5 (Fig. 2B). At the family level, Elmidae,

Baetidae Leptoceridae, Leptohyphidae, and

Chironomidae were the most abundant at all

sampling sites and times, and they predomi-

nated at site S5.

The species composition showed that an

unidentified taxon of the Orthocladiinae sub-

family, and another of the Chironomidae fam-

ily (hereinafter Chironomidae mf1), as well as

Macrelmis mf, Nectopsyche mf., Simulium mf.,

Leptohyphes mf., Smicridea mf., Anacroneuria

mf., Rhagovelia mf., Chimarra mf., Camelo-

baetidius mf., Baetodes mf., Thraulodes mf.,

Grumichella mf., were the most abundant and

frequent at the different sites and years of sam-

pling. However, the similarity analysis showed

differences between regulated and unregulated

sites for both, taxa and order levels. In addi-

tion, it denoted substantial differences in the

taxonomic composition in the regulated sites

during the ENSO El Niño period. The figure

that best represents the pattern is shown (Fig.

3). The orders that best represent the difference

in composition between ENSo and regulation

conditions were Trichoptera, Diptera, Colep-

tera, and Ephemeroptera.

Spatial and temporal patterns: The

discriminant analysis among sampling sites,

intervention states, and El Niño phenomena

on the environmental and biological variables

obtained between 65 % and 75 % of cases cor-

rectly identified through cross-validation; and

it explained between 70 % and 100 % of the

variance observed in the first canonical axis

(Fig. 4).

A gradient was observed at the sampling

sites with clear differentiation from the S5 site,

based on greater abundance, species richness

(Q0) and the presence of ETP organisms, and

other arthropods; accompanied by a notable

difference in water temperature, conductivity

and dissolved solids. The regulated sites were

distinguished by a greater presence of Diptera

and non-arthropod organisms, accompanied

by temperature difference and low concentra-

tions in TSS; and consequently, low turbidity.

On the other hand, non-regulated sites were

characterized by higher values in most of the

environmental and biological variables. The

El Niño phenomenon was differentiated by the

abundance of ETP and non-arthropods organ-

isms. The former dominating in the nonregu-

lated sites and the latter in the regulated sites,

while the La Niña phenomenon was character-

ized by the greater presence of Diptera and

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other arthropods. The NMDS ordination (stress

= 0.14, r2 = 0.53) separated the samples from

S5, while a mixture of samples from other sites

was observed (Fig. 5). It was supported by the

significant difference detected among sites

(ANOSIM, R = 0.3935, P = 0.0001), in which

pairwise comparison suggested differences of

S5 with every other sampling site, including

the site S6 on the same river (La Arenosa) (P =

0.0015). Every other comparison between sites

at the same river was not significant (P > 0.05).

Effects of regulation on diversity: The

model that best fit the abundance variable was

the model with Gamma distribution and loga-

rithmic link function; the values for this model

of AIC and BIC were 949.09 and 964.307,

respectively. By the Q0 index, the model with

the lowest AIC and BIC values (474.5 and

489.722, respectively) was the one that adjus-

ted to a Gaussian distribution with an identity

link function. Otherwise, for the Q1 (AIC =

378.38, BIC = 393.596) and Q2 (AIC = 353.14,

Fig. 2. Box plot of variability by sites at the Calderas system. Environmental variables on the left column and biological

variables on the right column. Whiskers represents the range of the values for each variable. A. Water temperature. B.

Abundance. C. Conductivity. D. Diversity order 0 (species richness). E. Dissolved oxygen. F. Diversity order 1. G. Total

suspended solids. H. Diversity order 2.

844 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 836–852, e49975, enero-diciembre 2022 (Publicado Dic. 07, 2022)

BIC = 368.362) indices, the best models were

those that fit a Gaussian probability distribu-

tion with an inverse link function. The esti-

mates and their respective standard errors are

summarized in table 1.

Regarding the model that is best adjust-

ed to the AM abundance variable, it can be

observed that there is a significant (P = 0.0278)

and negative effect of the regulation on the

abundance of AM. A significant and positive

effect of temperature (0.27365) and conductiv-

ity (0.03469) on this variable was also identi-

fied, which means that as temperature and

conductivity increase, the abundance of AM

also increases (Table 1).

For the Q0 variable, a negative (-7.906)

and highly significant (P = 0.000627) effect

of regulation was also found; suggesting that

regulation diminishes the richness of AM. For

this variable, as in abundance, very similar

effects were also found for temperature (Esti-

mate 3.989, P = 0.00000337) and conductivity

(Estimate 0.3451, P = 0.019788). Also, con-

trasting effects were observed between La Niña

phenomenon (Estimate -0.295, P = 0.92179)

and El Niño phenomenon (Estimate 5.923, P =

0.049414) on the richness of AM (Q0).

Regarding variables Q1 and Q2, only

effects of regulation were observed (P < 0.05);

For the other factors (site, ENSO), no effects

were identified.

DISCUSSION

Human intervention on rivers for hydro-

electric generation, by dams and reservoirs,

suppose a degradation of river ecosystems by

interrupting the natural flow of water, with

Fig. 3. Similarity analysis in the composition of aquatic macroinvertebrate species among sites and sampling times (ENSO

phenomena) at the Calderas system.

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Fig. 4. Discriminant analysis of the sampling sites, regulation condition, and ENSO phenomena, based on environmental

variables, abundance, richness, and composition of aquatic macroinvertebrate species at the Calderas system. Whiskers

represents the range of the values for each variable.

846 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 836–852, e49975, enero-diciembre 2022 (Publicado Dic. 07, 2022)

consequent reductions in the diversity of aquat-

ic biota (Anderson et al., 2018; Bredenhand &

Samways, 2009; Lees et al., 2016). However,

many of the responses of the macroinvertebrate

community of the tropical Andean rivers to the

regulation are still unknown. Therefore, this

work evaluated whether the regulation affects

the diversity of AM, as a consequence of the

potential decrease in environmental variabil-

ity in a system of three regulated rivers in the

Colombian Andes (Calderas system).

According to the initial hypothesis, a

reduction in seasonality of regulated rivers was

observed, which was reflected in little temporal

environmental variability. Under these condi-

tions, the results suggest that differences in

AM diversity, particularly richness and abun-

dance, were related to both sampling site

and effect of regulation on rivers. The three

regulated systems presented lower diversities

downstream to the reservoirs, regardless of the

hydrological moment or the climatic phenom-

enon (ENSO). Significant negative effects of

regulation were found on abundance, total rich-

ness (Q0), of common species (Q1) or of domi-

nant species (Q2), as has been documented in

regulated rivers in temperate zones (Martínez

et al., 2020), but unlike these, in the Calderas

system there is no seasonal component in the

diversity response. This reduction in seasonal-

ity contributes to explain the negative effect

of regulation, since the presence of dams and

diversions reduces flow peaks and creates

uniform and not very dynamic habitats, which

concentrate organic matter and favor the more

tolerant species.

The reduction of post-reservoir AM rich-

ness has been documented in some empirical

studies (Mesa, 2010; Milner et al., 2019), and

others summarized in the review by Wu et al.

(2019), in which an increase in the abundance

of pollution-tolerant groups, and the reduc-

tion of less tolerant groups such as ETPs, are

reported. However, natural interruptions in the

course, such as waterfalls up to 70 meters high,

seem to have less effect on the reduction of

ETP communities, as documented in rivers in

the Cerrado of Brazil (Andrade et al., 2020),

confirming that the decrease in seasonality has

an equal or greater effect on the composition

and abundance of tropical Andean macroinver-

tebrates than the loss of connectivity.

Fig. 5. Non-metric multidimensional (NMDS) ordination (stress = 0.014, r2 = 0.53) for the total set of sampling site of

aquatic macroinvertebrates together with the environmental variables, temperature, suspended solids (TSS), dissolved

solids (TDS) and dissolved oxygen (DO) at the Calderas system. Matrix data determined by Bray Curtis distances (9 999

permutations) of species abundances. Empty and fill symbols denote sampling sites before and after regulation respectively.

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On the other hand, even though the effects

on the flows associated with the ENSO / El

Niño events have been documented in this

region of the Colombian Andes (Poveda et al.,

2001), there were no significant effects of the

ENSO on the abundance of AM. Nevertheless,

both the dry (El Niño) and the rainy (La Niña)

ENSO periods were related to the lowest abun-

dances, in relation to the neutral years; except

in sites S2 and S4 where the dry bed condition

TABLE 1

Estimates for biological and physico-chemical variables measured in AM and their relationship to environmental factors in

the rivers of the Tafetanes-Calderas system.

Biological variables Physicochemical variables

Abundance of AM Dissolved oxygen

Estimate Error Standard P-value Estimate Error Standard P-value

Intercept 632.93 498.07 0.21 7.51 0.25 < 0.01

Drought season -426.67 325.24 0.19 0.15 0.16 0.35

Transition season -1 497.50 622.78 < 0.05 0.88 0.31 < 0.01

2017 - - N.A 0.28 0.12 < 0.05

2018 - - N.A -0.34 0.09 < 0.01

Niña 1 334.15 745.96 0.08 - - N.A

Niño 1 229.82 523.80 < 0.05 - - N.A

site 2 -67.40 199.73 0.74 -0.05 0.09 0.62

site 3 58.55 192.59 0.76 0.24 0.09 < 0.05

site 4 271.46 192.59 0.16 0.04 0.09 0.69

site 5 2 081.18 192.59 < 0.01 -0.16 0.09 0.09

site 6 243.73 192.59 0.21 0.01 0.09 0.92

Q0 TEMPERATURE

Intercept 40.45 8.61 < 0.01 17.30 1.08 < 0.01

site 2 -6.05 3.45 0.09 1.69 0.42 < 0.01

site 3 -3.29 3.33 0.33 2.02 0.42 < 0.01

site 4 -3.66 3.33 0.28 1.95 0.42 < 0.01

site 5 24.98 3.33 < 0.01 4.81 0.42 < 0.01

site 6 6.52 3.33 0.06 3.38 0.42 < 0.01

Q1 CONDUCTIVITY

Intercept 19.43 4.54 < 0.01 18.50 9.28 < 0.05

site 2 -2.89 1.82 0.12 2.32 3.61 0.52

site 3 -2.37 1.75 0.18 6.90 3.61 0.06

site 4 -6.10 1.75 < 0.01 7.14 3.61 < 0.05

site 5 1.14 1.75 0.52 12.51 3.61 < 0.01

site 6 -0.52 1.75 0.77 6.50 3.61 0.08

Q2 TSS

Intercept 14.44 3.72 < 0.01 -19.89 42.74 0.64

2017 - - N.S 50.39 21.06 0.02

2018 - - N.S 18.07 15.92 0.26

site 2 -2.02 1.49 0.18 -20.45 16.63 0.22

site 3 -1.68 1.44 0.25 -43.76 16.63 < 0.01

site 4 -4.94 1.44 < 0.01 -32.35 16.63 < 0.05

site 5 -1.23 1.44 0.39 -45.14 16.63 < 0.01

site 6 -1.35 1.44 0.35 -36.71 16.63 < 0.05

848 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 70: 836–852, e49975, enero-diciembre 2022 (Publicado Dic. 07, 2022)

maintains low levels, regardless of the hydro-

logical period, ratifying the reduction of the

effect of hydrological variability in regulated

systems. At these sites, they only presented

differences at moments of maximum precipita-

tion, when runoff or the discharge of the reser-

voirs increase the water level. In this sense, the

response of the AM to the ENSO hydrological

phenomena will depend on the conditions of the

local habitat and the interaction with anthropic

regulation. A positive effect of El Niño on

Richness (Q0) was also observed in Calderas

system, as has been documented in other stud-

ies, in response to the decrease in drag and

the increase in habitat heterogeneity (Blanco,

2003; Longo et al., 2010; Ríos-Pulgarín et al.,

2016; Rodríguez-Barrios et al., 2011), however,

the significance of this effect is restricted to

unregulated sites. This suggests a buffer effect

of reservoirs on hydrological extremes, and

consequently a decrease in the impact of ENSO

on diversity in regulated systems.

In terms of composition, effects of both

regulation and sampling site are also observed.

The results of this work showed greater abun-

dances of species of EPT and other arthropods

in the sites of non-regulated flow, while the spe-

cies which are indicators of organic contamina-

tion and tolerant to hydrological disturbance

(annelids, mollusks, and Diptera Chironomids)

predominated in the regulated sections as dry

beds. This is probably related to unfavorable

conditions in the downstream sites of the regu-

lation (S2, S4 and S6), where the first two are

dry beds, in which the permanently reduced

current favors puddle formation, modifying

the temperature and oxygen concentration. The

last site (S6) has the opposite effect since, after

regulation, its flow is significantly increased

when receiving the turbine waters of the Cal-

deras reservoir. This also implies a reduction

in temperature and an increase in organic

matter (mainly non-biodegradable), suspend-

ed solids and turbidity. Such fluctuations in

water level and water quality would affect

the AM community as a consequence of the

discontinuity in the ecological characteristics

(Hurtado et al., 2005).

Simplified communities like these, with

an abundance of tolerant taxa, have been doc-

umented in degraded environments (Mesa,

2010). However, it is important to say that

Chironomids, such as Orthocladiinae, were

found in both impacted and conserved rivers,

probably due to their species richness and wide

range of habitat preferences. The species in this

group have been found widely distributed in

all types of aquatic habitats in the Andes from

72 to 4 425 masl (Ospina-Torres et al., 2018).

This subfamily is phytophile, and is favored

by the presence of periphyton, particularly

filamentous algae (Cranston, 1995); so that

shallow and clear water sites such as S5 or as

a dry bed (S4) would offer abundant resources

for this group, despite the contrasts in envi-

ronmental quality.

Likewise, it is important to highlight the

differences in composition of the communities

(Fig. 4, Fig. 5), where site S5 stands out, not

only for its richness and diversity of common

species-weighted by its relative abundance

(Q1) but for a different composition, with 18

exclusive morphospecies and between 30 and

100 times more abundance of genera such

as Hexatoma, Macrelmis, Microcylloepus and

Nectopsyche; if it is compared to other sites.

These genera are recognized as bioindicators

in aquatic ecosystems. For example, Hexatoma

(Diptera) is highly related to riparian coverage

and is intolerant to pollution (Iñiguez-Armijos

et al., 2018). According to Ríos-Touma et

al. (2011), Elmids such as Macrelmis prefer

highly oxygenated surface waters which guar-

antee the formation of the plastron (Buss et al.,

2002); Microcylloepus are often found under

rocks, under the bark of submerged trunks,

or in dead leaves and submerged branches

(Iñiguez-Armijos et al., 2018); Nectopsyche

has a high dependence on riverside vegetation

(Ríos-Touma et al., 2011). The aforementioned

can be associated with a riverbank in better

conditions since site S5 has greater upstream

coverage and less deforestation in the river near

the canal; and, therefore, it has a greater offer

of allochthonous habitat and resources, as it has

been reported for other highly forested tropical

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streams (Iñiguez-Armijos et al., 2018). These

results ratify that riparian vegetation along

the catchment area is important to the AM

community (Martínez et al., 2020; Meißner

et al., 2019; Villeneuve et al., 2018). Thus,

the conservation status of the vegetation cover

and the structure of the habitat, and not only

the absence of regulation, seem to favor the

diversity of AM in this system. So that, the con-

servation of the forest adjacent to the riverbed

would be a potential buffer for the impacts gen-

erated by the regulation; and in turn, a source

of recolonization for the downstream-regulated

sections (Milner et al., 2019).

In terms of the influence of water quality

variables, the temperature was the parameter

that showed the greatest variation and also the

greatest effect on AM diversity. Since its varia-

tion was related to both the regulation and the

thermal floor of each river. Temperature effects

especially affected the creek La Arenosa (1 100

masl) after receiving the turbine waters that

enter from the Calderas reservoir (1 340 masl),

between sites S5 and S6, where the reduction

of between 1.4 and 4 °C in temperature, added

to the increase in flows, substantially modify

the habitat and contribute to the differences

found in the taxonomic composition, abun-

dance, richness, and diversity of species. This

effect is a consequence of regulation, that by

means of a transfer equates the temperature

of the river of a thermal floor that is naturally

warm with the temperature of a colder thermal

floor. The effect of temperature on diversity

is related to the metabolism, growth rate and

emergence periods of the different species

(Martínez et al., 2020).

Finally, since it is a mountain system with

low and medium flows, it is possible that the

relative importance of the regulation differs

regarding larger rivers. This is a future research

field in order to have better elements for the

management of regulated systems, incorporat-

ing both hydrological parameters and aspects

of land use and vegetation cover at different

scales, more comprehensively reflecting the

factors that regulate the ecology of each river

at a local and regional scale.

Regulated systems presented lower diver-

sities than non-regulated ones; due to, although

there were some temporary changes in environ-

mental variables, the taxonomic composition,

abundance, and total richness responded to spa-

tial differences, being greater in non-regulated

sites regardless of the hydrological moment.

However, the most notable spatial differences

are related to the site where the best habitat

supply favors greater richness and abundance.

Thus, the conservation status of the vegetation

cover and the structure of the habitat, not only

the absence of regulation, seems to favor the

diversity of aquatic macroinvertebrates in this

system. In this way, the conservation of the for-

est adjacent to the riverbed would be a potential

source of mitigation of the impacts generated

by the regulation.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank all members of the “Grupo de

Investigación de Limnología y Recursos Hídri-

cos” for their contribution in field activities and

laboratory processing and to the energy gener-

ating company ISAGEN, owner of the data, for

allowing the use of information.

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