Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

Effects of environmental stability and phycoperiphyton structure on the

macroinvertebrate community of regulated Andean rivers

María Isabel Ríos-Pulgarín1,2*; https://orcid.org/0000-0002-4543-6989

Valeria Henao-Lopera1 *; https://orcid.org/0000-0003-1281-6800

María Andrea Henao-Henao1; https://orcid.org/0000-0002-7809-0136

Isabel Cristina Gil-Guarín1; https://orcid.org/0000-0003-3445-1988

1. Grupo de Investigación en Limnología y Recursos Hídricos, Universidad Católica de Oriente, Rionegro, Colombia;

vale.h.l26@gmail.com; picarita02@gmail.com; isabelcristinagil84@gmail.com

2. Programa de Ingeniería Ambiental, Universidad Católica de Oriente, Rionegro, Colombia; mariaisabel.rios536@

gmail.com, mrios@uco.edu.co (Correspondencia*)

Received 19-VII-2022. Corrected 07-III-2023. Accepted 05-VI-2023.

ABSTRACT

Introduction: The variability in the structure of aquatic communities is frequently attributed to environmental

changes; however, in stable environments such as regulated rivers, trophic interactions could be another key

environmental factor determining the structure of these communities. These alterations could cause a greater

growth of algae, and in turn, changes in the functional groups and in the composition of the macroinvertebrate

community favoring the dominance of certain groups of organisms.

Objective: To identify the effects of environmental variations and changes in the structure of the phycoperiphy-

ton on the macroinvertebrate community of regulated Andean rivers.

Methods: We analyzed environmental and biological data collected in quarterly samples carried out between

2010 and 2018 in two rivers of the Central Andes (Antioquia - Colombia), for a total of 27 samples. Sample

collections used standardized methods. Different statistical models were used to establish spatial and temporal

patterns of the environmental variables, of the abundance and/or density and diversity of phycoperiphyton and

macroinvertebrates, as well as the trophic relationships that exists between them.

Results: We found that regulated rivers present relatively little environmental variability. The environmental

parameters with the greatest variation were temperature, turbidity, and orthophosphates; these last two were the

abiotic variables with the greatest contribution to benthic instability.

Conclusion: The presence of scraping and foraging macroinvertebrates was more affected by the stability of

the phycoperiphyton density than by environmental variables, showing the importance of trophic interactions in

regulated rivers and the bottom up control in these ecosystems.

Key words: ENSO; stability index; hydroelectric generation; regulation.

RESUMEN

Efectos de la estabilidad ambiental y estructura del ficoperifiton en la comunidad

de macroinvertebrados en ríos andinos regulados

Introducción: La variabilidad en la estructura de las comunidades acuáticas se atribuye frecuentemente a

cambios ambientales, no obstante, en ambientes estables como ríos regulados, las interacciones tróficas podrían

ser otro factor ambiental clave determinante de la estructura de estas comunidades. Estas alteraciones podrían

https://doi.org/10.15517/rev.biol.trop..v71i1.51800

AQUATIC ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

INTRODUCTION

Among the aquatic ecosystems, the tropi-

cal rivers of the Andes stand out for the diver-

sity and heterogeneity of the communities they

contain (Cavelier et al., 2008). In addition,

they are characterized by representing an abun-

dant water supply and high erosion processes

and transport of sediments, due to climatic

conditions as well as the geomorphology and

topography of the region (Gil-Gómez, 2014). In

Colombia, this abundance of water has favored

its use for hydroelectric generation, particularly

in eastern Antioquia, where a significant num-

ber of energy projects are concentrated. Conse-

quently, numerous rivers located in this region

of the country have been dammed.

One of the main effects of regulation,

beyond changes in water quality, is the altera-

tion of the flow regime and habitat for aquatic

communities (Ponsati, et al., 2015; Roldán-

Perez, 2016). Particularly physical, chemical,

and morphological alterations in the chan-

nels, both on the spatial and temporal scale

(Gil-Gómez, 2014; Roldán- Pérez & Ramírez,

2022) can directly affect the stability of the

structure of benthic communities such as phy-

coperiphyton and macroinvertebrates (Carlisle,

et al., 2011; García et al., 2017). For example,

flow regulation can cause modifications in

the characteristics of the substrata and/or the

disposition of allochthonous organic matter,

altering the river’s capacity to process organic

matter and causing changes in trophic func-

tional groups, including an increase in filter-

feeding organisms that are filter-collectors on

the shredders (Cabrera et al., 2021; Tank, et al.,

2010; Vimos-Lojano, et al., 2020). Or it can

also induce a proliferation of algae that in turn

alters the composition of the macroinvertebrate

community, favoring the dominance of species

that consume these resources (e.g., mayflies,

Tricoptera and Plecoptera-ETP) (Tonkin et al.,

2009). The ENSO/El Niño and La Niña phe-

nomena have also been documented for their

significant effects on the rainfall and drought

regime. Consequently, there are effects on

variations in the flow, temperature and water

chemistry (turbidity, nitrogen, dissolved oxy-

gen), as well as effects on the characteristics

of the habitat that include the availability of

substrates and the speed of the flow, causing

alterations in the taxonomic and functional

composition and, in general, in the structure of

the macroinvertebrate and phycoperifiton com-

munities (Ríos-Pulgarín et al., 2016). For this

reason, these phenomena should be considered

in studies on benthic communities in regulated

systems, both to assess possible synergistic

effects with regulation, and to avoid misinter-

pretations of the results.

provocar un mayor crecimiento de algas y, a su vez, cambios en los grupos funcionales y en la composición de la

comunidad de macroinvertebrados favoreciendo la dominancia de determinados grupos de organismos.

Objetivo: Identificar el efecto de los cambios ambientales y de la estructura del ficoperifiton sobre la comunidad

de macroinvertebrados de ríos Andinos regulados.

Métodos: Se analizaron datos ambientales y biológicos recolectados en muestreos trimestrales realizados entre

2010 y 2018 en dos ríos de los Andes Centrales (Antioquia - Colombia), para un total de 27 muestras. La reco-

lección de muestras empleó métodos estandarizados. Se utilizaron diferentes modelos estadísticos para establecer

patrones espaciales y temporales de las variables ambientales, de la abundancia y/o densidad y diversidad de

ficoperifiton y de los macroinvertebrados, así como las relaciones tróficas que existen entre ellos.

Resultados: Se encontró que los ríos regulados presentan relativamente poca variabilidad ambiental. Los pará-

metros ambientales con mayor variación fueron: temperatura, turbidez y ortofosfatos; las dos últimas variables

abióticas fueron las que más aportaron a la inestabilidad bentónica.

Conclusión: La presencia de macroinvertebrados raspadores y recolectores fue más afectada por la estabilidad de

la densidad del ficoperifiton que por las variables ambientales, evidenciando la importancia de las interacciones

tróficas en ríos regulados y el control bottoom up en estos ecosistemas.

Palabras clave: ENSO; índice de inestabilidad; generación hidroeléctrica; regulación.

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This is an important and necessary knowl-

edge, since these communities have a funda-

mental role in the contribution and transfer of

energy, either as intermediate or final links with

respect to other trophic levels (Mora-Day et al.,

2009), given that they consume the organic

matter produced by photosynthetic organisms

growing as riverside vegetation that is trans-

ferred to their predators (Fernández, 2012).

At the base of these trophic chains is the

phycoperiphyton, made up of different divi-

sions of algae developed on a substrate that fix

inorganic carbon and capture the sun´s energy,

converting it into organic compounds (Moreno-

Rodríguez, et al., 2017). The next link are the

macroinvertebrates, made up mostly of larval

arthropods, mollusks, and annelids that are

especially abundant in tropical Andean rivers

and that have an important role in the grazing

of the phycoperiphytic community (Holomuzki

et al., 2010).

Numerous authors have studied the rela-

tionship of environmental parameters with the

structure of aquatic benthic communities (Gor-

dillo-Guerra et al., 2014; Huertas-Farias et al.,

2019; Oscoz et al., 2007), but only a few have

considered the trophic connections between the

communities (Carrasco-Badajoz, et al., 2022;

Moreno-Rodríguez et al., 2017; Silva-Poma &

Huamantinco-Araujo, 2020;). These connec-

tions are important since phycoperiphyton is

a source of energy for macroinvertebrates and

can exercise bottom-up control (from producers

to consumers) in the aquatic ecosystem. Graz-

ing can exercise significant control over algal

density and biomass, but different responses

are expected, depending on the characteristics

of the producer and the herbivore, since the

morphology and chemistry of a producer can

affect its consumption risk (Holomuzki et al.,

2010). This aspect has not yet been explored

in regulated tropical Andean rivers, where the

effect of seasonality may be less than that of

biological interactions. To evaluate this interac-

tion, it is necessary to know the basic biology

of the taxa and to make use of statistical tools

that identify the relationships between the bio-

logical groups.

This study aims to identify the effects of

environmental variations and changes in the

phycoperiphyton structure on the macroinver-

tebrate community in regulated Andean rivers.

Given the regulation scenario, our starting

hypothesis is that changes in phycoperiphyton

density and diversity in these systems would

have an equal or greater effect than environmen-

tal variability on macroinvertebrate abundance.

MATERIALS AND METHODS

Study area: Punchiná is a hydroelectric

generating reservoir, with a storage capac-

ity of 62 million m3, located at 750 meters

altitude in the eastern part of the department

of Antioquia in Colombia (6º12’39” N &

74º50’26” W) in the municipalities of Guatapé

and San Carlos (Fig. 1). The reservoir and its

tributary basins (Guatapé and San Carlos riv-

ers) belong to the Holdridge (1979) “lower

montane tropical humid forest” life zone with

temperatures between 19 °C and 23 °C and

average annual rainfall between 1 800 mm

and 2 500 mm (Forero et al., 2014). It is a

region influenced by the intertropical conver-

gence zone (ITZ) that receives high radiation

and presents interaction between the northeast

and southeast trade winds, favoring condensa-

tion and precipitation. A bimodal precipitation

regime generates the distribution of rainfall in

two wet periods (April to May and October to

November) and two dry periods (December

to March and June to September) (Barrera-

Olarte, 2018). The soils are of low fertility,

acid, stony, and easily erodible, it is a for-

est vocation land (CORNARE, 2010). Before

emptying in the Punchiná reservoir the San

Carlos and Guatapé rivers can be characterized

by relatively deep, turbid waters with a laminar

flow and few emerged substrates or litter accu-

mulations (Ríos-Pulgarín et al., 2020). Both

tributaries are regulated by a complex system

of reservoirs: A second reservoir is found

upstream on the Guatapé River, and the San

Carlos River receives turbinated water from a

third reservoir through a tributary river.

Sampling design: This study was carried

out between 2010 and 2018 in three annual

sampling periods during different hydrological

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periods: dry season (June), transition (Septem-

ber) and rainy season (November) for a total

of 27 samples. In the Guatapé-RG2 and San

Carlos-RSC1 rivers, sections of 100 meters

each were selected to establish the sampling

sites. The El Niño-Niña/Southern Oscillation

(ENSO) conditions for each year were defined

according to the NOAA-NCEP ONI (Oceanic

Niño Index) report (2014) for the American

Pacific and comparisons between the mean

historical monthly precipitation of the study

basin during the sampling periods (IDEAM,

2018). Based on this information, the periods

2010-2011 and 2016 were defined as La Niña,

2012-2014, 2017 and 2018 as neutral, and 2015

as El Niño.

Sampling: At each sampling sites, the

temperature (oC), dissolved oxygen (DO)

(mg/l), the percentage of oxygen saturation

(%), pH, electrical conductivity (µS/cm) were

measured with a Hach HQ40D multi-parameter

instrument. Water samples for ex situ analysis

of turbidity (N.T.U.), solids (mg/l) (suspended,

dissolved and total), total iron (mg Fe/l), nitrites

(mg NO2-/l), nitrates (mg NO3-/l), ammoniacal

nitrogen (mg NH3/l), total phosphorus (mg P/l),

orthophosphates (mg PO4-3/l), and chemical

oxygen demand (COD mg/l) were taken. In

all cases, we followed standard methods for

examination of water and wastewater using the

22nd edition (Baird & Bridgewater, 2017) and

we collected biological samples (macroinverte-

brates and phycoperiphyton).

The phycoperiphyton samples were col-

lected in ten substrata immersed in the bed

along the 100 m stretch, using plastic brushes

and 10 cm2 quadrants until obtaining a scraping

area of 100 cm2 per site. Samples were stored

in plastic containers and preserved the contents

Fig. 1. Sampling sites in the tributaries of the Punchiná reservoir. Modified from Ríos-Pulgarín et al. (2020).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

with Lugol’s solution. Macroinvertebrates were

collected along the same stretch, using a D-net

with a 400 µm mesh eye in areas with sub-

merged vegetation, a screen net in sandy areas

(both with 0.5 mm mesh eye), and manual sam-

pling on substrates such as rocks or logs using

tweezers to form an integrated sample, with a

standardized effort of 20 minutes/rig/sample,

for a total of one hour of sampling per sample.

The specimens were stored in glass PET bottles

with 70 % alcohol.

Laboratory work and identification:

Both communities were analyzed in the Lim-

nology Laboratory of the Universidad Católica

de Oriente. Taxonomic determination of phyco-

periphyton was carried out following the keys

of Bicudo and Menezes (2006), Guiry & Guiry

(2018), and Ramírez (2000). The count of indi-

viduals per species was made using an Olym-

pus CKX41 inverted microscope following

the methodology of 30 random fields (Lund,

et al., 1958) and a magnification of 40X 10.

Density is reported as individuals per square

centimeter (ind/cm2) (Ross, 1979). Taxonomic

determination of the macroinvertebrates was

made to the lowest possible level following the

keys of Aristizábal (2017), Manzo & Archan-

gelsky (2008), McCafferty (1981), Merrit et

al. (2008), and Posada & Roldán (2003). The

count was carried out using a Carl Zeiss Stemi

508 stereo microscope at a magnification of

10X 40 and included the individuals collected

with the different instruments accumulated per

sample and expressed as abundance/sample.

The organisms were deposited in the macroin-

vertebrate reference collection of the Univer-

sidad Católica de Oriente CM-UCO and were

also registered with the Alexander von Hum-

boldt Biological Resources Research Institute

of Colombia using the Darwin Core format

(https://ipt.biodiversidad.co/sib/resource?r =

uco-002). Based on secondary information,

each taxon was assigned to one of the five tro-

phic functional groups (GT), according to the

classifications of Silva-Poma & Huamantinco-

Araujo (2022), Ríos-Pulgarín et al., (2016),

Chará-Serna, et al. (2010) and Tomanova et

al. (2006). The five groups were as follow: CF

(filterers), CG (gatherers), SH (shredders), SC

(scrapers) and PR (predators). In those cases, in

which the genus included species with trophic

flexibility or with different habits, the cor-

responding combinations were presented, for

example, as CF-CG.

Data analysis: Biological variables were

used to establish the basic structure of the

communities through the Hill numbers, in

terms of abundance or density, richness (Q0),

diversity of common species equivalents (Q1),

and dominant species (Q2) (Moreno, 2001),

using the PAST 3.12 Software (Hammer, et al.,

2001) The abundance of groups of macroin-

vertebrates, indicators of environmental water

quality, was estimated, categorizing the organ-

isms into the following groups: low quality

due to organic contamination (non-arthropods

Gastropoda, Bivalvia, Clitellata and Diptera),

high quality (ETP Ephemeroptera, Plecoptera,

Trichoptera), and variable tolerance in inter-

mediate scales (other arthropods). The effect

of the site and sampling period on the vari-

ability of the environment and the community

in terms of richness, diversity, and abundance

or density was established by creating gener-

alized linear models (GLMs) for each of the

variables. The independent variables (factors)

were the sampling site, the hydrological period,

the year, and the ENSO phenomenon; and the

dependent variables included all physical and

chemical variables, as well as the richness and

abundance or density of macroinvertebrates

and phycoperiphyton. For each parameter, the

models with the lowest AIC values (Akaike,

1974) were selected, in this case those of the

Gaussian family (log) for both environmental

and biological variables. Significances greater

than 95 % were considered for the FFM model

estimators for each parameter, corresponding

to the positive or negative effects of the fac-

tors on the dependent variables. GLM analyzes

were done using R-project software, version

3.6.3. (RStudio Team (2020). The environ-

mental and biological variables that showed a

significant response to the factors evaluated

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

using the GLM analyzes were included in the

canonical discriminant analysis (ADC). This

is an analysis that creates a function capable

of classifying factors (sites, years, or ENSO

phenomena), considering a series of discrimi-

nating variables (in this case, environmental

variables, and the taxonomic composition of

benthic organisms). The percentage of correct-

ly classified data was obtained through cross

validation. The spatial and temporal aggrega-

tion of the trophic guilds of macroinvertebrates

and algal divisions was visually explored by a

multidimensional scaling analysis (MDS) using

the Bray-Curtis similarity index as a measure

of distance. Both ADC and DMS analyzes

were done using RWizard software version 4.3

(Guisande et al. al., 2014).

The relationship between environmental

and biological variables, as well as the relative

effect of trophic resources (phycoperiphyton)

and environmental variables, were evaluated

using the factors shaping community assem-

blages (FCA) analysis that is based on the

instability of the environment (understood as

the variability in environmental parameters)

and the abundance and/or density of indi-

viduals of the biological group of interest, in

order to find the factors that most influence

the spatio/temporal changes of each of the

groups functionally or taxonomically consid-

ered (Manjarrés-Hernández et al., 2021). For

this, a principal component analysis (PCA) was

carried out by year and sampling site, using the

software past V 2.17 (Hammer et al., 2001) that

allowed a determination of the trophic guilds of

macroinvertebrates and the environmental vari-

ables that provide a greater contribution on the

variance, based on the Jolliffe criterion (1972,

1973). Taxa of 18 orders of macroinvertebrates

classified according to their trophic guild (cor-

responding to 73 % of the total abundance of

macroinvertebrates), and 4 phycoperiphyton

divisions (corresponding to 99 % of the densi-

ty) were conserved. With these results, the fluc-

tuation index of Dubois (1973) was estimated,

modified by Guisande et al. (2006) to calculate

the instability of the phycoperiphyton divisions,

of the trophic guilds of macroinvertebrates in

the environment.

Where s is the number of variables, pi the

relative proportion of variable i at a specific

time or space, pi the reference state, which is

calculated as the average of the relative propor-

tions for variable i during the study period or

considering the sampling sites. The FCA analy-

sis used artificial intelligence algorithms in

the R package randomForest (Liaw & Wiever,

2018) to determine the relationship between

environmental instability and the instability of

the phycoperiphytic community, as well as the

relationship between the selected groups of the

two benthic communities. 10 % of the data was

not included in the model for its validation.

Likewise, the FCA used the R relaimpo pack-

age (Grömping, 2006; Grömping, 2021) to find

the contribution of each one of the phycope-

riphyton taxa to the changes in the abundance

of macroinvertebrates and the contribution of

each one of the physicochemical variables to

the changes in the instability index of the phy-

coperiphyton divisions by means of hierarchi-

cal partitioning (Chevan & Sutherland, 1991).

The analysis was performed in the RWizard

version 4.3 software (Guisande, et al., 2014).

RESULTS

Environmental Variability: The GLM

analyzes made it possible to determine that at

a temporal level in 2012, 2013 and 2015 there

was a decrease (negative effect) in the concen-

trations of DO (average 6.96 -7.34mg/l) and

NO3- (average 0.15-1.59 mg/l). Likewise, on a

spatial scale a reduction in temperature (22.02

°C) and electrical conductivity (31.43 µS/cm)

was observed at the RSC1 site, with the pH

(7.42 pH Units) and TSS (31.05mg/l), the latter

values closely related to turbidity. In all these

cases the model was significant with P < 0.05

(Table 1 and Fig. 2). According to the FCA

hierarchical partitioning analysis that estimates

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

Fig 2. Spatial and temporal behavior of the biological and environmental variables that showed variability in the RG2

(Guatapé River) and RSC1 (San Carlos River) sites, between 2010 and 2018.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

the contribution of variables to environmental

instability both at a spatial and temporal level

(Fig. 3), turbidity and PO4-3 contributed 39.83

and 62.67 % to environmental instability, thus

accumulating more than 90 % of the contribu-

tion (R2 = 0.89).

Variability of the phycoperiphytic com-

munity: A total density of 3 973 809 ind/cm2

was recorded, distributed in 8 divisions, 13

classes, 37 orders, 65 families, and 122 taxa.

The divisions that contributed the most to the

total density were Bacillariophyta and Cyano-

bacteria with relative densities of 61 and 32

%; the genus Oscillatoria sp. registered the

highest relative density (17.73 %), followed

by Navicula sp. (15.03 %), Achnanthes sp.

(15.01 %), Lyngbya sp. (11.11 %), Synedra sp.

(6 %) and Gomphonema sp. (5 %). The RSC1

site showed significantly less diversity (nega-

tive effect) (P < 0.04). In 2013 and 2017, the

lowest Q0 diversity values were also observed,

with minimums of up to 8 taxa and an average

between 14 and 15 (Table 1). In 2013 the den-

sity increased (positive effect), with an average

of 251 439 ind/cm2 in RG2 and 20 678 ind/cm2

in RSC1. In conrast, in 2014 the lowest value

was recorded with an average of 2 359 ind/cm2

in RSC1 (Table 1).

Variability of the community of aquat-

ic macroinvertebrates: The total abundance

of macroinvertebrates was 9 465 individuals.

These were classified as 136 taxa, 64 families,

18 orders, 6 classes, and 4 phyla. In the RG2

site, ETP organisms represented 30 % of the

total abundance, non-arthropods 43.6 %, and

other arthropods 26.3 %. The most abundant

Table 1

Average, minimum, and maximum values, coefficient of variation and significance of the generalized linear model (MLG)

for the biological and environmental variables during the years of the ENSO periods, and sites studied: RG2 (Guatapé river),

RSC1 (San Carlos River)

Variable RG2 RSC1 P Values

Mean Range CV Mean Range CV Y P S P E

Temp. 22.6 21.7 25.2 0.049 22.6 20.6 24.1 0.049 – RSC1 0.00006 –

DO 7.36 5.94 8.24 0.11 7.37 5.24 8.53 0.104 2012

2013

2015

0.037 RSC1 0.00002 –

Cond. 36.76 33.1 60.70 0.23 36.61 21.24 51.10 0.23 – RSC1 0.00002 –

pH 7.28 6.56 8.50 0.06 7.28 6.40 8.63 0.06 – RSC1 0.012 –

NO31.03 0.16 1.94 1.03 1.02 0.03 2.03 0.53 2015 0.0000834 – –

Phyco.dens 92043.00 546.47 751954.08 20756.00 55135.08 841.02 598595.02 2.11 2013 0.0337 RSC1 0.00009 –

Q0 22.74 9 48 0.39 17.48 1 29 0.39 2017 0.0044 RSC1 0.0039 –

2013 0.0399

Q1 6.17 1 11.77 0.41 61.22 1 11.77 0.42 – RSC1 0.036 –

Q2 4.11 1 8.98 0.45 4.08 1 8.97 0.46 – RSC1 0.0123 –

Macro.Abun 175 0 742 0.9 178 28 575 0.88 2011 0.0011 – –

Q0 7 0 10 0.25 7 4 9 0.20 2011 0.00668 – –

Q1 6 0 9 0.24 6 3 8 0.19 2011 0.0117 RSC1 0.0129 –

Q2 5 0 8 0.24 5 3 7 0.19 2011 0.0273 RSC1 0.0024 –

2014 0.0398

2015 0.0182

2018 0.0249

*The models with the best fit and the lowest AIC criteria for the environmental variables and for the benthic communities

were of the Gaussian family (log). Abbreviations: Y = years, S = sites, E = ENSO. temp = water temperature, DO = dissolved

oxygen, Cond = electrical conductivity, pH, NO3 = nitrates, Fico.dens = ficoperiphyton density, Q0 = richness, Q1 =

equivalent diversity of common species, Q2 = dominant species, Macro.Abun = abundance of macroinvertebrates.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

genera were Melanoides (Neotaenioglossa) and

Leptonema (Trichoptera). At the RSC1 site,

the most representative groups were the ETP

with 60.5 % of total abundance and other

arthropods with 37.5 %. During the study,

the most abundant genera were Tricorythodes

(Ephemeroptera) and Rhagovelia (Hemiptera).

The scraper-filter feeders (CF-SC), collector-

shredders (CG-SH), and predators (PR) were

the ones with the highest contribution to the

total abundance (63 %). In the temporal scale,

abundance was relatively similar, although

it increased in 2013 and 2016 in RSC1 and

between 2010 and 2013 in RG2. The MGL

identified a significant negative effect on the

diversity of dominant species (Q2) in the years

2011, 2014, 2015 and 2018 (P < 0.002), espe-

cially in RSC1.

Patterns of environmental and biological

stability: The discriminant analysis obtained

more than 90.7 % of cases correctly identified

by cross validation, except when the sampling

years were analyzed, where only 50 % of the

cases were correctly identified. No patterns

of seasonal variation were found. Discrimina-

tion between sampling sites (100 % variance

explained by the first canonical axis) con-

firmed spatial environmental differences that

coincided with changes in macroinvertebrate

composition (Fig. 4). The RSC1 site was domi-

nated by ETP organisms and other arthropods

that were associated with high concentrations

of DO and TSS (total suspended solids). In

contrast, at the RG2 site non-arthropod organ-

isms stood out, associated with a higher tem-

perature and electrical conductivity. On the

time scale, only the year 2013 is discriminated

due to the increase in Cyanophytas and Bacil-

liariophytas, but with an explained variance of

less than 50 %. While for the ENSO periods,

the discriminant analysis explained 84 % of

variance in the first canonical axis, the La Niña

phenomenon was differentiated by the greater

presence of Charophyta and Chlorophyta, coin-

ciding with a high concentration of nutrients

(NO3- and PO4-3) and DO. The Bacillariophyta,

Cryptophyta, Cyanobacteria, Euglenozoa, Mio-

zoa, and Ochrophyta divisions as well as all

macroinvertebrate groups were associated with

drier El Niño periods and neutral periods asso-

ciated with increases in electrical conductivity

and temperature.

The EMD analysis also identified an

aggregation of benthic communities depending

on the sampling site (stress value of 0.068).

According to this analysis, spatial differences

prevailed in the density of algal divisions and

the abundance of macroinvertebrate trophic

guilds. At the RG2 site an aggregation pattern

of collector-filter and collector-scraper organ-

isms was observed, while at the RSC1 site the

guilds were more abundant, the same as the

phycoperiphyton (Fig. 5).

Fig. 3. Contribution of physicochemical variables to instability of the environment using the hierarchical partitioning

method, R2 = 0.89.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

According to the results of the princi-

pal component analysis, four phycoperiphy-

ton divisions, eight macroinvertebrate trophic

guilds, and a total of seven physicochemical

variables were included in the instability analy-

sis. Table 2 shows the greatest contributions of

environmental variables and phycoperiphyton

to the instability of the macroinvertebrate com-

munity. For both environmental and biological

variables, the model shows an R2 greater than

83 %. The trophic guilds that presented the

greatest response to environmental instability

Fig. 4. Discriminant analysis between sampling sites and times, based on environmental variables and composition of

benthic species. Abbreviations: Temp = water temperature, DO = dissolved oxygen, TSS = total suspended solids, Cond

= electrical conductivity, NO3 = nitrates, PO4 = orthophosphates, Bacill = Bacillariophyta, Charo = Charophyta, Chlo =

Chlorophyta, Crypto = Cryptophyta, Cyano = Cyanobacteria, Eugle = Euglenozoa, Mio = Miozoa, Ochro = Ochrophyta,

Dipt = Diptera, No Art. = no arthropods, Other Art. = other arthropods, ETP = Ephemeroptera, Trichoptera, Plecoptera.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

were scrapers (SC) and filter feeders (CF) that

on the spatial scale responded negatively to

oxygen and turbidity. On the time scale these

groups responded negatively to conductivity

and NO3- but to a much lesser extent. The

collector-shredders (CG-SH) responded only

in the spatial scale, positively to turbidity and

negatively to DO.

The contribution of algal divisions to the

instability of macroinvertebrates only affected

the guild of scrapers (SC), although significant-

ly higher than the environmental contribution

and at both a spatial and temporal level. The

divisions Charophyta and Chlorophyta showed

a higher and negative contribution to the insta-

bility of the scrapers, while Cyanobacteria

Table 2

Interaction between the instability of the physicochemical variables, the instability in the algal density, and the abundance

of macroinvertebrates in tributary rivers of the Punchiná reservoir (based on artificial intelligence algorithms from the FCA

analysis).

Contribution

Environmental Variables r2Resource (Divisions) r2

Stability Temporal Variables SC CF.SC 0.89 Variables SC 0.84

Temperature 67.5 -3.6 Bacillariophyta 252.990958

pH 112.3 90.9 Charophyta -396.76851

Conductivity -169 81.5 Chlorophyta -642.055658

Turbidity 112.5 108.3 Cyanobacteria 885.83321

Nitrates 48.3 -162.7

spatial Variables CG.SH CF.SC 0.88 Variables SC 0.83

OD -2 171.3 -1 702.8 Bacillariophyta 1 309.26547

pH 859.676 1 309.258 Charophyta -663.071129

Turbidity 3 032.89 -1 189.85 Chlorophyta -2 382.15325

Cyanobacteria 1 835.9589

Abbreviations: SC = Scrapers, CG.SH = Gatherers-Shredders, CF.SC = Filterers-Scrapers, CG-SH = Gatherer-Shredders.

Fig. 5. Multidimensional scaling representing the aggregation of biological data, according to the sampling site, based on

the composition of benthic communities.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

make a high positive contribution to this insta-

bility, both at the spatial and temporal levels.

The effect of Bacillariophyta is low at the

temporal level and moderate at the spatial level

(Table 2).

DISCUSSION

The physicochemical parameters showed,

for the most part, relative stability as expected

from environmental variability in regulated

systems. The pH showed adequate values for

the establishment of most aquatic species (6-8

pH units) (Arango et al., 2008). The tempera-

ture was characteristic of the tropics (annual

average higher than 18 °C and a maximum of

28 °C) (López et al., 2012). According to the

DO concentration (> 5 mg/l) and the chemical

oxygen demand (< 27 mg/l), both sites offered

adequate conditions for aquatic life (Gualdrón-

Durán, 2018; Roldán-Pérez & Ramírez, 2022)

consistent with the high slope that favors

oxygenation (Rivera, 2004). Likewise, inor-

ganic nutrients were found in relatively low

concentrations that do not show conditions

of enrichment.

No effect of hydrological seasonality was

detected, probably a consequence of regula-

tion; however, moderate temporal variations

were observed to be associated with the ENSO

phenomenon. This is the case of a decrease

in the concentration of DO in the years 2012,

2013, and 2015 corresponding to the El Niño

phenomenon at both sampling sites. The rela-

tionship between the concentration of nitrates

with the runoff and the hydrological cycle man-

ifested itself with an increase during the rainy

periods of 2015. For the structure of the benthic

communities, the algal community divisions

Cyanobacteria and Bacillariophyta were the

ones that most contributed to the total density.

According to Casco and Toja (2003) and Passy

(2007) the high densities of these divisions are

related to their specialized growth forms that

adhere to the substrates and that include differ-

ent habits such as prostrate, erect, filamentous,

chain-forming, or tubes and colonial, according

to the availability of resources and disturbances

such as flow oscillations (Passy, 2007; Ríos-

Pulgarín et al., 2016). The most representa-

tive macroinvertebrates were Ephemeroptera,

Trichoptera and Gastropoda, in relation to the

supply of resources and habitat in each river.

At the spatial level, in the RSC1 site the

lower values of diversity and density of phyco-

periphyton reflect low environmental stability,

favoring the growth of some genera such as

Oscillatoria sp, Navicula sp., Cylindrocystis

sp., Achnanthes sp., and Lyngbya sp. with

adaptations to flow fluctuations and the avail-

ability of low-quality substrates. The composi-

tion and abundance of macroinvertebrates also

showed spatial differences. The RSC1 site was

characterized by a greater abundance of the

orders Ephemeroptera, Trichoptera, Plecoptera

and others of Arthropoda, favored by physi-

cochemical and habitat characteristics such

as the presence of substrates like trunks, sub-

merged vegetation, shallower depth, and speed

of the current (Ríos-Pulgarín et al., 2020). In

contrast, in the RG2 site non-arthropod organ-

isms predominated, especially molluscs of the

orders Hygrophila and Neotaenioglossa that

are favored by the presence of submerged

vegetation and a high organic load (Baqueiro-

Cárdenas et al., 2007; Vogler et al., 2012). The

discriminant analysis corroborated the differ-

ences between sampling sites and associated

with the predominance of ETP macroinver-

tebrates and other arthropods in RSC1 with

high concentrations of OD and TSS. The abun-

dance especially of mollusks in RG2 coincided

with conditions of higher temperature and

electrical conductivity.

The effects of environmental regulation

determined the response on the temporal scale;

inorganic nutrients showed high concentra-

tions during the La Niña period as a result

of increased transport and fragmentation of

particulate organic matter upstream of the sam-

pling site (Reddy et al. al., 1999). The green

algae of the Chlorophyta and Charofita divi-

sions were related to the La Niña phenomenon,

because they are favored by the increase in

the concentration of nutrients (Eikland, et al.,

2017., Sarmiento Morales, 2017). During the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

dry conditions of El Niño, in contrast, cyano-

bacteria (Cyanophyta) predominated, charac-

terized by their ability to secrete mucilages that

provide them with enough moisture to protect

their reproductive structures (Casco & Toja,

2003) and diatoms (Bacillariophyta) that they

are favored by stable conditions in the and

an increase in temperature (Rivera Rondón &

Donato, 2008). This condition favors the prolif-

eration of certain groups of diatoms when there

are sufficient nutrients available (Casco & Toja,

2003). On the other hand, the nutrients did not

have significant effects on the algal densities

since their concentrations were relatively stable.

The effect of hydrological seasonality on ben-

thic communities was only observable during

the extreme conditions of the La Niña/ENSO

phenomenon. The low incidence of hydrologi-

cal disturbance favored diverse communities.

Under conditions of relative environmental

stability, biological interactions in the com-

munity structure gained importance. Biggs &

Smith (2002), Díaz-Quirós & Rivera-Rondón

(2004) and, Martínez & Donato (2003) have

suggested that long-term periods of hydrologi-

cal stability are necessary for the development

of a phycoperiphytic community with greater

species richness maintaining assemblages in

early stages of succession since hydrological

disturbance periodically removes taxa that do

not have adaptations to trawling (Ríos-Pulgarín

et al., 2016). The increase in the speed of the

water during the La Niña period generates

drag; therefore, most of the benthic organisms

thrive in the dry period of El Niño (Cantonati &

Spitale 2009; Carmona-Jiménez et al., 2016).

These organisms determined the differences in

the values of density or abundance during peri-

ods when environmental control predominates.

In the absence of such controls, the FCA results

suggested a significant effect of phycoperiphy-

ton on the macroinvertebrate community.

According to Fenoglio et al., (2020), the

most obvious trophic relationship between ben-

thic communities is grazing, carried out by

herbivorous invertebrates from biofilms on

substrates. So, in addition to habitat condi-

tions and physical and chemical factors, the

density of periphytic algae depends on the

diet of scraping macroinvertebrates that are

frequently found in the ETP group (Tierno de

Figueroa, 2019). Among these, the families

Baetidae, Leptohyphidae, and Leptophlebiidae

(Ephemeroptera), Perlidae (Plecoptera) stand

out, as well as the families Hydroptilidae,

Glossosomatidae and Xiphocentronidae (Tri-

choptera) that according to Springer (2010),

have genera that are phycoperiphyton scrapers.

In the case of the order Plecoptera, their diet is

based mainly on diatoms, species that are eas-

ily digested by macroinvertebrates, due to the

absence of lignin, even though their levels of

proteins, lipids, and carbohydrates are relatively

low (Bojorge-García & Cantoral-Uriza, 2016;

Diaz-Villanueva, 2001). For the order Trichop-

tera scraping algae is one of the most common

sources of food acquisition, with chewing-type

mouthparts, sucking algae cell contents (Wig-

gins, 2004). Organisms of the order Ephemer-

optera are also scraper or collector herbivores

and feed on algae and tissues of aquatic plants

(Flowers & De la Rosa, 2010). Another group

that has effects on the richness and density of

phycoperiphyton are the molluscs of the order

Gastropoda and the species Melanoides tuber-

culate (Coat et al., 2009; Putz, 1997) that was

particularly abundant in the study. Given that

the relationship between these two communi-

ties is positive, we can assume that the control

of the trophic web in these systems occurs from

the producers (bottom up).

The higher density of phycoperiphyton in

RSC1, coinciding with the lower abundance

of collector-scraper or collector-filter mac-

roinvertebrates and a greater abundance of

predators, is consistent with a lower incidence

of herbivory at this site, as demonstrated by

Savic et al., (2018). This negative dependence

on grazing has been documented using biomass

as a response, but an indirect and positive effect

of predation that decreases herbivores has also

been found (Hillebrand, 2009, Holomuzki et

al., 2010, Rakowski & Cardinale, 2016) and

favors the increase of phycoperiphyton. In

this sense, when analyzing the stability of

the different communities, a possible effect

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

of selective grazing of macroinvertebrates on

phycoperiphyton is evident, since Charophyta

and Chlorophyta decrease because of graz-

ing, while cyanobacteria are less affected due

to their mucilaginous cover, production of

toxins, and/or lower nutritional value. For its

part, Bacillariophyta, thanks to high reproduc-

tion rates, are abundant and constant, so they

do not show significant variations in supply.

Dunk et al., (2018) have documented the func-

tional responses of phycoperiphyton to grazing.

According to these authors, the prevalence of

algae with prostrate habits is since they tolerate

herbivory better than filamentous or erect ones

that are easily removed from the upper layer

of the biofilm. However, some species of the

scraper orders Gastropoda and Ephemeroptera

could remove prostrate algae (Holomuzki et

al., 2010). Although this dependency gains

importance due to environmental stability, the

results suggest that those variables that showed

instability may exercise indirect environmental

control over trophic guilds. This is the case of

temperature that favors collectors and scrapers

due to the increase in the supply of substrates.

Turbidity, that negatively affects predators due

to its dependence on vision, favors scrapers,

shredders, and filter-feeding herbivores. So,

the effects of grazing can vary according to the

prevailing environmental conditions. Peters et

al., (2007) suggest that aspects such as spatial

heterogeneity associated with substrates, nutri-

ent concentration, or hydrodynamic conditions

restrict the trophic guilds that are established.

This contributes to the incidence of herbivory

in the RG2 site associated with the predomi-

nance of mollusks that are favored by higher

concentrations of organic matter.

In summary, under conditions of environ-

mental stability, the increase in the densities of

phycoperiphyton would increase the scraping

macroinvertebrates that use them as a food.

Given the reduction in hydrological seasonality

associated with regulation, at RG2 and RSC1

herbivory acted as a determining factor of the

phycoperiphyton structure, and the effect of

environmental variables was only detected dur-

ing extreme conditions such as the ENSO, with

temperature and turbidity as the main factors

that presented greater instability and incidence

on the trophic guilds. This produces a smaller

effect of environmental instability than of insta-

bility of the supply of phycoperiphyton on the

macroinvertebrate community.

Sampling sites showed little temporal vari-

ability in environmental conditions due to

regulation. Under these conditions, phycope-

riphyton was regulated mainly by herbivorous

macroinvertebrates (scrapers), especially ETP

arthropods and some Gastropoda mollusks.

This trophic relationship was even more rele-

vant than the physicochemical conditions of the

environment in the structuring of the benthic

communities, confirming the initial hypothesis

and showing that in these systems the control of

the trophic web occurs from the producers (bot-

tom up), whose densities condition the abun-

dance and composition of macroinvertebrates.

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 acknowledgments

section. A signed document has been filed in

the journal archives.

ACKNOWLEDGMENTS

The authors thank the Limnology and

Water Resources Research Group of the Uni-

versidad Católica de Oriente and the power

generating company ISAGEN for managing

the inter-institutional agreement that made

reliable historical data available. Thanks to the

technical team of the project “Study of the his-

torical behavior of the Punchiná-San Lorenzo-

Calderas system and the changes that have been

generated in the hydrobiological communities

and the physicochemical variables between

2010 and 2018 for their collaboration during

the sampling and analysis in the laboratory and

to the reviewers for their contributions that will

improve the quality of this manuscript.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e51800, enero-diciembre 2023 (Publicado Jul. 25, 2023)

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