Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

Distribution of diversity of fishes in an Andean fluvial network

Daniel Valencia-Rodríguez1, 2*; https://orcid.org/0000-0002-8999-1757

Juliana Herrera-Pérez1, 3; https://orcid.org/0000-0002-6946-8950

David Botero-Escalante1; https://orcid.org/0000-0002-7674-1556

Luis García-Melo4; https://orcid.org/0000-0001-9691-0540

Diana Arenas-Serna1; https://orcid.org/0000-0002-8390-945X

Frank Álvarez-Bustamante1; https://orcid.org/0000-0002-0713-6774

Emerson Parra-R1; https://orcid.org/0000-0001-8685-7870

Luz Fernanda Jiménez-Segura1; https://orcid.org/0000-0003-0784-0355

1. Laboratorio de Ictiología, Departamento de Biología, Universidad de Antioquia, Medellín, Colombia;

jdbe8209@gmail.com, dianarenas1714@gmail.com, frankester3671@gmail.com, emerson221@gmail.com,

luz.jimenez@udea.edu.co

2. Laboratorio de Bioclimatología, Red de Biología Evolutiva, Instituto de Ecología A.C., Xalapa, Veracruz, México;

daniel.valencia@posgrado.ecologia.edu.mx (*Correspondence)

3. Laboratorio de Macroecología Evolutiva, Red de Biología Evolutiva, Instituto de Ecología, A.C., Xalapa, Veracruz,

México; juliana.herrera@posgrado.ecologia.edu.mx

4. Empresas Públicas de Medellín. Carrera 58 No. 42 - 125, Medellín, Colombia; luchojgm@gmail.com

Received 17-VIII-2022. Corrected 09-XII-2022. Accepted 29-III-2023.

ABSTRACT

Introduction: The distribution of freshwater fishes in the Colombian Andes results from the interaction between

historical and recent factors. Currently, the Andean landscape is facing rapid transformation processes. However,

the knowledge regarding species distribution and environmental requirements is advancing slower than the

transformations underway in the fluvial networks.

Objective: To understand the conformation of the fish assemblage in the middle and lower Cauca River basin,

considering the local environmental context before the construction of the Ituango Dam, and quantifying β

diversity and its two components (turnover and nestedness) amongst local fish communities.

Methods: 58 localities were monitored during nine years (between February 2010 and November 2018), the

period before the dam’s operation. The species richness (α-diversity), species turnover (β-diversity), and assem-

blage composition were estimated for the given localities.

Results: 114 species were recorded, representing ~ 49 % of the total richness of known species for the

Magdalena basin. The richness distribution showed that the number of species varies among the aquatic environ-

ments. Swamps presented the most significant number of species, followed by the Cauca River, while streams

had the lowest values of richness. The spatial analyses of β-diversity revealed a high variation component in the

study area due to species replacement between the aquatic environments.

Conclusions: The implementation of long-term monitoring allowed us to recognize that the Cauca River basin

conserves a great variety of species-rich environments. The species turnover indicates a high proportion of

endemism or multiple sites with unique species. Finally, our study will serve as a baseline to verify, over time,

whether the dam’s construction is associated with essential changes in the structure of fish communities.

Key words: assemblages; beta diversity; communities; conservation; Magdalena Basin.

https://doi.org/10.15517/rev.biol.trop..v71i1.52183

AQUATIC ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

INTRODUCTION

Fishes are the most biodiverse organisms

among vertebrates, with approximately 36 018

currently recognized species, among which 18

185 are freshwater fishes (Fricke et al., 2022).

Despite the relevance of this group in ecologi-

cal, economic, and social terms (Hermoso et

al., 2018), freshwater fishes face the highest

number of threats and are less known than other

vertebrates (Darwall et al., 2011; Miqueleiz et

al., 2020). Freshwater ecosystems are among

the most threatened ecosystems worldwide;

they are disappearing faster than terrestrial

ecosystems (Reid et al., 2019).

On the other hand, the Neotropical region

is one of the regions with the highest fish diver-

sity on Earth. Currently, nearly 6 200 freshwater

fish species have been described (Albert et al.,

2020), making this region an area with a unique

biological heritage. The Magdalena basin, with

235 fish species, is in the Northwestern tropi-

cal region of South America (DoNascimiento et

al., 2021). Although the diversity in the Magda-

lena basin is less than that of the Amazon and

Orinoco basins, this basin is considered one

of the regions on the planet with the highest

percentage of endemism (68 %), with a total

of 158 species (García-Alzate et al., 2020). In

addition, fish species of the Magdalena basin

provide multiple ecosystem services, such as

food for people and another biota. Also, these

species influence the local economy, culture,

and recreation and contribute to ecosystem

maintenance (Valderrama-Barco et al., 2020).

The composition and structure of the com-

munities have been associated with the eleva-

tion gradients and changes in environmental

factors along the cline. At a local scale, the

pattern observed in the Magdalena basin is a

decrease in species richness and an increase of

endemism with the increase in elevation (Car-

vajal-Quintero et al., 2015; Herrera-Pérez et al.,

2019) and the composition of fish communities

have been the result of these same conditions

Nomenclatura: AT1: Anexo Tabla 1; AT2: Anexo Tabla 2; AF1: Anexo Figura 1.

RESUMEN

Distribución de la diversidad de peces en una red fluvial andina.

Introducción: La distribución de los peces de agua dulce en los Andes colombianos es el resultado de la inte-

racción entre factores históricos y recientes. Actualmente, el paisaje Andino enfrenta procesos de rápida trans-

formación. Sin embargo, el conocimiento sobre la distribución de las especies y sus requerimientos ambientales

no avanza tan rápido como las transformaciones en curso en las redes fluviales.

Objetivo: Comprender la conformación del ensamble de peces en la cuenca media y baja del río Cauca, consi-

derando el contexto ambiental local antes de la construcción de la represa de Ituango, y cuantificar la diversidad

beta y sus dos componentes (recambio y anidamiento) entre las comunidades de peces locales.

Métodos: Se analizaron 58 localidades durante nueve años (entre febrero 2010 y noviembre 2018), período

previo a la operación de la represa. La riqueza de especies (diversidad α), el recambio de especies (diversidad β)

y la composición del conjunto se estimaron para las localidades dadas.

Resultados: Se registraron 114 especies, que representan ~ 49 % de la riqueza total de especies conocidas para la

cuenca del Magdalena. La distribución de la riqueza mostró que el número de especies varía entre los ambientes

acuáticos. Las ciénagas presentaron el mayor número de especies, seguidas por el río Cauca, mientras que las

quebradas presentaron los valores más bajos de riqueza. Los análisis espaciales de la diversidad β revelaron un

alto componente de variación en el área de estudio debido al reemplazo de especies entre los ambientes acuáticos.

Conclusiones: La implementación del monitoreo a largo plazo permitió reconocer que la cuenca del río Cauca

conserva una gran variedad de ambientes ricos en especies. El recambio de especies indica una alta proporción

de endemismo o múltiples sitios con especies únicas. Finalmente, nuestro estudio servirá como línea base para

verificar, con el tiempo, si la construcción de la represa está asociada con cambios esenciales en la estructura de

las comunidades de peces.

Palabras clave: ensamblajes; diversidad beta; comunidades; conservación; Cuenca Magdalena.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

(Albert et al., 2011). In mountain rivers, higher

elevation areas have a high variation in riverbed

slopes, higher water velocities, turbulence, and

more oxygenated waters. In lower elevations,

water systems are less turbulent and oxy-

genated (Jacobsen, 2008). Therefore, different

aquatic environments within a fluvial network

could play a crucial role in how communities

structure through dispersion and environmental

selection processes (Altermatt, 2013). More-

over, the Northwestern of the Andes is the

output of a long geological history of isolation

due to the differential uplift of physical barri-

ers over time, in which individuals of each fish

species survive new biotic and abiotic environ-

mental conditions (Lévêque et al., 2008).

The loss of biodiversity in freshwater eco-

systems reveals a rapid decrease in populations

and a great risk of extinction in freshwater

organisms (Reid et al., 2019). The Magdalena

basin is no exception, as aquatic ecosystems

are among the most affected by human activity

in Colombia (Angarita et al., 2018; Jiménez-

Segura et al., 2016; Rodríguez, 2015). Threats

such as fisheries pressure and non-native fish

species have already been reported (Hernández

Barrero et al., 2021; Lasso et al., 2020). Cattle

farms and agriculture on the floodplains have

reduced the area of the floodplain lakes and

their connection with the river. Water pollu-

tion due to poor sewage treatment in the cities,

sediment retention, and hydrological change

because reservoirs alter the river structure

and dynamics (Angarita et al., 2020). The

Magdalena River basin produces 60 % of the

hydropower in Colombia; the dams block 50 %

of the fluvial net in this basin, and the energy

production changes the flood pulse (Angarita et

al., 2018). As a result of the interaction of these

threats, ~ 48 % of fish species are included

within some of the IUCN threaten categories

(Mojica et al., 2012; Tognelli et al., 2019), and

artisanal fisheries landings have plummeted

(Hernández Barrero et al., 2021).

Monitoring is a valuable strategy to detect

changes in critical variables over time (Conly

& Van Der Kamp, 2001; Roero et al., 2016);

biota monitoring is one of the practical actions

to detect any change in their composition,

richness, and assemblage structure (Loures

& Pompeu, 2018; Valencia-Rodríguez et al.,

2022a) and let us look for their causes. Here,

we explore the spatial relationship between fish

assemblages and the different aquatic environ-

ments in the middle and lower Cauca River

basin (the main tributary to the Magdalena

River) prior to the construction of the Ituango

Dam. For the analyses, we used the monitoring

data conducted over nine years to explore the

composition of the ichthyofauna in the Cauca

River. This analysis focuses on species rich-

ness and changes in fish assemblage between

aquatic environments. In this study, we seek to

(i) strengthen the knowledge of how the fish

assemblage is conformed in the middle and

lower Cauca River basin, considering the local

environmental context prior to the construc-

tion of the Ituango Dam and (ii) quantify β

diversity and its two components (turnover and

nestedness) amongst local fish communities.

Answers to these questions make it possible

to understand the fish community’s structure

before dam construction. The results will help

measure the magnitude of change caused by

the dam based on the long-term data collected.

This not only allows for progress in the diver-

sity inventories but also provides opportunities

for conservation.

MATERIALS AND METHODS

Study area: The Cauca River is in the

Northwestern tropical region of South America.

It begins at 3 600 m above sea level (m.a.s.l.) in

the Colombian mountains, between Cauca and

Huila departments, running 1 350 km north-

ward and flowing into the Magdalena River

at 50 m.a.s.l. The Cauca River has an aver-

age flow rate of 1 800 m3.s-1, with temporary

variations due to climatic changes, with two

rainy seasons (May-June, October-November)

and two dry seasons (January-March, July-

September) within the annual cycle. Before

flowing into the Magdalena River, the Cauca

River basin drains through lands transformed

by agriculture, cattle farming, informal mining,

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

and the expansion of urban and suburban areas

(Jiménez-Segura et al., 2016).

In 2009, the Ituango Hydroelectric proj-

ect’s construction license in the Cauca River’s

middle section was approved by the Environ-

mental Authority in Colombia. This is the most

significant power generation project underway

in Colombia, as it will generate 2 400 MW of

energy, supplying 17 % of the overall hydro-

power installed capacity in Colombia. This

study covers the middle and lower Cauca

River basin (Fig. 1; AT1); the basin limits were

according to (Pérez-Valbuena et al., 2015). A

total of 58 sites were analyzed; the field visits

were conducted between February 2010 and

November 2018, the period before the dam’s

operation. Throughout these years, each site

was sampled four times per year, twice dur-

ing the dry season and twice during the rainy

season, except for the years 2010 and 2015, in

which it was only possible to make two visits,

one in the dry season and the other in the rainy

season during the first half of the year.

Due to the selectivity of the sampling

method for each species and the size of the fish,

the same sampling effort was used for each

site over time, depending on the environment

sampled. In continuous flow channels (Cauca

Fig. 1. Sampling design for ichthyofauna monitoring. MCR: middle Cauca River basin, MBC: middle basin creeks, MBS:

streams flowing into the middle Cauca River basin, LCR: lower Cauca River basin, LBS: streams flowing into the lower

Cauca River basin, and SWP: swamps.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

River, tributaries, and creeks), the sampling

effort was 30 throws using three cast nets (dif-

ferent mesh sizes 1, 3, and 5 cm). In addition,

to increase the probability of catching fish of

different species and sizes, area sweeps were

conducted using a portable electrofishing unit

with one amp pulsed current (340 V, 1–2 A,

dc) for 60 minutes in a 100 m-long transect

over the main channel of the water body. In

the swamps, the sampling effort involved two

gill nets (each measuring 100 m long and 3 m

high), one in the littoral zone and the other in

the central zone. The time of exposure to gill

nets was six hours (the maximum time allowed

by the local human communities), from 17:00

to 23:00. Nets had ten different mesh sizes,

ranging from 1 to 10 cm.

Fish data: Captured fish were anesthe-

tized using eugenol solution to reduce stress

during handling (Javahery et al., 2012). For

complex taxonomic groups, a sample of 20

specimens was taken to the laboratory, which

were included in the Ichthyology Collection

at the Biology Institute of the Universidad de

Antioquia in Medellín. The list of recorded spe-

cies and the number of specimens collected are

available in the supplementary files (AT2). The

taxonomic classification is according to Fricke

et al. (2022) and the most recent version of

the Colombia checklist (DoNascimiento et al.,

2021). The taxonomic determination followed

several taxonomic studies for specific groups

(Armbruster, 2005; Dahl, 1971; Harold & Vari,

1994; Hernández et al., 2015; Londoño-Burba-

no et al., 2011; Lujan et al., 2015; Ortega-Lara,

2012; Román-Valencia et al., 2013; Rosen &

Bailey, 1963; Skelton, 2001).

Data analysis: To verify the quality of the

information for each sampling site separately,

a completeness analysis was performed (AT3).

After verifying the quality of the informa-

tion, the sampling sites were grouped into six

aquatic environments. To select the samples

sites according to the type of environment,

a topological net proposed by López-Casas

et al. (2018) was used for the Magdalena

basin, which is based on a digital elevation

model (SRTM, 90 m) and follows Strahler’s

river order classification (Strahler, 1957). Each

sampling site was plotted on the topological

network, and the associated information was

extracted. Thus, creeks were assigned orders

1 and 2, tributary rivers were 3-5, and the

Cauca River was assigned an order of 6, while

swamps were assigned an order of 0 as they

are lotic water bodies. After this classification,

they were divided according to their geographi-

cal location in the middle or lower basin, as

follows: MBC – middle basin creeks, MBS –

streams flowing into the middle Cauca River

basin, MCR – middle Cauca River basin, LBS

– streams flowing into the lower Cauca River

basin, LCR – lower Cauca River basin, and

SWP – swamps (Fig. 1; AT1).

To estimate the number of species per

aquatic environment (alpha diversity), we used

the first three numbers of the Hill series (q0,

q1, and q2) (Hill, 1973), following the method

proposed by Jost (2006) and Chao et al.,

(2014), implemented in the iNEXT package

(Hsieh et al., 2016). Where q0 is the effec-

tive richness, q1 is equivalent to the Shannon

diversity exponent (i.e., common species), and

q2 is equivalent to the inverse of the Simpson

index (i.e., dominant species) (Jost, 2006).

Estimated richness about observed richness

allows for the estimation of the proportion of

species recorded by the sampling, which var-

ies between zero and one, where values near

one suggest good representativeness in the

number of species analyzed for the estimation

diversity (Hsieh et al., 2016). We understand

that each sampling method entails its own bias.

We assume such bias occurs in the same way

throughout all environments since all methods

were used equally depending on the sampled

environment. Thus, we used these estimations

for relative comparisons among environments.

The difference in richness among aquatic

environments was evaluated using the Kruskal-

Wallis test; when a significant difference was

detected (level of significance α = 0.05), post

hoc comparisons were conducted in pairs, using

the Wilcoxson sum rank test, with adjusted P

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

value according to Holm’s procedure (Holm,

1979). Holm’s procedure is considered a more

powerful correction (in other words, it is more

likely to detect an effect if there is one) than

Bonferroni’s for multiple comparisons, provid-

ing improved protection against a Type 1 error

(Wright, 1992).

To explore the differences in fish assem-

blages, we used multivariate, non-parametric

methods. Resemblance matrices were gener-

ated using the Jaccard similarity index (pres-

ence/absence) that were compiled into a matrix

of distances of fish species. Differences in

the spatial distribution of similarities among

environments were assessed with a permuta-

tional multivariate ANOVA (PERMANOVA)

using the adonis function in the vegan package

(Oksanen et al., 2015). To evaluate the dif-

ferences between the assemblies of fish, we

calculated the p-values corrected by Bonferroni

with the pairwise.adonis function in the pair-

wise Adonis package in R (Martinez Arbizu,

2020). The results were displayed on a non-

metric multidimensional scale graph (nMDS),

considering the stress of 0.20 as an acceptable

goodness of fit (Vinet & Zhedanov, 2010).

Similarity-profile analysis was performed, and

the results were overlaid on the nMDS plot to

demonstrate the structure among samples.

To evaluate fish beta (β) diversity in

the middle and lower Cauca River basin and

determine how much spatial variation was

due to richness differences and how much was

due to species replacement, we calculated the

Sørensen dissimilarity index (βsor) and its

components: turnover (βsim) and nestedness

(βnes; Equation 1) using the method proposed

by Baselga and Araújo (2010). This index is

based on presence-absence matrices and deter-

mines which of the components (βsim or βnes)

underlies variations in β diversity through the

following equation:

Where βsor is the Sørensen dissimilar-

ity and is made up of the Simpson similarity

(βsim), which consists of the substitution of

species in one site for different species in

another site (species replacement), describing

a spatial turnover that is not influenced by dif-

ferences in the species richness of each com-

munity, and βnes, which is the nestedness that

occurs when sites with less species richness

are a subgroup of the species at the sites with

higher species richness (Baselga et al., 2022;

Leprieur et al., 2011). All statistical analyses

and graphs were performed in software R (R

version 3.6.3) (R Core Team, 2020).

RESULTS

The sampling integrity and representative-

ness values were similar among environments

and exceeded 99 % (Table 1). The richness and

the effective number of species of order q=

0 was greater in swamps, lower Cauca River

Table 1

Fish diversity indicators according to sampling sites.

Indicators MCR MBS MBC LCR LBS SWP

Specimens 8 973 2 658 4 558 16 029 643 77 032

Species (S) 79 58 63 81 30 92

Extrapolated S 90.1 68.1 68.8 93.5 34.9 96.2

Common S 11.9 20.4 20.1 19.2 9.4 16.9

Dominant S 4.9 10.8 11.9 11.7 6.4 8.9

Unique S 320117

Sample coverage 1 0.99 1 1 0.99 1

*MCR: middle Cauca River basin, MBC: middle basin creeks, MBS: streams flowing into the middle Cauca River basin,

LCR: lower Cauca River basin, LBS: streams flowing into the lower Cauca River basin, and SWP: swamps.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e52183, enero-diciembre 2023 (Publicado Abr. 21, 2023)

basin, and middle Cauca River basin, and lower

in tributaries flowing into the lower Cauca River

basin (Table 1). The effective numbers of com-

mon species (order, q = 1) and dominant spe-

cies (order, q= 2) were similar in middle basin

creeks, streams flowing into the middle Cauca

River basin, and lower Cauca River basin. From

2010 to 2018, a total of 109 893 fish specimens

were collected in the 58 sampling sites, repre-

senting 11 orders, 33 families, and 114 species.

The region with the most significant number of

samples was swamping (77 032), lower Cauca

River basin (16 029), and middle Cauca River

basin (8 973) (Table 1). The Siluriformes (43

%) and Characiformes (38 %) orders repre-

sented 81 % of the total species sample, and

Gymnotiformes and Cyprinodontiformes rep-

resented 7 and 8 %, respectively. Characidae

was the family with the most species (18 %),

followed by Loricariidae (16 %).

The most abundant species was Cypho-

charax magdalenae (N= 21 465; 20 %), fol-

lowed by Triportheus magdalenae (N= 8 684;

8 %) and Astyanax magdalenae (N= 8 032;

7 %). The least abundant species and those

for which only one capture was recorded

were Apteronotus magdalenensis, Apteronotus

rostratus, Cetopsorhamdia boquillae, Chara-

cidium phoxocephalum, Cordylancistrus pijao,

Dupouyichthys sapito, Lasiancistrus cauca-

nus, Oreochromis mossambicus, and Saccodon

dariensis (AT2).

The distribution of total richness of the

species shows that the number of species was

different amongst the environments (X2 = 38.4,

P < 0.001; Fig. 2), where the swamps present

the greatest number of species (SWP), with an

average of 58.6 ± 5.5 of the total species in the

study area, followed by the lower and middle

Cauca River basins (LCR and MCR) with an

average of 47 ± 7.6, and 35 ± 7 of species

detected respectively. On the other hand, we

identified that the aquatic environments (MBC

and MBS) show similarities in the species rich-

ness values, with approximately 25 ± 5.7 of the

total species. Regarding streams flowing into

the lower Cauca River (LBS), we observed the

lowest richness values (15.2 ± 6, mean ± SD).

Thus, species richness is higher in the aquatic

environments in the lower basin and decreases

as the elevation increases towards the middle

basin (Fig. 2).

The nMDS and PERMANOVA analyses

showed the spatial structure of the assemblage

among the different aquatic environments. Fish

assemblages in the swamp (SWP) and the main

river channel of the Cauca River are discrete

units (Fig. 3); the last one has differences in

its middle and lower sections. In addition, fish

assemblage in rivers and creeks flowing to the

main river channel of the Cauca River could be

considered a single environment unit (namely,

tributaries) for fish (Fig. 3).

For average β diversity, we obtained a

value for βsor of 0.94, a value for βsne of 0.06,

and the β diversity component due to replace-

ment (βsim) was 0.88 (AF1). Our results sug-

gest that there is a high variation component

in the study area due to species replacement

(βsim) between the aquatic environments. In

Fig. 2. Species richness according to environment. The

shape of the violin diagram shows the data distribution,

where the widest sections represent a greater number of

species and narrower sections indicate a smaller number of

species observed. P value from the Kruskal-Wallis test is

shown for richness amongst environments. Environments

were identified from the middle basin toward the lower

basin, as follows: (MCR) middle Cauca River basin,

(MBC) middle basin creeks, (MBS) streams flowing into

the middle Cauca River basin, (LCR) lower Cauca River

basin, (LBS) streams flowing into the lower Cauca River

basin, and (SWP) swamps.