Histopathology and genotoxicity alterations in high Andean catfishes from the Upper Orinoco River Basin, Colombia

Alterações histopatológicas e de genotoxicidade em bagres alto-andinos da Alta Bacia do Rio Orinoco, Colômbia

Abstract

Freshwater ecosystem pollution has motivated an extensive list of studies due to deleterious impacts becoming a threat to aquatic organisms that inhabit these environments. This is the first approach to water pollution impact derived from human activities on native ichthyofauna in the Garagoa river basin in Boyacá (Colombian Andes). Therefore, the aim of the present study was to evaluate the occurrence of mercury and arsenic in catfishes and armored catfishes from the Garagoa River basin and the presence of hepatic alterations and genotoxicity in peripheral blood. Biomarkers of effect were analyzed in fishes caught in eight tributaries from Garagoa river basin. The increased presence of lesions in the hepatic architecture and nuclear abnormalities in peripheral blood erythrocytes in Dolichancistrus fuesslii, Chaetostoma joropo, Astroblepus latidens and Trichomycterus cf. knerii individuals could be associated with exposure of pollutants. The tissue alterations observed compromise the fish health, due to the biotransformation processes of xenobiotics such as mercury and arsenic and probably other contaminants. We need to increase surveillance in the Garagoa River to ensure ecological health, recognize hematological and tissue effects in native fishes, and develop effective monitoring strategies to mitigate sources of pollution.

Keywords:
arsenic; Garagoa river basin; genotoxicity; histology alterations; mercury

Resumo

A poluição dos ecossistemas de água doce tem motivado uma extensa lista de estudos devido aos impactos deletérios, tornando-se uma ameaça para os organismos aquáticos que habitam esses ambientes. Essa é a primeira abordagem ao impacto da poluição da água derivada das atividades humanas na ictiofauna nativa na bacia do rio Garagoa, em Boyacá (Andes da Colômbia). Portanto, o objetivo do presente estudo foi avaliar a ocorrência de mercúrio e arsênico em bagres e cascudos na bacia do rio Garagoa e a presença de alterações hepáticas e genotoxicidade no sangue periférico. Foram analisados biomarcadores de efeito em peixes capturados em seis sistemas aquáticos. O aumento da presença de lesões na arquitetura hepática e anormalidades nucleares nos eritrócitos do sangue periférico em indivíduos Dolichancistrus fuesslii, Chaetostoma joropo, Astroblepus latidens e Trichomycterus cf. knerii pode estar associado à exposição a poluentes. As alterações teciduais observadas comprometem a saúde dos peixes, devido aos processos de biotransformação de xenobióticos como o mercúrio e o arsênio e, provavelmente, outros contaminantes. Precisamos aumentar a vigilância no rio Garagoa para garantir a saúde ecológica, reconhecer os efeitos hematológicos e teciduais em peixes nativos e desenvolver estratégias de monitoramento eficazes para mitigar as fontes de poluição.

Palavras-chave:
arsênico; bacia do rio Garagoa; genotoxicidade; alterações histológicas; mercúrio

1. Introduction

Pollutants generated by human activities progressively alter aquatic environments and exert constant pressure on biota (Ding et al., 2022). Tons of xenobiotics incorporated by aquatic organisms, that could lead to progressive decline of subpopulations or induce modifications in physiological responses to adapt to environments influenced by chronic stressors such as pesticides, hydrocarbons, metalloids, and heavy metals (Pedraza and Espinosa-Ramírez, 2022; Alonso et al., 2020; Bashir et al., 2016; Couillard et al., 2008).

Heavy metals are found in the aquatic environment as a result from contamination from industrial, agricultural waste and by-products and domestic waste and volcanic activity. Mining can release toxic elements into aquatic systems (De Paula-Gutierrez and Agudelo, 2020), including mercury, arsenic and other pollutants, which can disrupt the development of aquatic fauna (Marlatt et al., 2022; Pedraza and Espinosa-Ramírez, 2022). In fish, the gills and skin are the main routes of exposure to contaminants, followed by the oral route through food ingestion; then, the xenobiotics are subject to hepatic metabolism processes (van der Oost et al., 2003). The main objective of biotransformation reactions is the excretion of endogenous substances, xenobiotics, and their metabolites into more soluble compounds (Papa et al., 2014). During these detoxification processes most of the chemicals are more polar, although others, such as heavy metals and metalloids can bioaccumulate in the muscle tissue (Hossain et al., 2022).

In Colombia, the bioaccumulation of metals in commercially important fishes in the Magdalena basin is well recognized (Pedraza and Espinosa-Ramírez, 2022; De Paula-Gutiérrez and Agudelo, 2020; Silva et al., 2020; López-Barrera and Barragán-González, 2016) and only a few ecotoxicological studies have evaluated the effects of pollution on fishes in the Orinoco region like Astyanax bimaculatus Linnaeus 1758 and the cichlid Aequidens metae Eigenmann 1922 (Corredor-Santamaría et al., 2022; Velasco-Santamaría et al., 2019) and commercial fish exposed to various pollutants (commercial characid Piaractus brachypomus Cuvier 1818 exposed to PAHs such as phenanthrene (Mora-Solarte et al., 2020) and also to herbicides surfactants (Eslava-Mocha et al., 2019). The threats of contamination to native fish species in headwater rivers of the high Colombian tropical mountains are unknown. Studies carried out in Venezuela (Kwon et al., 2012) and Tibet region determine biomagnification of persistent organic pollutants (POPs) and mercury (Hg) in the aquatic food web in high mountain systems (Zhang et al., 2014; Ren et al., 2017).

Boyacá is located on the eastern mountain range of Colombian Andes (NorAndean) and its economic activities include coal exploitation with traces of As, Pb, Se, Hg and Cd (Gómez-Rojas et al., 2016). the Garagoa river basin, drains 2500 km², about 10% of Boyacá department, and is part of the Orinoco River basin, hosts human activities of 35 municipalities, such as aquaculture, poultry, pig farming, agriculture, dairy sector industries, slaughterhouses, and emerald, coal, drag materials, iron, phosphate rock and gypsum mining (Colombia, 2018). In the Garagoa River basin have been recorded 12 fish families Apteronotidae, Astroblepidae, Cetopsidae, Characidae, Crenuchidae, Cyprinidae, Heptapteridae, Loricariidae, Pimelodidae, Poeciliidae, Salmonidae and Trichomycteridae, from 41 fish species (Urbano-Bonilla et al., 2021; Barrios-Alonso et al., 2025) with different degrees of threat according to the International Union for Conservation of Nature (IUCN) criteria (Mesa-Salazar et al., 2016; Villa-Navarro et al., 2021). The objective of the present study was to evaluate the presence of mercury and arsenic in catfish and armored catfish from the Garagoa River basin and the presence of hepatic and genotoxic alterations in the peripheral blood of these fish.

2. Material and Methods

2.1. Sampling sites

Fish and water samples were collected at different sites of the Garagoa river Basin located in the Cordillera Oriental (eastern Andean Mountains range) of Colombia, in the Upper Orinoco River Basin (Díaz-Rojas et al., 2023) where there is exploitation of coal and another mineral (Figure 1). For site selection, the spatial layout of the mining projects in the basin was considered, together with the accessibility to the sampling site. The water samples were collected in August 2021 and October 2021. Muscle samples were collected in October 2021.

Figure 1
Garagoa River basin with sampling points and mineral exploitation areas. Polygons in fuchsia show areas with mining titles.

2.2. Water samples

Water samples were simultaneously collected from each aquatic system sites to evaluate the physical-chemical conditions at each monitoring site including alkalinity, total hardness, ammonium, nitrate using Merck Kits. The electrical conductivity was measured using with YSI 30^® conductivity meter, pH with Handy Lab pH11^®, oxygen concentration, oxygen saturation and temperature with YSI 55^® Oximeter.

2.3. Fishes sampling and tissues analysis

In October 2021 (dry season), trawl nets 3 m wide × 1.5 m high (5 mm mesh) were used to caught wild specimens of catfish (Trichomycteridae and Astroblepidae) and armored catfish (Loricariidae). Fishing was carried out for approximately 50 minutes, or until enough material was caught (Table 1), trawling in a downstream-upstream direction following a zig-zag path and exploring the different types of micro- and meso-habitats along the collection reach.

Table 1
Liver and blood indicators of condition in fish species, mercury, and arsenic concentrations in muscle tissue of fish caught in the Garagoa river basin.

Sampling site	Site id.	Eviscerate weight by species (mean ± sd)	HSI (%)	HT (%)	Muscle tissue sampling unit	Hg (µg/kg)	As (µg/kg)
Juyasia river	13	Dolichancistrus fuessliiA (16 ± 5 g)	1.58 ± 0.28 n=3	26.90	pool 1 (specimen 1-3)	58.59	<9.15
Jenesano river	8	D. fuessliiA (50 g)	0.83 ± 0.07 n=6	15.41	specimen 4	72.61	<9.15
		D. fuessliiA (13 ± 7 g)			pool 2 (specimen 5-8)	76.27	<9.15
		D. fuessliiA (48 g)			specimen 9	66.93	<9.15
Bosque river -1	5	Astroblepus latidensB (1.11 g)	1.33	N.a	specimen 10	105.22	<9.15
Garagoa river -1A	9A	D. fuessliiA (12 ± 12 g)	0.84 ± 0.14 n=9	14.46	pool 3 (specimen 11-13)	56.74	12.47
		D. fuessliiA (33 g)			specimen 14	51.14	<9.15
		D. fuessliiA (10 ± 5 g)			pool 4 (specimen 15-19)	56.8	15.98
Garagoa river -2	10	Chaetostoma joropoB (6 g)	0.29	N.a	specimen 20	65.61	<9.15
		D. fuessliiA (7 ± 8 g)	0.41 ± 0.07 n=5	12.50	pool 5 (specimen 21-25)	61.39	<9.15
		Trichomycterus cf. kneriiC (70 g)	1.00	32.40	specimen 26	294.24	<9.15
El Salitre river	7	D. fuessliiA (5 ± 2 g)	1.05 ± 0.14 n=7	15.17	pool 6 (specimen 27-33)	57.77	<9.15

• HSI: hepatosomatic index when n > 1 values refer to mean ± SE; HT: hematocrit. n: Number of specimens; Site id.: sampling site identifier as used on map. N.a: not available. <: Values below quantification limit. Bold numbers indicate the maximum values recorded by species. IUCN red list status,
• ^A
  Near threatened;
• ^B
  Vulnerable;
• ^C
  Not evaluated.

The fishes were anesthetized by immersion in a 300 ppm solution of 2-phenoxyethanol (J. T. Baker^®, Phillipsburg, USA). The fishes were then weighed (HOPEX Germany^® digital scale) and the standard length (SL) was measured using an ichthyometer. Blood was drawn by dorsal approach at the culmination of the head (and at the bare margin before the dermal plates in loricarids) with a 1 mL syringe (25Gx5/8″ gauge needle) with heparin as anticoagulant. Hematocrit was measured from the blood samples by centrifugation (7,000 g for 5 minutes, Microhematocrit Centrifuge UNICO Model C-MH30^®. The fishes were then desensitized by medullary sectioning, the liver was removed, and a portion was fixed in 10% buffered formaldehyde for further histopathological analysis. The histological procedures were performed in the Laboratory of Toxicology and Biotechnology at Universidad de los Llanos, Villavicencio, Meta, Colombia.

2.4. Genotoxicity analysis

From each blood sample, a smear was performed to determine the frequency of micronuclei (MN) and other nuclear abnormalities (NA). The blood smears were stained for 10 min with Wright-Methanol dye (Merck^®) previously filtered (3 µm filter paper, Whatman^®). The reading of the slides was performed blindly, counting 1,000 cells per smear. Only blood cells with intact nuclear and cytoplasmic membranes were counted, discarding those with overlapping or altered membranes. MN were identified following criteria such as MN diameter less than 1/3 of the main nucleus, clearly separated from the nucleus, not refractile, with the same color and intensity and included in the cell cytoplasm (Grisolia, 2002). The MN count was expressed as a percentage (MN %), calculated from the number of micronucleated erythrocytes observed per 1000 red cells. Nuclear abnormalities were classified as nuclei presenting a small invagination in the nuclear membrane and containing euchromatin called blebbed, binucleated cells, nuclei with micronucleus characteristics connected to the nucleus by a stalk of nucleoplasmic material called lobed and invaginated nuclei called notched (Carrasco et al., 1990). The observations of MN and NA were performed under an optical microscope (Carl Zeiss Primo Star) coupled to a camera with 400X magnification.

2.5. Hepatosomatic index (HSI)

The liver of each fish was measured to calculate the HSI according to Araújo et al. (2018) Formula 1 where:

$$HSI=\left(Liverweight\left(g\right)/Fishweight\left(g\right)\right)\times 100$$ (1)

Decreases in organ weight relative to whole body weight can reflect organ toxicity or disease.

2.6. Histological analysis (DTC)

After tissues fixation in formaldehyde (pH 7.2) for five days, the tissue was dehydrated in increasing concentrations of ethanol, embedded in paraffin (MERCK^®, melting point 52-54 °C), and sectioned at 3 µm using a GMBH microtome (CUT 5062 SLEE^®), and subsequently stained with the Mayer and Harris hematoxylin and eosin (H&E) technique. Four sections for each tissue were evaluated in an optical microscope (Carl Zeiss Primo Star^®) coupled to a camera, with 400 and 1000 X magnification. The occurrence of histological lesions in each tissue was quantified with the degree of tissue change (DTC), which considers the severity of the alterations. DTC were classified as progressive stages of organ function impairment, stage I was estimated as changes that do not alter organ function; stage II implies deterioration of the function of the organ; in stage III, the changes are irreversible. The DTC value was calculated as follows, DTC = (10⁰ × ∑ I) + (10¹ × ∑ II) + (10² × ∑ III), in formula I, II and III are related to the number of alterations in each stage, counted in 30 photographic fields per fabric. DTC were distributed from 0 to 10 as normal tissue; 11 to 20 as mild to moderate tissue damage; 21 to 50 as moderate to severe damage; from 51 to 100 as reversible severe damage; and greater than 100 as irreparable damage (Abalaka, 2015).

2.7. Histometric evaluation

Measurements of the diameters (μm) and the area (μm²) of the nuclei of the hepatocytes of each tissue were made with the ImageJ program. The number of hepatocyte nuclei was counted in 30 photographic fields per tissue per fish with a grid with an area of 10,000 μm² (Corredor-Santamaría et al., 2021).

2.8. Mercury and arsenic analysis

Water and muscle samples were analyzed for Hg and As concentration by atomic absorption in the Laboratory of Toxicology at Universidad de Córdoba, Colombia.

2.9. Statistical analysis

Descriptive statistical analysis was performed expressing the data as mean ± SE. Homogeneity of variance (Levene's or Bartlett test) and normal distribution of data (Kolmogorov-Smirnov test) were performed to verify these assumptions. Since the data did not have a normal distribution to evaluate statistically significant differences in the response variables (DTC, area and diameter of hepatocytes nuclei, micronuclei frequency and nuclear abnormalities) according to sampling sites, a Kruskal-Wallis nonparametric analysis followed by Dunn's post hoc test was performed. In all cases, a value of p<0.05 was used as the level to consider statistically significant differences. Statistical procedures were performed using GraphPad v 5.0.

2.10. Ethics and legal aspects

The study complied with the Colombian guidelines for the care and use of animals for scientific and educational purposes. The procedures involving animal handling were performed according to the standards and procedures for the use of laboratory animals, with the authorization of the Ethics Committee of the Universidad Pedagógica y Tecnológica de Colombia - UPTC (Act 6 of August 12th, 2019; Agreement 096 of November 28, 2006, UPTC). All biological material collections were authorized by the Colombian environmental authority under the Permiso Marco de Recolección - Resolution ANLA 0724 of July 4, 2014. The vouchers were deposited in the fish section of the Museo de Historia Natural Luis Gonzalo Andrade from Universidad Pedagógica y Tecnológica de Colombia (catalog numbers UPTC-Pe-00167 to UPTC-Pe-00209).

3. Results

Four siluriform species were caught, two belong to Loricariidae, Dolichancistrus fuesslii (Steindachner 1911), Chaetostoma joropo (Ballen et al., 2016); one belongs to Astroblepidae, Astroblepus latidens Eigenmann 1918, and the other to Trichomycteridae, Trichomycterus cf. knerii Steindachner 1882 (Table 1). In loricarids, diet is composed of diatoms and other periphytic organisms (Ballen and Vari, 2012), while members of Andean Astroblepidae and Trichomycteridae consume mainly small benthonic macroinvertebrates (Maldonado-Ocampo et al., 2005). The D. fueslii caught ranged in size from 5 to 13 cm, with weights ranging from 5 to 52 grams. At the lowest points, there are smaller specimens with a notable difference in liver weight, which will be explained in the histology and histometry analysis (Table 1).

3.1. Hg and As analyses

The Garagoa river basin tributaries including the Juyasia, Jenesano, El Bosque, Garagoa and El Salitre rivers, receive the discharge of domestic and industrial wastewater, including mining wastewater (Colombia, 2018), which is related by the presence of metals identified in water. In August, mercury was present at all sites (0.21-0.31 µg/L), arsenic in only half of them (2.03-2.31 µg/L), with low concentrations, none of concern for human health (Copaja et al., 2016). In addition, in the October sampling, mercury was below the limits of quantification (0.12 µg/L) and arsenic was below than 0.45 µg/L.

3.2. Hg and As muscle analyses

Mercury was found in all fishes caught in the Garagoa River basin (Table 1). The Hg highest concentrations were found in T. cf. knerii (294.24 µg/kg), A. latidens (105.22 µg/kg), C. joropo (65,61µg/kg), and D. fuesslii with interval between 51.14 - 76.27 µg/kg. Therefore, it indicates active Hg bioaccumulation, however, the level of quantified arsenic was presented mainly in the Garagoa 1A River in D. fuesslii (12.47-15.98 µg/kg). The Jenesano and Garagoa Rivers at sites 1A and 2 recorded the highest number of specimens (three at each site) with the presence of mercury in muscle; by contrast, the arsenic concentration was observed only in the Garagoa 1A River (Table 1). It is worth mentioning that the fishes caught had small sizes (<150 mm of SL), so for tissue analysis it was decided to make a tissue pool per monitoring point (Atobatele and Olutona, 2015).

3.3. Histological and histometric analysis

The exposure to the complex mixture of contaminants such as arsenic and mercury present in the monitored water of Garagoa River basin could induce histological alterations in the liver tissue of the caught armored catfish (Table 1, Figure 2).

Figure 2
Histological changes in liver tissue in specimens of siluriform fish in Garagoa River basin. (A) Dolichancistrus fuesslii, Juyasia River; (B) D. fuesslii, Jenesano River; (C) Astroblepus latidens, El Bosque River; (D) D. fuesslii, Garagoa River -1A; (E) Chaetostoma joropo, Garagoa River -2; (F) D. fuesslii, Garagoa River -2; (G) Trichomycterus cf. knerii, Garagoa River -2, (H) D. fuesslii, El Salitre River. Nuclear pleomorphism (red arrowhead), cytoplasmic and nuclear degeneration (blue arrow), vacuolization (blue circle), pyknotic nuclei (black arrowhead). Hematoxylin & eosin stain. 400X.

Alterations in the liver tissue were observed in all fishes caught (n=33) with less frequency in specimens from the Juyasia and Jenesano Rivers (Figures 2A, B); although the lesions do not compromise liver function, these sites are influenced by the presence of contaminants. In the case of A. latidens, C. joropo and T. cf. knerii, all three specimens showed moderate alterations in the liver (Figures 2C, E, G), compared to D. fuesslii obtained from Garagoa 1A and 2 and Salitre sites (Figures 2D, F, H), which lesions were moderate to severe with the presence of nuclear and cytoplasmic vacuolization, nuclear pleomorphism, cytoplasmic and nuclear degeneration and pyknotic nuclei that could compromise organ function and reduce the ability to biotransform xenobiotic compounds.

Histopathological alterations in D. fuesslii in terms of the DTC were higher in fish caught at the Garagoa 1A site, followed by those caught at the Garagoa 2 and El Salitre sites compared to the Juyasia and Jenesano sites (Figure 3). It should be noted that in Garagoa 2 site a high concentration of mercury in muscle tissue were found (Table 1). In the case of the DTC, the specimens with single capture presented the following DTC order C. joropo (46.40 ± 1.26) > A. latidens (30.10 ± 1.01) > T. cf. knerii (23.57 ± 0.96) with moderate damage.

Figure 3
Degree of tissue change in liver tissue of Dolichancistrus fuesslii specimens caught in different Rivers of the Garagoa basin. Values are shown as mean ± SE (p<0.05). ^a,b,cDifferent letters indicate statistical differences between monitoring sites. The horizontal continuous lines show the distribution of degree damage.

Similarly, statistical differences were found in the histometric analysis in the number of hepatocytes, area, and diameter of nuclei (Figure 4). The Garagoa 1A River and Garagoa 2 River showed the highest number of hepatocyte nuclei, compared to the Juyasia River. At the same time, a greater area and nuclear diameter were found in the liver tissue of D. fuesslii specimens from the Garagoa River compared to fish from the Juyasia, Jenesano and El Salitre Rivers. With reference to the number, area and diameter of hepatocyte nuclei, C. joropo presented (27.40 ± 0.77µm; 25.77 ± 0,42µm and 5.70 ± 0.44µm), A. latidens (22.71 ± 0.58µm; 25.16 ± 0.23µm and 5.64 ± 0.02µm), T. cf. knerii (31.70 ± 0.42µm; 25.10 ± 0.39µm and 5.62 ± 0.04µm), respectively.

Figure 4
Histometric changes in the number, area (µm²) and diameter (µm) of nuclei of hepatocytes of specimens of the loricariid Dolichancistrus fuesslii captured in different Rivers of the Garagoa River basin. Values are presented as mean ± SE (p<0.05). ^a,b,cDifferent letters indicate statistical differences between monitoring sites.

3.4. Genotoxicity analysis

Regarding the analysis of genotoxicity in peripheral blood, a higher occurrence of micronuclei, lobed nuclei and notched nuclei was found in fishes from the El Salitre River, followed by the Garagoa 2 River (Figure 5). Furthermore, with respect to the frequency of MN, C. joropo presented 0.15 ± 0.04%; A. latidens 0.12 ± 0.04% and T. cf. knerii 0.05 ± 0.02%. In the case of AN, C. joropo presented 0.13 ± 0.02%; A. latidens 0.08 ± 0.02% and T. cf. knerii 0.07 ± 0.01%.

Figure 5
Frequency of abnormalities in peripheral blood of the loricariid Dolichancistrus fuesslii caught in different water bodies of the Garagoa River basin. (A) Micronuclei; (B) Another nuclear abnormalities. Values are presented as mean ± SE (p<0.05). ^a,bDifferent letters show statistical differences between monitoring sites for each variable.

4. Discussion

In high-altitude aquatic systems there is evidence of high bioaccumulation and subsequent biomagnification of persistent organic pollutants (POPs) and mercury (Hg) in the aquatic food web, even though levels in the aquatic environment were very low (Ren et al., 2017), this pattern occurs due to the longevity and slow growth of fishes in unproductive environments can be key factors in the accumulation of mercury levels comparable to those in areas affected by human activity (Zhang et al., 2014). It is important to note that geology in some local positive abnormalities of Hg located on the western flank of the Cordillera Oriental, department of Boyacá, probably correspond to anthropogenic sources related to plant activity thermoelectric that works in this state and use fuel coal for its production (Mendoza et al., 2020a).Towards the flank eastern Cordillera Oriental, southeast of Boyacá and east of Cundinamarca, a geochemical trend can be observed positive arsenic, lithologically associated with sediments of Lower Cretaceous age related to the Bata formations, Santa Rosa, Ubalá and Lutitas de Macanal, in the direction NNE-SSW, parallel to the arsenic anomaly of the western flank of this mountain range (Mendoza et al., 2020b). Although, fish metals bioaccumulation and subsequent biomagnification may be due to environmental conditions (e.g., pH, temperature, dissolved organic matter, biomethylation and demethylation rates, or bioavailability), size of food web, fish growth rate, fish ecological traits such as feeding habit, lifespan, trophic level, and availability of Hg in water or sediments (Zhang et al., 2014), and biogeochemical conditions (Dong et al., 2016). Indeed, the severity of toxicity varies significantly with the fish species, the level of the pollutant, and time of exposure.

The focus on effect biomarkers showed good sensitivity to pollution in the Garagoa River and suggest inclusion of ecotoxicological analyses in biomonitoring plans in Colombia. Food digestion and absorption is likely the most important process to drive the transfer organic Hg (MeHg) into the wild fish from their prey, suggesting that the food web structure has crucial importance for the higher mercury concentrations in top predators (Silva et al., 2020; Ren et al., 2017). In this study, the four species evaluated have different feeding habits. Dolichancistrus fuesslii feeds mainly on periphyton algae and fungal hyphae; C. joropo is mostly algivorous and occasionally feeds on Diptera larvae (Ballen et al., 2016); T. cf. knerii consumes a varied spectrum of food groups, invertebrates, fish, plant remains and detritus (Zamudio et al., 2008). Finally, astroblepids feed mainly of aquatic insects (Diptera, Ephemeroptera and Trichoptera) and to a lesser extent on Coleoptera, Lepidoptera, Anisoptera, Plecoptera and Hemiptera (Maldonado-Ocampo et al., 2005).

Fish species that consume benthic macroinvertebrates (i.e., species occupying a higher trophic level), such as A. latidens and T. cf. knerii, showed higher concentration of mercury than periphytivorous species (D. fuesslii, C. joropo). In addition, it should be highlighted that the highest concentration of mercury in T. cf. knerii was expected, since this trichomycterid had the largest size of all caught species (SL: 213 mm) and it has been shown that Hg concentrations increased with the body size of the fish and that the highest concentrations of Hg can be found in old predatory fishes (Silva et al., 2020). Trichomycterus cf. knerii has the level of mercury (294.24 µg/kg) comparable with iliophagues fishes from aquatic systems with influence of gold mining in northern wetland in Colombia (Pedraza and Espinosa-Ramírez, 2022), which contrasts with A. latidens (only 70 mm of length) was the second species with the highest mercury concentration with 105.02 µg/kg. The human community of the basin consumes these species (Roa-Fuentes, 2022, personal communication), so it is necessary to alert the authorities about possible health risks, mainly in the lower basin of the Garagoa River where larger specimens are found, which are frequently fished by the locals. Therefore, all species caught in Garagoa River are potential bioindicators of exposure to pollutants that are transferred in the food web, which allows inferring that they are sentinel species of the health of aquatic environments since they constitute a secondary link in the trophic chain with few direct predators (Allard et al., 2016). In this study histological and genotoxicity alterations were biomarkers of contamination effect in native species, expanding applications in neotropical ecotoxicology for native fishes in Garagoa River basin. The lowest his were found in the loricarids from the Garagoa 1A and 2 Rivers, and from the Jenesano River, which coincides with the presentation of greater histopathological alterations found in the liver of the specimens caught in the Garagoa River. It is recommended to analyze in greater detail the ecotoxicological effects on A. latidens and C. joropo due to their IUCN vulnerable category, where chemical contamination would be an additional factor of pressure on theses endemic species. Dolichancistrus fuesslii showed differentiated sensitivity to pollution and is therefore a good sentinel of the ecological quality of aquatic environments (Table 1).

Neves et al. (2018) reported hematocrit values (%) found in four amazonian siluriform species: Peckoltia oligospila (Günther 1864) (24.9 ± 3.9), Cochliodon sp. (22.1 ± 9.1), Lasiancistrus saetiger Armbruster 2005 (23.8 ± 8.7) and Pseudacanthicus spinosus (Castelnau 1855) (12.7 ± 4.6). In the current study, higher hematocrit was found in the caught species, which is probably associated with the high altitude since under these conditions there is a decrease in the content of dissolved oxygen in the blood and an increase in the hematocrit is a compensatory mechanism to fulfill the oxygen demand (Rosidah et al., 2018).

Regarding mercury concentrations, in periphytivorous species may be due to the significant role of periphyton in mercury bioaccumulation in river ecosystems (Bell and Scudder, 2007), including high-altitude systems in the neotropics, where intense mercury methylation has been reported in benthic biofilms and periphyton of green algae (Bouchet et al., 2018). A concentration of heavy metals increased with the trophic level (Dolichancistrus fuesslii → Chaetostoma joropo →→ Astroblepus latiden → → → Trichomycterus cf. knerii) suggesting that there would be an increase in Hg concentration after the transition from one trophic level to the next, which could indicate a possible biomagnification effect in the Garagoa River basin.

The liver in fish is the main organ of biotransformation of endogenous compounds and xenobiotics, and it is involved in the metabolic and biochemical processes necessary for the utilization of nutrients or the purification of environmental pollutants, including detoxification and excretion of xenobiotics (van der Oost et al., 2003). Exposure to pollutants allows fish to be used as bioindicators of aquatic systems (Liebel et al., 2013). Consequently, fishes are bioindicators of exposure to harmful compounds in animal tissues, which is notable in species with detritivorous habits that allow bioaccumulation of toxic substances and are robust sentinels of the health of aquatic environments where they constitute a secondary link in the trophic chain with few direct predators (Allard et al., 2016; Corredor-Santamaría et al., 2019).

Liver histopathology (Figure 2) have been evidenced in other studies that reported liver lesions including remarkable changes in architecture in Channa striatus (demersal fish) and Heteropneustes fosilis (catfish) inhabitants of the Kali River, India, with high levels of heavy metals (Cr, Ni Pb and Cd), with identification of tissue vacuolization, pyknosis, rupture of blood vessels and necrosis in fishes from contaminated sites compared to reference sites (Fatima et al., 2015). Also, in the carnivorous cyprinid Wallago attu and the herbivorous silurid Cirrhinus mrigala have been reported the occurrence of necrosis, degeneration of muscle fibers, edema, and blood loss due to blockage of blood vessels in fish caught in sites with high concentrations of metals (Ni, Cr, Pb, Hg) in the Chenab River in India, that receives industrial wastewater (Hussain et al., 2020).

In feral fishes living in the vicinity of a chlor-alkali plant with mercury cells, mercury levels between 1.48 and 1.78 mg/kg BW, hepatic alterations such as oxidative injury and hypoxemia has been reported (Raldúa et al., 2007), which can be related to the liver histopathological alterations observed. Hyperplasia and hypertrophy of hepatocytes of siluriform fish caught in the Garagoa River could indicate exposure to substances that induce cell proliferation or regenerative inflammatory processes, such as heavy metals (Wolf and Wheeler, 2018), like the results observed in this study. Considering the relationship between liver weight and body weight of the fish, this HSI in the specimens (Table 1) showed a trend between the HSI compared with the highest liver alterations found (Figures 2 and 3).

Regarding the increased alterations in the liver parenchyma, related to stage I (nuclear pleomorphism, cytoplasmic vacuolization and increased relative frequency of blood vessels), stage II (cytoplasmic and nuclear degeneration, cellular rupture, nuclear vacuolization, pyknotic nuclei and hyperemia) and stage III (focal necrosis) disturbances (Wolf and Wheeler, 2018); the alterations found in siluriform fish from the Garagoa River correspond to moderate to severe lesions associated to the possible oxidative stress in the hepatocytes, which can generate disturbances in the metabolism of endogenous substances and xenobiotics, affecting the capacity to respond to pollutants present in the water body. Ramos-Osuna et al. (2020) reported a reduction of HSI in the liver of Haemulopsis elongatus Steindachner 1879 and in the muscle of Pomadasys macracanthus Günther 1864 that contained high concentrations of mercury (3,748 μg/g and 0.574 μg/g), respectively, caught in the Gulf of California. It has been proposed that HSI reduction may be associated with stress by xenobiotic substances in exposed fish that requires the consumption of energy reserves in detriment of detoxification processes (van der Oost et al., 2003). In contrast, other studies have not found relationship between the presence of total mercury in muscle (52 µg/kg live weight) and his changes in HSI, such as in freshwater characin Brycon falcatus Müller & Troschel 1844, which is used for human consumption (Matos et al., 2018).

Alterations in nuclear morphology of peripheral blood erythrocytes are reported in studies assessing the occurrence to nuclear abnormalities in wild freshwater fish caught in natural water bodies receiving domestic and industrial wastewater containing xenobiotics capable of inducing genotoxicity at sublethal concentrations of PAHs such as naphthalene and metals such as mercury and cadmium, in native species such as the cyprinid Labeo rohita Hamilton 1822 from the Chenab River (Hussain et al., 2018), the characid Astyanax gr. bimaculatus Linnaeus 17587 and the cichlid Aequidens metae Eingenmann 1922 from the Ocoa River in Colombia (Corredor-Santamaría et al., 2016; Velasco-Santamaría et al., 2019).

Finally, both the occurrence of histological lesions in the hepatic parenchyma and the manifestation of genotoxicity with the presence of nuclear abnormalities, allow us to elucidate that all monitored water bodies in the Garagoa River basin are contaminated by the discharge of domestic and industrial wastewater, so neither site was found to be unaffected by the deleterious effect of human activities.

Biomarkers of effect make it possible to demonstrate exposure to xenobiotics such mercury, arsenic or probably other pollutants not monitored (e.g POPs, or emergent contaminant) were apparently sufficient to cause tissue damage and genotoxic effects. More exhaustive studies are required on the bioaccumulation capacity of these species in the basin and especially the possible genetic erosion that chemical pollution may be generating in native ichthyofauna.

It is evident that pollution containing metalloids and metals such as arsenic and mercury in the Garagoa and El Salitre Rivers has a greater deleterious impact on fishes inhabiting these water bodies; however, in loricariid fish species caught in Juyasia, Jenesano, and El Bosque Rivers were observed also lesions although in less extend. These disturbances can compromise fish health by reducing the biotransformation capacity of xenobiotics and affect the health and survival of this species. This study is pioneering in the ecotoxicology of fishes in aquatic environments of the Northeastern Andes, a center of neotropical endemism. This study highlights the need to propose management and conservation measures for the species according to their biogeographic, taxonomic, phylogenetic, and functional importance. For this basin, 41 fish species have been registered with different degrees of threat according to IUCN criteria, none includes ecotoxicological criteria, therefore we propose to continue with research on native fishes in points of the lower basin to detect possible alterations of food webs and monitor the genotoxic effects on larger fish populations. In particular, it is recommended to analyze in greater detail the ecotoxicological effects on A. latidens and C. joropo due to their vulnerable category, where chemical contamination would be an additional factor of pressure on these species. D. fuesslii showed differentiated sensitivity to pollution and is therefore a good sentinel of the ecological quality of aquatic environments. This is a first report of mercury and arsenic occurrence in Andean fishes of the Garagoa basin and although the World Health Organization has reported that methylmercury levels in their edible portion are 200-300 µg/kg for fish (WHO, 1990), our results should be considered into public health monitoring, since all four species evaluated are widely consumed by the inhabitants of the Garagoa River basin. It is necessary to elucidate the role of aquatic insects in the transfer of metals with possible bioaccumulation in Andean food webs, given their high diversity, abundance, richness (Barrera-Herrera et al., 2023) and its sensitivity to changes in the landscape (Díaz-Rojas et al., 2023) in the Garagoa River basin.

Finally, this work provides evidence of bioaccumulation of mercury in native fishes with feeding habits of algivorous and insectivorous, which warns of possible bioaccumulation in top predators in the lower parts of the Garagoa River basin. New ecotoxicological information must be generated on bioaccumulation, genotoxic and histological effects in endemic fishes species of the Orinoco basin, especially in headwater rivers with high influence of human activity such as mining, agriculture and urbanization.

Acknowledgements

The authors are grateful to students (Andrés Galán, Idalith Salamanca, Cristian Acuña) and research assistants (Jeffrey Mauricio Prieto) of the Research Group UDESA for their valuable participation during the sampling procedures. This study was supported by project SGI 3057 “Biomonitoreo de polutantes con peces nativos en sistemas lóticos andinos (Boyacá- Colombia)” funded by Vicerrectoría de Investigación y Extensión (VIE) - Universidad Pedagógica y Tecnológica de Colombia through the “Impulso a la investigación convocatoria Sostenibilidad de grupos 2021” call in collaboration with the Universidad de los Llanos. The SGI 3057 project is an extension of the “Importancia de las variables locales y del paisaje sobre las comunidades de peces y macroinvertebrados bentónicos de sistemas lóticos andinos” project financed by MinCiencias (Fondo Francisco José de Caldas – FFJC, Convenio especial de Cooperación 404-2019, CDR 15464-2020) and Universidad Pedagógica y Tecnológica de Colombia (SGI 2955). MAPM receives research support from Ministerio de Ciencia, Tecnología e Innovación - MinCiencias (Research call: 848-2019) and from Universidad Pedagógica y Tecnológica de Colombia (Research project code: SGI-3000).

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Publication Dates

• Publication in this collection
  31 Jan 2025
• Date of issue
  2024

History

• Received
  19 Apr 2024
• Accepted
  18 Oct 2024