Bacterial contamination in urban areas of the main Ecuadorian rivers
All rivers showed E. coli levels above standard concentrations for bathing-water recommended by the USA, European and Brazilian guidelines (Fig. 1), in concordance with other studies in Latin America, such as Colombia34, Mexico4, and Perú35. Most of the rivers in this study could be treated to produce drinking or bathing water, however, a drastic and expensive treatment would be necessary, being economically challenging in Ecuador.
Some studies in the USA reported lower levels of E. coli and total coliforms contamination than those reported in Latin America36,37. In particular, the study of Bower and colleagues37 demonstrated that 28 of the 74 analyzed samples did not exceed 235 CFU per 100 ml of E. coli showing a drastically lower level of contamination when compared to this study. In addition, other studies reported different levels of E. coli ranging from 3.1 × 105 to 6.4 × 105 CFU per 100 mL in Asia (India, Nepal and Iran), and 4.2 × 104 to 5.4 × 104 CFU per 100 mL in Spain5,38,39. Therefore, the contamination levels were higher than the results obtained in our study (5.00 × 103 to 2.50 × 104 CFU per 100 mL).
The selection of the sampling locations was an important step for the analysis of the water quality. In our study, all sampling locations were selected from dense urban areas and downstream of the most contaminated zones (Table 1). It is important to mention that the levels of total coliforms and E. coli were obtained at a similar order of magnitude, suggesting that most of the total coliforms were constituted by typical E. coli from animals and humans’ enteric origin. Most likely, these results evidenced environmental contamination of the rivers set by urban sewages, as previously reported40. Although all water samples were collected from areas of high population density, the contamination in our study was most probably due to the lack of wastewater treatment plants. Untreated sewage, combined with the geographical locations and the ambient temperatures, could contribute to the bacteria proliferation in surface waters6.
Next, we reported the presence of three Escherichia coli pathotypes (EAEC, EPEC, and EIEC). EHEC was not detected in any samples from our study. Although EHEC is one of the most prevalent E. coli pathotypes among environmental samples, Stanford et al. demonstrated seasonal variations in the prevalence of E. coli pathotypes41. The lack of positive EHEC results could be due to the cross-sectional study realized during a single season, showing one of the limitations of the present study. The EIEC was the most prevalent E. coli pathotype and it was found in five rivers. On the other hand, the EPEC and EAEC pathotypes were detected only once. More exactly, the EPEC was found in Zamora River while the EAEC was observed in Machángara River. These E. coli strains are more commonly found in rivers from developing countries, even in surface water resources42. E. coli pathotypes even on samples with low concentrations of total coliforms and E. coli constitute a greater threat to public health. All E. coli pathotypes are potentially dangerous to the population (particularly, in children). E. coli pathotypes may cause urinary tract infections, bacteremia, and bacterium-related diarrhea, being also the main cause of neonatal meningitis in humans and animals25. These findings represent a possible public health problem taking into account the type of distribution of the untreated water to the surrounding population, where the river water is usually used for numerous local practices (domestic, agricultural, live stocking, and even recreational activities). Currently, public health officials rely on infection reports by certain communities (such as indigenous, and rural communities) or public health outbreaks for assessing pathogen and/or chemical levels in water resources. So, future monitoring should be simultaneously realized in untreated wastewaters and natural freshwater resources. Finally, besides the standard quantification of E. coli and total coliforms, the detection of E. coli pathotypes could be useful as an additional indicator in water analysis to prevent waterborne disease outbreaks.
Physicochemical parameters of surface waters
The majority of values found in the rivers were below the maximum limits established by the local legislation. However, certain parameters, such as TSS (132.5 to 939 mg L−1 > 130 mg L−1), CODTOTAL (48.37 to 349.73 mg L−1 > 40 mg L−1), and TS (1657.50 to 3667.50 mg L−1 > 1600 mg L−1), were above Maximum Contaminant Levels (MCL; Fig. 2). In Ecuador, few studies assessed these chemical parameters in rivers 21,24. Voloshenko-Rossin and colleagues evaluated some physicochemical parameters in the San Pedro, Guayllabamba and Esmeraldas Rivers21, obtaining similar values of pH, conductivity, dissolved oxygen (DO), and turbidity when compared to our study. In Guayas, Damanik-Ambarita and colleagues studied the water quality of the Guayas River basin, evidencing also analogous values of pH, temperature, and DO. However, other physicochemical parameters were reported in lower levels when compared to our results, such as conductivity, turbidity, CODTOTAL, and TSS24. Other studies in Latin American countries also analyzed these basic parameters reporting similar levels of temperature, pH, and turbidity, such as Brazil42.
The high conductivity values were found in Guayas (4137.33 µS cm−1) and Esmeraldas (938.53 µS cm−1) Rivers. However, samples from the Guayas and Esmeraldas Rivers were collected in the urban area located near the Pacific Ocean, and so their high conductivity values could be associated with the presence of high concentrations of certain salts (such as Na and Mg) due to the entrance of sea waters. When measuring mixed water or saline water, conductivity values can easily achieve values greater than 5000 µS cm−1, in which case these rivers demonstrated normal conductivity values32. It is important to mention that samples from the Guayas River could have also shown a higher conductivity due to geological factors of the studied area, where it possesses clay soil. Therefore, it was expected to find high indices of conductivity among Guayas and Esmeraldas Rivers in opposite to rivers with granite associated soils (such as Toachi, Tomebamba, and Zamora Rivers), where this type of soil does not ionize and usually shows low conductivity values. In addition, brackish water samples with high conductivity values generally show higher values of TS and TSS, as previously detected in Guayas and Esmeraldas Rivers. Therefore, their higher TS and TSS values were considered normal among brackish systems32. On the other hand, DO values were quantified between 6.08 and 8.30 mg L−1, being slightly above the minimum value allowed by the Ecuadorian Legislation (at least 6 mg L−1 or 80% saturation). It is important to mention that DO values could vary with temperature12,18, where higher temperatures usually diminished dissolved oxygen levels in the water. The dissolved O2 range measured in the rivers of this study was found to be suitable for natural waters depending on turbulence, temperature, salinity, and altitude43.
Trace metals in surface waters
The majority of the elements were below the permitted limit for water aimed at agricultural use or for the preservation of aquatic and wildlife (Fig. 4)32,44. However, some levels of Cu, Pb, and Fe, and most levels of Zn and Al were the exceptions, showing high concentrations above the MCL at several sampling points. Although the maximum values recommended by the WHO are usually lower than the Ecuadorian legislation, it is important to mention that most of the elements were below both limits.
Nevertheless, Guayas and Machángara Rivers, indicators of the surface water quality of the two most populated cities of Ecuador (Guayaquil and Quito, respectively), and Chone River registered concentrations of Pb ten times higher than the maximum contaminant level (1 µg L−1). Lead is considered an important toxic heavy element in the environment, affecting almost every function in humans45. Even though lead is naturally present in the environment, anthropogenic activities (fossil fuels burning, mining, and manufacturing) contribute to its increase45. The Pb levels found in these three rivers were similar to the contamination levels reported by Cui et al. in urban zones of rivers in Northeast China (Harbin City)46. It is important to mention that the values of lead contamination in our study were very close to the limit of quantification (LOQ; 10.12 µg L−1). Therefore, it is plausible that these concentrations could not be accurately distinguished in these rivers. However, Machángara River already showed superior lead contamination (59.7 µg L−1) in a previous study23.
Cu was detected in the Guayas, Machángara, and Guayllabamba Rivers at concentrations exceeding the Ecuadorian guidelines. Similar contamination values of Cu were already reported in other countries, such as Bangladesh (50–100 µg L−1)47 and Canada (1–110 µg L−1)48. Some sources mentioned that these levels of Cu could be associated with the contamination from water pipes from households or industries49. However, other countries, such as Chile (170–630 µg L−1)50 and the USA (10–570 µg L−1)51, reported higher values of Cu on rivers. These higher concentrations could be explained by mining industries or activities near the water sources. Excess copper induces oxidative stress, DNA damage, and reduced cell proliferation leading to copperiedus52.
Although Zn is an essential element for all organisms, an excess of zinc plays a significant role in cytotoxic events in the cells. This element is involved in cell death of the brain, and its cytotoxicity induces ischemia or trauma53. In our study, eight rivers revealed Zn levels above the quality criteria32, ranging from 1.5 until 4.2 times higher than the MCL (30 µg L−1). These levels were still found below contamination levels from other studies realized in China46 and Brazil54. However, our levels of Zn are superior to the levels reported in Argentina55. These authors analyzed water samples from La Plata basin, showing levels of Zn between 0.2 and 11.9 µg L−1. Although their levels of Zn were below our results, these authors suggested that people would eventually experience high health risks through continuous consumption. So, these health risks are also plausible to the Ecuadorian population exposed to the rivers in our study.
Furthermore, Al and Fe were detected in values higher than those established by WHO (2011), by Ecuadorian legislation, or even in surface waters used for human consumption in the country56. As previously described, Al comes mainly from natural sources being one of the main constituents of the silicates that make up the mineral clay57. More exactly, Al concentrations were quantified between 0.49 and 30.80 mg L−1. Interestingly, seven rivers showed similar elevated Al concentrations (around 22 mg L−1). However, a previous study in Ecuador already reported analogous Al concentrations (17.30–18.25 mg L−1) in seven of eighteen rivers of Pichincha province23. These similar levels can probably be attributed to a strong build-up of Al from natural resources rather than directly from wastewater discharges due to anthropogenic activities. It is important to mention that Ecuador is a country famous for its large number of volcanoes contributing to the Al accumulation in soil and natural water resources58. Therefore, it is plausible that the high levels of Al in surface water on these locations did not differ significantly between them even with the anthropogenic activities in the urban areas of the rivers. Even though anthropogenic activities, such as discharge of industrial and domestic effluents, use of agricultural chemicals, land use, and cover changes, are typically the major factors that influence surface water quality. Accumulative exposure to this metal in low concentrations does not cause any harm to humans or animals. However, high concentrations of metals (such as Al) can trigger complications in the kidney due to metal accumulation and also induce cases of infertility in animals58 but its bioavailability depends on its species. Dissolved Al in water may induce risk for human health when reaching values for the internal aluminum load above 15 µg L−1 in urine or 5 µg L−1 in serum59. In Ecuador, the MCL of Al for the preservation of aquatic and wildlife in fresh and marine water is 0.1 mg L−1. Therefore, most rivers surpassed this legal value by more than 200 times, excepting the Guayllabamba River (approximately 5 times more than the MCL). The accumulative exposure of Al in these rivers could be potentially dangerous for aquatic life and even for human through regular water consumption. On the other hand, high concentrations of Fe were only detected in the Guayas (6.84 mg L−1) and Guayllabamba (0.46 mg L−1) Rivers, showing approximately a Fe concentration in the Guayas River of 10 times higher than the MCL (0.7 mg L−1) recommended by the World Health Organization44. Although this Fe concentration is not an immediate danger to public health, cumulative Fe contamination could cause hemorrhagic necrosis and disorders in the stomach mucosa60. So, further studies should monitor Fe variations in these rivers.
Previous studies18,60 reported similar metal analysis, showing also elevated concentrations of dissolved Fe, Mn, Al, Pb, and Zn. These large metal concentrations are usually associated with high soil erosion and discharges of contaminated water from different anthropogenic activities (such as industrial, oil, and agricultural), and followed by several public health issues in the surrounding communities, such as neurological problems, skin irritation, hormonal imbalances, atopic dermatitis, and thyroid problems2.
In Latin America, in the last decades, high concentrations of metals have been found in several rivers2,42,60. In Colombia, Cd and Pb were the highest metal values found nearby crops of vegetables and legumes2. These studies reported the contamination by several metals in water resources and warned for the use of these waters in the food industry (livestock and agriculture). Likewise, studies in the United States realized similar metal analysis in water supplies, showing significantly lower metal concentrations51,61. These low levels of metals in surface water could be due to the strict national regulations that control the heavy metal levels of effluents from large-scale industries61.
In summary, the main rivers of Ecuador showed unacceptable microbial, physicochemical, and metal levels for the preservation of aquatic and wildlife in freshwater, nor human consumption or bathing waters, and agriculture activities. To the best of our knowledge, this is the first study in Ecuador that simultaneously analyzed the microbial and physicochemical parameters in the three main natural regions (Coastal, Andean, and Amazonian), demonstrating statistically significant differences between these regions. However, this statistical analysis should be validated in future studies with a greater number of samples. Also, it is important to mention that there are some major limitations of the present study: (1) it is a cross-sectional study, and therefore unable to evaluate seasonal variations of microbial and physicochemical levels, (2) all physicochemical analyses were realized using water samples taken once in each river, (3) the sampling points were selected close to the main cities or even in urban areas, and it would be useful to extend this monitoring downstream in order to evaluate the extension of the observed contamination, and (4) this study only evaluated the presence or absence of several bacterial genera through PCR analysis without sequencing analysis.
Despite the increasing legislation in Ecuador, there is still an exceedance of the established standards, which suggests that practical control on effluent levels is underdeveloped. Finally, it is essential to evaluate a future scenario of reversing these high rates of microbial and chemical contamination by installing efficient wastewater treatment plants.
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