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Article

Human Impact in the Watershed of the Atoyac River in the Metropolitan Area of Puebla, Mexico

by
Ana Cristina Covarrubias-López
1,2,
Wendy Argelia García-Suastegui
1,2,
Rafael Valencia-Quintana
3,
Fabiola Avelino-Flores
1,4,
Aarón Méndez-Bermúdez
5 and
Anabella Handal-Silva
1,2,*
1
Posgrado en Ciencias Ambientales, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla 72570, Mexico
2
Departamento de Biología y Toxicología de la Reproducción, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla 72570, Mexico
3
Laboratorio de Toxicología Genómica y Química Ambiental, Universidad Autónoma de Tlaxcala, Tlaxcala 90062, Mexico
4
Centro de Investigaciones en Ciencias Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla 72570, Mexico
5
Institute for Research on Cancer and Aging, IRCAN, 06189 Nice, France
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(13), 10565; https://doi.org/10.3390/su151310565
Submission received: 10 May 2023 / Revised: 23 June 2023 / Accepted: 28 June 2023 / Published: 5 July 2023
(This article belongs to the Special Issue Chemical Pollutants in Water, Air, and Soil: Risk Assessment, Monitoring and Governance)
Browse Figures
Versions Notes

Abstract

:
The largest economic, population, administrative, and service production of the State of Puebla (east-central Mexico) is concentrated in the Metropolitan Area of Puebla (MAP), and its effect on the water quality of the Atoyac River is substantial. The anthropogenic contamination of the Atoyac River and its tributaries in the MAP was evaluated and characterized. For this purpose, industry types and industrial density (ID) were identified, and the physical–chemical quality of water in the urban Atoyac, Rabanillo, Zapatero Rivers, and the Covadonga and Echeverría Dams were analyzed. In addition, the cytotoxicity of water was evaluated using the biomodel Allium cepa by analyzing the mitotic index (MI) and the interphase index (II). The correlation between the physical–chemical variables of water and MI was estimated. The results included 4500 industries, among which are the construction, metallurgy, metalworking, food, and textile industries. The highest ID was found in the municipality of San Pedro Cholula. The greatest anthropogenic impact occurred in the Rabanillo River and the Echeverría Dam. Throughout the watershed, anoxic conditions were registered and 18 chemicals, most of which are toxic and carcinogenic, were detected. A Correlation analysis showed that the greatest antimitotic effect in Allium cepa was induced by turbidity, chemical oxygen demand (COD), and lead (Pb), with correlation coefficients of −0.919, p = 0.008; −0.864, p = 0.013; and −0.692; p = 0.030, respectively. It was concluded that if the population, industry, and natural resources are associated in the MAP under current conditions, the outlook, if nothing changes, is that the degradation of the water resource will be disruptive and probably unsustainable for any type of use.

1. Introduction

The environmental impact of population growth in large cities in both developed and developing countries is increasingly growing, which implies great challenges in terms of providing services such as public transport, housing, employment, security, and environmental care, among others. In Mexico, the situation is no different; there is the phenomenon of metropolization [1,2], characterized by the territorial expansion of a city towards other cities or municipalities with which it establishes an obligatory economic interdependence due to the concentration of production-related activity, the population and resources (food, energy sources, land, and water, among others) being unequally distributed. This process began in the 1940s, and until 2005, the National Institute of Statistics, Geography, and Informatics (INEGI); the National Population Council (CONAPO); the Ministry of Social Development (SEDESOL); and the Ministry of the Interior (SEGOB) recognized 56 official metropolitan areas, which together represented 7% of the country’s area. This area housed 56% of the total population and 77% of the urban population, who contribute to the generation of 75% of the country’s production [2]. In 2020, fifteen years later, the Ministry of Agrarian, Territorial and Urban Development identified 74 metropolitan areas, which houses 75.1 million people and represent 62.8% of the national population [2,3]. This means that the metropolitan phenomenon tends to increase urban and productive concentration, increasingly impacting social and environmental vulnerability. In this regard, Mexico does not have an adequate model of territorial occupation, which leads to an accelerated, disorderly, and unsustainable urban expansion of human settlements, accompanied by loss and degradation of the environment [3]. This situation is reflected in the Metropolitan Area of Puebla-Tlaxcala (MAPT). Within the national metropolitan context, the MAPT is located in the center of the state of Puebla and in the south of the state of Tlaxcala, ranking fourth in terms of population. It is a node of strategic articulation between the Central and South-southeastern regions of the country; it is also a provider of professional, financial, and higher education services.
The MAPT is located in the Alto Balsas watershed; its main river is the Atoyac, which is part of the Balsas watershed [4], where 10% of the electricity is used and 25% of the country’s hydroelectric energy is generated, constituting a strategic hub for the fight against poverty, economic growth, and food security [5,6]. On the other hand, CONEVAL highlights poverty as a common denominator in the inhabitants of metropolitan areas in Mexico and points to the metropolis of Puebla-Tlaxcala among those with the highest percentages of extreme poverty [7]. The Atoyac River runs through approximately 80% of the MAPT [7,8] and carries a large number of toxic pollutants from the state of Tlaxcala [8,9,10]. In this regard, Andrés E.R et al. (2022) emphasized that pollution in the municipalities of San Martín Texmelucan (Puebla) and Tepetitla de Lardizabal (Tlaxcala) are at a critical level of industrial pollution [11,12,13]. To the Atoyac River, the current coming from the Zahuapan River is added, forming an area where 59% of the inhabitants of Tlaxcala live [14]. This river enters the municipality of Puebla in the Covadonga Dam [14] and, on its way, receives discharges from the Rabanillo, Zapatero, and San Francisco Rivers located in six municipalities that together comprise 33.6% (2,212,002 inhabitants) of the total population of the state of Puebla in a territory that represents less than 2.54% (870.81 km) of the area of the state [15]. On the other hand, an important part of the economy of the state of Puebla is based on the industrial sector that represents 34% of the state’s GDP and is concentrated in the MAP. In this regard, it has been demonstrated for more than two decades that as a result of the high population and industrial concentration along the Atoyac River, there is increasing pressure on water resources and, as a consequence, the most critical points of organic and inorganic pollution generated by the states of Tlaxcala and Puebla are identified [7,9,14,15,16,17,18,19,20,21]. Adverse effects on human health, such as cytotoxicity-related cellular transformations, chromosomal damage, and reproductive abnormalities, have also been shown [7,16,18,21,22].
Studies carried out in the MAP on the effects of anthropogenic pollution on water quality in urban rivers and the identification of the cytotoxic effects are limited. An important investigation that evaluated the pollution of the Atoyac River reported that the contaminating mixture of toxic metals and volatile organic compounds induces aneugenic effects in the apical meristem of Allium cepa: as the concentration of contaminants increases, the mitotic index decreases [12]. Knowing about the existing environmental problems in the region, the purpose of the study was to evaluate the effects that human-generated activities produce on the rivers that cross the MAP; to identify the origin of chemical contamination; and in turn, to evaluate the potential cytotoxic effects generated by wastewater (WW) in the Allium cepa biomodel, as well as to demonstrate that the watershed in its current conditions is unsustainable and constitutes a challenge that requires the effective participation of society and the state to make decisions under a shared vision and thus achieve sustainability in the use of the resource.

2. Materials and Methods

2.1. Study Areas

The Atoyac River belongs to the Alto Balsas watershed, located in the Tlaxcala-Puebla Valley in the Hydrological-Administrative Region IV Balsas (RH18) [23,24,25]. This study was carried out in the MAP in the municipalities of Cuautlancingo, San Andrés Cholula, Coronango, San Pedro Cholula, Ocoyucan, and Puebla, all of them crossed by the urban Atoyac, Rabanillo, and Zapatero Rivers and where the Covadonga and Echeverría Dams are located.
The first study area (Z1) was the Covadonga Dam located on the Atoyac River between the state borders of Puebla and Tlaxcala in the municipality of Cuautlancingo (Puebla) [20,21,26,27]. In this area, the Atoyac and Zahuapan Rivers from the State of Tlaxcala converge and the industrial discharges from Cuautlancingo are added (Figure 1, Table 1 and Table 2). The municipalities of Coronango, San Pedro Cholula, and Cuautlancingo are crossed by the second study area, the Rabanillo River (Z2). This river is 13.47 km long and crosses 10 densely populated localities. It receives discharges of domestic and industrial wastewater flowing into the Atoyac River. The Zapatero River (Z3) is 7.42 km long and runs through the municipality of San Andrés Cholula, crossing densely populated urban areas and flows into the Atoyac River. The Echeverria Dam, the fourth study area (Z4), is located between the municipalities of Ocoyucan and Puebla, at the end of the MAP, before the Atoyac River is dammed in the Manuel Ávila Camacho Dam. The San Francisco River was not studied because it was piped (Figure 1, Table 2), [14,20,25,28].

2.2. Characterization of Physical–Chemical Parameters in the Study Areas

Six water samples were collected from each of the rivers (Rabanillo and Zapatero) before they flowed into the Atoyac River, while six water samples were collected directly in each of the dams (Covadonga and Echeverría) (Figure 1). In situ and in triplicate, the parameters of water temperature and pH were determined with the help of a portable Orion No. 9107 marker, oxygen (Winkler method) using the HANNA® HI 3810 Oxygen Kit (DO). In each sample zone, 500 mL of water was taken in triplicate at different times of the day and then mixed to obtain a composite sample. With this composite sample, the chemical oxygen demand (COD) was quantified with a Spectroquant kit with the range of 25–1500 mg/L, the measurements were conducted using a Nova 60 Spectroquant Merck photometer. Turbidity and color measurement was carried out on the Nova 60 Spectroquant photometer. To measure the biochemical oxygen demand (BOD5), an OxiTop Control OC 100 incubator was used. Incubation time was for 5 days at 20 °C.

2.3. Determination of Heavy Metals, Arsenic, Cyanide, and VOCs

For the determination of heavy metals (chromium: Cr, cadmium: Cd, copper: Cu, nickel: Ni, lead: Pb, arsenic: As, and cyanide: CN), different kits/tests (Spectroquant) were used following the photometric method. In the analysis of volatile organic compounds (B: benzene, CB: chlorobenzene, CF: chloroform, 1,4 DB: 1,4-dichlorobenzene, 1,2 DE: 1,2-dichloroethane, and TE: trichloroethylene), the method established in the Official Mexican Standard NMX-AA-103-SCFI-2006 [29] was used. Volatile organic compounds (VOCs) were determined via coupled gas chromatography or a toxic constituent extraction product (PECT) mass spectrometer test method. The compounds analyzed via this method must have a boiling point below 200 °C and must be insoluble or scarcely soluble in water.

2.4. Industrial Inventory in the Study Areas

Data on industries were obtained from the National Statistical Directory of Economic Units (DENUE) [30]. The DENUE publishes the information automatically on the website of the National Institute of Statistics and Geography (INEGI) through a system that allows visualization of the establishments that are georeferenced in digital cartography and satellite images (Table 1).
Table
Table 1. Types of industries in the municipalities belonging to the MAP.
Table 1. Types of industries in the municipalities belonging to the MAP.
MunicipalitiesTypes of IndustriesSub-
Total
ConstMetallMet-WorkFoodTexPottery/GlassPlasticMinChemAutoPaper/CardbPaintPharmOthers
Cuautlancingo14103241011227-23262--233
Coronango29115-2----1-----309
San Pedro
Cholula		11391334126152110-11471-31411
San Andrés Cholula3413121184106-263131240
Puebla9799029719118715994875020431811112255
Ocoyucan523-38-73111---52
Total15801395383250225192144906763602214154500
Notes: Const = construction: cement and brick; Metall = metallurgy; Met-work = metalworking; Tex = textile; Min = mining; Chem = chemistry; Auto = automotive; Paper/card = paper/cardboard; Pharm = pharmaceutical; Others: cosmetic and steel industries.
The economic units present in the municipalities of Cuautlancingo, San Andrés Cholula, Coronango, San Pedro Cholula, Ocoyucan, and Puebla in the MAP were identified and quantified. They are large, medium, and small industries generating polluting waste due to their productive activity. Industrial parks and corridors were also located; however, the DENUE does not count the industries located in those places. Additionally, micro-enterprises such as blacksmith shops, textile workshops, and printing presses were taken into account. Micro-enterprises which, due to their clandestine condition, are not registered in the DENUE [30], as well as those which, due to their productive activity, do not generate pollutants, were not considered. The main lines identified were the construction, metallurgy, metalworking, food, textile, ceramics and glass, plastics, mining, chemical, automotive, paper and cardboard, paint, and pharmaceutical industries, among others (Table 1).

2.5. Determination of Industrial Density

Industrial density (ID) (Table 2) was calculated based on the information reported by DENUE [30], using the following formula:
I D = N A
where ID is the industrial density.
N represents the number of industries established in each municipality.
A represents the area where the industries are located in km2.
Table 2 shows the industrial density (ID) distributed by municipality. The study areas are shared by more than one municipality.
Table
Table 2. Industrial and population density of the hydrological watershed of the MAP.
Table 2. Industrial and population density of the hydrological watershed of the MAP.
StateMunicipalitiesSampling
Areas		* Coords.Area
(km2)		Number
of
Industries		** Industrial
Density		*** Number of Inhabitants
PueblaCuautlancingo1 Z1, Z219°08′15.33″ N
98°13′29.62″ W		38.12336.11137,435
CoronangoZ219°04′11.16″ N
98°14′58.76″ W		36.853098.3846,836
San Pedro CholulaZ219°04′11.16″ N
98°14′58.76″ W		76.9141118.34138,433
San Andrés CholulaZ319°03′23.5″ N
98°16′49.5″ W		63.22403.79154,448
Puebla2 Z419°01′07.6″ N
98°13′58.0″ W		535.322554.211,692,181
Ocoyucan2 Z419°01′07.6″ N
98°13′58.0″ W		119.8520.4342,669
Notes: 1 Covadonga and 2 Echeverría Dams. * Coordinates by study zone. ** Industrial density (industries/km2). *** INEGI, 2020.
Additionally, Table 3 was constructed and indicates the percentage of population growth between 1980 and 2020 and shows the evolution over time of population density between 1980 and 2020 [31]. Industrial modernity in the MAP began between 1970 and 1980 [32].
Table
Table 3. Population and its density in the municipalities of the MAP.
Table 3. Population and its density in the municipalities of the MAP.
McpPop.
1980		Density
(1980)		Pop.
(1990)		Density
(1990)		Pop.
(2000)		Density
(2000)		Pop.
(2010)		Density
(2010)		Pop.
(2020)
[INEGI]		Density
(2020)		Growth Percentage 1980–2020
CU18,768565.8129,047875.7046,7291408.7779,1532386.28137,4353607.21537.53%
CO15,627424.0720,576558.3727,575748.3034,596938.8346,8361270.99199.71%
SPC57,498744.9878,1771012.9199,7941293120,4591560.75138,4331800.16141.63%
SAC26,032442.7237,788642.6556,066953.50100,4391708.14154,4482443.79451.99%
OC13,783114.7017,708147.3723,619196.5625,720214.0442,669356.16210.51%
PUE835,7591534.481,054,4541936.021,346,9162472.991,539,8192827.171,692,1813161.18106%
Note: Mcp = municipality. CU = Cuautlancingo. CO = Coronango. SPC = San Pedro Cholula. SAC = San Andrés Cholula. OC = Ocoyucan. PUE = Puebla. Pop = population. Density = inhabitants/km2.

2.6. Cytotoxic Analysis in Allium Cepa by Study Area

The experiments were conducted in triplicates. In each study area, 12 bulbs of A. cepa were germinated in WW at different dilutions (25, 50, and 100%), for 120 h (acute treatment), with a change of the water every 24 h from each area, respectively. In the negative or control groups, the bulbs were exposed to drinking water. A total of 48 bulbs of A. cepa were used and 144 root tips were obtained. For each root tip, the chromosomal behavior during mitosis was analyzed.
At the end of the treatment, in each bulb, the roots were counted, and their length was measured with a digital Vernier (AVEDISTANTE). From each bulb, three roots were selected, cutting 2 mm from the apical meristem, fixed in an ethanol–acetic acid solution (3:1) for 24 h. They were dehydrated in ethanol 70% (v/v) and then hydrolyzed in HCl 5N. Staining was performed with aceto-orcein. The total number of meristematic cells studied was 48,000, and they were observed with the Axioplan II, Carl Zeiss, and LEICA CME microscopes. To determine the cytotoxic effects, mitotic index (MI), interphase index (II), and phase indices (PI, MeI, AI, and TI), 1000 cells were counted for each dilution of WW and were compared with the control group [33]. For this purpose, the following formulas were used:
Mitotic   index = Num .   of   cells   in   mitotic   division Total   num .   of   cells   observed ∗ 100
Interphase   index = Num .   of   cells   in   interphase Total   num .   of   cells   observed ∗ 100
Phase   index = Num .   of   cells   in   x   mitotic   phase Total   num .   of   cells   in   mitosis ∗ 100

2.7. Correlation Analysis

The Pearson correlation coefficient was estimated to obtain the statistical relationship between the variables. In each of the four sampling areas, the values of fifteen variables were correlated: four physicochemical parameters (BOD5, COD, turbidity, and O2), five heavy metals (Cd, Cu, Cr, Ni, and Pb) and six VOCs (B: benzene, CB: chlorobenzene, CF: chloroform, 1,4 DB: 1,4-dichlorobenzene, 1,2 DE: 1,2-dichloroethane, and TE: trichloroethylene) in relation to the MI of the 100% water sample (Table 4). Additionally, the general correlation matrix was constructed. In this matrix, the averages of the fifteen variables described above, obtained from each study area, were correlated with the average MI of the 100% water samples (Table 5). Correlation matrices were performed by calculating Pearson correlation coefficients with significance p ≤ 0.05, using Minitab 19 software.
Table
Table 4. Correlations between physicochemical variables, heavy metals and VOCs, and MI in each of the study areas.
Table 4. Correlations between physicochemical variables, heavy metals and VOCs, and MI in each of the study areas.
Study
Zones		Correlations
Covadonga Dam (Z1)Cu—COD 0.999Pb—COD 1.000MI—Cd
−0.991
Rabanillo River (Z2)Cd—O2
−0.999		TE—O2
−0.997		CF—turb
1.000		CF—COD, turb
0.975		MI—Pb, CB, TE
−0.931, −0.985, −1.000
Zapatero River (Z3)Pb—O2
−0.997		CF—O2
−0.999		Turb-BOD5
1.000		MI—Ni, TE
−0.999, −1.000
Echeverría Dam (Z4)TE—O2
−1.000		B—turb
−0.999		MI—1,4 DB
−1.000
Notes: Correlation matrix: Pearson’s coefficient, MI: mitotic index, BOD5: biological oxygen demand, COD: chemical oxygen demand, Tur: turbidity, B: benzene, CB: chlorobenzene, CF: chloroform, 1,4 DB: 1,4-dichlorobenzene, 1,2 DE: 1,2-dichloroethane, TE: trichloroethylene.
Table
Table 5. General correlation matrix in the MAP.
Table 5. General correlation matrix in the MAP.
O2BOD5CODTurbCdCuCrNiPbBCBCF1,4 DB1,2 DETE
BOD50.407
COD* −0.935* 0.659
Turb* −0.8420.0870.785
Cd−0.5710.484−0.251−0.587
Cu−0.5470.493−0.220−0.545* 0.999
Cr−0.0640.8780.264−0.2740.8430.848
Ni−0.6650.389−0.367−0.673* 0.992* 0.9860.782
Pb0.676−0.3170.4980.912−0.808−0.775−0.641−0.850
B−0.6870.362−0.395−0.689* 0.988* 0.9810.763* 1.000* −0.853
CB−0.6890.360−0.399−0.694* 0.987* 0.9800.762* 0.999−0.8581.000
CF−0.5910.394−0.268−0.503* 0.982* 0.9880.777* 0.973−0.705* 0.9710.968
1,4 DB−0.6450.380−0.336−0.603* 0.993* 0.9920.775* 0.994−0.787* 0.993* 0.992* 0.992
1,2 DE−0.6890.360−0.399−0.694* 0.987* 0.9800.762* 0.999−0.858* 1.0001.000* 0.968* 0.992
TE−0.6890.360−0.399−0.6940.987*0.9800.762* 0.999−0.858* 1.0001.000* 0.968* 0.9921.000
MI−0.777−0.390* −0.864* −0.9190.2270.179−0.1080.338* −0.6920.3600.3670.1470.2590.3670.367
Correlation matrix: Pearson’s coefficient. * Significant correlation: p < 0.05. MI: mitotic index, BOD5: biological oxygen demand, COD: chemical oxygen demand, Turb: turbidity, B: benzene, CB: chlorobenzene, CF: chloroform, 1,4 DB: 1,4-dichlorobenzene, 1,2 DE: 1,2-dichloroethane, TE: trichloroethylene.

2.8. Statistic Analysis

ANOVA was used to compare the variance between the means of the different dilutions in each study zone. The results were presented as the mean ± standard error of the mean. The means of the MI and II percentages of A. cepa were subjected to ANOVA and the Tukey test, p ≤ 0.05. Statistical analyses were performed using Minitab 19.

3. Results

In the MAP, there are a total of 4500 industries distributed in six municipalities that are crossed by the Atoyac River and its tributaries. The industrial activity diversified into the industrial branches of construction, metallurgy, metalworking, food, textile, pottery and glass, plastic, mining, chemical, automotive, paper and cardboard, paint, pharmaceutical, and others. The top five industries account for 35.11, 31, 8.51, 5.6, and 5% of total industries (Table 1). The ID was calculated, and this was higher in the municipality of San Pedro Cholula, with 18.34, followed by Coronango, with 8.38; Cuatlancingo, with 6.11; Puebla, with 4.21; San Andrés Cholula, with 3.91; and Ocoyucán, with 0.43 industries/km2. It was observed that of the four study areas, the Rabanillo River (Z2) is located in the municipalities with the highest industrial density, followed by the Echeverría Dam (Z4) located between the municipalities of Puebla and Ocoyucan (Table 2). The physical–chemical parameters showed that the pH values in Z1-Z3 ranged between 9.32 and 9.5 and are outside the maximum permissible limits (MPL) of the Official Mexican Standards (NOM): NOM-001-SEMARNAT-2021 [34], Ecological Water Quality Criteria (EC) [35], and the Declaration of classification of the Atoyac and Xochiac or Hueyapan Rivers and their tributaries. The Z4 had a pH of 7.17 and is within the MPL showing significant differences compared with the other sampling areas. The DO values were low (0.39–1.98 (mg/L).
Concerning BOD5 and COD, their values exceeded the MPL of the NOM in the sampling areas and presented significant differences. When analyzing the coefficient between BOD5 and COD values in each study area, the following values were obtained: 0.2, 0.3, 0.7, and 0.89, corresponding to the Rabanillo and Zapatero Rivers and the Echeverría and Covadonga Dams, respectively. The values indicate that industrial WW predominates in rivers and domestic WW in dams. In the sampling zones, Cd, Cu, Cr, Ni, Pb, As, and CN were identified, which exceeded the MPLs of the NOMs. The highest concentrations of As, Cd, CN, and Ni were present in the Z4, compared with the rest of the zones, and the differences were significant. The concentrations of Cu, Cr, and Pb in Z1, Z2, and Z4 showed significant differences with respect to NOMs. The concentrations of VOCs in Z1 and Z3 are similar to the MPLs established in NMX-AA-103-SCFI-2006 [29]. In Z2 and Z4, the levels of VOCs such as chloroform, vinyl chloride, 1–4 dichlorobenzene, hexachlorobutadiene, and trichloroethylene exceeded the MPLs established in the NOMs. Z4 exceeded the MPLs for benzene, chloroform, 1,2-dichloroethane, 1,1-dichloroethylene, tetrachloroethylene, and carbon tetrachloride. The rest of the compounds (chlorobenzene, hexachlorobenzene, methyl ethyl ketone, and pyridine) are found within the MPLs.
The cytotoxicity of water was evaluated in the four study areas using the biomodel A. cepa at different dilutions (Figure 2). The growth and number of roots (data not shown) decreased to the extent that the concentration of WW increased compared with the control group in all study areas. In Z2, the differences were significant. In the Covadonga Dam (Z1), in the treatment at 25% of the number of roots and their length and at 50%, the root length was greater compared with the control but not significant. In the Rabanillo River (Z2), at 100% concentration, there was no root growth (Figure 2). The coefficient of the number of cells (data not shown) undergoing mitosis (MI) decreased as the concentration of WW increased, while the number of interphase cells increased (II). The trend was similar in the growth and number of roots in the four study areas. The largest number of cells in mitotic division was presented at the prophase stage, while in the subsequent phases, the number of cells in division decreased, compared with their corresponding control in all four study areas.
The correlations of fifteen variables between physical, chemical, heavy metals, and VOCs were determined in relation to the cytotoxic effect generated in the meristematic tissue of A. Cepa in each of the four sampling zones. In the correlations, the values of the variables obtained at 100% were taken into account, since it represents the real concentration of the WW sample. The variables that were statistically significant are presented in Table 4. In the Covadonga Dam (Z1), a high correlation was observed (between the increases in COD, and Cu and Pb (0.999, p = 0.02 and 1.000, p = 0.005), respectively. Also, there was a correlation between the increase in Cd and the decrease in MI (−0.991, p = 0.006).
In the Rabanillo River (Z2), there was a high correlation between the decrease in O2 and the increase in Cd and trichloroethylene (−0.999, p = 0.023 and 0.997, p = 0.048). There was also a high correlation between the increase in COD and chloroform with respect to the increase in turbidity (0.975, p = 0.043). There was a correlation between the increases in Pb, chlorobenzene, and trichloroethylene (−0.931, p = 0.002; −0.985, p = 0.046; −1.000 p = 0.012) and the decrease in MI. In the Zapatero River (Z3), there was a correlation between the decrease in O2 and the increase in Pb and chloroform (−0.997, p = 0.049; −0.999, p = 0.034). Additionally, between the increase in BOD5 and turbidity (1.000, p = 0.012) and between the increase in Ni and trichloroethylene (−0.999, p = 0.020; −1.000, p = 0.006) and the decrease in MI. In the Echeverría Dam (Z4), there was a correlation between the decrease in O2 and the increase in trichloroethylene (−1.000; p = 0.019) and between the increase in turbidity and decrease in benzene (−0.999, p = 0.033). It also increased BOD5 by 1.4 DB (−1.000, p = 0.002) and decreased MI (Table 4).
From the average of the four correlations, in relation to the average of the MI, a general correlation matrix for the MAP was constructed (Table 5). The results showed that there is a high correlation between the decrease in O2 (−0.935, p = 0.045) and the increase in COD and turbidity (−0.842, p = 0.015). There was also a correlation between the increase in COD and BOD5 variables (0.659, p = 0.034). There was an evident correlation between the increase in turbidity, COD, and Pb (−0.919, p = 0.008; −0.864, p = 0.013; −0.692 p = 0.030) in relation to the decrease in MI (Table 5).

4. Discussion

Economic development, industrialization, and the implementation of economic models leading to a sustained increase in consumption have had a significant impact on the four study areas (Figure 1). We found severe contamination with the mixture of eighteen chemical substances, the values of which were constant and consistent throughout the watershed, most of them being carcinogenic [36,37,38,39,40,41], and surpassed MPLs by NOMs. These substances probably come from the manufacturing, transformation, use, cleaning, maintenance, or consumption processes generated by about 4500 industries (Table 1), among which include Cr, Ni, Cu, Cd, Pb, As, CN, and VOCs (chloroform, vinyl chloride, 1–4 dichlorobenzene, hexachlorobutadiene, trichloroethylene, benzene, chloroform, 1,2-dichloroethane, 1,1-dichloroethylene, tetrachloroethylene, and carbon tetrachloride). These findings show that industrial waste is dominated by the construction (35.11%), metallurgy (31%), metalworking (8.51%), food (5.6%), textile (5%), and ceramics and glass (4.3%) industries (Table 1). Other studies agree that these industries discharge their WW directly to the Atoyac River [8,21,27,42]. Regarding the presence of heavy metals and some VOCs, in the Atoyac River, they are in agreement with other investigations [12,43,44,45,46,47,48]. In addition, substances such as benzene, chloroform, toluene, and xylene in the Atoyac River have also been previously reported [19,48].
The physicochemical characterization of the WW showed that the values of COD and BOD5 exceeded the MPLs of the NOM in the sampling areas and indicates that the water resource in the watershed has reached its maximum load capacity, i.e., it is saturated. This implies that it cannot carry out its natural self-purification process, meaning that the degradation of organic matter and its incorporation into the ecosystem does not occur [20,49]. This behavior explains why the ecosystem has lost its capacity for self-regeneration, either due to the large amount and diversity of discharges and their origin, or due to its complex composition that exceeded the dilution capacity of the system itself. Further, subsequent degradation is not facilitated by the low or null concentration of DO, which ranged between 0.68 ± 0.08 and 0.39 ± 0.05 mg/L in the Covadonga (Z1) and Echeverría (Z4) Dams, where the MAP begins and ends, respectively. This condition precludes microbial activity coupled with the nature and size of the discharge, which implies that rivers are anoxic throughout their entire length [50,51,52,53,54]. This situation led to the increase in the level of turbidity in the environment, which ranged between 250.33 ± 6.02 and 100 ± 0.09 Nephelometric units (NTU), which correspond to the Rabanillo River (Z2) and the Echeverría Dam (Z4), respectively. According to the Official Mexican Standard NOM−127-SSA1-1994 [55], water is required to have 5 NTU for consumption. Therefore, both zones do not comply with the NOMs. Turbidity is a variable associated with population growth, urbanization, and industry [25,56]. As suggested previously, these conditions have a negative impact on biodiversity [57]. For instance, the absence of fish, as occurs in the MAP, is a clear example of the inability of the system to support adequate aquatic life [58,59]. In this regard, other studies in the area obtained similar turbidity values [18]. The pH value ranged between 7 and 9.5, indicating that the water is alkaline, which could be associated with a reduced rate of photosynthetic activity; domestic WW discharges (soap and detergents); and industrial activity, specifically, textile by dyeing, washing, and bleaching processes [20,60,61]. The pH values coincide with those obtained previously [21]. Finally, correlation analyses (Table 4 and Table 5) confirm that there is a high correlation between the decrease in O2 (−0.935, p = 0.045) and the increase in COD and turbidity (−0.842; p = 0.015), as well as between the increase in COD and BOD5 (0.659; p = 0.034).
The cytotoxic analysis showed that the mixture of eighteen chemicals found in this work is cytotoxic because of the inhibition of cell division, seen in the decreased MI and increased II in the apical meristematic tissue of the root of Allium cepa. This antimitotic effect resulted in the partial inhibition of root growth, as occurred in Z1, Z3, and Z4, or total inhibition in the Rabanillo River (Figure 2). Cell division may be inhibited, either by slowing the mitosis process or by cell death, as probably occurred in the Rabanillo River (Figure 2). This could be attributed to the complex mixture of heavy metals and VOCs, which could inhibit the activity of the factor that promotes mitosis [60,62] or altered ATP levels and thus reduce the dynamics and motility of chromosomes [63]. These results are consistent with previous studies [64,65], showing decreased MI with increasing doses of Di(2-ethylhexyl)phthalate, triclosan, propylparaben, and glyphosate.
The same trend was also observed in the phase index data analysis, where the highest percentage of dividing cells was observed at the prophase stage and decreased as the concentration of WW dilutions increased. These results suggest that the mixture of heavy metals and VOCs blocks the Cdk and cyclin A-B complexes that allow the normal passage of dividing cells from prophase to metaphase and anaphase [66]. The same behavior was reported previously in Allium cepa in the presence of a biocide and heavy metals [33,57]. It was also observed that, as the concentration of the treatments increased, the rates of the metaphase, anaphase, and telophase decreased. This may be due to high concentrations of Cr, Pb, Ni, and Cd, which do not allow cells to enter the subsequent mitotic phases and coincide with what was observed by [67,68,69] showing that the increase in Pb may inhibit or accelerate cell division in the root meristem. This was seen in the Rabanillo River (Z2) and Echeverría Dam (Z4), which presented high concentrations of Pb and As, and Cd, CN, and Ni, respectively, and where inhibition and decreases in the number and length of roots occurred (Figure 2) [70].
The correlation analysis in the Rabanillo River (Z2) confirms a decrease in MI in the roots of Allium cepa and is link to the increase in O2, Pb, Cd, CB, and TE (−0.998, −0.931, −0.995, −0.985, and −1.000 (p ≤ 0.05) (Table 4). Also, the general correlation analysis highlights the high correlation of some metals such as Cu, Cd, and Pb and some VOCs such as benzene, chlorobenzene, chloroform, 1,4-dichlorobenzene, 1,2-dichloroethane, and trichloroethylene with MI. Derived from the above, it was concluded that the greatest antimitotic effect was induced by the physicochemical variables turbidity, COD, and Pb (Table 5).
Of the four study areas, the most polluted were the Rabanillo River (Z2) and the Echeverría Dam (Z4). Since the Rabanillo River is located in the municipalities with the highest industrial density, which are San Pedro Cholula, Coronango, and Cuatlancingo, and the Echeverría Dam is located in the municipalities with the highest population density between Puebla and Ocoyucan, it is not surprising that the results of the coefficient between the BOD5 and COD values were 0.2 and 0.7, respectively, indicating that in the Rabanillo River, industrial WW predominates, while in the Echeverría Dam, domestic WW predominates. These results are also corroborated by the corresponding correlation (Table 4 and Table 5) and cytotoxic analyses in Allium cepa.
Water quality is the result of its physical, chemical, and biological properties. According to the NOM, the Environmental Protection Agency (EPA), and the correlations made, the water of the rivers in the MAP is not recommended for any type of use. In terms of environmental impact, the production and consumption of goods and services in the MAP has brought not only greater demand for the liquid but also greater generation of industrial and domestic WW. If the values of the parameters reported in zones 1 and 4 of the MAP in 2017 (21) are compared with those of the present investigation, the physicochemical parameters such as turbidity, DO, COD, and BOD5 were similar; however, metals showed an alarming increase. In Z1, the values of Ni, Pb, Cr, Cu, and Cd reported previously were 0.006, 0.008, 0.013, 0.006, and 0.002 µg/L and, in Z4, were 0.025, 0.028, 0.033, 0.019, and 0.002 µg/L, while in the present investigation, in Z1, the values were 0.19, 1.92, 0.20, 0.28, and 0.20 µg/L and, in Z4, were 2.30, 0.85, 0.70, 4.20, and 0.50 µg/L, respectively.
Additionally, the decomposition of organic waste produces biogases that are unpleasant because of not only the odors they generate but also the potential danger due to their toxicity. Some of them are also greenhouse gases that contribute to climate change, among which are carbon dioxide (CO2), methane (CH4), hydrogen sulfide (H2S), and VOCs (benzene and trichloroethylene). In addition, the decomposition of solid waste and its contact with water and soil can generate leachate, which represents a risk to human and other organisms’ health. The organic waste that is disposed of leads to the proliferation of harmful fauna and the transmission of diseases such as salmonellosis, amebiasis, and dysentery, among others [19]. The facts described and analyzed in this study show that the possibilities of achieving an economically optimal, socially fair, and environmentally sustainable use of the resource under current conditions are severely limited; therefore, it is important to implement new technologies in terms of pollutant absorption [71]. Given this scenario, water management represents one of the most important challenges in MAP.

5. Conclusions

The water of the Atoyac River in the MAP is toxic because it contains a mixture of 18 chemical substances such as heavy metals (5), arsenic, cyanide, and VOCs (11); thus, it cannot be drunk or used for essential activities such as agriculture. In addition, it is a source of insalubrity, which can cause and transmit diseases. Of the four study zones, the most contaminated in the MAP was the Rabanillo River, followed by the Echeverría Dam. This is more likely because the Rabanillo River is located in the municipalities with the highest industrial density (San Pedro Cholula, Coronango, and Cuautlancingo) and the Echeverría Dam is located in the municipality with the highest number of inhabitants and industries (Puebla). The greatest antimitotic effect was observed in the Rabanillo River and was induced more likely by the parameters of turbidity, COD, and Pb.
Consequently, urban rivers in the Atoyac watershed in the MAP have become potential vehicles for disease and environmental disruption. This is caused, on one hand, by changes in land use, accelerated and poorly planned demographic and industrial growth and, on the other hand, by the scarcity of wastewater treatment plants in the municipalities and industries, as well as lax enforcement of the Official Mexican Standards. The chemical pollution in the MAP, in historical terms, reflects environmental deterioration, the effects of which result in an unsustainable development process. Therefore, it is urgent to change the productive system, where knowledge of water quality is taken into account and coalition spaces between the public, private, and citizen sectors are created to implement a new industrial policy oriented towards inclusive and sustainable goals. The present research provides evidence of the serious state of disturbances in the bodies of water in the MAP. It is recommended to implement control and monitoring programs for municipal and industrial discharges, as well as to incorporate suitable secondary and tertiary treatment in wastewater treatment plants. In addition, the Official Mexican Standards for water quality need to be complied with to guarantee the health of the population and the ecosystem. The cleanup of aquifers is a joint responsibility of citizens, industry, and the government. Finally, the Atoyac River watershed is fundamental for the social and economic development of the region and the country. Only through efficient, equitable, and sustainable management would it be possible to achieve a balance between the health of aquatic ecosystems and human needs.

Author Contributions

A.H.-S. conceived the project, designed the experiments, and wrote the paper; A.C.C.-L. performed the experiments; W.A.G.-S., R.V.-Q., F.A.-F. and A.M.-B. finalized the data. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Vicerrectoría de Investigación y Estudios de Posgrado (VIEP) with code 100089811-VIEP 2022 of the Benemérita Universidad Autónoma de Puebla (BUAP).

Data Availability Statement

Not applicable.

Acknowledgments

Ana Cristina Covarrubias López thanks the National Council of Science and Technology (CONACYT) for the scholarship awarded (No. 781617). Open-access publishing costs were covered by VIEP and the Science Institute of BUAP.

Conflicts of Interest

The authors have no conflict of interest to declare.

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Figure 1. Hydrological watershed of the Atoyac River and tributaries in the MAP.
Figure 1. Hydrological watershed of the Atoyac River and tributaries in the MAP.
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Figure 2. Changes in root length of A. cepa at different concentrations of WW in the sampling areas of the MAP. (*) indicates a significant difference (Tukey test; p < 0.05).
Figure 2. Changes in root length of A. cepa at different concentrations of WW in the sampling areas of the MAP. (*) indicates a significant difference (Tukey test; p < 0.05).
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Covarrubias-López, A.C.; García-Suastegui, W.A.; Valencia-Quintana, R.; Avelino-Flores, F.; Méndez-Bermúdez, A.; Handal-Silva, A. Human Impact in the Watershed of the Atoyac River in the Metropolitan Area of Puebla, Mexico. Sustainability 2023, 15, 10565. https://doi.org/10.3390/su151310565

AMA Style

Covarrubias-López AC, García-Suastegui WA, Valencia-Quintana R, Avelino-Flores F, Méndez-Bermúdez A, Handal-Silva A. Human Impact in the Watershed of the Atoyac River in the Metropolitan Area of Puebla, Mexico. Sustainability. 2023; 15(13):10565. https://doi.org/10.3390/su151310565

Chicago/Turabian Style

Covarrubias-López, Ana Cristina, Wendy Argelia García-Suastegui, Rafael Valencia-Quintana, Fabiola Avelino-Flores, Aarón Méndez-Bermúdez, and Anabella Handal-Silva. 2023. "Human Impact in the Watershed of the Atoyac River in the Metropolitan Area of Puebla, Mexico" Sustainability 15, no. 13: 10565. https://doi.org/10.3390/su151310565

APA Style

Covarrubias-López, A. C., García-Suastegui, W. A., Valencia-Quintana, R., Avelino-Flores, F., Méndez-Bermúdez, A., & Handal-Silva, A. (2023). Human Impact in the Watershed of the Atoyac River in the Metropolitan Area of Puebla, Mexico. Sustainability, 15(13), 10565. https://doi.org/10.3390/su151310565

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