Journal of Ecology and Environment

pISSN 2287-8327 eISSN 2288-1220

QR Code

Article

Home Article View

Research

Published online July 17, 2024
https://doi.org/10.5141/jee.24.021

Journal of Ecology and Environment (2024) 48:24

Bioassessment of the quality of surface waters of the Chipoco River using indicators of epilithic diatoms in macrophytes from the mining district of Hidalgo, Mexico

María Jesús Puy-Alquiza1* , Raúl Miranda-Aviles1 , Yuriko Jocselin Martínez Hernández2 , Miren Yosune Miranda Puy3 , Gabriela A Zanor4 and Cristina Daniela Moncada Sanchez1

1Engineering Division, Department of Mines, Metallurgy and Geology, University of Guanajuato, Campus Guanajuato, Guanajuato 36000, Mexico
2Department of Marine and Coastal Sciences, Universidad Autooma de Baja California Sur, La Paz 23080, Mexico
3Department of Agrogenomic Sciences, National School of Higher Studies, Leon Unit, National Autonomous University of Mexico, Leon 3709, Mexico
4Department of Environmental Sciences, Life Sciences Division, University of Guanajuato, Campus Irapuato-Salamanca, Irapuato 3655, Mexico

Correspondence to:María Jesús Puy-Alquiza
E-mail yosune.puy155@gmail.com

Received: February 13, 2024; Revised: April 28, 2024; Accepted: June 8, 2024

This article is licensed under a Creative Commons Attribution (CC BY) 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ The publisher of this article is The Ecological Society of Korea in collaboration with The Korean Society of Limnology

Abstract

Go to

Background: In this research work, epilithic communities of diatoms in macrophytes are listed and described to evaluate the ecological conditions of the surface waters of the Chipoco River, whose basin has been exploited for agricultural and mining purposes, degrading natural ecosystems. The diatoms studied are found in calcareous tufa deposits developed in swampy environments where little of their benthic microbiota has been studied, despite the regional relevance of these calcareous formations within the manganese mining district. To describe the diatoms and evaluate the ecological condition of the surface waters, the Chipoco River was divided into three sectors (North, Center, and South) collecting a total of 15 samples along 10 km. For the taxonomic identification of diatoms, scanning electron microscopy techniques, consultations with specialists and specialized literature were used. To evaluate the ecological conditions of the Chipoco River, the linear correlation coefficient was used, where the relationships between diatom species and environmental variables were evaluated. Likewise, species diversity was determined by applying the Shannon–Wiener index and Simpson’s dominance value (D) was calculated to detect diversity impoverishment processes.
Results: Ten genera of diatoms were identified in bryophytes of the species Plagiomnium cuspidatum that grow on the banks of said river. The linear correlation coefficient indicated that physicochemical characteristics such as total dissolved solids, temperature, and calcium, and hydrochemical characteristics of the water intervene in the distribution and abundance of four diatoms Rhoicosphenia abreviate, Epithemia turgida, Calloneis bacillum and Achanthidium minutissimum in the different sectors studied. The Shannon–Wiener diversity indices and Simpson’s dominance show that there is greater diversity and marked dominance of diatoms in the northern sector compared to the central and southern sectors.
Conclusions: Agricultural and mining activities and the poor sanitary infrastructure of human settlements have caused the Chipoco River to have poor ecological quality.

Keywords: calcareous tufas, diatoms, ecological, Mexico, quality

Introduction

Go to

Diatoms are unicellular, eukaryotic, and photosynthetic organisms with unique microscopic algae containing silica and different geometric shapes. It is known that they form microbial mats and are produced in wet places where photosynthesis is possible. These photosynthetically active organisms are responsible for 20%–25% of total terrestrial primary production, and approximately 40% of annual marine biomass production (Field et al. 1998), making them the most dominant group of organisms sequestering carbon from the atmosphere. These microorganisms live generally in marine, freshwater, and terrestrial ecosystems, but few studies describe them in an ecosystem of swampy calcareous tufas (Ajuaba et al. 2021), fluvial tufas (Beraldi-Campesi et al. 2016), fluvio-lacustrine tufas (Sanz Rubio et al. 1996). Epilithic diatoms have been widely used as ecological bioindicators to assess water quality, since they respond rapidly to environmental changes, especially organic pollution, and eutrophication, with a wide spectrum of tolerance, from oligotrophic to eutrophic conditions (Álvarez-Blanco et al. 2013; Çelekli and Lekesiz 2020; Çelekli et al. 2019; Gutiérrez López 2023; Lobo 2013; Lobo et al. 2014, 2015; Rimet 2012). In Mexico, the study of diatom communities in lotic environments (springs, rivers, streams) has focused mainly on two regions (central region and southern region). In the central region, studies have been directed at river basins such as: Papaloapan river basin (Tavera et al. 1994), the Pánuco River Basin (Montejano-Zurita et al. 2004), Balsas River Basin (Bojorge-García et al. 2010, 2014), Antigua River Basin (Vázquez et al. 2011), Lerma Basin-Chapala (Abarca-Mejía 2010; Mora et al. 2017; Mora Hernández 2018; Segura-Garcia et al. 2016), the upper basin of the Laja river (Mora et al. 2015), basin of the Turbio river (Velázquez Bucio 2007). Most of these works have been carried out for floristic purposes, and although some of them include analysis of the structure of the communities, or indicate important aspects of the ecological preferences of the species, few studies are focused on their application as ecological bioindicators (Abarca-Mejía 2010; Carmona-Jiménez et al. 2016; Mora et al. 2015; Salinas Camarillo 2018; Vázquez et al. 2011). While in the Southern Region, karstic environments dominate, hosting a series of aquatic ecosystems with special geological characteristics derived from the dissolution of limestone rock, which give rise to the formation of calcareous tufa deposits. The study of the diversity of diatoms in these karstic environments is limited (Beraldi-Campesi et al. 2016), despite the abundance of said deposits and their distribution in a variety of aquatic environments in different regions of the world. Calcareous tufas is a sedimentary rock composed of calcium carbonate deposited as calcite, aragonite or dolomite. These deposits are formed mainly by the precipitation of calcium carbonate, associated with karst outcrops on the continent (Carcavilla et al. 2019). These deposits are generated in aquatic conditions related to carbonate aquifers that adopt different morphologies and contain micro and macrophytes that provide varied and complex habitats for a wide range of aquatic organisms (crustaceans, diatoms, cyanobacteria, bacteria, fungi, among others) (Arenas et al. 2010; Carcavilla et al. 2019; Ford and Pedley 1996; Pentecost 2005). In the study area, these deposits are distributed along the Chipoco River, where a great diversity of macrophytes can be observed that grow on the banks of said River. It is known that the diatoms can adhere to and colonize a wide variety of substrates, including aquatic plants, rocky substrates, and sediments (Ávila and García 2015; Montoya-Moreno and Aguirre-Ramírez 2008; Moreno and Aguirre 2013). Rock surfaces represent a higher attachment rate for diatom colonization as they provide greater surface area, substrate roughness, substrate stability, and nutrient availability on rocky substrates compared to the diatom attachment rate on plants, the latter present a less rough surface, plant movement, light interference, competition with other organisms and differences in chemical composition (García del Cura et al. 2012; Quintana Zagaceta 2021). Despite this, in the study area the macrophytes present along the Chipoco River provide a stable substrate and a humid microenvironment for the colonization of diatoms, potentially increasing the diversity and abundance of species since the macrophytes provide shelter, food, and favorable conditions for their growth and reproduction. The study of diatoms associated with macrophytes provides us with relevant information between the diatom and the surrounding habitat, this being one of the objectives of said research. Based on the above, the objective of this research work was: 1) to contribute to the knowledge of the floristic study of diatoms that inhabit bryophytes of the species Plagiomnium cuspidatum that grow on the calcareous tufa deposits on the banks of the Chipoco River; 2) to evaluate the ecological conditions of the surface waters of the Chipoco River, applying the linear correlation coefficient where the relationships between diatom species and environmental variables were evaluated, 3) to evaluate the quality of the water by applying biodiversity indices such as the Shannon– Weiner index and Simpson’s index which are commonly used as they provide quantitative measures of biological diversity and help determine the state of health of the aquatic ecosystem. The joint use of these indices allows us to obtain a more complete image of the conditions of the ecosystem. Dominance value (D) was calculated to detect diversity-impoverishing processes. These studies are essential to understand the dynamics of aquatic ecosystems, evaluate the quality of water and water resources for their conservation and sustainable management in a context of global environmental change.

Study area

The study area is located within the Manganesiferous District of Molango in the north-central sector of the state of Hidalgo and belongs to the municipality of Tlanchinol. The municipality of Tlanchinol is located in the Sierra Madre Oriental in the physiographic subprovince of the Huasteco karst, which consists of an area of folded mountain ranges made up of limestone with the development of canyons and the presence of sinkholes, wells and caves. It has an altitude range of 60 m above sea level to 2,445 m above sea level, located hydrologically in the basin of the Pánuco. The climate that predominates in most of the study area is cold mountain. The average temperature in summer is 29°C and a minimum of 5.5°C, with the average annual precipitation being 550 mm. River from which the sub-basins of the San Pedro River, the Los Hules River and the Amajac River are derived, in the latter there are twenty-eight localities, highlighting the town of Chipoco because it is one of the most populated and where the Chipoco River crosses. The Basin has been exploited for agricultural and mining purposes, degrading natural ecosystems. The Chipoco River has a significant importance in the region’s hydrological system as it plays a crucial role in supporting local ecosystems and rural communities. Its flow characteristics are of great relevance for the management and planning of the area’s water resources. The Chipoco River is a deteriorated system since it crosses several communities and is in turn influenced by the waste from the Minera company. Three sections of the Chipoco River were studied, the North sector located at 1,069 m altitude, at the coordinates (21°00´37´´ N-98°73´84´´ W), obtaining the sample M-3, the Central sector located at 1,000 m elevation, at the coordinates (20°98´10´´ N-98°72´29´´ W), obtaining the sample M-2, and the southern sector located at 1,100 m elevation, at the coordinates (20° 98´57´´ N-98°72´12 W´´), obtaining the samples (M-1) (Fig. 1).

Figure 1. Location of the study area.

Materials and Methods

Go to

Sampling of the calcareous tufa deposits

Four samples were obtained from the calcareous tuff deposits that emerge along the banks of the Chipoco River. These samples were analyzed using the X-ray diffraction analysis technique to know their mineral phases.

Sampling of water

Fifteen water samples were taken along the Chipoco River. Five were taken in the northern sector (M-3), five samples in the central sector (M-2), and five samples in the southern sector (M-1). The water sampling was carried out in the month of February and July of the year 2022. For the sampling, conservation, and handling of the samples, the Official Mexican NOM-230-SSA1-2002 was followed. The samples taken were placed in coolers with refrigerating bags or closed ice bags for transport to the laboratory, at a temperature between 4°C and 10°C, taking care not to freeze the samples.

Physical characteristics of water

The temperature was measured by a mercury thermometer with a precision of 1°C. The pH was determined by a potentiometer model 610A (Corning, New York, NY, USA). The electrical conductivity (EC) was measured by a Conductivity Meter 850037 Sper Scientific (Scottsdale, AZ, USA). The total dissolved solids (TDSs) were measured by a TDS PURIKOR PK-TDS3 (Irvine, CA, USA), and the water hardness was calculated based on the content of calcium and magnesium salts.

Chemical analysis of the water

The X-ray fluorescence technique and X-ray diffractometer were used to analyze metals. The analysis was carried out in the LICAMM laboratory, the Mining, Metallurgy, and Geology Department of the University of Guanajuato.

Mineral phases of the calcareous tufa deposits

To determine the mineral phases of the four samples obtained from the calcareous tufa deposits that emerge along the banks of the Chipoco River, the X-ray diffraction technique was applied using the Rigaku ULTIMA IV X-ray diffractometer with CuKα radiation. The XRD patterns were compared to data from the International Center for Diffraction Data powder diffraction archive to determine the phases present.

Sampling of macrophytes and vascular plants

Macrophytes encompass different groups of plant communities (bryophytes, microalgae and cyanobacteria). Its collection is easy due to its size and location in the body of water (banks). Bryophyte sampling was carried out qualitatively, including visual observation and collection of the most representative types of the study area, with the most common species being P. cuspidatum. The diatoms studied are found in the bryophyte samples. These bryophytes are found growing in calcareous tufas deposits of Holocene age that outcrop in the Chipoco River within the manganese district of Molango Hidalgo. The bryophytes samples were analyzed using petrographic and analysis and scanning electron microscope (SEM). For petrographic analysis, samples were cut into thin sections with a circular rock cutter and mounted on glass slides with epoxy resins. The samples were ground and polished with carbide shot to a thickness of 0.3 mm. The sections were then covered with glass slides so that the texture and minerals in the stone could be characterized by microscopic analysis. The identification and characterization of minerals were carried out using the BX41 petrographic microscope, using flat light as cross-polarized light. The morphological aspects of the bryophytes and vascular plant samples were investigated by SEM observation without any metallic coating. For this, the SEM, model (JSM-6010 PLUS/LA; JEOL, Tokyo, Japan), was used, which was operated at 15 kV in low vacuum, while the scanning spectrometer measured energy dispersion (EDS), attached to the SEM, was obtained for semiquantitative chemical analysis. All the analyzes were carried out in the LICAMM laboratory of the University of Guanajuato. For the identification of the bryophyte species, the Bryophyte manual was used (Claudio Delgadillo 1990).

Diatoms observation to the scanning electron microscope, classification

The morphological aspects of the diatom were investigated by (SEM) observation with gold coating. The SEM instrument (JSM-6010 PLUS/LA) was operated at 15 kV in a low vacuum, while the EDS, was attached to the SEM, and was used for semi-quantitative chemical analysis. The SEM-EDS analyses were carried out in the laboratory LICAMM of Guanajuato University. For its observation the protocol of (Round et al. 1990), was used, describing it below: 1) The sample was filtered with a filter that does not dissolve with organic solvent. 2) The filters were placed in suitable containers for drying at critical points. 3) Fixed with a 2.5% glutaraldehyde solution in 0.1 M phosphate buffer prepared with filtered seawater. 4) To remove the salts, the samples were transferred to decreasing concentrations of seawater. 5) After fixing it was dehydrated in a series of growing ethanol. 6) Finally, the sample was dried to the critical point in the desiccator. The taxonomic determination was made according to the criteria of Mora Hernández (2017), Salinas Camarillo (2018), and Bahls et al. (2018).

Analysis of the Shannon–Weiner index

The Shannon–Weiner diversity index is an index used to quantify biodiversity, which encompasses the richness of species and their components, determining the pollution status of a body of water. It is considered a good indicator of the impact that the environment has on species. The index shows the heterogeneity of a community taking into account two factors, the number of species present and their relative abundance. According to Margalef (1983), the Shannon–Weiner index varies from 1 to 5, interpreting values less than 2 as low diversity, from 2 to 3.5 medium and greater than 3.5 as high diversity.

To determine the Shannon–Weiner diversity index, equation 1 was applied.

H=∑ i=1spi×In(pi)

Where H is the Shannon–Weiner index; pi, is the total proportion of numbers of individuals; ln (pi) natural logarithm of pi.

The Simpson index (D)

The Simpson index (D) also known as the species diversity index or dominance index. It is one of the parameters that allows us to evaluate which species is found in the greatest proportion in a sample. It is actually an index of dominance and wealth. It is used from an ecological point of view to quantify the biodiversity of a habitat. The Simpson index represents the probability that individuals taken at random within a habitat belong to the same species. That is, the closer its value is to unity, the greater the possibility of dominance of a species or population. The closer the value is to zero, the greater the biodiversity of a habitat.

The formula for the Simpson index is represented in equation 2.

D=∑ i=1Sni(ni−1)N(N−1)

Where S is the number of species; N is the total number of organisms present (or square units); n is the number of specimens per species.

Statistical analysis

Descriptive analysis (RStudio version 3.6) was used to calculate the mean and standard deviation of the physicochemical variables of the sampling stations. Experimental data between sampling stations were compared using one-way ANOVA. Diatom-environment and environment correlations were computed using the linear correlation coefficient test to evaluate the relationships among species diversity, diatom indices, and environmental factors.

Results

Go to

Chemical characteristics of the calcareous tufa deposits

Table 1 shows the different mineralogical phases found in the calcareous tufa deposits studied. The dominant mineral phases are silicates (quartz [SiO2], and moganite [SiO2]), carbonates (calcite [CaCO3], and magnesian calcite [{Ca, Mg} CO3]). Moganite is a mineral that is part of chalcedony. The formation of chalcedony is linked to the existing pH in the medium, so the presence of chalcedony is justified in alkaline pH. Chalcedony in carbonate tufa deposits is found as a replacement material for calcite and/or dolomite and cementing pores. The presence of silica (SiO2) may be due to local geological and environmental conditions. Silica could be incorporated through the interaction of silica-rich rocks and water; it may also come from decomposing organic material such as diatoms or other organisms that contain silica in their structure. Other identified mineral phases are arsenates (wallkilldellite, hidalgoite), the chlorite group minerals (pennantite), and other phyllosilicates (muscovite, pyrosmalite-[Mn]). These mineral phases are associated with the Molango manganese deposit, which is considered a large-scale marine sedimentary deposit typical of the Kimmeridgian-Tithonian in Mexico. The calcareous tufa deposits were formed on the Chipoco Formation, where manganese enrichment occurs, hence the presence of mineral phases related to the manganese deposit.

Table 1 . X-ray diffraction.

SampleXRDXRD diffractogram
M1Quartz- SiO2
Moganite- SiO2
Calcite, magnesian (Ca, Mg) CO3
Pyrosmalite - (Mn) (Mn+2 Fe)8(Si6O15) (OH, Cl)10
Muscovite - (K, Na) (Al, Mg, Fe)2(Si3.1Al0.9) O10(OH)2
Hidalgoite - PbAl3(AsO4) (SO4) (OH)6
Pennantite-1MIIb - Mn5+2 Al (Si3Al) O10(OH)8
Wallkilldellite, (Ca, Mn)4 Mn6+2 As4O16(OH)8 x 18H2O
M2Calcite CaCO3
Calcite, magnesian (Ca, Mg) CO3
M3 and M4Calcite - CaCO3
Quartz - SiO2
Moganite - SiO2

Mineralogical phases of calcareous tufa deposits.

XRD: X-ray diffraction.

Physical and chemical characteristics of water

The physicochemical characteristics of the water are shown in Table 2. The water of the northern section (M-3) of the Chipoco River has a temperature of 24.5°C, classifying these waters as mesothermal. Regarding pH, the water had a pH of 7.9 (alkaline). The EC was 130 µs/cm, while the TDSs was 230 ppm. The hardness was 500 ppm, indicating the presence of hard water. The alkalinity was 240 while no chlorine concentrations were recorded. The central sector (M-2) presented a temperature of 22.1°C, classifying these waters as mesothermal. Regarding pH, the water had a pH of 8.2 (alkaline). The EC was 530 µs/cm, while the TDSs was 187 ppm. The hardness was 500 ppm, indicating the presence of hard water. The alkalinity was 120, no chlorine concentrations were recorded, the southern sector (M-1) presented a temperature of 22.1°C, classifying these waters as mesothermal. Regarding pH, the water had a pH of 8.2 (alkaline). The EC was 535 µs/cm, while the TDSs was 197 ppm. The hardness was 500 ppm, indicating the presence of hard water. The alkalinity was 120, no chlorine concentrations were recorded. According to the above, the surface waters of the Chipoco River were classified as calcium bicarbonate (Table 2). None of the three sectors presented the presence of nitrites and ammonium. High concentrations of Al, Mg, Ca, Cu, Sn, Cl, and S were observed in the central and southern sector of the Chipoco River, while in the northern sector of the Chipoco River the elements that present the highest concentrations were Al, Ca, Mg, and S.

Table 2 . Physicochemical characteristics of the samples obtained in the Chipoco River.

SamplesSouthern sector of the
Chipoco River (M-1)		Central sector of the
Chipoco River (M-2)		Northern sector of the
Chipoco River (M-3)
Coordenates20°98´57´´20°98´10´´21°00´37´´
98°72´12´´98°72´29´´98°73´84´´
Altitude (m)1,1001,0001,069
pH8.28.27.9
Temperature (°C)22.122.124.5
Alcalinity120120240
Hardness (ppm)500500500
Electrical conductivity (µs/cm)535530130
Total dissolved solids (ppm)197187230
CO2 (ppm)8.28.28.0
Chlorine (ppm)NDNDND
Na2O (%)NDNDND
MgO (%)42.939.8523.6
CaO (%)
K2O (%)0.1260.236.58
Al2O3 (%)0.650.450.98
SiO2 (%)24.222.49.92
20.619.9421.7
SO3 (%)25.7542.7450
NO3 (%)NDNDND
NH4 (%)NDNDND
P2O5 (%)12.59.38.39
Fe2O3 (%)15.6411.540.087
Si (ppm)1616.917.1
Na (ppm)NDNDND
Al (ppm)642763765
Mg (ppm)210235340
Ca (ppm)257259359
K (ppm)0.200.250.33
Cl (ppm)68.870.232.2
S (ppm)1,1901,1051,121
Cu (ppm)3.772.100.078
Sn (ppm)12.26.50.067

ND: not detected.

Bryohyte and diatom assemblages

The bryophyte species where the diatoms were observed corresponds to the P. cuspidatum species of the plagiomnium genus of the Mniaceae family. P. cuspidatum is characterized as a small moss with shoots 1.5–4 cm tall and leaves approximately 3 mm long (Wyatt and Odrzykoski 1998). The leaves of P. cuspidatum taper gradually towards the tip, more so than other species in the genus. The leaf margins have sharp teeth and are absent on the lower half of the leaves, while the midrib is seen. The leaves are arranged in pseudo whorls, where the leaf arrangement originates from different levels, its leaves are about 2.5 to 3.5 mm long (Fig. 2). Plagiomnium cuspidatum does not reproduce asexually, but is dioecious (having antheridia and archegonia on separate plants) and synoecious (having archegonia and antheridia on the same plant). From the foot of the plant, there may be multiple setae that raise the capsules above the plant. The capsules usually have a conical cap. The spores measure between 18 and 40 μm and are numerous within the capsule (Fig. 2). In the three sectors of the Chipoco River, a total of ten genera of diatoms were obtained (Amphora, Achnanthidium, Epithemia, Simonsenia, Rophadolia, Nitzschia, Rhoicosphenia, Pinnularia, Caloneis, and Cyclotella). All correspond to penal and central diatoms (Table 3). Among penal diatoms, all correspond to class Bacillariophyceae. The generated diatoms are presented in Figure 3. The northern sector of the Chipoco River presents a greater richness of diatoms specises compared to those of the central and southern sector, being the most abundant Rhoicosphenia abbreviata with 25.64% of specimens, Epithemia turgida with 18.31% of specimens, Caloneis bacillum with 14.65%. of specimens, Achnanthidium minutissimum with 9.15% of specimens and Rhopalodia gibberula with 7.32% of specimens. The central diatom is represented by the genus cyclotella sp. and is observed in northern sector, represented by the class coscinodiscophyceae, this genus represents only 2.56%. The most abundant species in the central and southern sector of the Chipoco River were R. abbreviata with 44.55% of specimens, E. turgida with 34.65% of specimens and A. minutissimum with 4.9% of specimens. Species were not observed C. bacillum, R. gibberula. and Cyclotella sp. Taking into account the above, the genera with the highest number of species in the three sectors of the Chipoco River were R. abbreviata (45 to 70 species), E. turgida (35 to 50 species), A. minutissimum (5 to 25) and C. bacillum (40 species), with cosmopolitan and fresh species dominating, and brackish water habitats. The Northern sector was characterized by species such as R. abbreviata, A. minutissimum, and Nitzschia linearis that preferred conditions of higher concentration of Ca.

Table 3 . Checklist of identified diatoms species of the Chipoco River studied and their abundance with respect to the total number of species.

TaxaIDHabitatNorthern Chipoco River (3a, 3b, 3c, 3d, 3e) (%)Central Chipoco River (2a, 2b, 2c, 2d, 2e) (%)Southern Chipoco River
(1a, 1b, 1c, 1d, 1e) (%)
Rhoicosphenia abbreviata (C. Agardh) Lange-Bertalot 19801FW25.6444.5543.25
Epithemia turgida (Ehrenberg)
Kützing 1844		1FW18.3134.6532.15
Caloneis bacillum (Grunow)
Cleve 1894		1FW/MB14.650.00.0
Achnanthidium minutissimum (Kützing) Czarnecki 19941FW9.154.94.7
Rhopalodia gibberula (Ehrenberg)
O. Müller 1895		1FW/M7.320.00.0
Amphora pediculus (Kützing)
Grunow in Schmidt 1875		1FW5.494.94.7
Pinnularia sp.1FW2.561.981.95
Amphora sp.1FW/M9.151.981.95
Nitzschia linearis Smith 18531FW/M2.564.94.7
Simonsenia delognei (Grunow)
Lange-Bertalot 1979		1FW/M2.561.981.95
Cyclotella sp. (Kützing) Brébisson 18381FW/M2.560.00.0

ID: 1 known cosmopolitan species; FW: freshwater; MB: marine brackish; M: marine.

Figure 2. (A-E, G) Plagiomnium cuspidatum, leaves with sharp teeth, the arrangement of the leaves originates at different levels. (F) Capsule and conical lid. (H, I) Diatoms on the leaf of P. cuspidatum.

Figure 3. Scanning electron microscope photographs of diatoms found in the Chipoco river. (A) Epithemia turgida (Ehrenberg) Kützing 1844. (B) Amphora pediculus, (C) Amphora sp., (D) Caloneis bacillum, (E) Achnanthidium minutissimum, (F) Simonsenia delognei, (G) Rhopalodia gibberula, (H) Nitzschia linearis, (I) Cyclotella sp., (J) Rhoicosphenia abbreviata, (K) Pinnularia sp.

Shannon–Wiener index (H´) and Simpson index (D)

The number of species (S) in the sampled sectors of the Chipoco River are shown in Table 4. The specific diversity measured through the Shannon–Wiener index (H’) presented the highest values in the northern sector compared to those of the central and southern sector (Table 4). The values of the Shannon–Wiener diversity index vary from 1.40 to 2.10, which means that there is greater diversity in the northern sector compared to the central and southern sectors. This may be due to the fact that the physicochemical conditions and the rocky substrate through which the water of the Chipoco River passes vary along the three sections studied. Regarding the Simpson index (D), it showed a behavior similar to the Shannon–Wiener index, in which the northern sector presented greater diversity and dominance than the other two sectors, since the value of the index (D) was closer to zero compared to the central and southern sector whose value is closer to 1. According to Potapova and Charles (2002), the distribution, richness and dominance of diatom communities is a result of the physicochemical factors of the water rather than of the factors geological or climatic, so water chemistry is considered the main element for the composition of species (Soininen et al. 2004). However, in this research, the behavior that the northern sector presents with respect to the central and southern sectors in terms of the diversity and dominance of diatoms is due to the conditions of the substrate (calcareous tufa deposits) that influence the physicochemical characteristics of the water, difference from the central and southern sectors, where the influence lies in the waste dumped by rural communities and nearby mines that cause a decrease in the diversity and dominance of diatoms.

Table 4 . Shannon–Weiner index (H) and Simpson index (D).

SampleSpeciesSpecific wealth (S)piH = pi × ln (pi)piΛ21/Σ piΛ2
Northern sector of
the Chipoco River (3a, 3b, 3c, 3d, 3e)		Rhoicosphenia abbreviata700.25–0.340.065
Epithemia turgida500.18–0.310.033
Caloneis bacillum400.14–0.280.021
Achnanthidium minutissimum250.09–0.210.008
Rhopalodia gibberula200.07–0.190.005
Amphora pediculus150.05–0.150.003
Amphora sp.250.09–0.210.008
Simonsenia delognei70.02–0.090.0006
Nitzschia lineari70.02–0.090.0006
Pinnularia sp.70.02–0.090.0006
Cyclotella sp.70.02–0.090.0006
Total112731H = 2.1050.1485D = 6.7319
Central sector of
the Chipoco River (2a, 2b, 2c, 2d, 2e)		Rhoicosphenia abbreviata570.42–0.360.17
Epithemia turgida390.28–0.350.08
Achnanthidium minutissimum100.07–0.190.005
Amphora pediculus70.05–0.150.002
Amphora sp.70.05–0.150.002
Simonsenia delognei50.03–0.120.001
Nitzschia lineari50.03–0.120.001
Pinnularia sp.50,03–0.120.001
Total81351H = 1.5880.276D = 3.613
Southern sector of
the Chipoco River (1a, 1b, 1c, 1d, 1e)		Rhoicosphenia abbreviata450.44–0.360.1985
Epithemia turgida350.34–0.360.120
Achnanthidium minutissimum50.04–0.140.002
Amphora pediculus50.04–0.140.002
Amphora sp.20.01–0.070.0003
Simonsenia delognei20.01–0.070.0003
Nitzschia lineari50.04–0.140.002
Pinnularia sp.20.01–0.070.0003
Total81011H = 1.400.3271D = 3.0569

Where H is the Shannon–Weiner index; pi, is the total proportion of numbers of individuals; ln (pi) natural logarithm of pi.

Diatom assemblages environment relationships

Table 5 and Figure 4, shows the data obtained from the statistical analysis. According to the linear correlation coefficient between the physicochemical variables and their relationship with the abundance of diatoms, it is observed that in all sectors there is a positive correlation between TDSs, temperature, and calcium, with the abundance of four species of diatoms. Rhoicosphenia abbreviata, E. turgida, Calloneis bacillum, and Achanthidium minutissimum, so these physicochemical variables are optimal for the growth and reproduction of these species. The negative correlation is observed with the parameters of EC, magnesium, P205, and pH where R. abbreviata, E. turgida, C. bacillum, and A. minutissimum, decrease in abundance and distribution.

Table 5 . Descriptive analysis (RStudio version 3.6) and ANOVA.

Diatoms
North sector
Linear coeficient of correlationS1S2S3S4
pH■■■■
Temperature (°C)●●●●
Electrical conductivity■■■■
Total disolved solids●●●●
Calcium●●●●
Magnesium■■■■
P205■■■■
Center sector
Linear coeficient of correlationS1S2S3S4
pH■■■■
Temperature (°C)●●●●
Electrical conductivity■■■■
Total disolved solids●●●●
Calcium●●●●
Magnesium■■■■
P205■■■■
South sector
Linear coeficient of correlationS1S2S3S4
pH■■■■
Temperature (°C)●●●●
Electrical conductivity■■■■
Total disolved solids●●●●
Calcium●●●●
Magnesium■■■■
P205■■■■

S1: Rhoicosphenia abbreviata; S2: Epithemia turgida; S3: Calloneis bacillum; S4: Achnanthidium minutissimum diatoms.

●: positive linear correlation coefficient; ■: negative linear correlation coefficient.

Figure 4. Positive correlation between total dissolved solids, temperature, and calcium, with the abundance of four species of diatoms. S1: Rhoicosphenia abbreviata, S2: Epithemia turgida, S3: Calloneis bacillum, S4: Achnanthidium minutissimum.

Discussion

Go to

The mining district of Molango, Hidalgo, has several bodies of water such as the Chipoco River, which runs through calcareous tufa deposits linked to the nature of the karst aquifers that dominate the region. The water flows generated by the calcareous tufa deposits come from karst masses that influence the type of water and in turn the diversity and composition of macrophytes (Merz-Preiß and Riding 1999; Pentecost 2005; Pentecost and Zhaohui 2002). In the case study, the waters of the Chipoco River are classified as calcium bicarbonate waters, which derive from the dissolution of the substrate through which the water flows. This substrate is made up of calcareous tufa deposits of Holocene age, its main mineral component being calcium carbonate. These waters have a low level of nutrients to stimulate photosynthesis, but despite this the variety and diversity of its flora is high. Macrophytes, specifically bryophytes of the species P. cuspidatum, grow on the calcareous tufa deposits, housing in their structure a diversity of penal and central diatoms. In the surface waters of the Chipoco River, diatoms proliferate due to sunlight, carbon dioxide and nutrients found in macrophytes. From the hydro- chemical point of view, the studied sectors of the Chipoco River are well differentiated, establishing two groups, the first corresponds to the northern sector, enriched by calcium ions, and bicarbonates which are provided by the basement in which limestone, shale predominate. and dolomites, without direct influence of inorganic waste, since it is located away from mine discharges and communities. The low EC (130 µs/cm) shows low values of metal ions, while the second group (Central and South sector) is enriched by metal ions such as copper (Cu) and tin (Sn), and therefore carbonates, which are provided by the mines and the rocky basement that characterizes the manganese deposit. This group is impacted by inorganic and mining waste, its EC is high (530 µs/cm), evidenced by metallic contaminants and dissolved salts. With respect to the Hydrogen Potential, the north sector presented a pH of 7.9, moderately basic influenced by an alkaline terrain (rich in Ca2C03) through which the effluents pass, while the central and south sector, the pH is 8.2, considered basic, decreasing the availability of phosphorus and boron. Regarding the chemical elements, in none of the three sections were nitrites and ammonium observed, which represents well-oxygenated waters (Wetzel 2001). High concentrations of Al, Mg, Ca, Cu, Sn, Cl, and S were observed, in the central and southern section of the Chipoco River, derived from the chemical composition of the rock (calcareous tufas) and by the dumping of waste and acid water from the mines. While in the northern sector of the Chipoco River the elements that present the highest concentrations are Al, Ca, and Mg derived from the chemistry of the rock (limestone, shale and dolomite). These differences were reflected in the groups of diatom species present in the bryophytes that grow on the banks of the river, observing that in the central and southern sectors the diatomological flora was more alkaliphilic in nature since they developed in high pH environments (8.2) compared to those of the north sector. The high richness of diatom species found in the northern sector of the Chipoco River could be due to several factors such as the variety of macrophytes and vascular plants found on the banks of said river, as well as the physicochemical conditions of the water and hydro-chemical conditions of the substrate. The least wealth is shown in the central and southern sector of the Chipoco River, probably due to the pollution it presents due to the dumping of waste from the urbanization process of the communities and acidic waters from the mines. Regarding the identified diatoms, these respond to the concentration of major ions, observing a flora related to environments rich in Ca and Mg represented by R. abbreviata, Amphora pediculus, and A. minutissimum, similar to that reported by Gasse (1986), Patrick and Reimer (1966), and Martínez de Fabricius et al. (2003). While in the central and south sectors, diatoms of the species C. bacillum, R. gibberula, and Cyclotella sp. were not observed. The species R. abbreviata and Nitzschia lineari were observed in the three sections of the Chipoco River; these diatoms have been reported as sensitive to contamination by (Cox 1996; Krammer and Lange-Bertalot 2004). The presence of these diatoms along the Chipoco River may be due, according to Montoya and Espinoza (1985), to transforming organic matter into inorganic salts (nitrates, phosphates and sulfates, which are easily absorbed by algae and macrophytes, causing a significant increase in its biomass in water bodies. Something interesting to observe is that the species C. bacillum was the only species that presents a perfect linear correlation with the variables of temperature and calcium, being dominant in the northern sector, since in the sector center and south was not identified, this indicates that the hydrochemical characteristics of the water in the northern sector are more favorable than in the other two sectors. The dominance of C. bacillum, has also been reported in Lake Tanganyka (Cocquyt 1999), in upper Dilimi River (Ali et al. 2015), and Red Sea hills in north-eastern Sudan (Compère 1984), where they mention that C. bacillum, is alkaliphilous mainly occurring in fresh brackish waters with pH > 7, and chloride levels < 500 ppm (Van Dam et al. 1994). Likewise, the presence of C. bacillum in the North sector indicates that said sector is beginning to be influenced by agricultural activity, since taking into account Reynolds (1996), said taxa is closely related to environments that present intense agricultural activity.

Conclusions

Go to

Rivers are complex systems in which some environmental factors vary in time and space due to certain factors such as climatic conditions, geomorphological characteristics of the basin, geological diversity, anthropological influence, which together intervene in the richness and distribution of diatoms. In the area studied, ten genera of diatoms were identified that were found in bryophytes of the species P. cuspidatum that grew on the banks of said river. They correspond to pennate and central diatoms. Of the pennate type, the most abundant genera were Amphora, Achnanthidium, Epithemia, Simonsenia, Nitzschia, Rhoicosphenia, and Pinnularia. Of the central type, the most abundant genera were Cyclotella. Throughout the study, the constant presence of a group of eight species R. abbreviata, E. turgida, A.minutissimum, A. pediculus was highlighted; Amphora sp., Simonsenia delognei, Nitzschia lineari, Pinnularia sp. The presence of pollution tolerant diatoms such as R. abbreviata, A. minutissimum, and Nitzschia lineari were observed in all sections of the Chipoco River, which agrees with what was reported by (Cattaneo et al. 1998; Lobo et al. 2004; Sabater 2000). The abundance and richness of diatoms along the three sectors of the Chipoco River may be influenced by the physicochemical and hydro-chemical characteristics of the water, by the presence of organic matter (bryophytes and vascular plants), the nature of the substrate, agricultural activities, and by the waste that comes from surrounding communities and mines. In the northern sector, diversity and dominance is governed by physicochemical factors, the nature of the substrate and agricultural activities, while in the central and southern sectors it is conditioned by waste that comes from surrounding communities and mines, which alter the hydro-morphology of the river, and its hydro-chemical condition. The diatom taxa present reflected the deterioration of water quality conditioned by socioeconomic activities (agriculture, mining), and urbanization, showing a gradual decrease in diversity, number of species and dominance.

Authors’ contributions

Go to

MJPA conceived of the presented idea, wrote the manuscript. RMA drafted the manuscript and designed the figures. YJMH analysed the data. MYMP analysis of the results. GAZ contributed to sample preparation. CDMS contributed to sample preparation. All authors discussed the results and commented on the manuscript.

References

Go to
  1. Abarca-Mejía NC. Diatom community analysis and quality assessment of the polluted tropical Lerma River (Mexico) [PhD dissertation]. Berlin: Freie Universität Berlin; 2010.
  2. Ajuaba S, Arenas C, Capezzuoli E. Sedimentology of Pleistocene palustrine tufas and associated deposits of the Ebrón Valley (Iberian Ranges, Spain). Estud Geol. 2021;77(1):e137. https://doi.org/10.3989/egeol.44131.593.
    CrossRef
  3. Ali AD, Ezra AG, Abdul SD. Species composition and distribution of freshwater diatoms from upper Dilimi River, Jos, Nigeria. IOSR J Pharm Biol Sci. 2015;10(5):53-60.
  4. Álvarez-Blanco I, Blanco S, Cejudo-Figueiras C, Bécares E. The Duero Diatom Index (DDI) for river water quality assessment in NW Spain: design and validation. Environ Monit Assess. 2013;185(1):969-81. https://doi.org/10.1007/s10661-012-2607-z.
    Pubmed CrossRef
  5. Arenas C, Osácar C, Sancho C, Vázquez-Urbez M, Auqué L, Pardo G. Seasonal record from recent fluvial tufa deposits (Monasterio de Piedra, NE Spain): sedimentological and stable isotope data. Geol Soc Lond Spec Publ. 2010;336(1):119-42. https://doi.org/10.1144/SP336.7.
    CrossRef
  6. Ávila FJO, García GM. Phycoperiphyton associated to macrophytes in the swamp of Cerro San Antonio, Magdalena-Colombia. Intropica Rev Inst Investig Trop. 2015;10(1):74-83.
    CrossRef
  7. Bahls L, Boynton B, Johnston B. Atlas of diatoms (Bacillariophyta) from diverse habitats in remote regions of western Canada. . PhytoKeys. 2018;105:1-186. https://doi.org/10.3897/phytokeys.105.23806.
    Pubmed KoreaMed CrossRef
  8. Beraldi-Campesi H, Arenas-Abad C, Auque-Sanz L, Vázquez-Urbez M, Pardo-Tirapu G. Benthic diatoms on fluvial tufas of the Mesa River, Iberian Range, Spain. Hidrobiológica. 2016;26(2):283-97.
    CrossRef
  9. Bojorge-García M, Carmona J, Beltrán Y, Cartajena M. Temporal and spatial distribution of macroalgal communities of mountain streams in Valle de Bravo Basin, central Mexico. Hydrobiologia. 2010;641:159-69. https://doi.org/10.1007/s10750-009-0074-5.
    CrossRef
  10. Bojorge-García M, Carmona J, Ramírez R. Species richness and diversity of benthic diatom communities in tropical mountain streams of Mexico. Inland Waters. 2014;4(3):279-92. https://doi.org/10.5268/IW-4.3.568.
    CrossRef
  11. Carcavilla L, Vegas J, Cabrera AM. [Establishment of a specific typology of tuff formations. Madrid: Ministerio para la Transición Ecológica; 2019. p. 20.
  12. Carmona-Jiménez J, Ramírez-Rodríguez R, Bojorge-García MG, González Hidalgo B, Cantoral-Uriza EA. [Study of the indicator value of benthic algal communities: a proposal for evaluation and application in the Magdalena River, Mexico City]. Rev Int Contam Ambient. 2016;32(2):139-52. Spanish.
    CrossRef
  13. Cattaneo A, Asioli A, Comoli P, Manca M. Organisms' response in a chronically polluted lake supports hypothesized link between stress and size. Limnol Oceanogr. 1998;43(8):1938-43. https://doi.org/10.4319/lo.1998.43.8.1938.
    CrossRef
  14. Çelekli A, Lekesiz Ö. Eco-assessment of West Mediterranean basin's rivers (Turkey) using diatom metrics and multivariate approaches. Environ Sci Pollut Res Int. 2020;27(22):27796-806. https://doi.org/10.1007/s11356-020-09140-1.
    Pubmed CrossRef
  15. Çelekli A, Toudjani AA, Gümüş EY, Kayhan S, Lekesiz HÖ, Çetin T. Determination of trophic weight and indicator values of diatoms in Turkish running waters for water quality assessment. Turk J Bot. 2019;43(1):90-101. https://doi.org/10.3906/bot-1704-40.
    CrossRef
  16. Claudio Delgadillo M; Ma Ángeles Cárdenas S. [Bryophyte manual]. 2nd ed. Mexico City: Universidad Nacional Autónoma de México; 1990. Spanish.
  17. Cocquyt C. Diatoms from a hot spring in Lake Tanganyika. Nova Hedwig. 1999;68(3):425-39. https://doi.org/10.1127/nova.hedwigia/68/1999/425.
    CrossRef
  18. Compère P. In: Dumont HJ, el Moghraby AI, Desougi LA, editors. Limnology and marine biology in the Sudan. Dordrecht: Springer; 1984. p. 61-77.
    CrossRef
  19. Cox EJ. Identification of freshwater diatoms from live material. London: Chapman & Hall; 1996.
  20. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science. 1998;281(5374):237-40. https://doi.org/10.1126/science.281.5374.237.
    Pubmed CrossRef
  21. Ford TD, Pedley HM. A review of tufa and travertine deposits of the world. Earth Sci Rev. 1996;41(3-4):117-75. https://doi.org/10.1016/S0012-8252(96)00030-X.
    CrossRef
  22. García del Cura M, Sanz Montero ME, Ríos ADL, Ascaso C. Biofilms, textures and isotope signatures in recent and ancient travertines Alhama de Almería-Alicún (Province de Almería, Spain). Geotemas. 2012;13:84-8.
  23. Gasse F. East African diatoms: taxonomy, ecological distribution. Berlin: J. Cramer; 1986. p. 203.
    CrossRef
  24. Gutiérrez López Á. [Analysis of the quality of the water of rivers and reservoirs in the northeast of the province of Huelva based on the use of diatoms as bioindicators] [thesis]. Andalucía: Universidad Internacional de Andalucía; 2023. Spanish.
  25. Krammer K, Lange-Bertalot H. Süswasserflora von Mitteleuropa, Bd. February 4: Bacillariophyceae: Part 4: Achnanthaceae, Kritische Ergänzungen zu Achnanthes s.l., Navicula s.str., Gomphonema, Gesamtliteraturverzeichnis Part 1-4, Ergänzter Nachdruck. Heidelberg: Spektrum Akademischer Verlag; 2004. German.
  26. Lobo EA. In: Schwarzbold A, Burliga AL, Torgan LC, editors. Ecologia del perifiton. São Carlos: RiMa; 2013. p. 205-33. Portuguese.
  27. Lobo EA, Callegaro VLM, Hermany G, Bes D, Wetzel CA, Oliveira MA. Use of epilithic diatoms as bioindicators from loticsystems in southern Brazil, with special emphasis oneutrophication. Acta Limnol Bras. 2004;16(1):25-40.
  28. Lobo EA, Schuch M, Heinrich CG, da Costa AB, Düpont A, Wetzel CE, et al. Development of the Trophic Water Quality Index (TWQI) for subtropical temperate Brazilian lotic systems. Environ Monit Assess. 2015;187(6):354. https://doi.org/10.1007/s10661-015-4586-3.
    Pubmed CrossRef
  29. Lobo EA, Wetzel CE, Schuch M, Ector L. [Epilithic diatoms as indicators of water quality in Brazilian subtropical lotic systems]. Santa Cruz do Sul: Edunisc; 2014. Portuguese.
  30. Margalef R. [Limnology]. Barcelona: Ediciones Omega; 1983. p. 1010. Spanish.
  31. Martínez de Fabricius AL, Maidana N, Gómez N, Sabater S. Distribution patterns of benthic diatoms in a Pampean river exposed to seasonal floods: the Cuarto River (Argentina). Biodivers Conserv. 2003;12:2443-54. https://doi.org/10.1023/A:1025857715437.
    CrossRef
  32. Merz-Preiß M, Riding R. Cyanobacterial tufa calcification in two freshwater streams: ambient environment, chemical thresholds and biological processes. Sediment Geol. 1999;126(1-4):103-24. https://doi.org/10.1016/S0037-0738(99)00035-4.
    CrossRef
  33. Montejano-Zurita G, Cantoral-Uriza EA, Carmona-Jiménez J. In: Luna I, Morrone JJ, Espinosa D, editors. [Biodiversity of the Sierra Madre Oriental]. F: Universidad Nacional Autónoma de México; 2004. p. 111-26. Spanish.
  34. Montoya H, Espinoza J. [Algae from the Ventanilla oxidation lagoons, Callao, Peru]. Boletín de Lima. 1985;42(1):41-68. Spanish.
  35. Montoya-Moreno Y, Aguirre-Ramírez N. Periphytic algae assemblage in macrophyte roots in a Colombian tropical wetland. Hidrobiológica. 2008;18(3):189-98.
  36. Mora D, Carmona J, Cantoral-Uriza EA. Epilithic diatoms in the upper Laja River Basin, Guanajuato, Mexico. Rev Mex Biodivers. 2015;86(4):1024-40.
    CrossRef
  37. Mora D, Carmona J, Jahn R, Zimmermann J, Abarca N. Epilithic diatom communities of selected streams from the Lerma-Chapala Basin, Central Mexico, with the description of two new species. PhytoKeys. 2017;88:39-69. https://doi.org/10.3897/phytokeys.88.14612.
    Pubmed KoreaMed CrossRef
  38. Mora Hernández LD. An integrative approach to epilithic diatom diversity analysis in tropical streams from the Lerma-Chapala Basin, Central Mexico [PhD dissertation]. Berlin: Freie Universität Berlin; 2017.
  39. Moreno YM, Aguirre N. Dynamics of epiphytic algae assemblage in ayapel flood plain through flood pulse. Rev UDCA Actual Divulg Cient. 2013;16(2):491-500. https://doi.org/10.31910/rudca.v16.n2.2013.923.
    CrossRef
  40. Patrick R, Reimer CW. The diatoms of the United States, exclusive of Alaska and Hawaii. Philadelphia: Academy of Natural Sciences of Philadelphia; 1966. p. 668.
    CrossRef
  41. Pentecost A, Zhaohui Z. Bryophytes from some travertine-depositing sites in France and the U.K.: relationships with climate and water chemistry. J Bryol. 2002;24(3):233-41. https://doi.org/10.1179/037366802125001402.
    CrossRef
  42. Pentecost A. Travertine. Dordrecht: Springer Science Business Media; 2005. p. 445.
  43. Potapova MG, Charles DF. Benthic diatoms in USA rivers: distributions along spatial and environmental gradients. J Biogeogr. 2002;29(2):167-87. https://doi.org/10.1046/j.1365-2699.2002.00668.x.
    CrossRef
  44. Quintana Zagaceta CH. [The use of Diatoms as an indicator of changes environmental in sediments from Lake Yanacocha (Cuzco, Peru) during the late Holocene] [Bachelor thesis]. Lima: Universidad Nacional Agraria La Molina; 2021. Spanish.
  45. Reynolds CS. Algae. In: Petts GE, Calow P, editors. River biota: diversity and dynamics. Oxford: Blackwell Science; 1996. p. 257.
  46. Rimet F. Diatoms: an ecoregional indicator of nutrients, organic matter and micropollutants pollution [PhD dissertation]. Grenoble: Universidad de Grenoble; 2012.
  47. Round FE, Crawford RM, Mann DG. The Diatoms: biology and morphology of the genera. Cambridge: Cambridge University Press; 1990. 747 p.
  48. Sabater S. Diatom communities as indicators of environmental stress in the Guadiamar River, S-W. Spain, following a major mine tailings spill. J Appl Phycol. 2000;12:113-24. https://doi.org/10.1023/A:1008197411815.
    CrossRef
  49. Salinas Camarillo VH. Las diatomeas indicadoras de la calidad ecológica en ríos de la Cuenca de México [Thesis]. Mexico City: Universidad Nacional Autónoma de México; 2018.
  50. Sanz Rubio E, Hoyos M, Cañaveras JC, Sánchez Moral S, Calvo JP. Sedimentological characterization of Upper Miocene-Pliocene fluviolacustrine and tuffaceous systems of the Calatayud Basin (Zaragoza). Geogaceta. 1996;2(2):277-80.
  51. Segura-Garcia V, Almanza Alvarez JS, Ponce-Saavedra J. Diversity of epilithic diatoms communities related to physico-chemical parameters in the headwaters of the Zinapécuaro River, Mexico. Hidrobiológica. 2016;26(2):187-202.
    CrossRef
  52. Soininen J, Paavola R, Muotka T. Benthic diatom communities in boreal streams: community structure in relation to environmental and spatial gradients. Ecography. 2004;27(3):330-42. https://doi.org/10.1111/j.0906-7590.2004.03749.x.
    CrossRef
  53. Tavera R, Elster J, Marvan P. Diatoms from Papaloapan basin communities, Mexico. Algol Stud. 1994;74:35-65. https://doi.org/10.1127/algol_stud/74/1994/35.
    CrossRef
  54. Van Dam H, Mertens A, Sinkeldam J. A coded checklist and ecological indicator values of freshwater diatoms from The Netherlands. Neth J Aquat Ecol. 1994;28(1):117-33. https://doi.org/10.1007/BF02334251.
    CrossRef
  55. Vázquez G, Aké-Castillo JA, Favila ME. Algal assemblages and their relationship with water quality in tropical Mexican streams with different land uses. Hydrobiologia. 2011;667:173-89. https://doi.org/10.1007/s10750-011-0633-4.
    CrossRef
  56. Velázquez Bucio M, Israde Alcántara I. Paper presented at: Ecología y Manejo de Ecosistemas Acuáticos en Michoacán; 2006 Nov 26-30; Morelia, Mexico. Morelia: SCME; 2006. p. 46. 2007.
  57. Wetzel RG. Limnology: lake and river ecosystems. 3rd ed. San Diego: Academic Press; 2001.
  58. Wyatt R, Odrzykoski IJ. On the origins of the allopolyploid moss Plagiomnium cuspidatum. Bryologist. 1998;101(2):263-71. https://doi.org/10.2307/3244203.
    CrossRef

Stats or Metrics

Share this article on

Related articles in JEE

  • There is No Related Article.

  • Privacy Policy
  • Terms of Use
  • Refund Policy
This journal was supported by the Korean Federation of Science and Technology Societies Grant funded
by the Korean Government (Ministry of Education).
Business Registration) 205-82-04820 / Representative) Young-han Yoo
Close ✕

Journal of Ecology and Environment

pISSN 2287-8327 eISSN 2288-1220