International Journal of Environmental Science and Technology (2022) 19:1091–1104

https://doi.org/10.1007/s13762-021-03186-5

ORIGINAL PAPER

Evaluation of the bioaccumulation of heavy metals and 137Cs

in succulent plants Echeveria elegans
H. B. Ortiz‑Oliveros1   · D. Cruz2 · R. M. Flores‑Espinosa3 · I. Santillán‑Malaquías4 · G. Zarazúa‑Ortega5 · A. Villalva4

Received: 10 October 2020 / Revised: 9 January 2021 / Accepted: 28 January 2021 / Published online: 13 February 2021
© Islamic Azad University (IAU) 2021

Abstract
In this work, the bioaccumulation of metals and 137Cs in the Echeveria elegans plant is evaluated. This is a semidesert plant,
a highly adaptable and complex metabolism that is used extensively in urban gardens and green walls in urban centers. To
determine the accumulation potential, the root accumulation factor (RAF) and shoot accumulation factor (SAF) were used,
the transfer of metals from the root to the shoots was determined with the translocation factor (TF). Soil samples were
enriched with 80, 120, 250, and 320 mg/kg of ­CsNO3 to simulate the retention of 137Cs. The quantitative analysis in the
shoots and roots showed that the metals that present an RAF > 1 were Cu > Fe > Zn > Ni > Cr > Mn > Pb > Cs, the Pb and
Cs presented similar values. Likewise, the metals that presented a SAF > 1 were Zn > Cu > Fe > Mn; SAF < 1 were linked
to Ni > Pb > Cs > Cr. The RAF and SAF obtained showed that E. elegans accumulates metals preferentially in the roots. Pb
and Cs are the metals that bioaccumulate most efficiently in the plant. The study allowed us to conclude that E. elegans can
bioaccumulate metals such as Zn, Ni, Cr, Pb, and Cs, which suggests that it has the potential and characteristics to be used
as a biomonitor for contamination by metals and cesium.

Keywords  Bioaccumulation factor · Biomonitor · Cesium · Succulent plants · Translocation factor

Introduction

In the last 100 years, the planet has suffered a process of

Editorial responsibility: Tanmoy Karak.
* H. B. Ortiz‑Oliveros
huemantzin.ortiz@inin.gob.mx
1
Department of Radioactive Waste, National Institute
for Nuclear Research, A. P. 18‑1027. Col. Escandón,
Delegación Miguel Hidalgo, 11801 Ciudad de México, CP,
México
2 the transfer of various pollutants to the soil, water and air,
Faculty of Chemical Engineering, Benemerita Autonomous
University of Puebla, 72570 Puebla, C.P, Mexico
3 degradation and transfer of pollutants to the environment are
Department of Environmental Studies, National Institute
for Nuclear Research, A. P. 18‑1027. Col. Escandón,
Delegación Miguel Hidalgo, 11801 Ciudad de México, CP,
México
4
Autonomous University of the State of Mexico, Instituto
Literario 100, 50000 Toluca, CP, Mexico
5
Department of Nuclear Forensic and Analytical
Chemistry, National Institute for Nuclear Research,
A. P. 18‑1027. Col. Escandón, Delegación Miguel Hidalgo,
11801 Ciudad de México, CP, México
environmental degradation, which has been documented and
established beyond any doubt. This environmental deteriora‑
tion is mainly related to the accelerated growth of the world
population, which according to United Nations data is esti‑
mated at 7550 million inhabitants with an annual growth
rate of 1.10% (UN 2017). The high consumption of fossil
fuels (13,258 million tons of oil, approximately) to produce
energy (Exxon Mobil 2018) is another anthropogenic activ‑
ity that implies a high consumption of natural resources and
mainly. According to the World Health Organization, the
responsible for approximately 12.6 million deaths per year,
this means that around 23% of deaths in the world are pro‑
duced by living or working in unhealthy environments; risk
factors such as air, water, and soil pollution due to exposure
to chemicals, heavy metals, climate change, ultraviolet radia‑
tion, etc., contribute to more than 100 diseases or injuries
(WHO 2016). Other authors indicate that approximately 30
million people die every year due to air pollution, which

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1092 International Journal of Environmental Science and Technology (2022) 19:1091–1104
could be linked to heavy metals (Cetin et al. 2019; Bozdoğan
Sert et al. 2019).
The transfer and accumulation of heavy metals (As, Cr,
Cd, Cu, Pb, Ni, U, Cs, Zn, etc.) in the environment imply
important environmental and health problems (Alaboudi
et al. 2018; Bozdoğan Sert et al. 2019), due to their high
toxicity, easy dispersion, but especially for its persistence
and bioaccumulation in the ecosystem (Koedrith et al. 2013;
Turkyilmaz et al. 2018; Wu et al. 2018). Environmental pol‑
lution by heavy metals is caused by two primary sources:
natural and anthropogenic. In the first case, metals can accu‑
mulate and imply a risk (to health or the environment) due to
processes of leaching, weathering, chemical decomposition,
etc., of the mother rock; arsenic contamination of drinking
water is a typical example of a not unusual non-anthropo‑
genic pollution that threatens the entire population segments
(Volesky 2007). Metal contamination from anthropogenic
sources is diverse, for example, three anthropogenic sources
could contribute to the Pb enrichment combustion processes
(food, paper, plastics, textiles, rubber, wood, and metal melt‑
ing), plastic and textile industries, as well as metalworking;
and the re-deposition of old Pb coming from leaded gasoline
(Ávila-Pérez et al. 2019). It has been identified that the major
contamination sources of Zn are industrial activities, com‑
bustion of fossil fuels, incineration of municipal waste, and
agricultural activity due to fertilizer use (McBride and Spi‑
ers 2001; Fekiacova et al. 2015). Contamination of abiotic
systems by Cu can be related to the activities of the automo‑
tive, glass, paint, electroplating industries, and agricultural
and livestock activities (Mirzaei Aminiyan et al. 2018). The
accumulation of Cr in the environment is related to sev‑
eral industrial applications such as electroplating, dyeing
of textiles, leather processing, steel production, and tanning
industry, resulting in a discharge of chromium-containing
effluents (Sharma et al. 2020).
Different strategies have been implemented to deal with
contamination by heavy metals, these strategies can be
grouped into measures of: a) prevention of pollution through
the efficiency of industrial processes and improving pas‑
sive environmental monitoring techniques (using bioindi‑
cators) and continuous (direct quantification of metals); b)
protection, studying the effects of metals on biota; and c)
recovery/rehabilitation of affected resources, using treat‑
ment technologies (Ávila-Pérez et al. 2019; Malikova et al.
2019; Sevik et al. 2019; Ortiz-Oliveros and Flores-Espinosa
2020). Several remediation technologies have been devel‑
oped to treat heavy metal contaminated soils. The most used
are physicochemical treatments (vitrification, soil washing,
encapsulation, stabilization/solidification, engineering bar‑
riers, flushing, etc.) (Erenturk et al. 2020; Shu et al. 2020;
Wang et al. 2020); and biologicals (biosorption, phytoreme‑
diation, biotransformation, etc.) (Shah and Daverey 2020;
Wei et  al. 2020; Ubando et  al. 2021). Physicochemical
13
treatments are usually expensive, can cause changes in the
natural properties of the soil, and, in some cases, generate
secondary residues (Zhang et al. 2019). On the other hands,
biological treatments are more environmentally attractive,
with biosorption and phytoremediation being the most
effective and economical techniques (Alaboudi et al. 2018;
Wei et al. 2020). Phytoremediation is a technique that uses
aquatic or terrestrial plant species to remove heavy metals
from the ecosystem (Sharma et al. 2015). This technology
involves the accumulation of metals in plants by processes
of phytoextraction and phytostabilization, mainly (Alaboudi
et al. 2018). In this context, the study of the accumulation
of heavy metals in different species of plants (terrestrial and
aquatic) has increased in recent years, to be used as a low-
cost alternative for the decontamination of ecosystems, or to
be used for environmental biomonitoring (Turkyilmaz et al.
2018; Malikova et al. 2019). Currently, different species of
plants, mosses, lichens, etc., are being successfully used as
bioindicators to determine the concentration of heavy met‑
als in different cities of the world (Ávila-Pérez et al. 2019;
Bozdoğan Sert et  al. 2019). These metal-accumulating
organisms are an ideal low-cost alternative for environmen‑
tal monitoring as they can take up heavy metals from soil,
rainwater, and air and accumulate them into their tissues
(Sevik et al. 2019; Trujillo-González et al. 2020).
Echeveria elegans is an evergreen semidesert plant of the
order of the Saxifragales and the Crassulaceae family (Mon‑
roy-Ata and Vázquez-Benítez 2014). The genus Echeveria
is an exclusive group of America and Mexico is the center
of greatest diversity and endemism (83% of the 127 species)
(Thiede and Eggli 2007). E. elegans contains tight rosettes
and fleshy green leaves and long-stemmed pink flowers; its
propagation can be sexual (seed) or asexual (vegetative),
that is, through leaves or stems (Kim et al. 2019; Reyes
et al. 2011). This plant has fibrous and spindle-shaped roots
adapted for rocky substrates, as well as the ability to store
water in its leaves in the form of mucilaginous juices, which
is why it is commonly referred to as succulent plant. These
physical characteristics and great adaptability have allowed
them to be used extensively in gardens and recently on green
walls and roofs in the most important urban centers of the
world (Jiménez et al. 2014; Reyes-González et al. 2018).
An important characteristic of the Crassulaceae family is its
highly efficient water use mechanism, known as crassulacean
acid metabolism (Nobel 1983). This complex metabolism
has encouraged phytochemical investigation that has shown
the presence of secondary metabolites of pharmacological
importance (Kumar et al. 2016); as well as the potential to
be used as water harvesters or as raw material to develop oil/
water separation membranes (Godeau et al. 2017).
Considering the extensive use of E. elegans in green
walls and roofs, urban gardens, etc., as well as its complex
metabolic system, in this work, it is proposed to evaluate
International Journal of Environmental Science and Technology (2022) 19:1091–1104 1093
the bioaccumulation potential of heavy metals and 137Cs
(simulated by ­CsNO3) in this succulent plant and further
establish its possible utility as a biomonitor of contamination
by heavy metals and radionuclides. The research was done
in Mexico state (Mexico) in year 2020.
Material and methods
Study area
The site where the soil samples were extracted is located in
the northwest of the State of Mexico, at UTM coordinates:
516,695.45, 2,188,277.23, and 517,365.90, 2,188,932.92, as
shown in Fig. 1. At this site, during the 1980s, the mining
tailings were deposited causing hotspots of contamination,
years later the tailings were removed. The site is located at
2,400 masl (average) and has an area of 0.34 k­ m2. In this
Fig. 1  Study area
region, the climate is classified as semi-dry temperate with
rains in summer and autumn, with an average temperature of
16 °C and a thermal range of between 14 and 18 °C (INEGI
2015). The average annual rainfall varies between 583 and
638 mm. The region is characterized mainly by hyphalic
pheozem and cambisol soil types (INEGI 2015). Hyphalic
pheozem soils are characterized by presenting a surface layer
rich in organic matter and suitable for the development of
agricultural activities, but susceptible to erosion. The cambi‑
sols are distinguished by being suitable for the development
of livestock activities and urban development mainly. The
predominant land use around the extraction site is seasonal
agriculture (barley and corn crops) and induced pastures.
Soil physicochemical characterization and sampling
The collection and extraction of soil samples were
obtained in the northwest of the State of Mexico, at the
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1094 International Journal of Environmental Science and Technology (2022) 19:1091–1104
following UTM coordinates: 516,695.45, 2,188,277.23, and
517,365.90, 2,188,932.92.
The selection of the sampling points and the collection of
soil samples were carried out by Mexican and international
regulations (ISO 2002; NMX 2016). For the extraction of
the soil, a surface exploratory sampling (horizontal) was
used. The criteria used were based on the location of the
site, as well as on the edaphological and land use charac‑
teristics. Surface sampling was done with a stainless steel
nucleator. Composite samples were taken, consisting of five
simple samples, uniformly distributed and taken using the
staggering technique. The soil samples were homogenized
and fractionated by the quartering technique. Fractions of
400 g of soil were used for its physicochemical characteriza‑
tion and propagation of E. elegans.
Representative soil samples were characterized to deter‑
mine its main physicochemical properties. The density,
humidity, pH, and conductivity, as well as the elemen‑
tal composition, were evaluated. Density, humidity, pH,
and conductivity were estimated according to the United
States Department of Agriculture guidelines (USDA 1999).
pH measurements were conducted with a ThermoOrion
720A + pH-meter with an Ag/AgCl combination electrode,
the electrical conductivity was obtained with a HACH
equipment model SensION 156 Multi-parameters Meter.
The elemental composition of the soil was determined by
energy-dispersive X-ray fluorescence TX 2000 X-Ray Spec‑
trometer manufactured by Ital Structures. A primary fine
focus beam provided by the X-ray tube with a molybdenum
anode is monochromatized and is directed to the sample
at a glancing angle less than the critical angle. The tube
was operated at 40 kV and 30 mA. The fluorescent X-rays
derived from the sample were detected with a solid-state
lithium-drifted silicon detector of 20 mm2 front area, cooled
with liquid nitrogen. The energy resolution (FWHM) of the
Si(Li) detector was 140 eV for Mn Kα and its beryllium
window was 8 μm thick (Zarazúa et al. 2014).
Propagation of E. elegans specimens
Fourteen representative samples of 400 g of soil from the
study area were placed in pots, in which the specimens of E.
elegans were transplanted. The propagation of the specimens
was carried out by vegetative or asexual reproduction using
leaves of the original plant (Reyes et al. 2011). Four soil
samples were enriched with 80, 120, 250, and 320 mg/kg of
cesium nitrate (­ CsNO3) (Merck, 99%) to simulate the reten‑
tion of 137Cs and determine its accumulation in E. elegans.
All specimens were grown at room temperature and
under indirect exposure to sunlight. Irrigation was carried
out once every 10 days using 50 mL of water, in order
not to generate excess humidity (Reyes et al. 2011) and
13
maintaining strict surveillance and pest control. Finally,
specimens of E. elegans were grown for 28 weeks without
exception.
Determination of metals in soil and E. elegans
specimens
After 28 weeks of growth, the extraction and preparation of
the E. elegans and soil samples were carried out. With the
necessary care, the plants were extracted from each pot and
were washed with deionized water to remove the remains of
soil and organic matter. Then, the roots were separated from
the shoots of the plant, recording the weight and dimensions.
At the same time, 100 g of soil was extracted from each pot
for subsequent elemental analysis.
The shoot and root samples were labeled and dried at
controlled temperature and humidity. The dried samples
were analyzed by inductively coupled plasma optical emis‑
sion spectrometry (ICP-OES). The metal concentration (Cr,
Cu, Cs, Fe, Mn, Ni, Pb, and Zn) was determined follow‑
ing the procedure used by Ávila-Pérez et al. (2019). Previ‑
ously, the samples were digested in acid solution and using
a CEM-Mars-5 microwave oven at 1200 W, under the fol‑
lowing conditions: pressure from 276 to 586 kPa, increasing
to 827 kPa (for 10 min), and finally 10 kPa (for 15 min).
The digested samples were dried in an oven at °C until they
were completely dry. The product was mixed with 2 mL of
­HNO3, 2 mL of HCl and made up to 10 mL with deionized
water. Subsequently, all of the samples were analyzed in an
ICP-OES (Thermo Jarrel Ash Corporation) model Atomscan
Advantage Axial Type. The quantification of heavy met‑
als was carried out under the following analysis conditions:
sample uptake of 1.8 ­mLmin−1, the auxiliary flow rate of
1.0 Lmin−1, plasma flow rate 14 Lmin−1, nebulizer pressure
of 207 kPa, and generator power of 1150 W. The analysis of
the spectra was done by SPEC/PMT 2.1v software.
Statistic analysis
All experimental results were presented as mean and stand‑
ard deviation of the three replicate measurements. At the
same time, the normality of the analyzed data was checked.
Differences between pots with respect to mean concentra‑
tions of elements in soil and plants (shoots and roots) were
evaluated by ANOVA with the F-test at a significance level
of 95% (p ≤ 0.05). Pearson regression and correlation coef‑
ficients were calculated to examine the relationships between
the concentrations of elements in soil and plants (roots and
shoots) at a significance level of 95% (p ≤ 0.05). All calcu‑
lations were carried out using the Statgraphics 18® (trial
version).
International Journal of Environmental Science and Technology (2022) 19:1091–1104 1095

Accumulation and translocation of metals in E. Results and Discussion

elegans specimens
The estimation of the accumulation and translocation factors
was used with indicators to estimate the potential of E. elegans
to retain heavy metals. This accumulation of metals was esti‑
mated using both the root accumulation factor (RAF) and the
shoot accumulation factor (SAF). The RAF is expressed as the
relationship between the metal concentration in the root of the
plant ­(Croot, mg/kg) concerning to the metal concentration in
the substrate ­(Csoil, mg/kg) (Galal and Shehata 2015; Hao et al.
2019; Sarah et al. 2019; Du et al. 2020), as shown in Eq. 1.
Croot
RAF =
Csoil
SAF is defined by the relationship between the concentra‑
tion of metals in plant tissues ­(Cshoot, mg/kg) with respect to
the concentration of metals in the substrate (­ Csoil) (Nnorom
et al. 2020), as shown in Eq. 2.
Cshoot
SAF =
Csoil
The translocation factor (TF) or mobilization factor, was
estimated with Eq. 3, which represents the capacity of the plant
to absorb and distribute the pollutant from the root to the dif‑
ferent parts of the plant (Gupta and Sinha 2006; Ganeshkumar
et al. 2019).
Cshoot
TF =
Croot
Physicochemical characteristics of the soil
Table 1 presents the main characteristics of the soil obtained
from the study site and that was used as a substrate for E.
elegans. As can be seen in table, the soil used as a substrate
has a poor content of organic matter, acid pH, low salin‑
ity, and mineral content of approximately 47.9%. Soil pH is
an important chemical factor that determines the solubility,
chemical speciation, mobility, and therefore the bioavail‑
ability of micronutrients and heavy metals (Fageria and Nas‑
cente 2014). It has been established that the absorption of
(1) metals such as Cu, Cr, Fe, Mn, Pb, and Zn, by the roots of
the plants, decreases with increasing pH and increases with
decreasing pH (Fageria and Nascente 2014; Ahmadpour
et al. 2015). On the other hands, the results of the elemen‑
tal analysis of major components of the soil, obtained by
energy dispersive X-ray fluorescence, showed that the main
elements (percentage average) were: Si (30.51 ± 0.69%), Al
(9.47 ± 0.16%), Fe (3.90 ± 0.05%), Ca (1.40 ± 0.06%), Na
(2)
(1.01 ± 0.03%), Mg (0.84 ± 0.05%), and K (0.83 ± 0.02%).
The elemental composition and physical characteristics of
the soil are consistent with feozem soils where aluminosili‑
cates and silicon oxide predominate, as other authors have
observed (Negrete-Velázquez et al. 2010) and are consistent
with the high percentages of Si and Al observed.
Furthermore, in Table 1, the results of the estimation of
the total concentration of metals in the soil obtained by ICP-
(3) OES are presented. The results of the statistical analysis of
these data showed that Fe and Mn are the elements with
the highest concentration with values of 1168.7 ± 15.21
and 591.7 ± 24.4 mg/kg, these concentrations are within
the ranges of average values of all types of soils (Markert
1992; Wisłocka et al. 2006). Additionally, the concentration

Table 1  Physicochemical Parameters Mean Standard Coefficient of Maxime Minime

characteristics and total metal deviation variation (%)
concentration in the soil that
was used as a substrate for E. Density (g/cm3) 2.30 – – 2.42 2.18
elegans 
Electric conductivity (dS/m) 0.9 – – 1.1 0.7
Humidity (%) 19.7 – – 26.9 12.5
Organic material (%) 1.2 – – 1.5 0.9
pH 6.1 – – 6.5 5.7
Cr (mg/kg) 68.6 2.4 3.5 73 64.1
Cu (mg/kg) 27.9 1.3 4.8 31.5 26.2
Fe (mg/kg) 1168.7 15.2 1.3 1196.1 1137.9
Mn (mg/kg) 591.7 24.4 4.1 643.3 557
Ni (mg/kg) 41.9 1.3 3.1 44.1 39.7
Pb (mg/kg) 20.7 0.9 4.8 22.3 18.2
Zn (mg/kg) 87.9 1.7 2 85.1 91.7

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1096 International Journal of Environmental Science and Technology (2022) 19:1091–1104
of Zn, Cr, Ni, Cu, and Pb in the soil was quantified, as they
are considered the most interesting. In this context, it was
possible to determine that the soil used as a substrate has
the following composition: Fe > Mn > Zn > Cr > Ni > Cu >  to Cs, with respect to those that were not exposed to the
Pb. The concentration level observed for Zn (87.9 ± 1. mg/
kg) is in the normal range of agricultural soils (10– mg/
kg) (Kabata-Pendias 2004). Soils with Zn concentrations
higher than 400 mg/kg are considered contaminated soils
with a risk of toxicity for biota (EPA 2017). In the case of Cr
(68.6 ± 2.4 mg/kg), concentrations higher than these consid‑
ered normal (10–50 mg/kg) were observed (EPA 2017). In
addition, Cu (27.9 ± 1.3 mg/kg) is within the range of normal
concentrations in soil (5–30 mg/kg). Finally, Pb concentra‑
tions (20.7 ± 0.9 mg/kg) were observed higher than 10 mg/
kg considered typical in soils and located at the lower limit
of the interval considered toxic (Kabata-Pendias and Pendias
2001; EPA 2017). The observed Pb concentration could be
linked to the presence of secondary radiogenic lead by the
uranium mineral residues that remain at the sampling site,
after being removed in the 1990s, this phenomenon has been
observed by different authors in other sites world (Wisłocka
et al. 2006).
Physical characteristics of E. elegans specimens
After 28 weeks of culture, the E. elegans and soil samples
were extracted and prepared. With the necessary care, the
specimens were extracted from each pot (see Fig. 2). Table 2
shows the weights of the shoots and roots of E. elegans at the
time of extraction and after drying. The analysis of variance
Fig. 2  Specimens of E.
elegans harvested. a Collec‑
tion to extract the specimens. b
Example of the specimen after
28 weeks of growth. c Prepara‑
tions for recording the weight
and dimensions
13
carried out on the sizes and weights of the specimens
showed that there are no significant differences (p < 0.05)
between the shoots and roots of the plants that were exposed
metal. This suggests that the cesium concentrations to which
the four specimens of E. elegans were exposed did not cause
apparent damage to the organisms, which was reflected
in the growth of roots and shoots. Different authors have
reported that some heavy metals can cause growth retar‑
dation and decreased biomass production in plants (shoots
and roots) (Alaboudi et al. 2018). In the case of Cs, it has
been documented that it is toxic to plants when absorbed in
high concentration (intracellular). However, this phenom‑
enon rarely occurs under normal environmental conditions
(Rai and Kawabata 2020), as observed in our case. Addition‑
ally, from the results obtained, it can be established that E.
elegans does not present apparent physical stress associated
with its exposure to the concentration levels of metals in the
soil used as substrate.
Metal accumulation in E. elegans specimens
In Table 3, the total concentration of metals in the shoots
of the different specimens of E. elegans is presented. As
evidenced, the metals found in the highest concentration are
Fe (5568.6 mg/kg), Mn (2360.9 mg/kg), Zn (801.9 mg/kg)
and Cu (217.1 mg/kg), in lower concentration Ni (35.1 mg/
kg), Cr (16.72 mg/kg), and Pb (31.6 mg/kg). Comparing
the results of Tables 1 and Table 3, it was determined that
the metal ions that increased their concentration in the
International Journal of Environmental Science and Technology (2022) 19:1091–1104 1097

Table 2  Length and weight of Specimen Total Total weight (g) Shoot fresh (g) Root fresh (g) Shoot dry (g) Root dry (g)
roots and shoots of E. elegans length
specimens grown in the soil. (cm)
­Sp9, ­Sp10, ­Sp11, and ­Sp12
specimens in contact with soil Sp1 21 26.47 25.55 0.92 1.35 0.14
enriched with 80, 120, 250, and
Sp2 24 36.89 35.33 1.56 0.99 0.25
320 mg/kg of Cs, respectively
Sp3 23.9 23.44 22.49 0.95 0.88 0.12
Sp4 25.4 32.27 31.19 1.08 0.79 0.14
Sp5 22.4 47.20 44.48 2.72 1.56 0.42
Sp6 23.2 48.03 45.80 2.23 1.57 0.29
Sp7 17.6 36.24 34.60 1.64 1.34 0.20
Sp8 18.8 25.23 23.77 1.46 0.89 0.19
Sp9 20.6 33.65 31.80 1.85 1.02 0.31
Sp10 23.3 29.56 28.44 1.12 1.43 0.17
Sp11 15.6 18.85 17.93 0.92 0.71 0.12
Sp12 20.4 23.26 22.62 0.64 0.80 0.11

Table 3  Statistical summary of Metal (Shoots) Mean (mg/kg) Standard deviation Coefficient of variation (%) Maxime Minime
the total concentration of metals
in the shoots and roots of E. Cr 16.7 8.3 49.4 34.1 1
elegans specimens
Cu 217.1 63.8 29.4 316.5 121.1
Fe 5568.6 4301.3 77.2 16,626.4 109.5
Mn 2360.9 580.5 24.6 3140.7 1423.4
Ni 35.1 6.1 17.4 43.5 25
Pb 28.3 21.3 75.4 63.2 10
Zn 801.9 235.2 29.3 1054.9 216.2
Metal (Roots)) Mean (mg/kg) Standard deviation Coefficient of variation (%) Maxime Minime
Cr 416.3 269.9 64.8 876.9 18.5
Cu 2632.9 2547.7 96.7 9879.4 364.3
Fe 83,001.4 45,580.7 54.9 164,692 9261.5
Mn 3135.6 1258.3 40.1 5831.2 1247.5
Ni 802.4 511.4 63.7 1630.9 228.8
Pb 24.5 44.6 197.9 142.3 1.4
Zn 4068.7 2952.3 72.6 12,534.8 1104.5

shoots with respect to the soil were Fe > Mn > Zn > Cu,
these are considered essential for plants (Kabata-Pendias
2004). Regarding to non-essential metals such as Pb, this
increased their concentration in the plant concerning the
soil. Two potential sources of Pb could be involved: a) lead
of secondary radiogenic origin from uranium mineral resi‑
dues that remain at the sampling site after being removed
in the 1990s; and b) re-deposition of old Pb from leaded
gasoline. In Mexico, leaded gasoline was banned in 1990;
however, the re-deposition phenomenon has been observed
in other countries (Chrastný et al. 2018; Trujillo-González
et al. 2020). In this context, it has been observed that several
plants can readily take up atmospheric Pb after deposition on
the leaves, this atmospheric Pb deposition can be attributed
to anthropogenic activities, including vehicular emissions
(Ávila-Pérez et al. 2019). Likewise, the total concentration
of Ni and Cr in the shoots was lower than in the soil, in
the following order: Ni > Cr. The results of the comparative
analysis by Pearson regression to examine the relationships
between the concentrations of elements in soil and shoot
showed that although there are important concentrations of
soil metals in the shoots of E. elegans, there is no significant
correlation between them.
On the other hands, in Table  3, the total concentra‑
tion of metals in the roots of E. elegans is presented. The
results show that the concentration of Fe, Mn, Cu, Ni, Zn,
and Cr is higher in the roots than in the soil and shoots
(Fe > Zn > Mn > Cu > Ni > Cr). However, the Pb concen‑
tration is higher than that observed in the soil and statisti‑
cally similar to that registered in the shoots. Likewise, the
comparative analysis by Pearson’s regression to examine the
relationship between the concentration of Pb in the roots

13

1098 International Journal of Environmental Science and Technology (2022) 19:1091–1104

and the soil showed that there is no significant correlation

between them. The comparative analysis between the root
metals showed that there are statistically significant relation‑
ships between the concentration of the following metals: Cu
and Zn (r = 0.9; p < 0.05), Fe and Mn (r = 0.84, p < 0.05); Fe
and Ni (r = 0.82, p < 0.05), as well as between Mn and Ni
(r = 0.81, p < 0.05).
In Fig. 3, the total concentration of Cs in the soil, shoots,
and roots is presented. In this, it is observed that there is a
statistically significant correlation (r = 0.9, p < 0.05) between
the concentration of Cs in the soil and the concentration in
the shoots and roots. Likewise, it is observed that as the
amount of Cs in the soil increases (> 129 mg/kg), the con‑
centration of the metal decreases in the plant, which suggests
a maximum retention capacity; however, additional studies
are necessary.

Accumulation and translocation of metals

in Echeveria elegans specimens

Fig. 3  Total concentration of cesium in the soil, shoots, and roots of Figure 4 shows the bioaccumulation factors in: roots (RAF)
E. elegans 
and shoots (SAF), as well as the translocation factor of the
metals studied in E. elegans. The results of Fig. 4a show that

(a)

(c)

(b)

Fig. 4  Bioaccumulation factors, a RAF and b SAF. c translocation factor (TF). Estimated factors using the weighted average

13
International Journal of Environmental Science and Technology (2022) 19:1091–1104 1099
all metals have a RAF > 1, ordered from highest to lowest
are Cu > Fe > Zn > Ni > Cr > Mn > Pb > Cs; Pb and Cs (see
Table 4) show similar behavior. These results allow estab‑
lishing that E. elegans bioaccumulates in the roots mainly
Cu, Fe, Zn, and Mn, metals considered essential micronutri‑
ents for the metabolic functioning of plants (Kabata-Pendias
and Mukherjee 2007; Hooda 2010). However, it must not be
forgotten that although certain metals, such as Cu, Ni, and
Zn, are essential for the normal growth and development of
many organisms, they can become toxic at excessive levels
(Clemens and Ma 2016; Geng et al. 2019; Richardson et al.
2020). Therefore, it is evident that E. elegans has the poten‑
tial to bioaccumulate Cr, Pb, and Cs (see Table 4), elements
of interest from the toxicological point of view, and passive
environmental monitoring. The accumulation of metals in
the roots may be related to the secretion of organic acids that
modify the solubility of metals present in the insoluble form
in the soil by acting as ligands (Kohli et al. 2018; Khanna
et al. 2019). Kringstad (Kringstad 1975, 1978) reported the
presence of various organic acids such as malic and phor‑
bic in E. elegans. In addition, the plants of the genus Ech-
everia possess a highly efficient mechanism in the use of
water, known as Crassulacean acid metabolism, in which at
night they open their stomata to perspire and capture C ­ O2,
which is fixed in molecules such as malic acid and other
organic acids, through enzymatic carboxylation (Phase I)
(Lüttge 2004). During the day, the plants keep their stomata
closed, avoiding perspiring and losing water from their tis‑
sues (Phase III). At the same time, there is an active flow
of the organic acids stored in the vacuoles that are decar‑
boxylated, releasing the C ­ O2 inside the plant to carry out
photosynthesis. Between these two phases, there are transi‑
tions, where the stomata remain open for C ­ O2 uptake for
short periods during sunrise (Phase II) and sunset (Phase IV)
(Lüttge 2004). In these transitions, there is a direct fixation
of ­CO2 to carbohydrates, which occurs when the reserve of
organic acids accumulated in the vacuoles is depleted (Phase
IV). Phases II and IV respond sensitively to environmental
conditions such as: temperature, light intensity, humidity,
availability of water, and nutrients (Lüttge 2004, 2010).
In this context, the results obtained allow us to infer that
heavy metals could be bioaccumulated and transported
through E. elegans by the action of organic acids and follow
Table 4  Cesium accumulation in E. elegans  these accumulate in a greater proportion in the root and not
Sp9 (80 mg/kg) Sp10 Sp11 Sp12
(120 mg/kg) (250 mg/kg) (320 mg/
kg)
RAF 1.5 1.1 0.8 0.8
SAF 1.2 1.5 0.8 0.6
TF 0.8 1.3 0.9 0.8
the transport route of this metabolite. Studies regarding the
functioning of Crassulacean acid metabolism indicate that
the transport of organic acids during Phase I occurs through
a positive electrochemical gradient within the vacuoles,
where the acids are transported through the tonoplast in the
form of divalent anions via ionic channels or a specific car‑
rier. During the Phase III, the flow of organic acids into
the cytoplasm occurs by passive diffusion through the tono‑
plast membrane (Lüttge et al. 1995). Additional studies to
establish the mechanism of bioaccumulation and transport
of heavy metals in E. elegans are required. The complex‑
ity of this metabolism has been the driving force behind
various studies, such as the one carried out by Kumar et al.
2016, which reported the identification, in E. elegans, of
different phytochemicals (secondary metabolites) such as
triterpenoids, steroids, glycosides, saponins, and alkaloids.
In the case of Cr, the higher accumulation of metal in
roots might be attributed to the sequestration of Cr in the
vacuoles of root cells as a protective mechanism (Mang‑
abeira et al. 2011; Sharma et al. 2020). This statement is con‑
sistent with the mechanism of bioaccumulation and transport
of metals in E. elegans that was previously described.
On the other hands, Cs is usually immobilized in the soil
by sorption phenomena, where functional groups (active
sites) of aluminosilicates and iron oxides, as well as func‑
tional groups of organic matter, retain Cs, forming surface
complexes (Ortiz-Oliveros et  al. 2009; Thompson and
Goyne 2012; Yamaguchi 2014). The retained Cs can only
be moved by phenomena such as infiltration, surface runoff,
and erosive processes (Rai and Kawabata 2020). Despite
this, it has been observed that plants have a great capacity for
the absorption of inorganic ions, which causes the rediffu‑
sion of Cs. This bioavailable cesium is absorbed by the roots
through the same mechanism implemented in the absorption
of ­K+ (Ogura et al. 2014; Rai and Kawabata 2020).
In Fig.  4b, it is observed that the metals that have a
SAF > 1 are Zn > Cu > Fe > Mn, all necessary for the enzy‑
matic functions of the plant (Kabata-Pendias and Mukherjee
2007; Hooda 2010). As evidenced, Zn and Cu are the metals
with the highest mobility in E. elegans, which is consistent
with that observed in other plant organisms, this behavior
is associated with the fact that they are enzymatic cofac‑
tors linked to plant growth (Hooda 2010; Richardson et al.
2020). The metals with a SAF < 1 were Ni > Pb > Cs > Cr,
comparing these results with Fig. 4a, and Table 4 shows that
in the shoots, as an organism protection mechanism (exclu‑
sion process). For example, the mobility of Cr in the roots of
plants is low when compared to other metals (for example,
the essential ones), where the total concentration of Cr in
the roots is sometimes 100 times higher than in the shoots
(Shanker et al. 2005; Gupta and Sinha 2006; Sharma et al.
2020).
13

1100 International Journal of Environmental Science and Technology (2022) 19:1091–1104
Figure 4c shows the TF of the studied metals, the results
show that Pb and Cs have TF > 1 (5.06 and 1.0, respectively),
indicating that these elements efficiently transfer from the
roots to the shoots (Galal and Shehata 2015; Ganeshkumar
et al. 2019; Li et al. 2019), showing that the plant has the
potential to bioaccumulate these heavy metals. Likewise, the
elements with a TF < 1 were Mn > Zn > Fe > Cu > Cr > Ni,
this indicates that E. elegans does not effectively transfer
these metals from the root to the shoots (Ganeshkumar et al.
2019; Li et al. 2019; Du et al. 2020) and shows the potential
to phyto-stabilize them in the roots.
In general, the results shown by the accumulation and
translocation factors suggest that E. elegans significantly
retains metals in the root, showing it as a bioaccumulative
and phytostabilizing plant of Zn, Ni, Cr, Pb, and Cs. This
relationship of results indicates the potential utility of this
plant in the monitoring of contamination by metals, in par‑
ticular Zn, Ni, Cr, Pb, and Cs. These metals (except cesium)
are often associated with the combustion processes, vehicle
emissions, biomass burning, brick kiln emissions, manufac‑
turing industry, and suspended and deposited particles by the
action of the wind have been identified as the main sources
of heavy metals in large urban centers (McBride and Spiers
2001; Fekiacova et al. 2015; Mirzaei Aminiyan et al. 2018).
On the other hands, the results of the bioaccumulation and
translocation of cesium by E. elegans are relevant and show
the potential of this plant in passive monitoring in cities
near nuclear power reactors or for environmental radiologi‑
cal surveillance of radioactive facilities associated with the
fuel cycle. The concentration of stable cesium (133Cs) in the
environment is generally low (up to 25 µg/g of soil) and does
not affect human health or the environment (White et al.
2003; Rai and Kawabata 2020). However, the same does not
happen with the unstable cesium isotopes, in particular 134Cs
and 137Cs, these radionuclides are fission products that are
usually released into the environment by nuclear weapons
tests or accidents in nuclear power reactors (Ogura et al.
2014). 134Cs and 137Cs can be deposited in the soil and enter
the food chain, causing an exposure (external and internal)
to the population to β and γ radiation (Ogura et al. 2014;
Rai and Kawabata 2020). Given its risk to health and the
environment, its environmental monitoring is of concern to
society in countries with a developed nuclear industry.
Additionally, E. elegans has physical, metabolic, and
adaptability characteristics that allow it to with stand high
radiation, long periods of drought, extreme temperatures,
and high resistance to urban pollution, it also has a rapid
growth (Reyes-González et al. 2018). These characteristics
have allowed them to be used extensively in urban gardens
and recently on green walls and roofs in large urban centers
(Jiménez et al. 2014; Reyes-González et al. 2018), consti‑
tuting elements of urban plant cover in highly populated
and with high traffic density, such as the Metropolitan Zone
13
of Toluca Valley and Metropolitan Zone of Mexico Val‑
ley, which together have a population of 23,095,610 mil‑
lion inhabitants and an approximate of 12,703,000 vehicles
(INEGI 2015). Therefore, considering the physical charac‑
teristics of the plant, the potential for bioaccumulation of
metals, and the use of E. elegans as part of the urban plant
cover, they allow supporting the assertion that this plant has
the potential to be used as a biomonitor. Plants, mosses,
lichens, among others, are examples of organisms used
for environmental biomonitoring (Turkyilmaz et al. 2018;
Malikova et al. 2019; Bozdoğan Sert et al. 2019).
Conclusion
The experimental results allowed to determine that the soil
contains the following metals: Fe > Mn > Zn > Cr > Ni > C
u > Pb, of which Cr and Pb are above the values considered
typical. This Pb concentration could be related to the pres‑
ence of secondary radiogenic lead from the small remains of
uranium ore that remain at the site even after being removed
in the 1990s.
The evidence obtained, regarding the size and weight of
the E. elegans specimens that were exposed to Cs, allowed to
establish that the specimens do not present visible physical
stress, which suggests that E. elegans is apparently tolerant
and/or resistant to this nuclide.
On the other hands, the determination of metals in E.
elegans indicates that the metals accumulated in the shoots
are Fe > Mn > Zn > Cu > Ni > Cr > Pb. Meanwhile, Fe > Zn > 
Mn > Cu > Ni > Cr > Pb accumulate in the roots. With regard
to the accumulation of Cs, the results show that it is found in
significant concentrations both in the shoots and in the roots.
In addition, it was determined that as the concentration of
cesium in the soil increases (> 129 mg/kg), its accumulation
in the plant decreases, which suggests a maximum retention
capacity.
Likewise, the results of the study of the accumulation
and translocation factors showed that the elements with a
RAF > 1 were Cu > Fe > Zn > Ni > Cr > Mn > Pb > Cs, where
Pb and Cs presented similar values. Likewise, the metals
that presented a SAF > 1 were Zn > Cu > Fe > Mn; SAF < 1
were linked to Ni > Pb > Cs > Cr. The RAF and SAF values
allowed to establish that E. elegans preferentially accumu‑
lates metals in the roots in an exclusion process. In addition,
the translocation factor showed that Pb and Cs are the ele‑
ments that are best transferred from the root to the shoots.
In this context, the evidence indicates that the mecha‑
nism of bioaccumulation and translocation of metals in E.
elegans would be related to the functioning of Crassulacean
acid metabolism, where the organic acids of the plant would
modify the solubility of the metals present in insoluble form
International Journal of Environmental Science and Technology (2022) 19:1091–1104 1101
in the soil, acting as ligands and, later, following the trans‑
port route of these metabolite.
In general, the evidence shown by the accumulation and
translocation factors suggests that E. elegans significantly
retains metals in the root, showing it as a bioaccumulative
and phytostabilizing plant of Zn, Ni, Cr, Pb, and Cs. It is
worth highlighting the potential to bioaccumulate Cr, Pb,
and Cs, given the interest from the toxicological point of
view and environmental monitoring.
It should be noted that the bioaccumulation and trans‑
location of cesium by E. elegans are relevant and show the
potential of this plant in passive monitoring in cities near
nuclear power reactors or for environmental radiological sur‑
veillance of radioactive facilities associated with the fuel
cycle. Given its risk to health and the environment, its envi‑
ronmental monitoring is of concern to society in countries
with a developed nuclear industry.
Acknowledgments  This work is part of project DR-001 of the Radioac‑
tive Waste Department, National Institute of Nuclear Research (ININ).
Part of the chemical analyzes was carried out in the National Forensic
Laboratory of the ININ.
Author contributions  O–O H.B. contributed to conceptualization,
investigation, supervision, data curation, methodology, formal anal‑
ysis, writing — original draft, and writing — review & editing. C
D. was involved in writing — review & editing, data validation, and
chemical analysis. F-E R.M. contributed to methodology, writing —
review & editing. S-M I. was involved in sample extraction, species
propagation, and preliminary sample preparation. Z-O G. contributed
to formal analysis – sample digestion, and chemical analysis. V A. was
involved in sample extraction, geographic information system, and data
analysis. All authors have read and agree to the published version of
the manuscript.
Funding  This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Data availability  The results of all the experiments described are avail‑
able at the request of the corresponding author.
Compliance with ethical standards  ://doi.org/10.1016/j.ecoli​nd.2014.08.013
Conflict of interest  The authors declare that they have no conflict of
interests.
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