Environ Geochem Health
https://doi.org/10.1007/s10653-020-00581-8 (0123456789().,-volV)
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ORIGINAL PAPER
Geographical variations in arsenic contents in rice plants
from Latin America and the Iberian Peninsula in relation
to soil conditions
X. L. Otero . O. Atiaga . R. Estrella . W. Tierra . J. Ruales .
L. Zayas . V. Souza Jr. . T. O. Ferreira . G. N. Nóbrega . D. P. Oliveira .
H. M. Queiroz . L. M. Nunes
Received: 31 March 2020 / Accepted: 17 April 2020
Ó Springer Nature B.V. 2020
Abstract Arsenic is a ubiquitous, toxic element that
is efficiently accumulated by rice plants. This study
assessed the spatial variability in the total As (tAs)
contents and organic and inorganic forms in different
types of rice, plant parts (husk, stem, leaves and
phytoliths) and residues. Samples were collected in
different countries in Latin America (Ecuador, Brazil
and Peru) and the Iberian Peninsula (Spain and
Portugal). The tAs content in commercial polished
rice from the Latin American countries was similar
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10653-020-00581-8) con-
tains supplementary material, which is available to authorized
users.
X. L. Otero (&)
O. Atiaga
Departamento de Edafoloxı́a e Quı́mica Agrı́cola,
Facultade de Bioloxı́a, CRETUS Institute, Universidade
de Santiago de Compostela, Campus Sur,
15782 Santiago de Compostela, Spain
e-mail: xl.otero@usc.es
O. Atiaga
R. Estrella
Departamento de Ciencias de la Tierra y la Construcción,
Universidad de las Fuerzas Armadas ESPE, Av. General
Rumiñahui s/n, P.O. Box 171-5-231B, Sangolquı́,
Ecuador
W. Tierra
J. Ruales
Departamento de Ciencia de los Alimentos y
Biotecnologı́a, Escuela Politécnica Nacional, Quito,
Ecuador
(0.130–0.166 mg kg-1) and significantly lower than
in the rice from the Iberian countries
(0.191 ± 0.066 mg kg-1), and together, the tAs con-
centration in brown rice (236 ± 0.093 mg kg-1) was
significantly higher than in polished and parboiled
rice. The inorganic As (iAs) content in rice was similar
in both geographical regions, and the aforementioned
difference was attributed to dimethylarsinic acid
(DMA). The relative abundance of organic species
increased as the tAs content in rice grain increased. A
meta-analysis of our and previously reported data
confirmed the negative correlation between iAs/tAs
and tAs. At low tAs concentrations, inorganic forms
are dominant, while at higher values
L. Zayas
T. O. Ferreira
H. M. Queiroz
Departamento de Ciência do Solo, Escola Superior de
Agronomia Luiz de Queiroz (ESALQ), Universidade de
São Paulo, Piracicaba, Brazil
V. Souza Jr.
Departamento de Agronomia, Área de Solo, Universidade
Federal Rural de Pernambuco, Recife, Brazil
G. N. Nóbrega
Departamento de Geoquı́mica, Universidade Federal
Fluminense, Outeiro de São João Batista s/n8, Campus do
Valonguinho, Centro, Niterói, Rio de Janeiro 24020-14,
Brazil
D. P. Oliveira
Graduate Course in Ecology and Natural Resources,
Department of Biology, Federal University of Ceará –
UFC, Fortaleza, CE, Brazil
123

(tAs [ 0.300 mg kg-1) the concentration of organic
As increases substantially and DMA becomes the
dominant form in rice grain. On the contrary,
inorganic arsenic was always the dominant form,
mainly as arsenate [As(V)], in leaves and stems. The
presence in soils of high concentrations of amorphous
Fe and Al oxides and hydroxides, which are capable of
strongly adsorbing oxyanions (i.e. arsenate), was
associated with low concentrations of As in rice
plants. In addition, the presence of high concentrations
of As(V) in stems and leaves, low concentration of As
in phytoliths, and the As associated with organic
matter in stems and husk, together suggest that rice
plants take up more As(V) than As(III).
Keywords Soil properties
Arsenic speciation

Phytoliths
Local and intercontinental variability
Introduction
Rice is a staple food for almost half the world’s
population for which it is the main source of proteins
and calories (Cheajesadagul et al. 2013). The rate of
rice consumption varies worldwide (range between
0.90 and 650 g person-1 day-1) and is highest in
South-East Asia (Meharg and Zhao 2012).
The mean rice consumption in Latin America is
estimated to be 80 g person-1 day-1 (estimate for
2013) (FAOSTAT 2018); however, this value is
greatly exceeded in countries such as Peru or Ecuador,
where rice consumption per capita is the highest in
Latin American (134 g day-1 and 123 g day-1,
respectively). The consumption rate is slightly lower
in Brazil (88 g day-1) (FAOSTAT 2018). Rice pro-
duction is economically very important in these
countries: Brazil is the leading non-Asian rice pro-
ducer worldwide, with an annual production of ca.
10.6 million ton year-1; Ecuador produces ca. 1.5
million ton year-1, with more than 90% produced in
the coastal provinces of El Oro, Guayas and Los Rı́os.
Peru is the second largest producer in the region, with
ca. 3.2 million ton year-1 in 2016 (FAOSTAT 2018).
L. M. Nunes
Faculdade de Ciências e Tecnologia, Universidade do
Algarve, CERIS, Campus de Gambelas, Faro, Portugal
123
Environ Geochem Health
Within Europe, Italy is the main rice-producing
country, supplying almost 40% of the total, while
production in Spain (ca. 0.87 million ton year-1)
represents around 20%, and production in Portugal
(0.170 million ton year-1) accounts for 4% of the total
(FAOSTAT 2018). Rice consumption is considerably
lower in European countries than in Latin America.
Rice consumption is highest in Portugal (40.7 g pers-1
day-1) and is much lower in Spain (22.8 g pers-1
day-1) (FAOSTAT 2018).
Rice has been demonstrated to efficiently accumu-
late arsenic (As) in grains more efficiently than other
cereals, representing the second most important source
of As intake in South and South-East Asian countries
(see, e.g. Meharg and Zhao 2012; Rasheed et al. 2018).
However, the concentration of As in rice varies
depending on several parameters, such as plant variety
(genetic variation), geological setting (lithology), crop
management and environmental conditions (e.g. water
and soil properties, harvesting period, etc.) (Khan et al.
2010; Norton et al. 2012; Suriyagoda et al. 2018).
The As present in most agricultural soils is mainly
of geogenic origin (Smedley and Kinniburgh 2002),
although continuous crop growing and the use of crop
protection products can increase the contents of As
and other trace elements (Alloway 2013). In Latin
America, most of the As in soil is derived from
weathering of volcanic rocks and ashes, mainly of
intermediate to rhyolitic composition (Bundschuh
et al. 2012a, b). In Ecuador, the presence of high As
concentrations is associated with intense hydrothermal
activity in volcanic regions (Bundschuh et al. 2012a;
Cumbal et al. 2010; De La Torre et al. 2004) and, to a
much lesser extent, with mining activities (Appleton
et al. 2001). In Peru, water resources are naturally
affected by high concentrations of As, resulting from
weathering of Andean volcanic rocks and sulphidic
ore deposits (Bundschuh et al. 2012a).
Knowledge about As contents and the geochemical
behaviour of As in rice cropland soils is still scarce in
most countries in Latin America and to a lesser extent
in the Iberian Peninsula. There are no data available
for rice paddy soils in Peru; in Brazil, average As
concentrations below 10 mg kg-1 have been reported
(Segura et al. 2018), while in Portugal, the values are
lower than 15 mg kg-1 and in Spain they range
Environ Geochem Health
between 4.2 and 11 mg kg-1 (Signes-Pastor et al.
2016).
Rice is mainly cultured by flooding land, which
alters the redox conditions of soils (Meharg and Zhao
2012). The bioavailability of As is higher under
anaerobic than under oxic conditions due to the
reductive dissolution of iron oxyhydroxides, which
leads to the release of As into the interstitial water (Yu
et al. 2017) and favours the accumulation of As in rice
plants (Fransisca et al. 2015; Islam et al. 2016;
Yamaguchi et al. 2011).
Arsenic occurs in rice plants in many forms with
varying degrees of toxicity. The inorganic As(III) and
As(V) forms and the organic dimethylarsinic acid
(DMA) form are the predominant species in rice
plants; the inorganic forms are the most toxic (Chen
et al. 2016; Wang and Forsyth 2012; Zhu et al. 2008).
Information about the As contents of rice grown in
most South American countries remains scarce. Some
recently published studies conducted in Ecuador have
determined the total arsenic (tAs), inorganic arsenic
(iAs) and organic arsenic (oAs) contents in rice plants,
as well as the As contents in floodwater in paddy fields
in the two main rice-producing provinces (Otero et al.
2016; Nunes and Otero 2017). In Brazil, the informa-
tion available is limited to tAs and iAs contents (e.g.
Batista et al. 2010; Dos Santos et al. 2017; Segura et al.
2016), and studies of organic species are rare (Batista
et al. 2011; Pedron et al. 2016). In Spain, Torres-
Escribano et al. (2008) and Pizarro et al. (2003)
quantified iAs and tAs, while Signes-Pastor et al.
(2016) determined organic and inorganic species. This
type of study is scarcer in Portugal, although Pinto
et al. (2016) quantified tAs in white, parboiled and
brown rice, and Signes-Pastor et al. (2016) and Rego
et al. (2018) determined both organic and inorganic
species in field and supermarket samples of rice grains
(brown, parboiled and polished rice). No data have yet
been published for Peru.
The effects that the properties and composition of
paddy soils can have on the tAs content and its
speciation are of great importance. Soil composition
and properties, such as Eh–pH conditions, mineralogy
and geochemical species of Fe and Al (e.g. forms of Fe
and Al oxides and hydroxides) can affect the bioavail-
ability of As for rice plants (Meharg and Zhao 2012;
Kumarathilaka et al. 2018).
The present study aimed to contribute to a better
understanding of the relationship between soil
characteristics and the concentration of As in rice
plants and rice grains. For this purpose, soils and rice
samples from different edaphoclimatic environments
were sampled and analysed. Soils affected by different
degrees of weathering were chosen for study, i.e. soil
from the coastal and the humid tropical zones of
Ecuador (Orellana) and highly evolved soils from
Brazil (Otero and Ruales 2016; Espinosa et al. 2018).
The study provides new data on the contents of As and
its main species for countries where this information is
scarce, or non-existent (Peru). Finally, the study
evaluates the large-scale regional variability in tAs
and different As species in rice grains in two widely
separated regions: Latin America and the Iberian
Peninsula.
The specific objectives of the study were (1) to
assess the spatial variability in the total As contents
and contents of As forms at different scales: country,
continent and intercontinental, and (2) to study and
compare the tAs contents and contents of the organic
and inorganic species in different parts of rice plants in
relation to soil properties. For this purpose, samples of
commercial rice grain (brown and polished) and paddy
rice were analysed. In the samples from Ecuador, As
concentration and speciation were also determined in
stem, leaf and husk samples. The samples were
analysed to determine the tAs, inorganic forms
[As(V), As(III)] and organic species (dimethylarsinic
acid, DMA, monomethylarsonic acid, MMA, and
arsenobetaine, AsB). Finally, in order to better eval-
uate the factors determining arsenic accumulation in
rice plants, the physicochemical and mineralogical
properties of the soils from Ecuador and Brazil were
characterized.
Materials and methods
Sampling
Soil sampling
Soil sampling was only carried out in Ecuador and
Brazil. Samples were obtained from the superficial soil
layers (0–20 cm), usually 3–4 months after flooding.
Composite soil samples (in total 112) were produced
by mixing five subsamples (* 500 g) taken from
different points within cropland plots. In the
123

laboratory, the soil samples were dried at 45 °C and
sieved through a 2-mm mesh.
In Ecuador, intensive soil sampling was conducted
in the main rice-producing provinces of the country,
which together account for more than 95% of the total
production in Ecuador (INEC 2013; Otero et al. 2016).
A total of 102 samples were collected in the coastal
provinces of Ecuador, i.e. GuayAs (63 samples), Los
Rı́os (21 samples) and El Oro (10 samples), and eight
samples were collected in the eastern region of
Ecuador, in the province of Orellana (Fig. 1a–d).
The first three provinces are located in the coastal
region, with a predominant subtropical dry climate and
very silty soils developed over fluvial–marine sedi-
ments (Otero et al. 2016). The province of Orellana is
located in the eastern region of the country and has a
tropical humid climate and highly weathered soils,
mainly Oxisols (Espinosa et al. 2018). In Brazil, ten
composite soil samples were collected from the
Paraı́ba do Sul River valley (Tremembé, São Paulo),
one of the main rice-producing areas in the state of São
Paulo (Fig. 1e). The climate in the study area is
subtropical, and strongly weathered soils have devel-
oped on fluvial sediments, showing clear redoximor-
phic features and leading to Aquepts-type soils (Soil
Taxonomy 2014).
Commercial rice sampling
Commercial rice grains (polished, brown, parboiled)
were bought in local retail markets in Latin America,
i.e. Ecuador (16 samples), Brazil (6 samples) and Peru
(3 samples), and in the Iberian Peninsula region, i.e.
Spain (13 samples) and Portugal (2 sample) (Supple-
mentary Table S1; Supplementary material 1).
Field rice plant sampling
In order to evaluate arsenic partitioning in rice plants
from Ecuador, 55 grain samples, 13 stem samples, 12
leaf samples and 9 samples from other rice parts or by-
products (husk, discarded rice, polishing dust) were
obtained (Supplementary Table S1, Supplementary
material 2). For field samples (grains and whole
plants), 5–8 plants were combined. In the laboratory,
plant samples were rinsed 3–5 times with ultra-pure
water (Millipore). Dehusked rice grains (field grains)
were separated, and stems, leaves and rice husks were
dried at 45 °C, ground and stored in plastic bags until
123
Environ Geochem Health
analysis. Field rice grain samples were only collected
in the coastal provinces (El Oro, Guayas and Los Rı́os;
Map 1). In the province of Orellana, rice plants were
not fully developed at the time of sampling, and
therefore, only plants without grain were sampled.
Only commercial rice and rice processing by-products
obtained directly from local producers were analysed.
All rice plant and grain samples were first washed
once with pressurized tap water and twice with ultra-
pure water (Milli-Q); the samples were then dried at
45 °C, ground in an agate mill and stored in
polyethylene bags until analysis.
Analysis
Soil analysis
Soil pH, redox potential (Eh) and electrical conduc-
tivity were determined in situ with portable electrodes
(HANNA instruments INC, Woonsocket, RI, USA).
The Eh values were corrected by adding the potential
of a reference electrode (? 244 mV). Total organic
carbon (TOC) was determined in previously ground
soil samples, with a Leco100 S–C 144DR analyser
(LECO Corporation, St. Joseph, MI, USA). Particle
size was determined by the pipette method, following
Gee and Bauder (1986). Bioavailable As (AsMe) was
extracted by the Mehlich 3 method (Mehlich 1984),
and amorphous Fe (FeOx) and Al (AlOx) oxides and
hydroxides were extracted with a solution of 0.2 M
ammonium oxalate and 0.2 M oxalic acid 0.2 M at pH
3 (Blakemore 1978). The total concentration of arsenic
(total As) was extracted by acid digestion of soil
samples (9 ml of 14.4 M HNO3: 3 ml of 12 M HCl,
Merck, Darmstadt, Germany) in a microwave diges-
tion system (Milestone ETHOS-1) for 25 min. The
concentrations of total As and AsMe were determined
by ICP-OES (Perkin Elmer, Optima model 4300 DV,
Sunnyvale, CA, USA). Certified soil standards (SRM
2709a, SMR2710a, SRM2711a by NIST, USA) were
analysed, to validate the total As extraction method,
and the As recovery rate was [ 90%.
Mineralogical analysis of the clay fraction
(\ 2 lm) was carried out by X-ray diffraction
(XRD) analysis. Oriented aggregates of the clay
fraction saturated with Mg2? and random powder
mounts of unsaturated clays, silt and sand (fine and
coarse) fractions on glass slides were analysed. The
Mg2?-saturated samples were processed like oriented
Environ Geochem Health
aggregates (Mg) and were also solvated in glycerol
(Mg-Gli). These samples were also analysed after
heating for 3 h at 550 °C and 700 °C (Mg-K550 and
Mg-700) (Jackson 1979).
The XRD patterns were obtained in a Shimadzu
XRD 6000 diffractometer (Shimadzu Corporation,
Tokyo), by applying Cu-Ka radiation with a graphite
monochromator, at 40 kV and 30 mA current, at a
velocity of 1.0° 2h min-1 and a step size of 0.02° 2h.
The analyses were conducted in the range 2°–40° 2h
for oriented aggregates and the range 3°–70° 2h for
random powder samples.
Analysis of rice plants and grain
The tAs contents and contents of the organic (DMA,
MMA and arsenobetaine, AsB) and inorganic forms
[As(III) and As(V)] were determined in rice grain and
whole-plant samples.
The tAs was quantified in 0.5–1.0 g of plant sample
digested with a suprapure mixture of HNO3 and H2O2
according to Meharg and Rahman (2003): 5 mL
HNO3 (65%), 1 mL of H2O2 33% and 5 mL Milli-Q
water (w/v). The samples were left overnight before
being placed on a heating plate (Perkin Elmer SPB
48-50) at 95 °C for 3 h. The extract was filtered
through a 0.45-lm filter. The total As content was
determined by ICP-MS (Agilent Technologies, Palo
Alto, CA, USA).
Speciation of As was performed on 0.5 g aliquots of
rice plant samples, which were digested in 10 mL of
1% HNO3 (* 0.17 M) at 95 °C for 90 min in a
microwave digestion system (Milestone ETHOS-1)
(Zhu et al. 2008; Huang et al. 2010; Chen et al. 2018;
Ma et al. 2014). The samples were centrifuged at
10,000 rpm at 4 °C for 15 min, and supernatant was
filtered through a 0.45-lm filter and conserved at
- 20 °C until analysis. The different inorganic
[As(III) and As(V)] and organic (AsB, DMA and
MMA) forms were separated and quantified by HPLC
(Varian Prostar, Spectralab Scientific, Toronto,
Canada) coupled to an ICP-MS system (Varian
820-MS) (for further details of the method, see
Supplementary Material 1, Figs. S1, S2). The use of
1% HNO3 may overestimate the concentrations of
As(III), since HNO3 at concentrations below 0.28 M
(* 1.8%) could lead to a reduction of As(V) to As(III)
by thiolate compounds which are released during the
extraction of rice grains (Huang et al. 2010).
Standard reference material (SRM) (rice flour
1568b, NIST USA) was analysed (n = 4) at the same
time as the test samples. Mean values obtained for the
different As species in the SRM are as follows:
iAs 0.098 ± 0.011 mg kg-1, DMA 0.203 ± 0.01
mg kg-1 and MMA 0.018 ± 0.001 mg kg-1 (as
mean ± standard deviation), corresponding to recov-
ery percentages of 107 ± 12%, 113 ± 4% and
117 ± 7%, respectively (Supplementary Material 2).
The limit of detection (LOD) was determined for each
form as 2.5 times the standard error of the blank
(n = 4; Bruland et al. 1979): As(III) 6 lg kg-1,
As(V) 15 lg kg-1, DMA 13 lg kg-1, MMA
11 lg kg-1 and AsB 0.011 lg kg-1. The mean con-
centration and percentage recovery for tAs in SRM
(n = 4) were 0.349 ± 0.033 mg kg-1 and
123 ± 12%, respectively (LOD, 3 lg kg-1). Blank
values for tAs and As forms were 2–5 lg kg-1 (for
further details on the method, see Supplementary
Material 1).
The tAs and arsenic species were determined by the
Research Support Resources and an external projec-
tion area (RIAIDT, https://www.usc.es/gl/
investigacion/riaidt) of the general services unit of
the University of Santiago de Compostela. Blank
correction was applied to all concentrations reported
in this study. The concentrations of tAs and As species
were calculated on a dry weight (dw) basis.
Phytolith analysis in stems and husks
Phytoliths are microscopic silica bodies that are
abundant within intercellular spaces as well as inside
the cells of numerous plants that absorb orthosilicic
acid (Esteban et al. 2018; Piperno 2006). Interest in the
study of phytoliths is due to the similar structure of
orthosilicic acid and arsenite. The route of entry of
As(III) in the roots may be the same as that of silicon
(Meharg and Zhao 2012), and phytoliths may act as As
sinks (Meharg and Zhao 2012).
Phytoliths from husks and stems were extracted
according to Parr et al. (2001): 10 g aliquots of plant
sample were placed in porcelain plates and calcined
overnight at 600 °C. The remaining ashes were treated
with 20 ml H2O2 (30%, Merk) at 85 °C for 1 h to
extract the As associated with organic carbon; the
residue was then treated with a solution of 0.2 M
ammonium oxalate and 0.2 M oxalic acid for 8 h to
extract the As associated with carbonates, oxides and
123

hydroxides Fe/Al. Finally, the arsenic in the phytoliths
was extracted with 10 ml of 0.2 M NaOH for 168 h at
room temperature with continuous end-over-end
shaking (see Georgiadis et al. 2013, for further
details). The supernatant from each extraction was
removed after centrifugation at 10,000 rpm at 4 °C for
15 min, and residues were washed three times with
Milli-Q water and the supernatant was discarded each
time (Buján 2013). The concentration of As was
determined by ICP-MS (Agilent Technologies, Palo
Alto, CA, USA). Scanning electron microscopy
(SEM) and elemental analysis (EDS, energy-disper-
sive X-ray spectrum) of stem phytoliths were also
carried out in a LECO 435 VP analyzer. Microanalysis
was carried out with an OXFORD microprobe (model
ISIS 300) after internal calibration at 20 kV and a
waiting time of 100 s.
Statistical analysis
Analysis of variance and a Tukey’s post hoc HSD test
were used to test differences between means at a
significance level of p \ 0.05.
Results
General characteristics of rice soils
Soil pH in Ecuador and Brazil was neutral to slightly
acidic (range: 5.9–6.7, Table 1), as usually observed
for saturated soils in which reduction processes
consume protons, with pH being buffered by the
diffusion of CO2 (Vepraskas and Craft 2016). Extre-
mely acidic values (pH = 3.6) were observed in some
of the samples from the coastal provinces of Ecuador
(Guayas, Los Rı́os and Oro). Redox potential values
indicated oxic (Eh [ 300 mV) and suboxic conditions
(200–300 mV), except for some samples from Brazil,
which indicated anoxic conditions (Eh \ 100 mV).
Total organic C (TOC) was low: 1.9 ± 0.6% in the
coastal provinces and 4.4 ± 1.4% in samples from the
province of Orellana. The clay fraction was predom-
inant in soils from the coastal provinces of Ecuador and
in the Brazilian soils (23–88% and 37–46%, respec-
tively), while sand was the dominant fraction in soils
from Orellana (46–89%).
Total Fe concentrations were higher in soils from
the coastal provinces of Ecuador (mean value:
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Environ Geochem Health
4.2 ± 1.0%; Table 1) than in soils from Orellana
province (2.7 ± 0.7%) and Brazil (mean value
1.4 ± 0.4%). However, concentrations of amorphous
Fe/Al oxides (FeOx, AlOx) in soils from Orellana
province (FeOx: 0.72 ± 0.10%; AlOx: 1.30 ± 0.34%)
were much higher than in soils from the coastal
provinces (FeOx: 0.51 ± 0.20%; AlOx: 0.19 ± 0.12%,
Table 1). Thus, in Orellana province, the AlOx-
? ‘FeOx diagnostic criterion was higher than 2 for
some samples, a characteristic value of soils with
andic properties (e.g. Andosols), which have a high
fixation capacity for oxyanions such as arsenate and
phosphate (see e.g. IUSS Working Group WRB 2014).
The clay fraction mineralogy revealed three differ-
ent geochemical environments. Soils from the coastal
provinces of Ecuador (Guayas, Los Rı́os and Oro) are
characteristic of a moderately weathered soil environ-
ment, with a predominance of 2:1 phyllosilicates,
while soils in Orellana (eastern province with tropical
rainforest climate) are characterized by minerals with
a low degree of crystallinity. Poorly crystalline Fe and
Al oxides and hydroxides are characteristic of soils
affected by volcanic ashes, which is consistent with
the results of the ammonium oxalate extraction. Soils
from Brazil (Sao Paulo), developed from granitoid
gneisses, migmatites and biotite–gneiss (Ovalle et al.
2013) are highly weathered soils mainly composed of
kaolinite and crystalline Fe and Al oxides and
hydroxides (Fig. 2).
More specifically, soils from the coastal region of
Ecuador have developed on a substrate composed of
fluvial–marine sediments with a high proportion of
clay ([ 40%) in a flat, poorly drained area. Vertisol is
the most frequently described soil type in the area,
often showing redoximorphic features (Typic Haplud-
erts, Aeric Endoaquerts, Aquic Hapluderts; Moreno
et al. 2018). The clay fraction is mainly composed of
smectitic minerals, kaolinite, mica and quartz
(Fig. 2a). The marked presence of 2:1 minerals in an
area with subtropical humid conditions is considered a
result of the hydromorphic conditions found in rice
plantations, which promote the resilication of sec-
ondary minerals (bisialitization).
The province of Orellana is located in the Ecuado-
rian Amazon rainforest, the climate of which is
classified as a uniformly megathermal, very humid
tropical climate with high temperatures (average
annual temperature [ 22 °C) and precipitation
(2500–4500 mm) throughout the whole year (Sánchez
Environ Geochem Health
Table 1 Mean (± standard deviation, SD) values of soil properties (pH, Eh), composition (texture, total Fe, TFe, amorphous Fe oxyhydroxides, FeOx), total As and bioavailable

(0.009 ± 0.42)
0.130 ± 0.092

0.012 ± 0.003

0.127 ± 0.093

0.023 ± 0.008
(0.009–0.014)

(0.015–0.031)
et al. 2018). These conditions promote the rapid

(0.06–0.42)
AsMe weathering of primary minerals and the formation of
strongly weathered Oxisol-type soils (i.e. Typic

80

83
Hapludox), the mineralogy of which is dominated by

5
1:1 phyllosilicates such as kaolinite and Fe (goethite

1.07 ± 0.44

2.11 ± 1.00
(1.52–17.1)

(0.61–1.64)

(0.61–17.1)

(1.16–3.73)
4.86 ± 3.2

4.56 ± 3.2
and haematite) and Al (gibbsite) oxides and hydrox-
Mg kg-1
Total As

ides (Sánchez et al. 2018). However, the influence of

101
ash from nearby volcanoes (Reventor and Sumaco)
93

6
and processes related to relief and hydromorphy create
0.19 ± 0.12

1.11 ± 0.43

a more complex mineralogical assemblage. In the soils

(0.05–0.41)

(0.75–1.72)

from Orellana, the clay fraction is mainly constituted

AlOx

by kaolinite, with the presence of vermiculite, potas-

na
7

sium feldspars and mica, as well as pyrophyllite

(Fig. 2b). XRD analysis revealed that non-crystalline
0.51 ± 0.20

0.72 ± 0.10
(0.11–1.81)

(0.57–0.91)

minerals are an important component of the clay

FeOx

fraction, which can be explained by the influence of

36

na
8

volcanic ash in the area (Sánchez et al. 2018). The

presence of pyrophyllite (a mineral of metamorphic
4.2 ± 1.0

2.7 ± 0.7

4.1 ± 1.1

1.4 ± 0.4
(2.4–7.1)

(1.8–3.6)

(1.8–7.1)

(1.3–1.8)

origin) is a common mineralogical feature in soils in

TFe

the eastern area of the Amazonian lowlands (De-

83

91
8

larmelinda et al. 2017).

The Paraiba valley soils (São Paulo, Brazil) have
28 ± 20

67 ± 18

35 ± 24
(0.9–64)

(0.9–89)
(46–89)

(29–42)
35 ± 9
Sand

developed over fluvial sediments in a geological

23

29
6

environment dominated by granitic rock and gneiss,

under a subtropical humid climate. Soil mineralogy is
24 ± 13

22 ± 12

(21–25)
17 ± 8

23 ± 3
(3–53)

(6–25)

(3–53)

typical of highly weathered soils under tropical

Silt

23

29

environments and is essentially composed of kaolinite

6

and Fe and Al oxides and hydroxides (Fig. 2c).

49 ± 16

17 ± 14

42 ± 20
(23–88)

(37–46)
42 ± 6
(6–37)

(6–88)
Clay

Total and bioavailable arsenic in soils

23

29
6

2
As (AsMe). Minimum and maximum values are shown in brackets

The total As concentrations in soils from Ecuador

1.9 ± 0.6

4.4 ± 1.4

2.2 ± 1.1
(0.7–3.2)

(2.1–6.1)

(0.7–6.1)

ranged from 0.61 to 17.1 mg kg-1 (mean,

TOC

4.36 ± 3.40 mg kg-1) (n = 101). The mean concen-

61

69
na
%

tration of tAs was highest in soils from the province of

226 ± 93

226 ± 93

Los Rı́os (7.49 mg kg-1), followed by GuayAs

(92–485)

(92–485)

(186–14)
86 ± 60

(4.0 mg kg-1) and El Oro (3.30 mg kg-1). The lowest

MV
Eh

55

55

12
na

concentration corresponded to soils from Orellana

province (1.07 mg kg-1) and was significantly lower
6.7 ± 0.45
6.4 ± 0.6

5.9 ± 0.1

6.3 ± 0.6
(3.6–7.4)

(5.8–6.0)

(3.6–7.4)

(5.9–7.2)

than in soils from the coastal provinces [F(3,47) = 8.9,

p \ 0.05—Supplementary material Tables S3 and
PH

53

61

12
8

S4].
The bioavailable As fraction (AsMe) accounted for
Ecuador (all provinces)

1–5% of total As, reaching a mean value of

Brazil—Sao Paulo
Orellana province
Coastal provinces

0.130 ± 0.09 mg kg-1 in coastal provinces and of

0.012 ± 0.003 mg kg-1 in the tropical region
(Table 1). Arsenic bioavailability was also signifi-
Sample

Ecuador

Range

Range

Range

Range

cantly lower in Orellana than in coastal provinces

n

[F(1,81) = 4.9, p \ 0.05, Supplementary Table S5].

n

123
 Environ Geochem Health

123
 Environ Geochem Health

b Fig. 1 Location of sampling areas in Ecuador and Brazil. The

Ecuadorian provinces of El Oro, Guayas and Los Rı́os lie on
fluvial–marine sediments and represent an environmentally
homogeneous area, and they were therefore considered together
as ‘‘coastal provinces’’. By contrast, the province of Orellana is
located in the Amazonian region, characterized by high
temperatures and precipitation levels throughout the year and
by strongly weathered soils

In the Brazilian soils, the mean tAs concentration

was 2.11 ± 1.00 mg kg-1, and the bioavailable frac-
tion was 0.023 ± 0.007 mg kg-1 (Table 1).

Total arsenic (tAs) content of rice grains

Latin America

The mean tAs concentration in rice samples from

Ecuador was 0.130 ± 0.034 mg kg-1 for commercial
polished rice (range: 0.090–0.231 mg kg-1),
0.221 ± 0.014 mg kg-1 for brown rice (range:
0.097–0.231 mg kg-1) and 0.156 ± 0.021 mg kg-1
for parboiled rice (range: 0.137–0.178 mg kg-1)
(Table 2). The values for rice grains obtained from
cropland were similar to those obtained for commer-
cial rice (mean value: 0.107 ± 0.055 mg kg-1). Max-
imum tAs values in rice grain were obtained in Oro
province (0.186 ± 0.040 mg kg-1), followed by
Guayas province (0.097 ± 0.037 mg kg-1) and Los
Rı́os province (0.055 ± 0.043 mg kg-1).
The concentration of tAs was higher in rice plants
than in grains (Table 3). The mean values in husk were
0.195 ± 0.067 mg kg-1, ranging from 0.105 to
0.262 mg kg-1. The tAs concentrations were much
higher in rice dust (a by-product of rice grain
polishing) (1.340 mg kg-1). The lowest tAs values
were found in samples from Orellana province (brown
rice: 0.019 mg kg-1, discarded rice: 0.012 mg kg-1
and rice dust: 0.016 mg kg-1).
The mean concentration of tAs in commercial
polished rice from Brazil was Fig. 2 X-ray diffraction (XRD) patterns of soil samples from
0.166 ± 0.016 mg kg-1, while the mean value for Ecuador and Brazil. a XRD pattern of soil samples from the
parboiled polished rice was 0.160 mg kg-1 and for coastal zone, b XRD pattern of soil samples from Orellana
brown rice 0.220 ± 0.020 mg kg-1. The mean con- province, c XRD pattern of soil samples from Brazil (Sao
Paulo). V: vermiculite; K: kaolinite; S: smectite; Mi: mica; Fd:
centration in polished rice from Peru was K feldspar; Q: quartz; Py: pyrophyllite; HIV: hydroxy-
0.138 ± 0.039 mg kg-1. interlayered vermiculite; HIS: hydroxy-interlayered smectite

123
 Environ Geochem Health

iAs/tAs Iberian Peninsula

0.70
0.72
0.58
0.79

0.59
0.68
0.69

0.94

0.41
0.35
0.51
In the Iberian Peninsula, the mean tAs concentration
0.130 ± 0.034
was 0.191 ± 0.066 mg kg-1 in polished rice and
0.221 ± 0.014
0.156 ± 0.021
0.138 ± 0.017

0.166 ± 0.016
0.220 ± 0.020

0.138 ± 0.039

0.191 ± 0.066
0.310 ± 0.128
0.310 ± 0.128 mg kg-1 in brown rice, with a maxi-
mum value of 0.438 mg kg-1 (Table 2).

0.160

0.307
TAs
Table 2 Concentration of total As and forms of As (mg kg-1) in commercial rice samples from different countries (mean ± SD). LD: limit of detection

Arsenic forms in commercial rice grains

0.038 ± 0.011
0.056 ± 0.010
0.055 ± 0.018
0.128 ± 0.012

0.074 ± 0.020
0.067 ± 0.054

0.026 ± 0.006

0.093 ± 0.054
0.087 ± 0.066
Latin America: Ecuador, Peru and Brazil
oAs

0.092

0.180
P

The As(III) form was the dominant species in com-

mercial samples of polished, brown and parboiled rice
0.004 ± 0.008

0.009 ± 0.013
0.007 ± 0.008

0.002 ± 0.004
0.012 ± 0.001

0.005 ± 0.002

0.012 ± 0.013
0.004 ± 0.002
from Latin America, whereas the organic DMA form
prevailed in all samples from the Iberian Peninsula,
MMA

\ LD

0.029

0.40
except for brown rice, in which As(III) is the dominant
As form (Table 2). The tAs content in polished rice
0.031 ± 0.008
0.046 ± 0.009
0.042 ± 0.020
0.013 ± 0.007

0.071 ± 0.021
0.055 ± 0.053

0.021 ± 0.005

0.080 ± 0.046
0.081 ± 0.060

from Latin American and the Iberian countries was

significantly different (Latin Amer-
DMA

ica = 0.120 ± 0.061 mg kg-1, n = 46; Iberian Penin-

0.061

0.140

sula: 0.203 ± 0.096 mg kg-1, n = 10;

F(1,54) = 7.17, p = 0.003, Fig. 3) owing to the
0.003 ± 0.001
0.010 ± 0.001
0.004 ± 0.004
0.002 ± 0.001

0.001 ± 0.001
0.002 ± 0.003

significantly higher concentrations of DMA in the

\ LD-0.001

\ LD-0.001

latter (DMA in the Iberian Penin-

\ LD

\ LD
0.002
AsB

sula = 0.075 ± 0.030 mg kg-1; DMA in Latin Amer-

ica: 0.041 ± 0.022 mg kg-1; p \ 0.05,
F(1,54) = 7,45), while no significant differences were
0.053 ± 0.027
0.105 ± 0.052
0.090 ± 0.031
0.106 ± 0.014

0.096 ± 0.007
0.150 ± 0.039

0.131 ± 0.026

0.080 ± 0.042
0.118 ± 0.071
inorg As

observed in the remaining As forms (Fig. 3).

In Ecuador, As(IIl) was the dominant form in
0.110

0.157
P

commercial polished rice grain (mean concentration:

0.037 ± 0.018 mg kg-1; 40% of tAs), followed by
0.016 ± 0.012
0.049 ± 0.056
0.036 ± 0.002
0.033 ± 0.011

0.029 ± 0.008
0.037 ± 0.001

0.062 ± 0.005

0.025 ± 0.019
0.028 ± 0.014

DMA (0.031 ± 0.008 mg kg-1; 34% of tAs),

As(V) (0.016 ± 0.012 mg kg-1, 18% of tAs) and
As(V)

0.034

0.067

very low concentrations of MMA

(0.004 ± 0.008 mg kg-1, 4% of tAs) and AsB
(0.003 ± 0.001 mg kg-1, 4% of tAs). The same trend
0.037 ± 0.018
0.057 ± 0.003
0.054 ± 0.030
0.073 ± 0.017

0.067 ± 0.012
0.113 ± 0.040

0.069 ± 0.021

0.055 ± 0.027
0.091 ± 0.057

was observed for parboiled rice: As(III)

(0.054 ± 0.030 mg kg-1, 37% of tAs) [ DMA
As(III)

0.075

0.090

(0.042 ± 0.020 mg kg-1, 29% of

tAs) [ As(V) (0.036 ± 0.002 mg kg-1, 25% of
tAs) [ MMA (0.009 ± 0.013 mg kg-1, 6% of
Field samples (n = 8)

tAs) [ AsB (0.004 ± 0.004 mg kg-1, 3% of tAs).

Polished (n = 10)

Parboiled (n = 3)

Parboiled (n = 1)

Parboiled (n = 1)
Polished (n = 4)

Polished (n = 3)

Polished (n = 9)
Brown (n = 3)

Brown (n = 2)

Brown (n = 2)

Inorganic As accounted for more than 65% of the

tAs in brown rice. As(III) was the dominant form
(0.057 ± 0.003 mg kg-1, 36% of tAs), followed by
Type

Iberian Peninsula

As(V) (0.049 ± 0.056 mg kg-1, 30%), DMA

(0.046 ± 0.009 mg kg-1, 28% of tAs) and AsB
Country

Ecuador

(0.0010 ± 0.001 mg kg-1, 6% of tAs). The

Brazil

Peru

123
Environ Geochem Health

Table 3 Concentration of total As and forms of As (mean ± SD) in stem and leaf field samples from different provinces of Ecuador
Coastal provinces Oriental province (Orellana) p
Stem, n Leaf, n Stem, n Leaf, n Stem Leaf
mg kg-1 dw

tAs 0.675 ± 0.763 0.761 ± 0.667 0.042 ± 0.042 0.047 ± 0.018 \ 0.001 \ 0.001
As(III) 0.194 ± 0.083 0.249 ± 0.135 0.004 ± 0.004 0.003 ± 0.003 ns ns
As(V) 0.409 ± 0.538 0.529 ± 0.531 0.029 ± 0.025 0.026 ± 0.006 \ 0.01 \ 0.001
iAs 0.599 ± 0.608 0.778 ± 0.637 0.034 ± 0.029 0.030 ± 0.006 \ 0.001 \ 0.001
DMA 0.044 ± 0.049 0.039 ± 0.036 0.005 ± 0.012 0.003 ± 0.004 ns ns
MMA 0.025 ± 0.020 0.028 ± 0.021 0.001 ± 0.002 0.001 ± 0.001 ns ns
AsB 0.015 ± 0.025 0.004 ± 0.003 0.003 ± 0.002 0.014 ± 0.011 ns ns
oAs 0.091 ± 0.088 0.070 ± 0.055 0.008 ± 0.014 0.017 ± 0.016 ns ns
p indicates the existence of significant differences for stems and leaves between locations

concentrations of MMA were very low (below the LD) As(V) (0.033 ± 0.011 mg kg-1, 26% of tAs), DMA
(Table 2). (0.013 ± 0.007 mg kg-1, 10% of tAs), MMA
The concentrations of iAs were significantly higher (0.007 ± 0.008 mg kg-1, 5% of tAs) and AsB
in field rice grain samples than in commercial rice (0.0015 ± 0.005 mg kg-1, 1% of tAs).
grains (Table 2, F(1,22) = 9.3, p \ 0.05, Supplemen- In Brazil, As(III) was also the dominant form in
tary Table S6). As in the aforementioned rice types, brown rice 0.113 ± 0.040 mg kg-1, 52% of tAs) and
As(III) was the dominant form As(III) parboiled rice (0.075 mg kg-1, 38% of tAs), followed
(0.073 ± 0.017 mg kg-1, 57% of tAs), followed by by DMA (brown rice: 0.055 ± 0.053 mg kg-1, 25%

Fig. 3 a Mean (± standard deviation, SD) total As and
b comparison of inorganic and organic As fractions in
commercial rice from the Latin American and Iberian Peninsula
countries. In a different letters indicate significant differences
(p \ 0.05) between the tAs content of rice from Latin America
and the Iberian Peninsula. In b different letters indicate
significant differences (p \ 0.05) between As forms in rice
from Latin America and the Iberian Peninsula [e.g. the same
letter (a) in As(III) in Latin America and Iberian Peninsula
indicates than there are no significant differences in As(III)
between both geographical areas]

123

of tAs; parboiled rice: 0.061 mg kg-1, 30% of tAs)
and As(V) (brown rice: 0.037 ± 0.001 mg kg-1,17%
of tAs; parboiled rice 0.034 mg kg-1,17% of tAs). In
polished rice from Brazil, the mean concentrations of
As(III) (0.067 ± 0.012 mg kg-1, 39% of tAs) and
DMA (0.071 ± 0.021 mg kg-1, 42% of tAs) were
similar, while the mean concentration of As(V) was
lower (0.029 ± 0.008 mg kg-1, 17% of tAs)
(Table 2).
The concentrations of As(III) (0.069 ± 0.021
mg kg-1, 44% of tAs) and As(V) (0.062 ±
0.005 mg kg-1, 41% of tAs) were similar in polished
rice from Peru. The DMA concentration was lower
(0.021 ± 0.005 mg kg-1, 13% of tAs), and the AsB and
MMA concentrations were much lower than in the same
type of rice from Ecuador and Brazil (Table 2).
Iberian Peninsula
DMA was the dominant form in the rice from the
Iberian Peninsula, followed by As(III) and As(V) and,
to a lesser degree, MMA and AsB (Table 2). More
specifically, DMA was the predominant As form
(DMA: 0.080 ± 0.046 mg kg-1, 42% of tAs), fol-
lowed by As(III) (0.058 ± 0.029 mg kg-1, 37% of
tAs) and As(V) (0.027 ± 0.020 mg kg-1, 15% of
tAs). MMA and AsB concentrations were very low,
generally below the LOD. The As concentration was
much lower in parboiled rice than in polished rice.
Brown rice contained similar amounts of As(III)
(0.091 ± 0.057 mg kg-1: 45% of tAs) and DMA
(0.081 ± 0.060 mg kg-1: 40% of tAs) and lower
amounts of As(V) (0.028 ± 0.014 mg kg-1: 14% of
tAs).
Finally, the higher concentration of As(III) than
As(V) in rice grain could be due to the reduction of
part of the As(V) by thiolates compounds in rice grains
during the extraction process (Huang et al. 2010).
Arsenic content in rice plants (stems, leaves
and phytoliths) from Ecuador
Total arsenic in stems and leaves
The mean tAs content was 0.285 ± 0.288 mg kg-1 in
leaves and 0.883 ± 4.166 mg kg-1 in stems and
varied widely among samples in both cases. The mean
tAs contents in leaves (0.562 ± 0.234 mg kg-1) and
stems (2.551 ± 7.43 mg kg-1) were highest in plants
123
Environ Geochem Health
from El Oro followed by plants from the Guayas
province (leaf: 0.275 ± 0.282 mg kg-1; stem:
0.201 ± 0.180 mg kg-1), Rı́os (0.087 ± 0.036
mg kg-1 in leaves and 0.059 mg kg-1 in stems) and
finally Orellana province (0.047 ± 0.018 mg kg-1 in
leaves and 0.042 ± 0.042 mg kg-1 in stems)
(Table 3). The As concentrations in stems and leaves
were significantly higher in plants from coastal
provinces than in plants from the tropical rainforest
province (Orellana) [F(1, 175) = 60.6, p \ 0.05], but
there were no differences in relation to the different
plant parts [F(1,175) = 0.62, p [ 0.05] (Table 4,
Supplementary Tables S7, S8, S9).
Arsenic forms in stems and leaves
The dominant forms in stems and leaves were
As(V) [ As(III) [ DMA, while the concentrations
of these forms were much lower in MMA and AsB
(Table 3). The mean concentrations in stems were as
follows: As(V), 0.204 ± 0.400 mg kg-1; As(III),
0.092 ± 0.112 mg kg-1 and DMA, 0.023 ± 0.039
mg kg-1. The mean concentrations in leaves were as
follows: As(V), 0.236 ± 0.412 mg kg-1; As(III),
0.106 ± 0.150 mg kg-1; and DMA, 0.018 ± 0.029
mg kg-1 (Table 3).
The amounts of As accumulated in leaves and
stems were similar for all chemical species
[F(7,175) = 0.62, p [ 0.05]. However, concentrations
of inorganic species were significantly higher in rice
plants (both leaves and stems) grown in the coastal
provinces than in those from Orellana province; the
differences between provinces can be attributed to
As(V) (Table 3 and Tables S7–S9). Consequently, the
concentrations of organic species in rice plants from
the two provinces were similar, despite the large
differences in tAs.
Total arsenic in phytoliths
High production of biogenic silica (phytoliths) was
observed by SEM (Fig. 4 A–D). Sequential extraction
of As in ash samples showed that higher concentra-
tions of As are associated with recalcitrant organic
matter (AsH2O2 = 0.274–3.049 mg kg-1), and the
highest values corresponded to stem samples
(Fig. 4e). Mean concentrations of As associated with
carbonates and oxides (soluble in ammonium oxalate)
ranged between 0.062 and 0.358 mg kg-1 (Fig. 4f).
Environ Geochem Health

iAs/tAs
The As concentration was lower in phytoliths than in

0.86

1.00
0.94
the previously mentioned fractions, ranging between

na

na
0.012 and 0.081 mg kg-1 (Fig. 4g).

0.228 ± 0.071
As total

0.261 Discussion

1.340

0.012
0.016
Spatial variation in arsenic contents in rice grains
As organic

0.031 ± 0.012

The tAs contents in commercial rice from the Latin

American countries were similar (mean values for
0.000
0.001
P

Ecuador: 0.109 ± 0.066 mg kg-1, Peru: 0.138 ±

na

na

0.040 mg kg-1, Brazil: 0.171 ± 0.046 mg kg-1) and

0.010 ± 0.003

not significantly different [F(4,51) = 2.89, p [ 0.05].

However, the tAs concentrations were significantly
MMA

\ LD
\ LD

higher in commercial polished rice from the Iberian

na

na

Peninsula than in the same from Latin America

(Fig. 4a). These results are consistent with previous
0.017 ± 0.006

findings, in which rice produced in Spain and Portugal

was demonstrated to contain relatively high amounts
DMA

\ LD
0.001

of tAs(see e.g. Torres-Escribano et al. 2008; Signes-

na

na

Pastor et al. 2016). In this respect, Signes-Pastor et al.

0.002 ± 0.001

(2016) found that around 26% of commercial rice

Table 4 Concentrations of tAs and As forms in different types of rice processing by-products

samples exceeded the permissible As concentration

for infant food production (iAs = 0.100 mg kg-1 for
\ LD
\ LD
AsB

na

na

rice destined for producing food for infants and young

children: UE 2015). However, the chemical species
0.197 ± 0.060
As inorg

responsible for the high As contents in rice from the

Iberian Peninsula were not determined. Our results
Powdered residue generated during the rice polishing process. Rice dust
0.012
0.015

show that the difference between the two agroecolog-

P

na

na

ical areas (Iberian Peninsula and Latin America) is

caused by the high DMA content of rice from the
0.164 ± 0.055

Iberian Peninsula (Fig. 4b): this was the only As

fraction that was statistically significantly higher than
As V

0.011
0.011

in the rice from Latin American countries considered

na

na

together, while iAs concentrations in rice were similar

0.033 ± 0.026

in both geographical areas (iAs in the Iberian Penin-

Rice grain rejected for human consumption

sula: 0.086 ± 0.048 mg kg-1; Latin America:

As III

0.086 ± 0.042 mg kg-1, F(4,51) = 0,12, p [ 0.05).

na not analysed, LD limit of detection
0.001
0.004
na

na

Moreover, our findings suggest that the relation-

ships between As species in rice grain vary widely
Residue polishing riceb (n = 1)

depending on the tAs concentration. The iAs concen-

tration increases proportionally to tAs in rice grain
when tAs is low, while the iAs/tAs ratio in rice grain
Waste ricea (n = 1)

Wate ricea (n = 1)
Rice dustb (n = 1)
Orellana province

decreases rapidly at tAs values higher than approxi-

Coastal provinces

mately 0.200 mg kg-1 (Fig. 5a). Conversely, the

Husk (n = 5)

percentage of oAs, particularly of DMA—and to a

Location

lesser extent MMA—increases with tAs concentra-

tion. Thus, at high concentrations of tAs(around
b
a

123

Fig. 4 a–c Scanning electron micrographs (SEM) and d en-
ergy-dispersive X-ray spectroscopy (EDS) images of rice
phytoliths, showing high silicon concentrations. e Arsenic
concentration associated with recalcitrant organic matter.
f Arsenic concentration associated with oxides. g Arsenic
0.300 mg kg-1), the dominant As form in rice grain is
DMA (Fig. 5b), which explains the lower iAs/tAs
ratio in rice from the Iberian Peninsula than in rice
from the other countries (Fig. 5c).
123
Environ Geochem Health
concentration in rice phytoliths. Different letters indicate
significant differences (p \ 0.05) between As concentrations
in each extract (H2O2, ammonium oxalate and NaOH) for stems
and husks
Previous studies have shown that inorganic As
accumulates preferentially in the ovular vascular trace
(OVT), located on the surface of the grain, whereas
DMA remains in the endosperm (Carey et al. 2011;
Lombi et al. 2009; Zhao et al. 2013). This may be
Environ Geochem Health
particularly important in relation to the results
obtained. Rice plants have been demonstrated to be
incapable of methylating inorganic As forms, and it is
thought that DMA is directly assimilated from the soil
by the plant (Lomax et al. 2012; Jia et al. 2013). Soil
microorganisms are the main species responsible for
converting inorganic As(III) into methylated As
species (Zhao et al. 2013). Several factors contribute
to the As methylation process under flooded condi-
tions, such as the activity of anaerobic microorgan-
isms, extended flooded conditions for As(V) reduction
and increased substrate availability for As methylation
(Suriyagoda et al. 2018). In addition, the reductive
dissolution of Fe oxyhydroxides leads to desorption of
methylated organic and inorganic As species into the
soil solution, favouring the bioavailability of these As
forms to the plant (Mladenov et al. 2010).
The rate of uptake of DMA by rice roots is lower
than for iAs (around 1:20; Zhao et al. 2013) due to the
lower affinity of transporters for organic As at the
membrane level (Abedin et al. 2002; Raab et al.
2007a). It is not clear why DMA is preferentially
accumulated in rice grain, and membrane transporters
that mediate DMA loading and unloading into the rice
grain remain to be identified (Zhao et al. 2013).
However, other authors have pointed out that DMA
dominance in rice grain may be explained by the fact
that DMA transfers to the top of the plant more
Fig. 5 a Variations in iAs concentration and iAs/tAs ratio with
increasing concentration of tAs in rice grain. This graph was
constructed using data from the present study and data reported
by Meharg et al. (2009), Otero et al. (2016), Signes-Pastor et al.
(2016), Zavala et al. (2008), USFDA (2013) and Williams et al.
(2005). b Variations in concentrations of As forms with
increasing tAs content
efficiently than iAs, reaching the endosperm of the
grain due to its low affinity for the sulphydryl group of
phytochelatins (Norton et al. 2010; Carey et al. 2011;
Wu et al. 2016). By contrast, As(III) has a high affinity
for these groups and can be complexed, sequestered
and stored in vacuoles (Raab et al. 2007a, b), although
it is preferentially stored in stems, in leaves or in the
different grain coverings (ovular vascular trace, or
bran layers) (Lombi et al. 2009). The high iAs
concentrations obtained for husk and rice polishing
dust (iAs/Ast = 0.84–0.94, Table 4) indicate that
dehusking and polishing rice essentially removes iAs
forms (thereby decreasing their intake and the poten-
tial toxicity of the rice) and explain the higher iAs
contents in brown rice (Suriyagoda et al. 2018;
Meharg and Zhao 2012). In our case, considering all
samples of rice grain together, tAs and iAs concen-
tration in brown rice (tAs = 0.236 ± 0.093;
iAs = 0.111 ± 0.050 mg kg-1, n = 7) was signifi-
cantly higher than in polished (tAs: 0.187 ± 0.061,
iAs: 0.064 ± 0.036 mg kg-1, n = 25) and parboiled
rice (tAs: 0.153 ± 0.045; iAs:
-1
0.107 ± 0.032 mg kg , n = 5) [F(2,34) = 4.945,
p = 0.013].
The iAs concentrations in commercial samples
from the countries considered are within previously
reported ranges and are consistent with the data
available in the World Health Organization’s GEMS
Food Database for arsenic (WHO 2018a) (Fig. 6), and
they do not exceed iAs threshold value of
0.200 mg kg-1 established in current EU regulations
(EU 2015).
Arsenic in rice plants in relation to cropland
environment
Arsenic in rice grain
The cropland environment (i.e. water quality, soil
composition and properties) is one of the factors
determining the concentration of As forms in rice
plants (Norton et al. 2012; Khan et al. 2010;
Suriyagoda et al. 2018). The recommended total As
concentration in agricultural soils varies greatly
among countries (5–50 mg kg-1); however, Ewers
(1991) considered an iAs concentration of
20 mg kg-1 as hazardous for cropland soils. Total
concentrations of As in rice cropland soils from
Ecuador and Brazil (see also Segura et al. 2018), as
123

well as As concentrations in rice croplands in the
Iberian Peninsula (range 2.3–17 mg kg-1, median
value 8.7 mg kg-1; Signes-Pastor et al. 2016) were
always below the 20 mg kg-1 threshold. Neverthe-
less, the concentration of bioavailable As for the plant
(AsMe) in rice cropland soils in Ecuador and Brazil
(AsMe) accounted for \ 5% of total As; the As
concentration in soils is therefore within accept-
able levels for rice crops and is comparable to that
Fig. 6 Concentrations of a iAs and b iAs/tAs ratio in rice grain from the countries under study and in other countries. Data for other
countries are taken from GEMS Food Database (WHO 2018)
123
Environ Geochem Health
of uncontaminated soils (Pais and Jones 1997;
Matschullat 2000; Mandal and Suzuki 2002).
The low bioavailability of As may be related to the
high concentration of poorly crystalline Fe oxyhy-
droxides present in the soil (FeOx), as the high
adsorption capacity of these may exert a protective
effect, decreasing the concentration of bioavailable
As. Otero et al. (2016) observed that the concentra-
tions of AsMe and As present in floodwater in rice
croplands were negatively correlated with FeOx
Environ Geochem Health
Fig. 7 Eh–pH conditions in soils and waters and stability fields
of oxyhydroxides of Fe/Mn and arsenate and arsenite Adapted
from Masscheleyn et al. (1991)
concentrations in the soil. However, amorphous Fe
oxyhydroxides (i.e. FeOx) are readily reduced under
anoxic conditions (Canfield et al. 1992). The reduction
of these Fe forms would lead to the release of As into
interstitial water (Williams et al. 2007a, b). Redox
potential and pH values in soils from Ecuador were
measured nearly at the end of the crop season
(3 months), and Eh–pH conditions were observed to
be within the range of stability for Fe oxyhydroxides,
presumably because low concentrations of labile
organic matter limit the activity of Fe(III) oxyhydrox-
ide-reducing bacteria (see de Sousa et al. 2009; Otero
et al. 2016). An increase in labile organic matter,
particularly dissolved organic carbon (DOC), could
increase iAs mobilization and bioavailability (Mlade-
nov et al. 2010). DOC could stimulate Fe(III)-reducing
bacteria (FeRB), promoting a reduction in amorphous
Fe and leading to the release of adsorbed As into the
interstitial water (Chen et al. 2016; Mladenov et al.
2010; Kumarathilaka et al. 2018). In addition, DOC
can compete with iAs for the adsorption sites of Fe
oxyhydroxides (Mladenov et al. 2015).
The incorporation of materials rich in organic
matter (i.e. vermicompost, poultry manure), which
lead to the formation of DOC, has been shown to lead
to a decrease in As concentration in rice grain in As-
contaminated rice croplands, as a result of the high
affinity of organic matter for As (Paikaray et al. 2005).
Williams et al. (2011) concluded that organic matter
may enhance arsenic release from soils while also
reducing its bioavailability by sequestering dissolved
arsenic. The role of organic matter in rice croplands
should therefore be further studied and monitored.
The observed variations in rice from the Iberian
Peninsula and Latin American countries may indicate
differences in terms of rice-producing conditions.
However, no detailed information is available about
the composition or properties of rice cropland soils in
the Iberian Peninsula, and information about micro-
biological diversity in paddy soils is scarce. The study
findings seem to suggest that the effect of the
environment on As content in rice grain is related to
processes that deserve further study. In this respect,
previous studies have established that although the
reason for the geographical variation in the concen-
tration of arsenic forms in grain rice is not clear, it may
be related to differences in soil conditions and/or
microbiological community composition in rice crop-
lands (i.e. aerobic or anaerobic conditions and pres-
ence of methylating microorganisms, etc.) (Xu et al.
2008; Arao et al. 2009; Li et al. 2009; Norton et al.
2013; Zhao et al. 2013; Hu et al. 2015). Likewise, the
variety of rice may also influence the iAs retention
capacity in the stem, thus potentially protecting rice
grain from As accumulation (Suriyagoda et al. 2018).
Total As and As forms in rice plants (stems, leaves
and phytoliths)
Statistical analysis of the data showed that As species
differed significantly in stems and leaves between the
two environmentally different sites (coastal and trop-
ical rainforest provinces; F(7,175) = 11.2, p \ 0.05),
as a result of the prevailing geochemical conditions in
the rice production site, as indicated by the significant
joint effect [F(7, 175) = 9.2, p \ 0.05, Supplementary
Table S7]. Arsenic bioavailability strongly depends on
environmental factors (Zhao et al. 2009), indicating
that the soil As in the Orellana province is not as
bioavailable as in the coastal provinces due to the high
concentrations of poorly crystalline Fe/Al oxides and
hydroxides (bioavailable As in Orellana, AsMe:
0.012 ± 0.003 mg kg-1; bioavailable As in coastal
provinces: AsMe: 0.130 ± 0.092 mg kg-1; F(1,81) =
4.9, p \ 0.05, Table S5).
123
 Environ Geochem Health

The lower As concentrations in stems and leaves of Conclusions

rice from Orellana province than in rice from coastal
provinces (Table 3) are consistent with differences in The study findings lead to the following conclusions:
soil composition and properties. The Orellana pro-
1. The concentrations of As forms in rice grain
vince is located in the Amazonian region of the
varied spatially at local and intercontinental
country, where ferralitic soils are dominant. However,
scales.
soils developed over volcanic ashes are also present
2. At the local level (Ecuador), the tAs contents in
(Andosols; Spinosa et al. 2018), explaining the
rice plants and grains were much higher in coastal
presence of poorly crystalline colloids (see Fig. 2
provinces than in orient province (Orellana).
and Table 2, Fe/Al soluble in ammonium oxalate),
Detailed study of soil from paddy fields in
which can irreversibly adsorb As at acid pH (Livesey
Ecuador, comparing the coastal provinces and
and Huang 1981; Zhang and Selim 2005).
the equatorial zone, shows that the reactivity of
The order of abundance of the different As species
soil colloids with a low degree of crystallinity
in leaves and in stems was As(V) [ As(III) [ DMA,
plays an important role in the bioavailability of As
which differs from observations in other studies,
for rice plants.
according to which the predominant species in stem
3. Comparison at intercontinental scale revealed
and leaves were As(III) and DMA (Geng et al. 2017).
significantly higher tAs contents in commercial
This difference further indicates that local crop
rice from the Iberian Peninsula countries than in
conditions, as well as rice variety, can strongly affect
commercial rice from the Latin American coun-
the As forms present in the plant and, therefore, their
tries. However, speciation of the As forms indi-
potential toxicity. A previous study in the Iberian
cated that the difference is due to a higher content
Peninsula showed that a higher proportion of As in the
of oAs(especially DMA), as the iAs content was
soil was transferred to rice shoots in Catalonia and
similar in rice from the different Latin American
Portugal than in various other Spanish provinces
countries. The concentrations of iAs in rice from
(Signes-Pastor et al. 2016). In the aforementioned
the Latin American and the Iberian Peninsula
regions, soil As is expected to be present in more
countries are within the acceptable range for
insoluble and less labile forms, probably more influ-
human consumption.
enced by DOC dynamics, as suggested in previous
4. Meta-analysis of the present and previously pub-
studies (Khan et al. 2010; Williams et al. 2011).
lished data showed that the iAs/tAs ratio decreases
Finally, inorganic As species are redox sensitive,
as the tAs content of rice increases. This finding is
with arsenite predominating under reduced conditions
consistent with the results obtained for As speci-
(Eh \ 300 mV) and arsenate under oxidized condi-
ation, which indicated that for tAs higher
tions (Masscheleyn et al. 1991; Zhao et al. 2010). Rice
than * 0.300 mg kg-1, DMA is the dominant
roots can assimilate arsenic species through two
form of As in rice grain. Considering that As
pathways: arsenite through the silicic acid pathway
methylation occurs in soil, the mechanisms
and arsenate through the phosphate transport pathway
involved in iAs methylation in paddy fields
(see Meharg and Zhao 2012). Arsenite behaves in a
deserve further investigation. Future studies
similar way to silicic acid and is absorbed by rice roots
should focus on understanding the environmental
through silicon-specific transporters (Lsi1 and Lsi2;
parameters or conditions that favour As methyla-
Ma et al. 2008) and is specifically stored in rice stems,
tion in paddy soils. This could help in the design of
leaves and husk (as occurs with silicon) (Lombi et al.
management strategies aimed at reducing the toxic
2009; Norton et al. 2010). The Eh–pH conditions
forms of As in rice grain, for application in
indicate that arsenate is the main stable form of
countries with high rice consumption.
inorganic As in soils and water in rice fields (Fig. 7),
5. The results also show that iAs forms (the most
which explains the significantly lower concentrations
toxic forms of As) are mainly concentrated in
of As (mainly As III) in phytoliths and suggests that As
stems, husk and bran layers, and therefore,
in rice plants (stem, leave and husk) is mainly
polishing rice will contribute greatly to reducing
associated with organic forms (soluble in H2O2).
the As content of rice grain.

123
Environ Geochem Health
Acknowledgements This study is part of a research project
funded by the Universidad de las Fuerzas Armadas-ESPE
through Project 2015-PIC-017, Xunta de Galicia-Consellerı́a de
Educación, Universidades e Formación Profesional, Plan
Galego IDT, Consolidation of competitive research groups
(ref. ED31C2018/12), São Paulo Research Foundation—
FAPESP (grant number 2018/04259-2), Cross-Research in
Environmental Technologies (CRETUS, AGRUP2015/02, ref.
2018-PG100) and project PIJ15-10 financed by Escuela
Politécnica Nacional from Quito-Ecuador. TOF thanks the
National Council for Scientific and Technology Development
(CNPq, process 305996/2018-5). XLOP is grateful for the
financial support from the Proyecto PROMETEO (SENESCYT
Ecuador). We thank Marı́a José Santiso for assistance with
laboratory work and Augusto Pérez Alberti and Esther Sierra
Abraı́n for assistance with preparing the figures.
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