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Lotus roots accumulate heavy metals independently from soil in main production regions of China

Authors:
  • Huazhong Agricultural University; Hubei Hongshan Laboratory

Abstract and Figures

The global issue of heavy metal pollution causes concern on lotus root, a popular aquatic vegetable grown in sludge supposedly heavily contaminated. The relevance of heavy metals in soil and lotus roots in production remains unclear. In this work, four heavy metals, lead (Pb), cadmium (Cd), mercury (Hg) and arsenic (As), in lotus roots and ambient soil from main production areas of China were determined. The bioconcentration factor (BCF) of each heavy metal and correlation coefficient among heavy metals in soil and lotus roots were analyzed. Red soil (pH 6–7) in one location exceeded the maximum allowable limit of Cd by 91%, while soils in seven locations met the environmental requirements for producing safe lotus roots, including three red soils (pH 4–5), two moisture soils (pH 4–7), one cinnamon soil (pH 6–7), and one paddy soil (pH 6–7). Lotus roots were individually contaminated with Pb in two locations (red soil and paddy soil), As in two locations (red soil and cinnamon soil), and Hg in one location (red soil), exceeding the maximum allowable limit by 3–16%. Heavy metal levels of lotus roots produced in all investigated areas still met the safety standard as indicated by integrative pollution indexes (IPI). However, the close-to-limit IPI will certainly raise the safety concern for lotus root production. BCF of heavy metals decreased in an order of Cd (5.03–46.67%), Hg (2.42–7.20%), As (1.93–6.68%) and Pb (0.02–1.82%), showing lotus root's ability to accumulate metals varied with metal types. BCF and correlation coefficient showed that the lotus roots tended to accumulate heavy metals less efficiently from soil with higher levels of heavy metals, and vice versa. Heavy metal levels were positively correlated in soil but largely irrelevant in lotus roots. Thus, heavy metals in lotus roots were accumulated primarily independently from or partially negatively correlated with soil, complicating the enrichment mechanism of heavy metals in lotus roots. The possible causes of soil independent accumulation of heavy metals in lotus roots are discussed.
Content may be subject to copyright.
Scientia
Horticulturae
164
(2013)
295–302
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at
ScienceDirect
Scientia
Horticulturae
journal
h
om
epage:
www.elsevier.com/locate/scihorti
Lotus
roots
accumulate
heavy
metals
independently
from
soil
in
main
production
regions
of
China
Chunhui
Xiong1,
Yuyang
Zhang1,
Xiaoguang
Xu,
Yongen
Lu,
Bo
Ouyang,
Zhibiao
Ye,
Hanxia
Li
Key
Laboratory
of
Horticultural
Plant
Biology,
Ministry
of
Education,
Huazhong
Agricultural
University,
Wuhan
430070,
China
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
11
January
2013
Received
in
revised
form
10
August
2013
Accepted
12
September
2013
Keywords:
Heavy
metal
Bioconcentration
factor
Correlation
coefficient
Lotus
root
a
b
s
t
r
a
c
t
The
global
issue
of
heavy
metal
pollution
causes
concern
on
lotus
root,
a
popular
aquatic
vegetable
grown
in
sludge
supposedly
heavily
contaminated.
The
relevance
of
heavy
metals
in
soil
and
lotus
roots
in
production
remains
unclear.
In
this
work,
four
heavy
metals,
lead
(Pb),
cadmium
(Cd),
mercury
(Hg)
and
arsenic
(As),
in
lotus
roots
and
ambient
soil
from
main
production
areas
of
China
were
determined.
The
bioconcentration
factor
(BCF)
of
each
heavy
metal
and
correlation
coefficient
among
heavy
metals
in
soil
and
lotus
roots
were
analyzed.
Red
soil
(pH
6–7)
in
one
location
exceeded
the
maximum
allowable
limit
of
Cd
by
91%,
while
soils
in
seven
locations
met
the
environmental
requirements
for
producing
safe
lotus
roots,
including
three
red
soils
(pH
4–5),
two
moisture
soils
(pH
4–7),
one
cinnamon
soil
(pH
6–7),
and
one
paddy
soil
(pH
6–7).
Lotus
roots
were
individually
contaminated
with
Pb
in
two
locations
(red
soil
and
paddy
soil),
As
in
two
locations
(red
soil
and
cinnamon
soil),
and
Hg
in
one
location
(red
soil),
exceeding
the
maximum
allowable
limit
by
3–16%.
Heavy
metal
levels
of
lotus
roots
produced
in
all
investigated
areas
still
met
the
safety
standard
as
indicated
by
integrative
pollution
indexes
(IPI).
However,
the
close-to-
limit
IPI
will
certainly
raise
the
safety
concern
for
lotus
root
production.
BCF
of
heavy
metals
decreased
in
an
order
of
Cd
(5.03–46.67%),
Hg
(2.42–7.20%),
As
(1.93–6.68%)
and
Pb
(0.02–1.82%),
showing
lotus
root’s
ability
to
accumulate
metals
varied
with
metal
types.
BCF
and
correlation
coefficient
showed
that
the
lotus
roots
tended
to
accumulate
heavy
metals
less
efficiently
from
soil
with
higher
levels
of
heavy
metals,
and
vice
versa.
Heavy
metal
levels
were
positively
correlated
in
soil
but
largely
irrelevant
in
lotus
roots.
Thus,
heavy
metals
in
lotus
roots
were
accumulated
primarily
independently
from
or
partially
negatively
correlated
with
soil,
complicating
the
enrichment
mechanism
of
heavy
metals
in
lotus
roots.
The
possible
causes
of
soil
independent
accumulation
of
heavy
metals
in
lotus
roots
are
discussed.
©
2013
Elsevier
B.V.
All
rights
reserved.
1.
Introduction
Lotus
(Nelumbo
nucifera
Gaertn)
originated
in
China
and
has
been
cultivated
as
an
important
aquatic
vegetable
as
well
as
an
ornamental
plant
for
more
than
3000
years.
Almost
each
part
of
lotus
including
stems,
leaves,
and
seeds
can
be
used
as
vegetables
or
for
food
production.
The
main
edible
part
of
the
plant
is
lotus
root,
which
ranks
the
most
popular
aquatic
vegetable
in
China.
The
lotus
roots
have
a
recent
cultivation
area
of
more
than
133,000
ha
in
China
with
the
annual
20,000-ton
export.
For
a
long
time,
the
lotus
roots
have
been
considered
as
natural
“green
food”
in
both
domestic
and
international
markets.
However,
the
global
industrialization
and
urbanization
brought
about
the
environmental
pressure
for
agricultural
production.
Corresponding
author.
Tel.:
+86
27
87286867;
fax:
+86
27
87280016.
E-mail
address:
hxli@mail.hzau.edu.cn
(H.
Li).
1These
authors
contributed
equally
to
this
work.
Among
the
various
pollutants,
heavy
metals
are
the
mostly
con-
cerned
issue
for
aquatic
vegetable
production,
which
raises
the
question
of
whether
our
lotus
roots
are
still
green
food
in
the
con-
text
of
environment
deterioration.
The
various
pollutants,
especially
heavy
metals,
are
released
into
the
agricultural
environments
and
accumulated
into
the
plant
products
(Singh
et
al.,
2010).
The
heavy
metals
in
the
plants
finally
enter
human
body
through
the
food
chain,
causing
serious
threat
to
human
health
(Zhuang
et
al.,
2009).
Several
heavy
metals
such
as
iron
(Fe),
manganese
(Mn),
zinc
(Zn)
and
copper
(Cu),
are
essen-
tial
elements
for
human
health
as
enzymatic
cofactors.
However,
many
heavy
metal
elements
like
lead
(Pb),
cadmium
(Cd),
mercury
(Hg)
and
arsenic
(As)
are
toxic
to
environment
and
human
even
at
trace
concentrations
(Llobett
et
al.,
2003).
Due
to
the
crypticity,
indecomposability
and
duration
of
heavy
metals,
the
accumulation
of
heavy
metals
in
human
organs
(such
as
liver,
kidney,
bone,
etc.)
will
cause
severe
health
disorders.
For
example,
Pb
can
cause
renal
masses,
affect
cognitive
development
and
may
lead
to
adult
cardio-
vascular
disease.
Cd
may
induce
rickets,
and
is
closely
associated
0304-4238/$
see
front
matter
©
2013
Elsevier
B.V.
All
rights
reserved.
http://dx.doi.org/10.1016/j.scienta.2013.09.013
296
C.
Xiong
et
al.
/
Scientia
Horticulturae
164
(2013)
295–302
with
chronic
renal
failure
(Bandara
et
al.,
2008).
For
fetuses,
infants
and
children,
the
primary
health
effect
of
Hg
is
impaired
neurologi-
cal
development.
Hg
may
also
lead
to
impairment
of
the
peripheral
vision,
disturbances
in
sensations,
muscle
weakness,
and
lack
of
movement
coordination.
Ingestion
of
As
leads
to
gastrointestinal
symptoms,
and
disturbances
of
cardiovascular
and
nervous
system
functions.
Long-term
exposure
to
As
is
causally
related
to
increased
risk
of
cancer.
It
was
regarded
that
heavy
metal
transfer
from
soil
to
plants
was
a
key
pathway
for
human
exposure
to
metal
contamination
(Liu
et
al.,
2005).
The
heavy
metal
contamination
of
vegetables
is
frequently
reported
to
be
associated
with
heavy
metal
residues
in
soil,
which
poses
huge
health
risk
to
human
through
consump-
tion
of
vegetables
grown
in
polluted
soil
(Singh
et
al.,
2010).
In
field
with
heavy
metal
pollution,
high
Cd
and
Pb
contents
in
root
vegetables,
e.g.
carrots,
radish,
and
potatoes,
exceeded
up
to
2.5
times
and
11
times,
respectively,
of
the
maximum
allowable
lim-
its.
Systematic
contents
of
heavy
metals
in
leafy
vegetables,
e.g.
lettuce,
parsley,
dill,
and
orach,
reached
up
to
7
times
(Cd),
or
17
times
(Pb)
higher
than
normal
concentration.
Direct
propor-
tionality
was
found
between
heavy
metal
contents
in
soils
and
vegetables
(Lacatusu
and
Lacatusu,
2008).
Heavy
metal
concen-
trations
in
plants
grown
in
wastewater-irrigated
soil,
which
was
contaminated
with
heavy
metals,
were
significantly
higher
than
those
in
plants
grown
in
the
reference
soil
(Khan
et
al.,
2008).
The
heavy
metal
concentrations
in
vegetables
grown
in
contaminated
garden
soils
also
exceeded
the
maximum
permissible
limit
(Sharma
et
al.,
2009).
Given
the
close
correlation
of
heavy
metal
concentration
in
veg-
etable
and
ambient
soil,
it
is
highly
supposed
that
heavy
metal
concentration
in
lotus
roots
is
affected
accordingly
by
soil
heavy
metal
concentration.
Lotus
roots,
grown
in
sludge
and
silt
which
are
supposed
to
be
heavily
polluted
(Saruhan
et
al.,
2012),
call
for
an
overall
investigation
on
the
heavy
metals
in
lotus
roots
as
well
as
in
the
ambient
soil.
The
levels
of
heavy
metals,
As,
Cd,
Hg
and
Pb,
in
lotus
seeds
and
soil
were
investigated
at
rare
earth
min-
ing
area,
which
was
shown
to
meet
the
state
food
safety
standard
(Cai,
2012).
However,
the
heavy
metal
status
in
the
main
lotus-
producing
regions
remains
unclear.
In
this
work,
lotus
roots
as
well
as
ambient
soil
from
eight
main
producing
areas
in
China
were
collected
and
four
heavy
metals
including
Pb,
Cd,
Hg
and
As
were
determined
to
evaluate
the
pollu-
tion
degree
by
Single
Pollution
Index
(SPI)
and
Nemerow
Integrated
Pollution
Index
(IPI).
The
aim
of
this
work
is
to
investigate
the
heavy
metal
status
in
lotus
root
production
in
China,
and
to
check
whether
heavy
metal
accumulation
in
lotus
roots
is
closely
related
to
soil
heavy
metals.
2.
Materials
and
methods
2.1.
Producing
regions
and
plant
material
Main
production
areas
for
lotus
roots
are
located
in
the
central
China
(Hubei
and
Henan
provinces),
the
eastern
China
(Zhejiang
and
Shandong
provinces),
and
south
China
(Guangxi
province).
Eight
sampling
locations
were
chosen
from
lotus
root
main
pro-
ducing
areas,
namely
Wuhan
(HB-WH),
Hanchuan
(HB-HC)
and
Honghu
(HB-HH)
of
Hubei
province,
Xinzheng
of
Henan
province
(HN-XZ),
Yuhang
(ZJ-YH)
and
Jinhua
(ZJ-JH)
of
Zhejiang
province,
Jinan
of
Shandong
province
(SD-JN),
and
Liuzhou
of
Guangxi
province
(GX-LZ)
(Fig.
1).
The
eight
sampling
locations
lie
between
longitude
E10924–E12018and
latitude
N1931–N4324.
The
climate
ranges
from
warm
temperate
monsoon
climate
to
subtrop-
ical
monsoon
climate.
The
soil
type
and
climate
conditions
of
the
production
areas
are
listed
in
Table
1.
All
the
lotus
plants
grown
in
the
eight
sampling
locations
are
cultivar
Elian
No.
4
provided
by
Wuhan
Institute
of
Vegetable
Science.
2.2.
Sample
collection
and
heavy
metal
determination
The
lotus
roots
and
soil
from
the
eight
main
production
areas
in
Hubei,
Henan,
Guangxi,
Shandong
and
Zhejiang
were
collected
from
October
to
November
2009.
Both
soil
and
lotus
roots
sam-
ples
were
taken
from
four
corners
of
cultivation
field
as
well
as
the
diagonal
cross
point
(field
center),
giving
five
replicates
for
each
sample.
The
ambient
soil
of
lotus
root
was
taken
as
mixture
of
20
cm
depth
from
surface.
The
soil
was
dried
at
room
temperature,
ground
and
sifted
through
100
mesh
nylon
sieve,
and
stored
in
clean
aluminum
boxes.
Lotus
roots
were
cleaned
with
deionized
water,
dried
at
60–100 C
and
ground,
and
stored
in
clean
aluminum
boxes
before
determination
of
Pb,
Cd,
Hg
and
As.
State
standard
methods
of
China
were
applied
to
determine
the
concentration
of
Pb
(GB/T
5009.12-2003),
Cd
(GB/T
5009.15-2003),
Hg
(GB/T
5009.17-2003)
and
As
(GB/T
5009.11-2003).
Briefly,
the
plant
tissue
were
ground
and
digested
by
nitric
acid
mixed
with
perchloric
acid
(v:v
=
4:1),
and
soil
sample
was
digested
with
aqua
regia
(nitric
acid:hydrochloric
acid
=
3:1).
After
the
sample
diges-
tion,
Pb
and
Cd
were
detected
by
atomic
absorption
spectrometry
(AA240FS,
Varian,
USA),
and
Hg
and
As
were
determined
by
hydride
generation-atomic
fluorescence
spectrometry
(HG-AFS
8220,
Bei-
jing
Jitian
instrument
Co.
Ltd.,
China).
The
heavy
metals
of
Pb,
Cd,
Hg
and
As
in
soil
and
lotus
roots
were
analyzed
with
reference
to
the
China
state
standard
“Pollution-free
food:
environment
requirements
for
aquatic
vegetable
production”
(No.:
NY
5331-2006)
and
“Pollution-free
food:
aquatic
vegetable
(lotus
root)”
(No.:
NY
5238-2005).
For
soil
pH
determination,
10
g
of
dried
soil
were
mixed
with
25
ml
distilled
water
and
the
supernatant
was
used
for
pH
assay.
2.3.
Data
analysis
Individual
heavy
metal
residue
and
integrated
heavy
metal
residues
of
the
soil
and
lotus
samples
from
each
cultivation
region
were
evaluated
by
single
pollution
index
and
Nemerow
integrated
pollution
index,
respectively.
Single
pollution
index
of
heavy
metal
is
calculated
using
the
formula
as
follows:
Pi=Ci
Si
,
where
Piis
the
pollution
index
of
individual
heavy
metal;
Cidenotes
the
measured
value
of
individual
heavy
metal;
Sistands
for
allow-
able
maximum
limit
for
each
heavy
metal.
If
the
single
pollution
index
of
a
heavy
metal
is
more
than
1.0,
the
sample
is
considered
polluted
with
the
individual
heavy
metal
element.
However,
single
pollution
index
merely
reflects
the
pol-
lution
status
of
certain
heavy
metal,
without
giving
the
overall
information
of
compound
pollution.
Integrated
pollution
index
will
take
into
account
the
general
levels
of
different
heavy
metals,
and
highlight
the
effect
of
major
pollutants
in
the
process
of
pollution
evaluation.
The
formula
for
integrated
pollution
index
is
as
follows:
Pj=(P2
m+
P2
max)
21/2
,
where
the
Pjdenotes
the
integrated
pollution
index;
Pmstands
for
mean
of
single
pollution
indexes;
Pmax is
the
maximum
value
among
the
single
pollution
indexes.
C.
Xiong
et
al.
/
Scientia
Horticulturae
164
(2013)
295–302
297
Table
1
The
levels
of
heavy
metals
in
ambient
soil
of
lotus
roots
from
the
main
production
regions
in
China.
Production
area
Longitude
and
latitude
Climate
Soil
type
(pH)aHeavy
metal
Mean
(mg/kg)bMinimum
(mg/kg)
Maximum
(mg/kg)
Single
pollution
index
Integrated
pollution
index
Pollution
degree
SD-JN
E1170N3639Warm
temperate
semi-humid
monsoon
Moisture
soil
(6.66–7.32)
Pb
37.21
±
12.16
bc
16.00
47.15
0.12
0.63
Clean
Cd
0.24
±
0.09
bc
0.08
0.28
0.78
Hg
0.16
±
0.09
b
0.13
0.35
0.32
As
11.15
±
2.32
bc
7.10
12.91
0.45
HN-XZ E11334N4324Warm
temperate
continental
monsoon
Cinnamon
soil
(6.92–7.40)
Pb
20.47
±
2.88
de
17.70
25.25
0.07
0.32
Clean
Cd
0.10
±
0.01
d
0.08
0.12
0.34
Hg
0.18
±
0.02
bc
0.15
0.19
0.35
As
8.29
±
0.65
d
8.00
9.46
0.33
HB-WH E11430N1931North
subtropical
monsoon
climate
Red
soil
(4.14–5.23) Pb
27.76
±
5.75
cd
9.70
53.20
0.11
0.37
Clean
Cd
0.12
±
0.05
d
0.06
0.20
0.41
Hg
0.13
±
0.02
c
0.10
0.16
0.44
As
6.77
±
1.70
d
4.27
9.07
0.23
HB-HH E11327N2948Subtropical
humid
monsoon
climate
Moisture
soil
(4.13–5.56)
Pb
18.55
±
0.60
de
17.70
19.40
0.07
0.65
Clean
Cd
0.25
±
0.01
b
0.23
0.27
0.82
Hg
0.12
±
0.01
c
0.10
0.14
0.39
As
8.77
±
0.29
cd
8.35
9.18
0.29
HB-HC E11330N3538Subtropical
monsoon
climate
Paddy
soil
(6.66–7.32)
Pb
12.50
±
2.63
e
8.13
15.17
0.04
0.42
Clean
Cd
0.15
±
0.07
cd
0.07
0.26
0.51
Hg
0.14
±
0.05
bc
0.07
0.22
0.27
As
11.26
±
1.54
bc
8.79
13.07
0.45
GX-LZ cE10924N2420Subtropical
monsoon
climate
Red
soil
(6.92–7.40) Pb
75.40
±
22.23
a
38.45
98.85
0.25
1.49
Polluted
Cd
0.57
±
0.16
a
0.28
0.64
1.91
Hg
0.33
±
0.02
a
0.31
0.37
0.66
As
17.99
±
3.81
a
12.59
23.36
0.72
ZJ-JH E11938N297Subtropical
monsoon
climate
Red
soil
(4.14–5.23) Pb
44.80
±
3.39
b
40.00
49.60
0.18
0.78
Clean
Cd
0.14
±
0.01
cd
0.13
0.15
0.48
Hg
0.29
±
0.00
a
0.29
0.30
0.98
As
12.60
±
0.70
b
11.61
13.59
0.42
ZJ-YH E12018N3026Northern
subtropical
monsoon
climate
Red
soil
(4.13–5.56) Pb
40.34
±
4.16
bc
33.90
45.55
0.16
0.76
clean
Cd
0.13
±
0.02
d
0.12
0.16
0.45
Hg
0.29
±
0.03
a
0.28
0.35
0.97
As
9.12
±
0.45
cd
8.84
9.89
0.30
aAccording
to
China
state
standard
“Pollution-free
food:
environment
requirements
for
aquatic
vegetable
production”
(No.:
NY
5331-2006),
the
allowable
maximum
limit
of
soil
heavy
metals
for
vegetable
production
varies
with
soil
pH
value.
Based
on
different
soil
pH
range
of
production
areas,
allowable
maximum
limits
of
heavy
metals
in
soil
for
Jinan
Shandong
(SD-JN),
Xinzheng
Henan
(HN-XZ),
Hanchuan
Hubei
(HB-HC),
and
Liuzhou
Guangxi
(GX-LZ)
are:
Pb
300
mg/kg,
Cd
0.30
mg/kg,
Hg
0.50
mg/kg,
and
As
25
mg/kg;
allowable
maximum
limits
of
soil
heavy
metals
for
Wuhan
Hubei
(HB-WH),
Honghu
Hubei
(HB-HH),
Jinhua
Zhejiang
(ZJ-JH),
and
Yuhang
Zhejiang
(ZJ-YH)
are:
Pb
250
mg/kg,
Cd
0.30
mg/kg,
Hg
0.30
mg/kg,
and
As
30
mg/kg.
bThe
data
are
presented
as
mean
with
standard
deviation
from
five
replicates.
The
different
letters
behind
the
same
heavy
metals
indicate
significant
difference
by
Duncan’s
multiple
range
test
(P
<
0.05).
cThe
maximum
Cd
level
in
the
production
area
of
GX-LZ
exceeded
the
limit
by
113%.
The
levels
of
other
heavy
metals
in
GX-LZ
and
any
other
production
areas
are
within
the
limits.
The
values
over
the
corresponding
maximum
limits
are
marked
in
bold.
298
C.
Xiong
et
al.
/
Scientia
Horticulturae
164
(2013)
295–302
Fig.
1.
The
eight
sampling
sites
(denoted
by
)
in
the
main
production
regions
of
lotus
root
in
China.
Lotus
roots
and
the
ambient
soil
were
collected
from
one
site
in
South
China,
namely
Liuzhou
Guangxi
(GX-LZ),
three
sites
in
Eastern
China,
namely
Yuhang
Zhejiang
(ZJ-YH),
Jinhua
Zhejiang
(ZJ-JH)
and
Jinan
Shandong
(SD-JN),
and
four
sites
in
Central
China,
namely
Wuhan
Hubei
(HB-WH),
Hanchuan
Hubei
(HB-HC),
Honghu
Hubei
(HB-HH)
and
Xinzheng
Henan
(HN-XZ).
The
bioconcentration
factor
(BCF)
estimates
the
efficiency
of
a
plant
in
taking
up
heavy
metals
from
soil
and
is
calculated
as
follows
(Xue
et
al.,
2013;
Yoon
et
al.,
2006):
BCF
=CL
CS
where
CLand
CSstand
for
the
heavy
metal
concentration
in
lotus
root
and
in
its
ambient
soil,
respectively.
To
figure
out
whether
concentration
of
heavy
metals
in
lotus
roots
is
closely
related
to
heavy
metals
in
soil
among
eight
produc-
tion
regions,
we
carried
out
correlation
analysis.
All
the
40
samples
(5
samples
respectively
in
8
locations)
of
lotus
roots
as
well
as
soil
were
subject
to
correlation
analysis.
Correlation
analysis
between
heavy
metals
in
soil
and
lotus
roots
was
carried
out
using
Pearson
test.
The
correlation
analysis
and
the
bioconcentration
factor
(ratio
of
lotus
roots
to
soil)
give
different
biological
meaning.
The
SPSS
17.0
software
was
utilized
for
statistical
analysis
of
the
data.
3.
Results
3.1.
The
pollution
level
of
heavy
metals
in
ambient
soil
of
lotus
roots
Soil
heavy
metals
of
the
eight
lotus
root-producing
areas
were
determined
and
presented
with
reference
to
China
state
standard
“Pollution-free
food:
environment
requirements
for
aquatic
veg-
etable
production”
(No.:
NY
5331-2006)
(Table
1).
Among
the
eight
main
producing
areas
of
the
lotus
roots,
the
soil
Cd
in
collected
sam-
ples
of
lotus
root
field
in
Guangxi
(GX-LZ)
exceeded
the
allowable
maximum
limit
by
40.5–113%.
Heavy
metal
levels
in
soil
samples
of
other
lotus
root-producing
areas
met
the
requirements
of
state
standard.
The
soil
heavy
metals
in
the
eight
main
lotus-producing
areas
were
evaluated
by
SPI
and
IPI
(Table
1).
Among
all
the
heavy
metals
in
eight
main
lotus-producing
areas,
the
Cd
in
lotus
root
ambient
soil
of
Guangxi
area
(GX-LZ)
showed
the
highest
SPI
(1.91),
which
is
much
higher
than
the
maximum
limit
value
of
1.0,
indicating
soil
of
lotus
field
in
GX-LZ
is
heavily
polluted
with
Cd
residue.
In
two
lotus
root
producing
areas
in
Zhejiang
province
of
eastern
China,
Jinhua
(ZJ-JH)
and
Yuhang
(ZJ-YH),
the
SPI
of
Hg
climbed
close
to
1.0
(0.98
and
0.97,
respectively),
indicating
that
the
soil
of
lotus
pro-
ducing
areas
in
Zhejiang
is
potentially
threatened
by
Hg
pollution.
Comprehensive
pollution
evaluation
by
IPI
showed
that
among
the
eight
main
lotus-producing
areas,
only
the
soil
sample
of
Guangxi
area
(GX-LZ)
has
been
polluted
by
heavy
metals,
with
the
highest
IPI
of
1.49,
while
the
rest
of
the
regions
showed
the
IPI
much
less
than
1.0.
The
soil
of
lotus
field
in
Jinhua
(ZJ-JH)
and
Yuhang
(ZJ-YH)
of
Zhejiang
can
still
be
considered
unpolluted,
with
the
IPI
of
0.78
and
0.76,
respectively,
though
their
individual
heavy
metal
level
(Hg)
almost
reached
the
maximum
limit.
3.2.
The
pollution
level
of
heavy
metals
in
lotus
roots
The
heavy
metal
concentration
of
Pb,
Cd,
Hg
and
As
in
the
lotus
roots
collected
from
eight
main
producing
regions
in
China
were
determined,
and
the
data
are
presented
with
reference
to
state
standard
“Pollution-free
food:
aquatic
vegetables
(lotus
root)”
(No.:
NY
5238-2005)
(Table
2).
The
results
showed
that
lotus
roots
from
several
producing
regions
were
polluted
with
individual
heavy
metals.
The
maximum
Cd
levels
in
lotus
roots
from
SD-JN
(0.07)
and
HN-XZ
(0.06),
the
maximum
Pb
level
in
lotus
roots
from
HB-HH
(0.33),
and
the
max-
imum
Hg
levels
in
HB-HC
(0.02)
and
GX-LZ
(0.02),
exceeded
the
allowable
maximum
limits,
while
their
mean
values
still
met
the
standard
requirements.
The
mean
levels
of
individual
heavy
metals
in
lotus
roots
from
five
producing
regions
were
higher
than
the
allowable
maximum
limits,
including
As
in
HN-XZ
(0.55)
and
ZJ-
JH
(0.58),
Pb
in
HB-WH
(0.21)
and
HB-HC
(0.23),
and
Hg
in
ZJ-YH
(0.01),
with
the
SPI
between
1.03
and
1.16.
The
mean
levels
of
Cd
residues
in
lotus
roots
from
eight
regions
were
within
the
allow-
able
maximum
limit.
Either
the
maximum
level
or
the
mean
value
of
individual
heavy
metals
over
the
maximum
allowable
limit
was
C.
Xiong
et
al.
/
Scientia
Horticulturae
164
(2013)
295–302
299
Table
2
The
levels
of
heavy
metals
in
lotus
roots
in
main
production
areas
in
China.
Production
area
Heavy
metalsaMean
(mg/kg)bMinimum
(mg/kg)
Maximum
(mg/kg)
Single
pollution
index
Integrated
pollution
index
Pollution
degree
SD-JN
Pb
0.04
±
0.00
b
0.04
0.05
0.22
0.78
Clean
Cd
0.05
±
0.01
a
0.04
0.07
0.97
Hg
0.01
±
0.00
a
0.00
0.01
0.55
As
0.22
±
0.04
d
0.16
0.27
0.43
HN-XZ
Pb
0.05
±
0.01
b
0.04
0.06
0.24
0.96
Clean
Cd
0.05
±
0.01
a
0.03
0.06
0.95
Hg
0.01
±
0.00
a 0.01 0.01 0.88
As
0.55
±
0.11
ab
0.45
0.73
1.11
HB-WH
Pb
0.21
±
0.14
a
0.02
0.41
1.07
0.90
Clean
Cd
0.02
±
0.01
bc
0.00
0.03
0.35
Hg
0.01
±
0.00
a
0.00
0.01
0.60
As
0.35
±
0.09
cd
0.21
0.46
0.70
HB-HH
Pb
0.20
±
0.09
a
0.07
0.33
0.99
0.87
Clean
Cd
0.02
±
0.01
bc
0.01
0.03
0.43
Hg
0.01
±
0.00
a
0.01
0.01
0.85
As
0.32
±
0.04
cd 0.26 0.38 0.65
HB-HC
Pb
0.23
±
0.08
a
0.13
0.35
1.14
0.94
Clean
Cd
0.01
±
0.01
c
0.00
0.03
0.28
Hg
0.01
±
0.00
a
0.01
0.02
0.64
As
0.33
±
0.08
cd
0.19
0.39
0.65
GX-LZ
Pb
0.02
±
0.01
b 0.01 0.04 0.11
0.75
Clean
Cd
0.03
±
0.01
b
0.02
0.04
0.58
Hg
0.01
±
0.01
a
0.00
0.02
0.80
As
0.44
±
0.08
bc
0.31
0.50
0.88
ZJ-JH
Pb
0.03
±
0.01
b
0.03
0.05
0.16
0.97
Clean
Cd
0.03
±
0.01
b
0.01
0.05
0.68
Hg
0.01
±
0.00
a 0.01 0.01 0.95
As
0.58
±
0.17
a
0.34
0.82
1.16
ZJ-YH
Pb
0.01
±
0.00
b
0.00
0.01
0.04
0.80
Clean
Cd
0.01
±
0.00
c
0.01
0.01
0.22
Hg
0.01
±
0.00
a
0.01
0.02
1.03
As
0.28
±
0.04
d
0.22
0.34
0.56
aAccording
to
China
state
standard
“Pollution-free
food:
aquatic
vegetables
(lotus
root)”
(No.:
NY
5238-2005),
the
allowable
maximum
limits
of
different
heavy
metals
in
the
lotus
roots
are:
Pb
0.20
mg/kg,
Cd
0.05
mg/kg,
Hg
0.01
mg/kg,
and
As
0.50
mg/kg.
Thus
it
can
be
drawn
that
the
Pb
levels
in
lotus
roots
produced
in
Wuhan
Hubei
(HB-WH)
and
Hanchuan
Hubei
(HB-HC)
exceeded
the
limit
value
by
7%
and
14%,
respectively;
The
Hg
levels
in
lotus
roots
produced
in
Yuhang
Zhejiang
(ZJ-YH)
exceeded
the
limit
value
by
3%;
the
As
levels
in
lotus
roots
produced
in
Xinzheng
Henan
(HN-XZ)
and
Jinhua
Zhejiang
(ZJ-JH)
exceeded
the
limit
value
by
11%
and
16%,
respectively.
The
Cd
levels
in
lotus
roots
produced
in
main
production
regions
were
within
the
limits.
The
values
over
the
threshold
are
marked
in
bold.
bThe
data
are
presented
as
mean
with
standard
deviation
from
five
replicates.
The
different
letters
behind
the
same
heavy
metals
indicate
significant
difference
by
Duncan’s
multiple
range
test
(P
<
0.05).
observed
in
lotus
roots
in
all
eight
production
regions,
posing
chal-
lenges
of
heavy
metal
contamination
in
the
lotus
roots.
Fortunately,
the
integrated
pollution
index,
which
takes
into
consideration
the
general
effect
of
various
heavy
metals,
showed
more
optimistic
sta-
tus
of
heavy
metals
in
lotus
roots.
The
IPI
for
the
heavy
metals
in
lotus
roots
from
eight
main
producing
areas
were
all
below
the
threshold
of
1.0.
Interestingly,
the
lotus
roots
from
GX-LZ
showed
the
lowest
IPI
value
of
0.75,
though
its
root
ambient
soil
had
the
highest
IPI
of
1.49.
On
the
other
hand,
the
producing
region
of
HN-XZ
showed
the
lowest
IPI
of
0.32
in
soil,
and
the
fairly
high
IPI
close
to
allowable
maximum
limit
(0.96)
in
lotus
roots
(Tables
1
and
2).
3.3.
Different
enrichment
capacity
for
heavy
metals
in
lotus
roots
The
BCF
represents
the
ratio
of
the
heavy
metal
level
in
plants
to
that
in
soil,
which
can
be
used
to
evaluate
the
plant
capac-
ity
to
absorb
and
accumulate
heavy
metals
from
soil.
The
BCF
of
lotus
roots
for
four
different
heavy
metals
in
eight
main
producing
regions
are
presented
(Table
3).
Obvious
difference
in
BCF
for
heavy
metal
elements
was
observed
in
lotus
roots.
The
BCF
of
lotus
roots
for
Cd,
Hg,
As,
and
Pb
are
5.03–46.67%,
2.42–7.20%,
1.93–6.68%
and
0.02–1.82%,
respectively.
Thus,
it
could
be
drawn
that
lotus
root
exhibits
the
highest
enrichment
capacity
for
Cd,
and
the
lowest
enrichment
coefficient
for
Pb,
which
is
consistent
with
observation
in
other
vegetables
(Zhuang
et
al.,
2009).
Different
lotus
producing
regions
varied
in
lotus
root
BCF
for
heavy
metals.
HB-HH
and
HB-HC
showed
the
highest
enrichment
capacity
for
Hg
and
Pb,
with
the
BCF
of
7.20%
and
1.82%,
respec-
tively.
SD-JN
and
ZJ-YH
exhibited
the
lowest
enrichment
capacity
for
As
and
Pb,
with
BCF
of
1.93%
and
0.02%,
respectively.
HN-XZ
had
the
highest
BCF
for
Cd
(20.55%)
and
As
(6.68%),
while
GX-LZ
showed
the
lowest
BCF
for
Cd
(5.03%)
and
Hg
(2.42%)
(Table
3).
Table
3
The
bioconcentration
factors
of
heavy
metals
in
lotus
roots
in
main
production
regions
of
China.
Production
area
Bioconcentration
factor
(%)
Pb
Cd
Hg
As
SD-JN
0.12
20.55
3.44
1.93b
HN-XZ
0.24
46.67a4.97
6.68a
HB-WH
0.77
14.03
4.58
5.20
HB-HH
1.07
8.70
7.20a3.68
HB-HC
1.82a9.26
4.67
2.89
GX-LZ
0.03
5.03b2.42b2.46
ZJ-JH
0.07
23.78
3.23
4.59
ZJ-YH
0.02b8.21
3.55
3.05
a,b Represents
the
highest
or
lowest
bioconcentration
factor
among
eight
regions
for
individual
heavy
metal,
respectively.
300
C.
Xiong
et
al.
/
Scientia
Horticulturae
164
(2013)
295–302
The
BCF
analysis
showed
that
the
lotus
roots
tend
to
reduce
the
heavy
metal
accumulation
in
response
to
high
levels
of
heavy
metal
in
soil,
and
increase
the
enrichment
efficiency
under
low
level
of
heavy
metals
in
soil,
suggesting
the
complexity
of
heavy
metal
absorption
and
accumulation
in
lotus
roots.
Soil
in
Guangxi
produc-
ing
area
(GX-LZ),
for
example,
was
contaminated
with
Cd
residue
with
the
highest
concentration
of
0.64
mg/kg
(allowable
maximum
limit
0.3
mg/kg),
exceeding
allowable
maximum
limit
by
113%.
However,
Cd
levels
in
the
lotus
roots
in
GX-LZ
did
not
exceed
the
maximum
limit,
with
the
lowest
bioconcentration
factor.
Similarly,
the
lotus
producing
soil
in
GX-LZ
shows
the
highest
Hg
level
and
the
lowest
bioconcentration
factor
for
Hg.
The
soil
of
lotus
field
in
SD-JN
and
ZJ-YH
exhibits
the
fairly
high
levels
in
As
(the
third
highest)
and
Pb
(the
second
highest),
respectively.
However,
lotus
roots
in
SD-JN
and
ZJ-YH
show
the
lowest
enrichment
capacity
for
As
and
Pb,
respectively.
On
the
contrary,
the
soil
in
HB-HH
and
HB-
HC
contains
the
lowest
levels
for
Hg
and
Pb,
respectively,
but
the
lotus
roots
exhibited
the
highest
enrichment
efficiency
for
Hg
and
Pb.
HN-XZ
exhibits
the
lowest
level
for
Cd
in
soil,
but
shows
the
highest
enrichment
capacity
for
Cd
in
lotus
roots.
This
is
also
true
with
soil
As
level
in
HN-XZ,
in
which
the
very
low
concentration
of
As
level
in
soil
(seventh
highest
among
eight
regions)
is
associated
with
the
highest
bioconcentration
factor
(Tables
1
and
3).
3.4.
The
correlation
among
heavy
metals
in
soil
and
lotus
roots
The
correlation
between
heavy
metal
accumulation
in
soil
and
lotus
roots
among
eight
main
producing
areas
was
investigated
using
the
SPSS
software.
Because
the
pH
value
of
ambient
soil
may
affect
the
metal
availability,
pH
was
also
investigated
in
the
corre-
lation
analysis
(Table
4).
The
correlation
analysis
results
showed
that
heavy
metal
ele-
ments
in
soil
are
positively
correlated
with
each
other,
with
the
highest
correlation
coefficient
between
Cd
and
As
(0.80)
and
the
lowest
correlation
coefficient
between
Cd
and
Hg
(0.48).
The
cor-
relation
analysis
between
heavy
metals
in
lotus
roots
and
in
soil
showed
that
the
levels
of
Cd,
Hg
and
As
in
lotus
roots
were
not
correlated
with
any
of
the
heavy
metals
detected
in
the
soil.
The
Pb
level
in
lotus
roots
was
independent
from
soil
Cd
and
As.
It
is
interesting
that
the
Pb
level
in
lotus
roots
was
negatively
corre-
lated
with
Pb
and
Hg
levels
in
soil,
with
the
correlation
coefficient
of
0.47
and
0.56,
respectively.
The
heavy
metals
in
the
lotus
roots
were
not
significantly
corre-
lated
with
each
other,
except
for
a
positive
correlation
between
As
and
Hg
in
lotus
roots
with
the
correlation
coefficient
0.43
(Table
4).
Although
it
was
reported
that
the
Cd
in
roots
tended
to
be
nega-
tively
correlated
with
other
elements
(Quadir
et
al.,
2011),
in
this
study,
the
negative
correlation
was
not
significant
with
correlation
coefficient
from
0.20
to
0.06.
The
soil
pH
value
did
not
influ-
ence
the
heavy
metals
in
roots
lotus
or
soil,
except
for
a
positive
correlation
between
soil
pH
and
soil
As
level.
4.
Discussion
The
investigation
of
the
heavy
metals
in
main
root
lotus-
producing
areas
in
China
indicates
although
the
field
soil
of
main
lotus
root-producing
areas
in
China
primarily
meet
the
state
standard
for
safe
production
of
aquatic
vegetables,
either
the
mean
level
or
maximum
level
of
individual
heavy
metal
in
lotus
roots
is
found
higher
than
allowable
maximum
limit
in
each
of
the
lotus
root-producing
area.
However,
the
general
evaluation
of
heavy
metals
in
lotus
roots
is
supposed
to
meet
the
safety
standard
as
indicated
by
IPI.
This
can
only
mean
the
lotus
roots
are
tempo-
rarily
safe
but
will
certainly
arouse
serious
concerns
as
lotus
roots
from
nearly
half
of
the
producing
areas
showed
the
IPI
over
0.9
(Tables
1
and
2).
It
is
interesting
that
the
HN-XZ
had
the
highest
BCF
for
Cd
(46.67%)
and
As
(6.68%),
while
GX-LZ
showed
the
lowest
BCF
for
Cd
(5.03%)
and
Hg
(2.42%)
(Table
3).
This
is
reminiscent
of
the
fact
that
lowest
heavy
metal
accumulation
in
soil
was
accompanied
by
the
very
high
heavy
metal
levels
in
lotus
roots
in
HN-XZ,
while
the
low-
est
heavy
metal
levels
in
lotus
roots
and
highest
heavy
metal
levels
in
soil
were
simultaneously
observed
in
GX-LZ
(Tables
1
and
2).
This
again
arouses
the
complexity
of
heavy
metal
accumulation
from
soil
to
plants,
which
may
be
jointly
controlled
by
the
interaction
among
plant,
soil
and
metals.
However,
the
heavy
metal
residues
in
the
water
or
air
may
also
be
involved
in
the
heavy
metal
enrich-
ment
in
plants.
Further
correlation
analysis
between
heavy
metals
in
lotus
roots
and
in
soil
indicate
that
the
heavy
metals
in
soil
and
lotus
roots
are
primarily
unrelated
(Table
4).
The
rare
negative
cor-
relation
between
heavy
metals
in
soil
and
lotus
roots
was
observed.
The
Pb
level
in
lotus
roots
was
negatively
correlated
with
Pb
and
Hg
levels
in
soil,
with
the
correlation
coefficient
of
0.47
and
0.56,
respectively
(Table
4).
That
means
within
a
certain
concentration
range,
the
Pb
level
in
lotus
roots
tends
to
decline
with
the
increas-
ing
level
of
Pb
and
Hg
in
soil.
This
negative
correlation
between
heavy
metals
in
plants
and
soil
is
likely,
at
least
in
part,
attributed
to
a
potential
plant
defense
capacity
against
heavy
metal
stress.
Thus,
heavy
metal
residues
in
the
lotus
roots
are
accumulated
inde-
pendently
from
or
correlated
negatively
with
heavy
metal
levels
in
ambient
soil.
The
soil
independent
accumulation
of
heavy
metal
in
plants
is
supported
by
further
evidence.
Application
of
heavy
metal-
contaminated
sewage
sludge
as
fertilizer
did
not
increase
the
heavy
metals
in
plants
but
raised
the
mineral
matter
content
of
plants
as
well
as
the
plant
yield
(Saruhan
et
al.,
2010).
Despite
the
high
rates
of
heavy
metal-bearing
biosolids
applied
to
the
soil,
plant
uptake
of
Cd,
Cu,
Ni,
and
Zn
were
well
within
critical
concentrations
(Evanylo
et
al.,
2005).
However,
although
heavy
metal
load
of
the
soil
were
below
the
maximum
allowable
limit,
the
spinach
and
okra
showed
Pb
and
Cd
levels
higher
than
the
corresponding
limits
(Singh
and
Kumar,
2006).
Similarly,
there
was
no
obvious
heavy
metal
con-
tamination
in
the
soil,
but
relatively
high
concentrations
of
As,
Hg,
Pb,
and
Cd
in
wheat
and
corn
was
observed,
which
was
supposedly
attributed
to
the
interactive
effects
of
irrigation
and
fertilizer
used
(Jia
et
al.,
2010).
There
are
several
potential
causes
for
the
soil-independent
accu-
mulation
of
heavy
metals
in
lotus
roots.
Firstly,
the
plant
species
have
potential
capacity
to
defense
against
heavy
metal
stress.
Upon
high
levels
of
heavy
metals
in
the
growth
environment,
the
plant
may
activate
defense
machinery
to
reject
or
excrete
heavy
metal
elements
to
avoid
cell
toxicity
caused
by
extreme
levels
of
heavy
metals.
Secondly,
the
heavy
metal
pollution
generally
hap-
pens
in
form
of
compound
pollutants
(Damian
et
al.,
2010).
The
heavy
metals
in
the
soil
are
shown
to
be
jointly
correlated
with
each
other
(Table
4),
by
which
one
type
of
heavy
metal
in
soil
may
regulate
the
absorption
and
accumulation
of
another
type
of
heavy
metal
in
plants.
Thirdly,
once
absorbed,
the
heavy
metals
may
be
transferred
to
different
organs
or
tissues
from
lotus
roots.
In
HB-WH
and
GX-LZ,
the
Pb
and
Hg
levels
in
lotus
leaves
were
much
higher
than
those
in
lotus
roots,
stolons,
and
stems
(data
not
shown).
The
absorbed
heavy
metals
may
be
translocated
from
lotus
roots
and
accumulated
into
leaves
together
with
the
pro-
cess
of
transpiration.
This
hypothesis
is
supported
by
the
fact
that
translocation
of
As
from
roots
to
shoots
was
observed
in
plants
(Pajuelo
et
al.,
2007).
It
is
interesting
that
plants
manage
to
reduce
Hg2+ ions
to
Hg
and
promote
volatilizing
the
heavy
metal
which
is
facilitated
by
transpiration
(Battke
et
al.,
2005).
Finally,
the
lotus
is
subjected
to
a
variety
of
sources
of
heavy
metal
pollu-
tion
from
soil,
water
and
air.
The
lotus
has
been
demonstrated
to
accumulate
heavy
metals
from
water
and
the
enrichment
capacity
of
lotus
roots
was
higher
than
that
of
leaves
and
stems
(Mishra
et
al.,
C.
Xiong
et
al.
/
Scientia
Horticulturae
164
(2013)
295–302
301
Table
4
The
correlation
coefficient
among
heavy
metals
in
soil
and
lotus
roots
as
well
as
soil
pH
value.
R
pH
PbSCdSHgSAsSPbLCdLHgLAsL
pH
1.00
PbS0.14
1.00
CdS0.31
0.78** 1.00
HgS0.20
0.72** 0.48** 1.00
AsS0.42*0.65** 0.80** 0.56** 1.00
PbL0.34
0.47** 0.24
0.56** 0.28
1.00
CdL0.25
0.06
0.08
0.05
0.05
0.20
1.00
HgL0.03 0.17 0.10 0.07 0.02
0.06
0.18
1.00
AsL0.14
0.15
0.10
0.11
0.07
0.15
0.20
0.43** 1.00
R
means
the
correlation
coefficient.
PbS,
CdS,
HgS,
AsSand
PbL,
CdL,
HgL,
AsLrepresents
the
levels
of
Pb,
Cd,
Hg,
and
As
in
soil
(S)
and
lotus
roots
(L),
respectively.
*Indicate
significant
correlation
at
0.05
level,
which
are
also
marked
in
bold.
** Indicate
significant
correlation
at
0.01
level,
which
are
also
marked
in
bold.
2009).
Wastewater
irritation
also
led
to
significantly
higher
heavy
metal
levels
in
plants
(Khan
et
al.,
2008).
At
the
same
time,
evidence
has
shown
that
atmospheric
depositions
can
elevate
the
levels
of
heavy
metals
in
vegetables
(Shallari
et
al.,
1998;
Sharma
et
al.,
2008;
Pandey
and
Pandey,
2009).
Several
plant
species
from
industrial
sites
with
rather
high
concentrations
of
Pb
or
Cu
in
their
above-
ground
parts,
were
probably
related
to
contamination
by
soil
dust
(Shallari
et
al.,
1998).
Aerial
Hg
was
also
supposed
to
be
the
source
of
Hg
in
plants
(Jia
et
al.,
2010).
The
higher
levels
of
heavy
metals
in
lotus
leaves
than
those
in
lotus
roots
(data
not
shown)
may
come
from
direct
intake
of
atmospheric
pollutants,
which
might
probably
affect
heavy
metals
levels
in
lotus
roots.
This
hypothesis
is
partially
supported
by
the
fact
that
heavy
metals
were
maximum
in
leaves
followed
by
fruits,
and
minimum
in
roots,
which
also
indicated
a
contribution
of
heavy
metals
to
vegetable
leaves
from
atmosphere
(Pandey
and
Pandey,
2009).
Additionally,
heavy
metals
accumula-
tion
in
vegetables
were
reported
to
be
higher
at
market
sites
than
those
at
the
production
locations,
indicating
the
transportation
and
marketing
systems
of
vegetables
play
a
significant
role
in
elevat-
ing
the
contaminant
levels
of
heavy
metals
(Sharma
et
al.,
2009).
Thus
the
multiple
sources
of
pollutants
of
heavy
metals
add
to
the
complexity
of
heavy
metal
accumulation
in
lotus
roots.
Lotus
root
accumulates
heavy
metals
under
a
joint
action
of
plant
and
environment.
Migration
and
absorption
of
heavy
metals
from
soil
to
lotus
roots
may
also
be
influenced
by
lotus
cultivar,
soil
type,
rhizosphere
environment,
and
the
feature
and
status
of
heavy
metals.
The
heavy
metal
concentration
in
roots
was
shown
to
be
dependent
on
the
metal
type
and
root-zone
temperature
(Quadir
et
al.,
2011).
In
this
study,
the
enrichment
coefficient
of
heavy
metals
was
shown
to
vary
with
producing
areas