Bull Environ Contam Toxicol
DOI 10.1007/s00128-016-1872-x
Impact of Irrigation Using Water Containing CuO and ZnO
Nanoparticles on Spinach oleracea Grown in Soil Media
Divya Singh1 • Arun Kumar1
Received: 3 May 2016 / Accepted: 23 June 2016
Ó Springer Science+Business Media New York 2016
Abstract Wastewater reuse is an important adaptation
option for mitigating water stress in rapidly growing urban
centers. Reuse potential of nanoparticles (NPs) contami-
nated wastewater for irrigation of Spinacia oleracea grown
in soil media were assessed in this study. Irrigation of plant
were done with water containing CuO and ZnO NPs as
single compound and in binary mixture (10, 100, 1000 mg/
L) till 11 weeks. At 1000 mg/L, reduction in root length:
16 %, 12 % and 18 %, shoot length: 22 %, 16 % and
27 %, total weight 37 %, 27 % and 45 %, chlorophyll:
18 %, 7 % and 29 % and carotenoids: 46 %, 33 % and
54 % were found for CuO NPs, ZnO NPs and binary
mixture of NPs respectively. Uptake values were found to
be 5.65 ± 0.8 Zn2? and 3.48 ± 0.75 Cu2? mg/g for the
case of ZnO and CuO NPs respectively (at 1000 mg/L).
For mixture of NPs, uptake of 3.18 ± 1.05 mg/g of Cu2?
and 3.18 ± 1.05 mg/g of Zn2? ions were found. The
results shows that water containing low concentration of
NPs (10 mg/L) can be used for irrigating spinach grown in
soil media as no significant toxic effect on growth and
uptake of metal ion were found as compared to control.
The results of this study evaluated the suitability of reusing
water contaminated with NPs in agriculture. Further studies
are however required to understand the toxic mode of
action of mixture of NPs on growth and uptake
mechanisms.
Keywords Nanoparticles  Wastewater reuse  Mixture 
Irrigation  Spinacia oleracea
& Arun Kumar
arunku@civil.iitd.ac.in
1
Department of Civil Engineering, Indian Institute of
Technology Delhi, New Delhi, India
Agriculture sector demands almost 70 % of the total water
consumption, leading to burden on water sources. Cur-
rently around 7 % of world’s agricultural land is irrigated
using raw or partially treated wastewater directly or indi-
rectly. Given the usage of wide range of nanoparticles
(NPs) containing products, presence of these NPs in par-
tially treated wastewater is probable. Two NPs: copper
oxide (CuO) and zinc oxide (ZnO) have been used to fight
the undesirable growth of bacteria, fungi and algae. Thus,
ZnO and CuO NPs are among the most probable contam-
inants to environment (Ates et al. 2015). CuO and ZnO
NPs are found in industrial and domestic wastewater and
have negative effects on organisms like microbes and
invertebrates (Nations et al. 2011). It is likely that envi-
ronmental contamination by NPs will involve mixtures of
NPs not a single NP. In the literature, study focusing on the
impact of mixtures of NPs in plant systems are lacking
(Dimkpa et al. 2015). So this study tried to understand the
response of plant (spinach) irrigated with single and binary
mixture of NPs. Due to its taste and nutritional value,
spinach is a popular leaf vegetable and was selected for this
study. Earlier studies have focused on the effect of other
NPs on spinach growth (Yang et al. 2007) reported an
increase in growth of spinach exposed to TiO2 after
soaking spinach seeds in 0.25 % nano-anatase TiO2 solu-
tion for 48 h. After 35 days, enhancement in fresh weight,
dry weight, and contents of total nitrogen, chlorophyll, and
protein of spinach were also found. In another study, effect
of iron pyrite (FeS2) NPs on spinach seeds were studied
where seeds were soaked in NPs and grown in the field for
50 days. Results show that significantly broader leaf mor-
phology, larger leaf numbers, increased biomass were
observed (Srivastava et al. 2014).
The literature review indicated that the effect of expo-
sure to CuO and ZnO NPs on growth of spinach and the
123

associated metal uptake have not been studied. This
information is required in order to evaluate the feasibility
of irrigating spinach with CuO and ZnO NPs containing
water. The objective of this study was to understand effect
of on Spinach oleracea grown in soil media of irrigation
with water containing CuO and ZnO NPs applied as single
compounds or as a mixture. No study have been conducted
over the full life span of spinach and effect of exposure to
mixture of NPs have also not been investigated. Findings of
this study will help in determining the suitability of irri-
gation of spinach cultures using water containing CuO and
ZnO NPs.
Materials and Methods
Seeds of Spinacia oleracea (spinach) (Variety: Pusa bharti;
Lot no. 02-36-10-06-157) were purchased from National
Seed Corporation (NSC), Indian Agricultural Research
Institute (IARI), New Delhi, India. Spinach seeds were first
sterilized and then soaked in wet cotton in an incubator
with a controlled temperature of 25 ± 2°C for 24 h in the
dark (Singh and Kumar 2015). The soil for this research
were obtained from a garden (N 28° 320 44.200 , E 077° 110
28.900 ). Before using the soil, it was air-dried at room
temperature and characterized (Table 1b). Pre-soaked spi-
nach seeds were planted in the pot filled with same amount
(300 g) of soil (Dimkpa et al. 2012). Number of seeds (10
per pot) were kept to be equal in every pot. Pots were kept
in an open environment (Rodda et al. 2011) and seeds were
allowed to first grow for 3 weeks using deionised water
(DI) as irrigation water. The soil humidity were kept
between 40 % and 60 % of the field capacity (Hammel
et al. 2000) by daily measuring weight of each pot, and
adjusting moisture by adding deionised water (Almås et al.
Table 1 Characterization of
Parameters
irrigation water and soil
(A) Characterization of irrigation water [concentration 10 mg/L (n = 3)]
Size (nm)
pH
Measured ion conc. (mg/L)
Parameters
(B) Characterization of soil
Texture
pH
Soluble salt
123
Bull Environ Contam Toxicol
2006). Seedlings were sown in every pot and healthy
seedlings were thinned to 5 per pot after 3 weeks. ZnO NPs
(CAS No. 1314-13-2) (size: \100 nm) and CuO NPs (CAS
No. 1317-38-0) (size: \50 nm) were purchased from
Sigma-Aldrich Chemicals Pvt. Ltd., Bangalore, India.
Suspension of NPs were made in deionised water at three
concentrations values: 10, 100, 1000 mg/L and control. All
the experiment were conducted using deionised water. NPs
when in suspension, increase in size due to agglomeration.
This behavior is also reported in previously published lit-
erature (Trujillo-Reyes et al. 2013). This range have lower
value (10 mg/L) and higher value (1000 mg/L). The lower
concentration value used in the study represents environ-
mentally relevant concentration reported in earlier studies
(Mueller and Nowack 2008). Higher concentration values
([10 mg/L) were used to evaluate the effect on plant
during worst case scenario. Concentrations lower than
10 mg/L were not used in this study as concentration
\10 mg/L have not been shown to have any significant
changes in physiological parameters during seed germina-
tion (Singh and Kumar 2015). No work has been done on
exposure of CuO and ZnO NPs on growth of spinach. As
spinach is an important plant, understanding effect of
irrigation with water containing NPs is required. Also no
previous attempt have been made for binary mixture of
CuO and ZnO NPs on spinach. This study selected three
NPs concentration: 10, 100, 1000 mg/L to study the effect
on spinach. These concentrations values are on log scale so
that effect can properly be seen. This type of concentration
range has also been used in previous related studies
(Stampoulis et al. 2009; Thuesombat et al. 2014). Sus-
pensions were made for CuO NPs and ZnO NPs as single
compounds and in a binary mixture and were ultrasoni-
cated (100 W, 33 ± 3 kHz) for 1 h and used as irrigation
water. For initial characterization of NPs suspension
CuO NPs ZnO NPs Binary mixture
242 ± 69 138 ± 44 500 ± 102
9±1 8±2 8±1
Cu2? = 0.46 ± 0.07 Zn2? = Cu2? = 0.28 ± 0.01,
6 ± 0.3 Zn2? = 5 ± 0.23
Values Parameters Values
Clay-loam SO42- (mg/g) 94.55
5.8 NO3 (mg/g) 54.23
9.26 mS Mg (mg/g) 0.0004
Cu (mg/g) 4.004
Zn (mg/g) 10.08
Bull Environ Contam Toxicol
(irrigation water), dynamic light scattering (DLS)-based
particle size analyzer (Nicomp 380 ZLS-Particle sizing
system) was used for determination of size (size range
0.5 nm to 6 lm) and atomic absorption spectrometry
(AAS) (model 4141, ECI) was used for ion release were
used. As part of QA/QC protocol, calibration checks were
performed before sample analysis. DLS instrument was
calibrated daily with 90 nm polystyrene latex standards.
Measurements were conducted at 25°C with an equilibra-
tion time of 5 min to obtain the z-average particle size.
Size were displayed in terms of relative intensity of scat-
tered light versus diameter for a sample run. In case of
AAS, standards of different concentrations were freshly
prepared and used to prepare the calibration curve before
the sample analysis (Wavelength used for Cu were
324.7 nm and for Zn were 213.9 nm.). This exercise was
repeated three times independently and results are reported
in mean ± standard deviation (n = 3). The measured size,
pH and concentration of ions of the suspension used for
irrigation are reported in Table 1. The plants were exposed
to NPs in the form of irrigation water till the end of crop
life cycle. The plants were harvested at the end of crop
cycle as per methodology used previously (Maftoun et al.
2006). The root system of each spinach plant was removed
by first carefully breaking apart the soil with a metal
scoopula and then roots and shoots were separated. Root
length and shoot length were measured using a ruler
(value ± 0.05 cm). Fresh weight was measured and
chlorophyll and carotenoid contents were determined using
the methods described by Arnon 1949. These parameters
were also used previously to evaluate toxicity of NPs to
plants (Lin and Xing 2008; Lee et al. 2012; Nair and Chung
2014). In our study, fresh weight of plants will be used to
indicate effect of NPs production of spinach considering
that agricultural production can be measured as the fresh
weight of plant (Keating et al. 1999). Other parameters,
like shoot length, root length and chlorophyll content have
been considered as primary toxicity indicators (Rao and
Shekhawat 2014). The uptake of ions in the plant was
determined using AAS as per the method previously
described in (Dimkpa et al. 2012). All tests were conducted
in triplicates. R software (R version 3.1.2 (2014-10-31) was
used to study normality of data. Two-way Analysis of
Variance (ANOVA) and Tukey’s honest significant dif-
ference (HSD) test in Data Analysis Tool Pack of Micro-
soft Excel (MS Excel 2013) were used to study difference
of effects of concentrations for ZnO NPs and CuO NPs
single compounds and as a mixture. A comparison of
toxicity and uptake of ZnO NPs and CuO NPs was done
using a paired t test for the whole concentration range. All
statistical analyses were tested for a 0.05 level significance
test (a = 0.05).
Results and Discussion
Effects of NPs on root length, shoot length, root weight,
shoot weight, chlorophyll and carotenoids contents of spi-
nach were observed. In case of root length (Fig. 1a), a
slight increase with regards to control was observed at
lower concentration (10–100 mg/L) for all types of expo-
sure (p [ 0.05). For CuO, ZnO and binary mixture of NPs,
reduction in root length were found to be 16 %, 12 % and
18 % respectively at the highest concentration tested
(1000 mg/L) (p \ 0.05). In case of shoot length (Fig. 1b),
22 %,16 % and 27 % reductions in shoot length were
found at the highest exposed concentration (1000 mg/L)
for CuO, ZnO and binary mixture of NPs respectively
(p \ 0.05). Reductions in root length and shoot length were
found to be same for CuO NPs, ZnO NPs and mixture at all
exposure concentrations (p [ 0.05). Figure 1c shows
effects of the NPs on the total weight to S. oleracea plants
grown for 11 weeks. At the highest exposure concentration
(1000 mg/L), maximum reduction were found: 37 %, 27 %
and 45 % (p \ 0.05) for CuO, ZnO and binary mixture of
NPs, respectively. Results also showed that the yield is
affected highest exposure concentration of 1000 mg/L
only. Concentration less than 1000 mg/L have not resulted
in significantly different reduction in fresh weight from
control (p [ 0.05). Figure 1d, e shows effect of NPs on
total chlorophyll and carotenoid content (in mg/g leaf tis-
sue). Reduction in total chlorophyll content with regards to
control was not found to be significantly different from
control for ZnO NPs. For CuO and binary mixture of NPs,
reductions in total chlorophyll contents were found to be
highest at 1000 mg/L, with reduction of 18 and 29 %
respectively (p \ 0.05). Figure 1e shows effect on total
carotenoids content. Reduction in total carotenoids content
with regards to control were observed for all exposure
concentrations. At the highest exposure (1000 mg/L)
reductions were found to be 46 %, 33 % and 54 %
(p \ 0.05) for CuO, ZnO and binary mixture of NPs,
respectively. Reductions in root length, shoot length, total
weight, chlorophyll and carotenoid content at highest
exposure concentration were found to be similar for CuO
NPs, ZnO NPs and mixture. Figure 1f shows the uptake of
ions in the plant tissue exposed to single compound and
mixture of NPs to spinach till the end of life cycle (CuO
and ZnO NPs: uptake of Cu and Zn ions due to exposure of
CuO NPs and ZnO NPs respectively; Mix-Cu and Mix-Zn:
uptake of Cu and Zn ions due to exposure of mixture of
CuO and ZnO NPs). At highest exposure concentration,
maximum uptake in spinach plant was found for ZnO NPs
(5.65 ± 0.8 Zn2?mg/g). For CuO NPs, uptake was found
to be 3.48 ± 0.75 Cu2? mg/g. For the mixture of NPs, the
uptake of Cu2? and Zn2? ions, at the highest exposure
123

Fig. 1 Effect of NPs on a Root length b Shoot length c Total weight
d Chlorophyll content e Carotenoid content and f ion content of S.
oleracea plants. Values are reported as mean ± standard deviation
concentration, were found to be 3.18 ± 1.05 and
3.42 ± 0.86 mg/g dry weight, respectively. In case of the
mixture of NPs uptake of Cu2? and Zn2? ions were not
found to be significantly different from each other
(p [ 0.05). Higher inhibition by CuO NPs can be attributed
to aggregation properties of CuO NPs which might have
blocked the pores present on root surface. Further studies
need to be done for a better understanding of toxicity
mechanism. Also, Cu ions are reported to be more toxic to
plants than Zn ions (Warne et al. 2008).
Findings of this study were compared with that reported
in literature on toxicity of CuO and ZnO NPs to leafy
vegetables. At lower concentration (\100 mg/L) no sig-
nificant effect due to CuO and ZnO NPs was found. This
observation is reported in previous studies also (Dimkpa
et al. 2012). At highest exposure concentration of
1000 mg/L of CuO NPs, reductions in root length, shoot
length and total weight were observed to be 16 %, 22 %,
37 % respectively as compared to control. No study is
available in literature reporting toxic effects mixture of
ZnO and CuO NPs on spinach and thus this data could not
be compared. Previously, 11 % (p \ 0.05) reduction in
shoot length of cilantro (Coriandrum sativum) grown for
30 days in commercial potting mix soil amended with CuO
NPs (0, 20 and 80 mg Cu per kg) were found but no effect
on root length was observed. Also, CuO NPs at high con-
centration yielded more biomass, compared with control
(p \ 0.05) (Zuverza-Mena et al. 2015). Uptake of Cu2?
ions at highest exposure concentration was found to be
0.164 mg/g in the plant biomass. Our study also reported
123
Bull Environ Contam Toxicol
(n = 3) (asterisk indicates that value is significantly different from
control; p \ 0.05). Here Mix-Cu and Mix-Zn indicates uptake of Cu
ions and Zn ions in plants exposed to mixture of NPs respectively
observations similar to the published study. Another report
on lettuce grown in hydroponic media for 15 days (con-
centration: 0, 5, 10, 20 mg/L in Hoagland media) indicated
that at 10 mg/L of CuO NPs, reduction in root length of
lettuce (Lactuca sativa) was found to be 49.5 % (Hong
et al. 2015). At the highest exposure concentration uptake
of Cu2? ions was found to be 12.3 mg/g of plant dry
weight. In our study, the uptake was found to be approxi-
mately 0.15 mg/g for CuO NPs at exposure concentration
of 10 mg/L. The difference in uptake may be due to dif-
ferent media used in this study. In another study CuO NPs
(0, 10, 100 mg/L) were exposed to maize plant in hydro-
ponic media for 15 days where, root elongation of maize
was found to be significantly inhibited. Exposures of 10
and 100 mg/L CuO NPs to plant reduced root elongation
by 55 % and 84 % respectively (p \ 0.05), relative to
control. By day 14, 10 mg/L CuO NPs reduced the fresh
weight of root and shoot tissues by 60 % and 34 %
respectively (p \ 0.05), compared to the unexposed control
plants (Wang et al. 2012). The uptake values were
0.0005 mg/g for root portion and 0.00007 mg/g for shoot
portion at the highest exposure concentration i.e. 100 mg/
L. In our study, uptake of ions at this concentration was
found to be 0.40 mg/g for plant biomass. The significant
difference in uptake values from our finding can be
attributed to different exposure method and plant type
followed in this study. Also, in case of wheat, root length
and shoot length were found to be reduced significantly by
59 % and 13 % at exposure concentration of 500 mg/kg of
sand mixed with CuO NPs. As in our study no significant
Bull Environ Contam Toxicol
effect on total weight were found (Dimkpa et al. 2012). In
our study 18 % reduction in chlorophyll content were
found at highest exposure concentration of 1000 mg/L of
CuO NPs which were found to be very low as compared to
previously reported data. Dimkpa et al. 2012 reported
chlorophyll reduction of 38 % in leaves (at 500 mg/kg
sand) of wheat for CuO NPs. The reason for different
observations could be different growing conditions, envi-
ronment and the type of plant used for conducting the
experiments. Uptake of Cu2? ions in shoot portion dry
weight was found to be 0.375 mg Cu/g shoot dry weight at
exposure of 500 mg CuO NPs/kg of sand.
For ZnO NPs, reductions in root length, shoot length and
total weight were observed to be 12 %, 16 %, 27 %
respectively as compared to control (at 1000 mg/L). Other
studies have reported reductions in shoot length, root
length and fresh weight of 46 %, 71 % and 89 % respec-
tively (p \ 0.05) to B. juncea seeds during exposure of
ZnO NPs at 1500 mg/L of exposure concentration in
hoagland media. No uptake studies have been performed in
this study (Rao and Shekhawat 2014). Contrary to no sig-
nificant effect on chlorophyll content at 1000 mg/L in our
study, significant decrease in total chlorophyll content
(p \ 0.05) as compared to control were recorded at
1000 mg/L of ZnO NPs (Rao and Shekhawat 2014). The
difference may be due to use of two different types of
media, i.e. soil and hydroponic (for Brassica juncea grown
for 96 h). Another study on ZnO in hydroponic media
reports 50 % reduction in total weight of ryegrass grown in
hydroponic media for 12 days at highest exposed concen-
tration of 1000 mg/L of ZnO NPs for. Uptake of Zn2? ions
in this study was found to be 0.14 mg/g dry weight of plant
at highest exposure of 1000 mg/L (Lin and Xing 2008). In
case of another plant, wheat grown in sand matrix with
ZnO NPs for 14 days indicated 53 %, 8 % and 38 %
reductions in root length, shoot length and chlorophyll
content at 500 mg/Kg of exposure concentration. At this
concentration no significant effect of total weight were
reported in this study. Uptake of Zn2? ions in shoot portion
dry weight was found to be 2.076 mg Zn/g shoot dry
weight at exposure of 500 mg ZnO NPs/kg of sand
(Dimkpa et al. 2012). In our study, significant reduction in
total chlorophyll and carotenoids content as compared to
control were obtained at highest exposure concentration of
1000 mg/L for CuO NPs and binary mixture of CuO and
ZnO NPs. Previous studies have drawn the conclusion that
excess Zn2? and Cu2? ions results in chloroplast disorga-
nization and a reduction in the numbers of thylakoid and
grana induce the loss of chlorophyll pigments (Souza et al.
2005).
The difference in toxicity and uptake of NPs in plants
can be attributed to different species of plants and media
used. The amount of ions released in the media is also an
important factor. More uptake of Zn2? ions may be due to
higher solubility of ZnO NPs as compared to CuO NPs.
ZnO has greater solubility (logK = 11.16) than CuO NPs
(logK = 7.66) in suspension (Dimkpa et al. 2015). Release
of ions from CuO and ZnO suspensions also reflect more
dissolution of Zn2? ions from ZnO than Cu2? ions released
from CuO NPs. As shown in Table 1a, for 10 mg/L of
CuO, 0.46 ± 0.07 mg/g of Cu2? ions were found in sus-
pension at pH of 9. For ZnO NPs suspension,
6.01 ± 1.37 mg/g of Zn2? ions were present in suspension
at pH of 8.65. High release of Zn2? ions from the sus-
pension might be resulting in high uptake of Zn2? ions in
spinach. Mechanism of toxicity and uptake due to exposure
of NPs in irrigation water have not been studied. Although
there are some of the proposed mechanisms present in the
literature. Some study says that NPs can pass through the
epidermis and cortex through apoplastic pathway (Lin and
Xing 2008). CuO NPs can be transported in the plants via
xylem and phloem (Wang et al. 2012). ZnO NPs were
assumed able to increase the permeability of plant cell
walls by creating ‘‘holes’’ in the cell wall, and then enter
into the cells. After entering the cells, the NPs may be able
to transport between cells via plasmodesmata (Lin and
Xing 2008). However more studies are needed in order to
determine the mechanism by which Cu-based NPs or
compounds interfere with plant growth.
Presence of NPs in wastewater in inevitable and suit-
ability of this water for irrigation purpose is important to
explore. Considering that wastewater might contain mixture
of NP at a time, this study used single NP as well as mixture
of NPs for conducting the study. The findings of the study
will help in understanding actual practice of partially trea-
ted wastewater irrigation in a better way. Leafy vegeta-
bles being rich source of nutrients and common in daily use.
Also, leafy vegetables have more bioaccumulation factor of
metal ions than non-leafy vegetables (Ali and Al-Qahtani
2012). The results will help us in deciding which plant
should be grown in the fields prone to get NPs contaminated
wastewater for irrigation. This will further help in better-
ment of agriculture without compromising productivity. No
significant reduction in root length, soot length, total weight
were found for lower concentration (10–100 mg/L)
(p [ 0.05). For 1000 mg/L of exposure concentration,
reduction in all the parameters were found to be signifi-
cantly different from control (p \ 0.05). Also reduction
were found to be same for all three types of NP exposure.
Chlorophyll and carotenoids content were found to be
reduced for all exposure types and highest reduction was
observed at 1000 mg/L (p \ 0.05). Effect of NPs exposed
as single and in binary mixture to spinach were studied on
total biomass (yield). The results shows that effect on bio-
mass due to exposure of single NPs were not significantly
different than that for the case of binary mixture of NPs for
123

all studied concentration (p [ 0.05). This means, CuO NPs
and ZnO NPs either exposed as single NPs or in binary
mixture will not result in significant difference in total
biomass production for concentration range from 10 to
100 mg/L. So wastewater containing a mixture of CuO and
ZnO NPs is suitable for irrigation purpose without com-
promising the yield for concentration up to *100 mg/L.
The results shows that, 10 mg/L of NPs concentration in
wastewater will not be toxic to the plant. Water contain
higher concentration ([10 mg/L) need to be pretreated
before using for irrigational activities. In future, toxicity
mechanism need to be studied to understand long term
effect of NPs (as single compound and as a mixture) on
plants. Effects of size, charge and shape of NPs on toxicity
to plants also need be understood. Deionized water spiked
with NPs and ions were used for irrigating plants. Studies
using river water or wastewater effluent must be conducted
for a better understanding of exposure of CuO and ZnO NPs
on plant growth.
Acknowledgments The authors would like to thank the Council of
Scientific and Industrial Research (India) for helping out in con-
ducting this study. We are also thankful to IIT Delhi for providing
support for this study.
References
Ali MHH, Al-Qahtani KM (2012) Assessment of some heavy metals
in vegetables, cereals and fruits in Saudi Arabian markets. Egypt
J Aquat Res 38:31–37. doi:10.1016/j.ejar.2012.08.002
Almås AR, Lombnaes P, Sogn TA, Mulder J (2006) Speciation of Cd
and Zn in contaminated soils assessed by DGT-DIFS, and
WHAM/Model VI in relation to uptake by spinach and ryegrass.
Chemosphere 62:1647–1655. doi:10.1016/j.chemosphere.2005.
06.020
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphe-
noloxidase in Beta vulgaris. Plant Physiol 24:1–15
Ates M, Arslan Z, Demir V, Daniels J, Farah IO (2015) Accumulation
and toxicity of CuO and ZnO nanoparticles through waterborne
and dietary exposure of goldfish (Carassius auratus). Environ
Toxicol 30(1):119–128. doi:10.1002/tox.22002
Dimkpa CO, McLean JE, Latta DE et al (2012) CuO and ZnO
nanoparticles: phytotoxicity, metal speciation, and induction of
oxidative stress in sand-grown wheat. J Nanoparticle Res
14:1125. doi:10.1007/s11051-012-1125-9
Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2015) Nano-CuO
and interaction with nano-ZnO or soil bacterium provide
evidence for the interference of nanoparticles in metal nutrition
of plants. Ecotoxicology 24:119–129. doi:10.1007/s10646-014-
1364-x
Hammel W, Debus R, Steubing L (2000) Mobility of antimony in soil
and its availability to plants. Chemosphere 41:1791–1798.
doi:10.1016/S0045-6535(00)00037-0
Hong J, Rico CM, Zhao L et al (2015) Toxic effects of copper-based
nanoparticles or compounds to lettuce (Lactuca sativa) and
alfalfa (Medicago sativa). Environ Sci Process Impacts
17:177–185. doi:10.1039/c4em00551a
Keating B, Robertson M, Muchow R, Huth N (1999) Modelling
sugarcane production systems I. Development and performance
123
Bull Environ Contam Toxicol
of the sugarcane module. Field Crops Res 61:253–271. doi:10.
1016/S0378-4290(98)00167-1
Lee W-M, Il Kwak J, An Y-J (2012) Effect of silver nanoparticles in
crop plants Phaseolus radiatus and Sorghum bicolor: media
effect on phytotoxicity. Chemosphere 86:491–499
Lin D, Xing B (2008) Root uptake and phytotoxicity of ZnO
nanoparticles. Environ Sci Technol 42:5580–5585. doi:10.1021/
es800422x
Maftoun M, Moshiri F, Karimian N, Ronaghi AM (2006) Effects of
two organic wastes in combination with phosphorus on growth
and chemical composition of spinach and soil properties. J Plant
Nutr 27:1635–1651. doi:10.1081/PLN-200026005
Mueller NC, Nowack B (2008) Exposure modeling of engineered
nanoparticles in the environment. Environ Sci Technol
42:4447–4453. doi:10.1021/es7029637
Nair PMG, Chung IM (2014) Physiological and molecular level
studies on the toxicity of silver nanoparticles in germinating
seedlings of mung bean (Vigna radiata L.). Acta Physiol Plant
37:1719. doi:10.1007/s11738-014-1719-1
Nations S, Wages M, Cañas JE et al (2011) Acute effects of Fe2O3,
TiO2, ZnO and CuO nanomaterials on Xenopus laevis. Chemo-
sphere 83:1053–1061. doi:10.1016/j.chemosphere.2011.01.061
Rao S, Shekhawat GS (2014) Toxicity of ZnO engineered nanopar-
ticles and evaluation of their effect on growth, metabolism and
tissue specific accumulation in Brassica juncea. J Environ Chem
Eng 2:105–114. doi:10.1016/j.jece.2013.11.029
Rodda N, Salukazana L, Jackson SAF, Smith MT (2011) Use of
domestic greywater for small-scale irrigation of food crops:
effects on plants and soil. Phys Chem Earth Parts A/B/C
36:1051–1062. doi:10.1016/j.pce.2011.08.002
Singh D, Kumar A (2015) Effects of nano silver oxide and silver ions
on growth of Vigna radiata. Bull Environ Contam Toxicol.
doi:10.1007/s00128-015-1595-4
Souza JF, Dolder H, Cortelazzo AL (2005) Effect of excess cadmium
and zinc ions on roots and shoots of maize seedlings. J Plant Nutr
28:1923–1931. doi:10.1080/01904160500310435
Srivastava G, Das CK, Das A et al (2014) Seed treatment with iron
pyrite (FeS2) nanoparticles increases the production of spinach.
RSC Adv 4:58495–58504. doi:10.1039/C4RA06861K
Stampoulis D, Sinha SK, White JC (2009) Assay-dependent phyto-
toxicity of nanoparticles to plants. Environ Sci Technol
43:9473–9479. doi:10.1021/es901695c
Thuesombat P, Hannongbua S, Akasit S, Chadchawan S (2014) Effect
of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105)
seed germination and seedling growth. Ecotoxicol Environ Saf
104:302–309. doi:10.1016/j.ecoenv.2014.03.022
Trujillo-Reyes J, Vilchis-Nestor AR, Majumdar S et al (2013) Citric
acid modifies surface properties of commercial CeO2 nanopar-
ticles reducing their toxicity and cerium uptake in radish
(Raphanus sativus) seedlings. J Hazard Mater 263(Pt
2):677–684. doi:10.1016/j.jhazmat.2013.10.030
Wang Z, Xie X, Zhao J et al (2012) Xylem- and phloem-based
transport of CuO nanoparticles in maize (Zea mays L.). Environ
Sci Technol 46:4434–4441. doi:10.1021/es204212z
Warne MSJ, Heemsbergen D, Stevens D et al (2008) Modeling the
toxicity of copper and zinc salts to wheat in 14 soils. Environ
Toxicol Chem 27:786–792. doi:10.1897/07-294.1
Yang F, Liu C, Gao F et al (2007) The improvement of spinach
growth by nano-anatase TiO2 treatment is related to nitrogen
photoreduction. Biol Trace Elem Res 119:77–88. doi:10.1007/
s12011-007-0046-4
Zuverza-Mena N, Medina-Velo IA, Barrios AC et al (2015) Copper
nanoparticles/compounds impact agronomic and physiological
parameters in cilantro (Coriandrum sativum). Environ Sci
Process Impacts. doi:10.1039/c5em00329f