Journal of Cleaner Production 222 (2019) 835e843

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Journal of Cleaner Production

journal homepage: www.elsevier.com/locate/jclepro

Micro-nano bubble water oxygation: Synergistically improving

irrigation water use efficiency, crop yield and quality
Yaxin Liu, Yunpeng Zhou, Tianze Wang, Jiachong Pan, Bo Zhou, Tahir Muhammad,
Chunfa Zhou, Yunkai Li*
College of Water Resources and Civil Engineering, China Agricultural University, Beijing, 100083, China

a r t i c l e i n f o a b s t r a c t

Article history: Coordination of water saving, yield and quality increase remains an attractive problem in agricultural
Received 26 March 2018 production. Transporting irrigation water rich in micro-nano bubbles and fertilizers to the crop root zone
Received in revised form through subsurface drip irrigation is expected to be an effective technique. In present study, cucumber
18 February 2019
and tomato cultivated in greenhouse were subjected to investigate the effects of three mixing ratios of
Accepted 19 February 2019
Available online 27 February 2019
micro-nano bubble water and groundwater combined with three different oxygation frequencies on
irrigation water use efficiency, crop yield and quality. The results indicated that micro-nano bubble water
oxygation could significantly increase their yield, irrigation water use efficiency and fruit quality
Keywords:
Micro-nano bubbles
(p < 0.05) without increasing the amounts of irrigation water and fertilizer, which demonstrated a
Oxygation cleaner production being friendly to soil ecological environment and sustainability using water saving
Irrigation water use efficiency technology. In the optimal treatment, the yield, irrigation water use efficiency, vitamin C, and soluble
Crop yield sugar of tomatoes increased by 16.9%, 16.9%, 17.7% and 39.2%, while those for cucumbers were 22.1%,
Fruit quality 22.1%, 16.7% and 19.4%, respectively. This was mainly due to the increased soil oxygen content, longer
Subsurface drip irrigation retention time and stronger mass transfer ability of micro-nano bubbles. The recommended micro-nano
bubble water oxygation mode for tomato plantation was the mixing ratio of 1:4 combined with the
frequency of once every 5d, while that of cucumber being the mixing ratio of 1:0 with the same fre-
quency with tomato. The study aims to provide a novel concept for the synergistic realization of water
saving, yield increases and quality improvements in greenhouse crop production using subsurface drip
irrigation.
© 2019 Elsevier Ltd. All rights reserved.

1. Introduction development. To overcome the aforementioned issue, number of

The current growing scarcity of irrigation water become a
fundamental issue at global scale (Sun et al., 2016). The United
Nations has predicted, the global food demand will increase by 70%
and agricultural water consumption will increase by 19% till 2050
(Shah et al., 2018). Thus, it is critical to save agricultural water on
basis of ensuring food security. Traditional irrigation methods
usually increase crop yield by applying large amounts of water and
fertilizer, which is not conductive to water saving and soil ecolog-
ical environment. How to save water and fertilizer and meanwhile
increase yield has become a focal point for agricultural
* Corresponding author.College of Water Resources and Civil Engineering, China
Agricultural University, 17# Qinghua East Road, Haidian District, Beijing, 100083,
China.
E-mail addresses: liyunkai@126.com, yunkai@cau.edu.cn (Y. Li).
studies had explored and proposed a series of water-saving tech-
nologies such as drip irrigation (Li et al., 2016a,b; Lu et al., 2016),
partial root-zone irrigation (Liang et al., 2013). However, with the
continuous improvement of living standards, consumers’ con-
sumption demands have been shifted from quantitative to quali-
tative (Rajkumar et al., 2012; Li et al., 2016c). How to achieve
coordination of water saving, yield increases and quality
improvement with a minimum irrigation water and fertilizer
quantity has become a challenge in cleaner production for modern
agriculture, particularly for greenhouse production.
Oxygation is a functional drip irrigation technology that adding
the oxygen to irrigation water using the equipment or via chemicals
through a subsurface drip irrigation (SDI) system. Oxygation can
increase the oxygen content in soil by 2.4%e32.6% (Chen et al.,
2010), improving soil aeration and promoting the aerobic respira-
tion of crop roots (Niu et al., 2011), increasing the soil microbial

https://doi.org/10.1016/j.jclepro.2019.02.208
0959-6526/© 2019 Elsevier Ltd. All rights reserved.
836 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843
quantity and soil enzyme activity (Zhang and Wang, 2006; Li et al.,
2015). With oxygation, the yields of many different crops, such as
tomato (Jia et al., 2011), watermelon (Liu et al., 2010), corn (Abuarab
et al., 2013), cotton (Pendergast et al., 2013), have increased
significantly and varied within 10%e33%. The crop qualities were
also improved to some extents. Related studies on oxygation
mainly concerned the use of venturi air injectors, air pumps or
hydrogen peroxide (Glinski and Stepniewski, 1985; Torabi et al.,
2013; Wen et al., 2013). However, these three technologies deliv-
ered large sized oxygen bubbles to the crops root zone, and easily
causing chimney effect. In other words, the oxygen could easily
escape from the soil in the crop root zone. Hence, a method must be
established to increase the oxygation efficiency.
Micro-nano bubbles (MNBs) are the bubbles with diameters
between micro-bubbles and nano-bubblels, sized between
200 nm and 50 mm (Agarwal et al., 2011). Because of there mini-
mal diameter, large specific surface area and great pressure, MNBs
have some particular characteristics such as long storage time,
strong air solubility, strong adsorption, etc. (Takahashi et al.,
2003; Xiong et al., 2016). MNBs are of great value in the fields
of water aeration, water purification, biological pharmacy, medi-
cal and health care, and precision chemical reaction (Bao et al.,
2016). However, this technology has been rarely adopted in
agricultural irrigation so far. Therefore, a field experiment was
conducted using a MNB generator to deliver the irrigation water
rich in MNBs and fertilizer to the tomato and cucumber crop root
zones via SDI system, and the following aspects were evaluated:
(1) influences of micro-nano bubble water oxygation (MNBWO)
on the dry matter accumulation, yield and irrigation water use
efficiency (IWUE) of cucumber and tomato; (2) influences of
MNBWO on the nutritional quality and flavor indices of cucumber
and tomato; (3) proposing optimized MNBWO mode of cucumber
and tomato, including mixing ratio of MNB water and ground-
water, and the oxygation frequency.
2. Materials and methods
2.1. Experimental location and test materials
The study was conducted in a greenhouse at Tongzhou Experi-
mental Station of China Agricultural University (N39
360 -40
020 ,
E116
320 -116
560 ) from March to October, 2016. The experimental
area locates in a continental monsoon climate zone, which is
affected by winter and summer monsoons, exhibiting a windy
spring drought, high-temperature summer rains, cool autumns,
and cold and dry winters. The annual average temperature and
rainfall are 11.3
C and 620 mm. The experimental greenhouse was
60 m in length and 8 m in width. Tomato (Lycopersicon esculentum
M., ‘‘Zhongyan 99800 ) and cucumber (Cucumis sativus L., “Jinyou No.
2”) transplants were set on March 25, 2016 for spring cultivation
and July 30, 2016 for autumn cultivation. The physical and chemical
properties are presented in Table 1.
Table 1
Physical and chemical soil properties of the experimental site.
Soil texture Soil bulk density Field capacity
g/cm3 g/kg
loam soil 1.8 23.0
Available nitrogen Available phosphorus Available potassium
g/kg g/kg g/kg
0.6 0.8 3.0
2.2. Experimental design and treatments
In the present experiment, a full 32 factorial design was per-
formed to evaluate the effects of the mixing ratios of MNB water
and groundwater (M1/0, M1/4, M0/1) and the oxygation frequencies
(once every three days, five days and seven days, which referred to
F1/3, F1/5, F1/7), with a total of nine treatments (Wang et al., 2018).
The experimental arrangements details are shown in Table 2. The
experiment was arranged as a randomized complete block design
and each treatment was replicated four times. Each experimental
plot was 6 m long and 3 m wide. Cucumber and tomato plants were
cultivated in the row with the spacing of 30 cm and 50 cm,
respectively. The SDI laterals were laid in 5 cm underground with
the internal diametes of 16 mm and the emitter spacing of 30 cm,
delivering water at the rated outflow of 2.6 L/h. The crop planting
patterns and lateral arrangement of the SDI system are shown in
Fig. 1. Overall, 48 tomato plants were planted per treatment and 12
tomato plants per replication; while 60 cucumber plants per
treatment and 15 for each replication.
MNB water was produced by a mobile MNB generator, utilizing
the dissolved gas release method to generate MNBs, which is
known as a preferable method for generating large amounts of
MNBs suspension timely. Each MNB generator costs about 1720
USD, which can be used for 10 greenhouses, each with an area of
480 m2. The machine consisted of several parts, including a diesel
generator, compost storage tank, water storage tank, air pump MNB
generator, and self-priming pump, as is shown in Fig. 2. The
equipment included a water inlet and water supply, and the water
outlet was connected with the drip irrigation system by the quick
joints, as shown in the Supplementary Fig. 1. So the generator was
able to connect quickly with the subsurface drip irrigation system,
and meanwhile producing water rich in MNBs conveniently. The air
inflow volume was regulated by a gas flowmeter. The mean size and
numbers of bubbles in water were determined with the Nano-
Particle Tracking Analysis (NanoSight NS300, Marlern, UK), which
turned out to be 136.2 nm ± 12.1 nm and 6.23  108 particles/mL, as
is shown in the Supplementary Fig. 2. Several preliminary experi-
ments were conducted to investigate the dissolved oxygen con-
centration (DO) variations during oxygation and attenuation, as
well as along the arrangement of drip lateral which was 60 m in
length. The DO in water exhibited an initial increment followed by a
stabilization after 50 min, with the highest DO being 8.2 mg/L, as is
shown in the Supplementary Fig. 3. DO of MNB water maintained a
high level at 7.8 mg/L for as long as 200 h, which was decreased by
5% comparing to the initial concentration, while increasing by 95%
comparing to non-oxygenated water, as is shown in the
Supplementary Fig. 3. No dramatic variation in DO of micro-nano
bubble water was observed along within 60 m long dripline, as is
shown in the Supplementary Fig. 3.
The experimental irrigation quota and fertilizer applied in each
treatment were determined according to Zhang and Deng (2012).
Thus the irrigation and fertilization treatments were identical in all
treatments throughout the growth period except for when the
Total nitrogen Total phosphorus Total potassium
g/kg g/kg g/kg
2.4 0.6 11.8
Organic matter Cation exchange capacity pH
g/kg mol/kg
18.1 9.9 7.5
 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843 837

Table 2
Experiments treatments arrangement.

Treatment Number Mixing ratio Oxygation frequency Treatments name for cucumber Treatment names for tomato

1 1:0 1/3d CM1/0F1/3 TM1/0F1/3

2 1:4 1/3d CM1/4F1/3 TM1/4F1/3
3 0:1 1/3d CM0/1F1/3 TM0/1F1/3
4 1:0 1/5d CM1/0F1/5 TM1/0F1/5
5 1:4 1/5d CM1/4F1/5 TM1/4F1/5
6 0:1 1/5d CM0/1F1/5 TM0/1F1/5
7 1:0 1/7d CM1/0F1/7 TM1/0F1/7
8 1:4 1/7d CM1/4F1/7 TM1/4F1/7
9 0:1 1/7d CM0/1F1/7 TM0/1F1/7

Note: C: cucumber, T: tomato; M: the mixing ratio of micro-nano bubble water and groundwater; F: the MNBWO frequency.

Fig. 1. The crop planting patterns and lateral arrangement of subsurface drip irrigation system Unit: mm.

and then, the roots were rinsed. First, the plant roots and plant stem
and leaves (not including the fruit) were placed into separate paper
bags. Later the plant parts were dried at 105
C for 30 min, and then
it was weighed by an electronic balance until reaching a constant
weight at the constant temperature of 75
C. Then, the root-crown
ratio was calculated. The root-crown ratio is the ratio of root dry
weight to the dry weight of stem and leaves, which mainly used to
reflect the relationship between aboveground and underground
parts of a crop. A large root-crown ratio indicates that the root is
robust and well developed to a certain extent.

2.3.2. Yield, IWUE and quality

Fig. 2. The mobile machine integrating water, fertilizer and gas. Notes: 1. Diesel
generator 2. Micro-nano bubble generator used pump 3. Compost storage tank 4.
Water storage tank 5, 6. Self-priming pump 7. Air pump of micro-nano bubble
generator 8. The gas solution tank of micro-nano bubble generator.
irrigation frequency and mixing ratio were different. The specific
irrigation scheme was shown in Table 3.
2.3. Testing parameters
2.3.1. Dry matter accumulations
During the fruit-developing period of tomato and cucumber,
three plants were dug out randomly selected from each treatment,
The yield of each treatment, which consists of 4 lines, each with
a length of 6 m, was measured and converted into hectares. Soluble
solids were measured by a hand-held refractometer (produced by
ATAGO, Pvt. Ltd., Japan), and the total soluble sugars was deter-
mined by the anthrone colorimetric method, the vitamin C content
was determined by 2,6-dichlorophenolindophenol titration, the
titratable acidity content was determined by acid-base titration, the
lycopene of tomato was tested by ultraviolet spectrophotometer
(Gao, 2006), and the hardness value of the pulp was determined
using a hardness tester produced by (AIDEBAO Pvt. Ltd., China). The
IWUE of the crops was calculated according to Guo et al. (2018).
2.3.3. Soil oxygen content
The soil oxygen content of the three treatments (F1/5M1/0, F1/
5M1/4, F1/5M0/1) were measured using a Fibox4 dissolved oxygen
instrument (Presens, Pvt. Ltd., Germany) the day after irrigation
every hour from 5 a.m. to 8 p.m.
2.4. Statistical analysis
The experimental data were analyzed using the Microsoft Excel
software. Statistical analysis were undertaken by the software SPSS
838 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843

Table 3
The specific irrigation scheme.

Cucumber Tomato

Seedling stage flowering stage fruiting stage Seedling stage flowering stage fruiting stage
3 2
m /667 m

Irrigation quota 8.8 8.0 13.3 5.8 4.1 9.4

Irrigation amount 35.4 31.9 132.7 29.2 24.5 112.2

22.0 (Statistical Product and Service Solutions, IBM, USA) through
one-way analysis of variance (ANOVA), the least significant differ-
ence (LSD) analysis and general linear model regression analysis,
which depended on the p-value (Prob. > F) at the 95% confidence
interval. The p-value is the probability of seeing the observed F
value if the null hypothesis is true (there is no factor effect) (Verma
et al., 2015). In other words, the analysis for comparisons of treat-
ment means with p < 0.05.
3. Results and analysis
3.1. Effects of MNBWO on crops dry matter accumulation
The effects of MNBWO on crops dry matter accumulation are
shown in Table 4. The differences between the dry matter accu-
mulation and the root-shoot ratios of tomato and cucumber using
the MNBWO were statistically significant. Compared to the control
treatment, oxygation could significantly improve the amount of dry
matter accumulation of cucumber and tomato. The tomato dry root
weight in M1/0 and M1/4 were 29.2%e67.5% and 14.9%e38.8% higher
than that in M0/1, and those of cucumber were 80.8%e108.9% and
68.4%e85.0% higher, respectively. The dry matter accumulation
quantities and root-shoot ratios largely exhibited increasing trends
in the mixing ratio, whereas the root dry weights and of cucumber
and tomato reached their maximum values in CM1/0F1/5 and TM1/
0F1/5, so were the stem and leaves dry weights.
Under the same mixing ratio, comparing to F1/3, the oxygation
frequency of F1/5 and F1/7 showed advantages in tomato dry matter
accumulation. Under the M1/0 mixing ratio, the root dry weights of
F1/5 and F1/7 increased by 47.1% and 32.5% compared with that of F1/
3. In the case of cucumber, the root dry weight of F1/5 was higher
than those of F1/3 and F1/7, so were the dry weights of stem and
leaves. The root dry weight of F1/5 was increased by 3.4%e12.9% and
4.3%e21.1% than that of F1/3 and F1/7. The interaction of mixing ratio
and oxygation frequency had a significant effect on the root-shoot
ratios of tomato and cucumber, the dry weight of stem and leaves of
cucumber and the root dry weight of tomato.
3.2. Effects of MNBWO on crops yield and IWUE
The effects of MNBWO on the yields and IWUEs of tomato and
cucumber are shown in Table 5. The trend of IWUE was the same as
that of the yield, this was mainly because the indoor experiment
was conducted in green house without rainfall, and the irrigation
quota for each treatment was equal. Besides, the soil conditions
(texture, structure, etc.), groundwater level and the weather con-
ditions (solar radiation, temperature, sunshine, wind speed, hu-
midity, etc.) of each treatment were basically same, so the soil
water content and evaporation of different treatments were
approximately equal. Therefore, the difference of IWUE was due to
the difference of final yields. and the yield was exemplified to
analyze the effects of MNBWO.
The tomato yield increased significantly under MNBWO
compared to the results of control group. Under the oxygation
frequency of F1/3, generally, tomato yield increased with the mixing
ratio increaced. The tomato yields of M1/0 and M1/4 were 11.3% and
4.0% higher than that of M0/1, and their differences reached the
significant level. When the irrigation frequency was F1/5, the to-
mato yield of M1/4 was significantly higher than those of M1/0 and
M0/1, by 6.2% and 16.9%, respectively. Under the F1/7 oxygation
frequency, the average yield of the tomato in spring and autumn
was 61.5 t/hm2, which was obtained in TM1/0F1/5. Similar trend was
observed in the cucumber treatments. When the oxygation fre-
quency was F1/5, the yields of M1/0 and M1/4 were 22.1% and 8.4%
higher than that of M0/1. Under the oxygation frequency of F1/7, the
cucumber yields of M1/4 and M0/1 were almost the same, whereas

Table 4
Effects of MNBWO on the dry matter accumulation of crops.

Crop Tomato Cucumber

stems and leaves root root-shoot ratio stems and leaves root root-shoot ratio

Treatments g g % g g %

M1/0F1/3 96.6 ab ± 1.9 14.2c±1.3 14.7cd ± 1.0 50.3b ± 1.2 1.5 ab ± 0.1 2.9b ± 0.2
M1/4F1/3 95.7 ab ± 1.3 12.3cd ± 1.5 12.9d ± 1.3 37.2d ± 1.5 1.5 ab ± 0.2 4.0a±0.5
M0/1F1/3 83.7b ± 4.0 10.7d ± 2.0 12.8d ± 1.8 38.7d ± 0.4 0.8c±0.1 2.1c±0.2
M1/0F1/5 106.3a±4.5 20.9a±2.4 19.6a±1.5 55.5a±1.6 1.6a±0.1 3.0b ± 0.1
M1/4F1/5 102.1 ab ± 5.6 16.8bc±0.9 16.4bc±0.1 44.5c±1.4 1.5a±0.1 3.4 ab ± 0.4
M0/1F1/5 92.3b ± 3.7 12.5cd ± 2.4 13.8d ± 0.6 30.8e±4.3 0.8c±0.1 2.7b ± 0.2
M1/0F1/7 91.7b ± 10.4 16.1bc±0.5 17.8b ± 0.4 42.27c±1.3 1.6 ± 0.2 3.7a±0.4
M1/4F1/7 93.6b ± 5.5 17.3b ± 1.5 18.5 ab ± 0.5 33.3e±1.9 1.3b ± 0.2 3.8a±0.4
M0/1F1/7 79.9b ± 8.4 12.5cd ± 1.1 15.7c±1.2 31.6e±1.4 0.8c±0.1 2.4bc±0.4

F-value

M 7.6* 24.1* 23.1* 152.8* 86.6* 33.4*

F 5.4* 16.4* 36.6* 41.3* 2.6ns 2.0ns
MF 0.1ns 3.4* 5.5* 17.0* 1.4ns 3.6*

Note: After the same column data, different letters indicate the difference significance level; * indicate the difference in the level of p < 0.05 is significant, ns indicate the
difference is not significant (p > 0.05).
 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843 839

Table 5
Effects of MNBWO on yield and WUE of cucumber and tomato.

Crop Tomato Cucumber

Spring Autumn Spring Autumn

Treatments Yield WUE Yield WUE Yield WUE Yield WUE

t/hm2 kg/m3 t/hm2 kg/m3 t/hm2 kg/m3 t/hm2 kg/m3

M1/0F1/3 63.7b ± 2.9 25.5b ± 1.2 45.9b ± 3.2 20.9b ± 1.5 75.2b ± 1.2 25.1b ± 0.4 82.2a±2.2 27.4a±0.7
M1/4F1/3 61.3b ± 1.4 24.5b ± 0.6b 41.8bc±1.6 19.0bc±0.7 72.3cd ± 4.3 25.0cd ± 1.5 84.7a±3.4 28.2a±1.1
M0/1F1/3 59.9c±3.1 24.0bc±1.2 39.5bc±3.6 18.0c±1.6 66.2d ± 3.2 22.1d ± 1.1 76.3b ± 4.1 25.4b ± 1.4
M1/0F1/5 65.1 ab ± 1.9 26.0 ab ± 0.8 50.8a±3.1 23.1a±1.4 90.1a±3.6 30.0a±1.2 86.1a±2.1 28.7a±0.7
M1/4F1/5 68.4a±2.9 27.4a±1.2 54.5a±1.6 24.8a±0.7 76.0c±4.0 25.3c±1.3 80.7 ab ± 0.7 26.9 ab ± 0.2
M0/1F1/5 61.4b ± 1.1 24.6b ± 0.4 44.6b ± 2.7 20.3b ± 1.2 71.0cd ± 5.3 23.7cd ± 1.8 73.4bc±2.4 24.5bc±0.8
M1/0F1/7 57.0c±3.5 22.8c±1.4 42.1bc±3.5 19.1bc±1.6 85.0b ± 6.6 28.3b ± 2.2 77.6 ab ± 4.2 25.9 ab ± 1.4
M1/4F1/7 54.2c±3.5 21.7c±1.0 38.1c±3.5 17.3c±1.6 72.9c±5.4 24.3c±1.8 67.2c±2.6 22.4c±0.9
M0/1F1/7 48.2d ± 3.6 19.3d ± 1.4 38.1c±2.6 17.3c±1.2 74.3cd ± 2.5 24.8cd ± 0.8 69.0bc±3.3 23.0bc±1.1

F-value

M 56.5* 56.5* 11.0* 11.0* 65.6* 65.6* 40.6* 40.7*

F 13.3* 13.3* 39.7* 39.7* 6.5* 6.5* 39.6* 39.6*
MF 2.5ns 2.5ns 3.7* 3.7* 1.5ns 1.5ns 3.4* 3.4*

Note: After the same column data, different letters indicate the difference significance level; * indicate the difference in the level of p < 0.05 is significant, ns indicate the
difference is not significant (p > 0.05).

the yield of M1/0 was 13.5% and 16.0% higher, respectively. The cucumber increased by 6.6%e39.2% and 12.3%e63.8%, under
maximum cucumber yield of 88.1 t/hm2 appeared in CM1/0F1/5. MNBWO. The soluble sugar contents in M1/4 were higher than those
The effects of the oxygation frequency on the yields of tomato of M1/0 and M0/1, except for the oxygation frequency of F1/3, for
and cucumber were statistically significant. When the mixing ratio which no consistency between oxygation frequency and soluble
was M1/0, the cucumber yield of F1/5 was 12.3% and 8.5% higher than sugar was observed. The maximum soluble sugar contents of to-
that in F1/3 and F1/7. When the mixing ratio was M1/4, F1/5 was more mato and cucumber obtained in TM1/4F1/3 and CM1/4F1/5. The
favorable on cucumber yield increasing than F1/7, with an increase titratable acidity contents of tomato and cucumber decreased by
of 12.1%. In the case of tomato plantation, F1/5 led to a higher tomato 7.7%e21.5% and 8.8%e13.6% under MNBWO. As the mixing ratio
yield than F1/7 and F1/3, increasing by 6.4%e34.7%. There was no increased, the titratable acidity contents in both tomato and cu-
significant effect on the crop yield of the interaction of the mixing cumber exhibited a downward trend; the differences were signif-
ratio and the oxygation frequency, neither was IWUE. icant, except for F1/5, for which no consistency in the oxygation
frequency and titratable acidity was detecded. The minimum
titratable acidity in tomato and cucumber occurred in TM1/0F1/7 and
3.3. Effects of MNBWO on crops flavor indices CM1/0F1/3, respectively. The fruit hardness of cucumber decreased
by 4.1%e13.0% under MNBWO. As the mixing ratio increased, the
The influences of MNBWO on the flavor indices of tomato and fruit hardness of cucumber decreased continually and reached a
cucumber are presented in Table 6. MNBWO had a considerable minimum in CM1/0F1/7.
impact on the flavor indices of cumber and tomato. Compared with At the meantime, the oxygation frequency had a considerable
the control group, the soluble sugar contents of tomato and impact on the flavor indices of tomato and cucumber. When the
mixing ratios were M1/0 and M1/4, the soluble sugar contents of
tomato increased by 11.0%e30.0%. Under the mixing ratio of M0/1,
Table 6a
the soluble sugar contents of tomato in spring and autumn did not
Effects of MNBWO on flavor indices of tomato.
show consistent trend with oxygation frequency. Under the mixing
Treatments Tomato ratio of M1/4, the soluble sugar contents of cucumber in F1/5
Spring Autumn increased by 25.7% and 27.0% than those of F1/3 and F1/7. The
Soluble sugar Titratable acid Soluble sugar Titratable acid titratable acidity contents of tomato under F1/7 was 8.8%e18.7%
lower than that of F1/3 and F1/5. The fruit hardness or titratable
g/kg
acidity of cucumber exhibited no consistency with increasing
M1/0F1/3 49.7 1.8f±0.02 47.6 4.0b ± 0.2 oxygation frequency. The interaction of oxygen ratio and oxygation
M1/4F1/3 58.1 1.8ef±0.05 51.7 4.7a±0.2
frequency had a significant effect on the titratable acidity of both
M0/1F1/3 46.6 2.4b ± 0.05 36.0 4.9a±0.5
M1/0F1/5 41.9 2.2d ± 0.01 46.0 4.0b ± 0.3 crops.
M1/4F1/5 46.1 2.3c±0.01 47.0 3.7b ± 0.2
M0/1F1/5 29.5 2.5a±0.01 38.4 4.7a±0.2
M1/0F1/7 35.5 1.7g ± 0.00 39.6 3.5b ± 0.2
3.4. Effects of MNBWO on crops nutrition quality
M1/4F1/7 43.3 1.8ef±0.00 45.8 3.6b ± 0.3
M0/1F1/7 41.2 1.8f±0.02 31.2 4.3b ± 0.2 The influences of MNBWO on the tomato and cucumber nutri-
F-value tion quality are presented in Table 7. Compared with the control
treatment, the vitamin C contents of tomato and cucumber under
M e 361.5* e 6.9*
F e 83.1* e 14.9* oxygation frequency of F1/3 and F1/5 were 6.0%e19.1% and 10.2%e
MF 15.6* 7.4* 40.9% higher, with the difference being significant. Under the fre-
Note: After the same column data, different letters indicate the difference signifi-
quencies of F1/3 and F1/5, vitamin C of M1/4 were significantly higher
cance level; * indicate the difference in the level of p < 0.05 is significant, ns indicate than those of M1/0 and M0/1. Under the frequency of F1/7, vitamin C
the difference is not significant (p > 0.05). of M1/0 was higher than M1/4 and M1/7. The vitamin C contents of
840 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843

Table 6b
Effects of MNBWO on flavor indices index of cucumber.

Cucumber

Treatments Spring Autumn Autumn

Soluble sugar Titratable acid Soluble sugar Titratable acid Hardness

g/kg Kpa/m2

M1/0F1/3 5.8 1.3f±0.03f 8.0 1.1d ± 0.03 10.1c±0.3

M1/4F1/3 6.0 1.3e±0.05 7.5 1.2e±0.05 11.1b ± 0.4
M0/1F1/3 4.3 1.4a±0.02 7.0 1.3c±0.02 10.7b ± 0.2
M1/0F1/5 5.2 1.3e±0.02 7.3 1.3d ± 0.02 10.7b ± 0.3
M1/4F1/5 7.0 1.3de ± 0.01 10.1 1.3d ± 0.01 11.1b ± 0.3
M0/1F1/5 4.7 1.4c±0.02 5.6 1.5b ± 0.02 12.3a±0.4
M1/0F1/7 5.5 1.3e±0.01 6.4 1.3f±0.01 9.4c±0.3
M1/4F1/7 6.7 1.3e±0.01 6.8 1.5bc±0.01 9.4d ± 0.6
M0/1F1/7 4.6 1.5b ± 0.02 6.0 1.6a±0.02 10.3a±0.2

F-value

M e 340.8* e 332.0* 77.2*

F e 13.4* e 14.0* 27.5*
MF 13.6* 89.6* 24.8*

Note: After the same column data, different letters indicate the difference significance level; * indicate the difference in the level of p < 0.05 is significant, ns indicate the
difference is not significant (p > 0.05).

Table 7a
Effects of MNBWO on nutritional index of tomato.

Tomato

Treatments Spring Autumn

Vitamin C Soluble solids Lycopene Vitamin C Soluble solids Lycopene

mg/kg % mg/kg mg/kg % mg/kg

M1/0F1/3 9.0d ± 0.1 5.5a±0.3 80.1b ± 2.9 11.3bc±0.1 5.5a±0.1 53.3b ± 1.9
M1/4F1/3 10.7 ab ± 0.5 5.5a±0.3 81.3b ± 2.0 12.0 ab ± 0.9 5.5a±0.1 50.9b ± 1.3
M0/1F1/3 8.5d ± 0.3 4.9d ± 0.2 47.3c±2.0 10.7c±0.3 5.4d ± 0.2 38.5c±1.6
M1/0F1/5 11.3a±0.1 5.1b ± 0.1 92.1a±0.6 12.2a±0.1 5.1c±0.2 61.9a±0.5
M1/4F1/5 11.5a±0.3 5.0c±0.3 93.0a±2.2 12.3a±0.4 5.1cd ± 0.2 56.0 ab ± 1.2
M0/1F1/5 11.0b ± 0.2 4.4e±0.2 48.3c±1.4 9.4d ± 0.4 5.0e±0.2 37.2c±1.5
M1/0F1/7 11.0b ± 0.2 4.9cd ± 0.4 90.3a±2.6 11.5b ± 0.4 4.9d ± 0.2 55.8 ab ± 0.8
M1/4F1/7 10.6c±0.1 5.4a±0.2 91.9a±1.6 10.0cd ± 0.4 4.9a±0.1 59.0a±1.1
M0/1F1/7 10.8bc±0.1 4.6d ± 0.4 47.2c±1.3 9.8d ± 0.1 4.4b ± 0.4 33.4c±0.9

F-value

M 54.3* 31.5* 125.7* 45.7* 162.2* 27.5*

F 5.9* 5.4* 46.0* 13.6* 65.0* 4.8*
MF 0.5ns 1.0ns 10.0* 11.8* 10.1* 0.6ns

Note: After the same column data, different letters indicate the difference significance level; * indicate the difference in the level of p < 0.05 is significant, ns indicate the
difference is not significant (p > 0.05).

tomato and cucumber reached maximum values under TM1/4F1/5
and CM1/4F1/3, respectively. The soluble solid contents of tomato
and cucumber under MNBWO were 7.0%e14.4% and 3.7%e8.5%
higher than that of the control treatment. There was no significant
difference between the soluble solid of tomato in M1/0 and M1/4,
both of which were significantly higher than that of M0/1. There was
no noticeable difference between the soluble solid of cucumber in
M1/4 and M0/1, whereas that under M1/0 was significantly higher
than the other two mixing ratios. The soluble solid of tomato and
cucumber reached their maximum values in the M1/0F1/3 treatment.
The contents of lycopene under MNBWO were 52.0%e85.8% higher
than that of the control treatment, with the maximum value
occurring in TM1/4F1/5. There were no significant differences in the
lycopene contents of M1/0 and M1/4 with increases in the mixing
ratio, with both exhibiting significantly higher values than under
M0/1.
The effects of the oxygation frequency on the nutritional index
of tomato and cucumber were statistically significant. The vitamin
C of tomato under F1/5 was 4.8% and 15.5% higher than that of F1/3
and F1/7. The vitamin C contents of cucumber increased continu-
ously with increasing oxygation frequency, and the vitamin C of F1/3
was 4.4%e40.9% higher than those of F1/5 and F1/7;while the soluble
solid of tomato in F1/3 was 7.0%e14.6% higher than those of F1/5 and
F1/7. Under the ratio of M1/0, the soluble solid of cucumber increased
continually with increasing oxygation frequency, by 1.8%e7.2%,
whereas no consistent pattern was observed under the other oxy-
gation treatments. There was no consistent pattern in the lycopene
content with changes in irrigation frequency. The interaction of
oxygen ratio and oxygation frequency had a significant effect on the
titratable acidity contents of tomato and cucumber.
4. Discussion
How to guarantee agricultural water in food security is a global
problem (Sun et al., 2016), as is collaboratively improving IWUE and
crop yield (Sezen et al., 2007; Kumar and Dey, 2011). However, as
the economy and society continue to advance, the demands for
high-quality fruits and vegetables are increasing. The emphasis of
 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843 841

Table 7b
Effects of MNBWO on nutritional index cucumber.

Cucumber

Treatments Spring Autumn

Vitamin C Soluble solids Soluble solids

mg/kg % %

M1/0F1/3 6.9a±0.1 3.2b ± 0.1 4.5a±0.1

M1/4F1/3 7.0a±0.1 3.1a±0.1 4.2b ± 0.1
M0/1F1/3 4.9c±0.1 2.9c±0.2 4.2b ± 0.2
M1/0F1/5 6.0b ± 0.2 3.1c±0.1 4.1b ± 0.4
M1/4F1/5 6.3b ± 0.3 3.0c±0.1 3.5d ± 0.2
M0/1F1/5 4.7c±0.1 3.0c±0.1 3.6d ± 0.2
M1/0F1/7 5.8a±0.4 3.1bc±0.2 4.1bc±0.1
M1/4F1/7 4.98c±0.3 3.10bc±0.1 3.9c±0.3
M0/1F1/7 4.00d ± 0.2 2.90c±0.1 3.7d ± 0.2

F-value
M 207.2* 16.6* 28.9*
F 46.9* 12.4* 51.7*
MF 22.2* 8.5* 4.1*
Notes: 1. After the same column data, different letters indicate the difference sig-
nificance level; * indicate the difference in the level of p < 0.05 is significant, ns
indicate the difference is not significant (p > 0.05).
2. The Vitamin C content of cucumber in autumn was not tested due to improper
storage.
fruit consumption has been shifted from quantity to quality (Dorais
et al., 2001; Rajkumar et al., 2012). Therefore, how to conserve
water, increase production and improve fruit quality has become an
urgent need of agricultural irrigation.
4.1. MNBWO increases crops yield and IWUE
The experiment, using a mobile MNB generator for tomato and
cucumber MNBWO, found that the technology had significantly
improved the dry matter accumulation quantities, yields and
IWUEs of tomato and cucumber. And the dry matters and yields of
tomato were increased by 29.2%e67.5% and 7.8%e26.9%, respec-
tively, with MNBWO. Whereas those of cucumber increased by
80.8%e108.9% and 2.3%e16.3%. There were three main reasons for
these results as follows.
Firstly, oxygation can improve the soil oxygen content in the
crop root zone. Oxygen drives the synthesis of adenosine triphos-
phate and triphosphopyridine nucleotide and the reduction force
required for cell growth, which constitutes the core of the meta-
bolism of the whole plant. In other words, oxygen is essential for
the normal growth and development of plants (Sun et al., 2006). In
the present experiment, the oxygen content of the soil was deter-
mined in different mixing ratios, and the results are shown in Fig. 3.
Compared with general SDI, MNBWO can improve the soil oxygen
content in crop root zone, what's more, the soil oxygen content was
relatively stable within 24 h after oxygation, which can promote
root aerobic respiration thus increasing the amount of nutrients
transported to the canopy (Sey et al., 2010). A previous study
showed that oxygation can increase crop yield and WUE while
increasing the leaf photosynthesis rate (Bhattarai, 2005).
Secondly, oxygation can affect enzyme activities such as urease,
catalase, etc. in the soil and improve the soil microhabitat (Morard
and Silvestre, 1996). As one of the most active organic components
of soils, soil enzymes can be used not only to characterize the en-
ergy metabolism of soil matter, but also an important biological
index to evaluate soil fertility levels and the ecological environment
(Dong et al., 2009; Marx et al., 2001). For example, catalase is an
intracellular enzyme found in all aerobic bacteria and most facul-
tative anaerobes, but absent from obligate anaerobes (Alef and
Fig. 3. Soil oxygen content under different oxygation ratio. Note: CM1/0F1/5 stands for
the treatments which the mixing ratio of micro-nano bubble water to groundwater is
1:0 and the irrigation frequency is once in five days. CM1/4F1/5 and CM1/4F1/5 and so
forth.
Nannipieri, 1995). Catalase activity in soils is considered an indi-
cator of aerobic microbial activity and has been related to both the
number of aerobic microorganisms and soil fertility (Garcia and
Hernandez, 1997). Improvement on soil permeability increases
soil catalase activity (Li et al., 2016d) and the increasing of soil
catalase content can acceleratory promote the breakdown of
hydrogen peroxide into water and oxygen, thus reducing the
toxicity of hydrogen peroxide to crops. In addition, this enzyme is
also closely related to soil respiration intensity and microorganism
activities and is an important enzyme in the evaluation of soil
fertility (Trasarcepeda et al., 1999).
Thirdly, MNBs can promote the biological activities of plants and
animals. Studies have shown that under the same dissolved oxygen
conditions, the growth rate and dry matter accumulation of lettuce
in MNBs cultivation solution were greater than those excluding
MNBs (Ago et al., 2005; Pates, 2009; Ushikubo et al., 2010).
4.2. MNBWO increases crops flavor and nutrition quality
The results indicated that MNBWO could significantly improve
the fruit nutritional quality and flavor indices of crops. The vitamin
C and soluble sugar contents of tomato increased by 30.9% and
28.3%, and those of cucumber increased by 40.9% and 20.8%. The
lycopene content of tomato increased by 76.8%. These differences
may mainly result from the two following reasons.
Firstly, the rupture speed of MNBs in water is slow, and the
retention time significantly increased comparing to big bubbles
(Takahashi et al., 2007; Yang et al., 2012). According to the buoy-
ancy principle, the larger the bubble volume, the more buoyancy
will be received and the rising speed will be accelerated (Deng
et al., 2014). MNBs are small in diameter and rise very slowly. In
addition, as MNBs rise in water, they are also affected by the
movement of water molecules, so compared with large bubbles,
they appear to rise in a curve (Liu et al., 2017).
Secondly, MNBs have strong mass transfer ability since that the
specific surface area of gas and liquid determining the mass transfer
capacity of the air is inversely proportional to the diameter of air
bubbles in water. This is because that MNBs have small diameter, so
the gas mass transfer rate is very high (Li et al., 2013). Furthermore,
MNBs are stable in nature and high in oxygen content for crop
absorption (Attard et al., 2002; Yang, 2002). It may also be caused
by the special boundary propagation property of the MNBs (Li et al.,
2013), which make them easily attach to the crops roots and change
the root surface adsorption characteristics, improving nutrient
842 Y. Liu et al. / Journal of Cleaner Production 222 (2019) 835e843
absorption. This issue needs to be investigated further.
4.3. Effects of mixing ratios on crops yield and quality
Several studies have proven that oxygation can improve crop
yield and WUE (Bhattarai, 2005; Arvidsson, 1999; Niu and Guo,
2010), but limited studies focused on the effects of different mix-
ing ratios on crop yield and fruit quality. Three different mixing
ratios were designed to investigate the effects on the yield and
quality of tomato and cucumber in present study. Under the oxy-
gation frequency of once every 5d, the cucumber yield increased
continuously with increasing mixing ratio which reached
maximum in M1/0, whereas that of tomato reached maximum in
M1/4. It was speculated that the oxygen sensitivities of tomato and
cucumber are different. The tomato is more sensitive to soil hu-
midity and low-oxygen-stress (Bradford and Yang, 1981). An aera-
tion experiment using air pump showed that the tomato root
activity was maximum at an oxygation coefficient of 0.8 and was
minimum at an oxygation coefficient of 1.6 (Jia et al., 2011). Thus, a
suitable mixing ratio can enhance tomato root activity, which is in
line with the present results. Furthermore, cucumber has a longer
melon period and requires large amounts of water (Zou et al., 2005;
Zhou et al., 2012). In present experiment, the total irrigation
amount of cucumber was larger than that of tomato, and thus, the
demand for the oxygen content in the soil was larger. In terms of
fruit quality, the nutritional qualities of the fruits varied, with in-
creases in the mixing ratio under different oxygation frequencies.
Under the oxygation frequencies of once every 3d and once every
5d, the vitamin C contents of tomato and cucumber reached
maximum in M1/4. Under the oxygation frequency of once every 7d,
the vitamin C increased continually with increases in the mixing
ratio which reached maximum in M1/0. Under the frequency of once
every 7d, the irrigation water volume was slightly greater, thus, the
eliminated oxygen content was higher, and more oxygen was
needed to keep the soil oxygen content of the root zone at an
appropriate level. The fruit titratable acid and hardness values
decreased with increasing mixing ratio, which is consistent with
previous studies (Yan et al., 2017). Soluble sugar and lycopene
exhibited similar levels under the mixing ratios of 1:4 and 1:0, with
both being higher than that of the control treatment. This trend
may relate to the test set and the mixing ratio gradient. The dif-
ference of the total bubble amounts between the mixing ratios of
1:4 and 1:0 was large, and there may be a mixing ratio in this range
which has a greater role in promoting the fruit quality. The mech-
anism of fruit quality is more complex and must be investigated
further.
4.4. Effects of oxygation frequency on crops yield and quality
The yield, IWUE, soluble sugar and vitamin C of tomato all
reached their maximum vales in F1/5. The frequency of once every
3d may have led the surface soil to be in the wet state for a longer
time, resulting in more water loss by ineffective evaporation (Guo
et al., 2007). The oxygation frequency of once every 7d was
overly long. It may exceed the retention time of the MNBs in the
soil, causing some MNBs to escape from the soil. At the meanwhile,
studies have shown that MNBs moved to a distant areas in the
groundwater(Wan et al., 2001). Thus, the frequency of once every
7d may cause the MNBs to be transported to the soil depths with
the water that are beyond the shallow root system of cucumber and
tomato. Namely, the bubbles utilization of once every 7d was lower
than that of once every 5d; thus, the oxygation frequency of once
every 5d resulted in an adequate amount of moisture and oxygen
distribution to meet the absorption of water, fertilizer, oxygen re-
quirements of the crop root system, which improve the yield and
fruit quality of tomato and cucumber. The vitamin C value of cu-
cumber exhibited an increasing trend with increasing oxygation
frequency, because the fruit period of cucumber is longer than that
of tomato, requiring picking every day during the fruit period.
Therefore, the required frequency for cucumber oxygation was
higher.
5. Conclusions
MNBWO collaboratively improves the yield, IWUE and quality of
cucumber and tomato. In the optimal treatment, the yield, IWUE,
vitamin C, and soluble sugar of tomato increased by 16.9%, 16.9%,
17.7%, and 39.2%, while those values for cucumber were 22.1%,
22.1%, 16.7%, and 19.4%, respectively. The recommended mixing
ratio of oxygation was 1:4 and 1:0 for tomato and cucumber,
respectively; while the recommended oxygation frequency for
them was both once every 5d for with MNBWO.
Acknowledgements
The present study was financially supported by the National
Natural Science Foundation of China (51621061, 51709261), and
Beijing Agricultural Science and Technology Project (20170151).
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jclepro.2019.02.208.
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