Agricultural Water Management 168 (2016) 23–34

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Agricultural Water Management

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

A kinetic model for biofilm growth inside non-PC emitters under

reclaimed water drip irrigation
Bo Zhou a,b , Yunkai Li a,∗ , Peng Song a , Zhenci Xu c , Vincent Bralts b
a
College of Water Resources and Civil Engineering, China Agricultural University, Beijing 100083, China
b
Department of Agricultural and Biological Engineering, Purdue University, West Lafayette, IN 47907-2093, USA
c
Center for Systems Integration and Sustainability, Michigan State University, East Lansing, MI 48823-5243, USA

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

Article history: Emitter clogging is tightly related to the formation and growth of biofilms inside emitters applying
Received 5 August 2015 reclaimed water. In order to control emitter clogging and achieve highly efficient drip irrigation (DI)
Received in revised form 10 January 2016 system, understanding the kinetics of biofouling is important. In this paper, four types of non-pressure-
Accepted 11 January 2016
compensating (non-PC) flat emitters and five types of non-PC cylindrical emitters were selected for
Available online 3 February 2016
reclaimed water DI experiment, and the growing processes of biofilms components (Solid particles, SD;
Phospholipid fatty acid, PLFAs; Extracellular polymeric substances, EPS) inside emitter flow path were
Keywords:
tested. The results showed that the entire growing processes of biofilm SD, PLFAs and EPS could all be
Reclaimed water drip irrigation
Emitter
divided in proper order, i.e., growing adaptive period, rapid growing period and dynamic stable period. To
Biofilms be specific, biofilms were adapting to the growing environment in the initial 408 h, while their formation
Components velocity was relatively slow. It was followed by the rapid growing period when the system accumulatively
Growth kinetic model operated 408–1088 h. Then biofilm growth and detachment tended to reach dynamic balance till 1224 h.
Therefore, based on the prototype of Logistic growing model, the paper established a kinetic model of
biofilms growth (SD, PLFAs and EPS) after the comprehensive consideration of their growing response to
emitter types, flow path geometrical parameters and lateral positions. The model was verified to present
the biofilm growth process well (R2 > 0.85**, significant level a = 0.01). On the other hand, another model
was proposed to reflect the influential effects of biofilm components on emitter clogging degrees. When
combining these two models together, the results showed that the emitter clogging controlling meth-
ods should be carried out in the appropriate time in case of more serious emitter clogging. The control
point was the time when DI system operated 300 h accumulatively or before emitter clogging degree
reached 25%. The results in this paper could provide theoretical references to reveal DI emitter clogging
mechanism and to establish a controlling strategy against emitter clogging.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction
Reusing reclaimed water in agriculture has become one of the
most effective methods to alleviate water shortage worldwide, but
its complicated water quality brings potential risks to soil, crops,
environment and even human health (Qadir et al., 2007, 2010).
All these potential risks could be well controlled with drip irri-
gation (DI). This is because DI is quite controllable (Brenes and
Hills, 2001). However, it also brings higher risks to DI emitter clog-
∗ Corresponding author. Tel.: +86 10 62738485; fax: +86 10 62736203 15.
E-mail address: liyunkai@126.com (Y. Li).
ging, and makes clogging mechanism more complicated (Li et al.,
2012; Tarchitzky et al., 2013), as biofilms get involved with the
whole emitter clogging process (Yan et al., 2009; Zhou et al., 2013
Zhou et al., 2013). Therefore, describing the detailed biofilm growth
kinetic process is of vital importance to understand the emitter
clogging process.
Biofilms formation and growth processes are the comprehen-
sive reflections of multiple factors, including environmental factors
such as irrigation water quality (Nakayama and Bucks, 1991; Capra
and Scicolone, 2007), structural features such as emitter types
and flow path geometrical parameters (Li et al., 2006; Wu, 2006;
Zhou et al., 2013, 2014), hydraulic characteristics such as flow
velocity and water shear force (Percival et al., 2001; Beyenal and

http://dx.doi.org/10.1016/j.agwat.2016.01.007
0378-3774/© 2016 Elsevier B.V. All rights reserved.
24 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
Fig. 1. Layout of the drip irrigation experiment using reclaimed water.
Lewandowski, 2002; Markku et al., 2006; Li et al., 2012) and sys-
tem operational modes such as working pressure and irrigation
frequency (Duran-Ros et al., 2009; Elbana et al., 2012; Zhou et al.,
2015). Therefore, it is really difficult to maintain the effective
management of reclaimed water DI appropriately. In fact, for a
specific DI project, the controllable factors mainly include working
pressure, DI emitter types and their flow path geometrical param-
eters, which should be taken into serious consideration. Related
studies on biofilms attached inside DI emitters using reclaimed
water mainly focused on their difference under various treatments
till now, and merely limited samples were acquired to test their
dynamic growing characteristics. Yan et al. (2009) explored the
changing process of biofilm components attached inside emit-
ters applying reclaimed irrigation water. Souha et al. (2014)
qualitatively showed biofilms growing status inside DI emitters
using reclaimed water during different stages, through the results
acquired with Scanning Electron Microscope (SEM). Tarchitzky
et al. (2013) studied the increasing characteristics of total sus-
pended solids (TSS), total carbon (TC), calcium and magnesium ions
(Ca2+ + Mg2+ ) and total phosphorus (TP) of biofilms attached inside
reclaimed water DI system. Zhou et al. (2013) studied and analyzed
the differences of biofilms components (SD, PLFAs and EPS) among
eight types of emitters through reclaimed water DI experiment
in wastewater treatment plant. Oliver et al. (2014) demonstrated
the increasing trend of biofilm PLFAs in reclaimed water DI sys-
tem. However, merely one emitter sample was acquired to test
the biofilms inside emitters irrigated with reclaimed water in most
of these related studies, due to multiple experimental restrictions.
Therefore, this failed to reflect the randomness of biofilm formation
along DI laterals. Meanwhile, biofilm samples were taken at a low
frequency during the whole experiment, and could only show the
increasing trend of biofilm components as well as their differences
among different treatments. Overall, the results until now failed
to reflect the dynamic growing processes of biofilm components
accurately. Furthermore, there was no report of quantitative mod-
els of biofilm growth inside DI emitters using reclaimed water, and
all these issues mentioned above needed to be studied urgently, in
order to achieve highly-effective management of reclaimed water
DI.
Based on these, nine different types of non-PC emitters com-
monly used nowadays were chosen for a DI experiment that was
Table 1
Average water quality characteristics tested during the experiment.
CODcr (mg L−1 ) BOD5 (mg L−1 ) SS(mg L−1 ) NH4 + -N(mg L−1 )
17.94 ± 4.44 6.50 ± 2.06 6.05 ± 3.30 1.34 ± 1.13
TP(mg L−1 ) TN(mg L−1 ) pH Temperature(◦ C)
1.04 ± 0.47 9.63 ± 2.26 7.13 ± 0.07 21.16 ± 3.05
carried out in a wastewater treatment plant. This was then followed
by the proposition and validation of a kinetic model for biofilm
growth in emitters. The results acquired in this paper provided an
experimental reference to reveal the clogging mechanism.
2. Materials and methods
2.1. Reclaimed water DI and biofilm cultivation experiment inside
emitters
The experiment was carried out in the Beiqijia wastewater treat-
ment plant in Changping District, Beijing, China (N 40◦ 07 11 , E
116◦ 27 53 , + 33 m). In this plant, wastewater was treated with
Cyclic Activated Sludge System (CASS), and the reclaimed water
after secondary treatment was imported to the experimental DI
system. One 120-mesh screen filter and one 120-mesh disk filter
were placed in series as filtration treatment, and they were cleaned
once every three days. The working pressure as well as flow rates
was controlled mainly according to the shunt principle. The DI
system started from June 14th, 2013, with the constant working
pressure of 0.1 MPa adjusted every day before the experiment, and
operated 8 h every day (7:00 am–11:00 am, 2:00 pm–6:00 pm) till
November 14th, 2013, totaling 1224 h. The layout of the experiment
is shown in Fig. 1. During the experiment, reclaimed water quality
characteristics were tested and recorded by the online monitoring
system in the wastewater treatment plant at a fixed time every day,
and the average results are shown in Table 1.
Four types of flat emitters (marked as FE1-FE4) and five types of
cylindrical emitters (marked as CE1–CE5) were used in this experi-
ment. There were ten laterals for each emitter type; 12 m in length,
with the emitter spacing of 0.3 m. So emitters in each lateral were
numbered from No. 1 to No. 40 from the inlet to the outlet of the
 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34 25

Table 2
Drip irrigation emitters used in the experiment.

Emitters Rated outflow Flow path Flow coefficient Flow index Structure of Manufacturers
q (Lh-1 ) geometrical k x tested emitters
parameters (mm)
Length × Width × Depth

FE1 1.27 50.23 × 0.57 × 0.67 0.39 0.51 Plastro

FE2 1.01 48.20 × 0.50 × 0.64 0.15 0.83 Runtian, HEBEI

FE3 0.87 50.04 × 1.68 × 0.48 0.28 0.49 Netafim

FE4 1.51 50.15 × 1.10 × 0.78 0.32 0.67 Dayu, GANSU

CE1 1.81 142.35 × 1.27 × 0.99 0.55 0.52 Runtian, HEBEI

CE2 1.76 148.02 × 1.07 × 1.21 0.50 0.55 Shengyu, SHANDONG

CE3 1.93 352.39 × 1.30 × 1.02 0.58 0.52 Longda, HEBEI

CE4 3.02 152.23 × 2.40 × 0.75 1.02 0.47 Longda, HEBEI

CE5 3.32 152.23 × 2.40 × 1.01 1.03 0.51 Longda, HEBEI

lateral. The detailed structural parameters of emitters used in the
experiment are offered by the manufacturers and shown in Table 2.
2.2. Biofilm sampling and testing methods
During the experiment, emitter samples were cut out ten times
in total to test biofilm components, when the system operated for
240 h, 408 h, 600 h, 736 h, 832 h, 920 h, 1016 h, 1088 h, 1160 h and
1224 h, respectively; those were also the times when emitter clog-
ging degree reached approximately 10%, 20%, 30%, 40%, 50%, 60%,
70%, 80%, 90% and 100%, respectively. At each time of taking emitter
samples, one lateral of every type of non-PC emitter was chosen,
and they were removed from the whole system after sampling.
Whenever emitter samples were taken as mentioned above, the
outflow of emitters at the head part (No. 1–8), middle part (No.
17–24) and end part (No. 33–40) were tested, and then the emitter
outflows were modified in order to eliminate the effects of water
temperature as used by Pei et al. (2014), in order to obtain the exact
emitter clogging degree (CD). Five emitters were selected, which
were the closest to the targeted clogging degree, out of the eight
emitters tested at the head, middle and end part, respectively, as
the final samples prepared to test biofilm components.
A high precision electronic balance (accurate at 10−4 g) was used
to test the weights of each emitter sample immediately after the
samples were taken, in order to avoid the possible effects caused by
environmental changes on biofilm components, and then biofilms
were stripped by ultrasonic cleaning machine (model: KQ-600KDE;
manufacturer: Kunshan Shumei; working power: 600 kW; work-
ing temperature: 60 ◦ C). After the stoving process, biofilms were
weighted again and thus biofilm SD was acquired according to
the two weights of each emitter measured above. Meanwhile, five
emitter samples collected from the head, middle and end part of the
lateral in each treatment were stripped in the ultrasonic cleaning
machine, and the liquid samples were mixed together. The mixed
liquid samples were used to test EPS and PLFAs, respectively. The
mixture used for tests mention above eliminated the effects of ran-
domness of biofilm growth on the final result, in order to describe
the dynamic biofilm formation process as accurately as possible.
The detailed testing methods of EPS and PLFAs were described in
Zhou et al. (2013).
2.3. Growth kinetics model of biofilms components inside emitters
Based on the Logistic growing model, the growth kinetic model
of biofilms components (SD, EPS and PLFAs) was established after
the comprehensive consideration of their response to emitter
types, flow path geometrical parameters and lateral positions,
while neglecting the other influential factors (including water qual-
26 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
ity and temperature, microbial community, carrier characteristics,
working pressure, irrigation frequency, etc.), with the following
assumptions:
(1) The increase of biofilm components inside emitter flow path
per unit area (BIO) equals to the difference between its net growth
(BIOG ) and detachment (BIOD ); (2) The entire emitter flow path
is considered as a curve tube, and thus the biofilm growing back-
ground like nutrition supply and water flow characteristics are the
same among different structural units, and the ratio of BIOG on hor-
izontal surfaces to vertical surfaces is in direct proportion to RW/D
(RW/D = W/D, W and D are the width and depth of emitter flow
path, and 1/RW/D + 1 is defined as the emitter structural index);
(3) BIOG fits the accumulated operating time in traditional Logis-
tic growth model (Richards, 1959), and is in direct proportion to
the cross sectional mean flow rate (V) and emitter structural index
mentioned above, and the difference caused by lateral position
is represented by the maximum environmental accommodation
(BIOmax ); (4) BIOD is proportional to BIOG . Considering the biofilms
are unresponsive to hydraulic shear force () near the internal wall
of non-PC emitter flow path, the expulsion rate (KD ) is in direct
proportion to average water shear force before biofilms’ dispersion.
According to assumptions (2) and (3), BIOG is acquired as:
BIOmax V rapid growing period and the dynamic stable period. Besides,
BIOG = × a3 ×
1 + a1 × e−a2 ×T 1 + RW/D
According to assumption (4), BIOD is acquired as:
BIOD = K D × BIOG = a4 ×  × BIOG = a4 ×  × A × V 2 × BIOG
According to assumption (1), BIO is acquired as:
BIOmax v reached 117.67–613.56 g/m2 and 88.78–220.70 g/m2 at the end
BIO = BIOG− BIOD = × a3 ×
1 + a1 × e−a2 ×T 1 + RW/D
a3 − a5 ×  × A × V 2 v growing period, and biofilm SD in flat and cylindrical emitters
× (1 − a4 ×  × A × V 2 ) = ×
1 + a1 × e−a2 ×T 1 + RW/D
b1 × v − b2 ×  × A × V 3 BIOmax
× BIOmax = × (3)
1 + RW/D 1 + b3 × e−b4 ×T
In Eq. (1)–(3), BIO represents biofilm components inside emit-
ter flow path per unit area (g m−2 ); BIOG and BIOD represent
the net growth and detachment of biofilm components, respec-
tively (g m−2 ); BIOmax represents the maximum environmental
accommodation of biofilm components (g m−2 ); T represents the
accumulated operating time of reclaimed water DI system (h);
KD represents the biofilm expulsion rate;  represents the aver-
age water shear force near the internal wall of emitter flow path
(103 g m s−2 ), and it is approximately calculated by  = AV2 accord-
ing to momentum equation, among which  represents the DI water
density (g m−3 ), and A represents the cross sectional area of emitter
flow path (m2 ), and V represents the mean flow rate in cross section
under the working pressure of 0.1 MPa (m s−1 ); RW/D represents the
ratio of flow path width to depth; and a1 –a5 as well as b1 –b4 are all
fitting parameters of the model.
2.4. Path analysis of biofilm components on emitter clogging
degrees
Path analysis method is an important statistical method to study
the linear relations between multiple independent variables (x1 ,
x2 , . . ., xp ) and the responsive variable (y) (Bhatt, 1973; Li et al.,
2007). The correlation coefficients between independent variables
and the responsive variable are divided into direct impact and indi-
rect impact when using this method. Thus the relative importance
of each independent variable on the responsive variable and their
influential path are acquired.
In this paper, the path analysis method was used to study the
effects of biofilm components (SD, EPS and PLFAs) on emitter clog-
ging degree (CD). Meanwhile, multiple linear regression analysis
was carried out to eliminate the possible multicollinearity accord-
ing to Variance Inflation Factor (VIF). Thus how biofilm components
affect emitter clogging process was analyzed.
3. Results and analysis
3.1. Dynamic growing process of biofilm SD inside emitters
The dynamic growing process of biofilm SD per unit area inside
nine types of non-PC emitters at the head, middle and end parts of
the DI laterals are shown in Fig. 2, and the fitting results and statis-
tical results when applying the growth kinetic model established
in this paper are shown in Table 3.
As seen from Fig. 2 and Table 3, biofilm SD inside nine
types of non-PC emitters increased in “S shape” pattern with
the accumulated operation of the DI system. The biofouling pro-
cess was divided in order as the growing adaptive period, the
(1)
the demarcation points of these stages were consistent among
different types of emitters. For the first 408 h of the operation,
biofilms inside different types of emitters were in growing adap-
(2) tive period, and biofilm SD increased relatively slowly. In contrast,
biofilm SD in flat emitters increased quicker than those in cylin-
drical emitters, and biofilm SD in flat and cylindrical emitters
of the period, among which the maximum SD were found in
FE2 and CE2. Then the biofilms inside emitters entered the rapid
grew to 997.66–2467.95 g/m2 and 449.22–981.87 g/m2 , respec-
tively, till 1088 h, while the maximum SD was still found in FE2
and CE2. After this stage, biofilm SD tended to be in a dynamic
stable status, as they increased quite slowly or even decreased
slightly. At the end of the experiment, with the operation of
1224 h in total, biofilm SD in flat and cylindrical emitters were
1088.11–2318.03 g/m2 and 488.79–972.42 g/m2 , respectively, and
they ranked in the order as SDFE2 > SDFE1 > SDFE4 > SDFE3 and
SDCE2 > SDCE1 > SDCE4 > SDCE5 > SDCE3 . Still FE2 and CE2 showed the
highest biofilm SD, while FE3 and CE3 were found to be the lowest.
Although the entire growing process of biofilm SD inside emit-
ters at the head, middle and end parts of the lateral all fitted the
model established in this paper, as well as the similar growing trend
and same demarcation points for different periods, lateral position
showed significant impact on biofilm SD, resulting in the order of
SDHead < SDMiddle < SDEnd . According to the fitting parameters of the
model shown in Table 3, b1 and b2 showed no obvious regular-
ity with lateral position, while b3 decreased from the head to the
middle to the end part of the lateral, and b4 was on the contrary
increasing.
According to the statistical results, the growth kinetics model
established in this paper could describe the dynamic growing pro-
cess of biofilm SD well (R2 > 0.95**, significant level a = 0.01). The
mean bias error (MBE), mean absolute error (MAE), root-mean-
square error (RMSE) and residual sum of squares (SSE) varied
obviously among different types of emitter treatment, although
the statistical analysis indexes ranked as MBE < MAE < RMSE < SSE
among all treatments. On the other hand, MBE, MAE, RMSE and SSE
were all larger in flat emitters than those in cylindrical emitters,
and they increased from the head to the middle to the end part
of the lateral in all types of emitter treatments. The largest values
were found in FE2 and CE3, respectively.
 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34 27

Table 3
Fitting parameters of growth kinetic model of biofilms SD inside emitters.

Lateral position Emitters b1 b2 b3 b4 Correlation Mean Mean Root-mean- Residual

coefficient (r) bias absolute square sum
error error error (RMSE) of
(MBE) (MAE) squares
(SSE)

Head FE1 3.431 0.477 36.407 0.0037 0.99** 5.731 47.906 59.05 38361.79
FE2 3.014 0.637 57.534 0.0048 0.99** 2.736 51.846 64.49 45741.82
FE3 3.093 0.162 75.509 0.0057 0.99** −0.469 15.717 20.03 4412.61
FE4 5.808 −1.189 22.318 0.0037 0.99** 4.813 29.169 33.93 12666.43
CE1 5.182 −1.194 35.677 0.0042 0.99** 1.675 17.504 19.94 4372.64
CE2 6.196 −0.343 51.118 0.0048 0.99** −0.477 20.015 23.92 6291.22
CE3 8.553 −1.115 12.858 0.0026 0.97** 1.632 22.962 32.63 11714.82
CE4 7.708 −3.190 59.339 0.0050 0.98** −0.528 13.572 16.34 2936.31
CE5 7.737 −2.565 25.050 0.0044 0.99** 1.505 11.265 13.91 2127.37
Middle FE1 2.729 0.072 36.302 0.0046 0.99** 2.160 40.917 57.82 36776.02
FE2 2.709 0.101 51.690 0.0053 0.99** −4.428 75.896 85.68 80746.44
FE3 3.124 0.256 67.404 0.0058 0.99** −2.529 18.199 26.20 7546.68
FE4 5.761 −1.684 22.746 0.0038 0.99** 4.524 51.117 59.25 38614.91
CE1 5.472 −0.467 31.268 0.0044 0.99** 1.744 14.400 17.88 3518.44
CE2 6.027 −1.119 40.122 0.0049 0.99** −0.044 25.202 30.08 9955.80
CE3 7.434 −4.621 11.970 0.0027 0.95** 1.636 23.872 33.45 12310.86
CE4 7.505 −3.554 43.768 0.0051 0.99** 0.340 13.606 16.52 3000.54
CE5 8.212 −1.103 23.556 0.0045 0.99** 1.327 12.690 16.53 3004.06
End FE1 2.304 −0.675 34.896 0.0054 0.99** −4.596 75.890 92.68 94486.54
FE2 3.083 2.154 46.537 0.0056 0.98** −10.655 138.279 148.73 243338.95
FE3 4.048 4.276 59.603 0.0059 0.99** −4.369 38.298 46.19 23468.69
FE4 6.210 0.572 21.067 0.0039 0.98** 3.211 74.635 92.86 94842.28
CE1 5.490 −0.874 28.530 0.0046 0.99** 1.677 19.300 22.83 5732.30
CE2 5.783 −2.002 33.994 0.0049 0.98** 0.508 37.660 44.69 21971.08
CE3 8.154 −0.046 11.287 0.0027 0.97** 1.648 25.555 34.19 12860.30
CE4 7.972 −1.196 36.173 0.0053 0.99** 1.025 18.780 23.08 5861.36
CE5 8.610 0.030 22.294 0.0045 0.99** 1.189 20.317 25.20 6987.26

Note: In the table, ** means “significant” under significant level a = 0.01.

Table 4
Fitting parameters of growth kinetic model of biofilms PLFAs inside emitters.

Lateral position Emitters b1 b2 b3 b4 Correlation Mean Mean Root- Residual

coefficient (r) bias absolute mean- sum
error error square of
(MBE) (MAE) error (RMSE) squares
(SSE)

Head FE1 3.372 0.027 40.083 0.0044 0.98** 0 0.035 0.04 0.02
FE2 2.932 0.233 72.447 0.0049 0.99** 0.002 0.023 0.03 0.01
FE3 6.046 −0.916 30.254 0.0030 0.98** 0.004 0.027 0.03 0.01
FE4 2.801 0.127 68.104 0.0050 0.99** 0.003 0.036 0.04 0.02
CE1 5.330 −1.228 42.941 0.0048 0.99** 0 0.014 0.02 0.01
CE2 7.411 −0.352 40.571 0.0036 0.99** 0.001 0.011 0.01 0
CE3 10.857 0.529 18.045 0.0025 0.97** 0.001 0.017 0.02 0.01
CE4 8.575 0.699 32.369 0.0042 0.98** 0 0.015 0.02 0.01
CE5 8.951 −0.009 46.569 0.0046 0.99** 0.001 0.006 0.01 0
Middle FE1 3.004 −1.362 36.392 0.0046 0.99** −0.003 0.053 0.06 0.04
FE2 2.609 −0.056 70.622 0.0059 0.99** −0.006 0.038 0.06 0.03
FE3 6.850 0.358 20.882 0.0033 0.99** 0.002 0.031 0.04 0.02
FE4 4.004 4.327 51.734 0.0053 0.99** 0.004 0.027 0.04 0.02
CE1 5.485 0.322 39.943 0.0049 0.98** 0 0.017 0.02 0.01
CE2 6.274 −0.876 31.406 0.0044 0.99** 0.001 0.009 0.01 0
CE3 8.562 −0.003 12.956 0.0027 0.97** 0.001 0.014 0.02 0.01
CE4 8.678 0.455 23.653 0.0045 0.99** 0.001 0.010 0.01 0
CE5 8.407 −0.111 43.502 0.0051 0.99** 0 0.009 0.01 0
End FE1 3.699 1.741 33.740 0.0047 0.98** −0.005 0.090 0.11 0.13
FE2 2.714 0.139 67.061 0.0059 0.98** −0.011 0.066 0.09 0.08
FE3 5.762 −1.182 20.364 0.0037 0.96** 0 0.054 0.07 0.06
FE4 3.520 3.240 41.968 0.0055 0.95** 0.005 0.088 0.11 0.12
CE1 6.109 3.733 38.294 0.0050 0.98** −0.001 0.027 0.03 0.01
CE2 5.708 −1.750 27.035 0.0051 0.99** 0 0.013 0.01 0
CE3 7.413 −0.639 10.667 0.0029 0.97** 0.001 0.018 0.02 0.01
CE4 8.312 −1.386 18.933 0.0049 0.99** 0.001 0.012 0.01 0
CE5 8.377 0.286 43.641 0.0056 0.98** −0.001 0.014 0.02 0.01

Note: In the table, ** means “significant” under significant level a = 0.01.

3.2. Dynamic growing process of biofilm PLFAs inside emitters parts of the DI laterals are shown in Fig. 3, and the fitting results and
statistical results when applying the growth kinetic model estab-
The dynamic growing process of biofilm PLFAs per unit area lished in this paper are shown in Table 4.
inside nine types of non-PC emitters at the head, middle and end
28 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
Fig. 2. Dynamic accumulation of biofilms SD per unit area inside emitter flow path.
According to the results shown in Fig. 3, biofilm PLFAs rep-
resented quite a similar growing process to SD, which was also
divided into growing adaptive period, rapid growing period and
dynamic stable period, respectively, with the same demarcation
point. In the initial 408 h of the system operation, the biofilm PLFAs
in different flat and cylindrical emitters increased with the average
rates of (8.1 ± 1.7) × 10−4 g/m2 h and (2.7 ± 0.3) × 10−4 g/m2 h, till
they reached 0.23–0.50 g/m2 and 0.05–0.18 g/m2 , respectively,
at the end of the period. After entering rapid growing period,
biofilm PLFAs increased rapidly, with much faster increasing rates
of (17.9 ± 1.3) × 10−4 g/m2 h and (4.4 ± 0.2) × 10−4 g/m2 h and
thus reached 1.17–2.01 g/m2 and 0.26–0.55 g/m2 after the system
operated for 1088 h in total. From then on, biofilm PLFAs showed
dynamic balancing characteristics with average increasing rates of
(7.9 ± 1.4) × 10−4 g/m2 h and (2.8 ± 0.6) × 10−4 g/m2 h, and merely
increased to 1.22–2.03 g/m2 and 0.29–0.60 g/m2 at the end of the
experiment. Meanwhile, PLFAsFE2 > PLFAsFE1 > PLFAsFE4 > PLFAsFE3
and PLFAsCE2 > PLFAsCE1 > PLFAsCE4 > PLFAsCE5 > PLFAsCE3 were
observed. Similar to biofilm SD, maximum PLFAs were also found
in FE2 and CE2.
On the other hand, the variation trend among biofilm PLFAs
inside emitters at different positions of the lateral also revealed
PLFAsHead < PLFAsMiddle < PLFAsEnd . Besides, b3 and b4 decreased
and increased from the head to the end part of the lateral, respec-
tively, while b1 and b2 still showed no regularity as lateral position
changed.
In conclusion, the entire growing process of biofilm PLFAs
inside emitters fitted well to the growth kinetics model established
(R2 > 0.92**, significant level a = 0.01, Table 4). Similar to those of SD,
four statistical analysis indexes all increased from the head to the
end part of the DI lateral. MBE, MAE, RMSE and SSE of the growth
model were also found to be larger in flat emitters. But their largest
values were different among various flat and cylindrical emitters
in different positions of the DI lateral.
 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
Fig. 3. Dynamic accumulation of biofilms PLFAs per unit area inside emitter flow path.
3.3. Dynamic growing process of biofilm EPS inside emitters
The dynamic growing process of biofilm EPS per unit area inside
nine types of non-PC emitters at the head, middle and end parts of
the DI lateral is shown in Fig. 4, and the fitting results and statistical
results when applying the growth kinetic model established in this
paper are shown in Table 5.
As seen from Fig. 4 and Table 5, the proposed kinetic model
showed relatively worse results for EPS (R2 > 0.85**, significant
level a = 0.01), when compared with those of SD and PLFAs. This
was mainly because the EPS was secreted by microorganisms
(quantified by PLFAs), and then the basis to attach solid particles
(quantified by SD) and microorganisms. Therefore the EPS were
secreted and consumed at the same time, and their dynamic process
represented a more fluctuated characteristic. However, their entire
growing trend was similar to those of SD and PLFAs with the same
three periods. For the initial 408 h, biofilm EPS increased slowly but
relatively faster in flat emitters than in cylindrical emitters. They
29
grew to 1.33–4.77 g/m2 and 0.14–0.72 g/m2 , respectively, at the end
of the period, with the maximum EPS showed in FE4 and CE2. Then
EPS began increasing rapidly. However, slightly different from SD
and PLFAs, the increasing trend of EPS was still observed in the third
period when the system operated for 1088–1224 h. At the end of the
experiment, biofilm EPS inside different types of flat and cylindrical
emitters were 4.62–10.20 g/m2 and 0.65–3.19 g/m2 , respectively,
and flat emitters ranked as EPSFE2 > EPSFE1 > EPSFE4 > EPSFE3 . For
cylindrical emitters, the maximum biofilm EPS was found inside
CE2 and the minimum was in CE3. However, the EPSCE1 , EPSCE4 and
EPSCE5 showed inconsistent order for emitters at different lateral
positions, without significant difference observed. Overall, biofilm
EPS still showed increasing trend from the head to the end part of
the lateral, but b1 –b4 all showed no obvious regularity with laterals
position.
On the other hand, the statistical analysis results showed similar
variation characteristics as those of SD and PLFAs. But no maximum
were found in the same type of emitters.
30 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
Fig. 4. Dynamic accumulation of biofilms EPS per unit area inside emitter flow path.
4. Discussions
DI emitter clogging using reclaimed water is tightly related to
the biofilm formation and growth inside emitters (Yan et al., 2009;
Li et al., 2012; Zhou et al., 2013). This is because the dynamic
biofilms growth process has significant impact on DI emitter clog-
ging. Therefore, detailed and precise biofilm formation process is
the basis of revealing emitter clogging mechanism, and thus estab-
lishing the accurate and effective emitter controlling methods.
Related studies reported till now had limited samples and relatively
low sampling frequency. This was mainly because of the exper-
iment restrictions and testing methods. Therefore, these results
failed to overcome the randomness of biofilm growth, and could
not represent the biofilms growth process quantitatively and accu-
rately.
In this paper, the growing process of biofilm components (SD,
EPS and PLFAs) inside nine types of non-PC emitters was stud-
ied, through reclaimed water DI experiment. The results showed
that the entire growing processes of biofilm SD, EPS and PLFAs
inside all emitters appear in the order as adaptive period, rapid
growing period and dynamic stable period. At the beginning of
the experiment, biofilm components increased relatively slow. This
was mainly because the solid particles, microorganisms, organic
matters etc. in the water source just started to attach to the emitter
flow path via the sticky EPS secreted by microorganisms. The initial
biofilm structure attached or captured other particles, microorgan-
isms to form the stable biofilm structure continuously. However,
the microorganisms and their excretive EPS in biofilms were both
at a low level, resulting in relatively weak attaching ability. Biofilms
mainly grew in the flow stagnation area because of the relatively
lower water flow velocity (Li et al., 2013). Overall, they were still
adapting to the environment in the emitter flow path, and the
high water shear force led to their detachment and transportation
elsewhere. Therefore, biofilm components increased quite slowly
during this period. Hereafter, there were much more microor-
ganisms and viscid secretion in biofilms as microbial community
 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34 31

Table 5
Fitting parameters of growth kinetic model of biofilms EPS inside emitters.

Lateral position Emitters b1 b2 b3 b4 Correlation Mean Mean Root- Residual

coefficient (r) bias absolute mean- sum
error error square of
(MBE) (MAE) error (RMSE) squares
(SSE)

Head FE1 2.825 −1.461 9.759 0.0034 0.98** 0.026 0.336 0.41 1.89
FE2 3.279 0.324 15.767 0.0032 0.97** 0.029 0.416 0.53 3.04
FE3 8.661 0.509 19.113 0.0027 0.98** 0.008 0.141 0.19 0.38
FE4 2.238 −0.837 11.096 0.0043 0.98** 0.015 0.260 0.31 1.04
CE1 6.775 −1.286 7.625 0.0023 0.95** 0.004 0.084 0.11 0.14
CE2 7.710 −1.429 14.195 0.0028 0.97** 0.004 0.086 0.10 0.10
CE3 8.631 1.832 20.275 0.0030 0.98** 0.001 0.023 0.03 0.01
CE4 12.215 −1.104 16.940 0.0027 0.98** 0.004 0.071 0.09 0.08
CE5 27.022 −0.168 26.265 0.0019 0.96** 0.003 0.089 0.10 0.12
Middle FE1 2.761 0.412 6.465 0.0047 0.96** 0.045 0.495 0.58 3.76
FE2 1.894 −0.460 9.833 0.0062 0.95** 0.042 0.604 0.75 6.22
FE3 8.958 −1.764 22.327 0.0026 0.96** 0.023 0.190 0.28 0.85
FE4 2.810 −0.185 8.508 0.0027 0.99** 0.028 0.370 0.45 2.20
CE1 4.947 −0.867 6.854 0.0028 0.95** 0.008 0.115 0.15 0.23
CE2 7.594 0.202 16.472 0.0031 0.97** 0.005 0.060 0.07 0.06
CE3 10.395 −0.216 9.722 0.0019 0.90** 0.003 0.081 0.10 0.11
CE4 13.267 −0.001 17.714 0.0025 0.97** 0.007 0.093 0.10 0.12
CE5 10.449 0.108 14.351 0.0031 0.99** 0.004 0.055 0.08 0.06
End FE1 3.553 0.122 6.848 0.0027 0.97** 0.033 0.452 0.64 4.48
FE2 2.728 −2.221 10.189 0.0027 0.98** 0.033 0.311 0.49 2.59
FE3 10.442 −1.632 23.021 0.0024 0.99** 0.023 0.200 0.27 0.81
FE4 2.295 −0.199 4.837 0.0031 0.91** 0.036 0.775 0.96 10.17
CE1 8.649 −1.733 37.990 0.0031 0.99** 0.004 0.058 0.06 0.05
CE2 11.513 −0.359 32.373 0.0028 0.99** 0.008 0.072 0.09 0.09
CE3 7.980 −1.496 14.753 0.0029 0.97** 0.003 0.049 0.06 0.04
CE4 8.995 −1.560 32.733 0.0042 0.99** 0.009 0.050 0.06 0.04
CE5 17.228 −4.893 32.270 0.0026 0.99** 0.004 0.083 0.10 0.11

Note: In the table, ** means “significant” under significant level a = 0.01.

expanded rapidly with sufficient nutrition supply. Meanwhile, the
microorganisms in the internal layer of biofilms also could obtain
enough nutrition, thanks to the loose and cribrate surface struc-
ture. Microorganisms were extremely active in metabolism with
much more viscous EPS, and thus biofilms could absorb and capture
multiple matters in the water easier so as to grow faster. Although
this was accompanied by the detachment of mature biofilms, the
growth of biofilms was far greater than their detachment, so biofilm
components still showed obvious rapid and stable growing trend
during the period. When the biofilms continued to grow, there
was competition for nutrients between microorganisms, and much
more nutrients were needed to maintain their growth. Further-
more, much more EPS was needed to maintain the relative stable
biofilm structure. The results also revealed that EPS showed more
obvious increasing trend when compared with SD and PLFAs during
the later operation of the system.
Biofilm components in flat emitters were larger than those in
cylindrical emitters. However, the clogging degree of flat emitters
was smaller than those of cylindrical emitters. This was mainly
because the geometrical parameters of flat emitter flow path were
relatively small and accompanied with weaker randomness of
biofilm growth. Biofilms in flat emitters were more likely to grow
in the flow stagnation areas because of the relatively low water
shear force. Therefore, biofilm growth had no significant impact on
the water flow characteristics in the mainstream areas, and led to
less effect on emitter clogging. The results were consistent with
the results of Pei et al. (2014) that flat emitters had stronger anti-
clogging ability. On the other hand, biofilm SD, EPS and PLFAs all
increased from the head to the middle to the end part of the lateral.
The main reason was that the DI laterals were small in diameter,
the flow rates decreased from the head to the middle part and then
to the end part of the lateral. At the head part of the lateral, rel-
atively faster water flow could transport more nutrients per unit
interval, the biofilm pores at the head part were more likely to
be filled with microbial and EPS. Meanwhile, higher flow rate at
the head part led to high turbulence intensity and hydraulic shear
force, so biofilms were more likely to detach and transported along
to the end part and accumulated there eventually. Furthermore,
the biofilm growing characteristics in emitters at different lateral
position also explained the reason why Pei et al. (2014) found that
the entire emitters clogging degree became more serious from the
head to the end part of the lateral.
In order to control emitter clogging effectively, common emit-
ter controlling methods are usually applied in practical DI projects.
Meanwhile, CD was recommended to be less than 25%, according
to the emitter clogging standard proposed by ISO Standards (2003).
Actually, the dynamic changing process of biofilm components (SD,
EPS and PLFAs) also showed the “S shape” pattern with CD (take
SD for example, Fig. 5). To be specific, the results acquired in this
paper showed that the increasing rate of biofilm SD varied in the
“slow–fast–slow” trend as a function of the accumulated opera-
tion of the system (T). On the other hand, Fig. 5 also revealed that
the increasing rate of CD also showed the “fast–slow–fast” trend
with the increase of biofilm SD. After considering the two correla-
tions mentioned above, CD increased significantly with increased
SD when CD < 15% or at the initial 200 h of system operation. How-
ever, biofilm SD grew slowly during the stage, and thus failed to
increase CD rapidly. After the system operated for 200–300 h, i.e.
15% < CD < 25%, SD accelerated its growth but CD was less sensi-
tive to the increase of SD. Since then, CD exceeded 25%, and the
increase of SD would enhance CD significantly. In other words,
emitter clogging controlling methods were not effective to con-
trol biofilm formation when CD < 10% as commonly used nowadays.
Therefore, it is more suitable to apply emitter clogging methods
when the system operated for 300 h, thus guarantying its highly-
efficient operation.
In fact, emitter biofilm components (SD, EPS and PLFAs)
were influenced by each other with obvious linear relations
32 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34

Fig. 5. Relations between biofilm components, emitter clogging degree and system operation.

Table 6
Path analysis of biofilm components on emitter clogging degree.
2
Biofilm components Correlation coefficientR2 Direct impact |bi |Partial correlation coefficientbi Indirect impact |riy | rij bi Decisive coefficientR(i)

SD(x1 )—CD(y) 0.647 1.274** PLFAs(x2 ) 0.254 −0.671

0.025
EPS(x3 ) −0.925
PLFAs(x2 )—CD(y) 0.579 0.279** SD(x1 ) 0.250 −0.694
−0.567
EPS(x3 ) −0.944
EPS(x3 )—CD(y) 0.443 −0.981N SD(x1 ) 1.201 1.469 −1.831
PLFAs(x2 ) 0.268

Note: In the table, **means “significant” under significant level a = 0.01 and N means not significant.

(R2 EPS-SD = 0.912, R2 EPS-PLFAs = 0.962, R2 SD-PLFAs = 0.943, Fig. 6). In
order to reveal the key influential factor to CD among these biofilm
components and their influence paths, the path analysis results
are shown in Table 6. According to the multiple linear regres-
sion equations and the VIF acquired accordingly Eq. (4)–(6), taking
VIF = 10 as the criterion), EPS showed obvious multiple linear rela-
tions with SD and PLFAs, which meant that EPS was codetermined
by both SD and PLFAs. Meanwhile, SD and PLFAs had significant
direct impact on CD and ranked as |bSD | > |bPLFAs | with 1.274 and
0.279 (Table 6). However, the direct impact of EPS on CD failed to
pass the significance test, which was related to the multicollinear-
ity confirmed by Eq. (4)–(6), and this indicated that EPS’s direct
impact on CD was relatively weaker than those of SD and PLFAs.
On the other hand, the indirect impact of EPS reached 1.469, which
was obvious higher than those of SD (0.671) and PLFAs (0.694).
Moreover, the indirect impact of EPS on CD through SD (1.201)
 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
Fig. 6. Linear relations between biofilm components.
was much higher than that of PLFAs (0.268). Thus it could be seen
that SD would directly affect CD, as SD was the representation
of biofilm dry matters and reflected the entire growing status of
biofilms. EPS, on the other hand, did not have significant direct
impact on CD. As the sticky substances secreted by microorgan-
isms, EPS mainly took advantage of their viscidity to obtain the
solid particles, microorganisms, organic matters etc. to maintain
the stable biofilm structure and thus affected CD by influencing SD,
with the consequential impact on microbial community (PLFAs)
to some extent at the same time. On the other hand, PLFAs had
a more complicated influential path, as it could affect CD directly
while showing its impact on CD indirectly via EPS. In conclusion,
the direct and indirect impacts of biofilm SD, EPS and PLFAs were
complex. According to Table 6, their decisive coefficients ranked as
R(SD) 2 > R(PLFAs) 2 > R(EPS) 2 , which indicated that SD was the decision
variable to CD.
SD = 0.824 × PLFAs + 0.034 ×EPS
+ 0.141(F = 3674.03 ∗ ∗, VIF = 6.98) (4)
EPS = 0.067 × SD + 0.913 × PLFAs
+ 0.019(F = 2385.19 ∗ ∗, VIF = 10.46) (5)
PLFAs = 0.679 × SD + 0.381 × EPS
-0.059(F = 5774.51 ∗ ∗, VIF = 4.81) (6)
Note: F-value in Eq. (4)–(6) represents the significance test
results of multiple linear regression equations, and ** means “sig-
nificant” under significant level a = 0.01.
In conclusion, the paper studied the biofilm components
growing processes through the reclaimed water DI experiment
performed in wastewater treatment plant, and then the growing
kinetic model of biofilm components was established. However,
there were still some issues needed to be studied in the future:
33
(1) The experiment was accomplished in the wastewater treat-
ment plant with the reclaimed water treated under Cyclic
Activated Sludge System (CASS) technology. It is necessary to
carry out more DI experiments with reclaimed water treated
with other technologies, in order to further verify the feasibility
and veracity of the growing kinetic model of biofilm compo-
nents established in this paper. Furthermore, experiments with
crops planted are further needed to study how emitter types,
flow path geometrical parameters, irrigation frequencies and
working pressures etc. would affect biofilm formation inside
emitters as well as its fitting effects, in order to test the relia-
bility of the model.
(2) The studies on biofouling process using reclaimed water and
their inducing mechanism were mainly studied through an on-
site DI experiment. So how to calculate the fitting parameters
of the growth kinetic model without a long-term experiment
needs to be studied.
(3) The related studies, including emitter clogging process, biofilm
components, influential factors and method to predict or calcu-
late emitter clogging etc., should be integrate together to reveal
the bio-clogging mechanism.
5. Conclusions
Biofilm formation and growth inside emitter flow path is tightly
related to the drip irrigation emitter clogging using reclaimed
water, and studying the detailed growth process is the basis of
revealing the bio-clogging mechanism and then proposing the
emitter clogging controlling methods.
In this paper, the biofilms growth process was quantified by
establishing a growth kinetic model based on the Logistic growth
model. The established growth kinetic model of biofilms compo-
nents (SD, PLFAs and EPS) focused on their response to emitter
types, flow path geometrical parameters and lateral positions com-
prehensively, and proved to describe the biofouling process well
(R2 > 0.85**, significant level a = 0.01).
According to the kinetic growth model, the biofilms growth
process in non-PC DI emitters using reclaimed water could be
divided in order as growing adaptive period, rapid growing period
and dynamic stable period. At the initial 408 h, biofilms belonged
to growing adaptive period and their formation was relatively
34 B. Zhou et al. / Agricultural Water Management 168 (2016) 23–34
slow. It was followed by the rapid growing period at 408–1088 h,
with much more rapid increase of biofilm components. Then the
biofilm growth and detachment reached a balance and represented
dynamic stable status till 1224 h, during which biofilm components
increased slowly or even decreased slightly.
Actually, biofilms components had significant impacts on emit-
ter clogging degree (CD), as CD increased in the “fast–slow–fast”
trend with biofilm growth. When considering these two effects
together, the emitter clogging controlling methods could be
delayed to the reclaimed water DI system operated for 300 h
(i.e. CD < 25%), rather than being applied at the beginning of or
shortly after the system operated. The new strategy is able to
ensure the highly-efficient operation of the DI system. These results
acquired would provide important and valuable references to reuse
reclaimed water in agricultural irrigation, especially with DI.
Acknowledgements
We are grateful for the financial support from the National Natu-
ral Science Fund of China (51321001, 51179190, 51339007), Public
Welfare Project of PRC Ministry of Water Resources (201401078).
The first author also appreciates the financial support from the
China Scholarship Council (CSC) as a visiting PhD student at Purdue
University.
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