Journal of Environmental Management 271 (2020) 110948

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Journal of Environmental Management

journal homepage: http://www.elsevier.com/locate/jenvman

Research article

Responses of phytoremediation in urban wastewater with water hyacinths

to extreme precipitation
Hongjie Qin a, b, c, d, *, Muhe Diao e, Zhiyong Zhang b, d, Petra M. Visser c, Yingying Zhang b, d,
Yan Wang b, d, Shaohua Yan b, d, **
a
Key Laboratory for Agricultural Environment, Ministry of Agriculture and Rural Affairs, Beijing, 100081, China
b
Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China
c
Department of Freshwater and Marine Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE, Amsterdam, the Netherlands
d
China Ministry of Agriculture Key Laboratory at Yangtze River Plain for Agricultural Environment, Nanjing, 210014, China
e
Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany

A R T I C L E I N F O A B S T R A C T

Keywords: Climate change not only intensifies eutrophication and enhances the rainfall, but also elevates the contents of
Climate change greenhouse gases, which can further increase the intensity and frequency of extreme precipitation events. The
Extreme precipitation effectivity of phytoremediation of urban wastewaters by water hyacinths under an extreme rainfall event (up to
Phytoremediation
380 mm d 1) was investigated using self-designed fabrications with six flow rates (2–15 m3 d 1) in situ on pilot
Urban wastewater
Water hyacinth
scale for 30 days. The results suggest that water hyacinths had high N and P removal capacities even under
adverse conditions such as low dissolved oxygen concentrations (DO, <1 mg L 1) and high ammonium con­
1
centrations (NHþ 4 -N, >7 mg L ). Specifically, the highest removal yields of N and P were 13.14 � 0.47 g
N⋅m 2⋅d 1 and 2.12 � 0.04 g P⋅m 2⋅d 1, respectively. The results indicate that water hyacinths can be used for
3
water treatment to reduce the amounts of NHþ 4 -N, dissolved organic nitrogen (DON) and phosphate (PO4 ) even
during extreme precipitation events. Moreover, DO increased due to wet deposition, runoff and surface flows
during the extreme rainfall event, resulting in shifts between nitrification and denitrification processes which
significantly altered nitrogen forms in urban wastewater. Results of this study suggest that water hyacinths could
be recommended as a cost-effective and eco-friendly technology for urban wastewater phytoremediation in areas
suffering from frequent extreme precipitation events.

1. Introduction et al., 2009; Moss et al., 2011) increasing total rainfall (Reichwaldt and
Ghadouani, 2012). There is consensus that changes in the intensity of
In recent years, large volumes of wastewaters have been produced short-term precipitation are related to increasing temperatures world­
with the accelerated urbanization (Zhu et al., 2018; John et al., 2020). wide (Hegerl et al., 2015; Donat et al., 2016; Luong et al., 2017). In
According to European Commission Directive 91/271/EEC, urban addition, gradually rising temperature (IPCC, 2013) can also raise
wastewater is a mixture of domestic wastewater and rainwater (Al evaporation, which result in extreme rainfall events occurring more
Aukidy and Verlicchi, 2017). Excessive nutrients in urban wastewater, frequently (Douka and Karacostas, 2018). Accumulating evidence re­
especially nitrogen (N) and phosphorus (P) pose a serious risk of veals that the intensity and frequency of heavy precipitation event have
eutrophication in natural water bodies, which lead to deterioration of been strengthened (De Toffol et al., 2009; Fischer and Knutti, 2016;
water quality and severe degradation of aquatic ecosystems (Hu et al., Wang et al., 2017).
2008; Dalu et al., 2019). Eutrophication of water bodies caused by Prior to discharging into rivers, lakes or other natural water reserves,
human activities has been considered as a common environmental issue eliminating nutrients (especially N and P contents) in wastewater is an
and has gained attention worldwide (Conley et al., 2009). indispensable process and therefore has received a lot of attention
Moreover, global warming can exacerbate eutrophication (Jeppesen (Mor�ee et al., 2013; Li et al., 2020; Srinivas et al., 2020). Conveying

* Corresponding author. Key Laboratory for Agricultural Environment, Ministry of Agriculture and Rural Affairs, Beijing, 100081, China.
** Corresponding author. Institute of Agricultural Resources and Environment, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China.
E-mail addresses: hongjieqin111@126.com (H. Qin), shyan@jaas.ac.cn (S. Yan).

https://doi.org/10.1016/j.jenvman.2020.110948
Received 20 January 2020; Received in revised form 4 June 2020; Accepted 9 June 2020
Available online 16 July 2020
0301-4797/© 2020 Elsevier Ltd. All rights reserved.
H. Qin et al. Journal of Environmental Management 271 (2020) 110948

urban wastewater to wastewater treatment plants (WWTP’s) by com­ could be divided into three stages as follows: 1) before precipitation (BP,
bined sewer systems is a conventional method for wastewater treatment 0 - 10th d), 2), after precipitation (AP, 11th - 17th d), and 3) the recovery
in many urbanized areas (Al Aukidy and Verlicchi, 2017). However, the stage after precipitation (RP, 18th - 30th d).
wastewater may overflow from the sewer network in case of heavy
rainfall (Barco et al., 2008; Corada-Fern� andez et al., 2017), which may
2.2. The fabrication
bring large amounts of nutrients into lakes, aggravating eutrophication
and consequently leads to an ecological crisis (Feng et al., 2018; Huis­
The self-designed fabrications (length 10.0 m � width 1.0 m � depth
man et al., 2018). The processes of removing nutrients from wastewater
0.5 m) without a top cover were constructed of stainless steel (Fig. 1). To
require either chemical reagents or complementary facilities (Jin et al.,
keep the six cuboid boxes floating in the water, bubble floaters were
2014; Yang et al., 2020a), which are complex operations and produce
fixed on both sides of them. At one end of the box, a pump was bound for
large amounts of sludge. This sludge management is a huge challenge in
influent flow rate control. The pumps were semi-enclosed with plates to
many areas worldwide (Yang et al., 2015; Meng et al., 2019).
avoid hazards from the wastewater. An outlet pipe (5 cm in diameter)
Hence, it is urgent to develop cost-effective and eco-friendly tech­
was set at the other end of the box from where the treated wastewater
nologies for urban wastewater treatment, especially for emergency
was discharged.
treatment of rainstorm runoff. Phytoremediation is a mature and well-
accepted green technology, which removes contaminants (nutrients,
organic compounds, radio-nuclides, and toxic metals) from wastewater 2.3. Experimental setup
by plants (Sood et al., 2012; Shi et al., 2016; Rezania et al., 2019).
Compared to traditional techniques, such as chemical precipitation, Based on our previous studies and preliminary experiments, six flow
reverse osmosis, ion exchange, phytoremediation has several advan­ 2 m3 d 1, 4 m3 d 1, 6 m3 d 1, 8 m3 d 1, 10 m3 d 1 and 15 m3 d 1) were
tages such as being solar-driven, economical, and sustainable (Batty and set in the systems. Flow rates of the pumps were calibrated every 24 h.
Dolan, 2013; Qin et al., 2017). In recent years, water hyacinths have Healthy water hyacinths (Eichhornia crassipes (Mart.) Solms) with
attracted more attention because of their efficient absorption of nutri­ similar sizes and growth stages were collected and placed into each
ents (Yan et al., 2017; Avila et al., 2019), extensive tolerance to envi­ floating box with equal initial macrophyte biomass (4 kg m 2 wet
ronmental conditions (Rommens et al., 2003), and broad applicability in weight). The macrophyte biomass in different boxes was estimated at
a variety of wastewaters (Chavan and Dhulap, 2012; Rezania et al., about weekly intervals as wet weight per unit area (kg⋅m 2).
2015; Yu et al., 2018).
However, there are also concerns about phytoremediation of
wastewater by water hyacinths: (1) ecological risks because of easy 2.4. Water sample collection and analysis
transfer from one region to another; (2) necessity of frequent harvesting
because of large amounts of weeds covering the water surface; (3) Influent and effluent samples were collected in triplicate every day at
difficult resource utilization because of high water content (94%) in the 9:00 AM during the experiment. Water temperature, dissolved oxygen
macrophytes. Due to their very high growth rate (Mishra and Tripathi, (DO), and pH were measured in situ by using a multi-parameter water
2009), water hyacinths may indeed cause ecological and socio-economic analyzer (HQ40D, Hach, USA). To determine N and P concentrations,
disasters if they grow without control. However, these worries have 500 mL water samples were collected from both influent and effluent
been eliminated gradually with the technical systems on large-scale sampling sites and stored in polyethylene bottles in the fridge at 4 � C.
application, mechanized harvesting, and utilization of water hyacinth Total nitrogen (TN), total dissolved nitrogen (TDN), nitrate (NO3 ), ni­
3
being established in China (Wang et al., 2012; Yan and Guo, 2017). trite (NO2 ), ammonium (NHþ 4 ), total phosphorus (TP), and PO4 were

Although wastewater phytoremediation by water hyacinths have determined using an Auto-Analyzer (Sanþþ System, The Netherlands)
been reported extensively (Rezania et al., 2015; Yan et al., 2017), it is following standard methods (APHA, 1998). Dissolved organic nitrogen
still unknown how water hyacinths respond to extreme precipitation. (DON), removal yield, and removal efficiency were calculated as
Furthermore, most of previous studies were carried out either in labo­ follows:
ratories (Lu et al., 2014) or in open natural waters (Yan and Guo, 2017), ρðDONÞ ¼ ρðTDNÞ ρ NO3
�
ρ NO2
�
ρ NHþ4
�
(1)
where it was impossible to accurately determine the effects of phytor­
emediation, especially during extreme rainfall events. By using �
Removal yield g⋅m 2 ⋅d 1 ¼ ½ρðInfluentÞ ρðEffluentÞ�
self-designed fabrications to conduct in situ phytoremediation studies �
with water hyacinths, the effects could be accurately monitored. The � Flow rate Box area (2)
objectives of this study are to: (a) investigate the changes of urban
Removal efficiencyð%Þ ¼ 100% � ½ρðInfluentÞ ρðEffluentÞ� = ρðInfluentÞ
wastewater quality after extreme rainfall events; (b) determine the
removal yield of N and P by water hyacinths under different nutrient (3)
loadings; (c) evaluate the phytoremediation effects of water hyacinth
Where ρ indicates the concentration, and ρ(Influent) and ρ(Effluent) the
under extreme precipitation.
concentration of TN or TP in influent and effluent (g⋅m 3), respectively,
flow rate is pump flow rate (m3⋅d 1), and the area of the box is 10 m2.
2. Materials and methods

2.1. Site description 2.5. Statistical analysis

The study was carried out in an open pond (32� 020 17"N The normality of data among different treatments was assessed by
118� 520 06"E) in Nanjing (Jiangsu Province, China), where the water Shapiro-Wilk and the homogeneity of data was tested by Levene Sta­
was replenished by urban wastewater. During the 30-day experiment tistic. Subsequently, one-way ANOVA was performed at the 95% con­
(20th September to 20th October, 2016), the water temperature range fidence level followed by the least significant difference (LSD) post hoc
was 20.2� C–25.4 � C and the air temperature range was 16.2� C–28.9 � C. test (SPSS 18.0, Chicago, IL, USA). Pearson correlations between flow
During this period, with mainly sunny days, an extreme precipitation rate and physicochemical parameters of the effluent were analyzed with
occurred on the 11th day (380 mm d 1). After the extreme rainfall SPSS 18.0. In specific, correlations were tested by bivariate analysis and
event, the river flooded due to uphill rainwater convergence for about significances were verified by two-tailed test. All data were presented as
seven days. Based on the time of extreme precipitation, the experiment mean � standard deviation (SD).

2
H. Qin et al. Journal of Environmental Management 271 (2020) 110948

(a) (b) (c)

(d)

Fig. 1. Experimental devices: (a) panorama; (b) outlets; (c) inlets; (d) structural diagram.

3. Results L 1) and RP (14.46 � 0.74 mg L 1) stages (P > 0.05). The TN concen­

trations of effluents from all experimental boxes were significantly lower
3.1. Chemical properties of water samples than those of the influents (P < 0.05). TN values of the effluents were
positively correlated with the flow rates (Table S1).
The pH of the influent remained relatively stable and varied between The trend changes in NHþ 4 -N and DON were the same as those of TN
of 7.07 � 0.04 and 6.91 � 0.02 during the entire experiment (Fig. 2a). (Fig. 3b, e). The mean values of NHþ 4 -N in the influents of BP, AP and RP
Effluent pH values of all treatments slightly decreased during the were 6.55 � 1.29 mg L 1, 2.57 � 0.52 mg L 1, 6.72 � 0.68 mg L 1 and
experiment, and the 2 m3 d 1 group showed the most obviously the mean values of DON in the influents of BP, AP and RP were 4.71 �
decreasing trend. As shown in Table S1, effluent pH values were 2.96 mg L 1, 1.03 � 1.25 mg L 1, and 5.98 � 1.29 mg L 1, respectively.
significantly positively correlated with flow rates, which were not It is worth emphasizing that concentrations of NHþ 4 -N and DON in the
disturbed by the extreme precipitation (Table S2, Table S3, Table S4). effluents were 45.52%, 38.43%, 46.50% and 32.70%, 15.46%, 41.39%
The average DO concentrations of the influent were 0.68 � 0.17 mg of those in the influents of BP, AP and RP stages, respectively. For the
L 1, 2.30 � 1.18 mg L 1, and 0.81 � 0.23 mg L 1 in BP, AP, and RP, lowest flow rate treatment (2 m3 d 1), the NHþ 4 -N removal percentages
respectively, and showed a significant increase (P < 0.05) to the peak of were 70.20%, 85.23%, 92.07% in BP, AP and RP stages, respectively,
4.59 � 0.14 mg L 1 on the 11th day when the extreme precipitation and DON removal percentages were 90.67%, 64.46%, 99.53% in BP, AP
event occurred. No significant differences in DO were observed between and RP stages, respectively. For the highest flow rate treatment (15 m3
influent and effluent of the 2 m3 d 1 treatment during the AP stage d 1), the NHþ 4 -N removal percentages were 28.84%, 34.87%, 52.61%,
(Fig. 2b) (P > 0.05). However, DO concentrations in the effluent were and DON removal percentages were 99.83%, 99.36%, 83.92% in BP, AP
significantly higher than those in the influent of the 2 m3 d 1 treatment and RP stages, respectively.
in BP and RP stages (0.94 � 0.16 mg L 1 and 2.31 � 0.81 mg L 1) (P < Compared with other forms of nitrogen, NO2 -N showed a different
0.05). changing trend. After the extreme precipitation event, NO2 -N concen­
trations in the influent and effluent were significantly increased (P <
0.05) (Fig. 3c). Compared with the influent, NO2 -N concentrations in
3.2. Different forms of N in water the effluent were significantly lower at the beginning of the experiment,
and they were markedly higher after the precipitation (P < 0.05), and
Concentrations of different forms of nitrogen were determined then showed a decreasing trend to no differences in the end (P > 0.05).
regularly (Fig. 3). As shown in Fig. 3a, no significant differences of TN Complex changes in NO3 -N concentrations exhibited throughout the
concentrations in influent were found between BP (14.39 � 2.01 mg

3
H. Qin et al. Journal of Environmental Management 271 (2020) 110948

7.5
7.4 (a)
7.3
7.2
7.1
7.0
6.9
6.8 Rainstorm
pH

6.7
6.6
6.5
6.4
6.3
6.2
6.1
6.0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d)

6
(b)
5

Rainstorm
DO (mg L )
-1

0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d)

Fig. 2. Variations of (a) pH and (b) DO in the influents and effluents during the experiment.

entire experimental period (Fig. 3d). The changes of NO3 -N in the Changes of N removal efficiency were showed in Table S5. For the 2
influent were similar to those of NO2 -N which increased after the m3 d 1 and 15 m 3 d 1 treatments, the removal efficiency was 52.39 �
extreme precipitation. While, NO3 -N concentrations in the effluent of 9.41%, 40.08 � 17.05%, 68.52 � 8.81% and 33.85 � 10.75%, 10.07 �
the 2 m3 d 1 treatment was significantly higher than the values of the 3.43%, 27.11 � 8.37% in the BP, AP, and RP stages, respectively.
influent (P < 0.05) except for the AP stage.
The N removal yields in experimental fabrications were shown in
Fig. 4a. The N removal yields increased from 1.51 � 0.39 g m 2⋅d 1 to 3.3. Different forms of P in water
7.51 � 3.20 g m 2⋅d 1 in the flow rate treatments from 2 m3 d 1 to 15
m3 d 1 during the BP stage (P < 0.05). The removal yields of N reached TP and PO34 showed a similar trend as TN through the study period
up to 13.14 � 0.47 g m 2⋅d 1 in the treatment with the highest pump (Fig. 5a and b). TP concentrations in the effluents of all treatments were
flow rate. Although the removal yields showed a decreasing trend in the significantly lower than those of influents, especially for the low pump
AP stage, they still had considerable high mean values from 0.54 g flow rate groups (P < 0.05). In particular, the PO34 concentrations of the
m 2⋅d 1 to 1.07 g m 2⋅d 1 in different treatment boxes. During the RP effluent from 2 m3 d 1 box were 0.07 � 0.04 mg L 1, 0.02 � 0.01 mg L 1
stage, the removal yields increased to 1.95 � 0.30 g m 2⋅d 1, 2.72 � and 0.02 � 0.01 mg L 1 in BP, AP, RP stages, respectively. The PO34
0.54 g m 2⋅d 1, 2.88 � 0.69 g m 2⋅d 1, 3.20 � 1.45 g m 2⋅d 1, 3.72 � concentrations of the effluent were reduced by 89.69%, 88.81% and
1.61 g m 2⋅d 1, and 5.85 � 1.93 g m 2⋅d 1 respectively in different 96.77% compared to their influents, respectively (Fig. 5b).
experimental boxes from low flow rate treatments (2 m3 d 1) to the high The removal yields of P were shown in Fig. 4b. The highest P removal
ones (15 m3 d 1). yield (2.12 � 0.04 g m 2⋅d 1) was exhibited in the 15 m3 d 1 treatment
during the BP stage, and the mean values changed from 0.06 � 0.02 g

4
H. Qin et al. Journal of Environmental Management 271 (2020) 110948

22 10

20 (a) (b) 9
18 8
16
7
14
Rainstorm

NH4 -N (mg L )
-1
6
Rainstorm
TN (mg L )

12
-1

5
10

+
4
8
3
6

4 2

2 1

0 0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d) Time (d)

2.0 5.5

1.8 (c) (d) 5.0

1.6 4.5

4.0
1.4
3.5

NO3 -N (mg L )
1.2 Rainstorm

-1
NO2 -N (mg L )
-1

3.0
1.0
2.5
Rainstorm

-
0.8
-

2.0
0.6
1.5
0.4 1.0

0.2 0.5

0.0 0.0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d) Time (d)

14
13 (e)
12
11
10
9
DON (mg L )

8
-1

7
6
5
Rainstorm
4
3
2
1
0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d)

Fig. 3. Concentration changes of different forms of nitrogen in the influents and effluents. (a) TN; (b) NHþ
4 -N; (c) NO2 -N; (d) NO3 -N; (e) DON.

m 2⋅d 1 to 0.19 � 0.09 g m 2⋅d 1 in different experimental boxes soon 8th day. The biomass was almost the same for the six flow rates (~12.30
after the precipitation. kg m 2) on the 15th day. The increase in biomass was lower in all
With the decrease of the wastewater flow rate from 15 m3 d 1 to 2 treatments towards the end of the experiment. Except for 2 m3 d 1
m3 d 1, the mean values of P removal efficiencies increased from 50.51 treatment (17.35 kg m 2), no significant differences among the treat­
� 13.09% to 78.46 � 17.76%, from 31.13 � 11.57% to 73.32 � 7.42%, ments were observed during the entire study (P > 0.05).
and from 53.41 � 8.48% to 88.97 � 2.89% during BP, AP and RP stages,
respectively (Table S6). 4. Discussion

3.4. Water hyacinth biomass Many cases of wastewater phytoremediation by water hyacinths
have been reported (Yan et al., 2017; Tao et al., 2020) and it was
The biomass of water hyacinths was measured five times during the concluded that this method can be useful. Whether water hyacinths can
study (Table 1). In the beginning, the biomass of all treatments showed a also be used to take up excess nutrients after an extreme precipitations
large increase, and then reached a doubling of the initial biomass on the event when large volumes of urban wastewater may overflow from the

5
H. Qin et al. Journal of Environmental Management 271 (2020) 110948

14 2.5
(a) 2m d
3 -1
4m d
3 -1 3
6m d
-1
(b) 3
2m d
-1 3
4m d
-1
6m d
3 -1

12 3 -1
8m d
3 -1
10 m d
3 -1
15 m d
3 -1
8m d
3 -1
10 m d
3 -1
15 m d
2.0
10

P removal yield (g m d )
-1
N removal yield (g m d )
-1

-2
-2

8 1.5

6
Rainstorm
1.0
4 Rainstorm

2 0.5

0.0
-2
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d) Time (d)

Fig. 4. Dynamics of (a) N removal yield and (b) P removal yield during the experiment.

3.00

2.75 (a)
2.50

2.25

2.00

1.75
TP (mg L )
-1

1.50

1.25

1.00
Rainstorm
0.75

0.50

0.25

0.00
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d)

1.5
1.4 (b)
1.3
1.2
1.1
1.0
PO4 (mg L )

0.9
-1

0.8
0.7
3-

0.6
0.5 Rainstorm
0.4
0.3
0.2
0.1
0.0
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
Time (d)

Fig. 5. Changes of (a) TP and (b) PO34 concentrations in the influents and effluents.

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H. Qin et al. Journal of Environmental Management 271 (2020) 110948

Table 1 runoff, ammonia was converted to nitrite and nitrate through a

Biomass changes of water hyacinth. Different lowercase letters indicate statis­ two-stage nitrification process (Mehrani et al., 2020; Pathak et al., 2020)
tically significant differences between different time periods (P < 0.05). first by aerobic ammonia-oxidizing bacteria and archaea, and second by
Different uppercase letters indicate statistically significant differences between nitrite-oxidizing bacteria (Koch et al., 2014; Yang et al., 2020a). In
different flow rates for each time period (P < 0.05). addition, ammonia can also be oxidized to nitrate through complete
Time 2 m3 d 1 4 m3 d 1 6 m3 d 1 8 m3 d 1 10 m3 15 m3 ammonia oxidation process by Comammox (COMplete AMMonia OXi­
(d) (kg⋅m 2) (kg⋅m 2) (kg⋅m 2) (kg⋅m 2) d 1 d 1 diser) (van Kessel et al., 2015; Annavajhala et al., 2018). Rainfall events
(kg⋅m 2) (kg⋅m 2)
might lead to large changes in water physicochemical properties (Bouvy
0 4.00 � 4.00 � 4.00 � 4.00 � 4.00 � 4.00 � et al., 2003), and consequently, changes in the influent could greatly
0.15 a A 0.02 a A 0.13 a A 0.13 a A 0.13 a A 0.10 a A
alter the microbial community composition (Zhang et al., 2020), which
8 9.35 � 10.05 � 10.70 � 10.55 � 10.75 � 10.50 �
0.23 b A 0.30 b A 0.19 b A 0.27 b A 0.20 b A 0.20 b A can eventually affect the nitrogen removal. The dramatic increased DO
15 12.05 � 12.40 � 12.45 � 12.25 � 12.35 � 12.30 � after the extreme precipitation was an important driving force in
0.20 c A 0.11 b A 0.31 b A 0.18 b A 0.20 b A 0.23 b A changing nitrogen forms.
22 14.25 � 13.95 � 14.15 � 15.10 � 15.05 � 15.60 � In urban wastewater, the primary forms of nitrogen are NHþ 4 -N and
0.09 c A 0.21 b A 0.25 b A 0.15 c A 0.29 c A 0.25 c A
organic nitrogen, of which the latter is instantly changed to NHþ 4 -N
30 17.35 � 19.18 � 19.89 � 20.18 � 20.00 � 20.10 �
0.17 d A 0.14 c B 0.21 c B 0.20 d B 0.27 d B 0.20 d B (Qiang et al., 2020). NHþ 4 -N is the preferred N source for most aquatic
plants (Zhou et al., 2017), because NHþ 4 -N can be rapidly assimilated
into amino acids without further reduction requiring less energy than
sewer network, is yet unknown. Therefore, this study investigated the utilizing NO3 -N (Britto and Kronzucker, 2013). Nonetheless, high con­
phytoremediation effects of water hyacinths during such precipitation centrations of NHþ 4 -N can also be toxic to cells (Bitts� anszky et al., 2015).
event. Growth inhibition is one of the obvious symptoms of NHþ 4 -N toxicity to
The results indicated that the pH of the influents maintained a many plant species (Wang et al., 2016), and the toxicity tolerance of
neutral level (~pH 7.0) during the whole experiment, including during NHþ 4 -N differs widely among a variety of plant species (Wang et al.,
the period of extreme rainfall. Qin et al. (2016a) also showed that the pH 2019). Free-floating aquatic plants are usually more tolerant to NHþ 4 -N
did not change significantly in water hyacinth-growing areas. The pre­ than submerged macrophytes (Zhou et al., 2017). Specifically, ammo­
sent study showed that the pH of urban wastewater was decreased after nium transporters in water hyacinth cells could maintain NHþ 4 -N in the
flowing through the boxes with water hyacinths. Organic acids released cells at a safe level (Li et al., 2014), but water hyacinths would die at a
by organic matter attached on the root mats and CO2 released by mi­ concentration of 370 mg L 1 NHþ 4 -N or higher (Yan et al., 2017). The
crobial respiration under anaerobic conditions might be responsible for dramatic increase in water hyacinth biomass after the extreme rain fall
reducing pH values (Rommens et al., 2003; Perez-Fodich and Derry, events indicated that the contents of NHþ 4 -N in urban wastewater had
2019). probably limited toxicity to the plants. It is worthwhile to mention that
Oxygen, associated with nitrogen removal (Choudhury et al., 2018), biomass of water hyacinths under different flow rates were similar
plays a key role in regulating the major biogeochemical cycles in aquatic before 22 days. The potential factors caused this phenomenon are as
environments (Falkowski et al., 2008). DO sources in wastewater mainly follows: (1) nutrients (N and P) were obviously reduced by extreme
include three pathways: (1) oxygen transfers from air to water surface precipitation on the 11th day, which may inhibit the growth; (2) the
(water reoxygenation), (2) oxygen from wet deposition, runoff and growth rates could be reduced during the later stage of the experiment
subsurface flows, (3) root-excreted oxygen by aquatic plants (Qin et al., because of limited space in the cuboid box; (3) the photosynthetic ac­
2016b; Sanchez-Olivares et al., 2019). In this study, the rainfall events tivity might be inhibited by dust adsorbed on the leaf surface due to
contributed the most to DO increasing in the influents based on the atmospheric deposition while extreme precipitation could rinse the
second pathway. DO in water was dependent on the balance of oxygen leaves and increase the growth rate consequently. The underlying
influx and consumption which caused by respiration or aerobic mechanisms need to be explored by further studies.
micro-biodegradation (Qin et al., 2016b). Although oxygen is known to The approaches to remove NHþ 4 -N from contaminants in water-
be released from many aquatic plant roots (Stottmeister et al., 2003; medium mainly included plant absorption, sediment adsorption, NH3
Matsui and Tsuchiya, 2006; Dong et al., 2011), including water hya­ volatilization and nitrification (Sricoth et al., 2018). In this study, the
cinths (Valipour et al., 2015), DO concentrations can also be decreased contribution of volatilization to ammonia loss will have been small,
by water hyacinths in wastewater (Villamagna and Murphy, 2010; Qin because the volatilization of NHþ 4 -N is not significant at low pH (Mayo
et al., 2016a). Due to nitrification, nitrogenous compounds can be and Hanai, 2017; Yang et al., 2020b). Furthermore, 4.3 mg oxygen is
drivers of oxygen depletion in wastewater (Rockstro €m et al., 2009; required to completely convert 1.0 mg NHþ 4 -N to NO3 -N, so anaerobic
Qiang et al., 2020), and hence, the low DO concentrations in the high conditions limited the nitrification in boxes. Anammox oxidation has
flow rate boxes in this study might have been the result of high con­ been considered as a new pathway for NHþ 4 -N removal (Robertson et al.,
centrations of nitrogen-compounds running through the fabrications. 2012), which is a short-cut and cost-effective process in the nitrogen
High oxygen consumption caused by the high wastewater inflow with removal by directly converting NHþ 4 -N to N2 (Kartal et al., 2013), and
many aerobic microorganisms, may be another reason for the decrease has been recognized as an efficient alternative to the
of DO in most effluents. Water hyacinth mats in high flow rate fabri­ nitrification-denitrification process (Ma et al., 2016; Yang et al., 2020a).
cation could prevent water reoxygenation on a larger scale. In the lowest However, this process requires strict anaerobic conditions, which was
flow rate box (2 m3 d 1) reoxygenation was better: DO concentration not the case in this study. Therefore, most of the NHþ 4 -N in the high flow
showed an increasing trend, especially during the recovery stage after rate treatments is most likely removed by plant absorption, while in the
precipitation. lowest flow rate treatment (2 m3 d 1), nitrification might have been
Oxic-anoxic regime shifts may induce the changes between nitrifi­ mainly responsible for ammonia removal as DO in this treatment was
cation and denitrification (Khardenavis et al., 2007; He et al., 2016), higher, particularly after the extreme rainfall event.
which are mediated by shifts in the microbial community composition. Not only inorganic forms of nitrogen can be taken up by plants, but
Nitrogen in urban wastewater is usually present as organic nitrogen, also organic forms, such as amino acids, small peptides and proteins
ammonium, and nitrate (San-Martín et al., 2018), which was also (Na€sholm et al., 2009; Tegeder and Rentsch, 2010). However, it is
observed in present study. In BP and RP stages, ammonia was the main difficult to remove low-molecular weight and hydrophilic DON by
inorganic nitrogen compound with average DO concentrations below 1 physical and chemical treatment processes in WWTP’s (Pehlivanoglu-­
mg L 1. Once oxygen increased in the water due to wet deposition or Mantas and Sedlak, 2008). With the prospects of increased precipitation

7
H. Qin et al. Journal of Environmental Management 271 (2020) 110948

and surface runoff as a result of global warming, a further increase of CRediT authorship contribution statement
organic matter to the waters can be expected (Vaquer-Sunyer et al.,
2015). Hongjie Qin: Conceptualization, Writing - original draft, Method­
To address the issues on bioavailability and ecological significance of ology, Visualization, Investigation, Funding acquisition. Muhe Diao:
DON, numerous studies have been conducted in freshwater (Lusk and Software, Writing - review & editing, Formal analysis. Zhiyong Zhang:
Toor, 2016) and marine ecosystems (Letscher et al., 2013). Both inor­ Project administration. Petra M. Visser: Writing - review & editing,
ganic and organic nitrogen can significantly affect the nitrogen use ef­ Formal analysis. Yingying Zhang: Investigation. Yan Wang: Investi­
ficiency (NUE) and productivity of plants. In particular, NUE will gation. Shaohua Yan: Conceptualization.
increase with the increasing availability of organic nitrogen relative to
inorganic nitrogen (Franklin et al., 2017). Previous studies suggested Acknowledgements
that more than 87% of cyanobacterial nitrogen could be assimilated by
water hyacinths (Qin et al., 2017). In this study, over 99% DON could be This study was supported by National Natural Science Foundation of
removed after the extreme rainfall event which indicated that water China (Grant No. 41877510 and No. 41501545), National Science and
hyacinths could absorb or transfer DON very efficiently. Technology Major Project of Water Pollution Control and Treatment
Besides N, excess phosphorus (P) concentration is another primary (2017ZX07202004-007), Natural Science Foundation of Jiangsu Prov­
cause for eutrophication (Conley et al., 2009). To prevent the increasing ince, China (Grant No. BK20150549) and Key Laboratory for Agricul­
P in wastewater, European Commission Directive 98/15/EEC requires tural Environment, Ministry of Agriculture, China (Grant No.
that TP in the water discharged from urban WWTP’s to sensitive areas at KLAE201602).
a high risk of eutrophication should not exceed 1.0 mg P⋅L 1. Kumar and
Deswal (2020) investigated phytoremediation capabilities of four Appendix A. Supplementary data
floating aquatic plants on P removal from rice mill wastewater and
suggested that water hyacinth showed an evident higher removal effi­ Supplementary data to this article can be found online at https://doi.
ciency than duckweed and salvinia, but slightly lower than water let­ org/10.1016/j.jenvman.2020.110948.
tuce. Moreover, free-floating macrophyte Eichhornia crassipes (water
hyacinth) was more efficient on P removal than emergent macrophyte
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