Zhang2021 Article BioretentionForRemovalOfNitrog

Download as pdf or txt
Download as pdf or txt
You are on page 1of 17

Environmental Science and Pollution Research (2021) 28:10519–10535

https://doi.org/10.1007/s11356-020-12319-1

REVIEW ARTICLE

Bioretention for removal of nitrogen: processes, operational


conditions, and strategies for improvement
Hongwei Zhang 1 & Zulfiqar Ahmad 1 & Yalu Shao 1 & Zhonghua Yang 1 & Yufei Jia 1 & Hua Zhong 1

Received: 4 October 2020 / Accepted: 30 December 2020 / Published online: 14 January 2021
# The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021

Abstract
As one of the low-impact development measures, bioretention plays an important role in reducing the runoff peak flow and
minimizing runoff pollutants, such as heavy metals, suspended solids, and nutrients. However, the efficiency of nitrogen removal
in the bioretention system is unstable, owing to the different chemical properties of various forms of nitrogen and the limitations
of current bioretention system for nitrogen transformation. This review article summarizes the recent advances in bioretention
system in treatment of urban stormwater and agricultural runoff for nitrogen removal. The microbial characteristics and main
processes of nitrogen transformation in bioretention are reviewed. The operational conditions affecting nitrogen removal, in-
cluding climatic conditions, pH, wet-dry alternation, influent loads and nitrogen concentration, and hydraulic residence time are
discussed. Finally, measures or strategies for increasing nitrogen removal efficiency are proposed from the perspectives of
structural improvement of the bioretention system, optimization of medium composition, and enhancement of the nitrogen
removal reaction processes.

Keywords Stormwater runoff . Agricultural runoff . Bioretention . Nitrogen removal . Biotransformation . Denitrification

Introduction stormwater management measures, LID practices seek to pre-


serve pre-development hydrology conditions (Dietz 2007). It
With urbanization, a large number of natural green spaces is an approach that uses nature to manage surface runoff by
have been replaced by impervious surfaces, which not only emphasizing on-site water management, which can promote
contributes to the increase of stormwater runoff and flood natural storage, infiltration, and purification (Zhu et al. 2019).
peak flow (Jennings and Jarnagin 2002) but also the increase With the development of industry and agriculture, the problem
of pollutants in the runoff (Davis 2008). As a result, early of runoff pollutant removal has drawn growing attention,
urban stormwater runoff has become one of the primary pol- which is the main focus of the LID research in recent years
lution sources of surface receiving water bodies (USEPA (Houle et al. 2013).
2000; Davis and Birch 2009; Novotny 2010). The urban Nitrogen contamination has caused degradation of aquatic
stormwater runoff contains heavy metals, suspended solids, ecosystems around the world in recent decades and attracted
petroleum hydrocarbons, pathogen, salts, and nutrients such great attention (Howarth 2008). Control of point source of
as nitrogen and phosphorus, which needs to be focused on nitrogen has been a major focus of environmental regulatory
(Burton Jr. and Pitt 2001). As a novel runoff management agencies and resulted in strict regulations for wastewater treat-
technology, low-impact development (LID) was proposed in ment (USEPA 2000). In recent years, however, pollution from
Maryland in the 1980s. In contrast to the traditional stormwater runoff with non-point source characteristics has
caused increasing concern due to its significant impact on
Responsible editor: Philippe Garrigues surface water quality (Davis et al. 2006). Use of fertilizers
on urban vegetation, emission of automobile exhaust, deposi-
* Hua Zhong tion of atmosphere, and occurrence of animal wastes will re-
zhonghua21cn@126.com
sult in accumulation of nitrogen in the surface pavements. The
1
State Key Laboratory of Water Resources and Hydropower
increase of impervious areas in cities allows nitrogen in
Engineering Science, Wuhan University, Wuhan 430072, Hubei, stormwater runoff to be transported rapidly to receiving water
China bodies during rainfall events, which results in regional water
10520 Environ Sci Pollut Res (2021) 28:10519–10535

quality problems (Hsieh et al. 2007; Elliott et al. 2007; Osman et al. (2019) reviewed on bioretention for nitrogen
Davidson et al. 2010). With the rapid development of agricul- removal from urban stormwater with a focus on the perfor-
ture, the increasing grain output has met the growing demand mance of nitrogen transformation and design of the
of humans. However, the increase of fertilizer input leads to bioretention system. However, this is not enough for a full
the increasing proportion of nutrients transported from farm- and comprehensive understanding of such a method for nitro-
land to receiving water bodies, which threatens the quality of gen removal since the types of the treated runoff, the micro-
receiving water and human health (Ongley et al. 2010). organisms, and the operational conditions also have a great
Rainfall runoff is the main power to form and carry agricul- impact on the bioretention. The present review, in contrast, is
tural non-point source pollution. Generally, about half of ni- not only focused on urban stormwater but also on agricultural
trogen fertilizer is absorbed by crops, with the rest transferred runoff, which is different from the urban stormwater in terms
into the receiving waters through agricultural runoff, especial- of the types and loads of nitrogen contaminants and configu-
ly in the form of nitrate (Lupwayi et al. 2012). Therefore, the rations of bioretention system. In addition, this review inves-
reduction of nitrogen loads from such agricultural non-point tigates the nitrogen removal in bioretention from the perspec-
sources is also crucial for protection of the aquatic ecosystems tives of microbial characteristics and the operational condi-
(Ergas et al. 2009; Yang et al. 2010). tions and finally proposes the strategies for nitrogen removal
Bioretention system, also known as biofiltration or from the perspectives of structural improvement of the
stormwater biofilters, originated in the 1990s, is one of the bioretention system, optimization of medium composition,
LID techniques to combat the impacts of runoff pollution and enhancement of the nitrogen removal reaction processes.
(Coffman et al. 1994). Bioretention is a plant/soil/microbes-
based system that is widely used because of its ability to im-
prove water quality and hydrologic condition of the developed Bioretention design characteristics
landscape. The water quality can be improved through filtra-
tion, adsorption, plant uptake, biotransformation, and several Bioretention for urban stormwater runoff
other unknown naturally occurring mechanisms in
bioretention system. The bioretention cells are effective in Urban storm runoff contains various forms of nitrogen, in-
reducing the surface runoff and in removal of many pollutants, cluding organic, inorganic, particulate, and dissolved
such as heavy metals, oil and grease, and total suspended nitrogen. Therefore, it is particularly important to consider
solids (Davis et al. 2001; Hsieh and Davis 2005a; Houle the composition and proportion of nitrogen contaminants in
et al. 2013). The removal efficiency for nitrogen through stormwater runoff before designing the bioretention system.
bioretention system, however, is not very ideal due to the Pitt et al. (2004) collected and evaluated the representative
different chemical properties of various forms of nitrogen stormwater runoff data from 66 agencies and municipalities
and high mobility of nitrate in soil (Fan et al. 2019). Some from 17 states of the USA, and it was observed that the pro-
previous studies on nitrogen removal through bioretention portion of various forms of nitrogen was different with differ-
system and their efficiencies are summarized in Table 1. The ent land types and dissolved inorganic nitrogen (DIN)
efficiencies of bioretention system ranged from − 477 to 87% accounted for approximately 50% of the TN in general.
for nitrate removal and − 32.9 to 90% for total nitrogen (TN) Similarly, Taylor et al. (2005) characterized the composition
removal, showing great variance. As shown in Table 1, the of nitrogen in urban stormwater from different monitoring
efficiencies of bioretention system for nitrogen removal de- sites in Australia and found that half of the nitrogen contam-
pend on many factors, including the bioretention configura- inants was DIN. And it was also observed that the nitrogen
tions and operational conditions, which affect the activities of mainly existed in the dissolved state (accounting for about
microbes and nitrogen removal processes. The packing medi- 80%) rather than particulate nitrogen. The particulate nitrogen
um for bioretention is critical for pollution removal. Basically, in the urban runoff is predominantly in the form of organic
it contains more than half of the sand to keep good permeabil- nitrogen (Harris et al. 1996). Generally, the bioretention sys-
ity and a stable operation condition, while the other packing tem can effectively remove the particulate organic nitrogen
materials have different effects on nitrogen removal. For in- (PON) based on soil infiltration (Li and Davis 2014).
stance, woodchips, newspaper, and biochar are beneficial for Therefore, the removal of dissolved nitrogen is the main focus
nitrogen removal, while only the mixture of sand and soil of the bioretention research for urban stormwater runoff.
performs poor. In addition, the ability of pollutant removal Bioretention for the treatment of urban stormwater runoff
also depends on the regions of the bioretention, due to the needs to be able to cope with large runoff loads and a vege-
different climatic conditions, contaminant loads, and the soil tated impoundment area at the top is important for such a
properties. The use of plants at the surface and the structural function. Stormwater is directed to the surface impoundment
optimization of the bioretention also promote the overall effi- area of bioretention during the rainfall events, where it pools
ciency for nitrogen removal (Wang et al. 2017b). Recently, (typically 15 to 30 cm) and infiltrates, above which a
Table 1 A summary of nitrogen removal efficiency of bioretention

Experiment method Regions NOx-N (mg/L) NH3-N (mg/ TKN (mg/ TN (mg/L) Bioretention system characteristics Reference
L) L)

Cin R (%) Cin R (%) Cin R Cin R (%)


(%)

Column experiment Xi’an, China 8 68–80 8 78–90 — — 16 85–90 120.5-cm medium; 25.5-cm ponding layer; 10-cm mulch l (Xiong et al. 2019)
ayer; 70-cm mixture layer (88% sand and 12% soil by
mass); 15-cm gravel drainage layer
Column experiment Xi’an, China 6 26–60 3 59–81 — — 9 36–67 105-cm medium; 15-cm ponding layer; 70-cm mixture layer (Jiang et al. 2019)
(30% soil, 65% river sand and 5% wood chips by mass);
20-cm gravel drainage layer
Environ Sci Pollut Res (2021) 28:10519–10535

Column experiment TX, USA 0.8 − 35.4 — — — — 1.39 − 101.6-cm medium; 61-cm filter layer of limestone sand; (Hamedani et al. 2019)
32- 25.4-cm drainage layer
.9
In situ experiment Hefei, China 2 32.1 4 82.9 — — 8 68.1 105-cm medium with plants; 7-cm ponding layer; 70-cm (Singh et al. 2019)
mixture layer (50% coarse sand, 33.3% original soil, and
16.7% wood chips); 15 cm gravel drainage layer
Pilot-scale Brisbane, 9–14 87 56–76 79 — — 101–131 79 98-cm medium (68% sand, 12% coir peat and 20% biochar (De Rozari et al. 2018)
experiment Australia by mass) with plants
In situ experiment NC, USA 0.13 − 97 — — 1.08 43 1.17 33 50-cm sandy loam medium with a tree on surface (Smolek et al. 2018)
Column experiment Shenzhen, China 2.5 − 23–27 2.5 80 — — 10 17–53 62-cm medium with plants; 50-cm mulch/soil layer; (Wang et al. 2018a)
12-cm sand layer
Column experiment Shenzhen, China 2.5 47–77 2.5 80 — — 10 68–78 122-cm medium with plants; 50-cm mulch/soil layer; 12-cm (Wang et al. 2018a)
sand layer; 60-cm saturated zone with gravel and newspaper
In situ experiment Shanghai, China 1.10 19 0.58 47 — — 4.11 34 125-cm medium with plants; 5-cm mulch layer; 95-cm mixture (Wan et al. 2018)
layer (80% sand, 15% soil, and 5% wood chips by mass);
25-cm drainage layer
In situ experiment Xi’an, China 6 42.3 3 64.6 — — 9 50.7 105-cm medium with plants; 15-cm ponding depth; 5-cm pine (Jiang et al. 2018)
bark mulch; 70-cm silt loam layer; 15-cm gravel layer
In situ experiment Singapore 0.89 3.2 0.48 10 1.25 37 2.45 25 105-cm medium; 10-cm ponding depth; 40-cm sandy loam layer; (Wang et al. 2017a)
40-cm rock and wood chip anaerobic zone; 15-cm drainage layer
Column experiment Chongqing, 2.66 74.2 1.50 90.2 — — 4.81 62.6 80-cm medium with plants; 20-cm ponding depth; 40-cm mixture (Wang et al. 2017b)
China layer (20% soil and 80% sand by volume); 20-cm drainage layer
In situ experiment Wuhan, China 1.2 16.7 0.8 86 — — 2.0 34 105-cm medium; 70-cm mixture layer (85% sandy loam and 15% (Zhou et al. 2017)
sediment from lake); 35-cm drainage layer
In situ experiment Xi’an, China 0.70 − 3.3 0.95 − 1.9 — — 2.68 − 4.7 135-cm medium with plants; 5-cm aquifer; 60-cm planting soil l (Jiang et al. 2017)
ayer; 20-cm slag filler layer; 50-cm gravel layer
In situ experiment FL, USA 1.07 78.5 1.53 82.4 — — 2.07 72.5 125-cm medium; 30-cm ponding depth; 30-cm sand layer; (Peterson 2016)
30-cm pea gravel and wood chips layer; 5-cm impervious
liner; 30-cm stone drainage layer
Column experiment Shanghai, China 2.29 1 2.58 71 — — 7.47 41 110-cm medium; 5-cm gravel mulch layer; 80-cm soil layer; 10-cm drain- (Tang and Li 2016)
age layer
Column experiment Shanghai, China 2.29 84 2.58 83 — — 7.47 82 115-cm medium; 40-cm planting soil layer; 35-cm (Tang and Li 2016)
sand layer; 10-cm less permeable soil layer
10521
Table 1 (continued)
10522

Experiment method Regions NOx-N (mg/L) NH3-N (mg/ TKN (mg/ TN (mg/L) Bioretention system characteristics Reference
L) L)

Cin R (%) Cin R (%) Cin R Cin R (%)


(%)

In situ experiment MD, USA 0.3 − 120 0.15 > — — 1.62 4.3 60-cm loamy sand medium with plants on surface (Li and Davis 2014)
66-
.7
In situ experiment KS, USA 1.11 43 0.54 72 — — 1.33 20 71-cm medium (50% sand, 20% shredded hard wood mulch, (Chen et al. 2013)
and 30% sandy loam soil) with plants on surface
In situ experiment NC, USA 0.19 − 209 0.29 82 0.45 8 0.94 21 60-cm medium (86–89% sand, 8–10% silt, and 3–4% clay) (Brown and Hunt
with shrubs and trees 2011)
In situ experiment NC, USA 0.19 − 477 0.29 74 0.45 2 0.94 75 90-cm medium (86–89% sand, 8–10% silt, and 3–4% clay) (Brown and Hunt
with shrubs and trees 2011)
In situ experiment NC, USA 0.42 33 0.34 70 1.11 49 1.66 54 60-cm loamy clay medium with Bermuda grass on surface; (Passeport et al. 2009)
45-cm saturated zone
In situ experiment NC, USA 0.42 8 0.34 84 1.11 59 1.66 54 90-cm sandy loam medium with grass on surface; (Passeport et al. 2009)
75-cm saturated zone
In situ experiment NC, USA 0.41 4.9 0.34 70.6 1.26 44.4 1.68 32.1 120-cm loamy sand medium with vegetations on surface (Hunt et al. 2008)
Column experiment MD, USA 2 −41-23 2 52–84 — — — — 110-cm medium; 20-cm mulch/soil layer; 75-cm sand layer; (Hsieh et al. 2007)
15-cm drainage layer
Column experiment MD, USA 2 − 76–(− 2 6–18 — — — — 110-cm medium; 30-cm mixture media (25% mulch, 25% (Hsieh et al. 2007)
32) soil and 50% sand by mass); 55-cm sand layer; 10-cm
soil layer; 15-cm drainage layer
Column experiment MD, USA 2 − 64–19 2 2–23 — — — — 110-cm medium; 15-cm ponding depth; 5-cm mulch layer; (Hsieh and Davis
15-cm sandy loam layer; 75-cm sand layer 2005b)
Environ Sci Pollut Res (2021) 28:10519–10535
Environ Sci Pollut Res (2021) 28:10519–10535 10523

vegetated buffer strip combined with a 5 to 8 cm hardwood pollutants are recommended for agricultural runoff. It has
mulch is often laid to maintain soil moisture and filter PON shown that grassed swales have a good effect on removing
(Davis et al. 2006; Wan et al. 2018). Native plants with denser total suspended solid (TSS) and prolonging the retention time
and fine roots are often planted on the surface of the soil layer, of agricultural runoff, which can be adopted as an ideal pre-
which have particular functions in the bioretention system treatment method in bioretention system for agricultural run-
(Read et al. 2009). Plants can slow down the velocity of runoff off (Zhao et al. 2016). In addition, for the stable operation of
entering the retention compartment, maintain the permeability the system, the application of pretreatment sedimentation
of the soil media via the root growth, prevent clogging of the pools will also be beneficial to help retain particulate matters
soil layer, and enhance infiltration of rainwater, which is cru- and prolong the life of the bioretention (Ergas et al. 2010;
cial for the stable operation of the bioretention for urban Dietz 2016). The proportion of the catchment area can be
stormwater runoff (Hunt et al. 2012; Le Coustumer et al. increased in bioretention for agricultural runoff owing to the
2012; Muerdter et al. 2016). Plant roots can directly absorb lower level of land exploitation and utilization than those in
and assimilate DIN and the roots of the plants contribute to the urban areas, which can reduce the runoff loads in the single
enrichment of microorganisms, which play an important role rainfall process and improve the treatment efficiency. In order
in nutrient removal and organic matter degradation to remove high concentrations of nitrate, it is effective to use
(Masclaux-Daubresse et al. 2010). the solid carbon sources, such as woodchips and newspaper to
The filter media is a crucial part of the stormwater strengthen the denitrification, which can achieve high nitrate
bioretention, which should provide adequate permeability to removal efficiency (more than 80%) under typical loading
handle large runoff volumes directed from impervious areas rates of fertilized fields (Peterson et al. 2015).
and in the meantime reduce pollutant levels and support plant
growth. The hydraulic conductivity of the packing media pri-
marily depends on the size of conducting pores and larger Nitrogen transformation and microbial
pores conduct runoff more rapidly. A sandy media is favored characteristics in bioretention
for water conduction and high clay contents can be detrimen-
tal to infiltration (Hsieh and Davis 2005a). It is suggested to The main processes of nitrogen treatment and transformation
use sandy loam as medium with a 75 to 120 cm deep to in bioretention system include the following: (1) PON sedi-
remove nitrogen in urban stormwater runoff (Davis et al. mentation/filtration, (2) mineralization of the organic nitro-
2006; Bratieres et al. 2008). In order to improve nitrate remov- gen, (3) NH4+-N fixation (ion exchange), (4) microbial nitro-
al efficiency, either incorporating a continuously submerged gen uptake, and (5) microbial nitrogen transformation (i.e.,
anoxic zone with an overdrain or placing a less permeable soil nitrification and denitrification) (Collins et al. 2010). The fates
layer in the bottom can be applied (Kim et al. 2003; Hsieh of nitrogen in the bioretention system have been depicted in
et al. 2007). Fig. 1.
There are some transformation and removal processes of
Bioretention for agricultural runoff organic and inorganic nitrogen in the upper layer of the
bioretention under aerobic conditions. PON can be removed
Compared with urban runoff, the volume of agricultural run- by soil filtration, and dissolved organic nitrogen (DON) in
off produced in feedlots and dairy farms is similar to that of stormwater runoff can be transformed into ammonia nitrogen
urban area (Miller et al. 2004). However, although the local (NH4+) through microbial mineralization. NH4+ can be
hydrology of agricultural regions can resemble urban areas, adsorbed by negatively charged soil colloidal particles or soil
farming-related activities such as manure treatment and feed organic matters. In addition, plants on the surface of the
transportation can significantly contribute to higher concen- bioretention can absorb and assimilate inorganic nitrogen,
trations of nutrients and sediment than in urban stormwater mainly including NH4+ and NO3−. Assimilation is a process
(Young et al. 1980). In addition, due to agricultural activities in which microorganisms convert NH4+ or NOx− into micro-
in the watershed of the bioretention, there will be heavy load- bial cell mass or plant biomass, where it is temporarily stored
ing of particulate matters carried into the system along with as organic nitrogen (Tyler 1978). Another way to remove
the runoff, which may accumulate on the surface of the NH4+ from the bioretention system is microbial nitrification,
bioretention, blocking the system and reducing the permeabil- for which NH4+ is first converted to NO2− and subsequently to
ity capacity (Dietz 2016). NO3− under the aerobic condition. The above nitrogen trans-
In contrast to the bioretention for urban stormwater runoff, formation processes basically take place in the upper layer
the focus for the structural design of the bioretention for agri- with an aerobic condition in the bioretention system (Kim
cultural runoff is on the treatment of the particulate pollutants et al. 2003). While the uptake of nitrogen via assimilation by
and the removal of fertilizer nutrients, especially nitrate. microbes or by adsorption results in the temporary nitrogen
Pretreatment facilities for preliminary removal of these removal rather than permanent removal, which may have the
10524 Environ Sci Pollut Res (2021) 28:10519–10535

Fig. 1 Fates of nitrogen in bioretention system

potential of back release with the change of conditions their fates in the bioretention. It was found that the annual
(Collins et al. 2010). input of PON, DON, NH4+, or NOx− were 8.04, 2.18, 1.30,
In contrast to NH4+, NOx− is negatively charged and cannot and 2.57 kg/ha-year, respectively. And 16.8% of PON was
be absorbed by soil particles, so it has high mobility in removed by soil filtration, and 66.2% was transformed into
bioretention system and is easy to leach out along with rainfall DON. Only about 28.7% of DON was transformed into NH4+
events (Kang et al. 2009). Nitrate is removed permanently through ammonification, and others were leaching out. It had
through denitrification in the bioretention system, and N2 is a high removal efficiency (93.0%) to remove NH4+ by nitrifi-
the final product of microbial denitrification. Denitrification cation. However, the NOx− could not be efficiently removed
occurs under anoxic or anaerobic conditions, and it requires due to the lack of the appropriate condition for denitrification.
substrates, such as organic carbon source, sulfur, or iron, as Fan et al. (2019) have studied the nitrogen transformation
the electron donor to drive the reaction (Collins et al. 2010). process and established nitrogen balance model of
The denitrification process significantly affects the overall ni- bioretention system with submerged layer; it was found that
trogen removal in the bioretention; however, the denitrifica- the input of the TN, NH4+, and NO3− were 170.10, 68.96, and
tion process is often limited due to lack of proper conditions in 98.61 mg, respectively; 35.79, 43.97, and 36.62% of TN,
the bioretention system. Recent studies show that the effec- NH4+, and NO3− were retained in the bioretention; 60.24,
tiveness of the bioretention system can often be improved by 55.15, and 57.03% of TN, NH4+, and NO3− were removed;
optimizing operating conditions and factors influencing the and 3.97, 0.88, and 6.34% of TN, NH4+, and NO3− leached
denitrification process, such as the use of the carbon sources out of the bioretention system, respectively. In conclusion, the
and the construct of the saturated zone at the bottom of the NH4+ can be removed effectively by the bioretention system;
bioretention (Kaushal et al. 2008; Klocker et al. 2009). This however, the NO3− removal and nitrogen transformation pro-
will be discussed in detail in the following sections. cess will be affected significantly by the operational condition
Dissimilatory nitrate reduction to ammonium (DNRA) is a of the bioretention system.
microbial reaction reducing NO3− to NO2− to NH4+ (Tiedje Microbes play an essential role in nitrogen removal in
et al. 1983), which is a part of NOx− removal in the temperate bioretention. It has been found that the top layer of the medi-
and humid soil environment (Silver et al. 2001; Templer et al. um contains higher abundance and activity of denitrifiers, de-
2008). The optimum condition for DNRA is similar to that of spite that longer periods of saturation and the presence of
denitrification (Sgouridis et al. 2011); however, it is not con- saturated zones, which are beneficial for the enrichment of
tributive to the nitrogen removal in the bioretention since the the denitrifiers, are in deeper portions of the medium (Chen
nitrogen in NOx− is not removed but converted to NH4+, et al. 2013; Liu et al. 2014b; Waller et al. 2018). This is
which stays in the bioretention system. probably due to the degradation of plants and the accumula-
Li and Davis (2014) have conducted the quantitative anal- tion of particulate organic matters in the upper layer of the
ysis about the nitrogen composition in stormwater runoff and bioretention (Chen et al. 2013; Liu et al. 2014b; Waller et al.
Environ Sci Pollut Res (2021) 28:10519–10535 10525

2018). Although there are fewer population of bacteria in the vegetation cover, and the improvement of configuration to
saturated layer at the bottom of the bioretention, the overall enhance the hydraulic residence time.
percentage of denitrifiers within the population is higher Hydrological condition is another important climatic factor
(Willard et al. 2017). The anoxic or anaerobic conditions in that affects nitrogen removal efficiency. The permeability of
the saturated zone at the bottom are more suitable for denitri- the bioretention system in tropical regions should be better
fication to occur; however, the low carbon content within the than in other regions to cope with frequent and heavy rainfall,
saturated zone presents a less optimal environment for the and the use of mulch as well as the submerged zone is not
growth of denitrifiers. There are more denitrifying bacteria recommended in tropical regions (Goh et al. 2019). Therefore,
in the medium with low sand content (i.e., higher organic the application of healthy tropical shrubs with well-developed
matter content), while these characteristics are prone to result thick roots is proposed to ensure the effectiveness of the
in compaction and clogging and have shown to leach DON bioretention in the tropical zone, which can slow down the
from soil (Waller et al. 2018). Therefore, it is a more feasible horizontal flow, maintain a reasonable infiltration rate, and
option to construct bioretention with high proportion sand in the meantime improve nitrogen removal (Goh et al.
media and substrates favorable for denitrification, which is 2017). The nitrogen removal efficiency of bioretention system
beneficial for promoting infiltration and improving microbial in cold regions is low compared to warm regions. Inadequate
abundance and activity. nitrogen removal and nitrogen leaching is frequently observed
during the cold seasons in the bioretention system (Blecken
et al. 2010; Li et al. 2012; Kratky et al. 2017). The main reason
is that the low temperature reduces the microbial activity for
Operational conditions affecting nitrogen denitrification. Another reason is the ice blockages of soil
removal pores as well as settlement and subsequent release of nitroge-
nous contaminants from snow (Sansalone and Glenn 2002). In
Climatic conditions addition, plant dormancy and the de-icing agents, such as salts
will have an impact on plant health as well as the nitrogen
Climatic condition is one of the key factors affecting nitrogen removal efficiency (Denich and Bradford 2009; Li et al.
removal efficiency in bioretention system. The climatic con- 2012). It has been found that the bioretention in semi-arid
ditions are different across various regions where tropic areas regions with the vegetation adapted to the dry condition can-
receive frequent, short, and intense rainfalls, temperate re- not retain as much TN as the bioretention in wet regions since
gions face prolonged dry period and seasonal winter, and frig- plants require sufficient water for nitrogen assimilation and
id zones experience a long period of low temperature and denitrifiers require an anoxic condition for best performance
snowfall (Geheniau et al. 2015; Wang et al. 2017a). A critical (Houdeshel et al. 2015). Low microbial activity is one of the
effect of seasonal and climatic variables on nitrogen removal most important limitations of bioretention in semi-arid re-
is temperature change, which has a significant influence on gions. Therefore, it may be useful to increase the density of
microbial growth and nitrification/denitrification processes in plants on top of the bioretention to enrich the microbes and
bioretention system (Volokita et al. 1996; Foglar et al. 2005). improve nitrogen uptake in semi-arid areas. TN removal in the
Denitrification efficiency increases with the increase of tem- bioretention system also depends on the type of the nitrogen
perature within a proper range. It was observed that the re- species. For example, the efficiency of PON removal via fil-
moval efficiencies for nitrate were 8.0, 20.9, and 45.8%, re- tration is not affected by the cold climate, while the removal of
spectively, when the temperatures were 10, 23, and 28 °C in the dissolved nitrogen decreases significantly in low-
column experiments using soil as the packing material (Chang temperature regions (Kratky et al. 2017).
et al. 2011). This is because temperature has a significant
impact on the growth of nitrifying and denitrifying bacteria pH
and their enzymatic activities during nitrification and denitri-
fication processes. It was reported that the optimal tempera- Nitrogen removal processes in bioretention are heavily affect-
ture for denitrifying bacteria to grow and remove nitrate was ed by pH of the water for treatment. Many researchers have
between 28 and 30 °C (Yang et al. 2011; Chen et al. 2012) and found optimum pH value for denitrification is between the 7.5
nitrifiers could grow best at around 30 °C. Temperature is also and 8.0, and too high or too low water pH values are both
an important factor affecting the plant growth and the nutrient unfavorable for denitrification (Prakasam and Loehr 1972;
uptake by plants, which affects the nitrogen removal indirect- Thomas et al. 1994). It was demonstrated that denitrification
ly. Therefore, for improving nitrogen removal, specific mod- in bioretention system was significantly inhibited when the
ifications should be considered to design the bioretention sys- pH was less than 6.5 (Glass et al. 1997; Li et al. 2008). The
tem in cold environments, such as the application of solid optimum pH for nitrification was between 7.5 and 8.0, and
carbon sources to enhance microbial activity, the use of hardy nitrification was significantly inhibited when the pH was less
10526 Environ Sci Pollut Res (2021) 28:10519–10535

than 6.0 (Keen 1984; Hossain et al. 2010). It was shown that also have significant influence on nitrogen removal.
denitrification occurred at pH from 7.5 to 9.0, while nitrite Stormwater from intensive land use could be polluted more
accumulation increased with an increase in pH (Glass and seriously than from natural areas. The intensity of the
Silverstein 1998). With the increase in pH, nitrite accumula- stormwater can affect runoff water quality and a higher rainfall
tion becomes serious because pH affects the activity of nitrate intensity can generate more polluted stormwater to
and nitrite reductases at different degrees, and the inhibition of bioretention basin (Davis et al. 2009). Lower influent loads
nitrite reductase is more significant at higher pH. can promote matrix flow conditions that enhance TN attenu-
ation and treatment (Bratieres et al. 2008; Le Coustumer et al.
Wet-dry alternation 2009). The link between influent loads and nitrogen reduction
performance of bioretention system is strong, and low influent
Alternate wet and drought is one of the essential features of the volumes allow for more stormwater being intercepted and
bioretention system and it is of particular importance to ex- retained, leading to increased soil-water contact which is ben-
plore the effect of the wet-dry alternation on nitrogen removal eficial for higher sorption and biological uptake processes
efficiency of bioretention system. Wet-dry cycles will influ- (Davis et al. 2009; Laurenson et al. 2013). High influent loads
ence the soil moisture content, which in turn has an impact on will lead to much of the inflow passing the bioretention sys-
denitrification. A large number of studies have demonstrated tem as overflow or preferential flow, which significantly af-
that rewetting can lead to the release of nutrients containing fects the chemical and biological reactions for nitrogen re-
nitrogen and phosphorus in the soil after a long-term drying moval (Trowsdale and Simcock 2011). Since systems with
period (West et al. 1992; Cabrera 1993; Baldwin and Mitchell lower influent loads usually have a better TN removal effi-
2000). Leach-out of nitrate along with the rainwater in ciency, it is recommended to maximize the area of the
bioretention system has been frequently reported when the bioretention system relative to its catchment area to reduce
system is rewetted (Davis et al. 2006; Hatt et al. 2007). the influent loads.
There are several reasons for such nitrogen release. The rate Influent nitrogen concentration, which is directly related to
of mineralization of organic nitrogen in dry and aerated soils is the loads of nitrogen pollutants to the bioretention system, also
high, which leads to the increase in inorganic nitrogen con- has an impact on nitrogen removal efficiency. It was demon-
tents in the soil (Updegraff et al. 1995; Bridgham et al. 1998; strated that the TN removal efficiency was higher under the
Venterink et al. 2002). In addition, desiccation caused by air low inflow nitrogen concentration than the high concentration
drying can lead to microbial death and chemicals containing (Liu et al. 2014a; De Rozari et al. 2018). It was demonstrated
nitrogen will be released from the killed bacteria (Sparling and in a pilot-scale experiment that low concentration of nitrogen
Ross 1988; Scholz et al. 2010). Finally, as the bioretention contaminants and flow volumes resulted in strong removal of
system undergoes drying period, the denitrification efficiency NH4+ and moderate DON reduction (Hatt et al. 2009). NO3−
decreases, and it may lead to the accumulation of nitrate, concentration in the effluent was observed to increase linearly
which has high solubility and mobility. with increasing influent TN concentration in an urban
Although prolonged drying period impairs the denitrifica- stormwater bioretention system composed of 0.6-m topsoil
tion function of bioretention system, only one or two rainfall and 0.6-m expanded shale (Houdeshel et al. 2015).
events can restore the function of the system, even if the dry- Similarly, the removal efficiency of nitrogen contaminants
ing period lasts for 3 weeks (Zinger et al. 2007). Furthermore, was reduced with the increase in influent concentration when
rewetting of dried soils may enhance soil respiration and mi- the influent loads and the media thickness were the same in a
crobial activity, which ultimately results in enhanced denitri- 1.05-m bioretention composed of mixed fillers of fly ash,
fication (Denef et al. 2001). Most of the plants cannot uptake sand, blast furnace slag, and planting soil (Li et al. 2018).
and utilize organic nitrogen directly, but can effectively up- NH4+ removal, however, is less affected by the influent con-
take nitrate in the system; therefore, it is feasible to use suit- centration. This may be due to the strong adsorption capacity
able plants on the surface of the bioretention system to reduce of the bioretention media for NH4+ (Cho et al. 2009; Chen
the nitrate leaching caused by alternative wetting and drying. et al. 2013).
Application of some mediums with better adsorption ability,
such as biochar and zeolite, is also beneficial to reduce the Hydraulic residence time
nitrogen leaching, which is discussed in detail in the
“Optimization of medium compositions” section. Hydraulic residence time (HRT) is a crucial operational factor
that affects overall performance of bioretention system for
Influent loads and nitrogen concentrations nitrogen removal, as it is directly related to the reaction time
for nitrogen biotransformation (Zhang et al. 2007; Hui et al.
Influent loads and nitrogen concentrations in the influent, 2010). For example, TN removal efficiency was only 27%
which are related to the rainfall and catchment characteristics, when a 0.3-h HRT was used in the bioretention consisted with
Environ Sci Pollut Res (2021) 28:10519–10535 10527

sand, topsoil, and coir peat, while the removal efficiency was properties, and types of packing materials, and it must be
increased to 60% when the HRT was increased to 2.6 h by seriously considered when designing the bioretention system.
regulating the outlet location (Lucas and Greenway 2011a, b).
An attempt to control HRT by underdrain configuration dem-
onstrated that the bioretention with a short HRT (less than 3 h) New aspects about the measures or strategies
was effective for runoff volume reduction while not as well for for improvement of bioretention system
nitrogen removal (Brown and Hunt 2011). In contrast, it was for nitrogen removal
observed that there was a significant increase in TN retention
from 41 to 61% when HRT was increased from 1 to 6–8 h by Structural improvement of bioretention system
constricting the outlet in the sandy media bioretention (Lucas
and Greenway 2008). Similarly, TN reduction efficiency in- The biphasic or multi-layered structure is an improved design
creased from 41 to 82% when retention time was increased of bioretention system to increase the retention time and the
from 3.6 to 13.2 h (Tang and Li 2016). removal efficiency of runoff pollutants by creating sequential
HRT for the best performance of the bioretention system water saturated and unsaturated conditions (Yang et al. 2013;
depends on the nature of the packing materials. It was reported Peterson et al. 2015). In the biphasic bioretention system, the
that a 0.8-day (19.2 h) HRT was ideal for bioretention when runoff is first directed through the saturated zone, which
willow oak wood chips were used as the carbon source consisted of impervious liner and U-shaped reverse drainage
(Peterson et al. 2015). In another study, a 12-h HRT was below it (Fig. 2). The saturated zone maximizes the retention
suitable for achieving maximum efficiency of denitrification time of the runoff and promotes denitrification process. The
when sawdust was used as solid carbon substrate (Jin et al. treated overflow water then flowed into unsaturated zone from
2019). In contrast, in a study in which eucalyptus wood chips the outlet of U-shaped pipe. The unsaturated zone consisted of
were used as the solid carbon source, the nitrate removal effi- soil and filter layer, which is beneficial for further aerobic
ciency reached up to 71, 92, and 97.0% when HRT was 1, 2, treatment for nitrogen. The sequential anaerobic to aerobic
and 4 h, respectively (Lynn et al. 2016). The HRT can also be conditions can be especially beneficial for nitrogen removal
optimized by adjusting the structure of the bioretention sys- while maintaining increased retention time without
tem. In areas with low stormwater runoff, the HRT can be compromising hydraulic performance. Owing to the support
increased by constructing a less permeable layer or construct- of anaerobic environment, the design of the biphasic
ing saturated zone at the bottom of the bioretention. Whereas configurations can significantly improve the nitrogen removal
in the area with high and frequent rainfall runoff, the HRT can efficiency. It was reported that the nitrate removal efficiencies
be increased by changing the structure of bioretention, such as were approximately 60% for low-concentration loads (5 mg/
using the biphasic system (Yang et al. 2013). In summary, an L) and 34% for high-concentration loads (50 mg/L) in the
appropriate HRT is based on the level of contamination, soil biphasic system, and they were higher than that in the

Fig. 2 The structure of the biphasic bioretention system. (1) Plants, (2) soil medium layer, (3) sand medium layer, (4) gravel drainage layer, (5) bypass
drainage pipe, (6) impervious liner, (7) underdrainage pipe, (8) reverse drainage pipe, and (9) overflow from saturated zone
10528 Environ Sci Pollut Res (2021) 28:10519–10535

monophasic system, which were 37% for low-concentration The activated carbon is another ideal packing material to re-
loads and 23% for high-concentration loads (Yang et al. move DON in bioretention system. Vegetation residuals as well
2010). Additionally, the multi-layered bioretention contrib- as dissolution and conversion of influent PON to DON contrib-
utes to the establishment of denitrification and nitrification ute to the release of the DON in the bioretention system (Li and
zones, which is beneficial to the removal of TN. This can be Davis 2014). Therefore, DON removal is as important as the
partially achieved by configuring a less permeable medium nitrate removal and has significant influence on the TN removal
layer under a more permeable medium layer. This layered efficiency. It was reported the a 20-cm coal-activated carbon
configuration in bioretention will allow the formation of an- layer exhibited a great performance for removing DON (more
aerobic zone in the upper layer and promote the denitrification than 80%) from stormwater runoff (Mohtadi et al. 2017). The
in the system (Hsieh et al. 2007). DON in stormwater and agricultural runoff in bioretention sys-
tem consists mainly of humic materials (Berman and Bronk
2003), which can be effectively adsorbed by the activated carbon
Optimization of medium compositions in the bioretention (Bjorklund and Li 2017).
Zeolite is also a packing material used for enhancing nitri-
Due to the microporous structure and high specific surface area, fication and denitrification due to its high structural strength,
biochar is one of the excellent amendments to increase biological ideal capacity for adsorption, and appropriate pH range for
community diversity and abundance in soil (Lehmann et al. nitrogen removal (i.e., 7.5–8) (Khorsha and Davis 2017).
2011). In addition, biochar can absorb and retain nutrients, which Zeolite appears to be effective in removal of NH4+ in the
can subsequently improve the abundance of nutrients in soils for runoff due to its ideal capacity of NH4+ sorption. It also shows
plants (Ventura et al. 2013). For example, biochar is efficient in a trend of high ability of NH4+ exchange, indicating that rel-
retaining ammonium. The leaching of NH4+ in a variety of silty ative ease of accessibility for nitrifying bacteria and regener-
sand soils has been shown to be cumulatively reduced by the ation and continuous application of the zeolite (Khorsha and
addition of bamboo biochar (Ding et al. 2010). It will be more Davis 2017). The application of zeolite is recommended for
appropriate to add biochar to the upper aerobic zone of the enhancing NH 4+ removal in the nitrification zone of a
bioretention system combined with the plants for complete re- bioretention cell. In addition, owing to the electrostatic ad-
moval of NH4+ (Tian et al. 2019). This is because NH4+ can be sorption of nitrate anions on the surface of zeolite particles
firstly retained by the biochar and then irreversibly absored by with positively charged sites, the zeolite appears to be also
the plants at the surface of the bioretention system (Iqbal et al. effective in removal of the nitrate, ranged from 35 to 75%
2015; Tian et al. 2016). In the meantime, uptake of the adsorbed (Reddy et al. 2014). The efficiency, however, will decrease
NH4+ by the plants recovers the biochar. The adsorption of NH4+ under the mixed contaminant conditions, which may be due to
by biochar increases with the increase of the HRT, temperature, the competition between nitrate and other anionic pollutants
and pH, and decreases with the increase of the biochar particle for the binding sites on the surface of the zeolite (Chang et al.
size (Kizito et al. 2015). The use of the biochar is also beneficial 2011; Reddy et al. 2014).
for the removal of nitrate. It was found that biochar pyrolysed
from waste wood pellets demonstrated high removal efficiency Enhancement of the nitrogen removal reaction
(approximately 86%) for nitrate (Reddy et al. 2014). The main
reason is that the application of the biochar can increase porosity At present, the application of the bioretention is mostly based
and water saturation and thus improve the water retention capac- on the heterotrophic denitrification (HD) process (Waller et al.
ity of bioretention and increase the retention time for nitrogen 2018), for which organic matter is required as the electron
removal (Spokas et al. 2012). In addition, biochar provides a donor to drive the denitrification. Addition of external solid
stable carbon substrate and electrons for microbial communities carbon substrate to the bioretention system is crucial for HD
that perform denitrification (Saquing et al. 2016; Tian et al. since the carbon is usually insufficient for microbial activities
2019). For example, the use of biochar increases the abundance in the soil (Kim et al. 2003). The effectiveness of different
of the Bradyrhizobium and Mycobacterium, which can lead to solid carbon substrates in nitrate removal in bioretention sys-
complete denitrification without nitrite production (Anderson tem has been summarized in Table 2. DOC leaching and bio-
et al. 2011). Finally, nitrate can also be adsorbed to some extent film clogging, however, are two crucial problems for HD-
by some biochars, though the adsorption of nitrate by biochar is based bioretention systems for nitrogen removal since many
not as effective as that of NH4+. It has been suggested that the of the carbon substrates are readily hydrolyzed and growth of
adsorption capacity of biochar for nitrate can be improved by the HD microbes is usually fast (Iqbal et al. 2015; Mcphillips
increasing pyrolysis temperature during biochar production et al. 2018; Peterson et al. 2015; Waller et al. 2018).
(Mizuta et al. 2004; Ying et al. 2012). The above studies indicate The combination of autotrophic denitrification (AD) and
the great potential and a promising future of using biochar for HD is a good solution to the above-mentioned problem of
improving bioretention for nitrogen removal. HD-based bioretention system, which can not only ensure
Table 2 Heterotrophic denitrification performance using different solid carbon sources in bioretention system

Carbon source Experiment Influent NO3−-N HRT NO3−-N Remarks Reference


method concentration (h) removal
(mg/L) efficiency (%)

Woodchips Pilot-scale 1 3.1 99 The modifying bioretention systems contained the wood chips and internal water storage zone can (Lopez-Ponnada
experiment for improve nitrate removal under various conditions compared with the conventional system. et al. 2020)
bioretention
Rice husk biochar Column 8 6 90 The addition of biochar in the experimental columns provides sufficient carbon sources for (Xiong et al.
experiment for denitrification reactions, and it also provides a suitable environment for microbial attachment 2019)
Environ Sci Pollut Res (2021) 28:10519–10535

bioretention and growth.


Modified canna leaves Column 50 24 63.3 Nitrate is effectively removed and the accumulation of nitrite is also reduced when using the (Zhao et al.
experiment for modified agricultural wastes, such as canna leaves, rice straw and peanut shell as exogenous 2019)
bioretention carbon source.
Modified rice straw Column 50 24 65.0 (Zhao et al.
experiment for 2019)
bioretention
Modified peanut shell Column 50 24 65.5 (Zhao et al.
experiment for 2019)
bioretention
Woodchips Pilot-scale 2 24 85 The application of woodchips can enhance overall nitrogen treatment performance compared with (Wang et al.
experiment for the system without carbon sources. 2018b)
bioretention
Crude cotton wool Column 30.97 16.8 98.48 Crude cotton can serve as an efficient carbon source in bioretention to treat nitrate-contaminated (Aloni and
experiment for water. Low levels of nitrite can be kept due to a suitable hydrolysis rate of the cotton into simple Brenner 2017)
bioretention saccharine.
Woodchips Column 3 19.2 93 A longer retention time for the stormwater in the bioretention allows for greater nitrogen (Peterson et al.
experiment for reduction. The smaller size of woodchips will provide a more effective reduction. 2015)
bioretention
Sawdust Column 2 10 95 Overall, newspaper-supported biological denitrification shows best performance for nitrogen (Kim et al. 2003)
experiment for removal out of the set studied (newspaper, sawdust and wheat straw), and it is also effective by
bioretention performing in situ experiment in the field under conditions of intermittent loadings during
Newspaper Column 2 10 100 long-term operation. (Kim et al. 2003)
experiment for
bioretention
Wheat straw Column 2 10 100 (Kim et al. 2003)
experiment for
bioretention
Newspaper Pilot-scale 2.33 9 80 (Kim et al. 2003)
experiment for
bioretention
10529
10530 Environ Sci Pollut Res (2021) 28:10519–10535

(Peterson et al. 2015)


(Peterson et al. 2015)
(Peterson et al. 2015)
(Wang et al. 2017a)
the overall nitrogen removal efficiency but also avoid DOC

(Tang and Li 2016)

(Ergas et al. 2009)


(Lynn et al. 2015)
(Kim et al. 2003)
(Kim et al. 2003)
(Kim et al. 2003)
(Kim et al. 2003)
(Kim et al. 2003)
(Kim et al. 2003)
leaching and ensure the stable operation of the bioretention
for a long period. Compared to HD, the AD process is less

Reference
effective in nitrogen removal from stormwater runoff in the
bioretention system than HD, owing to the slow growth of
AD bacteria, while a significant advantage of AD is that
there is no need to use additional carbon source and it will

NO3−-N removal efficiency (%)


produce less sludge due to the low biomass yields of auto-
trophic denitrifying bacteria. In AD process, microorgan-
isms use inorganic substances, such as H2, NH4+, S0, Fe(II)
as electron donors and use inorganic carbon, such as CO2
and HCO3− as the carbon sources to reduce NO3− to N2
(Batchelor and Lawrence 1978; Liu et al. 2009). It has been
observed that the bioretention amended with biochar and

66.6
68.8
85.4

100
30
90
70
95

80
96

84
84

84
zerovalent iron (ZVI) exhibits a better performance for re-
moving nitrate, giving a removal efficiency of 31–96%,

leached TOC (mg/L)


which is in contrast to 6–90% for that of the control cell
(Tian et al. 2019). The biochar can serve as the carbon source
for HD process as well as increase the retention time. The
ZVI can be oxidized primarily by water to form ferrous iron

27.6
and hydrogen (Till et al. 1998), both of which can serve as

<5
<5






34
41
38
electron donors for AD process. Additionally, the
bioretention amended with reduced sulfur (S0) and solid or- HRT (h)
The effect of size for different types of substrates on nitrate removal performance in bioretention system

≥ 13.2
ganic carbon source is also efficient to remove the nitrogen,

19.2
19.2
19.2
12.5

10
10
10
10
10
NO3− removal efficiency greater than 94% has been ob-

2
3

6
served (Hang et al. 2020). During this process, NO3− is re-
Influent NO3−-N concentration (mg/L)

duced to N2, and S0 is oxidized to SO42− in the absence of


oxygen (Batchelor and Lawrence 1978; Sahinkaya and
Dursun 2015). The stoichiometric equation for the process
can be shown as:
55S þ 20CO2 þ 50NO−3 þ 38H2 O

þ 4NHþ
4 →4C5 H7 O2 N þ 25N2 þ 55SO4 þ 64H
2− þ
ð1Þ

The application of S0 as the denitrification substrates has


2.43
3.77
2.14
0.46
2.29

3.77

1.5
some disadvantages, as acid and sulfate formation reaction
2
2
3

3
3

occurs. Therefore, it is necessary to add alkaline substances


Size (mm)

0.6–1.18

such as limestone or bicarbonate to neutralize the pH for


2–2.36
13–25

< 50

better efficiency of the bioretention system (Ergas et al.


2–5

<2
<2
<4
9.5
13

4
5

2009; Kim et al. 2003).


Eucalyptus woodchips

The size of the substrates also has an effect on the nitro-


gen removal. The efficiency of the bioretention system for
Type of substrate

Oak woodchips
Oak woodchips
Oak woodchips

removal of nitrate in areas with heavy contamination could


Woodchips
Woodchips
Woodchips

Newspaper
Newspaper

be enhanced by adjusting the mass or particle size of the


Sawdust

substrates. Studies about the effect of size of substrates for


Sulfur

Sulfur
Sulfur

nitrogen removal in bioretention system have been summa-


rized in the Table 3. It has demonstrated that the substrates
Pilot-scale experiment
Pilot-scale experiment

with smaller particle size lead to a better removal perfor-


Column experiment

Column experiment
Column experiment
Column experiment
Column experiment

Column experiment
Column experiment
Column experiment

Column experiment
Column experiment
Experiment method

In situ experiment

mance of nitrate. The size of the substrate particles deter-


mines the specific surface area per unit volume. The smaller
size of the substrate gives larger available surface area for
Table 3

denitrifying microorganisms and larger area for biofilm


growth (Peterson et al. 2015). However, smaller substrate
Environ Sci Pollut Res (2021) 28:10519–10535 10531

size would be expected to cause leaching of more DOC due to Ethics approval and consent to participate Not applicable
a higher degradation rate (Shao et al. 2009; Robertson and
Consent for publication Not applicable
Cherry 2010). The results from these studies demonstrate that
it is necessary to adjust the size of the solid substrates based on
the loads of nitrogen contaminants for optimizing the perfor-
mance of the bioretention system. References
Aloni A, Brenner A (2017) Use of cotton as a carbon source for denitri-
fication in biofilters for groundwater remediation. Water 9:714–725.
Summary https://doi.org/10.3390/w9090714
Anderson CR, Condron LM, Clough TJ, Fiers MF, Stewart A, Hill RA,
Sherlock RR (2011) Biochar induced soil microbial community
Bioretention system plays an important role in the non-point change: implications for biogeochemical cycling of carbon, nitrogen
pollution management. Bioretention for the treatment of urban and phosphorus. Pedobiologia 54:309–320. https://doi.org/10.1016/
stormwater runoff needs to be able to cope with large runoff j.pedobi.2011.07.005
loads, while the focus of the bioretention for agricultural run- Baldwin DS, Mitchell AM (2000) The effects of drying and re-flooding
on the sediment and soil nutrient dynamics of lowland river–
off is on the treatment of the particulate pollutants and the floodplain systems: a synthesis. Regul Rivers Res Manage 16:
removal of fertilizer nutrients. The top layer of the 457–467. https://doi.org/10.1002/1099-1646(200009/10)16:
bioretention and the medium with low sand content contain 5<457::aid-rrr597>3.0.co;2-b
higher abundance and activity of denitrifiers; it is a more fea- Batchelor B, Lawrence AW (1978) Autotrophic denitrification using el-
emental sulfur. J Water Pollut Control Fed 50:1986–2001. https://
sible option to construct bioretention with high proportion doi.org/10.1016/0043-1354(78)90053-2
sand media and substrates favorable for denitrification, which Berman T, Bronk DA (2003) Dissolved organic nitrogen: a dynamic
is beneficial for promoting infiltration and improving micro- participant in aquatic ecosystems. Aquat Microb Ecol 31:279–305.
bial abundance and activity. https://doi.org/10.3354/ame031279
In order to attain a better efficiency of the bioretention Bjorklund K, Li L (2017) Removal of organic contaminants in
bioretention medium amended with activated carbon from sewage
system for the removal of nitrogen, some measures or strate- sludge. Environ Sci Pollut Res 24:19167–19180. https://doi.org/10.
gies for nitrogen removal from the perspectives of structural 1007/s11356-017-9508-1
improvement of bioretention, optimization of media and en- Blecken GT, Zinger Y, Deletic A, Fletcher TD, Hedstrom A, Viklander
hancement of reaction processes are proposed. It is recom- M (2010) Laboratory study on stormwater biofiltration: nutrient and
sediment removal in cold temperatures. J Hydrol 394:507–514.
mended to use biphasic or layered bioretention to strengthen
https://doi.org/10.1016/j.jhydrol.2010.10.010
the nitrogen removal. Some amendments such as biochar, Bratieres K, Fletcher TD, Deletic A, Zinger Y (2008) Nutrient and sed-
activated carbon, and zeolite are beneficial to retain nitrogen. iment removal by stormwater biofilters: a large-scale design optimi-
Application of substrates for denitrification should be a focus sation study. Water Res 42:3930–3940. https://doi.org/10.1016/j.
for improvement of performance of bioretention system; it watres.2008.06.009
Bridgham SD, Updegraff K, Pastor J (1998) Carbon, nitrogen, and phos-
will be promising to combine the AD with the HD to attain
phorus mineralization in northern wetlands. Ecology 79:1545–1561.
a more efficient and stable bioretention to remove nitrogen for https://doi.org/10.2307/176848
a long period. Brown RA, Hunt WF (2011) Impacts of media depth on effluent water
quality and hydrologic performance of undersized bioretention cells.
Authors’ contributions HWZ, ZA, and HZ conceptualized the review. J Irrig Drain Eng 137:132–143. https://doi.org/10.1061/(asce)ir.
HZ acquired the funding. HZ and ZHY supervised the work. HWZ and 1943-4774.0000167
ZA wrote the draft manuscript. HZ, YLS, ZHY, and YFJ reviewed and Burton GA Jr, Pitt R (2001) Stormwater effects handbook: a toolbox for
revised the manuscript. All authors read and approved the final watershed managers, scientists, and engineers. Lewis Publishers,
manuscript. CRC Press, Boca Raton (Fl)
Cabrera ML (1993) Modeling the flush of nitrogen mineralization caused
Funding This research was supported by the Major Science and by drying and rewetting soils. Soil Sci Soc Am J 57:63–66. https://
Technology Program for Water Pollution Control and Treatment of doi.org/10.2136/sssaj1993.03615995005700010012x
China (2017ZX07108–001) and National Natural Science Foundation Chang NB, Wanielista MP, Henderson D (2011) Temperature effects on
of China (51629901). functionalized filter media for nutrient removal in stormwater treat-
ment. Environ Prog Sustain 30:309–317. https://doi.org/10.1002/ep.
10479
Data availability All data generated or analyzed during this study are
included in this published article [and its supplementary information Chen P, Li J, Li QX, Wang Y, Li S, Ren T, Wang L (2012) Simultaneous
files]. heterotrophic nitrification and aerobic denitrification by bacterium
Rhodococcus sp. CPZ24. Bioresour Technol 116:266–270. https://
doi.org/10.1016/j.biortech.2012.02.050
Compliance with ethical standards Chen X, Peltier E, Sturm BSM, Young CB (2013) Nitrogen removal and
nitrifying and denitrifying bacteria quantification in a stormwater
Conflict of interests The authors declare that they have no conflict of bioretention system. Water Res 47:1691–1700. https://doi.org/10.
interest. 1016/j.watres.2012.12.033
10532 Environ Sci Pollut Res (2021) 28:10519–10535

Cho K, Song KG, Cho J, Kim T, Ahn KH (2009) Removal of nitrogen by Ergas SJ, Sengupta S, Siegel R, Pandit A, Yao Y, Yuan X (2010)
a layered soil infiltration system during intermittent storm events. Performance of nitrogen-removing bioretention systems for control
Chemosphere 76:690–696. https://doi.org/10.1016/j.chemosphere. of agricultural runoff. J Environ Eng 136:1105–1112. https://doi.
2009.03.025 org/10.1061/(asce)ee.1943-7870.0000243
Coffman L, Green R, Clar M, Bitter S (1994) Development of bio- Fan G, Li Z, Wang S, Huang K, Luo J (2019) Migration and transforma-
retention practices for storm water management. In: Current prac- tion of nitrogen in bioretention system during rainfall runoff.
tices in modelling the management of storm water impacts. Lewis, Chemosphere 232:54–62. https://doi.org/10.1016/j.chemosphere.
Boca Raton, pp 23–42. https://doi.org/10.14796/JWMM.R176-02 2019.05.177
Collins KA, Lawrence TJ, Stander EK, Jontos RJ, Kaushal SS, Foglar L, Briski F, Sipos L, Vukovic M (2005) High nitrate removal from
Newcomer TA, Grimm NB, Ekberg MLC (2010) Opportunities synthetic wastewater with the mixed bacterial culture. Bioresour
and challenges for managing nitrogen in urban stormwater: a review Technol 96:879–888. https://doi.org/10.1016/j.biortech.2004.09.
and synthesis. Ecol Eng 36:1507–1519. https://doi.org/10.1016/j. 001
ecoleng.2010.03.015 Geheniau N, Fuamba M, Mahaut V, Gendron MR, Dugue M (2015)
Davidson EA, Savage KE, Bettez ND, Marino R, Howarth RW (2010) Monitoring of a rain garden in cold climate: case study of a parking
Nitrogen in runoff from residential roads in a coastal area. Water Air lot near Montreal. J Irrig Drain Div Am Soc Civ Eng 141(6):
Soil Pollut 210:3–13. https://doi.org/10.1007/s11270-009-0218-2 04014073. https://doi.org/10.1061/(asce)ir.1943-4774.0000836
Davis AP (2008) Field performance of bioretention: hydrology impacts. J Glass C, Silverstein JA (1998) Denitrification kinetics of high nitrate
Hydrol Eng 13:90–95. https://doi.org/10.1061/(asce)1084- concentration water: pH effect on inhibition and nitrite accumula-
0699(2008)13:2(90) tion. Water Res 32:831–839. https://doi.org/10.1016/s0043-
Davis BS, Birch GF (2009) Catchment-wide assessment of the cost- 1354(97)00260-1
effectiveness of stormwater remediation measures in urban areas. Glass C, Silverstein JA, Oh J (1997) Inhibition of denitrification in acti-
Environ Sci Pol 12:84–91. https://doi.org/10.1016/j.envsci.2008.09.004 vated sludge by nitrite. Water Environ Res 69:1086–1093. https://
Davis AP, Shokouhian M, Sharma H, Minami C (2001) Laboratory study doi.org/10.2175/106143097x125803
of biological retention for urban stormwater management. Water Goh HW, Zakaria NA, Lau TL, Foo KY, Chang CK, Leow CS (2017)
Environ Res 73:5–14. https://doi.org/10.2175/106143001x138624 Mesocosm study of enhanced bioretention media in treating nutrient
rich stormwater for mixed development area. Urban Water J 14:
Davis AP, Mohammad S, Himanshu S, Christie M (2006) Water quality
134–142. https://doi.org/10.1080/1573062x.2015.1076861
improvement through bioretention media: nitrogen and phosphorus
Goh HW, Lem KS, Azizan NA, Chang CK, Talei A, Leow CS, Zakaria
removal. Water Environ Res 78:284–293. https://doi.org/10.2175/
NA (2019) A review of bioretention components and nutrient re-
106143005x94376
moval under different climatesfuture directions for tropics. Environ
Davis AP, Hunt WF, Traver RG, Clar M (2009) Bioretention technology:
Sci Pollut Res 26:14904–14919. https://doi.org/10.1007/s11356-
overview of current practice and future needs. J Environ Eng 135:109–
019-05041-0
117. https://doi.org/10.1061/(asce)0733-9372(2009)135:3(109)
Hamedani AS, Bazilio A, Cerda C, Manjarres A, Hall A, Shipley H,
De Rozari P, Greenway M, El Hanandeh A (2018) Nitrogen removal
Giacomoni M (2019) Assessing the performance of bioretention
from sewage and septage in constructed wetland mesocosms using
and sand filter media using columns and synthetic stormwater. In:
sand media amended with biochar. Ecol Eng 111:1–10. https://doi.
World Environmental and Water Resources Congress 2019: Water,
org/10.1016/j.ecoleng.2017.11.002
Wastewater, and Stormwater; Urban Water Resources; and
Denef K, Six J, Bossuyt H, Frey SD, Elliott ET, Merckx R, Paustian K Municipal Water Infrastructure. American Society of Civil
(2001) Influence of dry–wet cycles on the interrelationship between Engineers Reston, VA, pp 57–70. https://doi.org/10.1061/
aggregate, particulate organic matter, and microbial community dy- 9780784482360.007
namics. Soil Biol Biochem 33:1599–1611. https://doi.org/10.1016/ Hang Q, Wang H, He Z, Dong W, Chu Z, Ling Y, Yan G, Chang Y, Li C
s0038-0717(01)00076-1 (2020) Hydrilla verticillata–sulfur-based heterotrophic and autotro-
Denich C, Bradford A (2009) Cold climate issues for bioretention: phic denitrification process for nitrate-rich agricultural runoff treat-
assessing impacts of salt and aggregate application on plant health, ment. Int J Environ Res Public Health 17(5):1574. https://doi.org/
media clogging, and groundwater quality. In: Low impact develop- 10.3390/ijerph17051574
ment for urban ecosystem and habitat protection, pp 1–10. https:// Harris G, Batley G, Fox D, Hall D, Jernakoff P, Molloy R, Murray A,
doi.org/10.1061/41009(333)3 Newell B, Parslow J, Skyring G, Walker S (1996) Port Phillip Bay
Dietz ME (2007) Low impact development practices: a review of current environmental study final report. CSIRO Australia, Canberra.
research and recommendations for future directions. Water Air Soil https://doi.org/10.4225/08/5856cf3221739
Pollut 186:351–363. https://doi.org/10.1007/s11270-007-9484-z Hatt BE, Fletcher TD, Deletic A (2007) Hydraulic and pollutant removal
Dietz ME (2016) Modified bioretention for enhanced nitrogen removal performance of stormwater filters under variable wetting and drying
from agricultural runoff. J Environ Eng 142:06016007. https://doi. regimes. Water Sci Technol 56:11–19. https://doi.org/10.2166/wst.
org/10.1061/(asce)ee.1943-7870.0001144 2007.751
Ding Y, Liu YX, Wu WX, Shi DZ, Yang M, Zhong ZK (2010) Hatt BE, Fletcher TD, Deletic A (2009) Hydrologic and pollutant removal
Evaluation of biochar effects on nitrogen retention and leaching in performance of stormwater biofiltration systems at the field scale. J
multi-layered soil columns. Water Air Soil Pollut 213:47–55. https:// Hydrol 365:310–321. https://doi.org/10.1016/j.jhydrol.2008.12.001
doi.org/10.1007/s11270-010-0366-4 Hossain F, Chang NB, Wanielista M (2010) Modeling kinetics and iso-
Elliott EM, Kendall C, Wankel SD, Burns DA, Boyer EW, Harlin K, therms of functionalized filter media for nutrient removal from
Bain DJ, Butler T (2007) Nitrogen isotopes as indicators of NOx stormwater dry ponds. Environ Prog Sustain 29:319–333. https://
source contributions to atmospheric nitrate deposition across the doi.org/10.1002/ep.10415
midwestern and northeastern United States. Environ Sci Technol Houdeshel CD, Hultine KR, Johnson NC, Porneroy CA (2015)
41:7661–7667. https://doi.org/10.1021/es070898t Evaluation of three vegetation treatments in bioretention gardens
Ergas SJ, Sengupta S, Siegel R, Yao Y, Pandit A, Yuan X (2009) in a semi-arid climate. Landsc Urban Plan 135:62–72. https://doi.
Denitrifying bioretention systems for control of non-point nitrogen org/10.1016/j.landurbplan.2014.11.008
sources. Proc Water Environ Fed 2009:5085–5097. https://doi.org/ Houle JJ, Roseen RM, Ballestero TP, Puls TA, Sherrard J (2013)
10.2175/193864709793951900 Comparison of maintenance cost, labor demands, and system
Environ Sci Pollut Res (2021) 28:10519–10535 10533

performance for LID and conventional stormwater management. J Kim H, Seagren EA, Davis AP (2003) Engineered bioretention for re-
Environ Eng 139:932–938. https://doi.org/10.1061/(asce)ee.1943- moval of nitrate from stormwater runoff. Water Environ Res 75:
7870.0000698 355–367. https://doi.org/10.2175/106143003x141169
Howarth RW (2008) Coastal nitrogen pollution: a review of sources and Kizito S, Wu S, Kirui WK, Lei M, Lu Q, Bah H, Dong R (2015)
trends globally and regionally. Harmful Algae 8:14–20. https://doi. Evaluation of slow pyrolyzed wood and rice husks biochar for ad-
org/10.1016/j.hal.2008.08.015 sorption of ammonium nitrogen from piggery manure anaerobic
Hsieh CH, Davis AP (2005a) Evaluation and optimization of bioretention digestate slurry. Sci Total Environ 505:102–112. https://doi.org/
media for treatment of urban storm water runoff. J Environ Eng 131: 10.1016/j.scitotenv.2014.09.096
1521–1531. https://doi.org/10.1061/(asce)0733-9372(2005)131: Klocker CA, Kaushal SS, Groffman PM, Mayer PM, Morgan RP (2009)
11(1521) Nitrogen uptake and denitrification in restored and unrestored
Hsieh CH, Davis AP (2005b) Multiple-event study of bioretention for streams in urban Maryland, USA. Aquat Sci 71:411–424. https://
treatment of urban storm water runoff. Water Sci Technol 51:177– doi.org/10.1007/s00027-009-0118-y
181. https://doi.org/10.2166/wst.2005.0589 Kratky H, Li Z, Chen Y, Wang C, Li X, Yu T (2017) A critical literature
Hsieh CH, Davis AP, Needelman BA (2007) Nitrogen removal from review of bioretention research for stormwater management in cold
urban stormwater runoff through layered bioretention columns. climate and future research recommendations. Front Environ Sci
Water Environ Res 79:2404–2411. https://doi.org/10.2175/ Eng 11:23–37. https://doi.org/10.1007/s11783-017-0982-y
106143007x183844 Laurenson G, Laurenson S, Bolan N, Beecham S, Clark I (2013)
Hui H, Zhang Y, Cui C, Zheng S (2010) Effect of COD level and HRT on Chapter four. The role of bioretention systems in the treatment of
microbial community in a yeast-predominant activated sludge sys- stormwater. Adv Agron 120:223–274. https://doi.org/10.1016/
tem. Bioresour Technol 101:3463–3465. https://doi.org/10.1016/j. b978-0-12-407686-0.00004-x
biortech.2009.12.121 Le Coustumer S, Fletcher TD, Deletic A, Barraud S, Lewis J (2009)
Hunt WF, Smith JT, Jadlocki SJ, Hathaway JM, Eubanks PR (2008) Hydraulic performance of biofilter systems for stormwater manage-
Pollutant removal and peak flow mitigation by a bioretention cell ment: influences of design and operation. J Hydrol 376:16–23.
in urban Charlotte, NC. J Environ Eng Asce 134:403–408. https:// https://doi.org/10.1016/j.jhydrol.2009.07.012
doi.org/10.1061/(asce)0733-9372(2008)134:5(403) Le Coustumer S, Fletcher TD, Deletic A, Barraud S, Poelsma P (2012)
Hunt WF, Davis AP, Traver RG (2012) Meeting hydrologic and water The influence of design parameters on clogging of stormwater
quality goals through targeted bioretention design. J Environ Eng biofilters: a large-scale column study. Water Res 46:6743–6752.
138:698–707. https://doi.org/10.1061/(asce)ee.1943-7870.0000504 https://doi.org/10.1016/j.watres.2012.01.026
Lehmann J, Rillig MC, Thies J, Masiello CA, Hockaday WC, Crowley D
Iqbal H, Garcia-Perez M, Flury M (2015) Effect of biochar on leaching of
(2011) Biochar effects on soil biota–a review. Soil Biol Biochem 43:
organic carbon, nitrogen, and phosphorus from compost in
1812–1836. https://doi.org/10.1016/j.soilbio.2011.04.022
bioretention systems. Sci Total Environ 521:37–45. https://doi.org/
Li LQ, Davis AP (2014) Urban stormwater runoff nitrogen composition
10.1016/j.scitotenv.2015.03.060
and fate in bioretention systems. Environ Sci Technol 48:3403–
Jennings DB, Jarnagin ST (2002) Changes in anthropogenic impervious
3410. https://doi.org/10.1021/es4055302
surfaces, precipitation and daily streamflow discharge: a historical
Li YM, Li J, Zheng GH, Luan JF, Fu Q, Gu GW (2008) Effects of the
perspective in a mid-Atlantic subwatershed. Landsc Ecol 17:471–
COD/NO3(−)-N ratio and pH on the accumulation of denitrification
489. https://doi.org/10.1023/A:1021211114125
intermediates with available pyridine as a sole electron donor and
Jiang C, Li J, Li H, Li Y, Chen L (2017) Field performance of carbon source. Environ Technol 29:1297–1306. https://doi.org/10.
bioretention systems for runoff quantity regulation and pollutant 1080/09593330802379672
removal. Water Air Soil Pollut 228(12):468. https://doi.org/10. Li X, Liu Z, Wang C, Yu T, Zhou F (2012) The study of bioretention
1007/s11270-017-3636-6 applications for sustainable urban stormwater management in cold
Jiang C, Li J, Zhang B, Ruan T, Li H, Dong W (2018) Design parameters cl i m at e s. I n: C o n fe re n ce -c an a di a n So c ie t y fo r Ci v i l
and treatment efficiency of a retrofit bioretention system on runoff Engineering. Edmonton, Alberta, pp 1129:1–8
nitrogen removal. Environ Sci Pollut Res 25(33):33298–33308. Li J, Zhao R, Li Y, Chen L (2018) Modeling the effects of parameter
https://doi.org/10.1007/s11356-018-3267-5 optimization on three bioretention tanks using the HYDRUS-1D
Jiang C, Li J, Li H, Li Y (2019) Nitrogen retention and purification efficiency model. J Environ Manag 217:38–46. https://doi.org/10.1016/j.
from rainfall runoff via retrofitted bioretention cells. Sep Purif Technol jenvman.2018.03.078
25-32:25–32. https://doi.org/10.1016/j.seppur.2019.03.036 Liu H, Jiang W, Wan D, Qu J (2009) Study of a combined heterotrophic
Jin S, Feng C, Tong S, Chen N, Liu H, Zhao J (2019) Effect of sawdust and sulfur autotrophic denitrification technology for removal of ni-
dosage and hydraulic retention time (HRT) on nitrate removal in trate in water. J Hazard Mater 169:23–28. https://doi.org/10.1016/j.
sawdust/pyrite mixotrophic denitrification (SPMD) systems. jhazmat.2009.03.053
Environ Sci Water Res 5(2):346–357. https://doi.org/10.1039/ Liu J, Sample DJ, Bell C, Guan Y (2014a) Review and research needs of
c8ew00748a bioretention used for the treatment of urban stormwater. Water 6:
Kang WC, Song KG, Jin WC, Kim TG, Ahn KH (2009) Removal of 1069–1099. https://doi.org/10.3390/w6041069
nitrogen by a layered soil infiltration system during intermittent Liu J, Sample DJ, Owen JS, Li J, Evanylo GK (2014b) Assessment of
storm events. Chemosphere 76:690–696. https://doi.org/10.1016/j. selected bioretention blends for nutrient retention using mesocosm
chemosphere.2009.03.025 experiments. J Environ Qual 43:1754–1763. https://doi.org/10.
Kaushal SS, Groffman PM, Mayer PM, Striz E, Gold AJ (2008) Effects 2134/jeq2014.01.0017
of stream restoration on denitrification in an urbanizing watershed. Lopez-Ponnada EV, Lynn TJ, Ergas SJ, Mihelcic JR (2020) Long-term
Ecol Appl 18:789–804. https://doi.org/10.1890/07-1159.1 field performance of a conventional and modified bioretention sys-
Keen GA (1984) Nitrification in continuous culture: the effect of pH and tem for removing dissolved nitrogen species in stormwater runoff.
surface growth. Ph.D. Thesis, University of Aberdeen Water Res 170:115336. https://doi.org/10.1016/j.watres.2019.
Khorsha G, Davis AP (2017) Characterizing clinoptilolite zeolite and 115336
hydroaluminosilicate aggregates for ammonium removal from Lucas WC, Greenway M (2008) Nutrient retention in vegetated and
stormwater runoff. J Environ Eng 143(2):04016082. https://doi. nonvegetated bioretention mesocosms. J Irrig Drain Eng 134:613–
org/10.1061/(asce)ee.1943-7870.0001167 623. https://doi.org/10.1061/(asce)0733-9437(2008)134:5(613)
10534 Environ Sci Pollut Res (2021) 28:10519–10535

Lucas WC, Greenway M (2011a) Hydraulic response and nitrogen reten- 1.1). http://rpitt.eng.ua.edu/Research/ms4/Paper/Mainms4paper.
tion in bioretention mesocosms with regulated outlets: part I– html. Accessed 18 June 2020
hydraulic response. Water Environ Res 83:692–702. https://doi. Prakasam TBS, Loehr RC (1972) Microbial nitrification and denitrifica-
org/10.2175/106143010x12780288628697 tion in concentrated wastes. Water Res 6:859–869. https://doi.org/
Lucas WC, Greenway M (2011b) Hydraulic response and nitrogen reten- 10.1016/0043-1354(72)90038-3
tion in bioretention mesocosms with regulated outlets: part II— Read J, Fletcher TD, Wevill T, Deletic A (2009) Plant traits that enhance
nitrogen retention. Water Environ Res 83:703–713. https://doi.org/ pollutant removal from stormwater in biofiltration systems. Int J
10.2175/106143011x12989211840936 Phy toremedia tion 1 2:34 –5 3. https://doi.org/10.1080/
Lupwayi NZ, Lafond GP, Ziadi N, Grant CA (2012) Soil microbial response 15226510902767114
to nitrogen fertilizer and tillage in barley and corn. Soil Tillage Res 118: Reddy KR, Xie T, Dastgheibi S (2014) Adsorption of mixtures of nutri-
139–146. https://doi.org/10.1016/j.still.2011.11.006 ents and heavy metals in simulated urban stormwater by different
Lynn TJ, Yehdaniel H, Ergassarina J (2015) Performance of denitrifying filter materials. J Environ Sci Health A 49:524–529. https://doi.org/
stormwater biofilters under intermittent conditions. Environ Eng Sci 10.1080/10934529.2014.859030
32:796–805. https://doi.org/10.1089/ees.2015.0135 Robertson WD, Cherry JA (2010) In situ denitrification of septic-system
Lynn TJ, Ergas SJ, Nachabe MH (2016) Effect of hydrodynamic disper- nitrate using reactive porous media barriers: field trials. Ground Water
sion in denitrifying wood-chip stormwater biofilters. J Sustain Water 33:99–111. https://doi.org/10.1111/j.1745-6584.1995.tb00266.x
Built Environ 2:04016004. https://doi.org/10.1061/jswbay.0000812 Sahinkaya E, Dursun N (2015) Use of elemental sulfur and thiosulfate as
Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, electron sources for water denitrification. Bioprocess Biosyst Eng
Gaufichon L, Suzuki A (2010) Nitrogen uptake, assimilation and remo- 38:531–541. https://doi.org/10.1007/s00449-014-1293-3
bilization in plants: challenges for sustainable and productive agricul- Sansalone JJ, Glenn DW (2002) Accretion of pollutants in snow exposed
ture. Ann Bot 105:1141–1157. https://doi.org/10.1093/aob/mcq028 to urban traffic and winter storm maintenance activities. I. J Environ
Mcphillips L, Goodale C, Walter MT (2018) Nutrient leaching and green- Eng 128(2):151–166. https://doi.org/10.1061/(asce)0733-
house gas emissions in grassed detention and bioretention 9372(2002)128:2(151)
stormwater basins. J Sustain Water Built Environ 4(1):04017014. Saquing JM, Yu Y, Chiu PC (2016) Wood-derived black carbon (biochar) as
https://doi.org/10.1061/JSWBAY.0000837 a microbial electron donor and acceptor. Environ Sci Technol Lett 3:62–
Miller JJ, Handerek BP, Beasley BW, Olson ECS, Yanke LJ, Larney FJ, 66. https://doi.org/10.1021/acs.estlett.5b00354
Mcallister TA, Olson BM, Selinger LB, Chanasyk DS (2004) Scholz O, Gawne B, Ebner B, Ellis I (2010) The effects of drying and re-
Quantity and quality of runoff from a beef cattle feedlot in southern flooding on nutrient availability in ephemeral deflation basin lakes
Alberta. J Environ Qual 33:1088–1097. https://doi.org/10.2134/ in western New South Wales, Australia. River Res Appl 18:185–
jeq2004.1088 196. https://doi.org/10.1002/rra.665
Mizuta K, Matsumoto T, Hatate Y, Nishihara K, Nakanishi T (2004) Sgouridis F, Heppell CM, Wharton G, Lansdown K, Trimmer M (2011)
Removal of nitrate-nitrogen from drinking water using bamboo Denitrification and dissimilatory nitrate reduction to ammonium
powder charcoal. Bioresour Technol 95:255–257. https://doi.org/ (DNRA) in a temperate re-connected floodplain. Water Res 45:
10.1016/j.biortech.2004.02.015 4909–4922. https://doi.org/10.1016/j.watres.2011.06.037
Mohtadi M, James BR, Davis AP (2017) Adsorption of compounds that Shao L, Xu ZX, Yin HL, Chu HQ (2009) Rice husk as carbon
mimic urban stormwater dissolved organic nitrogen. Water Environ source and biofilm carrier for water denitrification. Pol J
Res 89:105–116. https://doi.org/10.2175/106143016x14 Environ Stud 18(4):693–699. https://doi.org/10.1016/j.jbiotec.
504669769010 2008.07.1534
Muerdter C, Ozkok E, Li LQ, Davis AP (2016) Vegetation and media Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate re-
characteristics of an effective bioretention cell. J Sustain Water Built duction to ammonium in upland tropical forest soils. Ecology 82:
Environ 2:11. https://doi.org/10.1061/jswbay.0000804 2410–2416. https://doi.org/10.1890/0012-9658(2001)082[2410:
Novotny V (2010) Integrating diffuse/nonpoint pollution control and wa- dnrtai]2.0.co;2
ter body restoration into watershed management. Jawra J Am Water Singh RP, Zhao F, Ji Q, Saravanan J, Fu DF (2019) Design and perfor-
Resour Assoc 35:717–727. https://doi.org/10.1111/j.1752-1688. mance characterization of roadside bioretention systems.
1999.tb04169.x Sustainability 11:13. https://doi.org/10.3390/su11072040
Ongley E, Xiaolan Z, Tao Y (2010) Current status of agricultural and Smolek AP, Anderson AR, Hunt WF (2018) Hydrologic and water-
rural non-point source pollution assessment in China. Environ Pollut quality evaluation of a rapid-flow biofiltration device. J Environ
158:1159–1168. https://doi.org/10.1016/j.envpol.2009.10.047 Eng 144:13. https://doi.org/10.1061/(asce)ee.1943-7870.0001275
Osman M, Yusof KW, Takaijudin H, Goh HW, Malek MA, Azizan NA, Sparling GP, Ross DJ (1988) Microbial contributions to the increased
Ghani AA, Abdurrasheed AS (2019) A review of nitrogen removal nitrogen mineralization after air-drying of soils. Plant Soil 105:
for urban stormwater runoff in bioretention system. Sustainability 163–167. https://doi.org/10.1007/bf02376779
11:415. https://doi.org/10.3390/su11195415 Spokas KA, Cantrell KB, Novak JM, Archer DW, Ippolito JA, Collins HP,
Passeport E, Hunt WF, Line DE, Smith RA, Brown RA (2009) Field Boateng AA, Lima IM, Lamb MC, Mcaloon AJ (2012) Biochar: a
study of the ability of two grassed bioretention cells to reduce synthesis of its agronomic impact beyond carbon sequestration. J
storm-water runoff pollution. J Irrig Drain Eng 135:505–510. Environ Qual 41:973–989. https://doi.org/10.2134/jeq2011.0069
https://doi.org/10.1061/(asce)ir.1943-4774.0000006 Tang N, Li T (2016) Nitrogen removal by three types of bioretention
Peterson M (2016) The effect of the antecedent dry conditions on nitrogen columns under wetting and drying regimes. J Cent South Univ 23:
removal for a modified bioretention system. Department of Civil 324–332. https://doi.org/10.1007/s11771-016-3077-1
and Environmental Engineering College of Engineering. Taylor GD, Fletcher TD, Wong THF, Breen PF, Duncan HP (2005)
University of South Florida Nitrogen composition in urban runoff–implications for stormwater
Peterson IJ, Igielski S, Davis AP (2015) Enhanced Denitrification in management. Water Res 39:1982–1989. https://doi.org/10.1016/j.
bioretention using woodchips as an organic carbon source. J watres.2005.03.022
Sustain Water Built Environ 1:9. https://doi.org/10.1061/jswbay. Templer PH, Silver WL, Pett-Ridge J, Deangelis KM, Firestone MK
0000800 (2008) Plant and microbial controls on nitrogen retention and loss
Pitt R, Maestre A, Morquecho R (2004) The national stormwater quality in a humid tropical forest. Ecology 89:3030–3040. https://doi.org/
database. The national stormwater quality database (NSQD, Version 10.1890/07-1631.1
Environ Sci Pollut Res (2021) 28:10519–10535 10535

Thomas KL, Lloyd D, Boddy L (1994) Effects of oxygen, pH and nitrate West AW, Sparling GP, Feltham CW, Reynolds J (1992) Microbial ac-
concentration on denitrification by Pseudomonas species. FEMS tivity and survival in soils dried at different rates. Soil Res 30:209–
Microbiol Lett 118:181–186. https://doi.org/10.1111/j.1574-6968. 222. https://doi.org/10.1071/sr9920209
1994.tb06823.x Willard LL, Wynnthompson T, Krometis L, Neher TP, Badgley BD
Tian J, Miller V, Chiu PC, Maresca JA, Guo M, Imhoff PT (2016) (2017) Does it pay to be mature? Evaluation of bioretention
Nutrient release and ammonium sorption by poultry litter and wood cell performance seven years postconstruction. J Environ Eng
biochars in stormwater treatment. Sci Total Environ 553:596–606. 143:04017041. https://doi.org/10.1061/(asce)ee.1943-7870.
https://doi.org/10.1016/j.scitotenv.2016.02.129 0001232
Tian J, Jin J, Chiu PC, Cha DK, Guo M, Imhoff PT (2019) A pilot-scale, Xiong J, Ren S, He Y, Wang XC, Bai X, Wang J, Dzakpasu M (2019)
bi-layer bioretention system with biochar and zero-valent iron for Bioretention cell incorporating Fe-biochar and saturated zones for
enhanced nitrate removal from stormwater. Water Res 148:378– enhanced stormwater runoff treatment. Chemosphere 237:124424.
387. https://doi.org/10.1016/j.watres.2018.10.030 https://doi.org/10.1016/j.chemosphere.2019.124424
Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1983) Yang H, Mccoy EL, Grewal PS, Dick WA (2010) Dissolved nutrients
Denitrification: ecological niches, competition and survival. Anton and atrazine removal by column-scale monophasic and biphasic rain
Leeuw Int J G 48:569–583. https://doi.org/10.1007/bf00399542 garden model systems. Chemosphere 80:929–934. https://doi.org/
Till BA, Weathers LJ, Alvarez PJJ (1998) Fe(0)-supported autotrophic 10.1016/j.chemosphere.2010.05.021
denitrification. Environ Sci Technol 32:634–639. https://doi.org/10. Yang XP, Wang SM, Zhang DW, Zhou LX (2011) Isolation and
1021/es9707769 nitrogen removal characteristics of an aerobic heterotrophic
Trowsdale S, Simcock R (2011) Urban stormwater treatment using nitrifying–denitrifying bacterium, Bacillus subtilis A1.
bioretention. J Hydrol 397:167–174. https://doi.org/10.1016/j. Bioresour Technol 102:854–862. https://doi.org/10.1016/j.
jhydrol.2010.11.023 biortech.2010.09.007
Tyler B (1978) Regulation of the assimilation of nitrogen compounds.
Yang H, Dick WA, Mccoy EL, Phelan PL, Grewal PS (2013) Field
Annu Rev Biochem 47:1127–1162. https://doi.org/10.1146/
evaluation of a new biphasic rain garden for stormwater flow man-
annurev.bi.47.070178.005403
agement and pollutant removal. Ecol Eng 54:22–31. https://doi.org/
Updegraff K, Pastor J, Bridgham SD, Johnston CA (1995) Environmental
10.1016/j.ecoleng.2013.01.005
and substrate controls over carbon and nitrogen mineralization in
northern wetlands. Ecol Appl 5:151–163. https://doi.org/10.2307/ Ying Y, Bin G, Ming Z, Mandu I, Zimmerman AR (2012) Effect of
1942060 biochar amendment on sorption and leaching of nitrate, ammonium,
USEPA (2000) Storm water phase II final rule: small MS4 storm water and phosphate in a sandy soil. Chemosphere 89:1467–1471. https://
program review. Fact sheet 2.0 doi.org/10.1016/j.chemosphere.2012.06.002
Venterink HO, Davidsson TE, Kiehl K, Leonardson L (2002) Impact of Young RA, Huntrods T, Anderson W (1980) Effectiveness of vegetated
drying and re-wetting on N, P and K dynamics in a wetland soil. buffer strips in controlling pollution from feedlot runoff. J Environ
Plant Soil 243:119–130. https://doi.org/10.1023/A:1019993510737 Qual 9:483–487. https://doi.org/10.2134/jeq1980.
Ventura M, Sorrenti G, Panzacchi P, George E, Tonon G (2013) Biochar 00472425000900030032x
reduces short-term nitrate leaching from a horizon in an apple or- Zhang ZP, Show KY, Tay JH, Liang DT, Lee DJ, Jiang WJ (2007) Effect
chard. J Environ Qual 42(1):76–82. https://doi.org/10.2134/ of hydraulic retention time on biohydrogen production and anaero-
jeq2012.0250 bic microbial community. Process Biochem 41:2118–2123. https://
Volokita M, Belkin S, Abeliovich A, Soares MIM (1996) Biological doi.org/10.1016/j.procbio.2006.05.021
denitrification of drinking water using newspaper. Water Res 30: Zhao J, Zhao Y, Zhao X, Jiang C (2016) Agricultural runoff pollu-
965–971. https://doi.org/10.1016/0043-1354(95)00242-1 tion control by a grassed swales coupled with wetland deten-
Waller LJ, Evanylo GK, Krometis LAH, Strickland MS, Wynn- tion ponds system: a case study in Taihu Basin, China. Environ
Thompson T, Badgley BD (2018) Engineered and environmental Sci Pollut Res 23:9093–9104. https://doi.org/10.1007/s11356-
controls of microbial denitrification in established bioretention cells. 016-6150-2
Environ Sci Technol 52:5358–5366. https://doi.org/10.1021/acs.est. Zhao Y, Song X, Cao X, Wang Y, Zhao Z, Si Z, Yuan S (2019) Modified
7b06704 solid carbon sources with nitrate adsorption capability combined
Wan Z, Li T, Liu Y (2018) Effective nitrogen removal during different with nZVI improve the denitrification performance of constructed
periods of a field-scale bioretention system. Environ Sci Pollut Res wetlands. Bioresour Technol 294:122189. https://doi.org/10.1016/j.
25:17855–17861. https://doi.org/10.1007/s11356-018-1954-x biortech.2019.122189
Wang J, Chua LHC, Shanahan P (2017a) Evaluation of pollutant removal Zhou Z, Li H, Song C, Cao X, Zhou Y (2017) Prevalence of ammonia-
efficiency of a bioretention basin and implications for stormwater oxidizing bacteria over ammonia-oxidizing archaea in sediments as re-
management in tropical cities. Environ Sci Water Res Technol 3:78– lated to nutrient loading in Chinese aquaculture ponds. J Soils
91. https://doi.org/10.1039/c6ew00285d Sediments 17:1928–1938. https://doi.org/10.1007/s11368-017-1651-2
Wang S, Lin X, Yu H, Wang Z, Xia H, An J, Fan G (2017b) Nitrogen Zhu Z, Chen Z, Chen X, Yu G (2019) An assessment of the hydrologic
removal from urban stormwater runoff by stepped bioretention sys- effectiveness of low impact development (LID) practices for man-
tems. Ecol Eng 106:340–348. https://doi.org/10.1016/j.ecoleng. aging runoff with different objectives. J Environ Manag 231:504–
2017.05.055 514. https://doi.org/10.1016/j.jenvman.2018.10.046
Wang CS, Wang F, Qin HP, Zeng XF, Li XR, Yu SL (2018a) Effect of Zinger Y, Deletic A, Fletcher T (2007) The effect of various intermittent
saturated zone on nitrogen removal processes in stormwater dry-wet cycles on nitrogen removal capacity in biofilters systems.
bioretention systems. Water 10:13. https://doi.org/10.3390/ Rainwater and Urban Design, Sydney
w10020162
Wang M, Zhang D, Li Y, Hou Q, Yu Y, Qi J, Fu W, Dong J, Cheng Y
(2018b) Effect of a submerged zone and carbon source on nutrient Publisher’s note Springer Nature remains neutral with regard to jurisdic-
and metal removal for stormwater by bioretention cells. Water tional claims in published maps and institutional affiliations.
10(11):1629. https://doi.org/10.3390/w10111629

You might also like