Ecological Engineering 159 (2021) 106085

Contents lists available at ScienceDirect

Ecological Engineering
journal homepage: www.elsevier.com/locate/ecoleng

Review

Three mechanisms of mycorrhizae that may improve stormwater biofilter T

performance
Yussi M. Palacios , Brandon K. Winfrey
⁎

Water Engineering, Department of Civil Engineering, Monash University, 23 College Walk, Clayton, VIC 3800, Australia

ARTICLE INFO ABSTRACT

Keywords: Stormwater biofilters rely on healthy plant communities to perform essential functions of stormwater man-
Green infrastructure agement. Mycorrhizae are a class of fungi which may confer benefits to plants growing in green stormwater
Pollutant removal infrastructure, just as they do in natural ecosystems. Few studies have investigated the roles of mycorrhizae
Fungi outside natural ecosystems or agricultural systems. This review describes three mechanisms of mycorrhizal
Plant performance
symbiosis which could influence plant function in stormwater biofilters. The first mechanism is mycorrhizae
Mycorrhizosphere-rhizosphere interaction
acting as an extension of plant roots, providing water and nutrient for plant growth and resistance to stress.
Plant stress resistance
Through this mechanism metal removal could also be improved. The second mechanism, mycorrhizal interaction
with the rhizosphere, can contribute to soil organic carbon and impact microbial community structures that
ultimately affect the N cycle. A third mechanism is discussed in relation to the impact of mycorrhizae on the
photosynthetic activity of plants and its subsequent effect on plant growth and resistance to environmental
stress. These three mechanisms will be placed into the context of how mycorrhizae could play a crucial role on
plant performance and nutrient and metal removal in stormwater biofilters.

1. Introduction
Stormwater biofilters are a widely adopted type of water sensitive
urban design (WSUD), primarily because of their demonstrated capa-
city to remove pollutants with minimal external energy sources, ease of
incorporation into the urban green infrastructure designs and relatively
low maintenance requirements. It has been widely reported that the
vegetation in biofilters is crucial for mechanical and biological pro-
cesses related to nutrient removal, permeability and hydraulic con-
ductivity (Dagenais et al., 2018; Le Coustumer et al., 2012; Payne et al.,
2015; Read et al., 2009), therefore researchers are increasingly focusing
on improving the performance and roles of plants in stormwater bio-
filters.
Mechanical benefits of vegetation in biofilters are related to changes
in filter media permeability over time. For example, Gonzalez-Merchan
et al. (Gonzalez-Merchan et al., 2012) monitored the development of
clogging in a field study for 7 years, observing progressive clogging for
2.8 years, but after the growth of vegetation, clogging stopped in-
creasing significantly. Virahsawmy et al. (Virahsawmy et al., 2014) also
found that in the presence of vegetation infiltration rates were around
150 mm/h higher than in non-vegetated areas of biofilters. The benefits
of plants on biofilter permeability is related to root structure. Plants
with higher root mass, rooting depth, and diameter help the system to
maintain hydraulic conductivity and reduce clogging (Goh et al., 2017;
Le Coustumer et al., 2012), which can be attributed to the creation of
macropores by the roots (Lewis et al., 2008). In relation to biological
processes, plants have been found to enhance removal of nitrogen,
phosphorus, metals, and, to a lesser extent, hydrocarbons through
processes like uptake, facilitation of rhizosphere processes, and gas
exchange (Dagenais et al., 2018). However, plants are only one com-
ponent of the biofilter ecosystem, which functions with the help of
microbial communities such as bacteria and fungi. These communities
are less studied and may play a crucial role on both mechanical and
biological processes. For example, Morse et al. (Morse et al., 2018)
studied plant-microbe interactions in four plants growing in biofilters,
observing that the abundance of dominant bacterial taxa were influ-
enced by plant species type. It was also found that correlations between
the abundance of denitrification genes, denitrification rates and NOx
removal were likely due to plant-microbe interactions, which indicates
the importance of studying how microbial N cycling affects water
quality over time. In regard to fungi, mycorrhizae may facilitate pro-
cesses in the root zone which have important implications for biofilter
functionality.
Mycorrhizae establish symbiotic associations with more than 80%
of terrestrial vascular plants (Smith & Read, 2008). The two most
common mycorrhizal morphotypes are ectomycorrhizae (ECM), which

⁎
Corresponding author at: Department of Civil Engineering, Monash University, 23 College Walk, Clayton, VIC 3800, Australia.
E-mail address: yussi.delgado@monash.edu (Y.M. Palacios).

https://doi.org/10.1016/j.ecoleng.2020.106085
Received 19 May 2020; Received in revised form 7 October 2020; Accepted 11 October 2020
Available online 28 October 2020
0925-8574/ © 2020 Elsevier B.V. All rights reserved.
Y.M. Palacios and B.K. Winfrey
develop an external and visible fungal mantle around the roots, and
vesicular arbuscular mycorrhizae (VAM), which are a type of en-
domycorrhizae that form intraradical structures in the roots. In both
cases, mycorrhizae also form an external hyphal phase referred to as the
mycorrhizosphere (Linderman, 1988) that extends the influence of
roots beyond the rhizosphere (Choudhary et al., 2016; Linderman,
1991). It is well established that mycorrhizal fungi affect the physiology
of plants, physical structure and chemistry of the soil, and have great
influence on the bacterial community associated to the rhizosphere
(Bulgarelli et al., 2017; Katznelson et al., 1962; Meyer & Linderman,
1986). These functions can benefit plant establishment, plant pro-
ductivity, and re-establishment after natural and/or human interven-
tion, among others (Curaqueo et al., 2014; Glassman et al., 2016; Wagg
et al., 2011). These benefits are well known and applied in other fields
such as in agriculture and ecosystem restoration, but are only just
starting to be explored in stormwater biofilters (Poor et al., 2018). Since
the first stormwater biofilters were described in 1999 (Winogradoff &
Coffman, 1999), thousands of stormwater biofilters studies have been
published. These studies have primarily focused on hydrology, hy-
draulics, and the contribution of media and vegetation to the system
functioning. Only three of these studies have investigated mycorrhizal
fungi in stormwater biofilters. Poor et al. (Poor et al., 2018) and Poor
and Kube (Poor & Kube, 2019) evaluated the role of mycorrhizal fungi
on nutrient and metal removal in biofilter mesocosm studies. In a field
study, (Winfrey et al., 2017) surveyed 32 biofilter plant communities in
three Australian cities for mycorrhizal colonisation of dominant plant
species. About 28% of biofilter plant communities exhibited mycor-
rhizal associations, some of which were observed in species which are
rarely mycorrhizal. Despite the relatively low prevalence of mycor-
rhizal colonisation observed in Australian biofilter plants, roles of these
mycorrhizae could have significant impacts on biofilter performance
and plant establishment (Winfrey et al., 2017).
In order to identify key roles of plants which mycorrhizae might
influence, we first investigated these roles in 205 peer-reviewed studies
published between 1999 to March 2020, which investigated the con-
tribution of plants to biofilter performance. Of these studies, 90, 76 and
30 focused on the contribution of vegetation to nitrogen, phosphorus
and heavy metal removal, respectively. Thirty-seven studies focused on
the contribution of plants to biofilter hydrology or hydraulics. In rela-
tion to environmental stress, 19 studies considered that biofilter plants
can be exposed to water or salinity stress, which affect the performance
of biofilters. Based on the known contribution that plants provide to
this system and some of the environmental factors that affect their
performance, we propose three mechanisms, summarised in Fig. 1,
where mycorrhizae can play a key role in the contribution of plants to
biofilter performance: 1) as an extension of plant roots, 2) in its inter-
action with the rhizosphere, and 3) in the photosynthetic activity of
plants.
2. Mycorrhizae as an extension of Plant roots
One gram of soil can contain up to 111 m of hyphae associated to
VAM (Miller et al., 1995; Smith et al., 2004) and 200 m associated to
ECM (Leake et al., 2004) with diameters between 2 and 20 μm, which is
one or two orders of magnitude narrower than roots (> 300 μm) (Smith
et al., 2010). These small diameters enable hyphae to access areas
unreachable for plant roots and water- and nutrient-filled micropores
(Smith et al., 2010). Also, it has been found that hyphae can adjust their
hyphal diameter depending on the size of the pores, allowing them to
reach compacted soil pores in dry conditions (Drew et al., 2003). The
extension of plant roots by mycorrhizae could enhance the role of plants
in biofilter media.
2.1. The role of root extension in nitrogen and phosphorus removal
Rain events in urban areas cause nitrogen (N) and phosphorus (P) to
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Ecological Engineering 159 (2021) 106085
enter our waterways from impervious surfaces, potentially causing
algae blooms and deteriorated aquatic health. Both N and P are present
in urban runoff in organic and inorganic forms (Li & Davis, 2016).
Plants assimilate N and P through their roots accessing the soil water.
Excessive N and P in urban runoff can be taken up by plants to a certain
extent, but some of these nutrients are re-delivered to the soil when
plants die-off and roots decay.
It has been reported that P particulate is generally removed by fil-
tration through the media (Li & Davis, 2008a; Li & Davis, 2008b; Li &
Davis, 2009; Liu & Davis, 2014) as well as soluble P through adsorption
(Lucas William & Greenway, 2008; Lucas William & Greenway, 2011).
Regardless, some studies show that P removal is enhanced in vegetated
vs. non-vegetated biofilters (Bratieres et al., 2008; Glaister et al., 2014;
Read et al., 2009).
The capacity of filter media to absorb P is determined by the amount
of amorphous iron oxide and aluminium oxide content in the filter
media (Li & Davis, 2016), as well as adsorption breakthrough and ex-
haustion of P, which accumulates and can eventually saturate the filter
media. Soluble P, especially phosphate, can be taken up by plant roots
and be relocated to the shoot (Kadlec & Wallace, 2009), allowing re-
moving P from the system by plant harvesting. Pruning plant material
in biofilters is a common practice as part of seasonal maintenance of
vegetation (Erickson et al., 2018; Payne et al., 2015). This practice is in
increasing interest since it has been discussed (Kadlec & Wallace, 2009;
Roy et al., 2009), mainly because improving the capacity of plants to
absorb phosphorus from the media could be a promising path to in-
crease P removal from biofilter, avoiding a long term P saturation in the
system.
Pore spaces that are unreachable for roots but reachable for hyphae
contain water and nutrients that can be absorbed and transferred from
hyphae to roots (Oades, 1984). It is well known that mycorrhizal plants
establish a bidirectional transfer of nutrients, where especially P and N
are taken up by the external mycelium and transferred to the plant in
exchange for organic C. Unlike non-mycorrhizal plants, these plants
develop two pathways to absorb nutrients, especially P (Javot et al.,
2007; Marcel, 2007). In the “direct pathway”, P transporters located in
the epidermis and hairs of the plant roots facilitate P uptake. Plant
orthophosphate transporters absorb P as orthophosphate from soil close
to the root surface, which is transferred to the roots (Smith et al., 2010).
In the “mycorrhizal pathway,” both fungal and plant P transporters
facilitate P uptake (Smith et al., 2010). The mycorrhizal pathway is
crucial for P uptake in mycorrhizal plants, even in cases when no effect
of mycorrhizae on plant growth has been observed (Hetrick et al., 1996;
Ravnskov & Jakobsen, 1995; Smith et al., 2003). Van der Heijden et al.
(Van der Heijden et al., 1998) inoculated 70 microcosms with 1 kg of
VAM, containing 1, 2, 4, 8, or 14 fungal species. They observed a de-
creasing soil P and increasing plant P with an increasing number of
VAM species, indicating that VAM was crucial for P uptake in the mi-
crocosms. If this same response is observed in mycorrhizal plants
growing in biofilters, P could be removed from the soil by the mycor-
rhizal pathway in addition to the direct plant P uptake by roots. Per-
manent removal of P from the system could be achieved by pruning the
plants Roy (Roy, 2017).
In the case of nitrogen, biofilters can have around 75–85% of N in
dissolved forms, meaning that most of the N removal depends on bio-
logical processes (Dagenais et al., 2018). Nitrogen is decomposed by
mineralization to ammonia, oxidized to nitrite and nitrate (nitrification
process), and finally released to the atmosphere by denitrification or
assimilation of nitrate through plants and microbes. In VAM plants, it
has been found that fungal hyphae developed outside the roots, also
known as extraradical mycelium, have a key role in N uptake; both
nitrate and ammonia are taken up by the fungal extraradical mycelium
before being converted and translocated from the extraradical to the
intraradical mycelium (fungal hyphae developed inside the roots) and
finally incorporated into plant proteins (Govindarajulu et al., 2005).
Because this fungal extraradical mycelium can reach micropores which
Y.M. Palacios and B.K. Winfrey
roots are unable to access, mycorrhizae could also affect the role of
plants in N removal in biofilter systems. To confirm this, studies on N
removal in biofilters that evaluate the effect of mycorrhizae could use
root exclusion and the addition of 15N-labelled nitrogen to the saturated
zone to evaluate movement of nitrogen through hyphae.
2.2. The role of mycorrhizal associations in metal removal
Metals are incorporated into plant tissue through the uptake of soil
water by roots, which can be toxic to plants or essential to growth.
Plants regulate metal concentrations in their tissue to reduce toxicity
and maintain levels of metals which are essential for their metabolic
processes, but toxic at higher concentrations (Clemens, 2001). Plant
physiological processes mediate the tolerance to these metals (Clemens,
2001), which can be affected by mycorrhizal colonisation (Liao et al.,
2003; Weissenhorn et al., 1995; Whitfield et al., 2004; Wu et al., 2007).
In biofilters, the removal of metals from stormwater runoff is largely
driven by sorption to filter media (Davis et al., 2003). Metal sorption
and desorption depend on filter media properties (Feng et al., 2012),
particularly organic matter content (Blecken et al., 2009a) and degree
of saturation (Sun & Davis, 2007). Long-term removal of metals fol-
lowing saturation of sorption sites may be enhanced by vegetation (Sun
& Davis, 2007). Metal uptake by plants varies by species, metal, and
operating conditions (Blecken et al., 2009b). Plant species with higher
metal tolerance and higher biomass are suggested to enhance the long-
term benefits of biofiltration in terms of metal removal (Sun & Davis,
2007).
Mycorrhizae may play a role in metal removal in biofilters in nu-
merous ways. Firstly, mycorrhizal associations can increase plant tol-
erance to metals in metal-contaminated soils (Aloui et al., 2011; Dueck
et al., 1986; Göhre & Paszkowski, 2006; Griffioen et al., 1994; Leyval
et al., 2002). This increased metal tolerance may be due to increased
metal transfer from belowground to aboveground plant parts or
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Ecological Engineering 159 (2021) 106085
Fig. 1. Diagrammatic representation of the three
mechanisms of mycorrhizae that can contribute to
the performance of biofilter. Mycorrhizae can 1) act
as an extension of plant roots, providing additional
water and nutrient for plant growth and resistance to
environmental stress. Through this mechanism metal
up taken could also be imporved. 2) Through its in-
teraction with the rhizosphere, mycorrhizae can
contribute organic carbon to soil and change bac-
terial community structures, which has a key role on
the nitrogen (N) cycle. 3) Mycorrhizae can enhance
energy production by increasing photosynthetic ac-
tivity of plants, having imprtant impact on plant
growth and resistance to stress.
increased biomass production (Göhre & Paszkowski, 2006), allowing
plants to cope with a higher metal concentration in soils. Aloui et al.
(Aloui et al., 2011) studied the effect of VAM on cadmium-stress miti-
gation in Medicago truncatula, in the context of its contribution to the
transfer of Cd from the soil to harvestable above-ground plant tissue.
They found that in the presence of VAM, plants increased their shoot
tolerance to Cd by 33%. However, some of these studies show that the
tendency to increase metal tolerance is both metal- and species-specific
(Aloui et al., 2011; Griffioen et al., 1994).
Mycorrhizae may also increase metal removal in biofilters through
the same mechanism that enhances P removal by increasing the volume
of soil accessible to plant roots, mycorrhizae may facilitate the in-
creased uptake of metals (Aloui et al., 2011). Additionally, as mycor-
rhizae enhance plant nutrition and growth, they provide a sink for the
additional “waste” carbon produced by their plant hosts through the
extended hyphal network (Smith & Read, 1997). This carbon can be
stabilised in the rhizosphere and enhance metal removal through in-
creased sorption (Aloui et al., 2011). In biofilters, additional organic
carbon in the filter media increased copper removal, one of the primary
metals of concern in urban runoff (Blecken et al., 2009a).
2.3. The role of mycorrhizal associations in plant drought tolerance
Plants growing in biofilters are exposed to alternating wet and dry
periods, depending on the environmental conditions. Some investiga-
tions have indicated that prolonged dry periods can impact plant
growth and pollutant removal performance in biofilters (Barron et al.,
2020; Hermawan et al., 2020; Muerdter et al., 2018). This is suggested
because dry seasons can lead to plant death in natural ecosystems
(McDowell et al., 2008). In biofilters, which often consist of sandy filter
media receiving runoff from an area 50–100 times their area (Payne
et al., 2015), plants must tolerate inundation and extended dry periods.
Because the filter media is engineered to maintain high hydraulic
Y.M. Palacios and B.K. Winfrey
conductivity, substrate moisture content can dry rapidly. Indeed, a field
inspection of about 100 stormwater assets revealed poor plant health
and plant death were the most common problems encountered in
stormwater biofilters, (Browne et al., 2014) The authors also identified
substrate moisture content was the most likely cause of diminished
plant health (Browne et al., 2014).
The expanded access to soil micropores can enable mycorrhizal
plants to perform better under dry conditions (Augé, 2001; Ruiz-lozano,
2003; Safir et al., 1971; Safir et al., 1972). Safir et al. (Safir et al., 1971)
compared the resistance to water transport between mycorrhizal and
non-mycorrhizal plants of Soybean. 28 days after the mycorrhizal in-
oculation, mycorrhizal plants presented 40% lower water transport
resistance than non-mycorrhizal plants, followed by doubling plant
height. Under drought conditions, Duan et al. (Duan et al., 1996) stu-
died the influence of mycorrhizae on hydraulic parameters of leaves of
Vigna unguiculata, observing higher stomatal conductance, transpira-
tion, and shoot water potential in mycorrhizal plants than in non-my-
corrhizal ones when soil water content was low. These results lead to
the conclusion that mycorrhizal plants could have access to an extra
source of water in dry soil, provided by the fungi. It was understood
that altered rate of water movement in mycorrhizal plants can be re-
lated to the improvement of P acquisition (Safir et al., 1971), but today
it is also known that mycorrhizae can affect water relations of plants by
other mechanisms unrelated to P uptake (Augé, 2001).
Ruiz-Lozano and Azcón (Ruiz-Lozano & Azcón, 1995) studied the
contribution of mycorrhizal hyphae to water uptake by growing my-
corrhizal Lactuca sativa in containers with three compartments: 1) a
root compartment containing mycorrhizal plants, 2) a hyphae com-
partment, where roots could not penetrate and 3) a second hyphae
compartment where water was supplied. Plants that were supplied with
water in the hyphal compartment 2 showed higher plant fresh weight,
leaf water content, and gas exchange than non-watered plants, in-
dicating that mycorrhizal hyphae can absorb and transfer water to
plants from areas plant roots cannot penetrate.
Other results have also shown that hyphae ability to access more
soil water can result in higher stomatal conductance and transpiration,
better diffusion of nutrients in dry seasons and lower concentration of
xylem abscisic acid in mycorrhizal plants (Augé, 2001; Duan et al.,
1996).
In areas where water stress is a major factor affecting plant health
(e.g., stormwater biofilters and green roofs), leaf water potential
(Farrell et al., 2013) and turgor loss point (Du et al., 2019) can be used
to quantify plant drought tolerance. Plants with lower leaf water po-
tential have been found to tolerate drought conditions (Carmo-Silva
et al., 2009). The extensive review prepared by Augé (Augé, 2001)
showed that 98 out of 110 studies presented positive effects of my-
corrhizae on host gas exchange, water relations, drought tolerance,
and/or growth. Even though more studies need to be done in green
infrastructure systems, these findings indicate that mycorrhizal in-
oculation of biofilter and green roof plants could potentially offer a
solution to one of the major issues of these systems.
3. Mycorrhizae and the rhizosphere
Mycorrhizae have the potential to change and/or increase soil or-
ganic carbon (SOC) composition, which can subsequently affect the
nutrient cycle and hydrocarbon removal through changes in the soil
bacterial community. The main carbohydrate components of mycor-
rhizal hyphae are trehalose, mannitol and glycogen (Bago et al., 2003;
López et al., 2007; Ramstedt et al., 1987). In the case of VAM spores, it
has been found that 28 spores/g soil can contribute up to 919 kg/ha of
spores, of which a large proportion corresponds to SOC (Sieverding
et al., 1989). A correlation between glycoprotein and hyphal length
density in soil suggests that mycorrhizae contribute significantly to soil
organic matter (Lal, 2003; Rillig, 2004; Rillig et al., 2001). Microbial
activity in the rhizosphere depends significantly on the amount of SOC.
4
Ecological Engineering 159 (2021) 106085
Attard et al. (Attard et al., 2011) found that SOC explained 81% of
potential denitrification variance in crop/temporary grassland sites,
indicating that differences in SOC availability have the potential to
change denitrification patterns. Roesti et al. (Roesti et al., 2005) found
that the bacterial community associated with Glomus spores was more
influenced by VAM than host plant identity, which was influenced by
the components of the spore wall, concluding that VAM spores could
provide particular conditions for specific bacteria to grow in the soil.
In biofilters, N removal is driven by biological processes related to
plant growth strategies and plant activity in the rhizosphere (Payne
et al., 2018). In the previous section, it was discussed that mycorrhizae,
acting as an extension or plant roots, could increase N absorption by
plants. By contributing organic carbon and changing the microbial
community in the rhizosphere, mycorrhizae could also contribute to
nitrogen removal in biofilters.
It is known that both VAM and ECM can facilitate the uptake of
soluble inorganic nitrogen, while ECM can also increase uptake of in-
soluble and soluble organic nitrogen (Smith & Read, 2008). However,
the potential mechanisms associated with mycorrhizal-related nitrogen
uptake in biofilters are yet to be described.
One gram of soil can contain up to 111 and 200 m of hyphae as-
sociated to VAM and ECM, respectively, and an estimated 200 to 1.8
million species of bacteria (Leake et al., 2004; Miller et al., 1995;
Roesch et al., 2007; Smith et al., 2004). The relationship between fungi
and soil microbial communities could be crucial for nitrogen removal in
biofilters. (Li et al., 2019) found that the ectomycorrhizal fungi Piso-
lithus tinctorius recovered archaeal amoA gene abundance and deni-
trification enzyme activity under acid rain. Other researchers have
found that VAM can facilitate nutrient uptake activity in plants by its
association with microorganisms such as plant-growth-promoting bac-
teria or nitrogen-fixing bacteria (de Novais et al., 2020; Yadav et al.,
2020). For example, Yadav et al. (Yadav et al., 2020) observed that the
activity of growth-promoting bacteria isolated from native soil in-
creased in wheat cultivars by the presence of VAM, resulting in in-
creases in nitrogen and phosphorus uptake, total chlorophyll content in
leaves and improvement of soil organic matter. In plant species more
closely related to those used in biofilters, Liu et al. (Liu et al., 2020)
studied the effect of mycorrhizae on nitrification and denitrification in
the rhizosphere of a Cyperaceae, Cyperus alternifolius. It was found that,
in plants inoculated with mycorrhizal fungi isolated from local soil,
nitrification and denitrification activity was promoted. Microbial
community structure and biomass analysis revealed changes to the ni-
trifier and denitrifier communities and higher soil microbial biomass in
VAM-inoculated plants (Liu et al., 2020). These results indicate that the
interaction of extraradical mycelium of mycorrhizae with the rhizo-
sphere could contribute to soil organic carbon and microbial commu-
nity structure and activity related to the N cycle in biofilters. Metage-
nomic analysis of microbial communities coupled with N processing in
biofilters with and without VAM-inoculated plants could reveal the
relative importance of mycorrhizae in N removal.
4. Mycorrhizae affects photosynthetic activity of plants
Biofilters are exposed to several environmental changes such as dry
seasons, wetting and drying cycles, temperature and salinity changes,
all of which can affect plant physiology and health. The most important
indicator of health in plants is its photosynthetic activity. It has been
observed that the photosynthetic performance of plants exposed to any
of these environmental stressors can be negatively affected, which is
followed by negative effects on plant growth (Mathur et al., 2019;
Sheng et al., 2008; Zhu et al., 2010). Mycorrhizae have been found to
increase the performance of photosynthesis of plants under water
(Huang et al., 2011; Zhu et al., 2012), temperature (Mathur et al.,
2018) and salinity (Sheng et al., 2008) stress conditions, indicating that
mycorrhizae could contribute to plant health by increasing the photo-
synthetic activity of biofilter plants, especially when they are exposed
Y.M. Palacios and B.K. Winfrey
to environmental stressors.
Mathur et al. (Mathur et al., 2019) studied the role of VAM in the
protection of the photosynthetic apparatus of Triticum aestivum under
water stress by measuring the maximum quantum yield of Photosystem
II (Fv/Fm), which is an indicator of plant photosynthetic efficiency.
They observed that mycorrhizal plants had 32% higher Fv/Fm compared
with non-mycorrhizal plants, as well as higher relative water content in
their leaves and soil. Other parameters such as non-photochemical
quenching and electron transport rate also revealed that mycorrhizal
plants were able to absorb more light for photosynthesis and increase
photosynthetic activity, indicating that mycorrhizal hyphae penetrated
deeper in the soil to provide water to the plants, which protected the
photosynthetic apparatus from dry conditions (Mathur et al., 2019).
Another study showed that inoculation with VAM increased chlorophyll
content and Fv/Fm in Zea mays in drought-stress and control conditions
(Zhu et al., 2012). Similar results have been observed in other plants
such as Cucumis melo (Huang et al., 2011) and Citrullus lanatus (Mo
et al., 2016).
Biofilters installed close to coastal areas can also be exposed to
seawater, affecting plant physiology and growth that lead to biological
immobilisation of N and P (Szota et al., 2015). This, in addition to
biofilters in colder climates commonly treating salt-laden runoff from
de-icing agents, has led to search for plant species that can tolerate
saline conditions while maintaining performance in a biofilter (Szota
et al., 2015; Tahvonen, 2018). It has been found that mycorrhizae can
increase plant tolerance to salt stress; Sheng et al. (Sheng et al., 2008)
tested the influence of VAM (Glomus mosseae) in maize plants growing
under increasing levels of NaCl from 0 to 2 g/kg dry substrate, finding
that under 1.5 g/kg of NaCl, mycorrhizal maize plants showed 24%
higher Fv/Fm and 100% higher net photosynthetic rate than non-my-
corrhizal plants. This increased photosynthetic activity resulted in 3.5
times higher water use efficiency and 2.5 times higher aboveground
biomass in mycorrhizal plants. Inoculation using G. mosseae on Prunus
maritima (beach plum) also resulted in an increase of Fv/Fm, among
other photosynthetic parameters, in plants grown under NaCl level of
2%, which indicated that G. mosseae can alleviate the effect of salt stress
on the photosynthetic activity of P. maritima (Zai et al., 2012). Ad-
ditionally, mycorrhizal Z. mays grown in salt-stressed environments had
increases in multiple photo- and non-photochemical indices when
compared to non-mycorrhizal Z. mays, suggesting the increase in pho-
tosynthetic performance due to mycorrhizal symbiosis can decrease
plant stress (Sheng et al., 2008).
Mycorrhizal plants can also better tolerate temperature stress
(Mathur et al., 2018). Photosynthetic and growth parameters were
compared between mycorrhizal and non-mycorrhizal Zea mays grown
under high-temperature stress of 44 °C. Mycorrhizal plants showed
higher Fv/Fm (0.818) than non-mycorrhizal plants (0.766), as well as
higher total chlorophyll content and net photosynthetic rate, which also
resulted in 30 cm higher shoot height and 12 cm higher leaf length in
mycorrhizal plants (Mathur et al., 2018). Another study performed on
Z. mays investigated the effect of high-temperature stress on photo-
synthesis of mycorrhizal and non-mycorrhizal plants by comparing
plants grown under 25, 35 and 40 °C (Zhu et al., 2011). Net photo-
synthetic rate and Fv/Fm decreased with increasing temperatures in
both mycorrhizal and non-mycorrhizal plants, indicating that 40 °C is a
high-temperature stress condition for this plant species, however, under
that high temperature, mycorrhizal plants showed higher net photo-
synthetic rate, Fv/Fm, and photosynthetic pigments accumulation than
non-mycorrhizal plants (Zhu et al., 2011).
Evaluating the effects of mycorrhizae on biofilter plant photo-
synthetic activity, wherein stressors can be enacted on replicated bio-
filter plants, would contribute to the understanding of plant health in
biofilters. Even though it is well known that biofilters can be exposed to
changing environmental conditions, especially highly variable substrate
moisture content, the effect of these factors on the photosynthetic ac-
tivity of plants grown in biofilters has not been fully studied and even
5
Ecological Engineering 159 (2021) 106085
less so the subsequent effect on biofilter performance. From the 205
peer-reviewed studies examined in this review concerning plant roles in
biofilters, one study considered net photosynthesis rate measurement
(Gong et al., 2019) and two studies considered chlorophyll a measure-
ment as an indication of plant photosynthetic response to pollutant
concentration in biofilter (Choi et al., 2019; Gong et al., 2019). Besides
these studies, we are not aware of any study describing photosynthetic
efficiency of biofilter plants, however, Fv/Fm has been used as an in-
dicator of plant health in green roof studies (Angela et al., 2006; Eksi
et al., 2015; Xie et al., 2018; Young et al., 2017). The role of mycor-
rhizae on the photosynthetic performance of biofilter plants could be
evaluated by measuring a wide range of photosynthetic parameters,
such as Fv/Fm, photosynthetic rate, non-photochemical quenching,
chlorophyll content and photosynthetic capacity. Studies in this research
area would contribute to the understanding of plant health in biofilters,
its effect on growth and biofilter performance.
5. Conclusions
The evidence of both the importance of plants in biofilters and the
role of mycorrhizae in plant establishment and performance suggest
that there are numerous benefits that mycorrhizae can provide to bio-
filters. Based on studies in natural and agricultural systems as well as in
laboratories, we identified three mechanisms in which mycorrhizae
may affect biofilter plant roles and thus biofilter performance: 1) my-
corrhizae can act as an extension of plant roots, providing extra water
and nutrient to plants by penetrating unreachable water and nutrient-
filled micropores in the soil. This could benefit plant growth and re-
sistance to stress as well as increase nutrient and metal removal from
stormwater. 2) In interaction with the rhizosphere, mycorrhizae could
also contribute SOC and impact bacterial community density and
structure in biofilters, both having an important role in the N cycle. 3)
Mycorrhizae could have an important role in the photosynthetic ac-
tivity of biofilter plants, improving plant growth and resistance to
stress, especially when they are exposed to changes in water avail-
ability, salinity levels or temperature.
We have identified mechanisms that could have significant effects
on biofilter performance. Yet, to our knowledge, only three studies have
evaluated mycorrhizae in biofilters to date (Poor & Kube, 2019; Poor
et al., 2018; Winfrey et al., 2017). Consequently, the importance of
evaluating these mechanisms in biofilters is clear. It is important to test
numerous biofilter plant species, inoculants, and environmental con-
ditions. Growing our knowledge of the roles of mycorrhizae and other
soil microorganisms may help to optimise performance, deliver more
reliable performance, and reduce maintenance costs of stormwater
biofilters. Indeed, this research needs to be conducted in a variety of
climatic and ecological regions, where different environmental stressors
and plant-fungal relationships may influence the mechanisms described
in this review.
Biofilters, containing engineered filter media rather than natural
soils, may not support mycorrhizae at the abundance observed in nat-
ural plant communities (Helgason et al., 1998). Indeed, mycorrhizae
are not abundant in Australian biofilters and did not increase with in-
creasing biofilter age (Winfrey et al., 2017). In contrast, older green
roofs supported more mycorrhizae (Chaudhary et al., 2019). In-
oculating biofilters with mycorrhizae may be an effective strategy to
improve biofilter function by improving the health of plants. In bio-
filters, species diversity decreases over time (Winfrey et al., 2018). In-
oculating older biofilters may improve persistence of certain plant
species that would otherwise not survive. In new biofilters, mycorrhizae
may aide plant establishment in sandy biofilter media, as is observed in
restoration of plant communities in mine tailings (Chen et al., 2007;
Hetrick et al., 1994) and sandy soils (Carrillo-Garcia et al., 1999).
However, introducing new mycorrhizal species into biofilters should
be carefully considered. The addition of ‘biofertilizers’ like microbial
and fungal inoculants could shift mycorrhizal communities towards
Y.M. Palacios and B.K. Winfrey
supporting undesired, exotic plant species (Hart et al., 2018). Because
mycorrhizae can be host-specific in their associations with plants and
the benefit to plant productivity they provide (Klironomos et al., 2000),
it is important to consider mycorrhizal species composition in potential
strategies to manage biofilters using inoculants. Currently, there are
significant knowledge gaps in how mycorrhizae might persist in bio-
filters and how they might enhance biofilter functions.
Funding
This work was partially supported by Monash University Faculty of
Engineering Linkage Seed Grant.
Authors contribution
1. Yussi M. Palacios contributed to the conceptualization, in-
vestigation and writing - original draft of the article.
2. Brandon K. Winfrey contributed to the conceptualization, in-
vestigation and writing - review & editing of the article.
We understand that the Corresponding Author (Yussi M. Palacios) is
the sole contact for the Editorial process. She takes up responsibility for
the integrity of work, from inception to finished article and commu-
nication with the other authors about submission progress.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
The authors declare the following financial interests/personal re-
lationships which may be considered as potential competing interests.
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