Salt tolerant plants increase nitrogen removal from biofiltration systems affected by saline stormwater

Accepted Manuscript Salt tolerant plants increase nitrogen removal from biofiltration systems affected by saline stormwater Dr Christopher Szota, Claire Farrell, Stephen J. Livesley, Tim D. Fletcher PII:

S0043-1354(15)30074-9

DOI:

10.1016/j.watres.2015.06.024

Reference:

WR 11365

To appear in:

Water Research

Received Date: 10 April 2015 Revised Date:

7 June 2015

Accepted Date: 16 June 2015

Please cite this article as: Szota, C., Farrell, C., Livesley, S.J., Fletcher, T.D., Salt tolerant plants increase nitrogen removal from biofiltration systems affected by saline stormwater, Water Research (2015), doi: 10.1016/j.watres.2015.06.024. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Title

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Salt tolerant plants increase nitrogen removal from biofiltration systems affected by saline

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stormwater

4 Author names and affiliations

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Christopher Szota1, Claire Farrell2, Stephen J. Livesley2 and Tim D. Fletcher1

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University of Melbourne, 500 Yarra Boulevard, Richmond, Victoria, 3121, Australia

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Waterway Ecosystem Research Group, School of Ecosystem and Forest Sciences, The

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University of Melbourne, 500 Yarra Boulevard, Richmond, Victoria, 3121, Australia

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Green Infrastructure Research Group, School of Ecosystem and Forest Sciences, The

12 Corresponding author

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Dr Christopher Szota

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Waterway Ecosystem Research Group

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School of Ecosystem and Forest Sciences

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The University of Melbourne

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500 Yarra Boulevard, Richmond, Victoria, 3121, Australia

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Email: ([email protected])

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Phone: (+61) 3 9035 6919

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ACCEPTED MANUSCRIPT Abstract

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Biofiltration systems are used in urban areas to reduce the concentration and load of nutrient

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pollutants and heavy metals entering waterways through stormwater runoff. Biofilters can,

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however be exposed to salt water, through intrusion of seawater in coastal areas which could

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decrease their ability to intercept and retain pollutants. We measured the effect of adding

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saline stormwater on pollutant removal by six monocotyledonous species with different

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levels of salt-tolerance. Carex appressa, Carex bichenoviana, Ficinia nodosa, Gahnia filum,

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Juncus kraussii and Juncus usitatus were exposed to six concentrations of saline stormwater,

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equivalent to electrical conductivity readings of: 0.09, 2.3, 5.5, 10.4, 20.0 and 37.6 mS cm-1.

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Salt-sensitive species: C. appressa, C. bichenoviana and J. usitatus did not survive ≥10.4 mS

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cm-1, removing their ability to take up nitrogen (N). Salt-tolerant species, such as F. nodosa

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and J. kraussii, maintained N-removal even at the highest salt concentration. However, their

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levels of water stress and stomatal conductance suggest that N-removal would not be

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sustained at concentrations ≥10.4 mS cm-1. Increasing salt concentration indirectly increased

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phosphorus (P) removal, by converting dissolved forms of P to particulate forms which were

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retained by filter media. Salt concentrations ≥10 mS cm-1 also reduced removal efficiency of

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zinc, manganese and cadmium, but increased removal of iron and lead, regardless of plant

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species. Our results suggest that biofiltration systems exposed to saline stormwater ≤10 mS

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cm-1 can only maintain N-removal when planted with salt-tolerant species, while P removal

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and immobilisation of heavy metals is less affected by species selection.

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Keywords

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Water sensitive urban design; stormwater treatment; biofiltration; salt-tolerant species;

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nitrogen; phosphorus

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ACCEPTED MANUSCRIPT 1. Introduction

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Impervious surfaces in cities produce large volumes of polluted stormwater runoff which

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flows via drainage systems and sewers directly into waterways. Stormwater is typically

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contaminated with a range of environmental pollutants including: nitrogen (N), phosphorus

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(P), hydrocarbons, heavy metals and sediment (Duncan 1999, Kabir et al. 2014, Taylor et al.

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2005), all of which can have adverse effects on the health of aquatic ecosystems and water

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resources (Walsh et al. 2005). The environmental and financial cost of managing polluted

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stormwater once it has entered a waterway is high, which has led government authorities to

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seek solutions that increase the interception and infiltration of stormwater runoff within the

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urban landscape.

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Biofiltration systems are stormwater control measures specifically designed to reduce

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concentrations of pollutants discharged into urban waterways, including: N, P, and heavy

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metals (Davis et al. 2009, Fletcher et al. 2014). They consist of an engineered profile of filter

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media (primarily sand) planted with vegetation that has high nutrient uptake potential (Hatt

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et al. 2008, Hsieh and Davis 2005). The majority of pollutants associated with particulates,

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including P and heavy metals, are physically removed from stormwater by the filter media,

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while dissolved forms can be removed with varying success through sorption and

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precipitation (Blecken et al. 2009, Glaister et al. 2014). Vegetation can significantly increase

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the removal of dissolved N and P (Bratières et al. 2008, Henderson et al. 2007, Read et al.

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2009) and to a lesser extent heavy metals (Sun and Davis 2007). While it was previously

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considered that denitrification by microbes was a major N-removal process, recent studies

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have shown that plant uptake can account for the majority of nitrate (NO3-) removal (Payne et

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al. 2014). Species selection is critical, with glasshouse column studies showing that some

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plant species removed almost all influent N, while others showed effluent N concentrations

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equivalent to, or even greater than, unplanted columns (Bratières et al. 2008).

77 Biofiltration systems are increasingly installed to mitigate the effects of new and existing

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urban developments on waterways. While installing a large number of small stormwater

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control measures throughout an urban catchment is likely to greatly improve hydrologic and

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water quality outcomes (Burns et al. 2012), competition for space often leads to the

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installation of fewer, but larger, biofiltration systems towards the bottom of a catchment,

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close to the receiving water. Further, coastal communities looking to integrate stormwater

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control measures have little choice but to install them close to the ocean (Felson et al. 2013).

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Integration of biofiltration systems in coastal zones increases the risk of exposure to salt

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water, from sources including seawater intrusion into coastal aquifers and groundwater, as

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well as from storm surges (Barlow and Reichard 2010, Cai et al. 2013). Biofiltration systems

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exposed to seawater may show reduced treatment performance due to the deleterious effect of

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elevated salt concentrations on biological immobilisation of N and P (by reducing plant

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growth and uptake); and on the physical and chemical processes in filter media which are

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largely responsible for removal of particulates and heavy metal pollutants.

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Plant species used in biofiltration systems have commonly been selected based on their

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potential for high uptake of dissolved N and P pollutants, although a range of other local

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drivers of species selection have also been considered (Hunt et al. 2015). Assessments of

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pollutant removal performance have typically been carried out in the absence of salinity and

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therefore selected species may not have the mechanisms to cope with saline stormwater.

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Exposing biofilter plants to elevated salt concentrations may lead to plant water stress, ion

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toxicity and nutrient imbalance, resulting in reduced physiological function, growth and

ACCEPTED MANUSCRIPT nutrient uptake in sensitive species, or glycophytes (Marschner 1995). Salt-tolerant species

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(halophytes) have developed mechanisms to tolerate high salinity. Such mechanisms include

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compartmentalisation of sodium and chloride in cell vacuoles or exclusion of salts at the root

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zone, so as to facilitate continued metabolic and physiological function at external

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concentrations ≥200 mM NaCl (Flowers and Colmer 2008). Therefore, the use of halophytes

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in biofilters has the potential to mitigate the negative effects of elevated salt concentrations

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on plant performance and maintain pollutant removal.

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aquaculture systems suggest that halophytes can effectively maintain removal efficiencies of

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N and P, even at salt concentrations equivalent to seawater (Buhmann and Papenbrock 2013,

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De Lange et al. 2013, Lymbery et al. 2013, Webb et al. 2012).

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Saline stormwater has the potential to reduce the removal efficiency of heavy metals by filter

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media in biofiltration systems (Blecken et al. 2009, Davis et al. 2003, Feng et al. 2012), by

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decreasing sorption through changes to pH and ionic strength. Seasonal pulses of saline

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stormwater, in countries where salt is used to prevent ice formation on roads, have been

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shown to cause leaching of previously immobilised copper, zinc, cadmium, lead and iron

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(Bäckström et al. 2004, Norrström 2005, Norrström and Jacks 1998, Paus et al. 2014b,

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Søberg et al. 2014). As such, saline stormwater may cause biofiltration systems to become a

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source, rather than a sink, for certain heavy metal pollutants.

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This paper explores the potential of using salt-tolerant plant species in biofiltration systems

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exposed to saline stormwater so as to maintain biofilter function. We specifically aimed to

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determine: (i) to what extent saline stormwater reduces the ability of biofiltration systems to

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remove pollutants including: N, P and heavy metals, and (ii) whether salt tolerant species can

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maintain pollutant removal under saline conditions.

ACCEPTED MANUSCRIPT 125 2. Materials and methods

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2.1. Species selection and column construction

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Six Australian monocot species, with a range of salt tolerances, were selected for this study.

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Two species are widely used in biofiltration systems: Carex appressa and Ficinia nodosa,

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and the remaining four represent alternative species: Carex bichenoviana, Gahnia filum,

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Juncus kraussii and Juncus usitatus.

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demonstrated abilities to intercept nutrient pollutants (Bratières et al. 2008).

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bichenoviana is found in dry soils and has a moderate level of salt tolerance. Gahnia filum is

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distributed around coastal saltmarshes and likely has moderate to high levels of salt tolerance.

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Ficinia nodosa is found close to coastal dunes, occurring in highly exposed sites and seeds

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have demonstrated significant salt tolerance (Guja et al. 2013).

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kraussii are commonly found in close proximity to salt marshes (Streever and Genders 1997),

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however, J. usitatus is also found in areas unaffected by salt. Juncus kraussii has been shown

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to be highly salt-tolerant in up to 70% seawater concentrations (Naidoo and Kift 2006).

Carex appressa has low salt tolerance; but has

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Carex

Juncus usitatus and J.

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Juvenile plants were planted into PVC columns in late spring (mid-November) 2013. PVC

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columns were constructed from 150 mm internal diameter pipe, cut to a height of 550 mm

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and an end-cap glued to the base. The interior of each column was roughened with coarse

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sandpaper to minimise preferential edge flows. A 20 mm hole was drilled in each end-cap

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for drainage and mesh (1 mm) placed over the hole. Each column was filled (from bottom to

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top) with: 40 mm of <7 mm diameter gravel, 30 mm of very coarse sand (1-2 mm diameter)

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and 30 mm of fine sand (0.15-0.25 mm diameter); to provide a 100 mm transition layer.

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Above this transition layer, 400 mm of filter media was added, leaving a ponding depth of 50

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mm. The filter media was well-graded, with particle size distribution (by volume) of: 0.5%

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ACCEPTED MANUSCRIPT silt and clay (<0.05 mm), 7% very fine sand (0.05-0.15 mm), 18% fine sand (0.15-0.25 mm),

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37% medium sand (0.25-0.5 mm), 28% coarse sand (0.5-1 mm), 9% very coarse sand (1-2

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mm) and 0.5% fine gravel (>2 mm). Prior to treatment, the filter media had a pH of 6.9, EC

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of 0.031 mS cm-1, cation exchange capacity of 19 cmol+ kg-1 and saturated hydraulic

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conductivity of 210 mm hr-1. After planting into the upper filter media, the columns were

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placed outside for three months until late summer (mid-February 2014) and irrigated daily

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with potable water and once a month with 2 g L-1 soluble NPK (20:20:20) fertiliser. One

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month before the start of the experiment, the columns were moved into a temperature-

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regulated glasshouse and were irrigated with 3L of potable water twice per week.

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Experimental design and dosing procedure

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Semi-synthetic stormwater was used as a base treatment for all columns and was developed

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from methods reported in previous studies (Bratières et al. 2008); where nutrient and heavy

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metal pollutants were added to sediment collected from a constructed wetland to achieve

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target pollutant concentrations derived from reviews of ‘typical’ stormwater pollutant

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concentrations (Duncan 1999, Taylor et al. 2005). Target pollutant concentrations were as

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per Bratières et al. (2008; see Table 2) for total nitrogen (TN), total dissolved nitrogen

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(TDN), oxidised nitrogen (NOx), ammonia (NH3), total phosphorus (TP), total dissolved

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phosphorus (TDP), filterable reactive phosphorus (FRP), zinc (Zn), manganese (Mn),

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cadmium (Cd), nickel (Ni), copper (Cu), chromium (Cr), iron (Fe) and lead (Pb). The target

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total suspended solids (TSS) concentration was approximately half that of Bratières et al.

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(2008), based on recent evaluations of TSS concentrations in Melbourne’s stormwater

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(Francey et al. 2010).

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ACCEPTED MANUSCRIPT Five replicate columns of all six plant species plus an unplanted (bare) column were dosed

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twice per week with 3L of semi-synthetic stormwater, in combination with salt treatments,

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for 3.5 months from mid-March to July 2014. The six salt treatment concentrations were: 0,

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20, 50, 100, 200 and 400 mM of NaCl; equivalent to EC of 0.09, 2.3, 5.5, 10.4, 20.0 and 37.6

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mS cm-1. The three highest salt treatments were gradually applied by stepping up salt

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concentrations by 50-75 mM over a 3 week period prior to the ‘start’ of the dosing period. At

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each dosing event, treatments were made separately in 110L tubs filled with 105 L of potable

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water de-chlorinated with sodium thiosulphate. A 1L stock solution of synthetic stormwater

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containing N, P and heavy metals was added to each tub, followed by the required salt

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treatment, added as NaCl (99.9%). The 110L tubs were agitated to minimise any salinity

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gradients before decanting each 3L volume used to dose each column. Slurry (0.5 mL) was

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added to each 3L volume and thoroughly mixed before dosing each column.

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Plant physiological function

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Leaf gas exchange was measured (0900-1500 hrs) 11 times (every 3-10 days) during the

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experiment using a Li-6400 (Li-Cor Inc., Lincoln, NE, USA); at a photon flux of 1500 µmol

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m-2 s-1, CO2 concentration of 400 µmol CO2 mol-1 and block (chamber) temperature of 25 ºC.

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Only data for stomatal conductance (gs) are presented. Relative humidity in the Li-6400

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chamber was maintained between 45 and 60%. To determine plant water status, pre-dawn

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(0400-0500 hrs) leaf water potential (ΨPD) was measured for all species with living leaves at

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the end of the experiment, using a Scholander-type pressure bomb (Soil moisture Equipment

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Corp., Santa Barbara, CA, USA) lined with wet tissue paper to reduce leaf water loss.

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Biomass measurements

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Plants were harvested at the end of the experiment and above-ground biomass was separated

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into ‘alive’ (green/chlorotic leaves and flowers) and ‘dead’ (brown and desiccated) tissues to

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determine proportion of alive above-ground biomass. Plant material was oven-dried at 70 ºC

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for one week.

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Inflow samples were taken on five occasions during the experiment to check for consistency

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in target pollutant concentrations. At the final dosing event, two inflow samples were taken

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from each 110 L tub and all columns were mounted above 4L buckets to collect the outflow.

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Inflow and outflow samples were refrigerated immediately after collection, then transported

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to a NATA accredited laboratory (Centre for Water Studies, Monash University) the

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following day for determination of pH, electrical conductivity (EC), TSS, TN, TDN, NOx,

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NH3, TP, TDP and FRP. A separate nitrified 60 mL sample was dispatched the same day to a

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NATA (National Association of Testing Authorities) accredited laboratory (Australian

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Laboratory Services, Melbourne) for analysis of total metals, including: Zn, Mn, Cd, Ni, Cu,

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Cr, Fe and Pb. Where pollutant concentrations were found to be below detection limits,

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concentrations were assumed to be half the detection limit (as per Bratières et al. 2008).

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Statistical analysis

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Statistical analyses were performed using R version 3.0.3 (R Core Team 2014). Analysis of

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Variance (ANOVA) was used to determine differences (α = 0.05) in biomass, physiological

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and pollutant removal performance within and between each species (including bare pots)

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across salt treatments. Data were tested for normality using the Shapiro-Wilk test and log-

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transformed where necessary. Tukey’s post-hoc tests were used to describe differences

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between means.

ACCEPTED MANUSCRIPT 223 Results

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Plant physiological function during the dosing period

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The physiological response of plants to increasing salt concentration was rapid, with all

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species showing reduced stomatal conductance (gs) within two weeks of treatment (Figure 1;

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all p<0.001). Differences in gs amongst plant species and salt treatments were maintained

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throughout the experiment, with no significant declines in gs after four weeks (all p>0.05)

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Alive above-ground biomass, plant physiological function and plant water stress at the end of

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the dosing period

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Carex appressa, C. bichenoviana and J. usitatus had reduced alive above-ground biomass at

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salt concentrations ≥20.0 mS cm-1 (all p≤0.001), with no alive above-ground biomass at the

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highest salt concentration for both Carex species, and only 16% alive biomass for J. usitatus

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(Figure 2). Only Ficinia nodosa did not decrease the proportion of alive biomass in response

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to increasing salinity (Figure 2; p=0.513), while J. kraussii and G. filum only reduced alive

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above-ground biomass at the highest salt concentration (p<0.001 and p=0.011).

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At the end of the experiment, all species showed reduced gs with increasing salinity (Figure

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2; all p<0.001), with effectively zero gs in all species except J. kraussii at 37.6 mS cm-1.

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Carex appressa, F. nodosa and J. usitatus were the most sensitive to increasing salt

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concentration, unable to maintain 50% gs (relative to control) at ≤10 mS cm-1.

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bichenoviana, G. filum and J. kraussii showed lower sensitivity and maintained gs >50% at

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≤20 mS cm-1.

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Carex

ACCEPTED MANUSCRIPT Pre-dawn leaf water potential (ΨPD) measurements suggest that C. appressa was the most salt

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sensitive species, with a significant (p<0.001) decrease at >5.5 mS cm-1 (Figure 2). At the

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highest salt concentration, Juncus kraussii was the least sensitive with a ΨPD of -2.1 MPa.

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Ficinia nodosa, G. filum and J. kraussii were moderately sensitive with significantly reduced

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ΨPD at EC >10.4 mS cm-1 (all p<0.001).

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Inflow water quality

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Inflow water samples differed among salt treatments for pH, TSS, TDP and FRP (Table 1).

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There was no clear trend for pH with increasing salinity, whereas TSS was significantly

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higher at ≥20 mS cm-1 (p=0.009). Inflow TP did not differ among salt treatments, however

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TDP and FRP decreased with increasing salt concentration (both p<0.001). While 42% of TP

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was dissolved (i.e., TDP) at the lowest salt concentration, the proportion of TP in dissolved

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form decreased as salt concentration increased, such that only 2% of TP was in a dissolved

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form at the highest salt concentration.

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Outflow water quality: EC, pH and TSS

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Outflow EC was not significantly different than inflow EC (all p>0.05) for all but the lowest

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salt treatment (p<0.001), which showed slightly higher outflow EC (0.111 mS cm-1)

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compared with inflow EC (0.090 mS cm-1). Outflow pH decreased with increasing salt

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concentration for all species (all p<0.001) except J. kraussii (p=0.090) and there were no

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differences between unplanted or planted columns (all p>0.05).

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significantly higher for the lowest salt concentration compared with all other treatments (all

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p<0.05). As a percentage of inflow, outflow TSS was 16.4% for the lowest salt treatment and

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3.4% when averaged across all other salt treatments.

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Outflow TSS was

ACCEPTED MANUSCRIPT Outflow water quality: nitrogen

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Outflow N was mostly in dissolved forms (86% for all columns) and planted columns

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removed 41% and 53% of inflow TN and TDN at the lowest salt concentration (Figure 4).

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All plant species except F. nodosa (p=0.158) and J. kraussii (p=0.691) showed reduced N-

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removal with increasing salt concentration (p<0.001); to the extent that outflow > inflow

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concentrations at 37.6 mS cm-1. F. nodosa and J. kraussii and unplanted columns showed no

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change in outflow TN and TDN with increasing salt (p>0.05). However, outflow TN and

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TDN for unplanted columns were 1.27 and 1.24-fold greater than inflow.

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Similar trends were observed for outflow NOx, where F. nodosa and J. kraussii showed no

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increase with increasing salt concentration (p>0.05) and were the only species not to show

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outflow > inflow NOx at 37.6 mS cm-1 (Figure 4). While outflow NOx was significantly

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higher for unplanted columns across all salt treatments (all p<0.001), outflow NH3 was

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similar between unplanted and planted columns (all p>0.05).

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reduced by 92% relative to inflow at the lowest salt concentration; however efficiency of NH3

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removal decreased to 32% at the highest.

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Outflow water quality: phosphorus

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In contrast to nitrogen, outflow TP decreased with increasing salt concentration for all

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columns (Figure 5; all p<0.001). Outflow TP was reduced by 22% relative to inflow TP at

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the lowest salt concentration, compared with 87% at the highest. Given the significant effect

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of salt on inflow concentrations of TDP and FRP (Table 1), differences in outflow

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concentrations were analysed relative to inflow. Outflow TDP and FRP were higher from

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unplanted columns except at 37.6 mS cm-1 (all p<0.001); where F. nodosa and C. appressa

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showed lower concentrations compared with all other species (p<0.001). Outflow TDP and

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FRP exceeded inflow concentrations at ≥2.3 mS cm-1 for unplanted columns and ≥10.4 mS

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cm-1 for all species.

299 Outflow water quality: heavy metals

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Planted and unplanted columns showed no significant differences in outflow concentrations

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of heavy metals at salt concentrations <37.6 mS cm-1. However, metals differed in their

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response to increasing salt concentration by increasing (Zn, Mn and Cd), decreasing (Fe and

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Pb) or showing no change (Cu, Cr and Ni).

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All columns showed removal efficiencies >85% for Zn, Mn and Cd at the lowest salt

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concentration (Figure 6). F. nodosa and J. kraussii showed significantly higher outflow Zn

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concentrations at the highest salt treatment relative to the lowest (both p<0.05). There was no

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difference in outflow Zn among columns at 37.6 mS cm-1 (p=0.954) and outflow exceeded

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inflow concentration by 13% when averaged for all columns. Outflow Mn increased at 37.6

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mS cm-1 and Cd at 20 mS cm-1, for all columns relative to the lowest salt treatment (all

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p<0.01). Unlike for Zn, removal efficiencies of >75% were maintained for Mn and Cd, even

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at the highest salt concentration. There were no significant differences in outflow Ni, Cu and

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Cr concentrations among salt treatments (all p>0.05), with all columns showing >75%

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removal.

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In contrast, outflow Fe and Pb concentrations actually decreased with increasing salinity,

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similar to the observed response for outflow TDP and FRP (all p<0.001; Figure 6). Again,

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there were no significant differences among plant species at any salt concentration (all

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p>0.05). Outflow Fe exceeded inflow by 15% at the lowest salt concentration and declined

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to 83% of inflow at the highest. Outflow Pb concentrations were much lower than inflow,

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with 80% removal at the lowest salt concentration, increasing to 96% removal at the highest.

323 Discussion

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Effect of salt concentration on nitrogen removal

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A key benefit of plants in biofiltration systems is their ability to remove dissolved N,

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primarily through uptake associated with biomass growth (Barrett et al. 2013, Henderson et

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al. 2007, Payne et al. 2014, Read et al. 2009). Carex appressa is a commonly used species

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for biofiltration systems as it has demonstrated high N-removal capacity (Bratières et al.

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2008). At low salt concentrations in this study, C. appressa demonstrated high N removal

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characteristics; along with C. bichenoviana, and J. usitatus. However, these three species

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were highly sensitive to increasing salinity, showing reduced N-removal (TN, TDN and NOx)

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at ≥10.4 mS cm-1 (≥100 mM NaCl). By the end of the experiment, these species also showed

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little alive above-ground biomass, with impaired leaf physiological function at salt

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concentrations ≥10.4 mS cm-1. Reduced N-removal may have been caused by suppression of

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NO3- uptake due to elevated Cl- concentrations in the cytoplasm (Marschner 1995); however,

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reduced growth and therefore N-demand as a result of increased water stress and chloride

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toxicity was the most likely cause for reduced N treatment efficiency in these salt-sensitive

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species (Flowers and Colmer 2008, Marschner 1995, Munns 2002).

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Reduced uptake of N by salt-sensitive plants under saline conditions therefore indirectly

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promotes leaching of NO3- through biofiltration systems. Further, at high salinities, columns

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planted with salt-sensitive species showed greater outflow concentrations than inflow for TN,

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TDN and NOx, indicating release of previously bio-assimilated N from senescing biomass

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(Payne et al. 2014).

Importantly, this highlights that biofiltration systems planted with

ACCEPTED MANUSCRIPT commonly used salt-sensitive species will not maintain N-removal from saline stormwater

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≥10.4 mS cm-1. Outflow TN and NOx concentrations from salt-sensitive species exceeded

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water quality default trigger concentrations for slightly disturbed lowland rivers in south-

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eastern Australia by 2 to 4-fold (0.5 mg L-1 for TN and 0.04 mg L-1 for NOx; ANZECC &

350

ARMCANZ 2000).

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The N-removal capabilities of biofiltration systems can be maintained, even under high

353

salinity levels (≤20 mS cm-1 or 200 mM NaCl), with appropriate selection of salt-tolerant

354

plant species. Two species (F. nodosa and J. kraussii) showed no increase in outflow TN and

355

NOx with increasing salt concentration.

356

increasing salt concentration, outflow TN exceeded water quality trigger concentrations by

357

57-63% and NOx by 2.6-4.6 times (ANZECC & ARMCANZ 2000). Halophytes, such as J.

358

kraussii, have demonstrated significant potential to remove N from highly saline wastewater

359

(Brown et al. 1999, Lymbery et al. 2006), most likely through compartmentalisation of toxic

360

Na+ and Cl- in certain tissues, enabling continued physiological function at elevated salt

361

concentrations (Flowers and Colmer 2008). Although F. nodosa and J. kraussii were able to

362

maintain alive above-ground biomass and N-removal efficiency at 37.6 mS cm-1 (400 mM

363

NaCl), their leaf physiological function was severely impaired, suggesting that N-removal

364

efficiency would decrease over time. However, despite similar N-removal efficiency and

365

plant water stress at high salt levels, J. kraussii was able to maintain higher stomatal

366

conductance at ≥10 mS cm-1 as compared with F. nodosa, suggesting it has greater potential

367

to maintain N-removal at elevated salinities in the medium to long-term. We therefore

368

suggest that plant species with demonstrated high salt-tolerance (e.g. J. kraussii) should be

369

preferentially selected for biofiltration systems exposed to saline stormwater between 10-20

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Despite maintaining removal efficiencies with

ACCEPTED MANUSCRIPT 370

mS cm-1 for two reasons: (i) they physiologically out-perform species with lower salt

371

tolerance when exposed to high levels of salt and (ii) they maintain high N removal.

372 Effect of salt concentration on phosphorus removal

374

In contrast to outflow N-variables, outflow TP decreased with increasing salt concentration.

375

Unplanted columns only showed marginally higher levels of outflow TP as compared with

376

planted columns, suggesting that the majority of removal happens through physical straining

377

and adsorption to the filter media. It is likely that outflow TP was influenced by changes to

378

the composition of inflow P, as a result of increasing salt concentration. While inflow

379

concentrations of TP were the same for all treatments, the concentration of dissolved P (TDP)

380

decreased significantly with increasing salinity.

381

increasing salt concentration as the majority of inflow dissolved P was converted to

382

particulate P forms; most likely through either precipitation with metal ions or sorption to

383

metal oxyhydroxides or clay particles, and subsequently retained by the filter media (Clark

384

and Pitt 2012, Erickson et al. 2012, LeFevre et al. 2015). As a result, outflow TP at the

385

highest salt concentration was equivalent to default local trigger values for receiving water

386

quality (0.05 mg L-1), as compared with the lowest salt concentration where outflow TP

387

exceeded the trigger value by 5.4 times (ANZECC & ARMCANZ 2000).

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Therefore, outflow TP decreased with

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389

Numerous studies have demonstrated that P is typically bound to suspended solids in storm-

390

and river-water (LeFevre et al. 2015, Withers and Jarvie 2008) and when suspended solids

391

reach estuarine or coastal waters, the high salinity causes them to flocculate and settle (House

392

et al. 1998). However, flocculation may not solely explain the decrease in the concentration

393

of dissolved P in inflow. Rather, an increase in the ability of clay particles (sediment) to sorb

394

dissolved P would be required as salt concentration increased (House et al. 1998). Inflow

ACCEPTED MANUSCRIPT 395

TSS increased with salt concentration, which suggests that high concentrations of Na+ caused

396

dispersion, rather than flocculation.

397

flocculation and dispersion can co-occur in filter media exposed to salt; where larger particles

398

flocculate, while fine particles disperse. In our study, increased dispersion with increasing

399

salt concentration may therefore have increased the available exchangeable surface on clay

400

particles; facilitating greater adsorption of dissolved P which has been observed in high ionic

401

strength solutions at pH >6 (Antelo et al. 2005, Barrow et al. 1980, Geelhoed et al. 1997).

402

Dissolved forms of P have proven the most difficult to remove in biofiltration systems

403

(Erickson et al. 2012, LeFevre et al. 2015) and it is significant that salt concentrations of >5.5

404

mS cm-1 (50 mM NaCl) effectively reduced inflow TDP to the extent that outflow P

405

concentrations decreased.

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Kakuturu and Clark (2015) recently demonstrated

406

Despite the fact that high levels of salt decreased inflow TDP, outflow concentrations of TDP

408

and FRP were higher than inflow concentrations, suggesting a source of dissolved P from the

409

columns. Desorption of P from sediment, precipitates or the filter media itself; perhaps even

410

that retained from the previous dosing event, were the most likely sources of TDP.

411

Liberation of TDP and FRP from media was more likely than P-loss from senescing biomass,

412

as unplanted columns showed higher outflow TDP and FRP with increasing salt

413

concentration compared with planted columns (Bratières et al. 2008, Read et al. 2008).

414

Lower outflow TDP and FRP at low salt concentrations from planted columns most likely

415

suggests plant uptake of TDP, which decreased as salt concentration increased.

416

appressa and F. nodosa showed the lowest outflow TDP and FRP concentrations, which is

417

somewhat surprising considering that these two species represented the worst (C. appressa)

418

and best (F. nodosa) performers with regard to leaf physiological function and N-removal

419

under saline conditions. However, when outflow TDP is expressed relative to inflow, actual

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outflow TDP and FRP concentrations were very low (<0.1 mg L-1) and plants had much less

421

impact on P removal compared with chemical conversion of dissolved to particulate P in

422

inflow.

423 Despite the complexities of interpreting P removal efficiency, higher salt concentrations in

425

semi-synthetic stormwater increased TP removal by filter media, independent of plant species

426

selection. While plant species differed substantially in their ability to take up dissolved P,

427

plant uptake only constituted a very small proportion of TP removal, compared with the

428

physical removal of particulate P by the filter media with increasing salt concentration.

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Effect of salt concentration on removal of heavy metals

431

Filter media removed >75% of Zn, Mn, Ni, Cd and Cu at the lowest salt concentration,

432

consistent with previous studies (Blecken et al. 2009, Davis et al. 2003, Kabir et al. 2014,

433

Read et al. 2008). Filter media have been shown to be largely responsible for heavy metal

434

removal in biofiltration systems (Davis et al. 2003), with the majority being sorbed to organic

435

matter or fine soil particles (Paus et al. 2014a) and only a small fraction taken up by plants

436

(Sun and Davis 2007). Although the filter media used in our study contained no added

437

organic matter, the majority of heavy metals were removed, suggesting that fine soil particles

438

(<3% silt and clay) sufficiently sorbed these metals at low salt concentrations. The lack of

439

difference in outflow concentrations between planted and unplanted columns at high

440

salinities also indicates that plants were not responsible for decreased removal efficiency,

441

despite previous studies showing large differences in removal efficiency among species

442

(Read et al. 2008).

443

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ACCEPTED MANUSCRIPT A large body of work exists for assessing mobilisation of heavy metals with salts as a result

445

of road de-icing in cold climates; as well as the effect of seasonal salinity regimes in estuarine

446

systems with polluted sediments (Du Laing et al. 2008, Norrström 2005, Paus et al. 2014b,

447

Søberg et al. 2014, Warren and Zimmerman 1994). In our study, outflow pH decreased by

448

approximately half a pH unit at high salt concentrations, most likely as Na+ forced H+ into

449

solution; therefore a direct pH effect may explain our observed increase in mobility of Zn, Cd

450

and Mn. Levels of pH are a major determinant of metal stability in soils and a decrease of 1-

451

2 pH units, as a result of elevated salt concentrations has been shown to mobilise Cd, Zn and

452

Cu and lead to leaching losses (Bäckström et al. 2004). Direct metal displacement by Na+

453

and divalent cations including Mg2+ and Ca2+ could also explain why Zn, Cd and Mn outflow

454

concentrations increased at higher salinities (Amrhein et al. 1992, Søberg et al. 2014).

455

However, as we did not assess outflow concentrations of all base cations, we cannot

456

definitively attribute our observed responses to this process. Despite this, Na+ displacement

457

of Cd2+ and Zn2+ from biofiltration sand has been demonstrated in response to relatively low

458

salt concentrations 1 – 4 g L-1; or ~1.5 – 6.2 mS cm-1 (Paus et al. 2014b, Søberg et al. 2014).

459

Outflow Cd increased at a lower salt concentration than Zn and Mn, potentially because Cd

460

has a high affinity for Cl compared with the other heavy metals (Du Laing et al. 2008,

461

Paalman et al. 1994); although the majority of heavy metals do form chloro-complexes at

462

elevated salinities (Amrhein et al. 1992, Bäckström et al. 2004, Norrström 2005, Norrström

463

and Jacks 1998, Paus et al. 2014b). Increased physical loss of fine soil particles as a result of

464

colloid dispersion is less likely to explain increased outflow concentrations of Zn, Mn and

465

Cd, as outflow TSS did not increase with salt concentration. Increased removal efficiency of

466

Fe and Pb is more difficult to explain; however, the fact that outflow Fe and Pb showed a

467

similar response as TDP suggests conversion from dissolved to particulate forms and

468

subsequent filtration by the media.

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ACCEPTED MANUSCRIPT 469 In the absence of outflow data for base cations, or the distinction between total and dissolved

471

heavy metals, the exact mechanisms for observed outflow metal concentrations in relation to

472

salt are difficult to identify. Despite this, removal efficiencies of >75% for all metals except

473

Fe and Pb were maintained at salt concentrations ≤10 mS cm-1. However, as studies have

474

shown significant metal leaching at much lower salt concentrations (Bäckström et al. 2004,

475

Norrström 2005, Søberg et al. 2014), as well as complex interactions between pulses of fresh

476

and saline runoff (Norrström 2005, Paus et al. 2014b); a conservative approach should be

477

taken with regard to the application of saline stormwater to biofiltration systems designed for

478

heavy metal removal.

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479 Conclusions

481

Semi-synthetic stormwater with salt concentrations ≥10.4 mS cm-1 effectively killed salt-

482

sensitive species such as C. appressa, C. bichenoviana and J. usitatus; removing their ability

483

to intercept pollutants. Salt-tolerant species such as F. nodosa and J. kraussii maintained N-

484

removal at higher salt concentrations (≤20 mS cm-1); however, their leaf physiological

485

function was greatly reduced, suggesting that sustained N-removal was more likely to be

486

sustained at salt concentrations ≤10.4 mS cm-1. Increasing salinity, rather than plant uptake,

487

increased removal efficiency of P; by converting dissolved forms of P to particulate forms in

488

the inflow and thus increasing removal by physical straining. Stormwater with salt

489

concentrations >10.4 mS cm-1 reduced removal efficiency of key heavy metals (Zn, Mn and

490

Cd), independently of plant species selection, suggesting that biofiltration may not be the

491

appropriate means to treat stormwater with salinity >10.4 mS cm-1. Existing biofiltration

492

systems exposed to saline stormwater are likely to continue to remove P and heavy metals,

493

but salt-sensitive species will not maintain physiological function, growth or N-uptake and

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ACCEPTED MANUSCRIPT 494

are likely to release N during senescence. However, this study demonstrates that biofiltration

495

systems planted with salt-tolerant species can maintain sufficient physiological function and

496

N-removal at salt concentrations up to 10.4 mS cm-1.

497 Acknowledgements

499

This research was funded by the City of Melbourne and Melbourne Water and we thank Ralf

500

Pfleiderer, Rachelle Adamowicz and Julia Peacock for their support and guidance. Joerg

501

Werdin and Harry Virahsawmy provided vital assistance in the construction, filling and

502

planting of the columns. Harry Virahsawmy assisted in creating the synthetic stormwater

503

treatment and in the collection of sediment for making the slurry. Joerg Werdin provided

504

significant assistance with the final harvest. Tina Hines at the School of Chemistry, Monash

505

University prepared and analysed all water quality samples. We also thank Nick Osborne for

506

providing technical assistance. Fletcher is funded by an Australian Research Council Future

507

Fellowship (FT100100144).

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Withers, P.J.A. and Jarvie, H.P. (2008) Delivery and cycling of phosphorus in rivers: A

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review. Science of the Total Environment 400(1), 379-395.

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Treatment (mS cm-1)

mS cm-1

TSS

mg L-1

TN

mg L-1

TDN

mg L-1

NOx

mg L-1

NH3

mg L-1

TP

mg L-1

TDP

mg L-1

FRP

mg L-1

Zn

mg L-1

Mn

mg L-1

Cd

mg L-1

Ni Cu

mg L-1

mg L-1

Cr

mg L-1

Fe

mg L-1

Pb

mg L-1

1.96 (±0.02) 1.84 (±0.02) 0.95 (±0.02) 0.276 (±0.002)

1.98 (±0.05) 1.82 (±0.02) 0.95 (±0.02) 0.284 (±0.002)

1.96 (±0.02) 1.80 (±0.01) 0.94 (±0.02) 0.286 (±0.002)

0.992

0.39 (±0.006) 0.040C (±0.001) 0.0048BC (±0.0010)

0.392 (±0.009) 0.015D (±0.003) 0.0030C (±0.0006)

0.402 (±0.012) 0.010D (±0.001) 0.0028C (±0.0007)

0.4 (±0.008) 0.010D (±0.001) 0.0026C (±0.0011)

0.545

0.145 (±0.006) 0.230 (±0.012) 0.0039 (±0.0001) 0.0300 (±0.0005) 0.062 (±0.008) 0.0244 (±0.0020) 2.93 (±0.12) 0.1266 (±0.0043)

0.125 (±0.005) 0.222 (±0.014) 0.0037 (±0.0002) 0.0284 (±0.0014) 0.059 (±0.008) 0.0254 (±0.0037) 2.77 (±0.05) 0.1210 (±0.0059)

0.156 (±0.028) 0.236 (±0.011) 0.0037 (±0.0001) 0.0280 (±0.0015) 0.056 (±0.007) 0.0306 (±0.0066) 2.80 (±0.07) 0.1214 (±0.0045)

0.126 (±0.011) 0.239 (±0.011) 0.0038 (±0.0002) 0.0300 (±0.0009) 0.054 (±0.011) 0.0372 (±0.0118) 3.09 (±0.18) 0.1236 (±0.0044)

10.4 6.6A (±0.02) 10.4D (±0.09) 68.8AB (±4.0)

1.98 (±0.04) 1.78 (±0.04) 0.96 (±0.02) 0.274 (±0.006)

1.98 (±0.02) 1.78 (±0.04) 0.94 (±0.01) 0.272 (±0.005)

1.98 (±0.04) 1.82 (±0.02) 0.94 (±0.02) 0.272 (±0.004)

0.412 (±0.006) 0.175A (±0.003) 0.0160A (±0.0017)

0.404 (±0.010) 0.085B (±0.003) 0.0086B (±0.0016)

0.152 (±0.006) 0.232 (±0.010) 0.0039 (±0.0001) 0.0296 (±0.0007) 0.069 (±0.011) 0.0236 (±0.0007) 3.06 (±0.10) 0.1324 (±0.0039)

0.158 (±0.012) 0.239 (±0.012) 0.0042 (±0.0002) 0.0306 (±0.0007) 0.066 (±0.008) 0.0252 (±0.0012) 3.17 (±0.09) 0.1296 (±0.0037)

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EC

P-value <0.001

5.5 6.3C (±0.01) 5.5C (±0.07) 65.8AB (±4.3)

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37.6 6.3C (±0.04) 37.6F (±0.64) 76.8B (±2.7)

2.3 6.4BC (±0.01) 2.3B (±0.04) 64.6AB (±3.5)

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pH

20.0 6.4B (±0.04) 20.0E (±0.19) 75.4B (±2.2)

0.09 6.6A (±0.04) 0.09A (±0.002) 62.6A (±1.4)

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Units

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Variable

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Table 1. Analysis of inflow water samples collected over the course of the experiment (n=5) for each salt treatment. Variables included: pH, electrical conductivity (EC), total suspended solids (TSS), total nitrogen (TN), total dissolved nitrogen (TDN), oxidised nitrogen (NOx), ammonia (NH3), total phosphorus (TP), total dissolved phosphorus (TDP), filterable reactive phosphorus (FRP), zinc (Zn), manganese (Mn), cadmium (Cd), nickel (Ni), copper (Cu), chromium (Cr), iron (Fe) and lead (Pb). Different letters represent significant differences (P<0.05) between salt treatments as determined from ANOVA. Variables showing significant differences between salt treatments are also highlighted in grey.

<0.001 0.009

0.536 0.991 0.061

<0.001 <0.001

0.362 0.901 0.362 0.482 0.783 0.548 0.243 0.417

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Figure 1. Stomatal conductance of salt treatments over time for each species. Mean stomatal conductance is expressed relative to the control treatment (0.09 mS cm-1) and bars represent mean standard error (n=5). Greyscale colour indicates salt concentration, where concentration increases from grey (2.3 mS cm-1) to black (37.6 mS cm-1).

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Figure 2. Alive above-ground biomass (as a proportion of total above-ground biomass), stomatal conductance (gs) and leaf pre-dawn water potential in relation to salt concentration, captured at the end of the experiment. Points represent means and bars represent mean standard error (n=5).

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Figure 3. Outflow concentrations of electrical conductivity (EC), pH and total suspended solids (TSS) collected from the last dosing event. Points represent mean values and bars represent mean standard error (n=5).

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Figure 4. Outflow concentrations of total nitrogen (TN), total dissolved nitrogen (TDN), oxidised nitrogen (NOx) and ammonia (NH3) as collected from the last dosing event. Points represent mean values and bars represent mean standard error (n=5).

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Figure 5. Outflow concentrations of total phosphorus (TP), total dissolved phosphorus (TDP), and filterable reactive phosphorus (FRP) as collected from the last dosing event. The left-hand pane shows actual outflow concentrations and the right-hand pane shows outflow expressed as a proportion (%) of inflow concentration. Points represent mean values and bars represent mean standard error (n=5).

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Figure 6. Outflow concentrations of zinc (Zn), manganese (Mn), cadmium (Cd), nickel (Ni), copper (Cu), chromium (Cr), iron (Fe) and lead (Pb) in relation to salt concentration, as collected from the last dosing event. Points represent mean values and bars represent mean standard error (n=5).

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We evaluated six plant species for use in salt affected biofiltration systems Plants removed nitrogen, while filter media removed phosphorus and heavy metals Salt tolerant plants maintained nitrogen removal, even at high salt concentrations High salt levels actually increased particulate phosphorus removal by filter media Removal of some heavy metals decreased at high levels of salt

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