Identifying plant species that bioaccumulate, hyperaccumulate, or stabilise As is vital for phytoremediation and has been widely studied (
Table 1) [
98]. It is stated that to confirm a As hyperaccumulating species, the above ground biomass must accumulate >1000 mg/kg of arsenic [
120,
121,
122,
123]. The first As hyperaccumulator was discovered by Ma et al. [
14]; the Chinese brake fern,
Pteris vittata, grew on chromated copper-arsenate-contaminated soil. The fronds of
P. vittata contained 1442–7526 mg/kg of As, and contaminated soil had As concentrations ranging from 18.8 to 1603 mg/kg [
14].
P. vittata growing on uncontaminated soil (0.47–7.56 mg/kg, As) was also analysed, and fronds bioaccumulated 11.8–64.0 mg/kg of As [
14]. In general, the expected bioaccumulation of As on uncontaminated soil is 3.6 mg/kg, almost half the bioaccumulation reported for
P. vittata [
14]. The search for additional As hyperaccumulators is currently underway, and reports have identified
Pteris umbrosa as a possible candidate [
98,
124]. A study by Zhao et al. [
124], aimed to identify additional
Pteris species for As hyperaccumulating characteristics.
P. vittata, Pteris cretica,
Pteris longifolia, and
P. umbrosa were exposed to 0–500 mg/kg of As and results showed similar As hyperaccumulating capabilities to those displayed by
P. vittata [
124]. For example, both
P. vittata and
P. umbrosa were efficient in bioaccumulating As in their fronds, 57.1 ± 9.0% and 56.8 ± 4.8%, respectively, a characteristic essential for phytoextraction [
125]. Pteris species are fern plants typically found in rainforests, along coasts, dry regions, and tropical and subtropical landscapes [
126]. The habitat of
P. umbrosa is the east coast of Australia, which might have implications for phytoextraction in non-coastal and arid to semi-arid regions such as Bendigo, a gold mining town in regional Victoria [
98]. Hyper/accumulating plant species currently identified for As are primarily fern species, which have specific climate requirements; this causes concern for their use in phytoremediation projects for gold mine waste locations [
16]. Fern species are unsuitable for arid to semi-arid climates, which are the common environments for gold mining towns. There is a need to identify plant species for phytoremediation projects that are compatible with arid to semi-arid climates, such as tussock grasses, and conducting studies with site-specific soil.
Table 1. Identified plant species and their abilities to phytoextract or phytostabilise arsenic in soil.
Plant Species |
Common Name |
Soil As (mg/kg) |
As Accumulation |
As Stabilisation |
Characteristic |
Reference |
Pteris vittata |
Chinese brake fern |
18–1603 |
1442–7526 mg/kg (fronds) |
|
Hyperaccumulator |
[14] |
Pteris vittata |
Chinese brake fern |
0.47–8 |
11–64 mg/kg (fronds) |
|
Hyperaccumulator |
[14] |
Pteris vittata |
Chinese brake fern |
500 |
6200–7600 mg/kg |
|
Hyperaccumulator |
[124] |
Pteris cretica |
Cretan brake fern |
500 |
6200–7600 mg/kg |
|
Hyperaccumulator |
[124] |
Pteris longifolia |
Longleaf brake |
500 |
6200–7600 mg/kg |
|
Hyperaccumulator |
[124] |
Pteris umbrosa |
Jungle brake fern |
500 |
6200–7600 mg/kg |
|
Hyperaccumulator |
[124] |
Pteris vittata |
Chinese brake fern |
|
57.1 ± 9% |
|
Hyperaccumulator |
[125] |
Pteris umbrosa |
Jungle brake fern |
|
56.8 ± 4.8% |
|
Hyperaccumulator |
[125] |
Cassia alata |
Ringworm bush |
1587 |
ca. 25 mg/kg (shoots) |
ca. 130 mg/kg (roots) |
Phytostabiliser |
[13] |
Pityrogramma calomelanos |
Silver fern |
135–510 |
5130–5610 mg/kg (young fronds) 2760–8000 mg/kg (old fronds) |
88–370 |
Hyperaccumulator |
[127] |
Pityrogramma calomelanos |
Silver fern |
20–8800 |
3820–8350 mg/kg (frond) |
88–370 mg/kg (root) |
Hyperaccumulator |
[128] |
Pteris vittata |
Chinese brake fern |
20–8800 |
4240–6030 mg/kg (frond) |
103–330 mg/kg (root) |
Hyperaccumulator |
[128] |
Athyrium filix-femina |
Lady fern |
74 ± 20.1 |
1.95 mg/kg (leaves) |
7.56 mg/kg (roots) |
Metallophyte |
[129] |
Geranium robertianum |
Herb Robert |
74 ± 20.1 |
1.95 mg/kg (leaves + stems) |
18.3 mg/kg (roots) |
Metallophyte |
[129] |
Rhizomnium punctatum |
Dotted thyme-moss |
218 ± 53.8 |
4.66 mg/kg (whole plant) |
|
Metallophyte |
[129] |
3. Co-Application of Soil Amendments
As discussed, plants can exhibit phytotoxicity and commonly require soil amendments to alleviate toxic conditions and improve plant growth and phytoremediation mechanisms [
16,
110]. Soil amendments also improve physical characteristics such as water holding capacity, permeability, infiltration, drainage, aeration, soil structure, and the microbial community [
95,
110]. There are a variety of inorganic and organic soil amendments that have been studied to enhance plant growth and element bioavailability (
Table 2).
3.1. Organic Amendments
A study by Huang et al. [
13] investigated phytostabilisation and the impacts of three different biochar amendments on mine tailings. Biochar is a carbonaceous material derived from pyrolysis methods that involve heating organic material (in a range of 500–900 °C in a limited oxygen environment) [
13,
130,
131]. The organic matter used to produce biochar is typically biomass, sewage sludge, agricultural waste, and compost [
13,
131]. Biochar has a porous structure, high surface area, and other physiochemical properties that improve soil characteristics such as carbon and water holding capacity (
Table 2) [
131]. The mine tailings had high As and Pb concentrations (1587.1 and 3642.7 mg/kg, respectively), a pH of 6.5, and were low in nutrients such as total carbon (0.3%) and total nitrogen (0.01%) [
13]. A greenhouse pot experiment was implemented over 100 days involving 10 treatments, three biochar types (
Hibiscus cannabinus core, sewage sludge, and chicken manure) at three biochar concentrations (0.4%, 1%, and 3%
w/
w) and one control (mine tailings only) [
13]. The results showed that overall plant shoots and roots increased in biomass and As shoot concentrations decreased by 54.9–77.5% [
13]. Sewage sludge biochar applied at 3% concentration provided the best results for plant growth [
13]. Plant height was 12.1 cm, and root length was 370.9 cm, compared to the control values of 8.1 cm and 112.4 cm for plant height and root length, respectively [
13]. Sewage sludge biochar did not immobilise As; further focus is needed on the potential As release during increased biochar application rates [
13]. Arsenic leaching as a result of organic soil amendments was also reported by Beesley et al. [
42]. Beesley et al. [
42] investigated mine waste soil amended with compost and biochar then monitored the effects on pore water and aqueous soil extracts. It was reported that As leaching was a concern and potential risk for further environmental pollution [
42]. Arsenic leaching into pore water was >2500 µg 1⁻¹ (World Health Organisation drinking water standard is 10 µg 1⁻¹) and was found to be related to pH, dissolved organic carbon, and soluble P [
42]. However, arsenic toxicity was reduced most effectively when compost and biochar were combined, and soil nutrients increased [
42]. A study by Simiele et al. [
132] researched the effects of combined biochar and iron-sulphate-assisted phytoremediation. Simiele et al. [
132] also reported an increase in soil nutrients such as increased pH, electrical conductivity (EC), and reduced metal(loid) concentrations in soil pore water. However, there was no improvement in plant growth, which is essential for phytoremediation projects. Beesley et al. [
42] concluded that field trials to further understand As leaching and effects of organic amendments are needed. Biochar should be investigated further to assess As leaching and its ability to improve soil properties and plant growth.
3.2. Phosphate and Organic Amendments
Barbafieri et al. [
16] investigated the use of phosphate as a soil amendment to improve phytoextraction using crop species suited to the Mediterranean climate and
P. vittata. Their results showed that phosphate was successful at improving As bioaccumulation, and plants showed no signs of phytotoxicity; however, biomass did not increase. A similar study by Niazi et al. [
133] reported that phosphate increased As phytoextraction and improved biomass for
Brassica species under spiked As concentrations of 0–75 mg/kg. Barbafieri et al. [
16] used soil collected from the field, an industrial area, with average As concentrations of 25–2595 mg/kg as a result of chemical plant productions. These As concentrations are considerably higher than the Niazi et al. [
133] study, and the use of As-rich field soil (non-spiked soil) introduced other soil As characteristics (e.g., speciation) that influence mobility and toxicity. For example, in Canada at Giant Mine, the dominant As species present was arsenic trioxide, which is the most bioavailable form of As for humans [
21,
134]. Additionally, a study by Cao et al. [
135] investigated As uptake by
P. vittata with chromated-copper-arsenate (CCA)-contaminated soil (135 mg/kg) and As-spiked soil (126 mg/kg). The study included soil amendments, which were phosphate rock, municipal solid waste, and biosolid compost. Cao et al. [
135] stated that phosphate enhanced As bioaccumulation and removed 8.27% of As from CCA soil and 14.4% from the spiked soil. Compost amendment improved As bioaccumulation in CCA soil but decreased in spiked soil, and it was concluded that soil characteristics influenced the compost treatment [
135]. Phosphate and compost treatment increased As leaching, but this was aided by
P. vittata As uptake. A study by Caille et al. [
55] investigated the use of co-application of phosphate and lime for As bioaccumulation, also using
P. vittata. This study used soil collected from mining and smelting locations in Cornwall, England, and reported that there was no increase in As bioaccumulation. It was also stated that natural As in legacy mine waste soils may not be as easily bioavailable as other sources of As, e.g., industry, CCA, and spiked, because of soil properties. There is a need to assess phytoremediation techniques and soil amendments using mine waste soil collected from the field as results vary depending on the As source and soil characteristics.
3.3. Lime and Organic Amendments
Hydrated lime and organic amendments have been studied to assist phytoremediation projects (
Table 1). A study by Clemente et al. [
94] conducted a field experiment 10 km from the Aznalcóllar mine in Spain to assess two crops of
Brassica juncea and soil amendments for phytoremediation. Field plots were initially fertilised with inorganic fertiliser (8:15:15 N:P:K). Seeds were planted and after the first crop, and the treatments were applied. Treatments included sugar beet lime and organic amendments including fresh cow manure and olive leaves/olive mill-waste mature compost. For the second crop, soils with a pH < 5 were limed before amendments were applied. It was identified that pH affected bioavailability and bioaccumulation over time as well as plant growth and biomass production. Organic matter improved plant survival and growth because soil conditions were enhanced. Manure treatment had the largest biomass production; however, it introduced weeds in the second crop. Compost treatment did not introduce weeds but was less effective at improving biomass and metal uptake. The soil amendments olive mill-waste compost and lime were also studied by Pardo et al. [
93]. Pardo et al. [
93] implemented a 2.5-year field phytostabilisation experiment using
Atriplex halimus and soil amendments, mature olive mill-waste compost, pig slurry, and hydrated lime. Plants assisted with organic amendments ameliorated essential soil nutrients, which improved the soil microbial community. For example, soil enzyme activities, β-glucosidase, urease, and arylsulphatase significantly increased when compost and pig slurry were applied compared to the control. Additionally, dehydrogenase activity and basal respiration also significantly increased for compost and pig slurry amendments compared to the controls. Overall, soil enzyme activity improved with the combination of plant and soil amendment and stimulated the soil microbial community. Phytostabilisation was achieved, ecotoxicity decreased, and water-soluble organic C increased notably with the compost and plant combination. Organic matter was lower in pig slurry, but the plant compensated for organic matter with leaf litter and plant roots. However, the lime treatment did not benefit from plant features because plants did not grow well. Organic amendments improved water-soluble N, and only compost enhanced available P. Water-soluble N was greater in limed soils, which may be a result of poor plant and microbial growth because N was mainly inorganic N and highly bioavailable. Additionally, Pardo et al. [
93] stated that the compost and plant treatment was most effective at decreasing ecotoxicity. A similar study by Clemente et al. [
95] also used
A. halimus and soil amendment compost, pig slurry, and hydrated lime for a field phytoremediation project in a semi-arid mine waste location at El Llano del Beal, Cartagena, Spain. Clemente et al. [
95] also reported that the compost treatment had soil-ameliorating capabilities by improving organic matter, total organic carbon, and soil microbial biomass -C and -N. Plant growth was enhanced by the hydrated lime by 58%, compost by 79% and pig slurry by 89%. Organic soil amendments outperformed the hydrated lime for plant growth, which is also supported by Pardo et al. [
93] and Clemente et al. [
94] who reported poor plant growth in lime treatments and greater biomass production in manure treatments, respectively. Compost as a soil amendment to assist phytoremediation has proven to enhance soil conditions, organic matter, the microbial community, and plant growth and avoid the input of weeds.
Table 2. Phytoremediation combined with organic and/or inorganic soil amendments.
Treatment |
Soil Amendment |
Plant |
Soil As (mg/kg) |
Advantages |
Disadvantages |
Reference |
Organic |
Hibiscus cannabinus core biochar (HB), sewage sludge biochar (SB) and chicken manure biochar (MB) (500 °C 3 h). |
Cassia alata |
1587 |
Plant height and root length increased for SB 3%. SB immobilised elements. HB significantly improved total C. Arsenic availability increased with SB at 3%. |
Conflicting results for As mobility and solubility as well as speciation may play a role. |
[13] |
Organic |
Compost (olive mill-waste + 10% cow manure) Biochar (Orchard prunings pyrolysed at 500 °C |
|
7490 |
Soil + compost + biochar treatment had largest decrease in ecotoxicity using the Microtox method. Soil nutrients and fertility improved. |
As leaching Unknown long-term effects of increased As bioavailability. |
[42] |
Inorganic and organic |
Hardwood biochar (500 °C, 3 h), iron sulphate |
Populus Euramericana clone I45/51, Salix pupurea, Salix vimnalis |
297 ± 30 |
Biochar + iron sulphate increased pH, EC, reduced metal(loid) concentrations in soil pore water. |
Biochar + iron sulphate had no effect on plant growth. |
[132] |
Inorganic |
Phosphate |
Lupinus albus, Helianthus annuus, Brassica juncea, Pteris vittata |
25–2595 |
No signs of phytotoxicity e.g., yellowing of leaves. Increased As bioaccumulation in roots and shoots. P. vittata and H. annuus were most successful at phytoextraction. |
No significant change in biomass growth. |
[16] |
Inorganic |
Phosphate |
Brassica napus, Brassica juncea |
0–75 |
As concentrations increased in shoots. Biomass increased. B. napus was most successful at As uptake. Improved physical and photosynthetic characteristics. |
Results varied between plants. |
[133] |
Inorganic and organic |
Phosphate rock, municipal solid waste and biosolid compost |
Pteris vittata |
135 and 126 |
Phosphate and compost increased As bioaccumulation. Plant mitigated leaching. |
Field soil and spiked soil had different results. |
[135] |
Inorganic |
Phosphate and lime |
Pteris vittata |
361 |
Lime balanced soil pH after phosphate application. |
Phosphate and lime had no significant effect on As bioaccumulation. |
[55] |
Inorganic and organic |
Fresh cow manure. Olive leaves/olive mill-waste mature compost. Sugar beet lime. |
Brassica juncea |
86–634 |
Manure had highest plant biomass production. Organic matter improved plant survival, growth, and soil conditions. |
Manure introduced weeds. As uptake was low, Brassica juncea was not suited for phytoextraction |
[94] |
Inorganic and organic |
Mature olive mill-waste compost Pig slurry Hydrated lime |
Atriplex halimus |
664 ± 28 |
Organic amendments with plants provided soil with essential nutrients, which improved the soil microbial community and were effective at phytostabilisation. Ecotoxicity decreased most notably with compost + plant. Limed soil had highest dissolved N in pore water, mainly inorganic N. |
Plants did not grow well in lime amendment. |
[93] |
Inorganic and organic |
Compost, pig slurry (PS), hydrated lime (HL). |
Atriplex halimus |
664 ± 28 |
Compost improved organic matter, total organic carbon, and soil microbial biomass -C and -N. Plant growth improved with amendments HL (59%), compost (79%) and PS (89%). As leaf concentrations decreased = phytostabilisation. |
HL did not significantly decrease bioaccumulation of As in fruits compared to organic amendments after 12 months |
[95] |