**7. Continuous and induced phytoextraction**

Phytoextraction, a phytoremediation method observed in 1885 by Bauman [11], is an excellent concept of soil purification, which is not yet commonly applied. In many centers worldwide research is being conducted on phytoextraction in the search for plant species capable of accumulating heavy metals in their aboveground parts. Within phytoextraction of heavy metals from soil we may distinguish the so-called continuous and induced phytoextraction.

Plants used in phytoextraction of heavy metals from soil should exhibit:


**6. The principle of phytoremediation**

588 Environmental Risk Assessment of Soil Contamination

such cases is a lengthy process.

accumulation and hyperaccumulation.

environmental matrices [49, 98, 108, 119]:

by microorganisms colonizing the rhizosphere.

elements.

ment,

organic substances,

atmosphere,

Among soil purification methods biological methods are increasingly often focused on as particularly promising [1, 99, 108]. One of these is phytoremediation, based on the activity of living organisms [40]. It is an alternative method, competitive in relation to other technologies extensively applied in pollutant removal from soil. There are methods facilitating deactivation or removal of toxic substances from the substrate. In most cases they are based on methods of physico-chemical extraction, but their application is connected with excessive costs and complete elimination of soil microorganisms. Reconstruction of semi-natural ecosystems in

Obvious advantages of this biological method include its applicability at the contamination site, as well as relatively low investment outlays and low operating costs at the simultaneous high effectiveness of the process [95]. In the opinion of Salt et al. [107], other factors promoting its more common use are connected with the fact that it is an environmentally friendly process,

The term phytoremediation originates from Greek *phyton* – a plant and Latin *remediare* – to purify. Salt et al. [108], Blaylock and Huang [14], Schnoor [109], Schwitzguebel et al. [111], McGrath and Zhao [86], Vassilev et al. [122], Vangronsveld et al. [121] and Larcher et al. [80] stated that phytoremediation is a technology using higher plants to stabilize and either remove or reduce amounts of soil pollutants, bottom deposits or surface and underground waters. Cunningham et al. [37] and Salt et al. [107] define a plant as a system of filters and pumps powered by solar energy and extracting from its environment and accumulating specific

As it was reported by Pandolfini et al. [96], this biological method is based on the practical use of three types of physiological response to substances found in the environment, i.e. exclusion,

The term phytoremediation refers to the following methods using higher plants to purify

**•** phytodegradation – the use of plants and microorganisms to degrade organic pollutants, **•** phytostabilization – the use of plants to reduce bioavailability of pollutants in the environ‐

**•** phytoextraction – the use of plants absorbing pollutants and accumulating them in organs removed from fields together with crops in order to purify soil from heavy metals and

**•** phytovolatilization – the use of plants to volatilize pollutants and release them to the

**•** rhizodegradation – the use of plants to supplement the bioremediation process performed

**•** rhizofiltration – the use of plant roots to absorb pollutants from water and sewage,

which does not disturb soil structure, and that it may use many plant species.


In continuous phytoextraction heavy metals are absorbed by plants and accumulated continuously with plant growth [14, 20, 46, 85, 110].

Apart from it being economically attractive, continuous phytoextraction is also environmen‐ tally friendly, leaving the site suitable for cultivation of other plants [37, 63].

In urbanized areas continuous phytoextraction may be used in two types of sites. One comprises degraded soils in post-industrial areas, while the other, highly promising as a future application of phytoextraction, is connected with soils in the vicinity of transporta‐ tion routes and in urban green areas. The potential of ornamental plant species most frequently planted in urban locations is investigated in many research centers worldwide.

Such species include also *Tagetes erecta* L. It results from studies conducted by Bosiacki [16, 17] that it is a species exhibiting tolerance to high concentrations of cadmium and lead. When comparing several cultivars of this species the author found that cv. 'Hawaii' has the greatest contents of cadmium and lead in individual aboveground organs. The highest cadmium content (96.06 mg kg-1 d.m.) was found in leaves of *Tagetes erecta* L. cv. 'Ha‐ waii', while that of lead (145.00 mg kg-1 d.m.) was recorded in stems. Accumulation of heavy metals in individual plant organs is not uniform. Bosiacki [15] observed variation in cadmium contents in individual organs of selected ornamental plant species. The highest content of this metal was detected in *Tagetes erecta '*Inca Yellow' in its roots, in *Salvia splendens* 'Fuego' in leaves and stems, while in *Helianthus annuus* 'Pacino' it was in inflorescences. Liu et al. [82] stated that *Calendula officinalis* L. accumulated more Cd and Pb in roots than in shoots, while *Althaea rosea* L. collected greater amounts of these elements in shoots than in roots.

Zhou and Wang [124] when investigating the effect of cadmium on growth in three ornamental plant species stated that *Salvia splendens* L. is most sensitive to Cd, while *Abelmoschus manihot* Medik and *Tagetes erecta* L were most resistant.

Phytoremediation of heavy metals from contaminated areas, including urbanized areas, according to Porębska and Gworek [101] may be conducted using many species of ornamental plants and vegetables, e.g. *Salix viminalis* L. (accumuating Zn and Cd), *Alyssum bertolonii* Desv. (Ni), *Brassica pekinensis* Rupr.(Pb), *Thlaspi caerulescens* J. Presl & C. Presl. (Zn). The same authors stated that wild-growing plants, commonly considered weeds in cultivation of agricultural and horticultural crops, may also be used in bioremediation, e.g. *Atriplex nitens* Schkuhr, *Artemisia vulgaris* L., *Chenopodium album* L., (accumulating greatest amounts of Pb among the tested plants) and *Lacuca serriola* L. (accumulating greatest amounts of Zn).

Antonkiewicz and Jasiewicz [6] assessed suitability of *Helianthus tuberosus* L., *Zea mays* L., *Sida hermaphrodita* Rusby, *Amaranthus sp.* L. and *Cannabis sativa* L. in phytoextraction of heavy metals from soil. In their study the highest contents of cadmium and zinc were detected in amaranth, while that of lead and nickel in Virginia fanpetals. Jerusalem artichoke had the greatest content of copper.

Antonkiewicz et al. [7] when investigating phytoextraction of heavy metals (Cd, Pb, Ni, Zn and Cu) from soil using Virginia fanpetals (*Sida hermaphrodita* Rusby) found that this species absorbed the highest rates of nickel from soil and the lowest of copper.

Many authors for phytoextraction of soils polluted with heavy metals recommended sun‐ flower, corn, rape, amaranth, willows, Miscanthus and strong growing cereals, while for phytoextraction in urban soils he recommended plants with high tolerance to pollution, e.g. London plane, northern red oak, Japanese larch, poplars, field maple, ashes and dogwoods, desert false indigo, false Spirea and forsythia.

Larcher et al. [80] conducted pilot-scale studies in the industrial area of Turin (Italy) using two plant species in phytoremediation of soil to remove heavy metals. They found *Helianthus* *annuus* L. "Holeko HO" and *Brassica juncea* Czern. "Red Giant" to be highly suitable for phytoremediation. Those authors stated that further studies in this respect are needed.

Such species include also *Tagetes erecta* L. It results from studies conducted by Bosiacki [16, 17] that it is a species exhibiting tolerance to high concentrations of cadmium and lead. When comparing several cultivars of this species the author found that cv. 'Hawaii' has the greatest contents of cadmium and lead in individual aboveground organs. The highest cadmium content (96.06 mg kg-1 d.m.) was found in leaves of *Tagetes erecta* L. cv. 'Ha‐ waii', while that of lead (145.00 mg kg-1 d.m.) was recorded in stems. Accumulation of heavy metals in individual plant organs is not uniform. Bosiacki [15] observed variation in cadmium contents in individual organs of selected ornamental plant species. The highest content of this metal was detected in *Tagetes erecta '*Inca Yellow' in its roots, in *Salvia splendens* 'Fuego' in leaves and stems, while in *Helianthus annuus* 'Pacino' it was in inflorescences. Liu et al. [82] stated that *Calendula officinalis* L. accumulated more Cd and Pb in roots than in shoots, while *Althaea rosea* L. collected greater amounts of these elements

Zhou and Wang [124] when investigating the effect of cadmium on growth in three ornamental plant species stated that *Salvia splendens* L. is most sensitive to Cd, while

Phytoremediation of heavy metals from contaminated areas, including urbanized areas, according to Porębska and Gworek [101] may be conducted using many species of ornamental plants and vegetables, e.g. *Salix viminalis* L. (accumuating Zn and Cd), *Alyssum bertolonii* Desv. (Ni), *Brassica pekinensis* Rupr.(Pb), *Thlaspi caerulescens* J. Presl & C. Presl. (Zn). The same authors stated that wild-growing plants, commonly considered weeds in cultivation of agricultural and horticultural crops, may also be used in bioremediation, e.g. *Atriplex nitens* Schkuhr, *Artemisia vulgaris* L., *Chenopodium album* L., (accumulating greatest amounts of Pb among the

Antonkiewicz and Jasiewicz [6] assessed suitability of *Helianthus tuberosus* L., *Zea mays* L., *Sida hermaphrodita* Rusby, *Amaranthus sp.* L. and *Cannabis sativa* L. in phytoextraction of heavy metals from soil. In their study the highest contents of cadmium and zinc were detected in amaranth, while that of lead and nickel in Virginia fanpetals. Jerusalem artichoke had the

Antonkiewicz et al. [7] when investigating phytoextraction of heavy metals (Cd, Pb, Ni, Zn and Cu) from soil using Virginia fanpetals (*Sida hermaphrodita* Rusby) found that this species

Many authors for phytoextraction of soils polluted with heavy metals recommended sun‐ flower, corn, rape, amaranth, willows, Miscanthus and strong growing cereals, while for phytoextraction in urban soils he recommended plants with high tolerance to pollution, e.g. London plane, northern red oak, Japanese larch, poplars, field maple, ashes and dogwoods,

Larcher et al. [80] conducted pilot-scale studies in the industrial area of Turin (Italy) using two plant species in phytoremediation of soil to remove heavy metals. They found *Helianthus*

*Abelmoschus manihot* Medik and *Tagetes erecta* L were most resistant.

tested plants) and *Lacuca serriola* L. (accumulating greatest amounts of Zn).

absorbed the highest rates of nickel from soil and the lowest of copper.

in shoots than in roots.

590 Environmental Risk Assessment of Soil Contamination

greatest content of copper.

desert false indigo, false Spirea and forsythia.

In urban green areas the predominant forms are lawns and turf-covered areas in escarpments, embankments, spoil tips, belts separating roadways, parking lots, gas stations, landfills and industrial waste dumps. Depending on the use of turf areas it is highly important to select appropriate species and cultivars of lawn grasses. It results from experiments conducted by Bosiacki and Zieleziński [23] on the potential of three grass species (*Poa pratensis* L. 'Evora', *Festuca arundinacea* Schleb. 'Asterix', *Festuca rubra* L. *sensu lato* 'Jasper') in phytoextraction of nickel that *Poa pratensis* L. 'Evora' and *Festuca arundinacea* Schleb. 'Asterix' are species showing the greatest capacity to accumulate this metal. In turn, *Festuca rubra* L. *sensu lato* 'Jasper' turned out to be the species showing the greatest capacity to accumulate cadmium and lead [21, 22].

Studies are also conducted on induced phytoextraction using plants producing large amounts of biomass, but additionally such substances as e.g. chelating carriers affecting mobility of individual elements and enhancing pollutant accumulation in plant organs (particularly aboveground parts) are introduced to the environment [35, 92, 123].

Chelating substances are to transform forms of heavy metals sparingly soluble or insoluble in water into forms available to plants. Studies are being conducted using different chelators, both natural and synthetic (e.g. humus substances, low molecular organic acids, citric acid, tartaric acid, amino acids as well as EDTA, EGTA, EDDS, HEDTA, CDTA, EDDHA, DTPA, NTA). Some of them are biodegraded in soil, while others in combination with a heavy metal may be leached to ground waters contaminating them. For this reason it is essential in this technology to determine an appropriate dose and date for the application of a given chelating agent.

It results from preliminary studies (unpublished data) conducted in 2012 by Bosiacki at the Department of Plant Nutrition, the Poznań University of Life Sciences, Poland that EDTA introduced to mineral soil contaminated individually with cadmium at 1.5 mg dm-3 in the form of cadmium sulfate (3CdSO4 8H2O), lead 100 mg dm-3 as lead acetate [(CH3COO)2Pb 3H2O] and nickel 50 mg dm-3 as nickel sulfate (NiSO4 6H2O) caused an increase in the contents of these metals in leaves of *Tagetes erecta* 'Taishan Orange'. Doses of EDTA were introduced to soil in the solution form 35 days after plants had been planted to mineral soil contaminated with these metals. Samples of plant material (leaves) were collected 25 days after the applica‐ tion of EDTA to soil. Contents of individual heavy metals in leaves of *Tagetes erecta* 'Taishan Orange' are presented in Figs. 3, 4 and 5. The research found that acid (EDTA) has improved the efficiency of phytoextraction of cadmium, lead and nickel in soil by Tagetes erecta L. 'Taishan Orange'.

Identification of compounds complexing toxic heavy metals and at the same time biodegrad‐ able in the soil medium is crucial for induced phytoremediation.

At present studies are being conducted at the Department of Plant Nutrition, the Poznań University of Life Sciences, Poland on the application of a biodegradable compound in phytoextraction of heavy metals from contaminated soils.

60

10

**Cd**

150

induced phytoremediation.

induced phytoremediation.

\*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ signific antly) Figure 3. The effect of increasing EDTA doses introduced to soil (contaminated with 1.5 mg Cd dm-3) on cadmium content in leaves of *Tagetes erecta* 'Taishan Orange' \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ significantly) **Doses EDTA (mg dm‐3)** 0 0 25 50 75 100

0 25 50 75 100

70,21c 80 **Figure 3.** The effect of increasing EDTA doses introduced to soil (contaminated with 1.5 mg Cd dm-3) on cadmium content in leaves of *Tagetes erecta* 'Taishan Orange' \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ signific antly) Figure 3. The effect of increasing EDTA doses introduced to soil (contaminated with 1.5 mg Cd dm-3) on cadmium content in leaves of *Tagetes erecta* 'Taishan Orange' \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ signific **Doses EDTA (mg dm‐3)**

antly)

Figure 4. The effect of increasing EDTA doses introduced to soil (contaminated with 100 mg Pb dm-3) on lead content in leaves of *Tagetes erecta* 'Taishan Orange' 268,34e 300 \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ significantly) Figure 4. The effect of increasing EDTA doses introduced to soil (contaminated with 100 mg Pb dm-3) on lead content in leaves of \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ significantly) **Doses EDTA (mg dm‐3)**

178,76d 200 250 **kg‐1d.m.)** *Tagetes erecta* 'Taishan Orange' 268,34e 300 **Figure 4.** The effect of increasing EDTA doses introduced to soil (contaminated with 100 mg Pb dm-3) on lead content in leaves of *Tagetes erecta* 'Taishan Orange' \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ significantly) Figure 4. The effect of increasing EDTA doses introduced to soil (contaminated with 100 mg Pb dm-3) on lead content in leaves of *Tagetes erecta* 'Taishan Orange'

111,25c

Figure 5. The effect of increasing EDTA doses introduced to soil (contaminated with 50 mg Ni dm-3) on nickel content in leaves of *Tagetes erecta* 'Taishan Orange' Identification of compounds complexing toxic heavy metals and at the same time biodegradable in the soil medium is crucial for \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ significantly) Figure 5. The effect of increasing EDTA doses introduced to soil (contaminated with 50 mg Ni dm-3) on nickel content in leaves of *Tagetes erecta* 'Taishan Orange' \*homogeneous groups were identified using the Duncan test, p = 0.05 (values denoted with identical letters do not differ significantly)

Identification of compounds complexing toxic heavy metals and at the same time biodegradable in the soil medium is crucial for induced phytoremediation. **Figure 5.** The effect of increasing EDTA doses introduced to soil (contaminated with 50 mg Ni dm-3) on nickel content in leaves of *Tagetes erecta* 'Taishan Orange'
