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Use of phytoremediation and biochar to remediate heavy metal polluted soils: A review

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Anthropogenic activities are resulting in an increase on the use and extraction of heavy metals. Heavy metals cannot be degraded and hence accumulate in the environment having the potential to contaminate the food chain. This pollution threatens soil quality, plant survival and human health. The remediation of heavy metals deserves attention, but it is impaired by the cost of these processes. Phytoremediation and biochar are two sound environmental technologies which could be at the forefront to mitigate soil pollution. This review provides an overview of the current state of knowledge phytoremediation and biochar application to remediate heavy metal contaminated soils, discussing the advantages and disadvantages of both individual approaches. Research to date has attempted only in a limited number of occasions to combine both techniques, however we discuss the potential advantages of combining both remediation techniques and the potential mechanisms involved in the interaction between phytoremediators and biochar. We identified specific research needs to ensure a sustainable use of phytoremediation and biochar as remediation tools.
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Solid Earth Discuss., 5, 2155–2179, 2013
www.solid-earth-discuss.net/5/2155/2013/
doi:10.5194/sed-5-2155-2013
© Author(s) 2013. CC Attribution 3.0 License.
Open Access
Solid Earth
Discussions
This discussion paper is/has been under review for the journal Solid Earth (SE).
Please refer to the corresponding final paper in SE if available.
Use of phytoremediation and biochar to
remediate heavy metal polluted soils:
a review
J. Paz-Ferreiro1,2, H. Lu2,3 , S. Fu2, A. Méndez1, and G. Gascó1
1Departamento de Edafologia, ETSI Agrónomos, Universidad Politécnica de Madrid, Avenida
Complutense 3, Madrid 28050, Spain
2Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South
China Botanical Garden, Chinese Academy of Sciences, Xingke Road 723, Guangzhou
510650, China
3University of Chinese Academy of Sciences, Beijing 100049, China
Received: 12 November 2013 – Accepted: 15 November 2013
– Published: 25 November 2013
Correspondence to: J. Paz-Ferreiro (jorge.paz@upm.es)
Published by Copernicus Publications on behalf of the European Geosciences Union.
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Abstract
Anthropogenic activities are resulting in an increase on the use and extraction of heavy
metals. Heavy metals cannot be degraded and hence accumulate in the environment
having the potential to contaminate the food chain. This pollution threatens soil quality,
plant survival and human health. The remediation of heavy metals deserves attention,5
but it is impaired by the cost of these processes. Phytoremediation and biochar are
two sound environmental technologies which could be at the forefront to mitigate soil
pollution. This review provides an overview of the current state of knowledge phytore-
mediation and biochar application to remediate heavy metal contaminated soils, dis-
cussing the advantages and disadvantages of both individual approaches. Research10
to date has attempted only in a limited number of occasions to combine both tech-
niques, however we discuss the potential advantages of combining both remediation
techniques and the potential mechanisms involved in the interaction between phytore-
mediators and biochar. We identified specific research needs to ensure a sustainable
use of phytoremediation and biochar as remediation tools.15
1 Introduction
Industrialisation and technical advances have led to an increase in the use of heavy
metals and heavy metal pollution. Contrary to organic substances, heavy metals are
non degradable and accumulate in the environment. While some soils can have a high
background level of heavy metals due to volcanic activity or weathering of parent ma-20
terials, in other soils anthropogenic activities, including smelting, mining, use of pesti-
cides, fertilisers and sludges are responsible for these high levels of heavy metals.
Soil heavy metal pollution has a pernicious eect on soil microbial properties (Yang
et al., 2012) and on the taxonomic and functional diversity of soils (Vacca et al., 2012).
Soil heavy metal pollution poses a risk to the environment and to human health (Roy25
and McDonald, 2013) due to biomagnification (increases in metal concentration as the
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element passes from lower to higher trophic levels). Some of these elements can be es-
sential for living organisms while some others are non-essential. Even concentrations
of essential elements beyond a certain threshold will have pernicious health eect as
they interfere with the normal metabolism of living systems. It is not the purpose of this
article to review the adverse eects of heavy metals on human or plant health. Kabata-5
Pendias and Pendias (2001) provide a list of toxic eects of heavy metals on plants
and the mechanism involved, while a summary of adverse eects of heavy metals on
human health was provided by Ali (2013). We would like to remind to the reader that
studies on heavy metal pollution are focused on As, Cd, Cr, Hg and Pb as they are
toxic, non-essential heavy metals, and on Cu, Ni and Zn which, although essential, can10
cause health problems in humans or can result in phytotoxicity at high concentrations.
With an increasing amount of literature on heavy metal remediation, we aim to sum-
marise the state of art of two of these techniques situated at the forefront of remediation
practices (phytoremediation, with a focus on phytoextraction and biochar soil amend-
ment) and to discuss their mechanism and how we could combine them to improve15
remediation eorts.
2 Phytoremediation
Phytoremediation is an umbrella term for a series of techniques that combine the disci-
plines of soil microbiology and chemistry and plant physiology (Cunningham and Ow,
1996). Currently the most extended practice for soil heavy metal remediation does not20
address the problem of contamination as it consists on encapsulation or digging and
dumping. Immobilisation or extraction can be expensive and, as a consequence, phy-
toremediation can be considered relatively attractive as it can be used at a relatively low
cost to restore or partially decontaminate a site compared to other options, as the cost
is 5 % of other alternative methods (Prasad, 2003). Other advantages would include its25
good perception as a remediation technique among the general public and being more
environmental friendly than other options, as the introduction of vegetation in the pol-
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luted area can also help to prevent erosion or contaminant leaching. Phytoremediation
consists in the use of plants to remove contaminants from the environment or to trans-
form them into less harmless forms (see Table 1 for a summary of phytoremediation
techniques). Phytoremediation is a relatively new technology as research studies have
been mostly conducted from 1990 onwards.5
Phytoextraction is the main and most promising technique to remove soil heavy
metals. It is based on the use of hyperaccumulators which uptake heavy metals and
then translocate them to aboveground tissues (Table 1). One common way of defin-
ing a hyperaccumulator is as a plant that can store heavy metals at a level 100-fold
greater than common plants without yield reduction (Chaney et al., 2007). On other10
occasions, these types of plants are defined on their basis to accumulate more than
100 mg kg1dry weight of Cd, more than 1000 mg kg1of Cu, Co, Cr, Ni or Pb, or more
than 10 000 mg kg1of Mn or Zn (Baker and Brooks, 1989). Some other authors have
mentioned that these values are conservative and propose these criteria to be lowered
(van der Ent et al., 2013). Species used for phytoextraction must not only accumulate15
high amounts of the target element but also have a high growth rate, tolerate the toxic
eects of the heavy metals, be adapted to local environment and climate, be resistant
to pathogen and pests, be easy to cultivate and repulse herbivores to avoid food chain
contamination (Ali et al., 2013).
To date, more than 400 species have been identified as hyperaccumulators, includ-20
ing more than 300 Ni hyperaccumulators (Li et al., 2003). In contrast with Ni only
a few plant species have demonstrated the potential to accumulate Cd, Cu, Pb, and Zn
(Brooks, 1998). Many phytoremediators belong to the taxonomical order of Brassicales
and phytoremediators are also abundant in Asterales, Solanales, Poales, Malpighiales,
Fabales, Caryophyllales and Rosales (Shao et al., 2011). The amount of metal ex-25
tracted from the soil depends not only of the plant species utilised but also on the type
of soil and climate of the region (Shao et al., 2011).
The mechanism and reasons of phytoaccumulation remain unknown. Metal concen-
trations are higher in the shoots compared to the roots, suggesting that there could be
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an ecological role, leading to protection against insect, herbivore or fungal attack, by
making the leaves toxic or unpalatable.
Phytoextraction has three main purposes: firstly, to remove the contaminant from
the soil or contain it, secondly phytoextraction of elements that have market value and
finally gradually improving soil quality to cultivate crops with higher market value (Van-5
grosweld et al., 2009).
There are a number of problems associated with the eectiveness of this remedia-
tion technique. Phytoremediation might not be suitable in areas were the heavy metal
concentration is too elevated as plants could show symptoms of phytotoxicity. In ad-
dition, most of the phytoaccumulators have slow growth rate or produce few biomass,10
limiting the amount of metal uptaken.
Manipulation of soil pH, soil nutrient content or soil organic matter can also be under-
taken to improve metal hyperaccumulation. In this sense, these additional agronomic
practices can be carried out when heavy metal concentrations in the soil are too ele-
vated to reduce plant stress (Adriano et al., 2004; Gabos et al., 2011; de Abreu et al.,15
2012). Thus, liming can allow the decrease of the heavy metal available fraction, thus
enabling vegetative growth, while fertilisers can improve phytoextractor growth. On the
other hand, both liming and fertiliser addition can alter the mobility and speciation of
soil heavy metals. As an example, Li et al. (2012) found that Cd removal from soil was
enhanced by the phytoaccumulator Amaranthus hypocondriacus after NPK or NP fer-20
tilisation due to an increase on plant biomass. However, they found that N alone did not
increase plant biomass and led to a limited increment in phytoextraction. Other stud-
ies (Huang et al., 2013) have found that P fertilisers can decrease soil pH, enhancing
the mobility of Cd and leading to increased phytoextraction by Sedum alfredii. When
adding a phosphate fertiliser to promote phytoremediation, the choice of amendment25
should be carefully chose as cations (K+, Na+, Ca+2or NH+
4) associated with the phos-
phate could aect the mobility of heavy metals (Bolan et al., 2003; Huang et al., 2013).
Indeed, plant growth (Oo et al., 2013) and the mobility of dierent elements in the soil
(Ahmad et al., 2013) can be related with soil salinity. For example, Stevens et al. (2003)
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observed that Zn2+and Pb2+mobility increased with the increment of electrical con-
ductivity. Dierences in soil pH caused by the addition of dierent phosphate fertilisers
can also lead to dierences in phytoextraction (Mandal et al., 2012). Urea has also
been used to alleviate plant stress and improve B phytoextraction by the plant species
Brassica juncea (Giansoldati et al., 2012).5
Organic amendments such as chicken manure have also been shown to increase
growth of the species Rorippa globosa (Wei et al., 2011). Chicken manure addition
resulted in a decrease in soil extractable Cd and thus, the concentration of Cd in the
shoots was lower in soils amended with chicken manure than in soils amended with
urea or in the controls (soil +phytoremediator). However, the total concentration of10
metal extracted in the shoots was in both cases higher than in the control. Other ma-
terials such as pig manure vermicompost can also be used to improve plant yield and
assist phytoremediation, as demonstrated by Wang et al. (2012) in an experiment using
Cd as target heavy metal and Sedum alfredii as phytoremediator. Indeed, the use of
organic amendments has numerous applications, for example, Siebielec and Chaney15
(2012) have demonstrated the eectiveness of biosolids compost in the rapid stabiliza-
tion of Pb and Zn and revegetation of military range contaminated soils increasing tall
fescue growth by more than 200 % while Clemente et al. (2012) recovered a land con-
taminated by mining activity with Cd, Cu, Pb, and Zn by combination of the halophytic
shrub Atriplex halimus L. with pig slurry.20
The use of chelators such as citric acid or EDTA has also been sometimes advised to
assist phytoremediation, with the aim of increasing the mobility of soil heavy metals and
thus plant extraction (Zhou et al., 2007; Freitas et al., 2013). However, we should bear
in mind that the use of chelators can originate other environmental problems including
toxicity for plants and metal leaching (Zhou et al., 2007).25
In addition, experiments should be done to account for the potential impact of climate
change on the capability of phytoextractors to accumulate heavy metals, which at the
moment is uncertain (Rajkumar et al., 2013).
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Finally, we would like to remark that pot experiments are a good first approach to
evaluate the potential of a phytoextractor, but they cannot substitute field experiments
as the uptake of heavy metals is higher in pots than for the same soil in the field
(see for example, Marschner, 1986). This can be due to dierences in soil moisture
or microclimate and to the fact that field-grown plants can reach down to less polluted5
soil.
3 Biochar
Biochar is a porous, carbonaceous product obtained from the pyrolysis of organic ma-
terials. Numerous materials can be used as feedstocks, including sludges, plant ma-
terials and manures. Although the use of charcoal (wood biochar) has been common10
since preterit times, the idea of using other feedstocks for biochar production is new
and relatively unexplored. Typically biochars have high cation exchange capacity and
are alkaline. Biochar has many potential benefits on soil properties as an increase in
soil biological activity (Lehmann et al., 2011; Paz-Ferreiro et al., 2012), diminishing soil
greenhouse gas emissions from agricultural sources and thus enhancing soil carbon15
sequestration due to its elevated content of recalcitrant forms of carbon (Gascó et al.,
2012). The changes brought about by biochar addition to the soil will cause alterations
in soil quality (Paz-Ferreiro and Fu, 2013) with the potential to increase agricultural
yields (Jeery et al., 2011; Liu et al., 2013). The multiple benefits of biochar for soil
have been compiled recently in the book by Joseph and Lehmann (2009). However,20
little information was available in this book about the eect of biochar on soil heavy
metals.
4 Studies on the eect of biochar on soil heavy metals
Table 2 shows a brief summary of the latest papers about the eect of biochar on soil
heavy metals. Fellet et al. (2011) tried to use biochar to remediate a multicontaminated25
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mine soil. Biochar addition did not result in the decrease of the total heavy metal con-
tent of the soil, however, biochar addition reduced the bioavailability of Cd, Pb and Zn
and the mobility (measured using a leaching experiment) of Cd, Cr and Pb.
Earthworms can be added to soil at some stages of ecological restoration due to
their well established positive eects on soil properties as organic matter content,5
soil formation, soil aeration and nutrient cycling. Sizmur et al. (2011) tested a pol-
luted soil collected in the vicinity of a Cu mine using biochar in combination with
compost and earthworms (Lumbricus terrestris). They found all treatments (biochar
alone, biochar +compost and biochar +compost +earthworms) to reduce the amount
of heavy metals compared to the control soils. A limiting aspect when using earthworm10
with remediation purposes is that their addition to soil could lead to the mobilization of
heavy metals and hence to an increase of plant heavy metal concentrations. Interest-
ingly, Sizmur et al. (2011) found that the treatments containing biochar and earthworms
did not result in higher heavy metal mobility or plant availability.
Park et al. (2011) studied the eect of two biochars in a heavy metal spiked soil and15
a naturally strongly polluted soil. They performed a sequential extraction of some heavy
metals. They found chicken manure biochar eective to reduce extractable concentra-
tions of Cd and Pb, but not Cu concentration, while green waste biochar was more
eective to diminish all of the heavy metals studied. Heavy metal fractions bonded to
organic matter increased after biochar addition. Both biochars also decreased Cd and20
Pb presence in soil pore water.
Uchimiya et al. (2012a) analysed the eects on soil heavy metals concentrations of
10 biochars prepared from 5 feedstocks at two dierent temperatures. They observed
that manures with a high or low proportion of ash or P were less eective to immobi-
lize heavy metals. In contrast, biochars prepared at 700C were more eective, which25
could be attributed to transformations in the material, including the removal of nitro-
gen containing heteroaromatic and leachable aliphatic functional groups. They found
Cu and Pb relatively easily to stabilize in soil, while Cd and Ni response depended
strongly on the type of biochar added to the soil.
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Beesley and Marmiroli (2011) detected a retention on biochar surface of As, Cd and
Zn. These authors proved that sorption of the metal was produced at the biochar sur-
face and that this process was not immediately reversible. Leachate concentrations of
Cd and Zn were reduced 300 and 45 folds, respectively. However, leachate concentra-
tions of As did not diminish.5
Namgay et al. (2010) reported that the concentrations of Cd, As and Pb in maize
shoots decreased after biochar application. Beesley et al. (2013) reported interesting
results, finding that As can increase in soil pore water after biochar addition, but trans-
fer to the plant be reduced. This would imply that, at least some biochars, could pose
no risk of increasing heavy metals in plants and hence are safe in terms of food chain10
transfer, but leaching of As to nearby waters must be considered. Karami et al. (2011)
added biochar to a mine soil polluted with Pb and Cu. They found that biochar addi-
tion reduced pore water Pb concentrations to half their values in the mine soil. When
biochar was combined with greenwaste compost the levels of Pb concentrations in
the pore water were 20 times lower than in the control. Jiang et al. (2012) found that15
the acid soluble fractions of Pb(II) and Cu(II) diminished by 18.8–77.0% and 19.7–
100.0 %, respectively, depending on biochar concentration. However, only 5.6–14.1 %
of acid soluble Cd(II) was immobilised. Hartley et al. (2009) observed no increase on
As transfer to plants in three soils planted with Miscanthus. They warned, however, that
alkalyne biochars could mobilise As. It is a well know fact that As behaves dierently20
to other metals with respect to pH, as As mobility is reduced in acid soils due to ad-
sorption on iron oxide surfaces. Zheng et al. (2012) studied the eect of three biochars
on dierent heavy metals (see Table 2) using a multi-polluted soil planted which they
planted with rice. They found Cd, Pb and Zn to be reduced on rice shoots, in particular
when using straw-derived biochar. However, As in rice shoots was increased by biochar25
addition. More importantly, we believe that this is the first study considering the eect
of particle size of biochar on plant heavy metals. The authors found that decreases in
particle size resulted in less Cd, Zn and Pb accumulating in the rice plants.
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Hydrochars could also be used for soil heavy metal inmobilization, however there is
a lack of studies on the topic. Hydrochars are produced after pyrolysis of organic matter
rich materials in the presence of subcritical liquid water. This technique can be applied
to obtain pyrolysed products from wet feedstocks. In principle the adsorption capacity of
hydrochars seems to be reduced compared to biochars or other adsorbents due to the5
fewer functional groups containing oxygen present on hydrochar surfaces. However,
Xue et al. (2012) have demonstrated experiments that the use of activated hydrochars
could overcome these problems. They performed a series of batch and columns ex-
periments to show how this type of hydrochar could reduce Pb on water. The potential
applicability of hydrochar to address soil heavy metal pollution remains untested. How-10
ever, hydrochars tend to be acidic and could possess phytotoxic or genotoxic risks
(Busch et al., 2013), which would deem them unsuitable in restoration projects.
There is a lack of studies concerning how pyrolysis conditions aect biochar prop-
erties as heavy metal sorbent. To fill this gap, Uchimiya et al. (2011b) performed an
experiment using wood and grass biochars prepared at 5 dierent temperatures and15
another one (Uchimiya et al., 2012b) used poultry litter prepared at 4 dierent temper-
atures to study lead retention. From the first experiment they suggested using biochars
prepared at high temperature (650to 800 C) for remediation purposes. In addition
they recommended to perform acid or other oxidant post-treatment in order to increase
oxygen-containing surface functional groups (carboxyl, carbonyl and hydroxyl) which20
have a great importance in relation to heavy metal sorption into biochar. In the case
of the chicken litter biochar they found that lower production temperatures were more
suitable than higher ones due to the stabilizing eect. Higher rates of amendment were
necessary in their experiments for chicken manure biochar to get the same remediation
eect than plant derived biochars.25
It is expected that as biochar is in contact with soil for a prolonged period of time,
oxidation, both biotic and abiotic, would result in the alteration of biochar, a process
known as aging. This process, which would result in the formation of carboxylic, phe-
nolic, carbonyl, quinones and hydroxyl functional groups and which can be emulated
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under laboratory conditions was studied by Uchimiya et al. (2010). These authors found
that the immobilization of heavy metals related to their lability, i.e. it followed the or-
der Cu(II) >Cd(II) >Ni(II). Aging did not impact heavy metal immobilisation, except for
a small increase in Ni.
All of the above experiments have been conducted under laboratory conditions.5
We would urge scientist to design experiments to help to demonstrate the benefits
of biochar against heavy metal pollution under field conditions. The only field study
available (Cui et al., 2011), to our knowledge, shows that biochar can be used to re-
duce Cd uptake in paddy fields. The study consisted on two annual measurements, so
it remains to explore the need to reapply biochar after more extended periods of time.10
5 Mechanism of interaction between biochar and heavy metals
Biochar characteristics are a function of several factors, including the type of feed-
stock, the particle size of the feedstock and temperature and conditions of pyrolysis.
The wide range of characteristics that biochar might posses makes some particular
materials more suitable than others to remediate dierent heavy metals. Therefore,15
when selecting a biochar for remediation purposes scientists should be aware not only
of soil type and characteristics but also on biochar properties.
Before reviewing the mechanisms implied in the interaction between biochar and
heavy metal it is necessary to note that biochar act on the bioavailable fraction of soil
heavy metals and that they can reduce also their leachability.20
One of the characteristics of biochars is possessing large surface areas which imply
a high capacity to complex heavy metals on their surface. Surface sorption of heavy
metals on biochar has been demonstrated on multiple occasions using scanning elec-
tron microscopy (Beesley and Marmiroli, 2011; Lu et al., 2012). This sorption can be
due to complexation of the heavy metals with dierent functional groups present in the25
biochar, due to the exchange of heavy metals with cations associated with biochar such
as Ca+2and Mg+2(Lu et al., 2012) or other such as K+, Na+and S (Uchimiya et al.,
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2011c) or due to physical adsorption (Lu et al., 2012). Also oxygen functional groups
are known to stabilise heavy metals in the biochar surface, in particular (Uchimiya
et al., 2011c) for softer acids like Pb(II) and Cu(II). In addition, Méndez et al. (2009)
observed that Cu2+sorption was related with the elevated oxygenated surface groups
and also with high average pore diameter, elevated superficial charge density and Ca2+
5
and Mg2+exchange content of biochar. Possibly, sorption mechanisms are highly de-
pendent on soil type and the cations present in both biochar and soil. Some other
compounds present in the ash, such as carbonates and phosphates (Cao et al., 2009;
Karimi et al., 2011) can also help to stabilise heavy metals by precipitation of this com-
pounds with the pollutants.10
Alkalinity of biochar can also be partially responsible of the lower concentrations of
available heavy metals found in biochar amended soils. Higher pH values after biochar
addition can result in heavy metal precipitation in soils. Biochar pH value increases
with pyrolysis temperature (Wu et al., 2012) which has been associated to a higher
proportion of ash content.15
Biochar can also reduce the mobility of heavy metals altering the redox state of those
(Choppala et al., 2012). As an example biochar addition could lead to the transforma-
tion of Cr+6to the less mobile Cr+3(Choppala et al., 2012).
The relative contribution of the dierent mechanisms to heavy metal immobili-
sation by dierent biochar remains unknown, although some authors like Houben20
et al. (2013a) postulate that it is mostly a pH eect.
6 Combining biochar and phytoremediation
There is an abundance of reports in the literature about amendments such as lime
and compost being used to reduce the bioavailability of heavy metals (Komárek et al.,
2013) and thus, having the potential to be combined with phytoremediators (de Abreu25
et al., 2012). Biochar, as reviewed before, can also stabilise soil heavy metals in soils
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and thus reduce plant uptake. However, until recently there was a lack of experiments
trying to combine both approaches to soil remediation.
Biochar is commonly reported in the literature to increase plant growth, hence there
is a potential of biochar to increase the yield of phytoremediators. This increase in plant
productivity is highly heterogeneous and has overall been quantified as 10% (Jeery5
et al., 2011; Liu et al., 2013). However, there are several factors that limit the accuracy
of the figure provided by Jeery et al. (2011) and Liu et al. (2013) and that could skew
the data. To date most of the field experiments have been conducted in the short-term,
being limited to a period of 1–2 yr and there are a high relative number of laboratory
mesocosms incubations (with a duration of 1–2 months) included in the dataset. Also10
the dataset in this review comprises a higher number of experiments in tropical latitudes
compared to temperate ones. Finally, we should bear in mind that a high heterogeneity
in the response was detected, depending on the type of soil and plant utilised.
Improvements in plant yield after biochar addition are often attributed to increased
water and nutrients retention, improved biological properties and CEC, eects on nutri-15
ent cycling and turnover and improvements in soil pH. Many of these eects are inter-
related and potentially they could act synergistically. In general, acid soils with a coarse
texture or a medium texture are more prone to produce increases in crop productivity
(Jeery et al., 2011; Liu et al., 2013). In the last years the scientific community has also
raise awareness over the improvement of plant responses to disease as an additional20
benefit of biochar soil amendment (Graber et al., 2010). As said before, biochar can
alter soil microbial community, possibly including an increase in beneficial organisms
that produce antibiotics and can protect plants against pathogens. Another mecha-
nism could be compounds included in biochar such as 2-phenoxyethanol, benzoic acid,
hydroxy-propionic and butyric acids, ethylene glycol and quinones suppressing some25
of the pathogens present in the microbiota (Graber et al., 2010; Elad et al., 2011).
In principle, biochar prepared from any material would have the potential to increase
plant yield and thus be used in combination with phytoremediation. However, the use of
sewage sludge biochar would be unadvised due to its generally negative eect on crop
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performance (Jeery et al., 2011). Caution should also be taken with the presence of
heavy metals in sewage sludge biochars, although some studies (Méndez et al., 2012;
Hossain et al., 2010) show that the metals present in the biochar are not in mobile
forms.
There has been a recent interest about the possibility of combining phytoremediation5
with other potential plant uses such as using plants that can be used to obtain bioen-
ergy (de Abreu et al., 2012). While heavy metal contaminated areas are not suitable
for food production, planting biocrops could promote soil organic matter stocks and
reduce soil pollutants (Hartley et al., 2009). Willow and poplar, have been commonly
used as biocrops and they can be utilised for phytoremediation purposes due to their10
high uptake of heavy metals and fast growing rates (Baum et al., 2009). And in fact,
it has been shown recently that biochar can improve the grennhouse gas balance of
other bioenergy crops such as Miscanthus (Case et al., 2013).
It is also worth to mention that for long phytoextractors were considered to be non-
mycorrhizal. However, in the last year it has been demonstrated that hyperaccumula-15
tors can form symbiosis with arbuscular mycorrhizal fungi (AMF) and these enhance
plant growth and lead to higher contents of metal extracted (Al Agely et al., 2005; Or-
lowska et al., 2011). Positive eects of biochar have been usually found in arbuscular
mycorrhizal fungi, although exceptions can be found in nutrient rich soils (Lehmann
et al., 2011).20
Biochar and phytoremediation techniques have been used recently to target at Cd
polluted soils (Houben et al., 2013b) using Brassica napus L. as Cd and Zn phytoex-
tractor in combination with Miscanthus biochar and for the case of multicontaminated
soils using dierent biochars and plant species (Fellet et al., 2014). The authors of this
last study used three biochars, produced from pruning residues from orchards, fir tree25
pellets and fir tree pellets mixed with manure at two dierent doses. Fellet et al. (2014)
observed higher concentrations of Pb in plants grown with the fir tree pellets biochar.
However, no increase in yield was obtained with this treatment, and the value of the
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translocation index, although significantly higher than in the control, was insucient for
the purposes of phytoextraction.
It seems plausible that one of the best approaches to combine biochar and phy-
toextractors would be in multi-contaminated soils, where both can target at dierent
elements. Biochar could also be used as a soil conditioner prior to plant colonization in5
acidic, polluted mine tailings.
7 Conclusions and research needs
Biochar and phytoremediation have the potential to be combined in the remediation
on heavy metal polluted soils (see Fig. 1). Biochar can reduce the bioavailability and
leachability of heavy metals in the soil. On the other hand phytoextractors can reduce10
the amount of soil heavy metals in polluted areas.
We anticipate that in the next years there will be a growing interest to study the
interaction between phytoremediators and biochars and we identify the next areas as
the ones warranting research:
Biochars have highly heterogeneous properties, which should be understood to max-15
imise the ecacy of soil remediation. We should comprehend, firstly, how these prop-
erties are relevant for heavy metal adsorption and how they contribute to the dierent
mechanism of heavy metal immobilisation and secondly how to optimise the choice of
pyrolysis conditions and feedstocks in order to produce the desired products.
Most experiments utilising biochar or phytoremediators alone and not in combination20
have been carried under laboratory conditions. In the case of phytoremediators this
can result in an overestimation of heavy metal extraction.
For biochar most of the experiments done (both in field and under laboratory condi-
tions) have been done in the short term, which poses an interrogation on the long term
fate of these heavy metals. In fact it could be expected that, due to aging processes,25
the ability of biochar to sequester heavy metals decreases with time. More research
will be needed to understand aging process in biochar.
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Thus, well designed large scale field trials will be essential to evaluate the feasibility
on the approach proposed in this article. The economics of these new remediation
processes should be assessed against other options.
Acknowledgements. J. Paz-Ferreiro thanks the Chinese Academy of Sciences for financial sup-
port (fellowship for young international scientists number 2012Y1SA0002).5
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Phytoremediation
and biochar in metal
polluted soils
J. Paz-Ferreiro et al.
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Table 1. Summary of the dierent techniques of phytoremediation.
Technique Description
Phytoextraction Plants accumulate contaminants in harvestable biomass i.e., shoots
Phytofiltration Sequestration of pollutants from contaminated waters by plants
Phytostabilization Limiting the mobility and bioavailability of polluting substances by
prevention of migration or inmobilization
Phytovolatilization Conversion of pollutants to volatile form followed by their release to the
atmosphere
Phytodegradation Degradation of organic xenobiotics by plant enzymes within plant
tissues
Rhizodegradation Degradation of organic xenobiotics in the rhizosphere by rhizospheric
microorganisms
Phytodesalination Removal of excess salts from saline soils by halophytes
2177
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5, 2155–2179, 2013
Phytoremediation
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polluted soils
J. Paz-Ferreiro et al.
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Table 2. Eect of biochar application on soil heavy metals. Blank indicates not specified in the
article.
Feedstock (temperature) Soil type Pollutants Reference
Mix of hardwoods (400 C) 3 soils As Hartley et al. (2009)
Rice husk, rice straw and rice bran
(400 C)
Anthrosol As, Cd, Pb, Zn Zheng et al. (2012)
Wastewater sludge (550C) Chromosol (Australian
system)
As, Cd, Cr, Cu, Pb, Ni,
Se, Zn, Sb, B, Ag, Ba,
Be, Co, Sn, Sr
Hossain et al. (2010)
Cu, Pb, Zn Sizmur et al. (2011)
Broiler litter (350 and 700 C), pecan
shells (450 C)
Abruptic Durixeralfs Cu, Cd, Ni Uchimiya et al. (2010)
Pecan shell (450C), broiler litter sam-
ples (700 C)
Typic Kandiudult and
Abruptic Durixeralfs
Cu Uchimiya et al. (2011a)
Chicken manure (550 C), green waste
(550 C)
Cd, Cu, Pb Park et al. (2011)
Forest green waste (600–800C) Peat Cu Buss et al. (2012)
dairy manure (350 and 700 C),
paved feedlot manure (350 and
700 C),
poultry litter (350 and 700 C), turkey
litter (350 and 700 C),
separated swine solids (350 and
700 C)
Typic Kandiudult Pb, Cu, Ni, Cd Uchimiya et al. (2012a)
Mix of hardwoods (400 C) As, Cd, Zn Beesley and Marmiroli (2011)
Mix of hardwoods (400 C) Anthrosol Pb, Cu Karami et al. (2011)
Orchard prune residue (500 C) Anthrosol Cd, Cr, Cu, Ni, Pb, Tl,
Zn
Fellet et al. (2011)
Eucalyptus As, Cd, Cu, Pb, Zn Namgay et al. (2010)
Wheat Straw (350–550 C) Anthrosol Cd Cui et al. (2011)
Rice Straw Ultisol Cu, Cd, Pb Jiang et al. (2012)
Orchard prune residues (500 C) Anthrosol As Beesley et al. (2013)
Miscanthus (600 C) Cd, Zn, PB Houben et al. (2013a)
2178
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Phytoremediation
and biochar in metal
polluted soils
J. Paz-Ferreiro et al.
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Abstract Introduction
Conclusions References
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J I
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32
689
Figure 1 690
691
692
Biochar +
phytoremediation
Increase in
CEC
Nutrient
management
(nutrients
present in the
biochar
and
improvement
of
nutrient
retention)
Raising soil
pH
Improved soil
physical
properties
Promotion of
mycorrhizal
fungi
Changes in
soil
biological
properties
Fig. 1. An overview of the potential positive eects attained by combining phytoremediation and
biochar in heavy metal pollution remediation.
2179
... Plant species frequently struggle to perform well and require assistance to improve phytoremediation. Some of these tools are soil amendments like biochar (Paz-Ferreiro et al. 2014), ethylene diamine tetra acetic acid (EDTA) (Shahid et al. 2014), endophytic bacteria (Afzal et al. 2014), arbuscular mycorrhiza (Gaur and Adholeya 2004), or even transgenic plants. The contaminant, the plant type and the soil all affect how effective remediation is. ...
... Meanwhile, some moderate detoxification activities, such as soil remediation such as chemical immobilization, foliar sprayings of benefit elements to crops, and phytoremediation, should also be taken to reduce the toxic elements accumulation in the crops . Chemical immobilization can effectively reduce the transportation of toxic elements between soil and crop, while phytoremediation can accumulate toxic elements into the hyper-accumulators and move out toxic elements from soils Paz-Ferreiro et al. 2014;Su 2014). ...
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Non-ferrous metal mining and smelting has emitted large amounts of associated toxic elements into the environment and poses potential health risks to human health. In this study, local residents' and miner's hair and urine samples were collected as bioindicators to assess the health risks and soil, vegetable, rice, and surface water samples were also collected to calculate the probably daily intake of the lead (Pb), zinc (Zn), copper (Cu), and arsenic (As). The results showed that all the collected paddy and vegetable soils were contaminated according to the assessment of impact index of comprehensive quality. About 32% of the rice samples exceeded the As concentration limit of the national food safety standards, but the other toxic element concentrations in rice and all the toxic elements in the vegetables were lower than the threshold limits. Multi-pathway intake of toxic elements and target hazard quotient showed rice was the most dominate pathway of the toxic element exposure, accounting for 68-82% of the total exposures. The excessive daily exposure to the toxic elements posed a high non-carcinogenic risk for residents. Hair Cu and As concentrations exceeded the Chinese resident normal hair concentrations by factors of 1.7-6.0, especially for the miners. The implication of this study is that proper mitigation strategy on toxic element pollution and human toxic element exposure is to reduce the intake of local agricultural products, especially rice and soil remediation are encouraged to improve the health of local residents.
... The adoption of effective agricultural management practices with long-term impacts is essential to maintaining and improving the sustainability of agroecosystems [1]. Many soil properties (such as ion exchange, soil organic matter, and water holding capacity, among others) can be contrived to increase the sustainability of agroecosystems, soil quality, and soil fertility and enhance water use efficiency (WUE) [2]. Biochar is one of the amendments that can improve many of these soil properties [3] and enhance agricultural productivity and sustainability [4]. ...
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... From the emerging pollutants the presence of antibiotic-resistant bacteria, antibiotic residues, and antibiotic-resistant genes in agricultural organic amendments is of great concern at the moment, due to the harmonious risks to human health [10]. Soil amendments should have characteristic such as environmental protection and should not have a negative impact on soil structure, soil fertility, or the ecosystem as a whole [11]. PGPR and biochar due to their different properties has attracted growing interest in the last few years to be the promising soil amendments in reducing risk associated with other soil amendments application under normal and stressed conditions [4,[12][13][14][15][16]. ...
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An understanding of the mineral nutrition of plants is of fundamental importance in both basic and applied plant sciences. The Second Edition of this book retains the aim of the first in presenting the principles of mineral nutrition in the light of current advances. This volume retains the structure of the first edition, being divided into two parts: Nutritional Physiology and Soil-Plant Relationships. In Part I, more emphasis has been placed on root-shoot interactions, stress physiology, water relations, and functions of micronutrients. In view of the worldwide increasing interest in plant-soil interactions, Part II has been considerably altered and extended, particularly on the effects of external and interal factors on root growth and chapter 15 on the root-soil interface. The second edition will be invaluable to both advanced students and researchers.
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Metal pollution is an important concern because of its potential to affect human health. Metals such as lead and cadmium can enter soil via the food chain and exceed normal limits, producing harmful effects. In this study, six common garden and residential plant species were grown in soils from Spelter, WV, USA, contaminated with a variety of metals including lead (Pb), zinc (Zn), cadmium (Cd), and copper (Cu). Plant species included radish, carrot, chicory, spinach, lettuce, and clover. Metal concentrations in plant tissues were compared with metal concentration in soil by a multi-step chemical extraction. The largest accumulation of Pb (126 mg kg−1) and Zn (1493 mg kg−1) was seen in radish roots, with Cd (40 mg kg−1) having the largest accumulation in carrot roots. Comparisons of plant availability with soil chemical extractions indicated that the combined soluble and exchangeable fractions could estimate available Zn and Cd for all six plant species. For Pb and Cu, however, the comparisons indicate that these two elements were not readily available in Spelter soils. A health risk assessment was carried out for residents at Spelter on the basis of edible tissue concentrations and publicly available consumption data. Uptake of Cd by carrot roots was about five times more than the regulatory limits for men, eight times more for women, and 12 times more for children. On the basis of the results, carrot and lettuce grown in these soils have the potential to cause toxicological problems in men, women, and young children resulting from Cd and Zn accumulation. Copyright © 2013 John Wiley & Sons, Ltd.