Water Air Soil Pollut (2015) 226: 279

DOI 10.1007/s11270-015-2550-z

A Review on Phytoremediation of Crude Oil Spills

Sara Yavari & Amirhossein Malakahmad &
Nasiman B. Sapari

Received: 5 September 2014 / Accepted: 22 July 2015 / Published online: 1 August 2015
# Springer International Publishing Switzerland 2015

Abstract Changes in crude oil production and distribu- their environmental effects. Furthermore, the paper fo-
tion have increased the incidence of oil spills throughout cuses on crude oil phytoremediation and its applications
the world. Oil spills often cause destructive effects on in polluted ecosystems.
aquatic and land ecosystems. The oil spill cleanup and
recovery techniques are challenging and usually involve Keywords Petroleum hydrocarbon . Pollution fate .
complex mechanical, chemical, and biological methods. Environmental effects . Bioremediation . Plant species
Usually, mechanical removal of free oil is utilized as an
effective strategy for cleanup in aquatic and terrestrial
environments; however, they are expensive and need
1 Introduction
specialist personnel and equipment. The other common-
ly used method is the application of chemical materials
The petroleum industry includes three major segments;
such as dispersants, cleaners, demulsifiers,
(1) the exploration and production or upstream opera-
biosurfactants, and soil oxidizers. Nevertheless, these
tion that mainly include the work in the oil field or
reagents can have potential harmful environmental im-
dealing with oil wells, (2) the refining and marketing
pacts, which may limit their application. As an alterna-
or downstream operation that processes crude oil and
tive, bioremediation can offer reduced environment risk;
gas into marketable products, and (3) the supply infra-
however, the limitations of microbial activity in the soil
structure or midstream operation which includes the
can make this option unsuitable. One area of bioreme-
structures used to transport crude oil and petroleum
diation is phytoremediation, which offers potential for
products (Walls 2010). During all these operations, the
restoring large areas of contaminated ground. Plants are
oil materials can contaminate the surrounding environ-
able to remove pollutants through processes such as
ment through accidental or deliberate seepages and reg-
biodegradation, phytovolatilization, accumulation, and
ulated discharging of wastes to aquatic, coastal, land, or
metabolic transformation. This review presents the fate
air ecosystems (Ebuehi et al. 2005).
of crude oil spills in aquatic and land ecosystems and
Accidental large-scale oil spills present a significant
volume of contaminants around the world. The Exxon
S. Yavari : A. Malakahmad (*)
Valdez spill in Alaska in 1989 and the BP Deepwater
Department of Civil and Environmental Engineering, Universiti Horizon spill in the Gulf of Mexico in 2010 are the two
Teknologi PETRONAS, 32610 Bandar Seri Iskandar, Malaysia worst environmental disasters in US history with a total
e-mail: amirhossein@petronas.com.my release of 0.75 and 4.9 million barrels of crude oil,
respectively, which are still affecting some of the most
N. B. Sapari
Department of Petroleum Engineering, Universiti Teknologi productive and vulnerable marine ecosystems (Atlas
PETRONAS, 32610 Bandar Seri Iskandar, Malaysia and Hazen 2011; Spier et al. 2013). In addition to such
279 Page 2 of 18
catastrophic accidents, small spills from low-level con-
tinuous seeps, offshore exploration, tank washings, and
other related activities can also cause a variety of envi-
ronmental problems because of the presence of toxic
compounds (Dowty et al. 2001; Wiese and Ryan 2003;
Lucas and MacGregor 2006; Yang et al. 2009).
The oil spills may contain crude oils or refined pe-
troleum products such as fuel oils and lube oils. The
toxic compounds in crude oils consist of a wide range of
hydrocarbons, nitrogen-oxygen compounds, sulfur
compounds, and heavy metals, which may cause acute
and chronic effects on flora and fauna (Murakami et al.
2008). Thus, remediation of these pollutions is vital.
Additionally, the combination of complex and toxic
hydrocarbons in crude oil makes its cleanup and recov-
ery processes extremely difficult. Typically, the treat-
ment methods for disposing contaminated sites include
thermal, physical, chemical, and biological processes
(Peng et al. 2009; Walls 2010; Ndimele 2010).
Generally, dependent on the type and quantity of pollu-
tion and weather conditions, one or a combination of
these techniques is used (Dave and Ghaly 2011). Each
technique has its own advantages and disadvantages.
The mechanical and chemical methods are often con-
sidered as primary methods for quick cleanup and pre-
vention of the oil spreading (Dave and Ghaly 2011).
However, their applications require costly equipment
and reagents and involve complex processes. They
may also subsequently cause mechanical damage or
toxic effects on the ecosystem (Walls 2010). In compar-
ison with some physical and chemical approaches, bio-
logical treatment is considered as a more effective and
economical method with less impact to the environment
(Yang et al. 2009). In biological treatment, microorgan-
isms or plants are used to remove pollutants. This offers
the advantages of less labor requirement and potential
complete mineralization of oil to CO2 and H2O (Kuiper
et al. 2004; McGuinness and Dowling 2009). However,
biological treatment can take a long time and is often
only applicable when time is not a limiting factor
(Kuiper et al. 2004). Also, the application of this method
can be limited by abiotic environmental factors such as
oil concentrations, nutrients, pH, temperature, and in-
sufficient oxygen (Chatterjee et al. 2008). The advan-
tages and disadvantages of thermal, physical, chemical,
and biological treatments of crude oil spills are summa-
rized in Table 1.
Phytoremediation, as an area of bioremediation, is
defined as the use of plants ability to extract, degrade,
Water Air Soil Pollut (2015) 226: 279
stabilize, and volatilize a large array of both organic and
inorganic contaminants located in soil and liquid sub-
strates, and air (Salt et al. 1998; Sandhu et al. 2007;
Gerhardt et al. 2009; Kabra et al. 2012; Ali et al. 2012).
Plants, either alone or in conjunction with microorgan-
isms, have been reported to be used successfully for the
bioremediation of contaminants. Some promising
achievements in pollutant removal by phytoremediation
techniques have been reported previously (Table 2).
However, there is scattered knowledge on the
phytoremediation of petroleum hydrocarbon pollutions.
This review presents gathered information on the fate
and environmental impacts of crude oil spills in land and
aquatic ecosystems. Further, phytoremediation and its
involved treatment mechanisms have been elaborated.
2 The Fate of Crude Oil Spills
Crude oil hydrocarbons are naturally occurring sub-
stances originated from aquatic algae laid down during
millions of years (Atlas and Hazen 2011). They are
mostly composed of compounds with different solubil-
ity, volatility, and susceptibility for biodegradation.
Spilled oil contains aliphatics (such as alkanes and al-
kenes) and aromatics that are prone to degradation and
an asphaltic fraction with double covalent bonds and
aromatics with more condensed rings, which are more
resistant to biodegradation (Dowty et al. 2001). To
successfully remediate an oil spill, characterizing the
oil hydrocarbons and prediction of fate and the short-
term and long-term behaviors of spilled oils are neces-
sary. Besides periodical large spills that result in consid-
erable impacts on shorelines and wetlands, multiple
smaller spills do occur each year on wetlands and rivers
leaving acute and chronic toxicological effects on flora
and fauna (Murakami et al. 2008; Mendelssohn et al.
2012).
When an oil spill enters the aquatic environment, it is
exposed to a series of compositional changes that affect
its physical and toxic properties (Mendelssohn et al.
2012). Most of toxic and volatile components are re-
moved by evaporation while a low percentage of them
will be oxidized by UV radiation in sunlight (Venosa
and Zhu 2003; Farmer et al. 2006). Some of toxic
compounds with low molecular weight dissolve into
the water and quickly become degraded (Venosa and
Zhu 2003). Some of them link to fine particles in the
water and settle to the bottom (Lee and Page 1997).
279 Page 2 of 18
catastrophic accidents, small spills from low-level con-
tinuous seeps, offshore exploration, tank washings, and
other related activities can also cause a variety of envi-
ronmental problems because of the presence of toxic
compounds (Dowty et al. 2001; Wiese and Ryan 2003;
Lucas and MacGregor 2006; Yang et al. 2009).
The oil spills may contain crude oils or refined pe-
troleum products such as fuel oils and lube oils. The
toxic compounds in crude oils consist of a wide range of
hydrocarbons, nitrogen-oxygen compounds, sulfur
compounds, and heavy metals, which may cause acute
and chronic effects on flora and fauna (Murakami et al.
2008). Thus, remediation of these pollutions is vital.
Additionally, the combination of complex and toxic
hydrocarbons in crude oil makes its cleanup and recov-
ery processes extremely difficult. Typically, the treat-
ment methods for disposing contaminated sites include
thermal, physical, chemical, and biological processes
(Peng et al. 2009; Walls 2010; Ndimele 2010).
Generally, dependent on the type and quantity of pollu-
tion and weather conditions, one or a combination of
these techniques is used (Dave and Ghaly 2011). Each
technique has its own advantages and disadvantages.
The mechanical and chemical methods are often con-
sidered as primary methods for quick cleanup and pre-
vention of the oil spreading (Dave and Ghaly 2011).
However, their applications require costly equipment
and reagents and involve complex processes. They
may also subsequently cause mechanical damage or
toxic effects on the ecosystem (Walls 2010). In compar-
ison with some physical and chemical approaches, bio-
logical treatment is considered as a more effective and
economical method with less impact to the environment
(Yang et al. 2009). In biological treatment, microorgan-
isms or plants are used to remove pollutants. This offers
the advantages of less labor requirement and potential
complete mineralization of oil to CO2 and H2O (Kuiper
et al. 2004; McGuinness and Dowling 2009). However,
biological treatment can take a long time and is often
only applicable when time is not a limiting factor
(Kuiper et al. 2004). Also, the application of this method
can be limited by abiotic environmental factors such as
oil concentrations, nutrients, pH, temperature, and in-
sufficient oxygen (Chatterjee et al. 2008). The advan-
tages and disadvantages of thermal, physical, chemical,
and biological treatments of crude oil spills are summa-
rized in Table 1.
Phytoremediation, as an area of bioremediation, is
defined as the use of plants ability to extract, degrade,
Water Air Soil Pollut (2015) 226: 279
stabilize, and volatilize a large array of both organic and
inorganic contaminants located in soil and liquid sub-
strates, and air (Salt et al. 1998; Sandhu et al. 2007;
Gerhardt et al. 2009; Kabra et al. 2012; Ali et al. 2012).
Plants, either alone or in conjunction with microorgan-
isms, have been reported to be used successfully for the
bioremediation of contaminants. Some promising
achievements in pollutant removal by phytoremediation
techniques have been reported previously (Table 2).
However, there is scattered knowledge on the
phytoremediation of petroleum hydrocarbon pollutions.
This review presents gathered information on the fate
and environmental impacts of crude oil spills in land and
aquatic ecosystems. Further, phytoremediation and its
involved treatment mechanisms have been elaborated.
2 The Fate of Crude Oil Spills
Crude oil hydrocarbons are naturally occurring sub-
stances originated from aquatic algae laid down during
millions of years (Atlas and Hazen 2011). They are
mostly composed of compounds with different solubil-
ity, volatility, and susceptibility for biodegradation.
Spilled oil contains aliphatics (such as alkanes and al-
kenes) and aromatics that are prone to degradation and
an asphaltic fraction with double covalent bonds and
aromatics with more condensed rings, which are more
resistant to biodegradation (Dowty et al. 2001). To
successfully remediate an oil spill, characterizing the
oil hydrocarbons and prediction of fate and the short-
term and long-term behaviors of spilled oils are neces-
sary. Besides periodical large spills that result in consid-
erable impacts on shorelines and wetlands, multiple
smaller spills do occur each year on wetlands and rivers
leaving acute and chronic toxicological effects on flora
and fauna (Murakami et al. 2008; Mendelssohn et al.
2012).
When an oil spill enters the aquatic environment, it is
exposed to a series of compositional changes that affect
its physical and toxic properties (Mendelssohn et al.
2012). Most of toxic and volatile components are re-
moved by evaporation while a low percentage of them
will be oxidized by UV radiation in sunlight (Venosa
and Zhu 2003; Farmer et al. 2006). Some of toxic
compounds with low molecular weight dissolve into
the water and quickly become degraded (Venosa and
Zhu 2003). Some of them link to fine particles in the
water and settle to the bottom (Lee and Page 1997).
Table 1 Comparison of advantages and disadvantages of thermal, physical, chemical, and biological treatments of oil spills

Treatment type Methods Materials Efficiency Advantages Disadvantages References

Thermal In situ burning 95 % High efficiency, low cost It can be used only in remote (Zengel et al. 2003;
area or ice-covered waters Mullin and Champ 2003;
because of the concerns of Buist et al. 2011)
control of the fire and harmful
Water Air Soil Pollut (2015) 226: 279

smokes
Physical Booming Mechanical tools 90 % Eco-friendly Expensive, time consuming, only (Erdogan and Karaca 2011,
Skimming effective in calm water Al-Majed et al. 2012)
Wiping
Water flushing
Tilling
Sorbents Inorganic mineral material Up to 80 g of oil per High sorption capacity Low efficiency, expensive, (Al-Majed et al. 2012)
(clay, perlite, vermiculite, gram of sorbent poor buoyancy properties
fly ash, volcanic)
Synthetic organic products Up to 100 g of oil per Significantly high sorption Low decomposition after usage, (Ceylan et al. 2009)
(polypropylene, rubbers) gram of sorbent capacity expensive
Organic vegetable products 45 % Relatively cheap, renewable, Low efficiency, low hydrophobicity, (Choi and Cloud 1992;
(rice hull, peat, bagasse, luffa) abundant in nature inadequate buoyancy characteristic Bayat et al. 2005;
Cojocaru et al. 2011;
Abdelwahab 2014)
Nanoparticles High adsorption affinity, Environmental concerns (Franco et al. 2014)
Iron oxide low-cost, possibility of
Nanoparticles in situ treatment
Alumina nanoparticles
Chemical Surfactants Biosurfactant (lecithin aescin, 42 % Easy production, reusable, Low efficiency (Urum and Pekdemir 2004)
fatty acyl glutamate) high specificity, and less
toxicity
Chemical surfactant 80 % High efficiency High toxicity and damage to
(sodium dodecyl sulfate) environment
Biological Bioremediation 80 % Eco-friendly, cost-effective, Ineffective in large coherent (Boopathy 2000;
suitable for in situ and ex spills, the possibility of Fernndez-lvarez et al. 2006;
situ treatments, permanent producing toxic metabolites, Nikolopoulou et al. 2007)
elimination of wastes microorganisms must be
tailored to specific conditions,
time consuming
Page 3 of 18 279
279 Page 4 of 18 Water Air Soil Pollut (2015) 226: 279

Table 2 Promising achievements in pollutant removal by phytoremediation techniques

Plant Removed pollutants Substrates Removal rate References

Eleocharis acicularis Pb, Cu, Cd, and Zn Aquatic 1120, 575, 195, and 213 mg.kg1 (Ha et al. 2011)
dry wt, respectivelya
Callitriche lusitanica Arsenic Aquatic 2346 mg.kg1 dry wt (Favas et al. 2012)
Fontinalis antipyretica Uranium Aquatic 4979 mg.kg1 dry wt (Favas et al. 2014)
Callitriche stagnalis 1963 mg.kg1 dry wt
Helianthus annuus Cobalt Soil 57.7 mg.kg1 dry wt (Lotfy and Mostafa 2013)
Zea mays Atrazine (pesticide) Soil 97 % decrease of soil (Ibrahim et al. 2013)
1 1
Iris pseudacorus Triazophos (pesticide) Soil 42.11 g.g fresh wt.day (Li et al. 2014)
Lemna minor & Dimethomorph pyrimethanil Aquatic 48 g.g1 fresh wt (Dosnon-Olette et al. 2009)
Spirodela polyrhiza (fungicides) 33 g.g1 fresh wt
Medicago sativa Polychlorinated biphenyls Soil 43 % decrease of soil (Xu et al. 2010)
Cannageneralis Benzene, toluene, ethylbenzene Soil 80 % decrease of soil (Boonsaner et al. 2011)
and xylenes (BTEX)
Cannageneralis COD Domestic wastewater 83 % COD removal (Konnerup et al. 2009)
Tagetes patula Textile dye Reactive In vitro, MS liquid 90 % decolorization (Patil and Jadhav 2013)
Blue 160 medium of the dye
Populus deltoids Perchloroethylene Aquatic 99 % removal (Andrew James et al. 2009)
Populus nigra

a
Accumulation rate in plants

Substantial quantities of the oil is broken up into small
droplets, dispersed on water surface and remain there
until they become decomposed by bacteria. Sometimes,
the droplets form a water-in-oil emulsion (mousse),
which increases the persistence of the slick (Kingston
2002).
Apart from aquatic environment, hydrocarbons spills
may also occur on land. The type of soil (sand, loam,
and clay) and the amount of existing organic matter
determine the fate of petroleum hydrocarbons and the
extent of damage to plants (Pezeshki et al. 2000). After
crude oil spill on soil, the low molecular weight and
high solubility components such as monocyclic aromat-
ic hydrocarbons will generally volatilize to the atmo-
sphere. The C10C16 n-alkanes are normally
biodegraded by indigenous bacteria. However, the
higher molecular weight fractions such as alkanes with
carbon numbers higher than 20; polycyclic aromatic
hydrocarbons (PAHs) such as naphthalene, anthracene,
phenanthrene, pyrene; and their alkylated derivatives
are more resistant towards biodegradation. They pene-
trate into soil micropores and remain in the soil matrix
(Dutta and Harayama 2001; Liang et al. 2009). These
heavy compounds have attracted significant concern
regarding their mutagenic and carcinogenic potentials
and their ability to bioaccumulate (Kuiper et al. 2004;
McGuinness and Dowling 2009). As an ultimate fate,
these heavy compounds may undergo volatilization,
photolysis, and chemical or microbial degradation
(Haritash and Kaushik 2009).
3 The Environment Impacts of Crude Oil Spills
Crude oil spillage can cause negative impacts on both
water and soil ecosystems (Liang et al. 2009). Lakes,
rivers, and wetlands offer valuable resources and aquatic
communities that can be threatened by oil spills. The
lethal and sublethal effects of oil hydrocarbons on fish
have been reported (Ramachandran et al. 2006; Snchez
et al. 2006; Murakami et al. 2008). Abnormal neurone
development, genetic damage, physical deformities, as
well as changes in biological activities such as feeding,
reproduction, and migration are examples of undesirable
effects (Jewett et al. 2002; Murakami et al. 2008).
Seabirds are other conspicuous victims of hydrocarbon
spills (Oropesa et al. 2007). Only 10 mL of oil slick can
affect feather microstructure of birds and lead to lethally
reduced thermoregulation (OHara and Morandin
2010). The negative effects of oil contamination on
shellfish, turtles, and some coastal vertebrate species
such as sea ducks and otters have been also reported
(Esler et al. 2000; Oropesa et al. 2007; Vias et al.
2009; OHara and Morandin 2010; Camacho et al.
Water Air Soil Pollut (2015) 226: 279
2013). The other negative side of aquatic oil spills is the
effect on human health. Studies indicate that aquatic
organisms are able to bioaccumulate high levels of
hydrocarbon fractions in their tissues. As the final effect
of the bioaccumulation of contaminants along with their
subsequent transfer via the food chain, the pollutants can
threaten human nutrient sources and health (Kingston
2002; Yang et al. 2009). Accumulation of polycyclic
a r o m a t i c h y d r o c a r b o n s ( PA H s ) i n c o c k l e
(Cerastoderma glaucum), oyster (Ostrea edulis), noble
pen shell (Pinna nobilis), blue mussel (Mytilus edulis),
and turbot (Scophthalmus maximus) has been reported
in areas with petroleum pollution (Baussant et al. 2001;
Len et al. 2013; Xiu et al. 2014).
Plants in aquatic and terrestrial areas can be exposed
to chemical and physical damage by oil hydrocarbons.
Fouling of plant leaves can reduce photosynthesis and
temperature regulation, while coating of roots can dis-
rupt root architecture and water and nutrient uptake
(Khan et al. 2013; Pezeshki et al. 2000). Moreover,
inhibited seed germination, decreased plant biomass
production, and increased plant morality have been
observed after oil contamination (Merkl et al. 2005a;
Yang et al. 2009). In terrestrial areas, the physical,
chemical, and biological characteristics of soils are af-
fected by petroleum hydrocarbon pollution. These com-
pounds penetrate macro- and micropores in soil and,
thus, limit water and air transport that would be neces-
sary for organic matter conversion (Erdogan and Karaca
2011).
4 Crude Oil Spills Removal Techniques
A complex of mechanical, chemical, and biological
approaches can be applied for the remediation of petro-
leum hydrocarbon contamination. The commonly used
mechanical techniques include collection and skim-
ming, wiping, water flushing, tilling, as well as cutting
vegetation and burning (Ghannam and Chaalal 2003;
Ndimele 2010). Mechanical removal of oil spills are
usually utilized as an initial strategy for cleaning up in
aquatic and terrestrial environments. However, they can
be expensive and need specialized equipment ( Al-
Majed et al. 2012). Therefore, other methodologies
can be considered.
In situ burning of oil is an alternative treatment,
which can be used for quick removal of thick film of
oil spilled on a water body or land. However, its
Page 5 of 18 279
application is limited according to the condition of the
environment. For example, some plant communities like
needle grasses are sensitive and may be damaged or
eliminated by fire (Zengel et al. 2003). In addition, in
situ burning could threaten human health and environ-
mental resources due to the smoke and the probability of
flashback and secondary fires (Evans et al. 2001; Mullin
and Champ 2003; Fingas 2012). Thermal desorption is
an ex situ burning technique that is growing in popular-
ity and use. It uses heat to burn, decompose, or destroy
the contaminants in soil leaving the mineral content of
the soil after treatment (Erdogan and Karaca 2011).
Sorbents are oleophilic and hydrophobic materials
used for oil spill cleanup in offshore and onshore lines.
They can be classified into inorganic minerals (e.g.,
clay, zeolites, silica gel), synthetic organics (e.g., poly-
urethane and polypropylene), and agricultural products
(e.g., straw, mangrove barks, kenaf) ( Al-Majed et al.
2012; Asadpour et al. 2014). Both inorganic minerals
and synthetic organic products have high sorption ca-
pacity, but they have low retention capacity and low
decomposition, respectively. Agricultural-based sor-
bents are relatively cheap, abundant, and eco-friendly;
however, low sorption capacity and low hydrophobicity
are their shortcomings ( Al-Majed et al. 2012).
The other commonly used method is the application
of chemical materials such as dispersants, cleaners,
demulsifiers, biosurfactants, and soil oxidizers. But
due to disagreements on effectiveness and possible tox-
icity effects of chemical materials, there are widespread
concerns over their applications (Pezeshki et al. 2000;
Calvo et al. 2009; Ndimele 2010; Kang et al. 2010). For
instance, Corexit 9500A oil mixture and other disper-
sants have been shown to be toxic on aquatic species
(George-Ares and Clark 2000; Chase et al. 2013).
Corexit has been reported to change the intracellular
oxidative balance and impede mitochondrial functions
in mammalian cells and affect human health (Zheng
et al. 2014).
Biological treatment is another cleanup technique
that developed in the 1980s, which uses the natural
ability of microorganisms and/or plants for removing
pollutants (Balba et al. 1998; Daz 2010; Khan et al.
2013). Onsite operation of this technology can be less
expensive and causes minimum site disruption, and
therefore, it has the greater public acceptance
(Boopathy 2000; Jagadevan and Mukherji 2004; khan
et al. 2013). However, biological treatment is most
effective at sites with low to medium level of
279 Page 6 of 18
contamination (Schnoor 1997). Also, the method may
require more time to reach optimal operational condi-
tions to achieve the remedial goals (Van Epps 2006).
5 Mechanisms Involved in Biological Treatments
5.1 Bioremediation Technique Using Microorganisms
Some microbial organisms are able to break down pe-
troleum hydrocarbons into simpler products through
enzymatic processes to obtain carbon and energy for
growth (Joutey et al. 2013). These processes are termed
as biodegradation. Biodegradation is an intercellular
activity which can occur aerobically or anaerobically
(Jagadevan and Mukherji 2004). Anaerobic degradation
is much slower than aerobic degradation and uses Fe,
Mn, sulfate, and CO2 instead of oxygen as electron
acceptors. In these reactions, hydrocarbons act as an
electron donor (Sierra-Garcia and de Oliveira 2013).
Due to the complexity of petroleum hydrocarbons, a
single microorganism type with distinctive enzymes is
not able to do a complete degradation. Recognition of
indigenous microbial populations in petroleum-
contaminated soil or water has been investigated
(Golyshin et al. 2003; Syed et al. 2010; Roy et al.
2013). Usually, a cooperation of diverse microorgan-
isms is required to degrade almost all of the components
(Ghazali et al. 2004). There are a host of species of
bacteria, archaea, and fungi involved in the biodegrada-
tion process (Joutey et al. 2013).
Attempts to accelerate the rate or extent of microbial
activities can result in the increase of hydrocarbon re-
moval from a contaminated area (Leahy and Colwell
1990; Kingston 2002; Ebuehi et al. 2005; Murakami
et al. 2008). There are a variety of physicochemical
pretreatments that can be used in these cases (Haritash
and Kaushik 2009). The application of chemical sol-
vents such as acetone and the use of ozone and UV
radiation, oxidation, and also thermal treatments have
been reported to be effective in increasing the rate of
diffusion of contaminants in media and consequent bio-
availability (Luers and Ten Hulscher 1996; Lee et al.
2001; Haritash and Kaushik 2009; Ishak and
Malakahmad 2013). However, their application is lim-
ited because of the formation of harmful chemical resi-
dues, high expenses, and energy consumption (Makkar
and Rockne 2003). Moreover, the acceleration rate of
degradation may be done by addition of indigenous or
Water Air Soil Pollut (2015) 226: 279
well-adapted microorganisms to existing native mi-
crobes in the contaminated soil, which is termed as
Bbioaugmentation^ (Pezeshki et al. 2000; Escalante-
Espinosa et al. 2005; Roldn-Martn et al. 2007; Liang
et al. 2009; Khan et al. 2013). In this approach, the
activity and efficiency of the introduced microorgan-
isms to actual field condition may be inhibited by biotic
and abiotic factors, and migration and competition with
autochthonous microorganisms (Suja et al. 2014).
Another strategy that is referred as Bbiostimulation^
involves the supplement of nutrients and oxygen to a
contaminated area for stimulation of metabolic activity
of microorganisms (Leahy and Colwell 1990; Dowty
et al. 2001; Molina-Barahona et al. 2004; Lin et al.
2009; Roy et al. 2014). Adequate concentration of nu-
trients (e.g., nitrogen, phosphorus, sulfur, iron) is needed
for incorporation into cellular biomass (Atlas 1995; Ron
and Rosenberg 2014). However, high application rates
of nutrients especially in the form of inorganic fertilizer
can lead to ammonia toxicity and/or eutrophication and
algal growth (Lung et al. 1993; Sarkar et al. 2005).
Similarly, the supply of oxygen can be increased in
polluted soil using techniques such as bioventing, land
farming, and composting to maintain aerobic conditions
(Boopathy 2000; Malakahmad and Jaafar 2013).
5.2 Bioremediation Technique Using Plants
Plants have different mechanisms for the removal and/or
degradation of organic hydrocarbons from impacted
soils. Although only a few degradation processes occur
directly in plant tissues, most degradation are the result
of the complex association of roots, root exudates, rhi-
zosphere, and microbes, which is termed as
rhizoremediation (Cai et al. 2010; Ndimele et al. 2011;
Khan et al. 2013). The specific physiology and bio-
chemistry of plant roots along with the activity of rhi-
zosphere microorganisms make plant metabolic systems
able to remediate toxic xenobiotics (Meagher 2000).
The ability of plants for remediation is clearer knowing
that there are more than 100 million miles of roots per
acre that offers a great potential for restoring large areas
of surface and depth contamination (Merkl et al. 2004;
Andersen et al. 2008; Gerhardt et al. 2009). The root
system of higher plants is associated not only with soil
environment but also with a vast community of meta-
bolically active microorganisms. The living plants cre-
ate unique habitats on and around the roots where the
microbial population is considerably higher than that of
Water Air Soil Pollut (2015) 226: 279
root free soil environment (Lu et al. 2010). Around 40 %
of a plants photosynthate can be exuded by plant roots
into the soil as sugars, organic acids, and aromatic
compounds, which are rich in carbon and energy for
microorganisms growth (Khan et al. 2013). These ex-
udates can initiate the chemotactic response of microbes
for motility towards the roots and formation of root
colonization, which consequently stimulate growth and
activity of microorganisms for the degradation of organ-
ic pollutants (Leigh et al. 2002; Gerhardt et al. 2009).
Studies showed that each species have distinct chemical
compositions and rates of exudation which have differ-
ent effects on microorganisms (Grayston et al. 1998;
Yang and Crowley 2000; Bais et al. 2006). Therefore,
the degradation activity is influenced by the individual
composition of plant exudates (Gleba et al. 1999). Plant
roots are also able to provide oxygen for microorgan-
isms in the rhizosphere and increase the oxidative deg-
radation of hydrocarbons through the penetration into
the soil and improvement of the soil structure. The
endproducts of degradation include alcohol, acids, car-
bon dioxide, and water, which are less toxic and less
persistent than the primary compounds (Gerhardt et al.
2009).
In addition to the stimulated microbial activity, the
plant also releases enzymes from roots such as
dehalogenase, nitroreductase, peroxidase, and laccase
that play a significant role in reduction of organic con-
taminants (Alkorta and Garbisu 2001). They contribute
in transforming petroleum hydrocarbons by catalyzing
the chemical reactions as well as the reduction of bio-
availability of the contaminants through binding them in
the rhizosphere or into soil organic matter, which is
termed as phytostabilization (Merkl et al. 2005a).
There are relatively little information on the direct
uptake of hydrocarbons by roots (phytoextraction) and
their consequent sequestration inside the plants tissue.
Only a small number of hydrocarbons can be absorbed
by plants from the soil as most of them have log Kow >4,
i.e., equilibrium constant that provides an indication of
constituent sorption onto soil (Alkorta and Garbisu
2001). After root uptake, hydrocarbons may experience
different fates. Some of them with the low molecular
weight can be released into the atmosphere through
transpiration processes (phytovolatilization). However,
the non-volatile compounds can be either sequestered in
root tissues via enzymatic modification or stored in the
vacuole or on the cell walls (phytoaccumulation)
(Gerhardt et al. 2009; Haritash and Kaushik 2009).
Page 7 of 18 279
6 Phytoremediation of Crude Oil in Polluted Soils
Various species of plants have been identified due to
their potential for phytoremediation of crude oil hydro-
carbons of polluted soils (Table 3). These plants are
initially characterized with good tolerance to
petroleum-contaminated soil. The four oclock flower
(Mirabilis jalapa L.) was successfully demonstrated as a
phytoremediator due to having a particular tolerance to
petroleum contamination. The removal efficiency of
total petroleum hydrocarbons (TPHs) was doubled by
M. jalapa over a 127-day period (Peng et al. 2009).
Forest tree species such as teak (Tectona grandis) and
gmelina (Gmelina arborea) have shown acceptable abil-
ities to thrive well in a contaminated habitat having
crude oil up to 10 % w/w of soil. However, biomass
and height of the test plants were significantly affected
at higher levels of oil treatments (Mary Agbogidi et al.
2007). Branquilho (Sebastiania commersoniana), a
Brazilian native tree, have been also proved to be toler-
ant to soil petroleum contamination. This tree decreased
petroleum hydrocarbons up to 94 % in contaminated
soil (Ramos et al. 2009). Seed germination and early
growth of seven plant species including corn (Zea
mays), millet (Panicum miliaceum), sorghum
(Sorghum bicolor), lettuce (Lactuca sativa), okra
(Abelmoschus esculents), watermelon (Citrullus
lanatus), and soybean (Glycine max) were evaluated in
experimental systems contaminated with oilfield-
produced water. Results indicated a high tolerance of
sorghum, okra, millet, and corn to oil phytotoxicity
compared to others (Pardue et al. 2015). Two crop
species, corn (Z. mays) and soybean (G. max), have also
demonstrated tolerance to crude oil-contaminated soils
(Issoufi et al. 2006).
The plant potential for petroleum hydrocarbon bio-
accumulation is another characteristic that makes plants
suitable for phytoremediation. A high bioaccumulation
of BTEX (benzene, toluene, ethylbenzene, and xylenes)
in shoots of canna lily (Canna indica L.) was reported
by Boonsaner et al. (2011). Canna removed 80 % of
BTEX in the root zone soil in 21 days. The tropical
ornamental shrub, siam weed (Chromolaena odorata
L.), showed high capability of phytoaccumulation in
soils contaminated with crude oil and heavy metals.
These species removed up to 80 % crude oil from soil
polluted with oil and heavy metals (Atagana 2011).
The physical and morphological characteristics of
roots in some vegetation make them able to attract more
279 Page 8 of 18 Water Air Soil Pollut (2015) 226: 279

Table 3 Potential terrestrial plants reported for petroleum hydrocarbon phytoremediation

Scientific name The initial concentration The removal Duration of References

of petroleum hydrocarbons rate phytoremediation

Mirabilis Jalapa 10,000 mg.kg1 41.6163.20 % 127 days (Peng et al. 2009)
1
Impatiens balsamina 500010,000 mg.kg 18.1365.03 % 4 months (Cai et al. 2010)
Canna indica 400495 mg.kg1 80 % 21 days (Boonsaner et al. 2011)
1
Chromolaena odorata 50,000 mg.kg 80 % 180 days (Atagana 2011)
Biden pilosa 30,000 mg.kg1 9% 64 days (Kuo et al. 2013)
Tectona grandis 115 % (w/w) of soil 3 months (Mary Agbogidi et al. 2007)
Tectona grandis 15.132.8 % (w/w) of soil (Yenn et al. 2014)
Gmelina arborea
Azadirachta indica
Michelia champaca
Sebastiania commersoniana 2575 g.kg1 94 % 424 days (Ramos et al. 2009)
Zea mays 10100 g.kg1 28 days (Issoufi et al. 2006)
Glycine max
Lolium arundinaceum 9.175 mg.kg1 (White et al. 2006)
Lolium multiflorum
Cynodon dactylon
Lolium multiflorum 6000 mg.kg1 59 % 80 days (Alarcn et al. 2008)
Cyperus rotundus 2.0510.2 % (w/w) of soil 32.650.01 % 180 days (Basumatary et al. 2012a)
Cyperus brevifolius 8 % (w/w) 61.286.2 360 days (Basumatary et al. 2012b)
Brachiaria brizantha Centrosema 5 % (w/w) of soil 180 days (Merkl et al. 2004)
brasilianum Calopogonium
mucunoides
Astragalus membranaceus 7799 % 80 days (Lee et al. 2008)
Aeschynomene indica
Panicum bisulcatum
Medicago sativa 20 g.kg1 33 to 56 % 1 year (Wiltse et al. 1998)

microorganisms around their roots and stimulate hy-
drocarbon degradation (Ansari et al. 2014). The roots
of mulberry (Morus spp.), apple (Malus domestica),
and osage orange (Maclura pomifera) trees have been
reported to release flavonoids and phenolic compounds
which stimulate PAH-degrading bacteria (Fletcher and
Hegde 1995). Garden balsam (Impatiens balsamina
L.) was reported as a potential ornamental plant for
effective removal of oil from contaminated soils.
During the 4-month culture period, the population of
living microorganisms around the plant root showed a
significant increase, which played the main role in oil
degradation (Cai et al. 2010). In a laboratory
phytoremediation study, degradation, volatilization,
and mass reduction of benzene in effluents was en-
hanced by hybrid poplar cuttings (Populus deltoids
Populus nigra) planted in flow-through reactors sup-
plied with benzene (Burken et al. 2001). Grasses such
as annual ryegrass (Lolium multiflorum), bread grass
(Brachiaria brizantha), nut grass (Cyperus rotundus),
and mullumbimby couch (Cyperus brevifolius Rottb.)
are considered to be ideal for phytoremediation due to
ramified, extensive, and fibrous root systems, which
offer a maximum root surface area (Merkl et al. 2004;
White et al. 2006; Basumatary et al. 2012a;
Basumatary et al. 2012b). The perennial grasses, tall
fescue (Festuca arundinacea Schreb.), and perennial
ryegrass (Lolium perenne L.) have been also selected
for oil phytoremediation having extensive root systems
and robust growth after establishment (Cook and
Hesterberg 2013).
Unlike surface root system, plant species with a tap
root system are able to reach deeper soil layers or the
water table and impact on deeper located contaminants
(Merkl et al. 2004). Deep-rooted trees such as poplars
(Populus spp.) and willows (Salix spp.) have been suc-
cessfully used for water uptake from groundwater con-
taining total petroleum hydrocarbons (Ferro et al. 2013).
Water Air Soil Pollut (2015) 226: 279
Poplars have been also demonstrated to have greater
population of oil-degrading microorganisms compared
to bulk soil (Jordahl et al. 1997).
7 Phytoremediation of Crude Oil Spills in Aquatic
Ecosystem
In aquatic ecosystems such as lakes, rivers, and wet-
lands, there are different types of plants termed macro-
phytes thriving in or near water that are emergent,
submergent, or floating (Bhatia and Goyal 2014).
They can be possibly used as oil hydrocarbon
phytoremediators. One of the characteristics that make
them suitable for phytoremediation is their ability to
grow fast. They are invasive and rapidly become abun-
dant. Thus, they can be replaced with new growth soon
after the damage caused by oil pollution (Bhatia and
Goyal 2014). The fibrous roots of some aquatic plants
can provide larger surface and denser rhizospheres for
microbial colonization (White et al. 2006). Ndimele
(2010) reported that water hyacinths (Eichhornia
crassipes) fibrous root systems are able to significantly
remediate the floating petroleum hydrocarbons on sur-
face waters. Biscuit grasses (Paspalum vaginatum Sw.)
were also reported to be potential candidates for petro-
leum hydrocarbons phytoremediation. Their root system
facilitated survival and growth in diesel-contaminated
sands (up to 30 g.kg1) (Sanusi et al. 2012). Reeds,
dominant coastal wetland plants, can also provide strong
vitality and great root surface area which is beneficial
for restoring the petroleum-contaminated wetlands
(Wang et al. 2011). Four fresh-marsh plant species,
alligator weed (Alternanthera philoxeroides),
maidencane (Panicum hemitomon), common reed
(Phragmites australis), and duck potato (Sagittaria
lancifolia) effectively phytoremediated South
Louisiana Sweet Crude oil in contaminated mesocosms
(Dowty et al. 2001).
In aquatic ecosystems, due to hypoxic and anoxic
conditions of sediments or soils, anaerobic degradation
of crude oil happens which is a very slow and incom-
plete process. Some macrophytes transport atmospheric
oxygen from the shoots to the roots and increase the
aerobic respiration of rhizosphere microbes (Pezeshki
et al. 2000; Moreira et al. 2011). This is a natural
mechanism of wetland plants, or submerged aquatic
macrophytes, which makes them able to oxygenate their
root zone to protect themselves against phytotoxins
Page 9 of 18 279
(e.g., Fe2+, Mn2+, and H2S) (Pezeshki et al. 2000).
Huesemann et al. (2009) have shown that eelgrass
(Zostera marina), a marine macrophyte, can significant-
ly remove polynuclear aromatic hydrocarbons and
polychlorinated biphenyls in submerged marine sedi-
ments. The enhanced rhizosphere biodegradation
through root exudates, oxygen, and plant enzymes was
the dominant removal process. Red mangrove
(Rizophora mangle L.) has also been reported to in-
crease the bacteria density in the rhizosphere ten times
more than bulk sediments, possibly through the entry of
oxygen into the sediments (Moreira et al. 2011).
Similarly, the aquatic weed cattails (Typha spp.) have
been demonstrated to release higher rates of oxygen into
their rhizospheres compared to the coastal salt marsh-
black rushes (Juncus roemerianus) with the difference
in oxygen release intensity between plant species found
to be related to the redox state of the rhizosphere
(Wiebner et al. 2002). In a horizontal-vertical flow con-
structed wetland, cattail and bulrush (Scirpus lacustris)
removed 99.9 % of phenanthrene (Machate et al. 1997),
while black rush, a dominant coastal salt marsh plant,
effectively reduced total petroleum hydrocarbons (TPH)
up to 15 % in contaminated sediments (Lin and
Mendelssohn 2009).
In floating species, where the root system does not
establish into a solid matrix, the ability of plants for
bioaccumulation and biosorption of pollutants from the
liquid medium make them able to be considered as
phytoremediators (Mkandawire and Dudel 2002;
Rahman and Hasegawa 2011). There are some
phytoremediation studies on floating plants such as
water lettuce (Pistia stratiotes Linn.) and duckweed
(Spirodela polyrrhiza Trev.) for removing crude oils of
oil-polluted water bodies. However, their performance
was not promising (Agbogidi and Bamidele 2009;
Akapo et al. 2011). In general, there are few studies to
identify the ability of aquatic species for crude oil
phytoremediation. Since most oil spills occur in aquatic
environments, the need to test the efficiency of aquatic
macrophytes seems to be necessary.
8 Enhanced Phytoremediation
Phytoremediation can be enhanced by inoculation of
plant roots with hydrocarbon (HC)-degrading and/or
plant growth-promoting bacteria (PGPB). HC-
degrading bacteria improve plant tolerance to
279 Page 10 of 18
hydrocarbon pollutants (Khan et al. 2013). They are able
to produce various enzymes to degrade organic com-
pounds and reduce phytotoxicity and evapotranspiration
of volatile hydrocarbons (Tara et al. 2014). PGPBs also
demonstrate beneficial effect on plants by inducing
plant growth or controlling biological disease (Khan
et al. 2013). There are various studies evaluating the
effect of plant species and bacterial activities on
phytoremediation efficiency. Phytoremediation poten-
tial of perennial ryegrass (L. perenne L.) inoculated with
HC-degrading bacteria was investigated on diesel oil-
contaminated soil (50 g.kg1). Based on the results, the
removal efficiency of the enhanced phytoremediation
reached 57.3 %, which was 7.3 % higher than the
phytoremediation alone (Chuluun et al. 2014). Also,
the introduction of HC-degrading Pseudomonas strains
to the plant species teak (T. grandis), gmelina
(G. arborea), neem (Azadirachta indica), and champak
(Michelia champaca) increased the phytoremediation
efficiency of the plants (Yenn et al. 2014).
Arbuscular mycorrhizal fungi (AMF) are another
microorganisms that may affect the outcome of a
phytoremediation attempt. Mycorrhizal hyphae act as
roots and provide a wider exploration of bulk soil by
creating a new interface of soil-plant interactions. They
are known to benefit plants through a series of changes
in plant physiology, nutrient availability, and microbial
composition (Joner and Leyval 2003; Khan 2006).
Phytoremediation of crude oil-contaminated soils
(6000 mg.kg1) has been reported to be increased by
annual ryegrass (L. multiflorum Lam.) inoculated with
an AMF (Glomus intraradices) in greenhouse condi-
tions (Alarcn et al. 2008). The germination and growth
of oxeye daisy (Leucanthemum vulgare) colonized by
mycorrhizae was also enhanced in crude oil-
contaminated soil (Noori et al. 2014). Black jack
(Biden pilosa), a medicinal herb, showed a 9 % increase
in degradation during a 64-day period of heavy oils after
infection by mycorrhizal fungi in soils polluted with
30,000 mg.kg1 petroleum hydrocarbon (Kuo et al.
2013).
Addition of fertilizer is another strategy to enhance
oil degradation by plants. Nitrogen and phosphorus are
often limiting factors in hydrocarbon degradation pro-
cesses. Therefore, a balance of nutrient can reduce com-
petition between plants and microorganisms for nutri-
ents in oil-polluted soils and subsequently increase the
oil degradation rates (Kirkpatrick et al. 2006;
Unterbrunner et al. 2007; Basumatary et al. 2012a). In
Water Air Soil Pollut (2015) 226: 279
a greenhouse experiment, the effect of controlled release
fertilizer on the growth and biodegradation potential of
ryegrasses (L. multiflorum Lam.) was studied in petro-
leum hydrocarbon-contaminated sandy soil. The results
showed that petroleum degradation was enhanced in the
plants treated by different concentrations of the fertilizer
(Cartmill et al. 2014). In a field study, the application of
nitrogen, phosphorus, and potassium (NPK) fertilizer
also increased the degradation potential of corn (Z.
mays) and elephant grass (Pennisetum purpureum) up
to 77.5 % in petroleum hydrocarbon-contaminated ag-
ricultural soils (Ayotamuno et al. 2006). Merkl et al.
(2005b) evaluated the effect of fertilizer levels (200,
300, and 400 mg.kg1 of NPK) on phytoremediation
efficiency of crude oil contaminated soil. They showed
that the highest concentration of fertilizer caused
highest oil dissipation (10.5 %) after 14 weeks. The
highest root biomass of ryegrasses (L. multiflorum
Lam.) was also obtained in crude oil-contaminated
soil amended with inorganic fertilizers (White et al.
2003). Lin and Mendelssohn (1998) showed that the
application of fertilizers can accelerate oil degradation
in the soil by marsh sods of smooth cordgrass
(Spartina alterniflora) and saltmeadow cordgrass
(Spartina paten).
As a viable and natural way, legumes can be used to
replenish nitrogen into the phytoremediation system.
Legume nodules containing bacteria (Rhizobium spp.)
are able to convert atmospheric nitrogen to inorganic
compounds such as ammonium ions which can be read-
ily absorbed by plants (Gothwal et al. 2008). The bio-
logical N2 fixation of legumes reduces the need for N
fertilizer. This property is significant in petroleum
hydrocarbon-polluted area where the C/N ratio increases
and causes nitrogen deficiency (Ndimele et al. 2011). In
a study, the association between a leguminous tree,
saman (Samanea saman), and its symbiotic microorgan-
isms played a critical role on the remediation efficiency
of petroleum hydrocarbons in contaminated soil (Bento
et al. 2012). Japanese panicgrass (Panicum bisulcatum),
milkvetch (Astragalus membranaceus), Indian
jointvetch (Aeschynomene indica), and alfalfa
(Medicago sativa) enhanced dissipation of PAHs in soils
through releasing enzymes and increasing microbial
activity (Wiltse et al. 1998; Lee et al. 2008). Legumes,
Centrosema brasilianum L., and calapo (Calopogonium
mucunoides) have also been reported as promising
plants for phytoremediation due to their high seedling
emergence and biomass production (Merkl et al. 2004).
Water Air Soil Pollut (2015) 226: 279
Phytoremediation can be also promoted by the proper
application of soil amendments such as agricultural
wastes and composts to contaminated soils. Soil amend-
ments are able to improve the physical properties and
nutrient content of soils and consequently increase mi-
crobial activities (Olutayo 2007). In a study by
Agamuthu et al. (2010), the application of barbados
nut (Jatropha curcas) for the remediation of hydrocar-
bon petroleum was improved up to 96 % with the
addition of some soil amendment agents such as banana
skin, brewery spent grain, and spent mushroom
compost. Wang et al. (2012) reported that the applica-
tion of compost can increase the pyrene degradation in
soil up to 46 % by Ryegrass (L. perenne) and alfalfa
(M. sativa). Similarly, addition of waste cotton and saw
dust as soil amendments increased the remediation po-
tential of cowpea (Vigna ungiculata L.) in crude oil-
polluted soil (Olutayo 2007).
9 Phytoremediation Cost
Phytoremediation has been always reported as a cost-
effective plant-based remediation (Garbisu and Alkorta
2001; Merkl et al. 2004; Gerhardt et al. 2009). A number
of studies have tracked the costs and economic analyses
of phytoremediation (U.S. EPA 2000; ITRC 2009;
Compernolle et al. 2012). There are many factors affect-
ing the final cost of a phytoremediation system such as
type, size, and depth of contaminated site, contaminated
media, site climate, vegetation type, and agronomic
practices (Van Epps 2006). Petroleum hydrocarbons at
different sites represent different mixtures from highly
mobile compounds (e.g., BTEX) to highly hydrophobic
ones, such as those bound strongly to soil matrix (e.g.,
PAHs) (Kamath et al. 2004). Therefore, different mech-
anisms of phytoremediation and different plants and
designs could be utilized in the remediation processes,
which put the cost of phytoremediation in a wide range.
Generally, the total cost of phytoremediation includes
its design, installation, annual operation, maintenance,
a n d m o n i t o r i n g ( U . S . E PA 2 0 0 0 ) . O n c e
phytoremediation has been selected, detailed system
design, treatability studies, and pilot trials may be re-
quired for the investigation of contaminated area condi-
tion, the toxicity of pollutants, and the suitability of
plants to ensure that the remedy is effective (U.S. EPA
2000; Van Epps 2006). Infrastructure and site prepara-
tion are activities that are performed in the installation
Page 11 of 18 279
phase. Since phytoremediation is considered as an ever-
growing system, the designed infrastructure should be
able to support the system for long-term functioning
(ITRC 2009). The installation outlay includes the cost
of fundamental activities such as debris removal, pH
adjustment, storm water management, fencing, and
some basic utilities to run pumps, automated irrigation
systems, and monitoring equipment (U.S. EPA 2000). It
also includes some expenditure for soil preparation such
as tilling, fertilizing, and drainage. The plant stock and
planting methods can also add expense to the installa-
tion phase (U.S. EPA 2000). While the cost of stock is
only 12 % of the total installation cost, the planting
methods require extensive physical/manual labor or
heavy machinery for planting and installation of some
additional engineering items, such as subirrigation sys-
tems, breather tubes, and root growth barriers (ITRC
2009). Apart from costs incurred during installation,
phytotechnology plantation involves expenditure for
regular maintenance and monitoring such as fertilizing,
irrigating, weeding, replanting, mowing, pruning, har-
vesting, removing plant waste, and inspecting plant
growth and remediation performance through analyses
(Kamath et al. 2004; Van Epps 2006).
Phytoremediation is considered a less expensive re-
mediation system compared to other alternatives such as
soil excavation, pump and treat, soil washing, or incin-
eration. A cost of $2500 to $15,000 per hectare has been
reported for petroleum hydrocarbon phytoremediation
compared to $7500 to $20,000 per hectare for in situ
microbial remediation (U.S. EPA 2000). A total 5-year
cost of $250,000 has been also calculated for
phytoremediation by hybrid poplar trees compared to a
cost of $660,000 for a pump-and-treat system (ITRC
2009). Excavation and high-temperature incineration
for total petroleum hydrocarbon-polluted soil was re-
ported to be applied at a cost of $500,000 per acre
compared to a full-scale phytoremediation system rang-
ing from $50,000 to $100,000 per acre (U.S. EPA 2000).
Schnoor (1997) reported a cost of $1035 per ton soil
for petrochemical phytoremediation using fine-rooted
grasses compared to $50150 per ton for in situ biore-
mediation, $120300 per ton for indirect thermal, $360
440 per ton for solvent extraction, and $2001500 per
ton for incineration. Based on a compiled report from a
survey of 75 petroleum hydrocarbon phytoremediation
projects, the cost of the design phase for a
phytoremediation system was ranged from $3500 to
$25,000 per acre site, while installation activity was
279 Page 12 of 18
cost from $7250 to $177,000 per acre site and annual
operation, and maintenance costs were ranged from
$5000 to $21,000 per acre site (Van Epps 2006).
Phytoremediation can lower the remediation costs up
to 50 to 80 %. The costs can be reduced further through
other different strategies such as selection of trees in-
stead of other vegetation (U.S. EPA 2000). Trees are
prop osed as the l owest-cost plant t ype for
phytoremediation (Garbisu and Alkorta 2001) with
deeper root system, suitable to low fertility and poor
structure sites and with high transpiration rates, which
makes them able to accept larger amount of pollutants
(Thawale et al. 2006). A single willow tree has been
estimated to be able to transpire 19 m3.day1 of water,
which is equal to the transpiration rate of 0.6 acre of
alfalfa (U.S. EPA 2000). The use of trees can also
decrease the cost for regular harvesting of plants espe-
cially if the periodical removal of sequestered pollutants
in plant tissue is necessary (Garbisu and Alkorta 2001).
Another strategy causing further cost reduction is the
multifunctional use of phytoremediation systems. The
use of commercial plants as phytoremediators such as
short rotation biofuel trees for energy purpose or timber
trees for wood products can offset some of the remedial
costs and offer both environmental and economic ben-
efits (Kuzovkina and Quigley 2005; Mary Agbogidi
et al. 2007; Berndes 2013; Yenn et al. 2014).
Optimization of agricultural practices is another ap-
proach that contributes to the reduction of
phytoremediation costs. Mechanical weeding, biologi-
cal pest control, reduced tillage, use of low-cost local
plant stock, and organic amendments are some of those
practices to minimize the costs (Mohamad et al. 2014).
Finally, it should be noted that although the
phytoremediation technique could be a cost-effective
option, it requires a longer duration rather than other
alternative technologies for the establishment of vegeta-
tion and achieving cleanup standards (Kamath et al.
2004).
10 Conclusion
Oil spills can have acute and chronic impacts on sur-
rounding ecosystems. Thermal, mechanical, and chem-
ical methods applied for the remediation of these con-
taminants are expensive, disruptive to the environment,
and energy consuming. Phytoremediation, as an area of
bioremediation, has been developed to be an eco-
Water Air Soil Pollut (2015) 226: 279
friendly and cost-effective cleanup technique. It uses
the ability of plants to extract, degrade, stabilize, and
volatilize the contaminants located in land and aquatic
environments. Therefore, phytoremediation is generally
applied as an in situ and non-destructive technique,
which not only remediates organic pollutants effectively
but also improves the soil condition and prevents soil
erosion. However, its application may be limited due to
the nature of plants. High initial concentrations of con-
taminants can cause oxidative stress and toxic and in-
hibitor effects on plant roots. Hence, phytoremediation
can be applied either in low polluted areas or as a final
treatment of highly polluted areas. Besides,
phytoremediation may not be effective in low-
temperature environment when the plant growth is slow
or stopped. Application of phytoremediation may re-
quire greater land areas compared to other remediation
methods. Phytoremediation of petroleum hydrocarbon
has potential to remediate polluted areas. Nevertheless,
phytoremediator species, phytoremediation sites, effi-
ciencies, and probable risks to achieve efficient remedi-
ation technique are factors that are required for further
investigations.
Acknowledgments The authors are thankful to the Ministry of
Education, Malaysia, for providing financial support (Grant No.
0153AB-J13) for this research under MyRA grant scheme.
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