Abstract
Changes in crude oil production and distribution have increased the incidence of oil spills throughout the world. Oil spills often cause destructive effects on aquatic and land ecosystems. The oil spill cleanup and recovery techniques are challenging and usually involve complex mechanical, chemical, and biological methods. 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 specialist personnel and equipment. The other commonly used method is the application of chemical materials such as dispersants, cleaners, demulsifiers, biosurfactants, and soil oxidizers. Nevertheless, these reagents can have potential harmful environmental impacts, which may limit their application. As an alternative, bioremediation can offer reduced environment risk; however, the limitations of microbial activity in the soil can make this option unsuitable. One area of bioremediation is phytoremediation, which offers potential for restoring large areas of contaminated ground. Plants are able to remove pollutants through processes such as biodegradation, phytovolatilization, accumulation, and metabolic transformation. This review presents the fate of crude oil spills in aquatic and land ecosystems and their environmental effects. Furthermore, the paper focuses on crude oil phytoremediation and its applications in polluted ecosystems.
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1 Introduction
The petroleum industry includes three major segments; (1) the exploration and production or upstream operation that mainly include the work in the oil field or dealing with oil wells, (2) the refining and marketing or downstream operation that processes crude oil and gas into marketable products, and (3) the supply infrastructure or midstream operation which includes the structures used to transport crude oil and petroleum products (Walls 2010). During all these operations, the oil materials can contaminate the surrounding environment through accidental or deliberate seepages and regulated discharging of wastes to aquatic, coastal, land, or air ecosystems (Ebuehi et al. 2005).
Accidental large-scale oil spills present a significant volume of contaminants around the world. The Exxon Valdez spill in Alaska in 1989 and the BP Deepwater Horizon spill in the Gulf of Mexico in 2010 are the two worst environmental disasters in US history with a total release of 0.75 and 4.9 million barrels of crude oil, respectively, which are still affecting some of the most productive and vulnerable marine ecosystems (Atlas and Hazen 2011; Spier et al. 2013). In addition to such catastrophic accidents, small spills from low-level continuous seeps, offshore exploration, tank washings, and other related activities can also cause a variety of environmental 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 petroleum 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 recovery processes extremely difficult. Typically, the treatment 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 pollution 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 considered as primary methods for quick cleanup and prevention 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 comparison with some physical and chemical approaches, biological treatment is considered as a more effective and economical method with less impact to the environment (Yang et al. 2009). In biological treatment, microorganisms 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 insufficient oxygen (Chatterjee et al. 2008). The advantages and disadvantages of thermal, physical, chemical, and biological treatments of crude oil spills are summarized in Table 1.
Phytoremediation, as an area of bioremediation, is defined as the use of plants’ ability to extract, degrade, stabilize, and volatilize a large array of both organic and inorganic contaminants located in soil and liquid substrates, 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 microorganisms, 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 substances originated from aquatic algae laid down during millions of years (Atlas and Hazen 2011). They are mostly composed of compounds with different solubility, volatility, and susceptibility for biodegradation. Spilled oil contains aliphatics (such as alkanes and alkenes) 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 necessary. Besides periodical large spills that result in considerable 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 removed 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). 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 aromatic hydrocarbons will generally volatilize to the atmosphere. The C10–C16 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 penetrate 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; Sánchez 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 (O’Hara 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; Viñas et al. 2009; O’Hara and Morandin 2010; Camacho et al. 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 aromatic hydrocarbons (PAHs) in cockle (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; León 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 disrupt 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 affected by petroleum hydrocarbon pollution. These compounds penetrate macro- and micropores in soil and, thus, limit water and air transport that would be necessary 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 petroleum hydrocarbon contamination. The commonly used mechanical techniques include collection and skimming, 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 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 environmental 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 popularity 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., polyurethane 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 capacity, but they have low retention capacity and low decomposition, respectively. Agricultural-based sorbents 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 toxicity 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 dispersants 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; Díaz 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 contamination (Schnoor 1997). Also, the method may require more time to reach optimal operational conditions 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 petroleum 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 microorganisms 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 biodegradation process (Joutey et al. 2013).
Attempts to accelerate the rate or extent of microbial activities can result in the increase of hydrocarbon removal 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 solvents 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 bioavailability (Luers and Ten Hulscher 1996; Lee et al. 2001; Haritash and Kaushik 2009; Ishak and Malakahmad 2013). However, their application is limited because of the formation of harmful chemical residues, high expenses, and energy consumption (Makkar and Rockne 2003). Moreover, the acceleration rate of degradation may be done by addition of indigenous or well-adapted microorganisms to existing native microbes in the contaminated soil, which is termed as “bioaugmentation” (Pezeshki et al. 2000; Escalante-Espinosa et al. 2005; Roldán-Martín et al. 2007; Liang et al. 2009; Khan et al. 2013). In this approach, the activity and efficiency of the introduced microorganisms 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 “biostimulation” 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 nutrients (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, rhizosphere, and microbes, which is termed as rhizoremediation (Cai et al. 2010; Ndimele et al. 2011; Khan et al. 2013). The specific physiology and biochemistry of plant roots along with the activity of rhizosphere 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 metabolically active microorganisms. The living plants create unique habitats on and around the roots where the microbial population is considerably higher than that of root free soil environment (Lu et al. 2010). Around 40 % of a plant’s 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 exudates 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 organic pollutants (Leigh et al. 2002; Gerhardt et al. 2009). Studies showed that each species have distinct chemical compositions and rates of exudation which have different 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 microorganisms in the rhizosphere and increase the oxidative degradation of hydrocarbons through the penetration into the soil and improvement of the soil structure. The endproducts of degradation include alcohol, acids, carbon 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 contaminants (Alkorta and Garbisu 2001). They contribute in transforming petroleum hydrocarbons by catalyzing the chemical reactions as well as the reduction of bioavailability 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 K ow >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).
6 Phytoremediation of Crude Oil in Polluted Soils
Various species of plants have been identified due to their potential for phytoremediation of crude oil hydrocarbons of polluted soils (Table 3). These plants are initially characterized with good tolerance to petroleum-contaminated soil. The four o’clock 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 abilities 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 tolerant 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 bioaccumulation 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 microorganisms around their roots and stimulate hydrocarbon 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 enhanced by hybrid poplar cuttings (Populus deltoids × Populus nigra) planted in flow-through reactors supplied 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 successfully used for water uptake from groundwater containing total petroleum hydrocarbons (Ferro et al. 2013). 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 wetlands, there are different types of plants termed macrophytes 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 abundant. 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 surface waters. Biscuit grasses (Paspalum vaginatum Sw.) were also reported to be potential candidates for petroleum hydrocarbons phytoremediation. Their root system facilitated survival and growth in diesel-contaminated sands (up to 30 g.kg−1) (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 incomplete 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 (e.g., Fe2+, Mn2+, and H2S) (Pezeshki et al. 2000). Huesemann et al. (2009) have shown that eelgrass (Zostera marina), a marine macrophyte, can significantly remove polynuclear aromatic hydrocarbons and polychlorinated biphenyls in submerged marine sediments. 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 increase 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 constructed 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 hydrocarbon pollutants (Khan et al. 2013). They are able to produce various enzymes to degrade organic compounds 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 potential of perennial ryegrass (L. perenne L.) inoculated with HC-degrading bacteria was investigated on diesel oil-contaminated soil (50 g.kg−1). 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.kg−1) has been reported to be increased by annual ryegrass (L. multiflorum Lam.) inoculated with an AMF (Glomus intraradices) in greenhouse conditions (Alarcón 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.kg−1 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 processes. Therefore, a balance of nutrient can reduce competition between plants and microorganisms for nutrients in oil-polluted soils and subsequently increase the oil degradation rates (Kirkpatrick et al. 2006; Unterbrunner et al. 2007; Basumatary et al. 2012a). In a greenhouse experiment, the effect of controlled release fertilizer on the growth and biodegradation potential of ryegrasses (L. multiflorum Lam.) was studied in petroleum 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 agricultural soils (Ayotamuno et al. 2006). Merkl et al. (2005b) evaluated the effect of fertilizer levels (200, 300, and 400 mg.kg−1 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 readily absorbed by plants (Gothwal et al. 2008). The biological 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 microorganisms 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).
Phytoremediation can be also promoted by the proper application of soil amendments such as agricultural wastes and composts to contaminated soils. Soil amendments are able to improve the physical properties and nutrient content of soils and consequently increase microbial activities (Olutayo 2007). In a study by Agamuthu et al. (2010), the application of barbados nut (Jatropha curcas) for the remediation of hydrocarbon 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 application 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 potential 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 affecting 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 mechanisms 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, and monitoring (U.S. EPA 2000). Once phytoremediation has been selected, detailed system design, treatability studies, and pilot trials may be required for the investigation of contaminated area condition, 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 preparation are activities that are performed in the installation 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 installation phase (U.S. EPA 2000). While the cost of stock is only 1–2 % 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 systems, 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, harvesting, 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 remediation system compared to other alternatives such as soil excavation, pump and treat, soil washing, or incineration. 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 reported to be applied at a cost of $500,000 per acre compared to a full-scale phytoremediation system ranging from $50,000 to $100,000 per acre (U.S. EPA 2000). Schnoor (1997) reported a cost of $10–35 per ton soil for petrochemical phytoremediation using fine-rooted grasses compared to $50–150 per ton for in situ bioremediation, $120–300 per ton for indirect thermal, $360–440 per ton for solvent extraction, and $200–1500 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 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 instead of other vegetation (U.S. EPA 2000). Trees are proposed as the lowest-cost plant type 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.day−1 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 especially 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 benefits (Kuzovkina and Quigley 2005; Mary Agbogidi et al. 2007; Berndes 2013; Yenn et al. 2014). Optimization of agricultural practices is another approach that contributes to the reduction of phytoremediation costs. Mechanical weeding, biological 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 vegetation and achieving cleanup standards (Kamath et al. 2004).
10 Conclusion
Oil spills can have acute and chronic impacts on surrounding ecosystems. Thermal, mechanical, and chemical methods applied for the remediation of these contaminants are expensive, disruptive to the environment, and energy consuming. Phytoremediation, as an area of bioremediation, has been developed to be an eco-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 contaminants can cause oxidative stress and toxic and inhibitor 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 require greater land areas compared to other remediation methods. Phytoremediation of petroleum hydrocarbon has potential to remediate polluted areas. Nevertheless, phytoremediator species, phytoremediation sites, efficiencies, and probable risks to achieve efficient remediation technique are factors that are required for further investigations.
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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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Yavari, S., Malakahmad, A. & Sapari, N.B. A Review on Phytoremediation of Crude Oil Spills. Water Air Soil Pollut 226, 279 (2015). https://doi.org/10.1007/s11270-015-2550-z
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DOI: https://doi.org/10.1007/s11270-015-2550-z