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International Journal of Phytoremediation Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/bijp20
Arundo donax L., a Candidate for Phytomanaging Water and Soils Contaminated by Trace Elements and Producing Plant-Based Feedstock. A Review F. Nsanganwimana
a b
a
b
, L. Marchand , F. Douay & M. Mench
a
a
Click for updates
INRA, UMR BIOGECO, Route d’Arcachon, Cestas cedex, France, Université Bordeaux, UMR BIOGECO, Ecologie des Communautés , Talence , France b
Laboratoire Génie Civil et géo-Environnement (LGCgE-EA 4515), Equipe Sols et Environnement, Groupe ISA , Lille Cedex , France Accepted author version posted online: 25 Aug 2013.Published online: 06 Feb 2014.
To cite this article: F. Nsanganwimana , L. Marchand , F. Douay & M. Mench (2014) Arundo donax L., a Candidate for Phytomanaging Water and Soils Contaminated by Trace Elements and Producing Plant-Based Feedstock. A Review, International Journal of Phytoremediation, 16:10, 982-1017, DOI: 10.1080/15226514.2013.810580 To link to this article: http://dx.doi.org/10.1080/15226514.2013.810580
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/termsand-conditions
International Journal of Phytoremediation, 16:982–1017, 2014 C 2014 INRA Copyright ISSN: 1522-6514 print / 1549-7879 online DOI: 10.1080/15226514.2013.810580
ARUNDO DONAX L., A CANDIDATE FOR PHYTOMANAGING WATER AND SOILS CONTAMINATED BY TRACE ELEMENTS AND PRODUCING PLANT-BASED FEEDSTOCK. A REVIEW F. Nsanganwimana,1,2 L. Marchand,1 F. Douay,2 and M. Mench1 Downloaded by [Northeastern University] at 09:33 22 October 2014
1
INRA, UMR BIOGECO, Route d’Arcachon, Cestas cedex, France, Universit´e Bordeaux , UMR BIOGECO, Ecologie des Communaut´es, Talence, France 2 Laboratoire G´enie Civil et g´eo-Environnement (LGCgE-EA 4515), Equipe Sols et Environnement, Groupe ISA, Lille Cedex, France Plants and associated microorganisms are used to remediate anthropogenic metal(loid) contamination of water, soils and sediments. This review focuses on the potential of Arundo donax L. (Giant reed) for alleviating risks due to soils, water, and sediments contaminated by trace elements (TE), with emphasis on its advantages and limits over macrophytes and perennial grasses used for bioenergy and plant-based feedstock. Arundo donax is relevant to phytomanage TE-contaminated matrices, notably in its native area, as it possesses characteristics of large biomass production even under nutrient and abiotic stresses, fast growth rate, TE tolerance and accumulation mainly in belowground plant parts. Cultivating A. donax on contaminated lands and in constructed wetlands can contribute to increase land availability and limit the food vs. plant-based feedstock controversy. To gain more tools for decision-taking and sustainable management, further researches on A. donax should focus on: interactions between roots, TE exposure, and rhizosphere and endophytic microorganisms; biomass response to (a)biotic factors; sustainable agricultural practices on marginal and contaminated land; integration into local, efficient, energy and biomass conversion chains with concern to biomass quality and production; Life-Cycle Assessment including contaminant behavior, as well as environmental, agricultural and socio-economic benefits and drawbacks. KEY WORDS: biomass, bioenergy, constructed wetland, metal, metalloid, phytoremediation
HIGHLIGHTS • Arundo donax has high productivity and tolerance to trace element exposure. • Arundo donax is relevant for phytomanaging trace element-contaminated land and water in its suitable climatic regions. • Arundo donax plantations add value to constructed wetlands, marginal and contaminated sites.
Address correspondence to Michel Mench, INRA, UMR BIOGECO 1202, Ecology of Communities, University of Bordeaux 1, Bˆat B2, avenue des Facult´es, F-33405 Talence, France. E-mail: [email protected] 982
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• Integrating Arundo donax into biomass production chains for bioenergy, cellulosic and paper industry, and green chemistry is a viable economic option. • Phytomanagement options using Arundo donax have to consider the invasive potential of this species, as a threat for surrounding ecosystems, and other problematic sides.
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RATIONALE FOR PHYTOREMEDIATION OF METAL(LOID)-CONTAMINATED SOILS AND WATER The worldwide development of industrial and mining activities, urbanization and agricultural sectors has resulted in metal(loid)-contaminated soils and waters (Adriano 2001; Babula et al. 2008; Mench et al. 2010; Moreira et al. 2011; Alloway 2013), which represent a threat to human health, living organisms, and ecosystem services (Lado, Hengl, and Reuter 2008; Rai 2008; Kavamura and Esposito 2010). For convenience, we will refer to both metals (e.g., Cd, Cu, Hg, Ni, Pb, Se, and Zn) and metalloids (e.g., As and Sb), with common concentrations in living organisms below 100 mg kg−1 DW (Adriano 2001; Robinson et al. 2009), as ‘TE’ (Trace Elements) throughout the paper. The remediation of TE-contaminated matrices is a challenge because of the non-degradability of TE in the environment and their accumulation in various ecosystem compartments. For TE-contaminated soils, conventional remedial options commonly involve excavation, physico-chemical treatments such as stabilization, soil washing, and chemical reduction/oxidation, and off-site disposal of soil to ‘secured’ landfills (Glick 2003; Dermont et al. 2008; Schwitzgu´ebel et al. 2011). For water decontamination, common options to remove TE include alkaline precipitation, ion exchange columns, electrochemical removal, filtration, and membrane technologies (Rai 2008). Such soil and water remedial options are generally expensive, may produce adverse effects on ecosystems and often require appropriate methods for waste disposal. Phytoremediation is a set of green, cost-effective and environment-friendly alternative technologies to physico-chemical processes for pollutant removal, which are based on the concomitant use of plants and microorganisms to alleviate pollutant linkages and risks due to excessive exposure to contaminants such as TE and other xenobiotics in soils, water and sediments (Galiulin et al. 2001; Garcia, Faz, and Conesa 2003; Mench et al. 2009; Vangronsveld et al. 2009; Tang et al. 2012). Phytoremediation of TE-contaminated land can take both forms: (1) phytoextraction, the uptake and concentration of TE from the soil into harvestable plant parts; and (2) phytostabilization, the use of plants and associated microbes to enhance TE immobilization in the rhizosphere and roots (Mench et al. 2010; Schwitzgu´ebel et al. 2011; Evangelou et al. 2012a, b). For matrices co-contaminated with TE and organics, phytodegradation and rhizodegradation, both based on the use of plant-microbe associations to degrade organic contaminants, can occur simultaneously with either phytoextraction or phytostabilization (Glick 2003; Lai, Juang, and Chen 2010; Schwitzgu´ebel et al. 2011). All phytoremediation options can be aided with chemical and biological agents (Mench et al. 2010). For quality improvement of polluted water, constructed wetlands (CWs) are an effective phytoremediation tool, cost-efficient and environmentally friendly bio-processes (Brix 1997; Marchand et al. 2010). However, to cut down costs that may result from phytoremediation works, the necessity to get financial opportunities from plant biomass has been highlighted (Maddison et al. 2009a, b; Mench et al. 2010; Vymazal 2011; Evangelou et al. 2012a). A sustainable management of TE-contaminated dryland and wetlands based on phytoremediation options, hereafter referred to as phytomanagement, suggests the use of plants
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F. NSANGANWIMANA ET AL.
whose biomass can be economically valuable (Robinson et al. 2009; Conesa et al. 2012; Evangelou et al. 2012a) and notably can substitute to non-renewable carbon material and promote C sequestration and other ecosystem services. Income and benefits from biomass products (e.g., biofuels, timber, biochemicals, animal feed, soil improvers, etc.) help to mitigate the cost run for the vegetation establishment. The vegetation cover improves soil functional properties, landscape aesthetics, and increases biodiversity (Wong 2003). In doing so, phytomanagement embarks on a win-win strategy that caters local industries in raw materials so as to increase the livelihood of local population (Marchiol and Fellet 2011). Biomass produced from contaminated dryland and wetlands is expected to increase the supply and support the current growing renewable energy market and bio-products within the framework of Bio-economy (Licht and Isebrands 2005; Marchiol and Fellet 2011; Evangelou et al. 2012a). Uses of macrophyte feedstock, e.g., handcraft and building raw materials, compost fertilizer, animal feed, pulp and paper production, and briquettes for cooking stoves, generate financial returns in many countries (Thenya 2006; Hoevers 2011). Macrophyte biomass is also a potential resource for bioenergy, biofuel (Grosshans et al. 2011), and other lignocellulosic derived bioproducts (Ribechini et al. 2012; Losfeld et al. 2012). Grown on contaminated/marginal lands and wetlands, Arundo donax together with other cellulosic feedstocks, can be processed for bioethanol (Ask et al. 2012), biochar production (Williams et al. 2009; Zheng et al. 2013), activated carbons for wastewater treatments and catalysis (Sun et al. 2012, 2013), high quality and cost-effective particleboards alternative to wood (Flores-Yepes et al. 2011; 2012), and by a new pulp/paper industry (Shatalov and Pereira 2008; 2013; Williams and Biswas 2010). How much TE-contaminated area can be phytomanaged, notably by A. donax in its native and suitable bioclimatic regions? Worldwide, some 22 million ha of land were estimated contaminated by TE (GACGC 1994). Figures on contaminated areas (in ha) are more available for the European Union (e.g., EU-18: 4 099 220-4 797 260, Switzerland: 2 600–37 000, Ukraine 5 000 000), North America (e.g., USA: 2 600 000), and developed Asian countries (e.g., Australia: 60 000, China: 8 100 000) than for emerging and poor countries (e.g., Africa 12 000 000) (Evangelou et al. 2012). There are up to 3 million potentially contaminated sites in the EU-15 and soil contamination requiring clean-up is estimated present at approximately 250 000 sites while TE are among the most common harmful contaminants (37%) (EEA 2007). Additionally, two million tons of sewage, industrial and agricultural wastes are discharged into the world’s waterways and 90% of wastewater in developing countries is discharged untreated into either rivers, lakes, wetlands, and into the oceans (Corcoran et al. 2010). Wastewater production is rising in line with the global population. Wetlands are among most affected environments by TE inputs due to their location in topographically depressed positions and high organic matter, clay and (oxi)hydroxide contents (Nehring and Brauning 2002; Vega et al. 2009; Gonzales-Alcaraz et al. 2013; Table 1). Wetlands can remove and/or immobilise contaminants and are considered as green filters against pollution and eutrophication (Vega et al. 2009). Worldwide wetland area available for phytomanagement is not well estimated, but various regional issues have been addressed and it is figured that worldwide 20 million ha of arable land are irrigated with wastewater (Corcoran et al. 2010). In particular, the Montreux Record registers wetland sites on the List of Wetlands of International Importance where changes in ecological character have occurred, are occurring, or are likely to occur as a result of technological developments, pollution or other human interference (RAMSAR 2011). Pollution by TE in aquatic ecosystems and its phytoremediation using wetland plants have been reviewed (Rai
985
Barbafieri et al. (2011)
Boularbah et al. (2006) Rai (2009b)
Rai (2009b)
Deng, Ye and Wong (2004)
Deng, Ye and Wong (2004)
Bragato et al. (2009)
2
3
4
5
5
6
4
Bonanno (2012)
References
1
Study #
Site characteristics
NW drained by Acquicella stream receiving domestic and industrial discharges A. donax NW, near abandoned Ingurtosu mining site and drained by Naracauli stream A. donax NW, near a polymetallic mining site E. crassipes∗ NW, receives industrial effluents from a thermal power plant L. minor∗ NW, receives industrial effluents from a thermal power plant P. arundinacea NW, receives wastewater and sediments from a Cu mine in Daye County P. australis CW receives effluents from Fankou Pb/Zn mine P. australis CW, located in the Venice lagoon watershed
A. donax
Plant species
—
17
NI
Guangdong Province (China) Padova (Italy)
Summer-Autumn
17
1.1–1.4 (2.9–4.5)
1.1–1.4 (2.9–4.5)
21–33 (1.2–1.8)
95
5770
14–20 (16–27)
14–20 (16–27)
290-570
< 31.5
NI
NI
NI
—
104 (16.3)
Cu
100
0.3 (< 0.5)
Cd
Hubei Province (China)
Belwadah (India)
Belwadah (India)
NI
Spring
Sardinia (Italy
South Morocco
Autumn
sampling season
Sicily (Italy)
Location
—
—
78–110 (11–22)
78–110 (11–22)
—
—
815 (< 0.5)
Mn
3290
112
6–10 (8–17)
383– 5756 6–10 (8–17)
2900
56.5 (< 1)
Pb
4805
713
47–55 (11–21)
1738– 8361 47–55 (11–21)
31000
271 (1.4)
Zn
36–57 — 83–108 (2.0–4.5) (0.8–63) (Continued on next page)
—
—
23–35 (16–36)
23–35 (16–36)
—
—
17.5 (0.7)
Ni
Total TE concentrations (mg kg−1 DW) in sediments (and in water, mg L−1)
Table 1 Site characteristics and TE concentrations in sediments. TE concentrations (mg L−1) in water are indicated within brackets.
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9
∗ submerged
NW at the mouth area of Imera Meridionale
Site characteristics
S. americanus CW, reservoir of industrial runoffs, near a dumping site for domestic wastes T. latifolia CW receives effluents from Fankou Pb/Zn mine T. latifolia CW, reservoir of industrial runoffs, near a dumping site for domestic wastes T. latifolia NW drained by Kheli stream receiving discharges from a Wastewater Treatment Plant
P. australis
Plant species
17
5–14
NI
February
NI
Guangdong Province (China) Potosi (Mexico)
Elazig (Turkey)
0.2–0.3
5–13
February
Potosi (Mexico)
0.7 (0.4)
Cd
Late summer
sampling season
Sicily (Italy)
Location
and floating species; NW: natural wetland; CW: constructed wetland. NI = Not informed.
CarranzaAlvarez et al. (2008) Sasmaz, Obek and Hasar (2008)
8
8
Bonanno and Lo Giudice (2010) CarranzaAlvarez et al. (2008) Deng, Ye and Wong (2004)
References
7
Study #
40
—
95
—
11 (84.5)
Cu
400
—
—
—
1209 (181.8)
Mn
40–60
—
—
—
29 (10.8)
Ni
5–15
20–56
3290
20–55
3 (0.4)
Pb
60–80
—
4805
0
10 (0.4)
Zn
Total TE concentrations (mg kg−1 DW) in sediments (and in water, mg L−1)
Table 1 Site characteristics and TE concentrations in sediments. TE concentrations (mg L−1) in water are indicated within brackets. (Continued)
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USE OF GIANT REED TO REMEDIATE CONTAMINATED WATER AND SOILS
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2008; Marchand et al. 2010). For instance, Gonzalez-Alcaraz et al. (2013) reported the phytomanagement of metal-polluted wetlands affected by mine wastes. A challenge is to determine where and when the life cycle of A. donax is relevant for the phytomanagement of TE-contaminated land and wetlands in line with biomass production. Therefore, this review focuses on the potential of A. donax for linking decreased exposure to contaminants and plant-based feedstock production in TE-contaminated ecosystems such as natural and constructed wetlands, and contaminated lands.
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ARUNDO DONAX: DESCRIPTION AND ECOLOGY Arundo donax L. (giant reed; other common names include carrizo, arundo, spanish cane, wild cane, danubian reed, giant Danube reed, etc.) is a perennial rhizomatous grass reaching 3–10 m tall, growing in many-stemmed cane-like clumps, sprouting from rhizomes, which form large colonies many meters across and penetrate deep into the soil up to 1 m (Sharma et al. 2005; Csurhes 2009; Ceotto and Di Candilo 2010). All details regarding morphological traits and taxonomy of the species have been fully developed in Csurhes (2009) and Pilu et al. (2012). Arundo donax is native to warm tropical Asia and the Mediterranean region. It is widely planted and naturalized in the mild temperate, subtropical and tropical regions of both hemispheres. It occurs in Southern Europe from the central Atlantic coast of Portugal, inland along the major rivers of the Iberian Peninsula, along the Mediterranean coast from Spain to Greece, including the warmer parts of the Adriatic coast (Lewandowski et al. 2003; Csurhes 2009). Apart from Europe, it is naturally found in eastern and southern Asia, parts of Africa and southern Arabic Peninsula. In addition to its native range, the global distribution of A. donax now includes naturalized populations in North and South America, Asia, Australia, New Zealand, and numerous islands across the Pacific and the Caribbean (Allinson 2007; Csurhes 2009). Arundo donax grows in a variety of soil types, from coarse sands to heavy clays, but generally prefers well-drained soils above the mean water level in freshwater streams (Lewandowski et al. 2003; Ceotto and Di Candilo 2010). It can also grow on infertile and saline soils but responds positively to nutrients (Williams et al. 2009). It tolerates a wide range of climates in areas that receive 300–4000 mm rainfall per annum. It is considered as a mesophyte (either hydrophyte or xerophyte), halophyte, growing along lakes, streams, drains and dumps, in wet soils (Mavrogianopoulos, Vogli, and Kyritsis 2002; Lewandowski et al. 2003; Csurhes 2009). AVAILABILITY OF PLANT-BASED FEEDSTOCK FROM CWS AND TE-CONTAMINATED LANDS: WHAT ARE ADVANTAGES FROM A. DONAX? Biomass Quantity, Quality and Potential Uses Plants growing in wetlands referred to as “macrophytes” are generally fast-growing and high biomass producers. Arundo donax, Phragmites sp and Typha sp are among the most productive (Table 2). Macrophytes tolerate and accumulate a range of TE, mainly in roots and rhizomes (Bonnano and Lo Giudice 2010; Marchand et al. 2010). High TE concentrations can occur in shoots of submerged and floating species (Table 2). In contrast, many rooted macrophytes used in CWs, including A. donax, have a TE-excluder phenotype, being not suitable for the phytoextraction option (Table 3). Harvested shoots of rooted
988
F. NSANGANWIMANA ET AL. Table 2 Peak-biomass (kg m–2) produced by macrophytes at the end of the growing season.
Plant species
AB biomass
BG biomass
growing medium
Location
References
Arundo donax
6.7 1.5–3.1 4–8 4–4.5 1.3–2.3 1.7– 5.1 2.3 0.23 2.2 1.4–1.8 2.8
2
NW NW CW CW CW CW CW CW NW CW NW
India Italy Tropical regions Tropical regions Czech Republic Czech Republic Morocco Morocco Morocco Estonia Oklahoma USA
1 2 3 3 4 4 5 5 5 6 7
Eichhornia crassipes Lemna minor Phalaris arundinacea Phragmites australis
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Scirpus americanus Typha angustifolia Typha latifolia
0.5–1.2 0.9–1 3 3.5 0.7–1.6
AB: Aboveground; BG: Belowground; CW: constructed wetland; NW: natural wetland. 1. Sharma et al., (1998); 2. Angelini, Ceccarini, and Bonari (2005); 3. Hoevers (2011); 4. Vymazal et al. (2011); 5. Ennabili, Ater, and Radoux (1998); 6. Maddison et al. (2009a); 7. Cronk and Fennessy (2001).
macrophytes usually have common TE concentrations, which are low compared to those in conventional fuels such as coals and lignites (Zhang and Zhou 2009). Consequently, recycling TE from rooted macrophyte ashes as ores is generally not a relevant option. The disposal of most macrophyte biomasses into landfills is mainly unjustified based on its ionome and not a financially viable option. Moreover decaying organic matter can release TE into the environment and may become a diffuse contamination source. The possibility of recycling ash from Phragmites australis and A. donax biomasses, collected in an urban stream affected by domestic sewage, as a fertilizer for agriculture and forestry has been investigated (Bonanno et al. 2013). Metal (Cd, Cr, Cu, Mn, Pb, and Zn) concentrations in ash were 1.5–3 times as high as the values in plant tissues but remained much lower than the legal limits for ash reutilization in agriculture and forestry. Biomass transformation using thermochemical and biological technologies and valorization of its different by-products must be also promoted to manage such TE-containing biomasses. With reference to its constituents namely lignin (10–25%), hemicelluloses (20–30%), cellulose (30–50%), hydrogen (5%), proteins (e.g., 6–17% DW for E. crassipes, Paepatung, Nopharatana, and Songkasiri 2009), lipids, and mineral matter, biomass of macrophytes such as Eichhornia sp, Typha sp and A. donax is a potential resource for bioenergy, and other bioproducts (Bhattacharya and Kumar 2010; Dipu, Kumar, and Thanga 2011; Fazio and Monti 2011). Macrophyte biomass properties suitable for bioenergy have been described and quantified (Table 4). Arundo donax is characterized by high conversion rate of biomass into ethanol, high cellulose content, and low N and ash contents. Major bioenergies include bioethanol as engine fuel and biogas, which can be used in generation of heat and electricity. Arundo donax offers competitive advantage over other biomass crops. Considering the same surface area, A. donax yields more bioethanol than other agronomic energy crops, i.e. corn and sugarcane, and has more energy output than other industrial crops including switchgrass (Figure 1). It can be an alternative for biorefineries using poplar or similar hardwood feedstocks (Bura, Ewanick, and Gustafson 2012). Promising technologies for the conversion of phytoremediation-based biomasses into energy or fine chemicals, e.g., solvolysis, gasification, combustion, flash pyrolysis, hydrolysis, biocatalysis, and methanisation, are currently developing (Carrier et al. 2011;
989
A. donax A. donax P. arundinacea P. australis P. australis T. latifolia
1 2 5 5 7 9
2.1 — 7.1 51 398 90
International Journal of Phytoremediation Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/bijp20
Arundo donax L., a Candidate for Phytomanaging Water and Soils Contaminated by Trace Elements and Producing Plant-Based Feedstock. A Review F. Nsanganwimana
a b
a
b
, L. Marchand , F. Douay & M. Mench
a
a
Click for updates
INRA, UMR BIOGECO, Route d’Arcachon, Cestas cedex, France, Université Bordeaux, UMR BIOGECO, Ecologie des Communautés , Talence , France b
Laboratoire Génie Civil et géo-Environnement (LGCgE-EA 4515), Equipe Sols et Environnement, Groupe ISA , Lille Cedex , France Accepted author version posted online: 25 Aug 2013.Published online: 06 Feb 2014.
To cite this article: F. Nsanganwimana , L. Marchand , F. Douay & M. Mench (2014) Arundo donax L., a Candidate for Phytomanaging Water and Soils Contaminated by Trace Elements and Producing Plant-Based Feedstock. A Review, International Journal of Phytoremediation, 16:10, 982-1017, DOI: 10.1080/15226514.2013.810580 To link to this article: http://dx.doi.org/10.1080/15226514.2013.810580
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [Northeastern University] at 09:33 22 October 2014
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/termsand-conditions
International Journal of Phytoremediation, 16:982–1017, 2014 C 2014 INRA Copyright ISSN: 1522-6514 print / 1549-7879 online DOI: 10.1080/15226514.2013.810580
ARUNDO DONAX L., A CANDIDATE FOR PHYTOMANAGING WATER AND SOILS CONTAMINATED BY TRACE ELEMENTS AND PRODUCING PLANT-BASED FEEDSTOCK. A REVIEW F. Nsanganwimana,1,2 L. Marchand,1 F. Douay,2 and M. Mench1 Downloaded by [Northeastern University] at 09:33 22 October 2014
1
INRA, UMR BIOGECO, Route d’Arcachon, Cestas cedex, France, Universit´e Bordeaux , UMR BIOGECO, Ecologie des Communaut´es, Talence, France 2 Laboratoire G´enie Civil et g´eo-Environnement (LGCgE-EA 4515), Equipe Sols et Environnement, Groupe ISA, Lille Cedex, France Plants and associated microorganisms are used to remediate anthropogenic metal(loid) contamination of water, soils and sediments. This review focuses on the potential of Arundo donax L. (Giant reed) for alleviating risks due to soils, water, and sediments contaminated by trace elements (TE), with emphasis on its advantages and limits over macrophytes and perennial grasses used for bioenergy and plant-based feedstock. Arundo donax is relevant to phytomanage TE-contaminated matrices, notably in its native area, as it possesses characteristics of large biomass production even under nutrient and abiotic stresses, fast growth rate, TE tolerance and accumulation mainly in belowground plant parts. Cultivating A. donax on contaminated lands and in constructed wetlands can contribute to increase land availability and limit the food vs. plant-based feedstock controversy. To gain more tools for decision-taking and sustainable management, further researches on A. donax should focus on: interactions between roots, TE exposure, and rhizosphere and endophytic microorganisms; biomass response to (a)biotic factors; sustainable agricultural practices on marginal and contaminated land; integration into local, efficient, energy and biomass conversion chains with concern to biomass quality and production; Life-Cycle Assessment including contaminant behavior, as well as environmental, agricultural and socio-economic benefits and drawbacks. KEY WORDS: biomass, bioenergy, constructed wetland, metal, metalloid, phytoremediation
HIGHLIGHTS • Arundo donax has high productivity and tolerance to trace element exposure. • Arundo donax is relevant for phytomanaging trace element-contaminated land and water in its suitable climatic regions. • Arundo donax plantations add value to constructed wetlands, marginal and contaminated sites.
Address correspondence to Michel Mench, INRA, UMR BIOGECO 1202, Ecology of Communities, University of Bordeaux 1, Bˆat B2, avenue des Facult´es, F-33405 Talence, France. E-mail: [email protected] 982
USE OF GIANT REED TO REMEDIATE CONTAMINATED WATER AND SOILS
983
• Integrating Arundo donax into biomass production chains for bioenergy, cellulosic and paper industry, and green chemistry is a viable economic option. • Phytomanagement options using Arundo donax have to consider the invasive potential of this species, as a threat for surrounding ecosystems, and other problematic sides.
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RATIONALE FOR PHYTOREMEDIATION OF METAL(LOID)-CONTAMINATED SOILS AND WATER The worldwide development of industrial and mining activities, urbanization and agricultural sectors has resulted in metal(loid)-contaminated soils and waters (Adriano 2001; Babula et al. 2008; Mench et al. 2010; Moreira et al. 2011; Alloway 2013), which represent a threat to human health, living organisms, and ecosystem services (Lado, Hengl, and Reuter 2008; Rai 2008; Kavamura and Esposito 2010). For convenience, we will refer to both metals (e.g., Cd, Cu, Hg, Ni, Pb, Se, and Zn) and metalloids (e.g., As and Sb), with common concentrations in living organisms below 100 mg kg−1 DW (Adriano 2001; Robinson et al. 2009), as ‘TE’ (Trace Elements) throughout the paper. The remediation of TE-contaminated matrices is a challenge because of the non-degradability of TE in the environment and their accumulation in various ecosystem compartments. For TE-contaminated soils, conventional remedial options commonly involve excavation, physico-chemical treatments such as stabilization, soil washing, and chemical reduction/oxidation, and off-site disposal of soil to ‘secured’ landfills (Glick 2003; Dermont et al. 2008; Schwitzgu´ebel et al. 2011). For water decontamination, common options to remove TE include alkaline precipitation, ion exchange columns, electrochemical removal, filtration, and membrane technologies (Rai 2008). Such soil and water remedial options are generally expensive, may produce adverse effects on ecosystems and often require appropriate methods for waste disposal. Phytoremediation is a set of green, cost-effective and environment-friendly alternative technologies to physico-chemical processes for pollutant removal, which are based on the concomitant use of plants and microorganisms to alleviate pollutant linkages and risks due to excessive exposure to contaminants such as TE and other xenobiotics in soils, water and sediments (Galiulin et al. 2001; Garcia, Faz, and Conesa 2003; Mench et al. 2009; Vangronsveld et al. 2009; Tang et al. 2012). Phytoremediation of TE-contaminated land can take both forms: (1) phytoextraction, the uptake and concentration of TE from the soil into harvestable plant parts; and (2) phytostabilization, the use of plants and associated microbes to enhance TE immobilization in the rhizosphere and roots (Mench et al. 2010; Schwitzgu´ebel et al. 2011; Evangelou et al. 2012a, b). For matrices co-contaminated with TE and organics, phytodegradation and rhizodegradation, both based on the use of plant-microbe associations to degrade organic contaminants, can occur simultaneously with either phytoextraction or phytostabilization (Glick 2003; Lai, Juang, and Chen 2010; Schwitzgu´ebel et al. 2011). All phytoremediation options can be aided with chemical and biological agents (Mench et al. 2010). For quality improvement of polluted water, constructed wetlands (CWs) are an effective phytoremediation tool, cost-efficient and environmentally friendly bio-processes (Brix 1997; Marchand et al. 2010). However, to cut down costs that may result from phytoremediation works, the necessity to get financial opportunities from plant biomass has been highlighted (Maddison et al. 2009a, b; Mench et al. 2010; Vymazal 2011; Evangelou et al. 2012a). A sustainable management of TE-contaminated dryland and wetlands based on phytoremediation options, hereafter referred to as phytomanagement, suggests the use of plants
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whose biomass can be economically valuable (Robinson et al. 2009; Conesa et al. 2012; Evangelou et al. 2012a) and notably can substitute to non-renewable carbon material and promote C sequestration and other ecosystem services. Income and benefits from biomass products (e.g., biofuels, timber, biochemicals, animal feed, soil improvers, etc.) help to mitigate the cost run for the vegetation establishment. The vegetation cover improves soil functional properties, landscape aesthetics, and increases biodiversity (Wong 2003). In doing so, phytomanagement embarks on a win-win strategy that caters local industries in raw materials so as to increase the livelihood of local population (Marchiol and Fellet 2011). Biomass produced from contaminated dryland and wetlands is expected to increase the supply and support the current growing renewable energy market and bio-products within the framework of Bio-economy (Licht and Isebrands 2005; Marchiol and Fellet 2011; Evangelou et al. 2012a). Uses of macrophyte feedstock, e.g., handcraft and building raw materials, compost fertilizer, animal feed, pulp and paper production, and briquettes for cooking stoves, generate financial returns in many countries (Thenya 2006; Hoevers 2011). Macrophyte biomass is also a potential resource for bioenergy, biofuel (Grosshans et al. 2011), and other lignocellulosic derived bioproducts (Ribechini et al. 2012; Losfeld et al. 2012). Grown on contaminated/marginal lands and wetlands, Arundo donax together with other cellulosic feedstocks, can be processed for bioethanol (Ask et al. 2012), biochar production (Williams et al. 2009; Zheng et al. 2013), activated carbons for wastewater treatments and catalysis (Sun et al. 2012, 2013), high quality and cost-effective particleboards alternative to wood (Flores-Yepes et al. 2011; 2012), and by a new pulp/paper industry (Shatalov and Pereira 2008; 2013; Williams and Biswas 2010). How much TE-contaminated area can be phytomanaged, notably by A. donax in its native and suitable bioclimatic regions? Worldwide, some 22 million ha of land were estimated contaminated by TE (GACGC 1994). Figures on contaminated areas (in ha) are more available for the European Union (e.g., EU-18: 4 099 220-4 797 260, Switzerland: 2 600–37 000, Ukraine 5 000 000), North America (e.g., USA: 2 600 000), and developed Asian countries (e.g., Australia: 60 000, China: 8 100 000) than for emerging and poor countries (e.g., Africa 12 000 000) (Evangelou et al. 2012). There are up to 3 million potentially contaminated sites in the EU-15 and soil contamination requiring clean-up is estimated present at approximately 250 000 sites while TE are among the most common harmful contaminants (37%) (EEA 2007). Additionally, two million tons of sewage, industrial and agricultural wastes are discharged into the world’s waterways and 90% of wastewater in developing countries is discharged untreated into either rivers, lakes, wetlands, and into the oceans (Corcoran et al. 2010). Wastewater production is rising in line with the global population. Wetlands are among most affected environments by TE inputs due to their location in topographically depressed positions and high organic matter, clay and (oxi)hydroxide contents (Nehring and Brauning 2002; Vega et al. 2009; Gonzales-Alcaraz et al. 2013; Table 1). Wetlands can remove and/or immobilise contaminants and are considered as green filters against pollution and eutrophication (Vega et al. 2009). Worldwide wetland area available for phytomanagement is not well estimated, but various regional issues have been addressed and it is figured that worldwide 20 million ha of arable land are irrigated with wastewater (Corcoran et al. 2010). In particular, the Montreux Record registers wetland sites on the List of Wetlands of International Importance where changes in ecological character have occurred, are occurring, or are likely to occur as a result of technological developments, pollution or other human interference (RAMSAR 2011). Pollution by TE in aquatic ecosystems and its phytoremediation using wetland plants have been reviewed (Rai
985
Barbafieri et al. (2011)
Boularbah et al. (2006) Rai (2009b)
Rai (2009b)
Deng, Ye and Wong (2004)
Deng, Ye and Wong (2004)
Bragato et al. (2009)
2
3
4
5
5
6
4
Bonanno (2012)
References
1
Study #
Site characteristics
NW drained by Acquicella stream receiving domestic and industrial discharges A. donax NW, near abandoned Ingurtosu mining site and drained by Naracauli stream A. donax NW, near a polymetallic mining site E. crassipes∗ NW, receives industrial effluents from a thermal power plant L. minor∗ NW, receives industrial effluents from a thermal power plant P. arundinacea NW, receives wastewater and sediments from a Cu mine in Daye County P. australis CW receives effluents from Fankou Pb/Zn mine P. australis CW, located in the Venice lagoon watershed
A. donax
Plant species
—
17
NI
Guangdong Province (China) Padova (Italy)
Summer-Autumn
17
1.1–1.4 (2.9–4.5)
1.1–1.4 (2.9–4.5)
21–33 (1.2–1.8)
95
5770
14–20 (16–27)
14–20 (16–27)
290-570
< 31.5
NI
NI
NI
—
104 (16.3)
Cu
100
0.3 (< 0.5)
Cd
Hubei Province (China)
Belwadah (India)
Belwadah (India)
NI
Spring
Sardinia (Italy
South Morocco
Autumn
sampling season
Sicily (Italy)
Location
—
—
78–110 (11–22)
78–110 (11–22)
—
—
815 (< 0.5)
Mn
3290
112
6–10 (8–17)
383– 5756 6–10 (8–17)
2900
56.5 (< 1)
Pb
4805
713
47–55 (11–21)
1738– 8361 47–55 (11–21)
31000
271 (1.4)
Zn
36–57 — 83–108 (2.0–4.5) (0.8–63) (Continued on next page)
—
—
23–35 (16–36)
23–35 (16–36)
—
—
17.5 (0.7)
Ni
Total TE concentrations (mg kg−1 DW) in sediments (and in water, mg L−1)
Table 1 Site characteristics and TE concentrations in sediments. TE concentrations (mg L−1) in water are indicated within brackets.
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9
∗ submerged
NW at the mouth area of Imera Meridionale
Site characteristics
S. americanus CW, reservoir of industrial runoffs, near a dumping site for domestic wastes T. latifolia CW receives effluents from Fankou Pb/Zn mine T. latifolia CW, reservoir of industrial runoffs, near a dumping site for domestic wastes T. latifolia NW drained by Kheli stream receiving discharges from a Wastewater Treatment Plant
P. australis
Plant species
17
5–14
NI
February
NI
Guangdong Province (China) Potosi (Mexico)
Elazig (Turkey)
0.2–0.3
5–13
February
Potosi (Mexico)
0.7 (0.4)
Cd
Late summer
sampling season
Sicily (Italy)
Location
and floating species; NW: natural wetland; CW: constructed wetland. NI = Not informed.
CarranzaAlvarez et al. (2008) Sasmaz, Obek and Hasar (2008)
8
8
Bonanno and Lo Giudice (2010) CarranzaAlvarez et al. (2008) Deng, Ye and Wong (2004)
References
7
Study #
40
—
95
—
11 (84.5)
Cu
400
—
—
—
1209 (181.8)
Mn
40–60
—
—
—
29 (10.8)
Ni
5–15
20–56
3290
20–55
3 (0.4)
Pb
60–80
—
4805
0
10 (0.4)
Zn
Total TE concentrations (mg kg−1 DW) in sediments (and in water, mg L−1)
Table 1 Site characteristics and TE concentrations in sediments. TE concentrations (mg L−1) in water are indicated within brackets. (Continued)
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USE OF GIANT REED TO REMEDIATE CONTAMINATED WATER AND SOILS
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2008; Marchand et al. 2010). For instance, Gonzalez-Alcaraz et al. (2013) reported the phytomanagement of metal-polluted wetlands affected by mine wastes. A challenge is to determine where and when the life cycle of A. donax is relevant for the phytomanagement of TE-contaminated land and wetlands in line with biomass production. Therefore, this review focuses on the potential of A. donax for linking decreased exposure to contaminants and plant-based feedstock production in TE-contaminated ecosystems such as natural and constructed wetlands, and contaminated lands.
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ARUNDO DONAX: DESCRIPTION AND ECOLOGY Arundo donax L. (giant reed; other common names include carrizo, arundo, spanish cane, wild cane, danubian reed, giant Danube reed, etc.) is a perennial rhizomatous grass reaching 3–10 m tall, growing in many-stemmed cane-like clumps, sprouting from rhizomes, which form large colonies many meters across and penetrate deep into the soil up to 1 m (Sharma et al. 2005; Csurhes 2009; Ceotto and Di Candilo 2010). All details regarding morphological traits and taxonomy of the species have been fully developed in Csurhes (2009) and Pilu et al. (2012). Arundo donax is native to warm tropical Asia and the Mediterranean region. It is widely planted and naturalized in the mild temperate, subtropical and tropical regions of both hemispheres. It occurs in Southern Europe from the central Atlantic coast of Portugal, inland along the major rivers of the Iberian Peninsula, along the Mediterranean coast from Spain to Greece, including the warmer parts of the Adriatic coast (Lewandowski et al. 2003; Csurhes 2009). Apart from Europe, it is naturally found in eastern and southern Asia, parts of Africa and southern Arabic Peninsula. In addition to its native range, the global distribution of A. donax now includes naturalized populations in North and South America, Asia, Australia, New Zealand, and numerous islands across the Pacific and the Caribbean (Allinson 2007; Csurhes 2009). Arundo donax grows in a variety of soil types, from coarse sands to heavy clays, but generally prefers well-drained soils above the mean water level in freshwater streams (Lewandowski et al. 2003; Ceotto and Di Candilo 2010). It can also grow on infertile and saline soils but responds positively to nutrients (Williams et al. 2009). It tolerates a wide range of climates in areas that receive 300–4000 mm rainfall per annum. It is considered as a mesophyte (either hydrophyte or xerophyte), halophyte, growing along lakes, streams, drains and dumps, in wet soils (Mavrogianopoulos, Vogli, and Kyritsis 2002; Lewandowski et al. 2003; Csurhes 2009). AVAILABILITY OF PLANT-BASED FEEDSTOCK FROM CWS AND TE-CONTAMINATED LANDS: WHAT ARE ADVANTAGES FROM A. DONAX? Biomass Quantity, Quality and Potential Uses Plants growing in wetlands referred to as “macrophytes” are generally fast-growing and high biomass producers. Arundo donax, Phragmites sp and Typha sp are among the most productive (Table 2). Macrophytes tolerate and accumulate a range of TE, mainly in roots and rhizomes (Bonnano and Lo Giudice 2010; Marchand et al. 2010). High TE concentrations can occur in shoots of submerged and floating species (Table 2). In contrast, many rooted macrophytes used in CWs, including A. donax, have a TE-excluder phenotype, being not suitable for the phytoextraction option (Table 3). Harvested shoots of rooted
988
F. NSANGANWIMANA ET AL. Table 2 Peak-biomass (kg m–2) produced by macrophytes at the end of the growing season.
Plant species
AB biomass
BG biomass
growing medium
Location
References
Arundo donax
6.7 1.5–3.1 4–8 4–4.5 1.3–2.3 1.7– 5.1 2.3 0.23 2.2 1.4–1.8 2.8
2
NW NW CW CW CW CW CW CW NW CW NW
India Italy Tropical regions Tropical regions Czech Republic Czech Republic Morocco Morocco Morocco Estonia Oklahoma USA
1 2 3 3 4 4 5 5 5 6 7
Eichhornia crassipes Lemna minor Phalaris arundinacea Phragmites australis
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Scirpus americanus Typha angustifolia Typha latifolia
0.5–1.2 0.9–1 3 3.5 0.7–1.6
AB: Aboveground; BG: Belowground; CW: constructed wetland; NW: natural wetland. 1. Sharma et al., (1998); 2. Angelini, Ceccarini, and Bonari (2005); 3. Hoevers (2011); 4. Vymazal et al. (2011); 5. Ennabili, Ater, and Radoux (1998); 6. Maddison et al. (2009a); 7. Cronk and Fennessy (2001).
macrophytes usually have common TE concentrations, which are low compared to those in conventional fuels such as coals and lignites (Zhang and Zhou 2009). Consequently, recycling TE from rooted macrophyte ashes as ores is generally not a relevant option. The disposal of most macrophyte biomasses into landfills is mainly unjustified based on its ionome and not a financially viable option. Moreover decaying organic matter can release TE into the environment and may become a diffuse contamination source. The possibility of recycling ash from Phragmites australis and A. donax biomasses, collected in an urban stream affected by domestic sewage, as a fertilizer for agriculture and forestry has been investigated (Bonanno et al. 2013). Metal (Cd, Cr, Cu, Mn, Pb, and Zn) concentrations in ash were 1.5–3 times as high as the values in plant tissues but remained much lower than the legal limits for ash reutilization in agriculture and forestry. Biomass transformation using thermochemical and biological technologies and valorization of its different by-products must be also promoted to manage such TE-containing biomasses. With reference to its constituents namely lignin (10–25%), hemicelluloses (20–30%), cellulose (30–50%), hydrogen (5%), proteins (e.g., 6–17% DW for E. crassipes, Paepatung, Nopharatana, and Songkasiri 2009), lipids, and mineral matter, biomass of macrophytes such as Eichhornia sp, Typha sp and A. donax is a potential resource for bioenergy, and other bioproducts (Bhattacharya and Kumar 2010; Dipu, Kumar, and Thanga 2011; Fazio and Monti 2011). Macrophyte biomass properties suitable for bioenergy have been described and quantified (Table 4). Arundo donax is characterized by high conversion rate of biomass into ethanol, high cellulose content, and low N and ash contents. Major bioenergies include bioethanol as engine fuel and biogas, which can be used in generation of heat and electricity. Arundo donax offers competitive advantage over other biomass crops. Considering the same surface area, A. donax yields more bioethanol than other agronomic energy crops, i.e. corn and sugarcane, and has more energy output than other industrial crops including switchgrass (Figure 1). It can be an alternative for biorefineries using poplar or similar hardwood feedstocks (Bura, Ewanick, and Gustafson 2012). Promising technologies for the conversion of phytoremediation-based biomasses into energy or fine chemicals, e.g., solvolysis, gasification, combustion, flash pyrolysis, hydrolysis, biocatalysis, and methanisation, are currently developing (Carrier et al. 2011;
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A. donax A. donax P. arundinacea P. australis P. australis T. latifolia
1 2 5 5 7 9
2.1 — 7.1 51 398 90
