Climate Change and Plant Abiotic Stress Tolerance || Can Carbon in Bioenergy Crops Mitigate Global Climate Change?

Part Three

Approaches for Climate Change Mitigation

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Climate Change and Plant Abiotic Stress Tolerance, First Edition. Edited by Narendra Tuteja and Sarvajeet S. Gill.� 2014 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2014 by Wiley-VCH Verlag GmbH & Co. KGaA.

14

Can Carbon in Bioenergy Crops Mitigate Global

Climate Change?

Abdullah A. Jaradat

Abstract

Different forms of carbon (C) cycle continuously through several pools in naturaland managed ecosystems and spheres. Carbon’s recent “commodification,” as anegative environmental externality, has rendered it a “scarce” and “tradable”element. Although C supply in nature is not limited, energy is required to make itavailable as a plant nutrient, assimilate it in plant tissues, and sequester it astemporary or recalcitrant C in soils. Human demand for C-based energy and plant-fixed C has accelerated, and altered its global cycle, raised its atmospheric content,contributed to climate change through global warming, and impacted severalprovisioning, regulating, and supporting ecosystem services. Agroecosystems areboth sources and sinks of C. In a carbon dioxide-constrained world, plant-fixed andsequestered C in natural and managed ecosystems has a potential role inmitigating climate change, providing C-neutral and renewable bioenergy, andpositively affecting ecosystem services. Due to the intricacies of the complex,interconnected biogeochemical cycles involving C, nitrogen, and water in whichsoils play an important role, bioenergy crops do not provide an easy solution toclimate change mitigation, they may contribute to it. This chapter presents a criticalreview assessing the state of knowledge, and exploring opportunities andchallenges of the role of C in bioenergy crops in mitigating global climate change,while sustainably providing other ecosystem services.

14.1

Introduction

A perennial and complex question for scientists to answer in the early years of thetwenty-first century [1–4] is how global climate change – with increasing atmo-spheric carbon dioxide concentration [CO2] and rising temperature – will affectcarbon (C) sequestration? Practically, however, the question goes beyond Csequestration to address a wide range of interrelated economic, developmental,

Climate Change and Plant Abiotic Stress Tolerance, First Edition. Edited by Narendra Tuteja and Sarvajeet S. Gill.� 2014 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2014 by Wiley-VCH Verlag GmbH & Co. KGaA.

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food, biodiversity, nutrients and water cycling, and environmental issues. Arguably[5–10], the most pressing issue is how to manage bioenergy crops and soils for awarming Earth in a food-insecure and energy-starved world? Global warming willcertainly affect the C cycle, and the two interrelated nitrogen (N) and water cycles[10–13], but the direction of the effect, so far, is either unclear or the evidence isinconclusive to make a concrete projection [14–16].Since the early 1800s and after the onset of the industrial revolution followed by

the expansion of agriculture, the clearing of forests, and especially the burning offossil fuels, a dramatic increase in the atmospheric [CO2] from around 270 to400 ppm (or m mol mol�1) (www.co2now.org) has resulted in global warming andimpacted several complex, interconnected biogeochemical cycles, involving C, N,and water, in which soils play an important role [11,17,18]. Over the last twocenturies, the industrial and agricultural revolutions fundamentally and simulta-neously altered the composition of the biosphere and the role of biomass in socialmetabolism [19–21]. The C footprint reflects the level of social metabolism andserves as an important environmental protection indicator [19,22]. The biogeo-chemical effects are an important aspect of climate impacts of biofuels at local andglobal scales. The current anthropogenic C flux of þ8.4 Pg C year�1 is large(Pg¼ petagram¼ 1015 g¼ 1 gigaton, Gt; 1 billion metric tons); it mostly irreversiblytransforms C from its terrestrial pool to the atmosphere, which has relatively asmall capacity of about 770 Pg C; therefore, the anthropogenic C flux leads tosignificant increases in the content of C in the atmosphere at an alarming rate ofabout 2.2 ppm year�1 [4,23,24].The soil content of organic C constitutes less than 5% of the mass of soil material

and is generally concentrated mainly in the upper 20–40 cm. However, that contentvaries greatly, from less than 1% by mass in some arid-zone soils (Aridisols) to 50%or more in waterlogged organic soils (Histosols) [25–28]. In addition to theircontent of organic C, soils in arid and semi-arid regions also contain large reservesof inorganic C in the form of CaCO3 and MgCO3 [26,28]. The current content of Cin soil is below its ecological potential; therefore, it is possible to sequester moreCO2 in soils. Soil-based processes can serve as a C sink, where C is sequentiallyremoved from the atmosphere through bioenergy crops, forestry, and landmanagement activities. According to the Kyoto Protocol, the sequestered C may besubtracted from a country’s allowable level of emissions and thus mitigateanthropogenic CO2-induced climate warming [1,3,23].The public and private sectors are increasingly interested in stabilizing [CO2] and

other greenhouse gases (GHGs) to mitigate the risk of global climate change,which places new and more challenging demands on agriculture, land and waterresources, biodiversity, and the environment [13,29,30]. The greenhouse effect isthe process by which absorption of infrared radiation by atmospheric gases warmsthe Earth’s atmosphere and surface. More recently, however, there is a growinginterest in balancing ecosystem services, including provisioning, supporting, andregulating services, as a result of global climate change [31–33]. Biomass has thepotential to become one of the major global primary energy sources duringthe twenty-first century and the future demand for biofuels is one component of

346 14 Can Carbon in Bioenergy Crops Mitigate Global Climate Change?

http://www.co2now.org

the expanding human demand for photosynthetically fixed C [13,34], and the needis urgent for information and technologies in order to make wise decisions aboutland-use options [35–37] and to derive more realistic estimates of future bioenergypotentials [38–40]. Yield expectations of bioenergy plantations also differ widely,from 70 to 600Mgha�1 year�1. Differences in yields of bioenergy plantationslargely result from assumptions on land suitability, choice of bioenergy crop, andmanagement [41–44].The sustainability of bioenergy production in different parts of the world may not

be totally realistic [43,45–48]. Given the limited land area that is available currentlyor in the foreseeable future for bioenergy production, the contribution of bioenergycrops to global climate change mitigation is likely to remain less than 10% of globalenergy supply in 2050 [49–51]. The International Energy Agency has projected thatbioenergy could supply over 20% (or 800 EJ year�1 (EJ¼ exajoule¼ 1018 joules¼ 0.95� 1018 BTUs¼ 0.95 quads)) of the world’s primary energy by 2050 [52],whereas the AR4 report of the Intergovernmental Panel on Climate Change [13]suggested that the global bioenergy potential could be as high as 500 EJ year�1.Currently, however, the total global biomass harvest for food, feed, fiber, woodproducts, and traditional wood used for cooking and heat amounts to approxi-mately 12 billion tons of dry matter of plant material per year with a chemicalenergy value of about 230 EJ [35,50,53].Experience shows that bioenergy policies in one region can have impacts not only

on its own but also on another region’s social, economic, and ecologicalsustainability [35,53]. Modernized bioenergy agroecosystems will be importantcontributors to the sustainability of future bioenergy agroecosystems, whereasbiomass derived from bioenergy crops will play an important role in global climatechange mitigation and will increase the share of renewable energy sourcesworldwide [7,54]. Using bioenergy crops as biological systems to store C andreduce GHG emissions is a potential mitigation approach for which equityconsiderations are complex and contentious [1,26,55–61]. The development anduse of biofuels as energy carriers that store energy derived from biomass is anotherbiology-based mitigation approach [37,62–64]. Nevertheless, positive impacts onecosystem services will be more important when second-generation dedicatedbioenergy crops are deployed on a large scale in the landscape [31,32,65–67].Bioenergy crops need to be grown within the context of sustainable agroecosys-

tems, in which provisioning, supporting, and regulating ecosystem services,including bioenergy and food, can be sustainably produced [68–70]. The impact ofbiofuels on food production, availability, and prices remains the subject ofconsiderable debate, as does their potential to contribute to energy security, globalclimate change mitigation through GHG emissions, and agricultural development[66,71,72]. The amount of biofuel that can be produced globally in an environmen-tally responsible and economically sustainable way is limited, and the need foradditional land resources provides one of the major constraints [29,73–77]. Thegrand challenge for biomass production is to develop crops with a suite of desirablephysical and chemical traits while increasing biomass production by a factor of 2 ormore [24,27,28,78–80]. Conventional grain and oilseed crops and crop residues,

14.1 Introduction 347

perennial herbaceous and woody crops, perennial oilseed crops, halophytes, andalgae, among others, are candidate bioenergy crops that can sequester C and areexpected to combat global climate change [81– 83]. Germplasm and geneticresource databases (e.g., Genetic Resources Information Network (GRIN); www.ars-grin.gov) include detailed information on wild and semi-domesticated peren-nial grasses [34,84–89] and woody plant species that can produce starch [90–94], oil[95–104], and lignocellulose [105–110]. These genetic resources are readily availablefor plant breeders and others to select, breed, genetically modify, and developenvironmentally friendly bioenergy crops from. A large number of potentialbioenergy crops are being evaluated for their growth rate, tolerance to biotic andabiotic stresses, and low requirements for biological, chemical, or physicalpretreatments [60,90,92,110–117]. Currently, bioenergy agroecosystems based ontraditional sources and first-generation crops are not sustainable, and theirexploitation may contribute to environmental degradation. New genetic resourcesare being developed through selection, screening, and breeding [118–122], andtechnological breakthroughs are being employed [123–126] to develop dedicatedbiofuel crops with better GHG profiles and with a suite of eco-physiological traits tomaximize radiation interception, water-use efficiency (WUE) and N-use efficiency(NUE), improved lignocellulosic accessibility to enzymatic degradation, and toconfer environmental sustainability.The bioenergy sector is strongly expanding, and thus likely to affect all other

sectors of national and world economies [8,31,127–131]. Reduction in GHGemissions, increase in energy security, promotion of rural development, andincrease in export revenues, especially in developing countries [20,22,40,49,128–134], are some of the positive objectives behind bioenergy production[25,30,35,135,136]. Nevertheless, correctly addressing the C implications ofbioenergy is critical because a large number of studies and policies plan on usingvery large quantities of biomass assuming that bioenergy is an almost C-neutralreplacement for fossil fuels [52,137–143]. Therefore, a critical review assessing thestate of the knowledge, and exploring the opportunities and challenges of the roleof C in bioenergy crops in mitigating global climate change, while sustainablyproviding other ecosystem services, is very relevant and timely.

14.2

The Many Faces of Carbon

From coal, charcoal, soot, and graphite to diamonds, C plays a major role in humanlife and in many ecosystem services [144–146]. A tetrahedrally, 4-fold coordinatedatom, the element and its isotopes have diverse chemical characteristics andactivities. In the vast majority of its compounds, C is a tetravalent element.Recently, however, higher coordination numbers have been found. Although afairly inert element and most of its modifications may only be reacted under harshconditions, C is the central element in organic chemistry, with many ways ofbonding with itself. Carbon, due to its medium position in the periodic table, reacts


http://www.ars-grin.gov

http://www.ars-grin.gov

with oxygen (O) as well as with hydrogen (H) and may adopt any oxidation numberfrom extreme positive (þ4 in CO2) to extreme negative (�4 in CH4).Carbon is exchanged among the biosphere, pedosphere, lithosphere, hydro-

sphere, and atmosphere on Earth, in various forms. Carbon can take differentforms, from a simple element to its compounds such as CO2, carbohydrate,limestone, and carbonate ions because it circulates throughout nature [22,146]. Asthe fundamental building block of life, C cycles continuously through theatmosphere, oceans, plants, animals, soils, and rocks. The main atmospheric formof C, besides its central role as input in photosynthesis, CO2 is an important GHG.Organic C compounds are important contributors to the beneficial chemical andphysical properties of soils, and are critical to their productivity [147,148]. TheEarth’s biosphere contains some 2000 Pg of organic C, about 75% of which residesin soils and 25% in plants [13]. Mainly driven by the photosynthesis activity ofplants, C continuously cycles through soils with losses via oxidation (mainlyrespiration), leaching, and physical erosion [10,34,92,149,150]. It is now recognizedthat the loss of soil organic C generally means an increase in atmospheric CO2.Similarly, an increase in soil organic C generally means a decrease in the amount ofC in the atmospheric pool of CO2; however, C stocks under different land usesdiffer substantially [44,73,151,152].

14.2.1

Carbon: A Scarce Commodity

Carbon, a terrestrial element, was described recently as a “scarce” element. It ismostly found in a form other than the pure form. It is the 17th most frequent(180 ppm) element, with silicon (Si) as the second-most frequent element, which isabout 1300 times as abundant. Nevertheless, C is essential for the assembly of allorganic matter [22,147,153–155]. The amount of C in soils represents about 80% ofthe C found in terrestrial ecosystems on Earth. The amount of C found in livingplants and animals is comparatively small (560 Gt) relative to that found in soil(2500 Gt). Soil C, either organic C (1550 Gt) or inorganic C (950 Gt), isapproximately 3.1 times larger than the atmospheric C pool (800 Gt) [156]; however,the oceans have the largest C pool, at about 38 400 Gt, mostly inorganic C. Currentestimates [53] indicate that C inputs from photosynthesis by terrestrial vegetationfix more C than C loss through soil respiration, resulting in a potential soil storagerate of around 3.0 Gt C year�1.Carbon as part of GHGs is a negative environmental externality; its “commodi-

fication,” as part of the Kyoto Protocol, rendered it a “scarce” and therefore tradableunit that can be transferred or sold not necessarily as a physical GHG, but totrading in the right to emit GHGs [134,157] or through the Clean DevelopmentMechanism, which is a mechanism for project-based emission reduction activitiesin developing countries. Therefore, for this “previously free commodity,” permis-sion to “pollute” gave it a new value as a private asset and at the same time gave itexchange value due to its “scarcity.” Due to its increasingly central role in socialmetabolism [19–21,133], and perceived “scarcity,” C may become the world’s

14.2 The Many Faces of Carbon 349

biggest commodity market and it could become the world’s largest market overall[84,158]. Soil and biomass-based C “engineering” are creating new opportunities todevelop attractive value-added C management technologies [23].The C footprint, expressed as kg CO2eq ha

�1 year�1, is a measure of the exclusivetotal amount of CO2 emissions directly and indirectly caused by an activity oraccumulated over the lifecycle of a product [36,91,145,159]. It is quantified usingseveral indicators such as the global warming potential, which represents thequantities of GHGs that contribute to global warming and global climate change[1,4,145,160]. When estimating the C footprint of biofuel crops, the impacts ofagroecosystems on environmental variables in the upstream and downstreamprocesses need to be considered [145]. Improvements in C quality, quantified by thecomposition and structure of biochemicals in bioenergy crops, will optimizeenergy production and will improve its calorific value, GHG profile, and globalclimate change mitigation potential [48,106,161–163]. In general, the proximity ofbiomass source and C sink greatly reduces the energy and emission footprint of aprocess or a product [155]. Carbon, ecological, and water footprints, forming a“footprint family,” are interrelated [36,145,159,164,165]. Carbon and N are the twodominant elements affecting biota and soils; their significance is magnified bytheir incorporation in three major GHGs: CO2, CH4, and N2O [166,167]. Incontrast to other important elements (e.g., phosphorous (P) and potassium (K)), thesupply of N and C is not limited, but energy is required to make them available asplant nutrients.

14.2.2

Carbon and Nitrogen Cycles

The global cycles of C and N have been dramatically altered as a result ofanthropogenic activities. An average of about 9 Pg C was added to the atmosphereeach year since 2000, largely through fossil fuel combustion and biomass burning[45]. Similarly, the N cycle is being altered through industrial and agriculturalactivities with large amounts of non-reactive N2 being converted to reactive N (e.g.,NO3) and redistributed, through several processes, among terrestrial, freshwater,and marine ecosystems [168]. Species and genotypic variation in plant traitsaffecting above-ground biomass production, below-ground C allocation, and plantN cycling determines, to a large extent, the C: N ratio [22,129,150,164] and controlssoil C sequestration [37,69,167]. The global cycles of C and N are intrinsicallycoupled through numerous biogeochemical processes. The relative proportion of Cand N (i.e., C: N ratio) is a significant controlling factor of the rate of organic matterdecomposition; therefore, N limitations can constrain C accumulation in terrestrialecosystems due to a slower cycling of nutrients [10–12,36,129,166–169]. However,plasticity of the C: N ratio in plant tissues of various biofuel crop species canbe manipulated to affect a substantial increase in C storage as a result oflarger C: N ratios [22,129,150,164], whereas disturbance of (semi)-naturalecosystems (e.g., grasslands) through land-use change to grow bioenergy cropscan have a considerable impact on biogeochemical cycles [11,83,169,170], and


may accelerate both soil C and N cycles, especially at the establishment phase[92]. Nevertheless, C and N cycling, as ecosystem services, can be decoupledand valued separately [84]; the transitions of C and N among solid, liquid, andgaseous phases, and among different chemical compounds and chemicalstates, can be explored [152].Carbon uptake by terrestrial ecosystems plays an important role in defining

changes in atmospheric [CO2] and changes in climate, whereas changes in land useaffect the cycling and storage of C in ecosystems. The sensitivity of soil C pools toglobal warming is a big uncertainty in the C cycle, and the flux of recently fixed Cfrom plant to soil is one of the least understood and poorly quantified parts of the Ccycle [34]. However, the magnitude of change in C storage depends on howphysical, chemical, or biological processes are altered over time under differentland-use systems [73]. The terrestrial C sink is expected to decline with increasedglobal warming as the CO2 fertilizing effect loses out to increased C loss due toplant and soil respiration; however, the magnitude, intensity, and timescale ofchanges in the soil C pools are unclear [27].The biomass-derived C cycle, unlike the petrochemical C cycle, is nearly balanced

[171]. However, crop and soil management practices have implications for Ccycling in soils [127]. Therefore, understanding the processes controlling C fluxesbetween plant roots, microbial biomass, soil, and the atmosphere is important forpredicting the C cycle and managing C sequestration in soils [34]. In addition,climate variables (e.g., temperature) are known to influence plant physiology (e.g.,sugarcane) and modify C allocation in biofuel crop plants through effects on leafarea index [172].Although interdependent, the C and N cycles vary according to the type of biofuel

crop [22,152,164,168,169]. Several interacting biological and physiographic factors,such as precipitation, temperature, topography, soil characteristics, presence andactivities of soil microbes and invertebrates, and land management, drive bothcycles [48]. Consequently, the C and N cycles can be significantly affected bychanges in any of these factors, and these changes may mitigate or exacerbateGHG concentrations and global warming [1,3,4]. There is a functional relationbetween crop N content and CO2 uptake from the atmosphere [12,169,173].Increased fertilizer use for biofuel production will accelerate the N cycle, and mayresult in N losses to the environment and additional emissions of reactive N[12,166]; however, greater GHG mitigation potential can be achieved if perennialand rhizomatous crops (e.g.,Miscanthus) with unique N and C cycling are deployedfor biofuel production [11]. On the other hand, increases in N availability lead toincreases in C storage, especially in temperate and boreal ecosystems where lack ofN may limit C storage [174–176]. Indirect effects of increased fossil fuel use andland-use change on the N cycle may lead to increased CO2, CH4, and N2O contentin the atmosphere, with reactive N being deposited mostly in groundwater,vegetation, and soils of terrestrial ecosystems [129,166]. Therefore, knowledge ofland-use history is essential to the understanding and manipulation of N-stimulated C storage [22,129,168], and to quantify and evaluate the impact ofbioenergy crops in a CO2-constrained world [146].

14.2 The Many Faces of Carbon 351

14.3

Are Bioenergy Crops Carbon-Neutral?

Biomass, as a renewable energy source, has been advocated by policy makers as ameans of combating anthropogenic global climate change [146] and was viewed fora long time as “C-neutral” – its use as an energy source was presumed not torelease net CO2 to the environment [1,13,138]. However, the assumption of C-neutrality has recently been challenged, using life cycle analysis, and energetic andglobal warming potential guidelines [177], under several environmental, manage-ment, and soil conditions [10,177,178], and based on modeling and simulationstudies [179]. A group of scientists publically questioned the treatment by US policymakers of all biomass energy as C-neutral, arguing that it could underminelegislative emissions reduction goals [138]; further, they argued that “an approachfocused on smokestack emissions, independent of the feedstocks, would encouragefurther fossil fuel energy production, to the long-term detriment of the atmo-sphere.”Although biofuels have the potential to be C-neutral or even C-negative on

ecological timescales [180], a clear distinction should be made between C-neutralityand climate-neutrality [10]. While the assumption of C-neutrality may be reason-able when the bioenergy product is derived from fast-growing biomass feedstockssuch as annual crops [90,92,114,181], it becomes questionable for bioenergyderived from slow-growing feedstocks [106,182–185]. As for climate-neutrality, thebioenergy agroecosystem may require several decades to be C-neutral and theequivalency of both neutrality concepts may not be valid [10]. For bioenergyagroecosystems involving C-based energy vectors (e.g., ethanol or biodiesel) to beenvironmentally effective, their design must be consistent with ecological rules ofC circulation in nature [45,89,186–188] and when integrated with a value-added Cmanagement strategy [23,75], or included in a biorefinery, they can become C-neutral or even C-negative [49,180].The motivating fundamental of C-neutrality was based on the fact that the

atmosphere is the origin and final destination of captured and omitted CO2 frombiofuels [177]. However, biofuels are not strictly C-neutral, and the C emissionsfrom biofuel chains can vary significantly depending on the biomass feedstock,management practices, land-use change and history, conversion technologies, andrelated materials and fuel inputs [189]. Emissions of CO2, N2O, and CH4 duringcrop production may reduce or completely counterbalance CO2 savings of thesubstituted fossil fuels and therefore impact C-neutrality [49]; also, land conversionto biomass production entails additional CO2 emission through soil organic Closses, which may offset C-neutrality as well [177,178]. For the combined objectivesof energy independence, combating global climate change, and achieving C-neutrality, extensive use of biofuel crops may increase net global warming due toincreased emissions of N2O from additional N fertilizers [12,166,190] andincreased C flux from soils due to land-use change [170,191].The time-lag between biogenic CO2 emissions and capture through regrowth of

bioenergy crops would result in a certain climate impact, even for biofuel


agroecosystems that are long-term C-neutral [1,179]. The temporal factor of time-lag between CO2 emissions to, and removal from, the atmosphere generally followsthe standard conventions of life cycle analysis and zero discount rate [179] inevaluating GHG balances of bioenergy crops, thus ignoring the time-to-atmo-spheric decay, global warming potential, and C-neutrality [1,13,138]. The short- andlong-term C footprints of biomass emissions on the biosphere will likely bedifferent [138]. Permanently sequestered C contributes to lowering atmospheric[CO2], whereas temporarily stored C can be beneficial only in reducing climateimpacts caused by cumulative CO2 [179]. Therefore, as measured by globalwarming potential, when grown in crop rotations with long duration they exertlarger environmental impact than when grown in short crop rotations; however,the latter have less climate impact per unit of CO2 emitted from biofuels than theformer. Nevertheless, and based on the C-neutrality assumption, for example, morethan 50 times the current global production of ethanol would be required to achievea very small portion of emissions reductions and an average growth rate in biofuelproduction of 8% would be required over the next 50 years to achieve that objective.On one end of the “C-neutrality” spectrum are bioenergy agroecosystems based

on first-generation crops [57,66,192–196], where C-neutrality, although question-able [143], may be achieved on a short-term basis. No differences in biogeochemicalliabilities can be demarcated for first-generation crops whether grown forbioenergy or for grain production, such as corn (Zea mays L.) and soybean (Glycinemax); both are characterized by excessive NO3 leakage, soil C and P loss, and CO2

and N2O emissions [146]. The first-generation bioenergy crops are not optimizedfor low C footprints [36,145,159]. Although C emitted during fuel combustion isbalanced by C fixed by photosynthesis, bioenergy is not necessarily C-neutralbecause of GHG emissions released during crop growth, field management,feedstock processing, and transport [49].On the other hand, not all perennial bioenergy crops are C-neutral, although they

emit less N2O than first-generation bioenergy crops because they usually do notrequire N fertilizer [58] and fewer inputs [79,197]. At the other end of the C-neutrality spectrum are bioenergy agroecosystems based on microalgae, which areconsidered C-neutral. Microalgal bioenergy systems, currently operated on a small-scale or laboratory basis [198], have a higher photon conversion efficiency thanbioenergy crops, can be harvested batch-wise nearly all year round, can couple C-neutral biofuel production with CO2 sequestration, and produce non-toxic andhighly biodegradable biofuels. Consequently, these as-yet experimental systemshave small C, N, water, and environmental footprints [36,159]. Between these twoextremes are bioenergy agroecosystems based on lignocellulosic biomass fromthird-generation or dedicated biofuel crops (e.g., Miscanthus and short-rotationcoppice), which are potentially C-neutral sources of bioenergy that do not contributeto increased atmospheric [CO2] [105]; short-rotation coppice crops, for example,produce 11–16 units of usable energy per unit of non-renewable fossil fuel energyused to grow, harvest, and deliver the biofuel [175]. These crops can providesignificant amounts of environmentally friendly bioenergy [105] and when convertedto ethanol, it may avoid between 86% and 113% of GHG emissions if “E85” is used

14.3 Are Bioenergy Crops Carbon-Neutral? 353

in flexifuel vehicles instead of gasoline [11,57]. The “energy return on investment”[108], which represents the amount of net new energy produced by these bioenergycrops, is positive and provides a rough estimate of their C-neutrality.

14.4

Recalcitrant Carbon in Bioenergy Crops

Bioenergy agroecosystems are sinks and sources of GHGs; their potential role inmitigating global climate change depends on a dual strategy of decreasing GHGemissions while increasing sinks so that the net impact on global warmingpotential is less than at present [1,4,199]. Reductions in GHG emissions can beachieved by decreasing heterotrophic conversion of organic C to CO2, and byminimizing the release of CH4 and N2O [48,58,143,200–203]. Biomass and soilorganic matter, in addition to oxidized CH4 by soil bacteria, comprise major Csinks. These sinks can be enhanced by increasing net primary productivity (whichcharacterizes the gross terrestrial C sink), thereby actively reducing atmospheric[CO2] [27,200], and by promoting more oxidation of CH4 [10,176,200]. Additionally,judicious biochar management, as part of a comprehensive C management schemefor bioenergy production, will contribute to this objective [155,204].Accumulation in, and release of, C from the different pools takes place at

different timescales [41], and GHGs are not released as a single pulse after beingstored in the biosphere or in the anthroposphere [179]. Therefore, the time-lagbetween emissions and capture of biogenic CO2 through re-growth of bioenergycrops results in a certain climate impact, even for a bioenergy agroecosystem that isC-neutral over time [179]. Consequently, the benefits of temporary C loss dependon the time horizon adopted when assessing global climate change impacts and aretherefore not purely science-based, but may include value judgment [36].Different components of soil organic C differ substantially in their residence

time in soil [147,148]. Generally, organic C is stored in three different pools: above-ground biomass, litter, and soil, including root biomass. When changing land use,these storage pools can change until a new equilibrium is reached (approximatelyafter around 20 years depending on many factors) and atmospheric CO2 is nolonger sequestered in soil organic matter. Even relatively small changes in theirsizes can impact GHG balance. The potential to sequester C in soil is very site-specific and highly dependent on many factors, including climate, soil character-istics, number and sequence of bioenergy crops in rotation, and former andcurrent management practices, among others [85,205].Recalcitrance and, consequently, the rate of turnover of soil organic C

components is determined by chemical structure [99], environmental conditions,and accessibility to microbial and other biological factors in the soil [206]. Soil Cwill decrease if soil is exposed to accelerated oxidation or erosion, or if the input oforganic matter is reduced [99]. A critical management problem in bioenergytechnologies addressing C sequestration is the recalcitrance or permanence ofdeposited C in soil [23]. This state can be achieved when biomass-derived C is


biomineralized, (i.e., reacted into a more stable, non-degradable form bymicroorganisms) or by plant species that can biomineralize atmospheric CO2

directly [155,207]. Biochar, a product of pyrolysis [155], increases C and soil organicmatter stability as a result of its slow mineralization when compared with soilorganic matter. However, the amount of C-negative bioenergy generated frombiofuel crops through pyrolysis is reduced; some energy cannot be recovered fromthe biomass feedstock and remains in the biochar.Different global climate change mitigation results are achieved by different C

storage strategies in the biosphere [156,208,209]. Whether temporary C storage inbiosphere sinks can mitigate global climate change impacts or can only reducethose impacts related to the cumulative effect of high temperature is a subject ofcontinued scientific [168,208] and management debate [36,60,210]. Defined as Cthat is stored in the biosphere for a few years and then released before the onset ofserious global climate change impacts, temporary C storage could worsen the directimpact of high temperature or impacts caused by the rate of change of temperature[208]; its benefits are more or less linearly related to its storage time in soil [36,156].The efficient global climate change mitigating potential of temporary stored-C maynot be realized in less than 50 years of storage [168,210]. Therefore, it may not bereasonable to provide incentives for temporary C storage; however, to achievemeaningful global climate change mitigation, C accounting rules for biospheresinks need to be specifically formulated so that long-term storage of C stocksare assured before incentives can be provided and credits can be issued tobioenergy farmers and producers [60,157,211].Permanent C storage, as recalcitrant C, can lower atmospheric [CO2] considerably

and contribute to long-term global climate change mitigation [37,63]. The cycling,storage, and level of C recalcitrance in biofuel agroecosystems are affected by land-usechange, the magnitude of which depends on how physical, chemical, and biologicalprocesses are altered over time under different land-use options [73]. However,redirecting net primary productivity within a bioenergy production agroecosystem torecalcitrant C pools with long turnover times can be achieved if non-living organicmatter is protected from decomposition, oxidation, or burning [44,148,206],deforestation rates are reduced, and short-rotation woody crops and short-rotationcoppice harvest age is increased [83,168,181]. However, long-term effects of increasedatmospheric [CO2] on C storage in bioenergy agroecosystems are still a subject ofscientific debate. Water [24,212–215] and nutrient [82,135,210,216] availability may, inthe long-term, limit the effect of enhanced [CO2] on the agroecosystem C uptake. Onthe other hand, the sustainability of increased [CO2] beneficial “fertilizing” effectdepends partly on whether bioenergy crop plants acclimate to the higher CO2 levels.

14.5

Climate Change Mitigation Potential of Bioenergy Crops

If most soils are below their ecological potential C content [23], then shiftingatmospheric CO2 to these soils is technically feasible as a means of global climate

14.5 Climate Change Mitigation Potential of Bioenergy Crops 355

change mitigation. On average, the rate of C sequestration ranges from negative orzero under arid and hot climates to around 1Mg C ha�1 year�1 under humid andtemperate climates [211]. Management practices, soil conditions, bioenergy crops,and climate variables determine, to a large extent, the soil C sequestration rate andconsequently its global climate change mitigation potential. Long-term C seques-tration, which is the net difference between C input to and C output from the soil,has received much attention recently as a potential management-induced globalclimate change mitigation strategy [37,41,63,216]. The potential of using bioenergycrops to replace fossil fuels and help mitigate global climate change by providingrenewable, low-C energy has been recognized by governments in the developed aswell as the developing world. Many countries already have renewable energystrategies that pose challenging targets for biofuel production [110]. As a potentiallow-C energy source, biofuels may offer C savings and global climate changemitigation, but this depends, among other factors, on how and where they areproduced [217]. Also, appropriation or redirection of net primary productivity [53](in this context it indicates biosphere potential to supply primary food energysource for non-autotrophic species including humans) and the protection ofalready sequestered C would be additional effective global climate changemitigation strategies, especially when planning land use [41,44,173,216,218] orland-use change [73,151,152,219].Using the respective estimates of 1500 and 720 Pg for C contained in soil and

atmosphere [55], and the current 400 ppm for atmospheric [CO2], a 1% change inthe amount of C sequestered in soils would equate to a change of approximately8 ppm in atmospheric [CO2], provided all other components of the C cycleremained constant. If, for the sake of argument, 750 Mha of land are availableworldwide for bioenergy crops and a total biomass of approximately 1.6Gt year�1

can be produced, then a net 4.4� 10�9Gt C ha�1 year�1 can be sequestration frombioenergy crops, especially if diversified agroecosystems are established oneconomically marginal land [220]. However, given the current and future limitedland area that is available for bioenergy production, the contribution of bioenergycrops to global climate change mitigation is likely to remain small (less than 10% ofglobal energy supply in 2050) for the foreseeable future [49]. Nevertheless, globalclimate change mitigation potential should not be equated with sustainability ofbiofuel production [48,221,222]; the latter depends on ecological processes thatmaintain high-yielding crops with low GHG emissions [11,71,135].A proliferation of studies, advocating or opposing biomass-for-bioenergy in an

effort to mitigate global climate change, covers a wide range of bioenergy crops,production strategies, and conversion technologies. The bioenergy literature isreplete with a wide range of positive and negative results and recommendations[28]. For example, bioenergy derived from biomass (6.5� 1010Mt year�1) and cropresidues (714.7� 106 t) in China could account for 10% and 16% of national energysupply in 2010 and 2020, respectively. The biofuels produced from these feedstocksare expected to reduce GHG emissions of SO2 (54% of national emissions in 2003),NOx, and CO2 (30% of emissions in 2003) [223]. On the other hand, studiesconducted in Europe and the United States reported GHG improvements (over


fossil fuels) of biofuels derived from first-generation crops ranging from �35% to65% for sugar beet, from �55% to 85% for rapeseed, and from �40% to 78% forsoybean; whereas positive values (40 –70%) were reported for oil palm (Elaeisguineensis ) in Malaysia and Indonesia [20,95] and sugarcane (85–100%) in Brazil[31,154,224] as compared with 67– 115% for lignocellulosic ethanol and 60 –115%for biodiesel from a number of second-generation crops [77,225].The global warming potentials of the most important GHGs are already

established (http://www.eccarbon.com) with CO2 assigned 1.0 global warmingpotential unit as the reference GHG against which others are measured, and CH4

and N2O assigned 21.0 and 310.0 units, respectively; their residence times in theatmosphere range from 12 years for CH4 to 100 and 114 years for CO2 and N2O,respectively. The time-lag between the immediate release of CO2 from using fossilfuels and its eventual uptake by biomass, which can take many years [226], isusually overlooked when considering the use of biofuels for global climate changemitigation. Although a plethora of agronomic information is available on manyfirst- and second-generation crops and their biofuel characteristics (e.g., corn,sugarcane, and rapeseed), the information on their global warming potential,environmental impact, and global climate change mitigation potential is contra-dictory or incomplete, and highlights major gaps in our knowledge that need to beaddressed before a truly quantitative assessment of the global climate changemitigation potential of these and other bioenergy crops can be made [29].The timescale at which C is sequestered plays a major role in whether

management practices contribute to global climate change mitigation[27,28,227,228]. If we accept 50 years as the minimum time for C mitigationpotential to be realized through terrestrial C storage or sequestration [228], then wemay be faced with uncertainty about the GHG mitigation potential of mostbiofuels. For that reason, biofuels derived from first-generation crops andassociated convergent technologies may have negligible effect on GHG mitigation[35]; since the average residence time of their biogenic CO2 in the atmosphere isrelatively short, it is assumed that their global warming potential is small ascompared with perennial bioenergy crops. However, crop diversification androtations can lead to increased opportunities for global climate change mitigationthrough C sequestration. The longer the rotation period, the larger may become theclimate impact of bioenergy crops; this only means that short-rotations have lessclimate impact than longer rotations per unit of CO2 emitted from biofuelcombustion.Perennial bioenergy crops, whether second-generation, third-generation, or

dedicated biofuel crops, may have higher global climate change mitigationpotentials when their productivity, “time-to-harvest,” and productive lifespan areconsidered. The dedicated biofuel crops can enhance and maintain soil structureand function due to their agronomic, physiological, and structural characteristics,therefore they have greater global climate change adaptation and mitigationpotential than first-generation crops [147,211]. For example, short-rotation coppiceplantations could store 1.25Mg C ha�1 year�1 in above-ground biomass andsequester up to 0.9Mg C ha�1 year�1 [229], short-rotation woody crops up to


http://www.eccarbon.com

13.0Mg C ha�1 year�1 as net energy potential [73], and perennial grasses sequesterup to 1.1Mg C ha�1 year�1 [85], whereas the direct use of existing crop reserveprogram grasslands for cellulosic feedstock production would avoid C debt entirely,and provide modest and immediate global climate change mitigation [87]. GreaterGHG mitigation potential of a bioenergy crop can be attributed, among otherfactors, to more efficient C and N cycling [11]; however, the efficiency of Csequestration is reduced when C and N are not adequately balanced [211]. Changesin agroecosystems in response to global climate change will alter C and N flowsresulting from changes in crops, residue amounts and qualities, and mineraliza-tion of organic matter; therefore, GHG emissions could be reduced more efficientlyby managing C and N simultaneously [82,230].

14.5.1

Biomass versus Bioenergy Density

Biomass was exploited, for millennia, as a source of bioenergy using simple andsophisticated conversion technologies, such as direct burning, anaerobic digestion,combustion, gasification, fermentation, esterification, and pyrolysis[23,103,195,204,221,231–235]. Energetically, plants differ in their biochemicalcomposition and in the amount of glucose to produce a unit of organic compounds[78,231,236]. Their calorific value is a measure of their energy content. The majorchemical macromolecules differ in their energy content (MJ kg�1, dry mass basis);it is low for sugars, starch, cellulose and hemicelluloses (14–16), and vegetativebiomass (17), and intermediate (25) for proteins and lignin as compared with thehigh value (38–40) for lipids. The higher content of low-molecular-weightunpolymerized carbohydrates in biomass is a valuable trait; when used forfermentation, the higher the content of these carbohydrates, the lower the energyinputs in the biofuel refining process and the better the GHG profiles of theproduced biofuel. Compared with most fossil fuels, the energy density of biomassis relatively low (10–40%). However, this drawback can be overcome by densifica-tion procedures, which render biomass a better energy source [237]. Biomass yield,energy content, and energy availability from bioenergy crop plants are influencedby biomass composition. Besides their effect on energy yield, biomass yield andcomposition affect GHG profiles and global climate change mitigation potential ofbioenergy crops [78,234]. For example [83,238], hybrid poplar, switchgrass, and reedcanary grass produced 6.15, 5.8, and 4.9MJm�2 year�1, respectively, as energyyield; however, reed canary grass had the largest net GHG emission ratio of 3.65, ascompared with switchgrass (2.42) and hybrid poplar (2.37).Energy retained by plants is not proportional to accumulated biomass due to

large differences in chemical composition between and within bioenergy cropspecies and throughout plant ontogeny [239]. Generally, the higher heating value asan indicator of energetic value of biomass on a dry weight basis ranges from 14 to23MJ kg�1 [181]; it was estimate [240] at 23.2–25.6 3MJ kg�1 for lignin,18.6 3MJ kg�1 for cellulose and hemicelluloses, 17.1 3MJ kg�1 for corn cobs, 17.483MJ kg�1 for corn stover, and 18.27 3MJ kg�1 for wheat straw. Energetic value,


calorific content, and environmental impact of biomass depend on the chemicaland physical properties of its macromolecules; the gross energy content of biofuelproduced per unit land area determines its global warming potential and globalclimate change mitigation potential. Speci fic energy density (MJ kg�1) of severalbioenergy carriers including chaff/stover 14.6, dry biomass yield 10– 16, wood 16 –21, charcoal 30, ethanol 23.5 –26.8, methanol 20 –22.5, butanol 36, fat 37.8,sunflower oil 40, biodiesel 37.8, CH4 55, and crude oil 41.9, as well as biofuel yield(l ha �1) of common crops associated with biofuel production for bioenergy cropssuch as corn 172, oats 217, Calendula 305, hemp 363, cotton 325, soybean 446, flax478, Camelina 583, saf flower 779, sunflower 952, castor bean 1413, rapeseed 1190,Jojoba 1818, Jatropha 1892, Chinese tallow 4700, oil palm 5950, and algae around95 000, can be found at the Oak Ridge National Laboratory Web site: https://bioenergy.ornl/papers/misc/energy_conv.html/.Although energy content of biomass (on dry, ash-free basis) is relatively similar (17–

21MJkg�1) for most bioenergy crops [30,94,126], existing differences between andwithin bioenergy crop species in biomass and energy yield are attributed to differencesin feedstock characteristics and production environments [20,47,111,241–244]. Netenergy value is mainly affected by the productivity of the bioenergy crop; values rangingfrom �2.89 to 4.88MJ l�1 of ethanol produced from dryland corn and from 3.68 to6.85MJ l�1 under irrigation illustrate the magnitude of these differences.Differences between bioenergy crops in energy output, expressed as ethanol

yield, can be attributed in part to quantitative and qualitative differences incarbohydrate content [245,246] which ranges from 94% in sugar beet to 70–76% inwheat and corn grain, 67% in softwood, and 66% in hardwood. The primary netenergy yield (GJ ha�1 year�1) of a number of second-generation crops (with no Napplication), including bioenergy corn (294), willow (257), Miscanthus (224), andswitchgrass (140), are variable and large as compared to those of first-generationcrops, such as grain and straw of winter oilseed rape, winter wheat, and wintertriticale (around 118); however, primary net energy can be improved by 2–100%with N fertilizer application [12,22,152,164,169,173,190]. Similarly, net energyratios (output/input) are equally variable among crops that produce ethanol orbiodiesel and also differ between and within bioenergy crops.Most net energy ratio estimates for first-generation crops such as sugar beet (1.2–

2.2), wheat (1.2–4.2), corn (1.2–1.8), soybean (1.4–3.4), and rapeseed (1.2–3.6) aresmall in comparison with net energy ratio for second-generation biofuel crops suchas sugarcane (2.2–8.4) and oil palm (8.6–9.6) [203]. Cellulosic second-generationcrops have a higher biofuel yield and lower GHG emissions per hectare, and have agreater reduction in GHG emissions per unit biofuel produced than first-generation crops. As a result, they produce greater reductions in GHG emissionsassociated with fossil fuels and better GHG profiles [11,49,52,59,144,159,207,247],which can be demonstrated by percent of CO2 released for the corresponding fossilfuel (i.e., CO2 profile). For example ethanol produced from first-generation crops,such as corn, wheat and sugar beet has CO2 profiles of 90%, 60%, and 30–70%,respectively; whereas ethanol produced in Brazil has a value of 15%. On the otherhand, biodiesel produced from rapeseed and soybean has CO2 profiles of 40–80%


https://bioenergy.ornl/papers/misc/energy_conv.html/

https://bioenergy.ornl/papers/misc/energy_conv.html/

and 25–60%, respectively, as compared with ethanol produced from cellulosicfeedstocks of second-generation crops (12–25%) or biomass-to-liquid biodiesel(15%). Conversion efficiency (compared to 100% for fossil fuel) depends largely onbiomass type and conversion technology. Relatively high conversion efficiencieshave been reported for oil from oil crops (88%) and oil from algae (80%) using oil-to-fuel conversion technology. A much smaller value was reported for lignocellu-loses (39%) compared to 80% for starch or sugar using fermentation. Biomasspelleting upgrades its physical and chemical properties, and calorific value. Inaddition to the environmental advantages, pelleted biomass has higher bulkdensity, increased energy density, and higher heating value [44,165].

14.5.2

Temporal Changes of Carbon in the Soil---Bioenergy Crops---Atmosphere Continuum

Differences in chemical composition during plant ontogeny may be caused, in part,by temporal changes of C and in response to its cycling within the soil–crop–atmosphere continuum [239], both of which largely depend on photosynthesis uptakeof atmospheric CO2. The soil C pool is approximately 3.5, 4.5, and 22.7 times the sizeof the atmospheric, plant, and microbial biomass C pools, respectively. Almost all(99.9%) C present in the world’s biota is contributed by plant and microbial biomass.Annual fluxes of C between the atmosphere and land, and between the atmosphereand the oceans, are about 123 and 92 Gt, respectively. Therefore, 123 Gt represents Cuptake by photosynthesis, which can be described as the gross productivity potentialof the global terrestrial system [149,150,180,210,248–250]; around 50% of which isreturned to the atmosphere almost immediately through plant respiration. Theremaining amount is the net primary productivity; the human appropriation of whichis slightly over 50% [19]. Depending on the nature of its storage in the soil, this C hasthe potential to persist for decades, centuries, or millennia. In reality, however, mostof it is lost because of land use, land-use change, biotic stresses, fires, and otherdisturbances. It is debatable, if we can control what the plants do with C, the fate ofthe C in the atmosphere will be in human hands.Carbon circulates from one of its interconnected pools to another [23]; adverse

effects, however, are mainly associated with its irreversible flux into the atmosphereas CO2, where it is recently increasing at an alarming rate (around 2.2 ppm year�1).Therefore, the best C management strategy is to shift the anthropogenic C fluxback from the atmosphere (that currently has a relatively small C capacity of around770 Pg), preferably to a calcitrant form in the soil C pool. However, one of the leastunderstood and poorly quantified parts of temporal changes in the C cycle is theflux of recently fixed C from the plant to the soil via the rhizosphere – a sink thatreceives, on average, 5–21% of the fixed C [34]. Understanding the processcontrolling C fluxes in the plant root–microbial biomass–soil–atmosphere con-tinuum is important for predicting and managing C sequestration in soils.Temporal C dynamics, quantified by the amount of C stored in, and emitted or

removed from, a bioenergy agroecosystem depends, among other factors, on croptype, management practices, and soil and climate variables [18]. With increased


bioenergy plantations, changes in land use will continue to impact biogeochemical(and biogeophysical) cycles [172], with far-reaching impacts on both global C cycleand C budget [99]; the latter has changed significantly due to anthropogenicincreases in atmospheric [CO2]. However, a “reverse” land-use change from annualto perennial crops will help reduce overall annual GHG fluxes (around 3.8 t CO2eqha�1 yr�1). This reduction is largely brought about by decreased fertilizer use andincreased below-ground biomass C storage as soil organic C and soil organic matter[84]. In spite of its small percentage of total soil mass, soil organic matterconstitutes a large part of the global organic C stock; small but stable changes inthis stock could significantly impact global C fluxes [177]. Therefore, changes insoil organic C and soil organic matter are key factors in future bioenergyproduction; they will largely determine the long-term C balance of bioenergy crops[49]. Quantifying C sequestration in soil, unlike measuring its storage in above-ground biomass, is not an easy task. In particular, what constitutes the functionalpools of soil organic matter and the response of those spools to managementpractices remains poorly understood, especially in the context of perennialbioenergy crops such as short-rotation coppice plantations [168].Temporal changes in soil C are likely to occur because of land-use change

associated with bioenergy agroecosystems, both at the initial stages and throughouttheir life cycle. Accurate measurements of their impact on GHG fluxes and theireffectiveness in global climate change mitigation, estimated as Ceq [13,46], iscritical for C balance in these agroecosystems. If larger amounts of C are allocatedto above-ground structural C pools to maximize yield, then C sequestration will beadversely affected and may not reach optimum levels [24]. If soil C densities arehigh, such as in boreal forest [210] and peatland [19] ecosystems, slight temporalchanges in C uptake and release, let alone land-use change for bioenergyproduction, can have a substantial effect on the net soil–atmosphere C flux andglobal warming potential. Temporal changes in soil C and N storage in fast-growingperennials (e.g., hybrid poplar) can add an appreciable amount of C in the soil in arelatively short time. For example, hybrid poplar sequestered 24.4Mg C ha�1 moresoil C than adjacent soils under agricultural row crops after 15 years [168].However, spatio-temporal analyses of perennial crop biomass yield suggest that Cdynamics can be solely affected by climate variability; under optimum growth andproduction conditions, perennial bioenergy crops can combine the lowest biomassvariability and the highest biomass yield [251] – a characteristic that might renderthem highly competitive with food crops for prime land.

14.6

Carbon in Bioenergy Crops

The C footprint captures a large portion of overall environmental effects for manyproducts and services [145]. Expressed as kg CO2eq ha�1 year�1, besides its utilityas an environmental protection indicator, the C footprint differentiates betweendifferent GHGs [178], is negatively correlated with global warming potential, and

14.6 Carbon in Bioenergy Crops 361

reflects the level of social metabolism [22]. From a bioenergy agroecosystemsperspective, some quantitative estimates of the impacts of biofuels on environ-mental variables in the upstream and downstream processes need to be consideredwhen estimating their C footprint [145]. Data on current global bioenergy use areuncertain. Most researchers agree on a range of 14–60 EJ year�1, the vast majoritythereof being firewood, dung, or charcoal burned in simple cooking or heatingstoves, often creating heavy indoor pollution and with a large C footprint [43].Most, if not all, first-generation crops were not optimized for a low C footprint

[35,36,145,159]. Although C emitted during combustion is balanced by C fixed byphotosynthesis, bioenergy is not necessarily C-neutral because of GHG emissionsreleased during crop growth, field management, feedstock processing, andtransport. Microalgal bioenergy systems, as compared to other bioenergy agroeco-systems, have the smallest C footprint, along with small N, water, andenvironmental footprints [49]. In between these extremes, the second-generationcrops display intermediate values. The reduction in the emission of CO2eq thatresults from replacing fossil fuels with biofuels varies from 8.1 g MJ�1, calculatedas corn ethanol equivalent produced under conventional tillage corn–soybeanrotation, to 24 g MJ�1 for switchgrass and hybrid poplar [83,86,167,252]. If, in thenext around 50 years, perennial grasses and short-rotation woody crops dominatethe plant-based bioenergy crops, the decrease in net GHG emissions associatedwith bioenergy crops is expected to reach 25–30 g CO2eq MJ�1 ethanol [2,253] andtheir C footprint will be much lower than present values.Although second-generation crops account for only a small fraction of bioenergy

production (e.g., around 3% of the current European bioenergy production), theyemit 400% to 100% less N2O than first-generation crops [49] and may improve theglobal C balance in spite of land-use change [76]. Perennial bioenergy crops havethe potential to sequester additional C in soil biomass if established on formercropland at a rate of about 0.44 and 0.66Mg soil C ha�1 year�1 for short-rotationcoppice and Miscanthus, respectively [49,184,238,254,255]. The fast-growing short-rotation coppice plantations, for example, add an appreciable amount of C in thesoil. Hybrid poplar sequestered 24.4Mg C ha�1 more soil C than agricultural rowcrops after around 15 years [168]. Large reductions in the C footprint can beachieved by deploying hundreds of plant species that are known to directlybiomineralize atmospheric CO2 at low environmental cost [23]. Also, negative CO2

intensities and lower C footprints can be achieved when biomass-based energyagroecosystems are integrated with a value-added C management strategy [23].Soil- or biomass-based C engineering are creating new opportunities to developattractive value-added C management technologies that are cost-effective and canlead to significant GHG reduction [23].

14.6.1

Carbon in Traditional Bioenergy Plants

The total global biomass harvest for food, feed, fiber, wood products, and traditionalwood use for cooking and heat amounts to approximately 12 billion tons of dry


matter of plant material per year with a chemical energy value of 230 EJ [52].Biomass in the form of firewood has been used as an energy source since antiquity,and prior to the development of steam and internal combustion engines, much ofthe energy allocated to transportation was derived from plant-based sources in theform of animal feed [62]. However, the human demand for biomass and its socio-economic use have changed dramatically over time. Currently, biomass contributes10–14% of the world’s energy supply [29,239]; significant differences betweendeveloping countries or regions exist [19]. The most important type of bioenergyhas been and continues to be wood fuel, which represents approximately 15% oftotal primary energy consumption in the developing countries.Firewood is still being gathered as a biofuel, and trees are likely to be damaged by

exploitative, unregulated harvesting practices, resulting in wide-ranging detrimen-tal environmental and livelihood impacts in many parts of the developing world[82]. Even with the relative availability of fossil fuels, traditional biofuels remain themajor energy source in a number of countries (e.g., Bhutan 86%, Nepal 97%).Continued exploitation contributes to land degradation and desertification[7,71,204]. Energy from biomass has the largest impact on local communities inmany, if not all, parts of the world because of its direct effects on rural livelihoodand employment, food availability and accessibility, freshwater supply, socialexclusion, and lifestyle changes [35].The indigenous plants that are being exploited by traditional societies as

feedstocks for biofuels are either wild or semi-domesticated. Simple selection fromtheir gene pool would improve specific traits and properties that can enhance theirenergy output and its quality. Moreover, this will enhance the ability of theirproduction under managed agroecosystems, minimize the damage to andexploitation of natural ecosystems, and mitigate global climate change impact[103]. Agroforestry as a traditional land-use adaptation may potentially supportlivelihood improvement of traditional societies through simultaneous productionof food, fodder, and firewood as well as global climate change mitigation [175].Innovations in the domestication of useful species may strengthen the role ofagroforestry in developing countries [255]. Conventional bioenergy plants are notoptimized for low GHG footprints. Although C emitted during combustion isbalanced by C fixed by photosynthesis, bioenergy is not necessarily C-neutralbecause of GHG emissions released during plant growth, feedstock gathering,processing, and transport [49].

14.6.2

Carbon in First-Generation Bioenergy Crops

Currently, C stored in first-generation crops is being used, mainly in developedcountries, to produce the vast majority of liquid biofuels as an energy source for thetransportation sector [194,256,257]. Since it is a local resource, it may decrease theenergy and raw material dependence from other parts of the world. However,accurate evaluation of the environmental benefits from their biofuels has been acontroversial issue [56]. Crops, such as corn, sugarcane, oil palm, and rapeseed,


have been bred and developed to divert and store a large part of photosynthesis-fixed C into their seed for food production [239]. In addition, their residues areincreasingly considered as sources of biomass for liquid biofuel production[25,258]. With the long-term goal of producing 1 Pg of lignocellulosic biomass inthe United States and 4–5 Pg in the world, a large part of crop residues will beneeded to accomplish this goal [190]. The potential availability of first-generationseed and residue already is, or shortly may become, limited by soil fertility andproductivity. In addition, effective savings of CO2 emissions and fossil energyconsumption are limited by the high energy input required for first-generationcrop cultivation and conversion [258]. As an important determinant of ecologicalsustainability of bioenergy production, the continued use of first-generation cropsfor bioenergy production may lead to continued loss of biodiversity, competitionwith food crops for land use, and result in high production cost [35] whether theyhave negligible [35,37,62] or positive [63,64,258–260] effects on GHGmitigation.Biofuels derived from first-generation crops rely on fermentation of sugars to

produce ethanol [252] or on trans-esterification of plant oils to produce biodiesel[104]. It is generally well understood that first-generation crops are limited in theirability to achieve targets for fossil oil-product substitution, global climate changemitigation, and economic growth altogether [103,245,246]. For most first-genera-tion crops, the annual change in above-ground C is, at least theoretically, equal tozero if the whole biomass is used for energy production. The cost and sustainabilityof these crops, with the exception of sugarcane [261], have large C footprints, andare considered as expensive sources to meet environmental goals and to provideenergy alternatives [36,134,145,159]. These limitations can be partly overcome bythe utilization of lignocellulosic materials from their residues [25,82]; however,their use may become sustainable if a balance can be reached between soil fertilityand conservation objectives, on the one hand, and bioenergy production, on theother. Due to the energetic, environmental, and economic characteristics ofbiofuels produced from first-generation food crops, with the exception of sugarcaneethanol [262], they are being replaced, however not entirely, by dedicated, high-yielding lignocellulosic plants grown in both short and long rotations as well as byagriculture and forestry residues. Such a shift will significantly change the waybiofuel feedstock production affects the C cycle and flux [214].

14.6.3

Carbon in Second-Generation Bioenergy Crops

The recently identified limitations of first-generation biofuels produced from foodcrops has placed a greater emphasis on second-generation biofuels produced fromlignocellulosic feedstocks [105–110,263]. The second-generation crops are expectedto be more efficient than first-generation crops, and to provide fuel made fromcellulose and non-oxygenated, pure hydrocarbon fuels such as biomass-to-liquidfuel [225]. Biofuels produced biochemically or thermochemically from lignocellu-losic second-generation crops have more energy content (GJ ha�1 year�1) thanmost first-generation crops biofuels, could avoid many of the environmental


concerns, and may offer greater cost reduction potential in the longer term[30,264]. However, technical barriers remain for growth and fuel production fromsecond-generation crops. As with first-generation crops, the environmentalconsequences of second-generation crops depend largely on the type of feedstock,and how and where it is produced [105,106,263].Feedstock from agriculture or forestry residues, fast-growing short-rotation

coppice and short-rotation woody crops trees, and perennial grasses as second-generation biofuel sources offer promising technical, environmental, and eco-nomic solutions to problems faced with first-generation crops [35]. Unlike first-generation crops, second-generation crops until fairly recently [151] had minimaleconomic value, and they have not been supported by breeding and improvementinvestment [24]. Nevertheless, per area energy yield and the mitigation potential ofGHG emissions are inherently higher for second-generation crops [233]; they areless dependent on favorable climatic and soil conditions and require fewer inputsof agrochemicals, thus reducing their direct competition with food crops for land[205]. If the assumptions are realistic [220], planting second-generation crops onabandoned and degraded cropland, and using grassland with marginal productivityto grow low-input high-diversity perennials, may fulfill 26–55% of the currentworld liquid fuel consumption [74]. Also, if cellulosic feedstocks were planted oncropland that is currently used for ethanol production in the United States alone,more ethanol (þ82%) and grain for food (þ4%) could be produced while at thesame time both N leaching (�15% to �22%) and GHG emissions (�29% to�473%) will be significantly reduced [57].The net GHG emissions from using either cellulosic ethanol or biomass-to-liquid

technologies are substantially less than for ethanol from first-generation crops[245,265]. Early second-generation crops included some of the most extensivelystudied cellulosic perennial crops such as Panicum virgatum L., Phalaris arundina-cea L., Medicago sativa L., Pennisetum purpureum Schumach., and Cynodon spp.[126,225]. These were the original energy feedstocks used for draft animal power.Switchgrass (P. virgatum), a C4 warm-season perennial grass, demonstrated highproductivity across several environments, is suitable for marginal and erosivelands, needs low water and nutrient inputs, and has positive environmentalbenefits [266,267]. New cultivars with improved biomass yield and chemicalcomposition have been released in the Unites States [238,254,268]; however,switchgrass needs comprehensive breeding efforts, although its genetic resourcescan offer tremendous variability and great potential for energy improvement.Miscanthus (Miscanthus� giganteus), a cool hardy, vegetatively propagated C4

grass native to Asia, is an environmentally friendly species, its N requirements arelow and it can cycle N fertilizer efficiently. Moreover, Miscanthus has the capacityof fixing 5.2–7.2 t C ha�1 year�1, which results in a negative C balance[184,238,254,255]. Low-input, high-density mixtures of perennial grasses grown ondegraded lands were advocated [220] as better bioenergy sources than singlespecies, and may provide similar bioenergy gains and greater GHG benefits thancurrent corn ethanol produced from crops grown in monoculture on fertile soilwith high inputs. Indigenous perennial grass species are considered as better


bioenergy crops because they are likely to be well adapted to local environmentsand because they are less likely to adversely affect biodiversity than are non-nativespecies, which may become invasive.On average, increasing species richness in perennial herbaceous polycultures

increased productivity and weed suppression, but well-adapted species producedhigh biomass yield regardless of richness [199,269]. Non-edible plant oils (e.g.,from Jatropha curcas L., Euphorbiacea; 30–50% oil) and soapnut (Sapindusmukorossi and S. trifoliatus; 52% oil) as new sources for biodiesel production havethe advantage of not competing with edible oils produced from crop plants[270,271]. Other oil crops include Azadirachta indica, Calophyllum inophyllum, andPongamia pinnata, among 75 oil plants that contain 30% or more oil in their seed,fruit, or nut [103,272,273]. Major plant families with oil-producing plants includeAmaryllidaceae, Apocynaceae, Asclepiadaceae, Compositae, Convolvulaceae, Cruci-ferae, Euphorbiacea, Flacourtiaceae, Lauraceae, Leguminosae, Malvaceae, Mora-ceae, Myrcaceae, and Palmae.The unique cellulose biosynthesis and biomass production model of fast-growing

short-rotation coppice and short-rotation woody crop plantations creates a strongsink tissue that forces the tree to prioritize the channeling of C flow towards thesynthesis of xylem biopolymers [162], thus affecting C cycling and flux[83,117,168,181]. Short-rotation coppices are among the most promising dedicatedcrops for bioenergy production and global climate change mitigation [181]; theyinclude Salix, Populus, Robinia, and Eucalyptus species. Short-rotation coppiceproducts are combusted for heat or electricity generation, and can be processed toproduce ethanol. Short-rotation coppice willow or poplar can be productive for25–30 years and produce between 7 and 12 oven dry t ha�1 year�1 [274]. Deciduoustrees in short-rotation coppice plantations with high wood density (mainlydeciduous species) accumulate and sequester more C than coniferous tree specieswith light wood density, when evaluated at identical biomass volumes. Althoughshort-rotation coppice plantations may result in more biomass and have largerpotential for global climate change mitigation than herbaceous perennial bioenergycrops, may have a negative impact on biodiversity. The potential for C sequestrationunder short-rotation coppice and short-rotation woody crops is a considerableuncertainty in our understanding of how many tree plantations might be used topartially offset increasing atmospheric [CO2].Oil palm-based biofuel agroecosystems, when properly managed, have minimal

impact on soil C stocks and can maintain up to 98% of soil organic C under nativevegetation over time [154], thus adding recalcitrant C to the agroecosystem[20,95,99]. However, short-term soil C sink potential, C cycling, and sequestrationin oil palm agroecosystems is not well quantified, although such information isneeded for C budget inventories and sustainability assessment [20,95]. There wereno significant effects of plantation age on soil organic matter, microbial biomass,potential soil respiration, or solid surface CO2 flux, implying soil C was in dynamicequilibrium over a relatively long (11–54 years) period since planting. However, theshort-term C sink may significantly increase in root biomass with plantation age[100]. Although it can be produced in an environmentally friendly manner to help


mitigate global climate change and preserve biodiversity, oil palm, as it is currentlypracticed, contributes to GHG emissions, impacts local environments, and replacesimportant C sinks in peat lands [20,95]. Significant progress continues to be madeto overcome the technical and economic challenges, and second-generation biofuelproduction will continue to face major constraints to full commercial deployment[262]; however, genotypic variation in traits affecting C assimilation, and partition-ing, and plant N cycling as important controls on C sequestration [162,167] needsto be identified, evaluated, and used in developing future second-generationbiofuel crops.

14.6.4

Carbon in Third-Generation Bioenergy Crops

The third-generation crops include, for the purpose of this chapter, crassulaceanacid metabolism (CAM) and boreal plants, Eucalyptus spp., and microalgae[198,235]; the CAM and boreal plants are potential sources of feedstocks for directcellulose fermentation [141,163], Eucalyptus for bioenergy production throughthermoconversion [141,264], and algae for biodiesel. Successful development ofthese plant species as third-generation crops depends on a detailed understandingof complex genetic, enzymatic, and thermodynamic mechanisms that direct C flow,and of cellulytic bacteria metabolism, capable of degrading cellulose and utilizing itas a source of C. Under aerobic conditions, cellulose is generally degraded intowater and CO2, while under anaerobic conditions CH4 and H2 are also produced[124,275,276]. The CAM pathway, as a photosynthesis adaptation, optimizes WUEof C assimilation in arid habitats, responds to elevated [CO2] on marginal lands[161], and, therefore, offers a means of drought tolerance in bioenergy crops [277].CAM plant species have higher WUE (i.e., CO2 fixed per unit H2O lost) that can be3- and 6-fold higher than that of C4 and C3 plants, respectively. For example,Cardoon (Cynara cardunculus L.), a CAM plant, serves as a multifunctionalbioenergy crop that can produce solid and liquid biofuels. The heating value of thedry biomass yield with and without the seed is on average 18.5 and 16.5GJ t�1,respectively, with an input/output energy ratio of up to 1:27. The seed (whichaccounts for 15–20% of biomass) is 25% oil that can be converted into biodiesel;the biomass can be converted into ethanol [163].A large and diverse germplasm pool of boreal plant species is available for CH4

production. These plants are easy to cultivate, harvest, and store, are tolerant toweeds, pests, diseases, drought, and frost, and have good winter hardness, and areable to grow on poor soils with low nutrient inputs [176]. Boreal plants also includeperennial grasses such as Phleum pretense and Phalaris arundinacea that canproduce 2900–4000 and 3800–4200m3 CH4 ha

�1, respectively, and are among themost efficient producers of herbaceous biomass under boreal conditions [176].Boreal plants, such as Ananas comosus, Opuntia ficus-indica, Agave sisalana, andAgave tequilana, are already being used to produce bioenergy with sizable globalclimate change mitigation potential. Opuntia spp. produce large biomass (47–50Mgha�1 year�1) for forage and fodder under natural and managed agroecosys-


tems. Agave as an economically viable source of ethanol with a zero-waste platformin Mexico produces 50Mgha�1 year�1 with 27–38% sugar, and distilled ethanolyields of 14 000 l ha�1 and an additional 33 500 l ha�1 from cellulose digestion [176].Eucalyptus spp., native to Australia, have fast growth, tolerance to biotic and

abiotic stresses, indeterminate growth habitat, coppicing, and lignotuber produc-tion traits [162]. Eucalyptus plantations under tropical conditions can produce large(70m3 ha�1 year�1) biomass in relatively short (around 5 year) rotation. Worldwide,four species and their hybrids (i.e., E. grandis, E. urophylla, E. camaldulensis, and E.globulus) comprise about 80% of plantations. In particular, E. globulus is a widelyadapted species that is being used in breeding for fast growth, and comprises mostplantations in Australia and Brazil, where its oil is produced in addition to biomassfor biofuel and bioenergy production. Lignin content of the species (around 34%) ishigher than most hardwood species, which suggests that short-rotation plantationsof Eucalyptus spp. can be ideal for bioenergy production through thermoconversion[93,264].High-lipid algae species are an efficient and promising source of biodiesel with

favorable environmental benefits and potential positive global climate changemitigation impact [198]. Depending on the species, algae contain 20–40% lipids byweight, and can produce a wide range of feedstocks for the production of biodiesel,bioethanol, biomethane, and biohydrogen; however, algae cultivation requiresspecific light, temperature, and density conditions. Microalgae function asminiature biochemical factories, their photosynthesis is more efficient thanterrestrial plants, and they are efficient CO2 fixers [235]. Algae, at 10 gm�2 day�1

and 30% triglycerides, can produce 12 000 l of biodiesel ha�1 year�1, and at50 gm�2 day�1 and 50% triglycerides, can produce up to 98 500 l of biodiesel ha�1

year�1 as compared with rapeseed (1190 l ha�1 year�1), Jatropha crucas (1890 l ha�1

year�1) and oil palm (5950 l ha�1 year�1) [272]. Microalgal systems have a higherphoton conversion efficiency, can be harvested batch-wise nearly all year round, canutilize brackish and saline water resources [278]. Additionally, these algae cancouple CO2-neutral fuel production with CO2 sequestration, and produce non-toxicand highly biodegradable biofuels. The optimization of strain-specific cultivationconditions is a big challenge due to its complexity. Microalgae can be improved forbiofuel production through a series of processes, including screening availablenatural isolates, genetic engineering, selection, and adaptation. Microalgal biofuelsare likely to have much lower impacts on the environment and the world’s foodsupply than conventional biofuel-producing crops [198,220,235].Salinity is increasingly an important agricultural problems that result from, or is

aggravated by, global climate change. In view of the competitive nature of the non-salt-tolerant glycophytes as biofuel sources for land and water resources, halophytesprovide alternative solid, liquid, and gaseous biofuel sources that can thrive onbrackish and saltwater or in saline soils [277,279]. These salt-tolerant plant speciesare common feedstocks for fuel, food, and feed in developing countries. Carbonsequestration and global climate change mitigation, rehabilitation of degradedland, and stabilizing agroecosystems by providing niches and protection for otherflora and fauna are among their many ecosystem services. Halophytes are not a


single taxonomic group of plants; they include forbs, grasses, shrubs, and trees.Most halophytes can be utilized or domesticated as bioenergy crops. These plantshave unique characteristics in that they can complete their normal annual life cycleunder conditions of over 15 dSm�1 root zone salinity.Due to their ability to adapt to diverse and harsh environments, halophytes can

occupy important niches in many ecosystems and do not compete with other plantspecies [278,280]. Some of the species that are being used for fuel production insaline environments are found in the genera Acacia, Eucalyptus, Casuarina,Melaleuca, Prosopis, Rhizophora, and Tamarix. Frost-sensitive Eucalyptus spp. andfrost-tolerant Populus spp. are capable of biomass production under salineconditions. Eucalyptus rudis and Acacia saligna, as bioenergy crops, have highpotential for rapid growth and can be easily established in large plantations[93,281]. Experimental Salicornia farms yield 17–20 and 2.0Mgha�1 year�1 ofbiomass and combustible oil using seawater (around 35 dSm�1), respectively.Giant reed (Arundo donax), a perennial rhizomatous grass, tolerates salinity up toaround 18 dSm�1 and produced 11 000 l of ethanol from 45Mgha�1 year�1 ofbiomass using biomass-to-liquid technology. In spite of their great potential asbioenergy crops, very few halophytes have been identified so far as potentialsources of liquid fuels besides A. donax. Wild sugar beet (Beta maritima) and thenipa palm (Nypa fruticans) have been identified as sources for liquid biofuels;whereas, Kallar grass (Leptochloa fusca) is a promising source of biogas production.Continued efforts of selection and breeding will be needed for successful and long-term sustainability of halophytes as bioenergy crops and to help mitigate globalclimate change will depend on continued efforts of selection and breeding[121,122].

14.7

Genetic Improvement of Bioenergy Crops

A rich history of breeding annual, perennial [118], and tree [162] crops resulted intremendous yield increases and in large, structured genetic diversity in populationsof these crops. As we can, in hindsight, view qualitative and quantitative traits thatmade certain wild plants desirable for domestication to become today’s food andfeed crops, we are now prospectively defining criteria to choose wild or semi-domesticated plants as potential bioenergy crops [109,282]. Classical breeding andgenetic modification techniques are already available to develop biofuel crops withdesired morphological, phenological, and biochemical traits [118,121]. Theseinclude large C uptake, partitioning, and sequestration; high bioenergy yield anddensity; large C :N ratio; modified lignin biosynthesis; preprocessing in planta viaexpression of specific enzymes such as cellulases and cellulosomes; and cell walllignocellulose characteristics that make the feedstock more amenable to processingby one or a combination of biological, physical, and chemical pretreatments.Genetic improvement to develop bioenergy crops more adapted to adverse

environmental conditions with higher growth rate and high calorific value will have

14.7 Genetic Improvement of Bioenergy Crops 369

to explore genetic correlations between yield-related traits, and identify “earlydiagnostic” indicators of biomass and bioenergy yields and energy densities[2,127,183,244,254,268–270,283–286]. Many of the traits that need manipulating toimprove bioenergy yield and density are unlikely to be amenable to simple geneticmodification, and will require a combination of classical and novel gene discoveryapproaches [284–286]. Such innovations in feedstock yield improvement, cropadaptation to marginal lands, plant modifications to increase amenability forbioprocessing, and modifications to allow multiproduct production from a singlebioenergy crop are required to meet current and future bioenergy needs and forenvironmental protection [22,46,49,87,111,128,129,287].In-depth understanding of genetic and physiological mechanisms that control

yield-related traits or yield components is important to achieve large gains in drybiomass yield of perennial lignocellulosic bioenergy crops. Also, new geneticresources with wide genetic diversity for yield-related traits, “climate-ready” genes,and transgenic solutions to biotic and abiotic stresses will accelerate dry biomassyield and bioenergy gains, and improve environmental footprints of futurebioenergy crops [286,288]. The open question, however, is whether bioenergy yieldwill increase faster than the projected 1% per year using advanced geneticimprovement technologies?

14.7.1

Genetics, Breeding, Transgenics, and Carbon Sequestration

Breeding of bioenergy crops implies breeding for adaptation to long-term globalclimate change, the production of genotypes with lower genotype� environmentinteraction for dry biomass yield and bioenergy yield [118–122], and may involveinnovative plant design via accelerated domestication [109,282]. It is unrealistic toassume that large-scale plantations of bioenergy crops can be started with little orno domestication; large deployment of wild or semi-domesticated species in thelandscape as bioenergy crops will inevitably lead to unforeseeable biological andenvironmental problems [30]. A basic breeding program for bioenergy crops entailscollection and evaluation of genetic resources, genetic analyses and development ofselection criteria, novel tools for selection and testing new varietal concepts, andgenetic improvement for biomass yield and bioenergy plant- and biofuel-relatedproperties [119,282]. Plant domestication efforts should explore the widest geneticdiversity from wild species to identify genetic resources for higher drought andcold tolerance, increased WUE, NUE, and photosynthesis, synchronized growthphases with environmental conditions, and reduced or elimination of plantinvestment in reproductive organs [109]. Plant genetic resources have already beenmined to improve lignocellulosic biomass accessibility to enzymatic degradation[119,141,276].A thorough understanding of how gene products function in the chemistry,

synthesis, and architectural construction of the cell wall [276] will help modifyplants to engineer lignin and cellulose so that they breakdown more easily, speed-up plant growth, and increase yield [286]. Data integration from next-generation


genomic technologies [162] and genetic engineering could produce crop plantswith reduced biomass conversion costs by developing crop cultivars with lesslignin, crops that self-produce cellulase and liginase enzymes for cellulose andlignin degradation, respectively [289], plants that have increased depolymerizedpolysaccharides [290], larger biomass yield using genes for delayed flowering[121,239,268], or enhanced C allocation as recalcitrant organic matter in the rootsfor transfer to the soil organic C pool. Preprocessing in planta via expression ofcellulases and cellulosomes could potentially reduce the cost of enzymaticsaccharification of lignocellulosic biomass [286]. One of the major targets in thedomestication, breeding, and development of bioenergy crops is the alteration ofthe ratios and structure of the macromolecules involved in the structure of theplant cell wall. These alterations may allow for easy postharvest deconstruction ofthese macromolecules at the cost of a less rigid plant that may become subjected tobiotic and abiotic stresses. The genetic engineering industry is actively developingmethods to use genetic modification and to simplify and streamline processes tobreakdown the structural carbohydrates in the cell wall (i.e., cellulose, hemicellu-lose, and lignin) so as to produce inexpensive and environmentally friendly biofuelsmore easily and efficiently from plant biomass [268].A wealth of genomic resources and tools that can be put to immediate use and

achieve advances in biomass yield and GHG profiles of current and futurebioenergy crops is already available from previous and current research on foodcrops, some of which are still being used as first-generation biofuel crops [276].Genomic information gathered from across the biosphere, including potentialbioenergy crops and microorganisms able to breakdown biomass, is improving theprospects of significant cellulosic biofuel production from second-generation cropsas dedicated bioenergy crops with reduced conversion costs and favorable GHGprofiles [225]. Complete genome sequences are available for a number of importantbioenergy crops, such as popular, sorghum, and the model grass Brachypodium[290]. Tree genomic research already identified genes for increased C partitioningto above-ground woody matter, increased cellulose availability for enzymaticdigestion, manipulated genes for N metabolism, delaying senescence, anddormancy, and increased photosynthesis and adaptation to drought and salinity.Genomic information and resources are being developed that will be essential foraccelerating their domestication. Populus trichocarpa was the first tree and potentialbioenergy crop to have its genome sequenced [94]. The high degree of geneticsynteny among perennial grasses or short-rotation coppice genomes shouldfacilitate the translation of gene function discovery to more genetically recalcitrantspecies [83,119]. Value-added genes that cannot be transferred through crossingand selection can be incorporated into potential bioenergy crops throughtransformation methods (e.g., Agrobacterium-mediated transformation of switch-grass) can be used to incorporate value-added genes that cannot be transferredthrough crossing and selection. It is speculated that a transgene (e.g., for reducedlignin content) should not cause environmental harm; however, a bioenergy cropwith reduced lignin content may become more susceptible to biotic and abioticstresses [30].


Fast-growing perennial bioenergy crops, developed by genetic modificationtechnology, can gain higher dry biomass yield, reduce GHG emission through acombination of lower inputs and reduced or no tillage [60,73,112–114,117,167,181,234], and offer global climate change adaptation and mitigationthrough multiple resistances or tolerances to biotic and abiotic stresses, herbicides,salinity, and environmental toxicity [280]. The next generation of bioenergy crops isbeing developed using marker-assisted selection [124,125,276]. Hybrids andtransgenics have been developed with large dry biomass yield, more efficient plantarchitecture to increase light interception [127], tolerance to biotic and abioticstresses, NUE, and WUE. Heritability for dry biomass yield in perennial grasses ishigh enough to allow plant breeders to predict and demonstrate adequate gainfrom selection; however, yield gains vary across selection cycles [119,238].Significant breeding advances have been documented in several perennial grassspecies for dry biomass yield and the potential for increasing this yield isconsiderable because of the large genetic diversity available within the species[78,137,183,184,254,267,283,291,292]. Lignocellulosic yield of perennial grassesand short-rotation coppice trees parallels their dry biomass yield; for example,Bermuda grass (Cynodon dactylon L. Pers.) genotypes bred for high dry biomassyield produced twice as much as unimproved genotypes and recent yield trialsindicated that switchgrass yields were 50% greater than those achieved in early2000 [293]. Therefore, instant determination of net energy value is a valuable toolfor plant breeders and growers to tailor genotypic development, hybrid selection,and crop management to produce the highest dry biomass yield [288]. In addition,self-incompatibility in some perennial grasses (e.g., switchgrass) may allow for thedevelopment of high-yielding single-cross hybrids and the use of F1 hybrids willhave the potential of significantly increasing dry biomass yield [290].Breeders of bioenergy crops need to optimize plant C allocation among plant

components, which requires phenotypic and genotypic data, and a crop model thatcan capture the impact of different C allocation schemes on growth, biomass, andbioenergy production [94]. Moreover, they need to conduct expensive long-termexperiments involving perennial species in the presence of genotype� environ-ment interaction [283,291]. The challenges involving breeding and deployment ofgenetically modified bioenergy crops include regulatory approvals, market adop-tion, and public acceptance [127]. However, the use of genetic modificationtechnologies is central to the strategy of the US Department of Energy to deploy,within 10–15 years, bioenergy crops having optimized cell wall characteristics,enhanced biomass and bioenergy yield, and stress tolerance [127]. Breedingobjectives of bioenergy crops include the improvement of biomass yield, quality,and conversion efficiency, either through selection among progeny obtained bycrossing parents with desirable traits or as a way to enhance the agronomicperformance of promising mutants and transgenic plants [125,288]. In short-rotation coppice tree breeding, for example, breeders must reduce the number ofyears required to complete a generation of testing and its deployment, improveunderstanding of the genetic control of desirable timber traits, and produce fast-growing short-rotation coppice cultivars [181].


Although significant genetic diversity exists for traits related to C sequestration,information on how targeted genetic changes in new bioenergy crops couldinfluence soil C sequestration are limited [167]. Availability of substantial geneticdiversity suggests that a number of important biomass-related traits exhibitgenetically induced variation [271,272]. However, high genetic diversity levels maycomplicate agronomic studies designed to understand, and possibly minimize, theimpact of genotype� environment interaction on BDY: Biomass Dry Yield andenergy-related traits [294,295]. The genotype� environment is typical of widelydistributed plant species, which are usually locally adapted [263,291]. Prolongedselection and breeding of bioenergy crops could result in producing highlydifferentiated genotypes with lower genetic diversity than their wild progenitors aswas the case in several first-generation crops [81,270,285]. Gene flow betweennewly domesticated bioenergy crops and their progenitors or wild relatives couldlead to the introduction of adaptive or maladaptive genes, disruption of co-adaptedgene complexes, and genetic assimilation [81,118].

14.7.2

Genetic Models and Ideotypes of Bioenergy Crops

The ideotype concept for food crops in the 1960s was instrumental to under-standing the physiological reasons behind the breeding success of the GreenRevolution. A model plant was expected to divert larger amounts of fixed C to thedeveloping grain. Therefore, the cereal ideotype was phenotypically characterizedby a short stem, small erect leaves, a low number of tillers, and a large and awnedear. As yield is a property of a population of plants and is poorly correlated with theperformance of an individual plant in the population [118,183,245,251,293], thecereal crop ideotype was designed to be a weak competitor to reduce intra-cropinterference and thereby maximize yield per unit area. Advancing appropriategenetic models for bioenergy crops is indispensable in the development ofagroecosystem approaches to improve several traits related to dry biomass yieldand bioenergy production, and to enhance global climate change adaptation andmitigation. Therefore, the ideotype for a bioenergy crop seems to be quite differentfrom that of a food crop. A number of traits to maximize radiation interception,WUE, and NUE have been suggested to develop bioenergy crop ideotypes[72,282,296]. Traits that may provide a variety of ecosystem services (e.g., Csequestration, biological pest control, pollination, and biodiversity conservation) ascomponents in the sustainable production of bioenergy should be considered inbioenergy crop models and ideotypes [31,275,297].As corn and sorghum have a close evolutionary relationship with future

bioenergy perennial grasses, they were suggested as genetic models for theimprovement of future perennial C4 bioenergy grasses. Two other grasses, rice(Oryza sativa) and brachypodium (Brachypodium distachyon), a grass with a smallgenome, were suggested as comparative models for grass cell biology [284,298].Recognition of poplar as a model tree and sequencing of its genome representsignificant recent advances [24]. Relatively recently [181], alternative growth


strategies have been identified in short-rotation coppice bioenergy crops (e.g.,willow) where some genotypes were characterized by a large number of thin stems,and relatively low leaf area index and specific leaf area, whereas another group hadlarger-diameter stems, and high leaf area index and specific leaf area; bothstrategies gave high yields, suggesting that multiple ideotypes of a bioenergy cropmay need to be selected depending on genetic diversity and trait association. Withcontinued investment in perennial bioenergy crop species there is the potential,given the large pools of genetic diversity, to develop improved genotypes withhigher dry biomass yield, WUE, NUE, and improved GHG profiles [24,110].These model crops can help provide answers to how advanced C metabolism

arose and what its genetic controls are [149,163,184,299]; how different specieswith advanced C metabolism partition fixed-C into structural and non-structuralcarbohydrates; and what is the genetic basis of physiological and architecturaltraits, such as tillering, canopy formation, stalk reserve retention, perennial growthhabit, WUE, and NUE. Identifying whether these traits are determined by majorgenes or quantitative trait loci is of foremost importance [284,285].

14.8

Carbon Management in Bioenergy Crops

Carbon management depends to a large extent on proper land use and manage-ment [41,44,135,147,151,300]. Managed agroecosystems carry historical C debtsand are bound to lose C much faster than they accumulate; therefore, an alternativeeffective C management strategy in the land-use sector is to protect existing Cstocks [41,55,83,301]. However, land and C management decisions for bioenergyproduction and global climate change mitigation may become constrained byexisting land-use systems, C stocks, and timing of land-use change[73,151,219,302]. Many variations of land use and C management practices doexist, and options to enhance C input and reduce its emissions are alreadyavailable, even under the worst projected global climate change scenarios [55].Carbon management technologies can be used to intensify C pools, C conversion,CO2 capture, or CO2 sequestration [23]. Whether it minimizes atmospheric CO2

emissions from its sources and/or maximizes CO2 removal from the atmosphereby sinks, C management can achieve its objectives by increasing total Csequestered in soils and stored in biomass, and by reducing GHG and energyoutputs mainly from land use and land-use change [23,41,151,302].The anthropogenic C (about þ4.38 Pg C year�1) constitutes the flux to be handled

by economically effective C management technologies. Energy system designsinvolving C-based energy vectors integrated with value-added C managementtechnologies already constitute key components of C management systems [23,75].While climate protection may have been a rationale for promoting biofuels[12,42,57,180], public support for biofuels rested on their value for rural economicdevelopment and was amplified by concerns about energy security[7,9,158,189,239,303]. Biospheric C management may result in increased or


decreased C stocks in one or more of its pools; the process, which is not directlyand entirely under human control, however, can be reversed, either accidentally orintentionally through subsequence land-use change [23,41,151,302]. The non-Cbenefits of biospheric C management might also gain greater protection inaddition to ensuring that biospheric C management does achieve its global climatechange mitigation objectives [208].Although many environmentalists promoted biofuels, climate concerns may

have not been a solid foundation for public biofuel policies [42] (see Section 14.14).Carbon management strategies focus on offsetting anthropogenic emissionsthrough human-enhanced natural removal of C from the atmosphere to other Cpools. There are several cost-effective and environmentally friendly C managementtechnologies that can significantly accelerate this beneficial shifting of CO2 fromthe atmosphere to other C pools [23]. Biomass-based energy technologiesintegrated with value-added C management include biofuels (oils, ethanol, diesel),anaerobic digestion with coproduction of C-rich fertilizers, biogas upgrading tobiomethane, biofertilizers, mineral fertilizers, food products, pharmaceuticals,cosmetics, basic chemicals, polymers, biochar, biosyngas, biohydrogen, andsynthetic natural gas [23,262].Much of the plant biodiversity is located on lands that are relatively less

productive and poorly suited for biomass or biofuel production. A critical issue forboth C management and biodiversity on marginal lands is where, how much, andhow biomass is produced [287]? Smallholders and pastoralists in marginal landsmay consider adopting a C management system if financial payments canadequately compensate for giving up short-term gains, if collateral benefits can begained from ecosystem services, or if C-friendly land use can diversify globalclimate change adaptation options and enhance their income [69,227].

14.8.1

Managing Carbon Sources and Sinks

Assuming that bioenergy, as an ecosystem services, can contribute to increasedbiomass and soil C sinks [300], and in spite of current and future limitations tohuman appropriation of competing ecosystem services [17], the annual demand forbiomass for bioenergy is expected to double in 2020 (from around 5.7 to 10 EJ)[232], then the need is urgent to predict future terrestrial C dynamics and theirinfluence on atmospheric CO2 growth. Proper management strategies of Creservoirs (i.e., sources and sinks), including accurate estimates of natural, direct,and indirect human-induced effects on these sources and sinks, become moreurgent [250]. Estimates of global C reservoirs (i.e., sources and sinks) indicate thatbetween 1800 and 1994, of the total sources (457 Pg C), 53% came from fossil fuelcombustion, around 9% from terrestrial ecosystems, and 38% from land-usechange [6,233,248]. Sink estimates, during the same period included 36% absorbedby the atmosphere and 26% absorbed by the oceans; the remaining 38% constitutethe residual terrestrial sink. Estimates of the sources and sinks at the decadal scaleindicate the magnitude and changes in the natural sink capacity of 56.7% and 60%

14.8 Carbon Management in Bioenergy Crops 375

during the 1980s and 1990s, respectively, and 51.7% from 2000 to 2005[143,144,304]. Soils constitute a major reservoir of Earth’s C. In particular, soilorganic C, a storehouse of plant nutrients, provides essential ecosystem services[26–28,135,190] and regardless of its role in global climate change mitigation, theproper management of the soil organic C pool is essential for sustainable land use[72,82,135,136,198].Annually, plants and soils combined absorb approximately 1 Pg C more than they

emit; therefore, increasing soil organic matter concentrations by 5–15% in the top2m could decrease atmospheric [CO2] by 16–30%. Soil organic matter turnover isgoverned by accessibility (e.g., by decomposers) and not necessarily by recalcitrance(i.e., sequestration) [206]. However, the global potential sequestration rate of soilorganic C is about 0.8 Pg year�1 and potential soil C sink capacity is about 80–100 Pg. This capacity is equivalent to an atmospheric drawdown of 40–50 ppm ofCO2. For this to happen, however, crop residues and other biomass must bereturned to the soil. Although hotly debated, removal of crop residues for biofuelcan create a negative soil C budget and deplete the soil organic C pool whosesensitivity to predicted global climate change and global warming is uncertain[25,82].Soil resources play an important role in global climate change processes due

to their function as sinks and sources of GHGs [100,250]; however, theyrepresent a massive stock of potentially unstable C [206], acting as a bufferagainst atmospheric CO2 increase and as a potential sink for additional C. Thebuffering capacity depends on the balance between photosynthesis, decom-poser activity, and C sequestration [206]. Deforestation, responsible for 30% ofthe anthropogenic increase in atmospheric [CO2] over the past 200 years, isconsidered as the leading threat to the terrestrial C sink [31,60,255,259]. If, forexample, a land-use change of rainforests, peat lands, savannas, or grasslandsin the United States, Brazil, and Southeast Asia is implemented to producebiofuels, it would lead to a large C debt by releasing 17–420 times more CO2

than the annual GHG reductions that the biofuels would provide by displacingfossil fuels [217,305]. REDD (Reduced Emissions from Deforestation andForest Degradation) is a mitigation action that seeks to preserve existing Cstocks in forests (typically tropical rainforests) and peat lands. The approachwould be additional to project-based efforts such as the Clean DevelopmentMechanism in order to solve issues such as permanence, leakage, monitoring,and baselines in the forestry sector. Nevertheless, shifting atmospheric CO2 tothe soil is currently feasible because many soils are below their ecological Csequestration potential [23,50]. Perennial bioenergy crops, when managed withminimum or no tillage and reduced external inputs, will maximize both thesoil C sink [306] and C stored in below-ground plant biomass [193]. Somebioenergy crops have a large capacity to fix atmospheric C (e.g., 5.2–7.2 t C ha�1 year�1 for Miscanthus) and result in negative C balance; however,unlike soils under annual row crops [307], C sequestration may continueunder perennial grasses [247], short-rotation woody crops, and short-rotationcoppice [92] until the soil reaches its sink capacity in about 20–50 years.


14.8.2

Managing Nutrient Composition, Cycling, and Loss

Uncertainties about the GHG mitigation potential of biofuels depend, in part, onnutrient cycling efficiencies of bioenergy crops, whereas sustainability of biofuelproduction depends on ecological processes that maintain high-yielding crops withlow GHG emissions [11]. Nutrients are removed from biofuel agroecosystem everytime biomass is harvested; therefore, plant species with high NUE may be the mostviable options for sustainable biofuel crops because GHG emissions associatedwith fertilizers would be minimal [11]. Biomass removal at harvest has environ-mental implications beyond the immediate impact on nutrient and C cycling insoils [127]; changes in natural nutrient and C cycles could negatively affect localbiodiversity, reduce soil quality, enhance erosion, and eventually deplete nutrientlevels [308]. For example, nutrient fertilizer requirements to meet a sustainablebiomass supply of 1 billion tons will remove 16.9, 5.2, and 18.2 Tg of N, P2O5, andK2O, respectively, from US agricultural land [90]; on the other hand, recyclingbiochar produced after gasification of agricultural biomass returns the nutrients toagricultural land and increases C sequestration [155,204].The implications for GHG balances of bioenergy agroecosystems arise from an

increase of synthetic fertilizer application to replace nutrients removed withbiomass or lost from the soil through leaching and to sustain biomass yields [215].As a complex heterogeneous mixture of organic and inorganic matter, biomasscontains different components, including solids, fluids, and minerals of differentorigins, and with different ratios and chemical bonds [231]. The chemicalcomposition of biomass, hence its quality, depends on several factors, includingplant species, organ, and age, growing conditions, management practices,including fertilizer and pesticide application, and harvest time and pretreatment[231,308]. Mineral nutrients are undesirable in biomass feedstock because they canultimately become atmospheric pollutants that must be mitigated irrespective ofthe type of fuel that is produced [294]. Although they are important attributes ofbiofuels, the quality and chemical composition of biomass have not receivedadequate attention. Changes in biofuel quality can drastically impact net energyoutput [308] and may be caused by crop-specific mineral uptake or during biomasspartitioning and processing [252,292]. These changes may limit the effectiveness ofconversion processes and decrease the energy value; the latter decreases withincreased ash content. For every 1% increase in ash concentration the heating valueis reduced by about 0.2MJ kg�1 [252,292]. New bioenergy crops and cultivars withspecific mineral contents (e.g., low ash, N, chlorine (Cl), and K) will be needed to fitthe demands of emerging bioenergy applications [231].Based on their elemental concentration (on dry weight basis), nutrients in

biomass can be classified as major (above 1.0%), minor (0.1–1.0%), or trace below0.1%) elements. Major nutrients, in decreasing order, are C, O, H, N, and Ca;minor nutrients include Si, Mg, Fe, P, Cl, and Na, whereas the most importanttrace elements are Mn and Ti. Bioenergy crops are usually classified on the basis oftheir chemical composition and mineral content to evaluate their suitability for


different conversion processes [231]. Similar contents of C, H, and O, andsignificant differences in the contents of N and ash-forming nutrients, have beenreported for different bioenergy crops [236]. A group of nutrients in woody plants(e.g., Al, Mn, Na, and Si) exhibited larger variation than others (e.g., Ca, Cl, Fe, K,Mg, and P). In general, however, bioenergy crops have high Cl and S contents,which are strongly associated with corrosion and HCl emissions [231]. On the otherhand, woody bioenergy crops, annual and fast-growing crops, have the largestcontents of ash, moisture, and highly mobile Cl, K, Mg, N, P, and S, as comparedwith woody bioenergy crops [308].The ability of some perennial species to fix N [11,309,310] and recycle mineral

nutrients on an annual basis by programmed senescence and mobilization ofmineral nutrients from vegetative tissues to rhizomes for subsequent reuse is apromising strategy for minimizing external fertilizer inputs [290]. However, Ndemand of a high-yielding bioenergy crop may not be fully met without such inputsor else soil nutrient reserves will be seriously depleted [294]. On the other hand,perennial biofuel crops with high nutrient retention capability may provide anotherecosystem service by reducing high nutrient loadings in areas such as riparianbuffers [164]. Due to extended growing seasons, high evapotranspiration rates, andextensive root systems, perennial bioenergy crops (e.g., short-rotation coppice,Miscanthus, and switchgrass) have the inherent advantage of exploiting fully a longgrowing season, nutrient recycling, and reducing nutrient losses to the environ-ment [39,114,173,296,311,312]; reduced soil erosion and leaching, and relatedimprovements in water quality may ensue, as well [173,291,313]. For example,switchgrass can replace corn and soybean on productive lands with 75–90%reduction in N and P losses. In comparison, rising corn cultivation would lead to anincrease of 10–30% in the annual average flux of dissolved inorganic N to theMississippi River [215] and the cultivation of oilseed rape may not be environmen-tally friendly because Brassica spp. emit more methyl bromide than any other crop[314,315].Legumes are less productive than grasses or perennials and may not be used as

bioenergy crops per se; however, when rotated with bioenergy crops, they minimizenutrient loss and enhance their cycling [81,144,309], Nevertheless, the energysavings obtained through less N input must be balanced with the loss of potentialyield. For most legume species, the biological nitrogen fixation is of the order of200–300 kgNha�1 year�1; a maximum of 450 kgNha�1 year�1 was reported forLupinus albus – a potential bioenergy legume crop. The cost of N uptake forinoculated L. albus is 2.9–6.1 gC g�1 N and when supplied by N fertilizer the costwould be 25–40% less. Legumes can provide positive inputs as fast-growing covercrops, provide additional biomass yield, enrich soil organic matter, and provideprotein feedstock for the chemical industry [81,126]. Even with legumes, removal ofbiomass for bioenergy reduces biomass that can be active in agroecosystemnutrient and water dynamics, C fluxes, food webs, and other ecosystemservices [79].Changes in soil composition and structure will affect nutrient cycling, directly or

indirectly through such processes as runoff, soil erosion, downstream surface


waters and aquifers, and GHG emissions [45]. In particular, the fate and transportof C and N during biomass production are of major environmental and economicconcerns [15,31,97,111,129,131,313–315]. The C and N cycles are driven bymultiple factors (see Section 14.2.2), and changes to any of these factors can havesignifi cant effects on the growth and composition of biofuel crops, andconsequently on local C and N cycles; when implemented across millions ofhectares, local changes will either mitigate or exacerbate GHG concentrations at aregional scale [45,301]. Long-term effects of increased atmospheric CO2 onterrestrial C storage and sequestration are still a subject of scienti fic debate mainlybecause nutrient availability may, in the long-run, limit the effect of enhanced[CO2] on ecosystem C uptake [210].

14.8.3

Managing Land-Use Change

The land used to grow bioenergy crops for biofuels increased from 13.8 Mha in2004 (around 1% of global cropland) to 26.6Mha in 2007, and according to theInternational Energy Agency (http://www.greenfacts.org) will have to occupy 4.2%of global cropland (around 58.5Mha) and produce around 300 Ml of liquid biofuelsin 2030. It was estimated that land area (Mha) required to meet 100% of biodieselworld demand by 2030 would be 173 for Jatropha, 48 for oil palm, or 361 forsoybean. Whereas, land area (Mha) required to meeting 100% of ethanol demandwould be 147 for corn, 70 for sugarcane, or 116 for sweet sorghum. It wasestimated [279] that the mean annual CO2 emissions (Mt CO2 year

�1 by 2030) fromland-use change to bioenergy crops under different scenarios (above), where eachcrop is assumed to meet 100% of biodiesel demand if planted to different cropsmay range from 537 for Jatropha to 1119 for soybean; however, to meet 100% ofethanol demand the mean annual CO2 emissions will vary from 216 for sugar caneto 706 for corn. These emissions are likely to be greater than the savings expectedfrom the first 30 years of growing these bioenergy crops. In comparison,conventional croplands, on average, are currently losing soil organic C at a meanrate of 0.17MgCha�1 year�1, which is equivalent of 623 kg CO2eq ha

�1 year�1 [53].Evidently, the bioenergy sector is bound to keep expanding, and thus likely to affectall other national and international sectors of the economy, especially foodproduction [18,108,141,164]. The net GHG exchange depends on several factors,including original C stock, fertilizer application rate and soil N reserves, climaticand environmental conditions, and land and residue management practices[59,113,141]. Also, crop production for food or biofuels leads to a different netexchange of CO2 if fertilizer is applied and when land-use change occurs[12,73,151,219,302].The GHG benefits from biofuels could potentially be altered by direct and

indirect land-use change [44,60,73,151,152,218,300]. A wide range of C intensities(g CO2 MJ�1) for ethanol due to direct (�52 to 54) and indirect land-use change (0to 327), and for biodiesel (�98 to 481) were caused by several factors, including thebioenergy crop itself, the type of the land used or displaced, and the amortization


http://www.greenfacts.org

period [151]. Net sequestrations (i.e., negative values) were caused by land-usechange from food to cellulosic crop production, whereas net commissions (i.e.,positive values) were caused by land-use change from rangeland to sugarcaneproduction [59,151,224,316]. These C intensities were associated with a wide rangeof pay-back time ranging from 0 to 93 years for ethanol and from 7 to 423 years forbiodiesel.Land-use change impinges on agroecosystem C balance by altering C cycling,

storage, and sequestration; the magnitude of these changes depends on howphysical, chemical, or biological processes are altered over time under differentland-use schemes [73]. Additionally, land-use change may impact atmosphericcomposition and local air quality [182], result in soil organic matter losses [177],and cause greater demand for water and energy [84,317]. When implemented at theregional scale, land-use change may cause changes in surface albedo and triggerfluxes of heat and humidity; therefore, massive land-use change and land cover canhave a variety of ecological effects [300], and may impact biogeochemical cyclesacross the globe [172]. Nevertheless, the largest ecological impact of biofuelproduction may well come from market-mediated land-use change [186]. Inresponse to greater demand and higher market prices, an unprecedented land-usechange resulted in a remarkable 19% increase in land area under corn between2006 and 2007 in the United States, and led to reduced crop diversity in parts of theMidwest [143,147]. In response to rising demand for biodiesel, an estimated1.7Mha of oil palm plantations in Indonesia have already been established on C-rich peatland [20]. Deforestation and land-use change contribute 15–25% of globalC emissions [20]. Converting low-land tropical rainforest to oil palm plantations isestimated to result in a C debt of 610 Mg CO2eq ha�1, which would take 86–93years to repay. More than 50% of the world’s rainforest has been lost to agriculturesince the industrial revolution; it has been replaced, mostly, by oil palm with aglobal production of 35Mt year�1. The respective figures for peatland are 6000MgCO2eq ha�1 and 840 years [20]. Land-use change from pastureland to short-rotationwoody crops induced N2O emission of 4.2–5.5Mg CO2eq ha�1; almost 90% and10% of this flux was attributed, respectively, to direct N2O emissions from soil andto indirect emissions through N leaching [92].In order to be a viable energy source, land use for bioenergy crops will have to

environmentally and economically compete successfully with other land uses for ashare of the finite land resources, and the extent to which bioenergy crops displaceother crops will influence global land use and the global agroecosystem[35,50,216,233,248,318,319]. Future availability of land area for bioenergy cropswill be sensitive to developments in, and balance between, food demand and supply[248]; therefore, careful decisions about future land use and land-use changerequire a comprehensive analysis in order to avoid negative future outcomes [35].Biofuel production opportunities in developing countries are being fueled by theapparent relative availability of land to grow bioenergy crops; however, this raisesconcerns about potential added social and environmental pressures, including Cdebts, and environmental consequences due to land-use change and land clearingsuch as GHG emissions and loss of biodiversity [6,255,275,297,302,320]. Under


developing country conditions, diversified and integrated food/bioenergy land-useagroecosystems are proposed to simultaneously protect and promote a variety ofecosystem services (see Section 14.11). Due to their resilience, such integratedagroecosystems are capable of adapting to global climate change more thanmonocultures,. However, if land use agroecosystems that maximize both C andprofit are not realistic [18], then smallholders are advised to manage theirintegrated food/bioenergy farming for profit and choose for an acceptable ratherthan a maximum level of stored or sequestered C.Based on International Energy Agency 30-year projections and depending on the

C intensity of bioenergy crops, allocating around 58.5 Mha to meet biofuelmandates and requirements will put intense pressure on land both for the purposeof natural resources conservation, sustainable utilization, and provisioning ofecosystem services (see Section 14.11) and for food production purposes (seeSection 14.12.1). Furthermore, clearing of natural ecosystems to grow bioenergycrops may create a C debt of greater GHG emissions than the fossil fuels theyreplace. Therefore, the effect of large-scale deployment of bioenergy crops willripple not only through the global economy, but also through the global ecology viachanges in commodity prices and the resultant land-use change [126,136]. Thus, itmust be ensured that any further land expansion for biofuel production willprovide a positive contribution to global climate change mitigation, knowing thatland-use change is the source of the most significant GHG emissions. To illustratethis point, land-use change from tropical forest to sugarcane plantation caused aloss of around 31 and 120 t Cha�1, respectively, in soil C and in above-groundbiomass pools [205]. The effects of land clearing for biofuel production onagroecosystem C debt (Mg C ha�1) are illustrated by the impact of land-usechange to produce biodiesel from soybean (201) and oil palm (941); and ethanolfrom corn (19) and sugarcane (45) [35]. The US Environmental Protection Agencyestimates indicated that corn ethanol and soybean biodiesel caused enough land-use change to call into question whether these biofuels meet GHG reductionrequirements [19].

14.8.4

Biogeochemical Liabilities of Carbon in Bioenergy Crops

Agriculture, the most intensive land use, covers more than 30% of the global landarea, uses around 70% of the fresh water, and therefore contributes to massivechanges in Earth’s biogeochemical cycles [129]. Land management and land-usechange have considerable influence on biogeochemical cycles [170]. Ecologicalimpacts of biofuels, and therefore on biogeochemical and biogeophysical cycles,are mediated through their effects on land, air, and water [186]. However, asindicated earlier (see Section 14.8.3), land-use change to grow more biofuels, inresponse to market forces, may cause the largest ecological impact. Surface energyfluxes and the hydrologic cycle – both affecting climate across temporal and spatialscales [10] – are regulated by several biogeophysical factors, such as changes insurface reflectivity, evapotranspiration, and surface roughness. Radiative forcing is


induced if the albedo value of the land surface changes at the time when a biomasscrop is either planted or harvested.Changes in land use will greatly impact biogeochemical and biogeophysical

cycles across the globe [172]; the UN Environment Programme, for example,highlighted the potential environmental impacts on several biogeochemicalprocesses associated with millions of hectares of additional cropland necessary tomeet the future global biofuel needs [212]. If we are to quantify the major pools andfluxes in the biogeochemical cycles of water, C, N, and other nutrients in biofuelcrops, and to determine how and on what timescale interactions with soil biotaaffect these biogeochemical cycles [307], then the lingering question is how todecouple persistent organic pollutants from biogeochemical cycles of water, C, N,and other nutrients under global climate change [321]? In particular, what wouldbe the fate and transport of C and N during biomass production, if we know thatthey interact, at multiple spatio-temporal scales, with other biogeochemicalprocesses [45]?Changes in biogeochemical cycles are attributed to shifts in vegetation, decreased

organic C due to soil organic matter decomposition, and rise in pH; soil organicmatter, in turn, closely controls many soil properties and major biogeochemicalcycles [11,17,164,169,321]. Therefore, desirable biogeochemical properties mayinclude increased soil organic matter, increased N mineralization potential, andreduced NO3 leaching [82,135,206,215,247]. With photosynthesis and respirationbeing the principal C exchange processes between soil and atmosphere, small butstable changes in soil organic matter could critically impact the global C fluxes[177]; the latter is considered an important process in understanding andforecasting global changes in biogeochemical cycles and, in due course, inpredicting global climate change.The intensive, and usually short, production season of annual crops under

temperate climates and summer rains involves long periods with little or no waterand nutrient uptake; the biogeochemical implications of such agroecosystemsinclude integrated surface runoff, soil erosion, nutrient loss, and groundwatercontamination by agrochemicals [17,321]. Intensive grain production, extensivebioenergy crop deployment, and projected global climate change, if combined, willexacerbate these environmental problems, and may worsen landscape and waterenergy balances, and water quality problems through eutrophication and acidifica-tion [16,80,277,322,323]. Longer growing seasons, if triggered by future globalclimate change in the upper latitudes, may prompt higher biomass productivitywith implications for the hydrological cycle and water use, if and when bioenergycrops are deployed at a large scale [14]. Theoretically [324], the conversion of annualto perennial bioenergy crops across the central United States will impart asignificant local-to-regional cooling as a result of land-use change. The coolingeffect is related to larger evapotranspiration and smaller radiative forcing; the lattercan develop in response to higher albedo and would lead to significant implicationsfor stored soil moisture. Under current weather conditions, two second-generationbioenergy crops (Miscanthus and switchgrass) utilize about 57% more water thancorn for total seasonal evapotranspiration. However, projected higher atmospheric


[CO2] (around 550 ppm) is likely to decrease their evapotranspiration/water use byabout 10%; if higher temperatures were to be combined with reduced summerrainfall, a sharp increase in evapotranspiration will reduce soil-moisture storage.The biogeochemical effects of land-use change from annual to perennial bioenergycrops are expected to impart important aspects of climate impacts of biofuels, atlocal and global scales. Ecological implications of such land-use change of marginaland crop reserve program lands, for example, include impacts on C sequestration,soil organic matter decomposition, soil quality, biotic stress dynamics, and wildlifehabitats [89].The biogeochemical liabilities of grain-based crop production for bioenergy (i.e.,

first-generation crops) are similar to those of grain-based food production; theyinclude excessive NO3 leakage, soil C and P loss, N2O production, and attenuatedCH4 uptake [164]. Bioenergy crops, as energy carriers, may offer ecologicaladvantages over fossil fuels by contributing to the reduction of GHGs andacidifying emissions. The biogeochemical positive effect of cellulosic ethanol, forexample, is evident by comparing the 1 : 5 ratio of fossil energy input to new energygenerated against 1 : 1.4 for grain-based ethanol. There is a risk, however, ofpolluting water and air, losing soil quality, enhancing erosion, and reducingbiodiversity [313].Due to their unique biogeochemical attributes, multifunctional bioenergy crop

plantations produce several environmental benefits [66,325] and ecosystem services[28]. These include vegetation filters for waste water and sewage sludge treatment,shelter belts against soil erosion, soil C sequestration, increased soil fertility, andremoval of pollutants and toxic elements. Perennials, as compared with annualbioenergy crops, have a more positive impact on the environment [313], and whenincluded in alley cropping systems, they impart additional microclimate benefits[326]. Perennials will positively affect biogeochemical cycles as C is sequesteredbelow ground, GHGs are abated, and less NO3 and P are delivered in surface andground waters [45]. However, benefits for land use and GHG emission reductionderived from perennial bioenergy crops have to be weighed against biogeochem-ical-related environmental impacts such as acidification and eutrophication [147],which mainly occur during biomass harvesting and processing [105]. Usefulpredictions about the future of bioenergy crop plantations and their functionalcharacteristics can be made if plant eco-physiologists and terrestrial ecosystemecologists connect simultaneous changes in multiple biogeochemical cycles(e.g., rising CO2 and enhanced N deposition, nutrients cycling, sediments), withglobal climate change (e.g., temperature and rainfall) and land-use change[4,17,18,147,167,179,297].

14.9

Carbon Quality in Bioenergy Crops

Biomass includes cellulose, hemicelluloses, lignin, lipids, simple sugars, starch,water, hydrocarbons, ash, and other components. The concentration of each class

14.9 Carbon Quality in Bioenergy Crops 383

of compounds varies depending on the type of tissue involved, the phase of growthin which it was collected, and the conditions under which growth occurred [237].On account of its high content of structural and non-structural carbohydrates,biomass contains much more O than do fossil fuels [231,237,240]. Biomass ofdifferent origins and types has rather similar elemental composition; in general, itcontains 30–60% C, 5–6% H, 30–45% O, and small amounts of N, S, and Cl,generally accounting for less than 1% of its dry weight [237].One of the objectives of breeding and selection programs of bioenergy crops,

besides yield, is the improvement, if not the optimization [106] of biomass qualityand its conversion efficiency, and feedstock quality [125,288], as well as improvingits GHG profiles [276]. However, biofuel quality and chemical composition havenot received adequate attention given that it is an important aspect in theintroduction and use of bioenergy crops. Plant species differ in their conversionefficiency of solar energy [161]; it is about 3.7% and 2.4% for C4 and C3 plants,respectively; when factoring in WUE, CAM plants can achieve slightly higherefficiencies than C4 plants. This 60% increase in photosynthesis efficiency, iftranslated into fermentable biomass, gives C4 plants a considerable advantage overC3 plants as biofuel feedstocks [106].Biofuel quality changes due to crop-specific mineral uptake, may change with

biomass partitioning, and can drastically impact net energy output, thus limitingthe effectiveness of conversion processes and decreasing net energy value. Sincenet energy value is negatively correlated with ash content [252,292,308], the heatingvalue of the bioenergy source decreases by 0.2MJ kg�1 with every 1% increase inash concentration. The bioenergy industry demands different bioenergy crops andbiomass quality traits for different applications [106]. Specific mineral contents(e.g., low ash, N, Cl, and K) are needed in new bioenergy crops to fit this demand.Several factors determine the chemical composition of biomass, including plantspecies, plant organ and its age, growing conditions, and management practices(e.g., fertilizer and pesticide application, and harvest time and pretreatment) [231].Although genetic diversity is available in many plant species, and well

documented in the literature for biofuel yield and conversion efficiency [81], littleis documented about genetic diversity in quality-related traits of bioenergy crops.Some bioenergy crops (e.g., switchgrass, transgenic short-rotation coppice) havebeen bred or genetically modified to produce cultivars with increased biomass andfeedstock quality [89]. Lignin, a major component of the cell wall of vascular plants,has long been recognized for its negative impact on cellulosic biofuel production[289]; it accounts for about 50% of the over 1.4� 1012 kgC sequestered each year[171]. Plant species or genotypes that allocate large amounts of C to structuralcomponents, like lignin, generally have low-quality biomass for ethanol productionusing current conversion technologies [90]. Transgenic trees with reduced lignin,modified lignin, or increased cellulose and hemicellulose will improve theefficiency of feedstock conversion info biofuels and its overall quality. Highcontents of lignin and cellulose in perennial biomass are desirable when they areused as solid biofuels [327]. Genetic modification of bioenergy crops to alter thechemical composition or structure of biomass will render the conversion process


less expensive and improve biofuel yield and quality [290], while metabolicengineering will improve on content and composition of oilseed crops, and isexpected to improve biodiesel quality [193].

14.10

Life Cycle Assessment

Major challenges for harnessing agriculture’s potential contribution to biofuel andbioenergy production, while promoting soil C sequestration, are dealing with thecomplexity of the underlying processes and the spatio-temporal variability inresponse to management [135,199,255,328], global climate change, and theirinteraction [44,55,177,230]. When producing renewable bioenergy, and designingand implementing global climate change mitigation programs, it is important touse an unbiased approach to quantify C fluxes and soil organic C changes, andachieve cost efficacy [8,116,241]. Scientific and technological developments in thisarea have increased substantially in the past few years, and many of the models,such as those used in life cycle analysis, and information sources needed areavailable to practitioners [17,18,146,167]. Models provide a means of integrating theeffects of soil, climate, and management influences on GHG emissions, whiledirect measurements provide the ground truth, enable uncertainties to bedetermined in a robust approach [54,111,170,329], and avoid reaching the pointwhere “intensification of bioenergy production would turn [netpresentvalue]negative” [41,48]. The GEMIS (Global Emissions Model for Integrated Systems)model [203], for example, maintains a database for energy, material, and transportsystems, and includes the total life cycle in its calculations of impacts. The GEMISdBase covers for each process: efficiency, power, direct air pollutants, GHGemissions, solid wastes, liquid pollutants, and land use. Most life cycle analyseshighlight the need for detailed site-specific modeling of soil organic C changes andfor consequential life cycle analysis of the whole fuel cycle, including transport anduse [147].As a C tracking and accounting process [105], life cycle analysis requires a

comprehensive database covering the lifetime of a particular biofuel [203]. Thedatabase should include an accounting of all GHG emissions associated withgrowing, processing, and transporting bioenergy crops and biofuels. Also, the landcategories that will be cleared in response to increased biofuel demand and the Cstocks present in those land categories along with the rates of release of Cassociated with the land conversion should be taken into consideration. Alternativescenarios may need to be taken into consideration, such as the potential C uptakerates in those land categories if the current land-use pattern continues and thequantity of fossil fuels to be replaced by biofuels to meet the projected demand. Animportant component of the database are the bioenergy crops to be used (e.g., C3,C4 or oilseed, lignocellulosic crops, etc.), their potential biofuel yields, and thelikely rates of change in future yields, as well as the quantities of byproducts ofthese bioenergy crops and their potential uses [265,267]. In addition, it was

14.10 Life Cycle Assessment 385

suggested to revise the global warming potential equivalency factor, currently usedfor CO2 emissions from biomass combustion in life cycle analysis, from its currentvalue of 1.0 and to assign a value between 0.0 and 1.0, depending on the length ofcrop rotation of harvested biomass, include the albedo dynamics [10], and factor-inthe probability distribution in life cycle analysis modeling of GHG fluxes [179],Many bioenergy crops and feedstocks have been analyzed, using life cycle

analysis, based on their C and energy balances to determine whether a particularbioenergy system is better than conventional systems in terms of energyproduction efficiency and GHG emissions reduction [329]. Several factors affectthe magnitude of the components contributing to net GHG fluxes and N losses inbioenergy cropping systems [191,215]; these factors vary with respect to length ofthe plant life cycle, biomass or seed yields, feedstock conversion efficiencies,nutrient demand, soil C input, and N losses, among others [277]. Therefore,assessment of the GHG implications of land use and land-use change to bioenergycrops is a very complex and contentious issue. Life cycle analysis is comprehensivemethodology used to verify whether bioenergy is a reliable and sustainable meansof reducing GHG emissions [51,196,201] and mitigating global climate change[37,63,64]. Also, life cycle analysis is expected to provide an accurate evaluation ofwater and human health issues [105], besides the other environmental benefitsfrom biofuels, which continue to be controversial issues [56]. While the primaryfocus of previous life cycle analysis studies has been on the net GHG impacts ofbiofuel production, increasing attention is now being paid to adopting acomprehensive life cycle analysis inventory approach that counts for WUE [212],and water sources and quality (i.e., blue and green water), as well as for pollutioneffects, coproduct allocation, and spatial heterogeneity [213].Most life cycle analysis studies reported significant net reductions in GHG

emissions and fossil energy consumption when ethanol and biodiesel are used toreplace fossil fuels [142,188]. A few studies examined the impacts of land-usechange on local air pollution, acidification, eutrophication, and ozone depletion,and concluded that the positive impacts on GHG emissions may carry anadditional environmental cost [188]. Several life cycle analysis studies concludedthat bioenergy is the better land use option, delivering the most mitigation benefitswhere bioenergy crop growth rates are high, biomass is used efficiently, initial Cstocks are low, and the whole process is considered within a long-term perspective[142]. Land converted from first- to second-generation bioenergy crops showed anincrease in C sequestration of up to 1.1 t C ha�1 over 5 years. Other studies reportedincreases in soil C at rates of 0.2–1.0 t C ha�1 year�1 for several decades [143]. Pay-back time for grassland agroecosystems converted to sugarcane or oil palm is lessthan 10 years because these ecosystems have the lowest C reserves and the highestyielding bioenergy crops [51,188]. Although C sequestration related to land-usechange might broaden the GHG mitigation benefits of bioenergy crops beyondGHG emissions savings, the positive effects on GHG emissions may carry a cost inother environmental areas. Therefore, a much more careful analysis is needed tounderstand the trade-offs in any particular situation [142]. The wide range of thecombined direct and indirect land-use changes, estimated in g CO2eq C MJ�1,


when converted to fatty acid methyl esters of rapeseed was estimated at 117–260 inthe European Union, 45–84 for oil palm in Indonesia, and 51–100 for soybean oilin Brazil. However, when converted to ethanol it was estimated at 36–48 forsugarcane in Brazil, 72–130 for corn in the United States, and 17–34 for short-rotation coppice when used in biomass-to-liquid technology in Brazil. Theseestimates demonstrate the large variability within and among crops, agroecosys-tems, and countries, and suggested that GHG emissions from indirect land-usechange were considered more important than emissions from direct land-usechange [203].

14.11

Ecosystem Services of Carbon in Bioenergy Crops

The biofuels debate is a paradigm shift in how land should be appropriated, andhow to reconcile sustainable intensification of land use, conservation of naturalresources, and the production of ecosystem services, including food and bioenergy,among others [318]. The value of C stored in biomass or sequestered in soils wasunderestimated in the past. Carbon provides a multitude of climate regulationservices, the impact of which may change over temporal and spatial scales. As aresult of rising atmospheric [CO2], currently at around 2.2 ppm year�1, C presenteda dramatic example of the “tragedy of the commons” [207], and provided a massive“disservice” epitomized by deteriorating ecosystem services and increased globalwarming [4,160]. The current trends of increasing atmospheric [CO2], globalwarming, and climate change are expected to impact further the supply ofecosystem services that are vital for human welfare [330]. Ecosystem disservices arelikely to increase as a result of intensification of crop production for food andbioenergy, particularly in developing countries were demand for energy-intensivefood is expected to rise [5,44]. Typically [41], agroecosystems lose C faster than theyaccumulate it; this may entail deterioration or loss of attendant ecosystem services[19,69]. Multifunctional bioenergy agroecosystems [11,69,84,329], with theirdesigns consistent with ecological rules of C circulation in nature, are expected tosimultaneously provide bioenergy, arrest or reverse C loss, and protect and promotea variety of ecosystem services [5,19,31,69].Ecosystem services have been classified using several ecological, environmental,

and economic principles [31–33]; however, quantifying their levels and values hasproven difficult [297]. Ecosystem services may be predicted by simulating expectednutrient pools and fluxes [84], and their production can be modeled usingecological production functions and economic appraisal methods, where the valueof multiple ecosystem services can be quantified at a spatio-temporal scale[8,128,129,297,323]. The Millennium. Ecosystem Assessment classification [67],which became widely accepted as a framework for understanding and assessing thebenefits that ecosystems provide, organized the goods and services derived, directlyor indirectly, from C in bioenergy crops and agroecosystems into provisioning,regulating, supporting, or cultural ecosystem services. These ecosystem services,

14.11 Ecosystem Services of Carbon in Bioenergy Crops 387

from a bioenergy perspective, are interlinked and interdependent in a highly non-linear manner [5,33,67]. For agriculture, in general, and bioenergy agroecosystems,in particular, relationships between ecosystem services are typically regarded astrade-offs between provisioning and regulating services [5,297]. Although trade-offsamong different ecosystem services are regarded as inevitable, irreversible, anddiffer at spatial and temporal scales [5,33,67], little evidence of trade-offs was found,for example, between ecosystem services and biodiversity conservation; land-usescenarios that enhance biodiversity conservation also enhanced the production ofother ecosystem services [267]. However, trade-offs exist between C storage andwater quality, and between environmental improvement and financial returns [65].A conservative estimate (US$33 trillion) of the annual value of ecosystem services

globally is almost double the value of the global GNP [180]. However, monetaryvaluation of non-market ecosystem services, such as C sequestration, fossil fueldisplacement, and improvement of water quality, adds another dimension to thetrade-off picture, especially from the producers’ perspective [84]. Valuation ofecosystem services changes over time and our assumption of C sequestration, forexample, as a positive ecosystem services is a modern phenomenon made relevantby recent attention to increased atmospheric concentrations of GHG, especiallyCO2 and reactive N [84]. Until recently, ecosystem services provided by C alreadystored in ecosystems has been disregarded or undervalued [67]. Recent high-profileefforts, however, have called for integrating ecosystem services values intoimportant societal decisions [65].Maintaining, if not improving, soil fertility through C management is a vital

ecosystem services and considered by many as the essence of maintaining asustainable bioenergy agroecosystem [180,190,221,248]. Positive correlationsbetween C content in soil and soil productivity have been found for various cropsand in different bioenergy production regions [232]. Soil C storage is a vitalecosystem service, resulting from interactions of several ecological processes.Human activities affecting these processes can lead to C loss or improved storage[156]. Carbon stored on land can be lost by human action through harvest orremoval of vegetation, land-use change from forestry to short-rotation coppiceplantations, short-lived products, and land degradation, or inadvertently throughforest disturbance or soil processes [41]. Also, soil organic C and N are subject to arange of biological processes capable of generating or consuming GHGs [58].Therefore, permanence of C sequestration in soils is a central managementstrategy to ensure that C-mediated ecosystem services can be sustainably derivedfrom bioenergy crops [23]. Moreover, if markets for C sequestration emerge,payments for sequestered C may make it more profitable for landowners to chooseland use that favors C storage and sequestration [267], such as perennial-based(short-rotation coppice and short-rotation woody crops) bioenergy agroecosystemsthat require a short time to achieve C-neutrality [229] or afforestation programs thatlead to a net increase in soil organic C in forest soils despite the losses due to globalwarming [330]. Given time, the perennial nature of grasses and short-rotationcoppice and short-rotation woody crops tree species, through C sequestration indeep soil profiles, may improve soil properties, as more C is stored in their prolific


and deep root systems reduce bulk density and improve water infiltration rates intothe deeper soil profile [329].Perennial bioenergy crops (short-rotation coppice and short-rotation woody

crops) also can regulate local climate through modification of the microclimate andat the global scale through reductions in atmospheric C by sequestration [175].Several of the above-mentioned C-dependent or C-mediated ecosystem servicesdepend on modification of soil properties [329], and include positive aspects suchas soil formation, nutrient recycling, filtration and purification of runoff, andregulation of micro- and macro-climates [175,180]; the latter depend on the totalamount of C stored in the terrestrial biosphere. The net land-atmosphere C flux isdetermined by net primary productivity, and C losses due to soil heterotrophicrespiration, fire, biomass harvesting, and land-use change [330].

14.12

Eco-Physiology and Carbon Sequestration

In the next 10–30 years, yield improvements of bioenergy crops will likely beachieved through increased radiation interception and radiation-use efficiency(RUE); in the shorter term, however, yield gains will be achieved primarily byclosing the yield gap in developing countries [318]. Better light interception andhigher RUE have important roles in maximizing biomass yield; both can beimproved through quantification and modification of plant architecture [290]. Also,bioenergy crop species or cultivars can be assigned to agro-ecological zones whereRUE and WUE are potentially balanced or where irrigation water is available toachieve maximum RUE [318]. The wide range of RUE estimates for sugarcane inZambia (1.8%) and Brazil (1.4%), wheat in the United Kingdom (0.9), and corn inthe United States (0.8) reflect differences in biomass yield potential among thesecrops [318]. The difference between 1% and 2% in annual conversion efficiency ofMiscanthus, for example, translates into around 30 t ha�1 of increased biomassproduction (from 30 to 61 t ha�1) that can be attributed to better light interceptionand RUE when compared with switchgrass, which achieved only 35% of that yield[254,266]. The successful sugarcane-based biofuel industry in Brazil is attributed,in part, to higher RUE as a result of matching varieties to local soils and climateconditions, thus minimizing genotype� environment interaction [318].A model bioenergy crop plant can be viewed as a solar energy collector and

thermochemical energy system to synthesize, process, and store energy in a usableform [264]. The biomass yield of a model bioenergy crop (C ha�1 year�1) is afunction of the number of cells per unit area multiplied by the amount of C per cell.These two factors, singly or in combination, can be used to enhance biomass andbioenergy yields [181]. Numerous physiological and eco-physiological traits neededto maximize radiation interception, RUE, WUE, and NUE, and to conferenvironmental sustainability will enhance plant biomass and bioenergy productionif targeted for improvement [12,149,152,212,317]. Several eco-physiological traitscan help change thermal time sensitivity, extend the growing season, and increase

14.12 Eco-Physiology and Carbon Sequestration 389

harvestable biomass without depleting root biomass. These include, but are notlimited to, high growth rate, response to light competition, canopies with lowextinction coefficients, leaf traits for efficient light capture (including optimum leafarea index and high specific leaf area), C4 or CAM photosynthesis pathway inaddition to large WUE, long canopy duration, large capacity for C storage biomassand sequestration in the soil, and low nutrient (e.g., N and S) requirements[28,183]. Large genetic diversity is available in germplasm of perennial short-rotation coppice and lignocellulosic grasses for eco-physiological traits such as leafarea, leaf area index, and specific leaf area, branching habit, and biomasspartitioning patterns. These traits have been shown to influence clonal biomassproduction potential [70,245] and can be used to develop improved bioenergy crops.Bioenergy crops with vegetative storage organs (e.g., stems in C4 sugarcane androots in C3 sugar beet) are able to accept assimilates for storage over longer periodsthan grain crops. In addition, a longer vegetative growth phase, where feasible, orprevention of flowering extend the period of biomass accumulation [290], whereaseliminating fruit or seed production is likely to increase total biomass and mayreduce potential invasiveness in newly introduced or domesticated bioenergy crops[249,269]. However, large-scale deployment of bioenergy crops with a long growingseason and long vegetative growth phase may trigger changes in surface reflectivity,evapotranspiration, and surface roughness; such eco-physiological traits playimportant roles in regulating surface energy fluxes and the hydrologic cycle – bothaffect climate across various temporal and spatial scales [10].Enhanced photosynthesis, improved stress tolerance, and optimized metabolic

pathways, including C partitioning and allocation, are some of the grand challengesin plant physiology research with potential applications in, and impact on, biomassand bioenergy production. Biotechnological advances are expected to speed up thedevelopment of bioenergy crops with desirable attributes, such as increased yieldsand conversion efficiency, optimal growth, better WUE and NUE, and tolerance tomultiple biotic and abiotic stresses [151]. For example, genetic modificationtechnologies are central to the strategy of the US Department of Energy to deploy,within 10–15 years, bioenergy crops with optimized cell wall characteristics,enhanced yield, and higher stress tolerance [127]. The discovery of alternative Cfixation routes raises possibilities that novel pathways can be utilized to fixatmospheric CO2 into useful biochemicals as energy carriers [144]. Syntheticbiology may allow for new opportunities to completely re-engineer more efficientphotosynthesis and novel C fixation pathways [144], and, therefore, the productionof high biomass and bioenergy yields.If bioenergy crop production would be restricted in the future mostly to marginal

areas [287], then it is time to explore and develop new bioenergy crops and varietieswith higher biomass productivity and multiple abiotic stress tolerances undermarginal conditions. Increased stress tolerance in crop plants allows for marginallands to be brought into cultivation and extends the range of plant adaptation,especially for species that are temperature- or drought-limited [127]. Bioenergycrops exhibit broad climatic tolerances, which allows tremendous flexibility inselecting appropriate crops and genotypes to fit specific agro-ecological zones of the


world; however, identifying bioenergy crops capable of producing high yields onmarginal lands or degraded soils with minimal inputs to fit what was described aslow-input high-diversity [74] will be a tremendous challenge to the sustainability ofthe global bioenergy industry [249]. Rising CO2 (currently at about 393 ppm) offersthe potential to stimulate the productivity of C3, but not C4, bioenergy crops, andmay offset yield losses caused by global climate change-induced water andtemperature stress [161]; through its influence on several physiological processesand its effect on leaf area index, temperature modifies C allocation, C storage, andbiomass yield [172]. The question remains whether elevated atmospheric CO2

confers drought tolerance in bioenergy crops during periods of water stress [24]?

14.13

Climate Ethics and Carbon in Bioenergy Crops

If humanity is already living beyond sustainability, and human appropriation of netprimary productivity will increase beyond the current estimate of 130% of Earth’scapacity just to keep pace with the production of food and fibers [19], andconsidering the bioenergy production potential of global biomass plantations underenvironmental and agricultural constraints [233], then demanding an additional5 EJ from bioenergy sources by 2020 may not be realistic or feasible [232].Assuming that the global bioenergy potential could be as high as 500 EJ year�1 [52],then the recent estimates [233] of transitioning to a low-C energy economy, whilemeeting increasing future energy demands, would be attainable; however, itrequires the rapid development of a large global bioenergy sector, producingbetween 150 and 400 EJ year�1 in 2050.Significant funds have been granted to research in both public and private sector

institutions that would expand the technological capability for the production andutilization of biofuels since the year 2000. At the same time, the capacity to produceethanol from the existing first-generation crops has expanded considerably in thesame period, especially in the United States and Brazil [57,77,252]. World demandfor biofuels is on the rise because of several socio-economic factors. These includegrowing energy needs, rising oil costs, the search for clean, renewable sources ofenergy, and the desire to increase farm incomes in developed countries. On theother hand, the need for food and feed crops – such as corn and sugarcane – to beused as feedstocks for biofuel has increased significantly; the impact of suchincreased demand on the global food systems, among other sectors of the worldeconomy, has been significant [6,7,111,157,158,239,273].In the opinion of some observers [28,62], the role that biofuels will play in global

climate change adaptation is unclear and the suggestion that growing crops forbiofuel rather than food will help farmers cope with global climate change impliesthat biofuel crops would have an “unambiguous agronomic advantages over foodcrops, but the current evidence for such a case is speculative.” What is more likelyis that in a world with well-developed markets for biofuel, the production of biofuelcrops will prove more economically attractive than the production of food crops for

14.13 Climate Ethics and Carbon in Bioenergy Crops 391

some farmers who have been harmed by global climate change. Nevertheless,dedicating all US corn and soybean production to biofuels would meet only 12%and 6% of the US gasoline and biodiesel demand [19]. In the International FoodPolicy Research Institute (IFPRI) 2005–2006 Annual Report Essay “The promisesand challenges of biofuels for the poor in developing countries” (http://www.ifpri.org/pubs/), the IFPRI warned that “The biofuel option may lead to extractivefarming practices and would result in an agrarian stagnation and perpetual fooddeficits.”The growing threat of food insecurity, which was confounded by the emphasis on

biofuels in many countries, obliged many [3,9,24,157,158,239,273] to call for acritical appraisal of agronomic strategies needed to enhance and sustainproductivity while mitigating global climate change, and, among other objectives,improve biodiversity, restore water and soil quality, and improve environmentalhealth. This call was echoed by The Nuffield Council on Bioethics, an independentorganization based in the United Kingdom, who issued an advisory report onbiofuels stating, in part, that “Biofuels development should not be at the expense ofpeoples essential rights . . . should be environmentally sustainable . . . shouldcontribute to net reduction of total greenhouse gas emissions and not exacerbateglobal climate change . . . should recognize the rights of people to just reward. . . and costs and benefits of biofuels should be distributed in an equitable way”(cf. [62]). World agriculture is at a crossroads! While the number of food-insecurepeople has exceeded 1 billion, agriculture requires more land, water, chemicalfertilizers, labor and (bio)energy [158]. Even if bioenergy production becameeconomically feasible for some farmers [62] and created additional demand forcrop production, then biofuel production may increase farm income and enhancerural development [9,21,96].

14.13.1

Biofuel versus Food

The bioenergy option was proposed to combat global climate change without dueconsideration of its impact on land use and soil fertility [157,211], and the earlypolicies promoting it have overlooked the complex relationships between foodavailability, accessibility, land degradation, and social conflicts [35]. Bioenergy andfood – two interlocked provisioning ecosystem services – should have beenaddressed simultaneously and in relation to the environment on which theydepend, knowing that biofuel production from food crops is expected to increase170% by 2020 [186]. The food requirements for a growing world population andfeed required for livestock strongly influence bioenergy potentials, and only anintegrated approach would optimize food and bioenergy supplies [38]. Therefore,rigorous accounting rules need to be developed that measure the impact of biofuelson the efficiency of the global food system, GHG emissions, soil fertility, water andair quality, biodiversity, and other ecosystem services [19].In the last decade, soils dedicated to bioenergy crop production increased

markedly and further increases will compete with food production [6,38,43,158].


http://www.ifpri.org/pubs/

http://www.ifpri.org/pubs/

Therefore, managing soils for a warming Earth in a food-insecure and energy-starved world presents a challenge for farmers, scientists, politicians, and, aboveall, the human race [158]. The debate over food versus biofuel production and thecharacteristics of environmental impacts caused by the production of bothecosystem services need to be considered within a framework of the uses andinterdependencies among land, water, and fossil energy resources. It is oftenargued [158] that the current food supply is adequate for the entire global demand,but that unequal distribution leads to food shortages in parts of the world;undoubtedly, biofuels will continue to significantly impact upon food security,more so in countries threatened by global climate change and as powerfulemerging economies scramble to take control of land, through land leasing andinvestment (e.g., in Africa) in pursuit of their own food and (bio)energy security.Whether it is actual or perceived, the negative impact of biofuel production on

food prices may have tempered the enthusiasm about their potential to reduceGHG emissions and address energy security concerns [157]. In order to minimizeadverse effects on food and feed production, it was suggested that a significant partof bioenergy can be produced on marginal lands and countries of South Americaand sub-Saharan Africa where the agricultural land base can be quadrupled toaccommodate new second-generation crops [196]. Such opportunities, largely dueto land-use change possibilities and lower opportunity costs of marginal lands, mayhelp those countries transition away from subsistence farming; bioenergy cropsmay not displace food or feed crops. Nevertheless, based on current biofuelproduction technologies, it is highly unlikely that most developing countries will beable to displace any significant share of their fossil fuel consumption. The UnitedStates, Canada, and Europe, for example, could displace a small portion (around10%) of their gasoline consumption with biofuel if they allocate 30–70% of theircroplands. Such large diversion of land area for biofuel production is highlyunlikely and would result in significant increases in food prices similar to those of2008. Therefore, unless and until second-generation-based sustainable productionsystems on marginal lands [75,218,229,317] and more efficient conversiontechnologies [105,264] are developed, more productive land will be diverted forbioenergy production [49,65,74,87,217,301]. This may happen if the currenteconomic incentives remain, in which case farmers may resort to using more cropresidues and biomass from double- or mixed-cropping systems where food andbioenergy crops are grown on the same land [5,35,44]. These land use options mayhave the potential of producing biofuel without decreasing food production orclearing natural habitats [273]. However, these options may lead to unsustainablefood and bioenergy production. Retention of crop residues is essential to maintainand provide ecosystem services such as C sequestration, soil and water conserva-tion, and maintaining soil fertility and productivity [25]. Therefore, the future ofbiofuels will depend, to a large extent, on their ability to mitigate negative impactson food availability and security in developed [7,273] as well as developing countries[6,157,158].Scientific breakthroughs and productivity gains (per unit of land and unit of

time) similar to those realized during the past 50 years could free enough farmland


for second-generation crop production and, at the same time, feed a population of 9billion people in 2050 [118]. Climate-smart and integrated food/bioenergyagroecosystems, such as agroforestry, can contribute to meeting the projected(around 70%) increase in food production by 2050, while providing sustainablebioenergy and protecting the environment. Agroforestry, as a part of a multi-functional working landscape in temperate regions, has the potential to reconcileproductivity and environmental protection, and to reduce atmospheric C andprovide multiple ecosystem services by C sequestration, conservation, andsubstitution [175]. The main limitations could be land area and agronomicresources that can be allocated for bioenergy crops without compromising foodproduction [106]; potential availability of such land area is sensitive to develop-ments and balances between food supply and demand [248], which are poorlyunderstood on demographic and socio-economic grounds [8,129,131,133].Most plants converted into biofuels today are modern food crops grown in large-

scale monocultures that are more efficient at producing grains with high starch andprotein contents [19], overdependent on external inputs, and responsible for N2Oemission and N leaching [233]. In order to meet future food and (bio)energyrequirements, it will be necessary, in the first place, to improve the efficiency of Cfixation and NUE in crops [144]. Doubling crop yield on the basis of genotypicselection, although possible to achieve, is unlikely to be realized on a large scale.Crop production for food or biofuels leads to different CO2 net exchange iffertilizers are applied and when land use changes. The net CO2 exchange dependson the original C and N stocks, fertilizer application rate, climatic andenvironmental conditions, and agronomic practices, including residue manage-ment [12]. If substantiated under field conditions, independently grass-fixed N mayhave implications for cereal production that extend beyond biofuel production[290]. It may be possible to grow bioenergy crops that can sequester more C and fixN in rotation with food crops that typically deplete soils of both nutrients.

14.13.2

Biofuel versus Water

Globally, agriculture accounts on average for 70% of fresh water use, whilecontributing to massive changes in the Earth’s biogeochemical cycles [129]. Large-scale bioenergy plantations present opportunities and pose challenges to the globalwater sector; much depends on the choice of plant species, crop genotypes,biophysical and environmental condition of production sites, managementpractices, and water availability and management options [165,277,278]. Biofuelsare a rapidly growing class of water-intensive products whose production is largelyinfluenced by government policies [76,84,331] (Section 14.13). Recent sharpincreases in the production of water-intensive biofuels have raised widespreadconcerns over their environmental impact [212]; bioenergy crops can be waterdemanding to the point of compromising the natural availability of water [313]. Fullexploitation of bioenergy production potential of global biomass plantations underenvironmental and agricultural constraints will further increase the pressure on


natural ecosystems with a doubling of current land use and irrigation waterdemand [233]; if land-use change that increases evapotranspiration rates isimplemented, it can significantly influence local hydrological cycles [214]. Althoughtrade-offs exist between C storage and water quality [65], both can be affected byland-use change, and the later mainly by NO3 leaching into surface andgroundwater [84].Water consumption in biofuel production has different social and ecological

consequences depending upon the state of the resource base from which the wateris drawn [213]. Biofuel agroecosystems affect water cycling and downstream waterquality [164]. Water demand associated with bioenergy crop production on dry andmarginal lands is inextricably linked with land quality, where soil organic C playsan important role in biomass production [317]. Increased soil organic C under suchconditions improves soil water-holding capacity as well as soil biological, chemical, andphysical properties [55]. Drought-tolerant bioenergy plant species, with high WUE, canbe utilized to exploit approximately 18% of the terrestrial surface in semi-arid regionsfor biofuel production and without competing with food production [290].Adequate water supplies to produce economic and sustained crop yield is one of

the most important factors determining the biophysical capacity to produceadequate amounts of food and biofuel. The most critical factor, however, issufficient land area with suitable soil quality to support plant growth underfavorable thermal regimes [38,63,131]. Currently, the water demand of bioenergycrops is modest, but may increase due to rising energy prices, geopolitics, andconcerns over the impact of GHG emissions and expansion of biofuel production[14,14,111]. This could lead to more intensive competition between food andbiofuel for land and water resources, particularly in water-scarce or water-deficitcountries [165].Growing bioenergy crops for biofuels currently accounts for around 100 km3

(1%) of all water transpired by crops worldwide and about 44 km3 (2%) of allirrigation water withdrawals. Water availability may prove to be the limiting factorfor the establishment and growth of bioenergy crops and for biofuel production.For example, deep-rooted bioenergy crops, such as perennial grasses, short-rotationcoppice, and short-rotation woody crops, are usually more drought tolerant, capableof sequestering more C, more likely to modify the water and nutrient dynamics insoils, may negatively compete with other plant communities, and therefore impactbiodiversity [275]. Root volume and geometry of bioenergy crops (e.g., fibrousversus tap roots) play major roles in improving soil physical and hydrologicalproperties, including bulk density, water holding capacity, and infiltration rate [19];these improvements may lead to higher WUE [161].The C4 perennial grasses, intrinsically, have higher WUE, NUE, and RUE than

C3 grasses, especially under humid warm climates [249]. The WUE of C3 plants is2–3 g dry mass kg�1 water, which is 30–50% of the efficiency of C4 plants, many ofwhich may achieve 4–6 g dry mass kg�1 water [106]. For example, due to its highWUE, the C4 Miscanthus requires 100–300 l water kg�1 biomass; in comparison,WUE of corn or sorghum crops are near the upper end of this range [294], whereasCAM plants have WUE 3- and 6-fold higher than C4 and C3 plant species,


respectively [161]. Elevated, compared to ambient, [CO2] may lead to increasedabsolute plant (fine) root production; such root structure may improve waterextraction and allow better access to stored soil moisture [24]. Indirectly, this maylead to increased WUE, delayed leaf senescence, and larger leaf area index[24,225,296]; such traits are indicative of increased above- and below-groundbiomass accumulation found in bioenergy crops grown in elevated [CO2] [24]. Onthe other hand, fast-growing bioenergy crops are sensitive to drought; they may notachieve or maintain the required agronomic (or economic) thresholds necessary forsuccess as bioenergy plantations [24].Water requirements of different bioenergy crops per unit of energy produced

varies largely due to plant, environment, and management factors [165,203]. Forexample, total water requirements estimated as evapotranspiration (m3 GJ�1) forrapeseed (100–175, oil palm (46–250), soybean (143–500), sugarcane (18–35), sugarbeet (70–180), corn (100–300), wheat (40–350), sweet sorghum (56–230), andlignocellulosic bioenergy crops (11–170) reflect large differences within and amongspecies. The water footprint (m3 GJ�1) of bioenergy crops relates the energy yield ofa crop to its actual water use under actual field conditions during the growingseason, and depends on crop type, agroecosystem, and climate; it is intended tocomplement existing standards of life cycle analysis and develop appropriate Cfootprint metrics [214]. Variation in water footprint estimates for similar crop typesdepends on agroecosystem and climatic conditions. On average water footprintestimates are small (24m3GJ�1) in higher latitudes (e.g., Netherlands), medium(58–61) under continental climates (e.g., United States and Brazil), and large (143)in hot climates (e.g., Zimbabwe) [165], to meet increasing evaporative demand.These estimates are 70–400 times larger than the water footprint of primary energycarriers [96], suggesting that expanding bioenergy plantation, especially underirrigation, may lead to significant increases in water demand. Most of the waterneeded to produce biofuel crops (more than 90%) expressed as water footprint(range from 1400 to 20 000 l of water l�1 of biofuel) is used in the production of thefeedstock [323]. Ethanol’s water footprint is much smaller (50m3GJ�1) from corn,sugar beet, and sugarcane than that for biodiesel (400m3 GJ�1) from rapeseed andJatropha [203]. Similarly, when sugar beet and potato were used for ethanolproduction, their water footprints (60 and 100m3GJ�1, respectively) were betterthan that for sweet sorghum (400m3GJ�1), and water footprints estimate forsoybean and rapeseed when used to produce biodiesel (400m3GJ�1) were betterthan that for Jatropha (600m3GJ�1), although the latter is considered a drought-tolerant species [272,295]. Therefore, crops and conversion technologies (e.g.,combustion versus ethanol or biodiesel) should be selected to achieve the highestwater footprint; it is more efficient to use total biomass than a fraction of the crop(e.g., seed) for biofuel production when water is limiting [226].The spatio-temporal variations of impacts on water resources are predicted to be

accentuated by global climate change [214]; longer growing seasons are predictedfor the higher latitudes, with implications for the hydrological cycle under globalclimate change and potential effects on WUE and biomass production in theseareas [14]. Global warming, as a result of global climate change, has a critical role in


altering the water cycle where extensive bioenergy crops are being produced, suchas the Midwestern United States [14]; it may place additional stress on scarce waterresources if bioenergy crops require increased irrigation or have high water use[320]. Under future global climate change scenarios, C3 as compared to C4 treespecies are expected to have better WUE and to maintain higher photosynthesisactivity; therefore, C3 trees will be favored as bioenergy crops for large-scaleplantations [24]. Due to longevity of such plantations (around 25 years), foresight ofsuitable species to plant with reference to future global climate change is necessaryin order to minimize potential agronomic and economic losses [24]. However, thequestion remains: how, under future global climate change, the interlinked water,C, and N cycles will be influenced by extensive cultivation and production ofperennial lignocellulosic plantations, at different spatial scales [307]?

14.13.3

Biofuel versus Biodiversity

Large-scale biomass plantations often entail the destruction of large areas of naturalecosystems, thus reducing biodiversity and impacting ecosystem services of suchecosystems [217]. Competition over land for food, feed, and bioenergy productionis likely to push agricultural activities further into those semi-natural habitats withrich biodiversity and high C reserves [12]. The large-scale cultivation of bioenergycrops could become a threat to many areas that have already been fragmented anddegraded, are rich in biodiversity, and provide habitats for many endangered andendemic species [233]. Increased biofuel production will impact biodiversity andmost likely will result in habitat loss, increased and enhanced dispersion of invasivespecies, and pollution resulting from increased fertilizer and herbicide use[269,275,297]. Moreover, the future status of biodiversity will be impacted by factorssuch as extinction of genetically distinct populations, reduced effective populationsizes, and habitat uniformity due to large-scale deployment of bioenergy cropmonocultures on the landscape [275].Worldwide, direct and indirect land-use changes, including deforestation [20] and

conversion of grasslands and savannas [99] to bioenergy crops, are the greatestthreat to biodiversity. However, positive impacts on biodiversity may be achieved ifthe rate and direction of change of atmospheric composition and global climatechange can be adjusted, and if bioenergy crops and cropping systems can helpreduce GHG emissions [328]. Biodiversity loss due to land-use change reachedalarming rates in the corn belt of the United States (around 60%) [66,257] and inlow-land oil palm plantations of Southeast Asia (around 85%), as compared tonatural habitats in their respective ecosystems [186]. Deforestation and massiveland-use change for oil palm production in Southeast Asia (see Section 14.8.3) isthreatening biodiversity because oil palm plantations support much fewer speciesthan forests [35]. Although oil palm can be produced in an environmentally friendlymanner to help mitigate global climate change and preserve biodiversity, currentlyit contributes to GHG emissions, impacts local environments, and replacesimportant C sinks [226].


The development of lignocellulosic bioenergy crops and biofuel productionprocesses that use a variety of feedstocks could increase diversity in agriculturallandscapes and enhance arthropod-mediated ecosystem services [66]. On the otherhand, pollution from fertilizers and pesticides associated with large-scale deploy-ment of bioenergy crops as monocultures is anticipated to impact terrestrial andaquatic biodiversity; eutrophication caused by nutrient pollution often leads tochanges in biogenic habitats [269]. Nevertheless, perennial lignocellulosic grassesand woody plants, when properly managed, can enhance C sequestration, providehabitat, conserve biodiversity, and improve soil and water qualities, as compared toannual grain crops [164,300,313].The potential is high for some vegetatively propagated species (e.g., P. virgatum

and Miscanthus spp.) to become invasive. These plants are likely to tolerate poorsoils and grow in dense stands, compete with native species, and will have a largenegative impact on native biodiversity. Non-native species and genotypes may leadto the extinction of native species, alter the composition of ecological communities,and deprive communities of some ecosystem processes such as water filtration andnutrient cycling. In order to minimize potential invasiveness, it was suggested [269]to identify plant traits that contribute to or avoid invasiveness in potential bioenergycrops, and incorporate desirable traits such as sterility, reduced seed production,and inability to reproduce vegetatively, into germplasm of bioenergy crops. Sterilityin bioenergy crops (e.g., poplar) may deprive pollinators of a food source andnegatively reduce a valuable ecosystem services [83]. Biological control usinginsects as natural enemies is an ecosystem services that is strongly influenced bylocal landscape structure.If conflicts over land use can be minimized, then objectives of bioenergy

production and those of biodiversity conservation can be integrated [187].Recommendations [320] have been formulated to resolve such conflicts, includingpreservation of areas of significant biodiversity value, mitigation of negative effectsrelated to indirect land-use change, and promotion of agricultural practices withfewer negative impacts on biodiversity. The development of indicators usingfunctional traits of plant species and communities could complement existentbiodiversity monitoring systems [302]; thereby, the effects of alternative land useand land-use change on biodiversity can be contrasted, and those with a positiveinfluence on conservation management practices promoted. Furthermore, resultscan be generalized to similar habitats and can be assessed by relatively rapid fieldappraisals across different eco-regions.

14.14

Synthesis of Research Needs and Priorities

The 1992 UN Framework Convention on Climate Change called for stabilization ofGHG concentrations in the atmosphere at a level that would prevent dangerousanthropogenic interference with the climate system. A target less than 450 ppm ofatmospheric CO2 concentration was established to avoid serious impacts to the


environment; assuming a business-as-usual scenario and an annual increase of2.2 ppm, atmospheric concentration of CO2 will reach, and most likely, will exceedthis level in about 25 years. It is premature to conclude that bioenergy crops maynot provide an easy or direct solution to the GHG, global warming, and climatechange problems; they may contribute to it. Carbon-neutrality of bioenergy crops isa central, but debatable issue in climate change mitigation, and more research isneeded to quantify the C budget of different bioenergy crops and their respectiveconversion technologies. Direct and indirect GHG emissions from bioenergy cropsraise complex scientific issues that require careful specification of an appropriate Caccounting framework that correctly represents both the short-term cost and long-term benefits of substituting biofuel for fossil fuel. Also, the neutrality has beenchallenged on the grounds that such a characterization ignores differences intiming of C release and subsequent re-sequestration in bioenergy crops. It wasargued that treating all biomass as C-neutral could undermine legislative emission-reduction goals, encourage anthropogenic CO2 emissions, and may result innegative long-term effects on the environment.Sustainable biofuel production, as a part of biologically enhanced C sequestration

system, can play a positive role in reducing CO2 emissions, mitigating globalclimate change, enhancing environmental quality, and strengthening the globaleconomy; however, it will take tremendous research effort and science-based policyto determine how efficient C sequestration for climate change mitigation can be.Breakthroughs in C sequestration, as a developing but not fully mature field ofR&D, could expand the world’s future options for de-carbonization, and in dealingwith the GHG emissions, global warming, declining soil fertility, food security, lossof biodiversity, and bioenergy production. Carbon sequestration through biologicalcapture of CO2 and stabilization in soils is one of the major climate changemitigation approaches under consideration by public and private research centersand agencies. Dynamics of the complex processes leading to C sequestration,however, must be evaluated in the context of local soil and bioenergy cropattributes, including biogeochemical cycles and soil spatial variability.A challenging task is to develop a comprehensive methodology that can reduce

atmospheric CO2 concentration, minimize its global warming potential, andsequester it in a recalcitrant and stable form. This methodology should produce ascientifically defensible soil C sequestration accounting system that also would besuitable to the business sector, should soil C, or more precisely the right to emitCO2, become a publically traded commodity. The proper deployment and manage-ment of biomass crops can accelerate the natural rate of C sequestration (about2.0GtC year�1) and sequester several Gt year�1 beyond this rate; however, for Csequestration to be a viable option, it needs to be safe, predictable, reliable,measurable, and verifiable. Improvement in monitoring and verification ofprotocols for C sequestration in the plant–soil ecosystems and C fluxes in theatmosphere–plant–soil continuum are needed for quantitative economic and policyanalysis, whereas field-scale experiments on large-scale ecosystems will benecessary to understand both physiological and geochemical processes regulatingC sequestration and to provide proof-of-principle testing of new sequestration

14.14 Synthesis of Research Needs and Priorities 399

concepts. Future research, therefore, needs to develop specific models foremerging bioenergy crops, platforms that facilitate acquisition and sharing of high-quality field experimental data for model development and testing, and anintegrated framework for efficient execution of large-scale simulations andprocessing of input and output data.Plant roots and the changes they effect on soil biogeochemistry through the

rhizosphere are critical to the storage and stability of C in soil. When rhizospherebiota are included, the below-ground fraction of plant-derived C may far exceed theabove-ground fraction. The possibility of sequestering inorganic C, within or evenbelow the rhizosphere, is attractive because it utilizes a pathway that is comparableto soil organic C sequestration, has a high-capacity, reduces CO2 fluxes back to theatmosphere, and can have synergistic effects on both biomass production and soilorganic C stability. However, the rhizosphere-mediated effects on C sequestrationare not well understood. High metabolic activity of rhizosphere-soil microbialcommunities can be responsible for 30–50% of CO2 emissions as respiration fromsoil, depending on plant type, ecosystem, climate, and depth.The potential benefits of using perennial grasses and fast-growing trees as

bioenergy crops for cellulosic ethanol production are well established; however,uncertainties about the timing of eventual large-scale use of cellulosic convergenttechnologies for biofuel production make a strong case for further research. Theirbioenergy potential will increase as these crops and more efficient conversiontechnologies come online. Due to their longevity, the potential impact of climatevariability on the stability of C sequestered in soils and stored in perennialbioenergy crops must be evaluated. Net C benefit of these crops would be site-specific, and extensive research and database development would be needed to fullyunderstand their impact on the ecosystem C balance under different managementregimes and in different agroecological regions. In spite of this potential, their deeproots can deliver fixed C deep into the soil, and this C may activate deep soilmicrobial communities and cause increased decomposition of the stable deep soilorganic matter, thus offsetting the C sequestration benefits. Therefore, there is aneed to understand how deep-rooting plants in association with the rhizosphereaffect soil C stability and to develop appropriate management practices to achievethis objective. The net C benefit of perennial bioenergy tree crops would be site-specific; extensive research would be needed to fully understand the impact ofafforestation on ecosystem C balance under different management regimes and indifferent agroecological zones.In-depth R&D is needed on perennials with the CAM pathway to understand and

utilize the multiple molecular, physiological, and ecological processes underlyingthe unique C sequestration, high leaf content of easily fermentable non-structuralcarbohydrates, high WUE, and drought tolerance of these plants. Such research isexpected to result in jointly maximizing C sequestration and biomass productionfrom marginal and degraded lands. The substantial biomass increases underelevated CO2 on marginal lands suggest that research efforts should be directedtowards exploiting the potential of these plants as low-input sources of bioenergyand as a means of stimulating sustainable economic growth in developing


countries. However, a long-term research question regarding perennial bioenergycrops is how, under future global climate change, the interlinked water, C and Ncycles will be influenced by extensive cultivation and production of these crops, atdifferent spatial scales.The turnover time is a larger and more significant gap in our understanding of

biologically enhanced C sequestration systems than in the net production potentialof bioenergy crops; the latter varies globally by only a factor of 10, whereas theformer can vary by a factor of 1000 between the soil surface and 1m deep. About75% of the Earth’s terrestrial C is stored as labile organic C in the top 1m of soil,and there is tremendous potential to sequester additional C in this and deeper soillayers. The rapid turnover time for labile soil C makes the labile pool particularlyimportant in the response to environmental changes caused by changes in climateor land cover. However, the gaps in our knowledge of C dynamics as it getsdeposited deeper in soils prevent reliable predictions of the effect of ecosystemmanagement and global change on C dynamics in deeper soil layers and ultimatelyon the surface-to-atmospheric CO2 fluxes. It is generally accepted that even a smallchange in C input rate to subsurface soil layers, or changes in decomposition ratesof the C stored at depth, could lead to large changes in soil-to-atmosphere CO2

fluxes. If annual C fluxes into and out of soils are almost 10 times larger than fossilfuel combustion emissions, then the development of appropriate managementpractice to effect even a small change in gross CO2 fluxes from the soil will producesignificant sequestration benefits. Therefore, C stabilization in soils is a highpriority and deserves more in-depth research because it has the potential to be amuch more recalcitrant sink than C stored in plant tissues, especially in food orfiber crops. Field experimental research, when integrated with model development,will elucidate and quantify C dynamics at depth and its direct influence on surfaceCO2 fluxes.Partitioning of C between different soil pools with different turnover times is

affected by land cover; therefore, understanding and managing the consequencesof land use and land cover changes as a result of conversion to bioenergy crops,along with the attendant changes in land management, are necessary to evaluateand manage the direct and indirect effects of future expansion of biomassproduction. Degraded lands present an immediate and promising opportunity forexpanding bioenergy crop production; these lands offer a means for near-termterrestrial C sequestration because of the potential to rebuild and possibly exceedhistorical C stocks through integrated management of biological, chemical, andphysical soil components. However, there is a need for appropriate research-basedmanagement practices to prevent further land degradation and increased pressureon fragile lands and natural resources on which subsistence farmers depend. Suchpractices should enhance the interaction between C sequestration and soil fertility,and minimize the risk of C release from soil in response to changes in regionalweather patterns. The rate of C sequestration in response to management practicesis not finite in magnitude and will reach a steady state; therefore, managementpractices should be evaluated based on optimization of C sequestration, and tocombine the objectives of reduced GHG emissions and C sequestration.

14.14 Synthesis of Research Needs and Priorities 401

The recent advances in ecology and microbial biology offer promising newpossibilities for enhancing terrestrial C sequestration, such as biochar that hasbeen proposed as a new approach to C sequestration. It maintains high Cconcentrations as well as other nutrients; it is relatively stable and acts to stabilizeother organic matter in soil. Potentially, biochar represents a significant componentof a biologically enhanced C sequestration system; preliminary results indicate thatits effect on crop productivity is variable, and its mitigation potential of N2O andCH4 emissions need further research. Biochar’s chemical and physical character-istics are affected by the choice of bioenergy crop and process conditions, and itsefficacy, durability, and fate in soil are not known. Research gaps and futurechallenges include developing appropriate technologies to decipher and optimizeits agronomic and C sequestration performances, and its interaction with, andeffects on, soil biogeochemical processes, including microorganisms, cationexchange capacity, water relations, and aggregate stability. The latter protect C and,in turn, are influenced by organic C input in soil. Large-scale agronomic research toevaluate sources of biochar and the effect of its application rates, methods, andtiming on C sequestration, as well as its synergies with the biofuel life cycle andenvironmental impact, especially in developing countries, will enable biochar toplay a major role in climate change mitigation, while supporting C storage inbioenergy crops and sequestration in soil.A high C :N ratio (e.g., in wood 300 : 1) is of great value for C sequestration at a

small N cost. Research-based estimates are needed of the magnitude of N-stimulated C storage and sequestration through N fertilizer application, and itsimpact on global N and C budgets. Both the quantity and quality of C stored inbioenergy crops, with emphasis on the C :N ratio, need improvements throughselection, breeding, genetic manipulation, and field testing; breeding and selectionfor positive response to increased atmospheric CO2 concentration are challengingundertakings that can be facilitated by the use of simulation models. Geneticdiversity for agronomic, (eco)physiological, and bioenergy-related traits, especiallycell wall composition, biochemistry, and structure, need to be identified in potentialbioenergy crops. Germplasm collection, characterization, and evaluation of keyplant traits are prerequisites for strong breeding programs, and will guide breedingand genetic engineering for C capture, and biofuel and bioenergy improvements.When not available in natural germplasm, synthetic biology research may lead tolarge improvements in efficiently capturing and converting C into high biomassand bioenergy yields. Genetic correlations between yield-related traits need to beinvestigated to identify “early diagnostic” indicators of biomass and bioenergyyields and energy density.Recalcitrance of soil organic matter is attributed to biochemical (C in soil organic

compounds that resist decomposition), physical (C isolated physically fromdecomposers), and chemical (C is bound chemically with mineral surfaces of siltand clay particles) stabilization. Therefore, management practices that enhancetheir stabilization need to be developed and implemented. The relationshipbetween soil management and C and N stabilization in soil organic matter isdifferentially influenced by soil texture. The physical protection of soil organic


matter within soil aggregates is the most sensitive to disturbance and representsthe greatest opportunity for agricultural management, including tillage and residuemanagement, to affect C storage in soils. Most of the C in soil is stored in soilorganic matter and recruitment of soil organic matter is reduced when residues areremoved. However, the effect of residue removal is still being debated by manyresearchers. The impact can vary from location to location with the climate, soiltype, and crop management. This issue can be resolved through better knowledgeof how to manage biomass production, residue removal, and microbial andphysical processes that regulate soil nutrient cycling and availability. Researchcould involve feedback between soil functions, including buffering capacity fornutrients, water, C, and N, and bioenergy crop growth and production.Humanity is faced with the question of how to meet growing food, feed, and (bio)

fuel needs while contributing to the reduction of poverty and hunger. The maindrivers behind government support for biofuels in developed, but not developing,countries are concerns about climate change and energy security, and the politicalwill to support the farm sector through increased demand for agricultural products.If developing countries are to benefit from the growth of renewable bioenergyproduction and still maintain adequate levels of food security, then they need to useinnovative quantitative and analytical techniques to help assess the potentialbenefits and risks of biofuels, and to explore ways to provide income-generatingopportunities for their farmers while minimizing resource degradation andfood insecurity. Many developing countries with tropical climates have thebiophysical potential and may have a comparative advantage in growing high-density bioenergy crops; however, without the necessary productivity improve-ments where a large proportion of food crops could be used for biofuel production,aggressive growth in bioenergy crops could have adverse environmental, economic,and social effects.Continued investment in R&D by public and private sectors, coupled with

appropriate policy support mechanisms, are essential if significant C sequestration,bioenergy production, and full commercialization is to be achieved within the nextdecade. In the meantime, two questions remain to be answered: “Are we able toprovide bioenergy without the negative impacts on C emissions?” and “Is it is moresustainable to intensify low-intensity bioenergy agroecosystems or extensify thosewith high-intensity in order to optimize output of ecosystem services per unit GHGemissions?”.

14.15

Conclusions

The value of C stored in biomass or sequestered in soils was underestimated in thepast. Recently, however, C in biofuels and anthropogenic CO2 in the atmospherehave a high place on the global agenda, largely due to rising concerns about energysecurity, higher energy prices, and increasing concerns about global climatechange. Significant potential exists for producing biofuels that possess high

14.15 Conclusions 403

productivity and sustainability profiles. The combination of all biomass sourcesmay provide between 130 and 270 EJ year�1 in 2050, equivalent to 15–25% of theworld’s future energy demand. Bioenergy crops account for 20–60% of the totalpotential depending on land availability and share of irrigated land. Globalwarming will certainly affect the C and N cycles, but the direction of the effect isunclear and will vary from place to place. Understanding the possible changes inthese cycles is complicated by the feedbacks that exist between them. If theavailability of reactive N in soils increases, not only N cycling and N trace gasemissions, but also the C cycle and, thus, the biosphere–atmosphere CO2 and CH4

exchange are affected. The current debates on the relationships between bioenergycrops and GHG emissions, and bioenergy development and rural development,attest to the uncertainties in the future development of bioenergy. The recentundesirable experiences on food availability and accessibility, forest degradation,and social conflicts attest to these complex relationships. This debate is a paradigmshift in how we evaluate the human appropriation of natural resources, includingland use. Sustainable intensification of land use will only become possible when allissues across all forms of production, including food, energy and materials arereconciled. Maintaining soil fertility – under food, feed, or biofuel crops – is theessence of maintaining a sustainable system; a better understanding and morepractical attention to nutrient cycles is mandatory. Sustainable biofuel productionsystems could play a highly positive role in mitigating climate change, financingenvironmental quality, and strengthening the global economy, but it will takesound, science-based policy and additional research efforts to make this happen.Sequestering C through biological capture of CO2 and stabilization in soils has

been a major climate change mitigation approach under consideration by publicand private research agencies. Carbon cycles continuously through the atmosphere,oceans, plants, animals, soils, and rocks; its main atmospheric form, CO2, besidesits central role as input in photosynthesis and production of biomass, is animportant GHG. There is a growing recognition by the general public that therelationships between agriculture, food, feed, bioenergy, and global climate change– with C as a common component – have to be better understood. Thisunderstanding is necessary in order to gain more realistic estimates of futurebioenergy potentials and their role in mitigating global climate change. Biomass, asa renewable energy source, has been considered as C-neutral (i.e., its use as energysource will not add to the atmosphere more CO2 than what it takes). Biomass andbioenergy supply and demand have direct effects on rural livelihood and employ-ment, food availability and accessibility, freshwater supplies, and lifestyle changes.Conventional grain and oilseed crops and their residues have been used asbioenergy sources. However, the production of bioenergy from these crops mayimpact food and feed production. Other crops that can capture atmospheric CO2

more efficiently are being developed as sources of biofuel, including perennialgrasses, new oilseed crops, and fast-growing trees that are more efficient thanconventional grain or oilseed crops in producing biomass for bioenergy. Theamount of biofuel that can be produced globally in an environmentally andeconomically responsible way is limited.


Available land, adequate water, and fertilizer supplies to grow bioenergy crops aremajor constraints. In addition, new management practices and technologies areneeded to improve energy yield of the new bioenergy crops and to minimize theirenvironmental impact. Sustainable biofuel production systems could play a highlypositive role in mitigating climate change, financing environmental quality, andstrengthening the global economy, but it will take sound, science-based policy andadditional research efforts to make this happen. More importantly, biofuelsdevelopment should not be at the expense of people’s essential rights, should beenvironmentally sustainable, should contribute to net reduction of total GHGemissions and not exacerbate global climate change, should recognize the rights ofpeople to just reward, and the costs and benefits of biofuels should be distributedin an equitable way.

Acknowledgments

This research was funded by USDA-ARS project no. 3645-61600-001-00D, Morris,MN. The use of trade, firm, or corporation names in this publication is for theinformation and convenience of the reader. Such use does not constitute an officialendorsement or approval by the US Department of Agriculture (USDA) or theAgricultural Research Service of any product or service to the exclusion of othersthat may be suitable. USDA is an equal provider and employer.

References

1 Cherubini, F., Peters, G.P., Berntsen, T.,Strømman, A.H., and Hertwich, E. (2011)CO2 emissions from biomass combustionfor bioenergy: atmospheric decay andcontribution to global warming. GCBBioenergy, 3, 413–426.

2 Janssson, C., Wullschleger, S.D., Kalluri,U.C., and Tuskan, G.A. (2010)Phytosequestration: carbonbiosequestration by plants and theprospects of genetic engineering.BioScience, 60, 685–696.

3 Lal, R. (2010) Managing soils for awarming earth in a food-insecure andenergy-starved world. J. Plant Nutr. SoilSci., 173, 4–15.

4 Huber, S.C. (2011) Grand challenges inplant physiology: the underpinning oftranslational research. Front. Plant Sci.,2, 48.

5 Bogdanski, A. (2012) Integratedfood–energy systems for climate-smartagriculture. Agric. Food Sec., 1, 9.

6 Erb, K.-H., Haberl, H., and Plutzar, C.(2012) Dependency of global primarybioenergy crop potential in 2050 on foodsystems, yields, biodiversity conservationand political stability. Energy Policy,47, 260–269.

7 Karp, A. and Richter, G.M. (2011) Meetingthe challenge of food and energy security.J. Exp. Bot., 62, 3263–3271.

8 Pimentel, D., Marklein, A., Toth, M.A.,Karpoff, M.N., Paul, G.S. et al. (2009) Foodversus biofuels: environmental andeconomic costs.Hum. Ecol., 37, 1–12.

9 Sage, C. (2013) The interconnectedchallenges for food security from a foodregimes perspective: energy, climate andmalconsumption. J. Rural Stud., 28, 71–80.

10 Bright, R.M., Cherubini, F., andStromman, A.H. (2012) Climate impacts ofbioenergy: inclusion of carbon cycle andalbedo dynamics in life cycle impactassessment. Environ. Impact Assess. Rev.,37, 2–11.

References 405

11 Davis, S.C., Parton, W.J., Dohleman, F.G.,Smith, C.M., Del Grosso, S.J. et al. (2010)Comparative biogeochemical cycles ofbioenergy crops reveal nitrogen-fixationand low greenhouse gas emissions in aMiscanthus� giganteus agro-ecosystem.Ecostystems, 31, 144–156.

12 Erisman, J.W., van Grinsven, H., Leip, A.,Mosier, A., and Bleeker, A. (2010) Nitrogenand biofuels, an overview of the currentstate of knowledge. Nutr. Cycle Agroecosyst.,86, 211–223.

13 Parry, M.L., Canziani, O.F., Palutikof, J.P.,van der Linden, P.J., and Hanson, C.E.(2007) Climate Change (2007) Impacts,Adaptation and Vulnerability. Contributionof Working Group II to the Fourth AssessmentReport of the Intergovernmental Panel onClimate Change, Cambridge UniversityPress, Cambridge.

14 Le, P.V.V., Kumar, P., and Drewry, D.T.(2011) Implications for the hydrologiccycle under climate change due to theexpansion of bioenergy crops in theMidwestern United States. Proc. Natl.Acad. Sci. USA, 10, 15085–15090.

15 Thelen, K.D., Gao, J., Hoben, J., Qian, L.,Saffron, C., and Withers, K. (2012) Aspreadsheet-based model for teaching theagronomic, economic, and environmentalaspects of bioenergy cropping systems.Comput. Electron. Agric., 85, 157–163.

16 Wu, M., Demissie, Y., and Yan, E. (2012)Simulated impact of future biofuelproduction on water quality and watercycle dynamics in the upperMississippi river basin. Biomass Bioenergy,41, 44–56.

17 Gopalakrishnan, G., Negri, M.C., andSalas, W. (2012) Modeling biogeochemicalimpacts of bioenergy buffers withperennial grasses for row-crop field inIllinois. GCB Bioenergy, 4, 739–750.

18 Huang, Y., Yu, Y., Zhang, W., Sun, W., Liu,S. et al. (2009) Agro-C: a biogeophysicalmodel for simulating the carbon budget ofagroecosystems. Agric. Forest. Meteol.,149, 106–129.

19 Gomiero, T., Paoletti, M.G., and Pimentel,D. (2010) Biofuels: efficiency, ethics, andlimits to human appropriation ofecosystem services. J. Agric. Environ. Ethics,23, 403–434.

20 Obidzinski, K., Andriani, R., Komarudin,H., and Andrianto, A. (2012)Environmental and social impacts of oilpalm plantations and their implications forbiofuel production in Indonesia. Ecol. Soc.,17, 25.

21 Walker, R.V. and Beck, M.B. (2012)Understanding the metabolism ofurban–rural ecosystems.Urban Ecosyst.,15, 809–849.

22 Cucek, L., Klemes, J.J., and Kravanja, Z.(2012) Carbon and nitrogen trade-offs inbiomass energy production. Clean Technol.Environ. Policy, 14, 389–297.

23 Budzianowski, W.M. (2012) Value-addedcarbon management technologies for lowCO2 intensive carbon-based energyvectors. Energy, 41, 280–229.

24 Oliver, R.J., Finch, J.W., and Tylor, G.(2009) Second generation bioenergy cropsand climate change: a review of the effectsof elevated atmospheric CO2 and droughton water use and the implications for yield.GCB Bioenergy, 1, 97–114.

25 Lal, R. (2005) World crop residuesproduction and implications of its use as abiofuel. Environ. Int., 31, 575–584.

26 Lal, R. (2007) Soil science and thecarbon civilization. Soil Sci. Soc. Am. J.,71, 1425–1437.

27 Lal, R. (2008a) Sequestration ofatmospheric CO2 in global carbon pools.Energy Environ. Sci., 1, 86–100.

28 Lal, R. (2008b) Carbon sequestration.Philos. Trans. R. Soc. Lond. B, 363,815–830.

29 Kotchoni, S.O. and Gachomo, E.W. (2008)Biofuels production: a promisingalternative energy for environmentalcleanup and fuelling through renewableresources. J. Biol. Sci., 8, 693–701.

30 Petersen, J.-E. (2008) Energy productionwith agricultural biomass: environmentalimplications and analytical challenges. Eur.Rev. Agric. Econ., 35, 385–408.

31 Oja, E., Martin-Ortega, J., and Chiabai, A.(2012) Defining and classifying ecosystemservices for economic valuation: the case offorest water service. Environ. Sci. Policy,19–20, 1–15.

32 Wallace, K.J. (2007) Classification ofecosystem services: problems andsolutions. Biol. Conserv., 139, 235–246.


33 Fisher, B., Turner, R.K., and Morling, P.(2009) Defining and classifying ecosystemservices for decision making. Ecol. Econ.,68, 643–653.

34 Chaudhary, D.R., Saxena, J., Lorenz, N.,and Dick, R.P. (2012) Distribution ofrecently fixed photosynthate in aswitchgrass plant–soil system. Plant SoilEnviron., 58, 249–255.

35 Acosta-Michlik, L., Lucht, W., Bondeau, A.,and Beringer, T. (2011) Integratedassessment of sustainability trade-offs andpathways for global bioenergy production:framing a novel hybrid approach. Renew.Sustain. Energy Rev., 51, 2791–2809.

36 Brand~ao, M., Levasseur, A., Kirschbaum,M.U.F., Weidema, B.P., Cowie, A.L. et al.(2012) Key issues and options inaccounting for carbon sequestration andtemporary storage in life cycle assessmentand carbon footprinting. Int. J. Life CycleAssess., 18, 230–240.

37 Rootz�en, J.M., Berndes, G., Ravindranath,N.H., Somashekar, H.I., Murthy, I.K. et al.(2010) Carbon sequestration versusbioenergy: a case study from South Indiaexploring the relative land-use efficiency oftwo options for climate change mitigation.Biomass Bioenergy, 34, 116–123.

38 Haberl, H., Erb, K., Krausmann, F.,Bondeau, A., Lauk, C. et al. (2011)Global bioenergy potentials fromagricultural land in 2050: sensitivity toclimate change, diets and yields. BiomassBioenergy, 35, 4753–4769.

39 Hastings, A., Clifton-Brown, J.,Wattenbach, M., Mitchell, C.P., Stampfl,P., and Smith, P. (2009) Future energypotential ofMiscanthus in Europe. GCBBioenergy, 2, 180–196.

40 Beringer, T., Lucht, W., and Schaphoff, S.(2011) Bioenergy production potential ofglobal biomass plantations underenvironmental and agriculturalconstraints. GCB Bioenergy, 3, 299–312.

41 Bottcher, H., Freibauer, A., Scholz, Y.,Ciais, P., Mund, M. et al. (2012) Settingpriorities for land management to mitigateclimate change. Carbon Balance Manag.,7, 5.

42 DeCicco, J.M. (2012) Biofuels andcarbon management. Climate Change,111, 627–640.

43 Haberl, H., Beringer, T., Bhattacharya,S.C., Erb, K.-H., and Hoogwijk, M. (2010)The global technical potential of bio-energyin 2050 considering sustainabilityconstraints. Curr. Opin. Environ. Sustain.,2, 394–403.

44 Smith, P., Davies, C.A., Ogle, S., Zanchi,G., Bellarby, J. et al. (2012) Towards anintegrated global framework to assess theimpacts of land use and managementchange on soil carbon: current capabilityand future vision. Global Change Biol.,18, 2089–2101.

45 Dale, V.H., Lowrance, R., Mulholland, P.,and Robertson, G.P. (2010) Bioenergysustainability at the regional scale. Ecol.Soc., 15, 23.

46 McBride, A.C., Dale, V.H., Baskaran, L.M.,Downing, M.E., Eaton, L.M. et al. (2011)Indicators to support environmentalsustainability of bioenergy systems. Ecol.Indicat., 11, 1277–1289.

47 Effroymson, R.A., Dale, V.H., Kline, K.L.,McBride, A.C., Bielicki, J.M. et al. (2012)Environmental indicators of biofuelsustainability: what about context? Environ.Manag., 51, 291–306.

48 Popp, A., Lotze-Campen, H., Leimbach,M., Knopf, B., Beringer, T. et al. (2011) Onsustainability of bioenergy production:integrating co-emissions from agriculturalintensification. Biomass Bioenergy,35, 4770–4780.

49 Don, A., Osborne, B., Hastings, A., Skiba,U., Carter, M.S. et al. (2011) Land-usechange to bioenergy production in Europe:implications for the greenhouse gasbalance and soil carbon. GCB Bioenergy,4, 372–391.

50 Ziegler, A.D., Phelps, J., Yuen, J.Q., Webb,E.L., Lawrence, D et al. (2012) Carbonoutcomes of major land-cover transitionsin SE Asia: great uncertainties andREDDþ policy implications. Global ChangeBiol., 18, 3087–3099.

51 Berndes, G., Hoogwijk, M., and van denBroek, R. (2003) The contribution ofbiomass in the future global energy supply:a review of 17 studies. Biomass Bioenergy,25, 1–28.

52 Haberl, H., Sprinz, D., Bonazountas, M.,Cocco, P., Desaubies, Y. et al. (2012)Correcting a fundamental error in

References 407

greenhouse gas accounting related tobioenergy. Energy Policy, 45, 18–23.

53 Alexandrov, G. and Matsunaga, T. (2008)Normative productivity of the globalvegetation. Carbon Balance Manag., 3, 8.

54 Malins, C. (2012) A model-basedquantitative assessment of the carbonbenefits of introducing iLUC factors in theEuropean renewable energy directive. GCBBioenergy, doi: 10.1111/j.1757-1707.2012.01207.x.

55 Baldock, J.A., Wheeler, I., McKenzie, N.,and McBratney, A. (2012) Soils and climatechange: potential impacts on carbon stocksand greenhouse gas emissions, and futureresearch for Australian agriculture. CropPasture Sci., 63, 269–283.

56 Benoist, A., Dron, D., and Zoughaib, A.(2012) Origins of the debate on the life-cycle greenhouse gas emissions andenergy consumption of first-generationbiofuels – a sensitivity analysis approach.Biomass Bioenergy, 40, 133–142.

57 Davis, S.C., Parton, W.J., Del Grosso, S.J.,Keough, C., Marx, E. et al. (2011) Impact ofsecond-generation biofuel agriculture ongreenhouse-gas emissions in the corn-growing regions of the US. Front. Ecol.Environ., 10, 69–74.

58 Drewer, J., Finch, J.W., Lloyd, C.R., Baggs,E., and Skiba, U. (2011) How do soilemissions of N2O, CH4, and CO2 fromperennial bioenergy crops differ fromarable annual crops? GCB Bioenergy,4, 408–419.

59 Khatiwada, D., Seabra, J., Silveira, S., andWalter, A. (2012) Accounting greenhousegas emissions in the lifecycle of Braziliansugarcane bioethanol: methodologicalreferences in European and Americanregulations. Energy Policy, 47, 384–397.

60 Meenakshi, K., Mohren, G.M., andDadhwal, V.K. (2010) Carbon storageversus fossil fuel substitution: a climatechange mitigation option for two differentland use categories based on short andlong rotation forestry in India.Mitig.Adapt. Strat. Global Change, 15,395–409.

61 Popp, A., Dietrich, J.P., Lotze-Campen, H.,Klein, D., Bauer, N. et al. (2011) Theeconomic potential of bioenergy forclimate change mitigation with special

attention given to implications for the landsystem. Environ. Res. Lett., 6, 034017.

62 Thompson, P.B. (2012) The agriculturalethics of biofuels: climate ethics andmitigation arguments. Poiesis Prax,8, 169–189.

63 Thomson, A.M., Calvin, K.V., Chini, L.P.,Hurtt, G., Edmonds, J.A. et al. (2010)Climate mitigation and the future oftropical landscapes. Proc. Natl. Acad. Sci.USA, 107, 9633–1963.

64 Smith, P., Olesen, J.E., Eitzinger, J.,Orlandini, S., and Stefanski, R. (2010)Synergies between the mitigation of, andadaptation to, climate change inagriculture. J. Agric. Sci., 148, 543–552.

65 Goldstein, J., Caldarone, G., Duarte, T.,Ennaanay, D., Hannahs, N., Mendoza, G.et al. (2012) Integrating ecosystem-servicetradeoffs into land-use decisions. Proc.Natl. Acad. Sci. USA, 109, 7565–7570.

66 Landis, DA., Gardiner, MM., Werf, W., andSwinton, SM. (2008) Increasing corn forbiofuel production reduces biocontrolservices in agricultural landscapes. Proc.Natl. Acad. Sci. USA, 105, 20552–20557.

67 Millennium Ecosystem Assessment (2005)Ecosystems and Human Well-Being: CurrentState and Trends, Island Press, Washington,DC.

68 Kell, D.B. (2012) Large-scale sequestrationof atmospheric carbon via plant roots innatural and agricultural ecosystems: whyand how. Philos. Trans. R. Soc. Lond. B,367, 1589–1597.

69 Stringer, L.C., Dougill, A.J., Thomas, A.D.,Spracklen, D.V., Chesterman, S. et al.(2012) Challenges and opportunities inlinking carbon sequestration, livelihoodsand ecosystem service provision indrylands. Environ. Sci. Policy, 19–20,121–135.

70 Tharakan, P.J., Robinson, D.J.,Abrahamson, L.P., and Nowak, C.A. (2001)Multivariate approach for integratedevaluation of clonal biomass productionpotential. Biomass Bioenergy, 21, 237–247.

71 Karp, A. and Shield, I. (2008) Bioenergyfrom plants and the sustainable yieldchallenge. New Phytol., 179, 15–32.

72 Gonz�alez-García, S., Gasol, C.M.,Gabarrell, X., Rieradevall, J., Moreira, M.T.,and Feijoo, G. (2009) Environmental


aspects of ethanol-based fuels fromBrassica carinata: a case study of secondgeneration ethanol. Renew. Sustain. EnergyRev., 13, 2613–2620.

73 Arevalo, C.B.M., Bhatti, J.S., Chang, S.X.,and Sidders, D. (2011) Land-use changeeffects on ecosystem carbon balance: fromagricultural to hybrid poplar plantation.Agric. Ecosyst. Environ., 141, 342–349.

74 Cai, X., Zhang, X., and Wang, D. (2011)Land availability for biofuel production.Environ. Sci. Technol., 45, 334–339.

75 Fahd, S., Fiorentino, G., Mellino, S., andUlgiati, S. (2012) Cropping bioenergy andbiomaterials in marginal lands. The addedvalue of the biorefinery concept. Energy,37, 79–93.

76 Havlík, P., Schneider, U.A., Schmid, E.,Bottcher, H., Fritz, S. et al. (2011) Globalland-use implications of first and secondgeneration biofuel targets. Energy Policy,39, 5690–5702.

77 Nass, L.L., Pereira, P.A.A., and Ellis, D.(2007) Biofuels in Brazil: an overview. CropSci., 47, 2228–2237.

78 Hu, Z., Sykes, R., Davis, M.F., Brummer,E.C., and Ragauskas, A.J. (2010) Chemicalprofiles of switchgrass. Bioresour. Technol.,101, 3253–3257.

79 Johnson, M.-V., Kiniry, J.R., Sanchez, H.,Polley, H.W., and Fay, P.A. (2010)Comparing biomass yields of low-inputhigh-dversity communities with managedmonocultures across the Central UnitedStates. Bioenergy Res., 3, 353–361.

80 Jaradat, A.A. (2010) Genetic resources ofenergy crops: biological systems tocombat climate change. Aust. J. Crop Sci.,4, 309–323.

81 Eisenbies, M.H., Vance, E.D., Aust, W.M.,and Seiler, J.R. (2009) Intensive utilizationof harvest residues in Southern PinePlantations: quantities available andimplications for nutrient budgets andsustainable site productivity. Bioenergy Res.,2, 90–98.

82 Ferre, C., Leip, A., Matteucci, G., Previtali,F., and Seufert, G. (2005) Impact of 40years poplar cultivation on soil carbonstocks and greenhouse gas fluxes.Biogeosci. Discuss., 2, 897–931.

83 Chamberlain, J.F. and Miller, S.A. (2012)Policy incentives for switchgrass

production using valuation ofnon-market ecosystem services. EnergyPolicy, 48, 526–536.

84 Cherubini, F. and Jungmeier, G. (2010)LCA of a biorefinery concept producingbioethanol, bioenergy, and chemicalsfrom switchgrass. Int. J. Life Cycle Assess.,15, 53–66.

85 Follett, R.F., Vogel, K.P., Varvel, G.E.,Mitchell, R.B., and Kimble, J. (2012) Soilcarbon sequestration by switchgrass andno-till maize grown for bioenergy.Bioenergy Res., 5, 866–875.

86 Gelfand, I., Zenone, T., Jasrotia, P., Chen,J., and Hamilton, S. (2010) Carbon debt ofconservation reserve program (CRP)grasslands converted to bioenergyproduction. Proc. Natl. Acad. Sci. USA,108, 13864–13869.

87 Geotto, E. (2008) Grasslands for bioenergyproduction: a review. Agron. Sustain. Dev.,28, 47–55.

88 Hartman, J.C., Nippert, J.B., Orozco, R.A.,and Springer, C.J. (2011) Potentialecological impacts of switchgrass (Panicumvirgatum L.) biofuel cultivation in theCentral Great Plains, USA. BiomassBioenergy, 35, 3415–3421.

89 Hinchee, M., Rottmann, W., Mullinax, L.,Zhang, C., Chang, S. et al. (2009) Short-term woody crops for bioenergy andbiofuels applications. In Vitro Cell. Dev.Biol., 45, 619–629.

90 Johnson, E. and Tschudi, D. (2012)Baseline effects on carbon footprints ofbiofuels: the case of wood. Environ. ImpactAssess. Rev., 37, 12–17.

91 Niki�ema, P., Rothstein, D.E., and Miller,R.O. (2012) Initial greenhouse gasemissions and nitrogen leaching lossesassociated with converting pastureland toshort-rotation woody bioenergy crops innorthern Michigan, USA. BiomassBioenergy, 39, 413–426.

92 Rockwood, D.L., Rudie, A.W., Ralph, S.A.,Zhu, J.Y., and Winandy, J.E. (2008) Energyproduct option for Eucalyptus speciesgrown as short rotation woody crops. Int. J.Mol. Sci., 9, 1361–1378.

93 Tuscan, G.A., DiFazio, S., and Jansson, S.(2006) The genome of black cottonwood,Poplus trichcarpa (Torr & Gray). Science,313, 1596–1604.

References 409

94 Abdullah, A.Z., Salamatinia, B.,Mootabadi, H., and Bhatia, S. (2009)Current status and policies on biodieselindustry in Malaysia as the world’s leadingproducer of palm oil. Energy Policy,37, 5440–5448.

95 Achten, W.M.J., Almeida, J., Fobelets, V.,Bolle, E., Mathijs, E. et al. (2010) Life cycleassessment of Jatropha biodiesel astransportation fuel in rural India. Appl.Energ., 87, 3652–3660.

96 Gm€under, S., Singh, R., Pfister, S.,Adheloya, A., and Zah, R. (2012)Environmental impacts of Jatropha crucasbiodiesel in India. J. Biomed. Biotechnol.,doi: 10.1155/2012/623070.

97 Odeh, I.O.A., Tan, D.K.Y., and Ancev, T.(2011) Potential suitability and viability ofselected biodiesel crops in Australianmarginal agricultural lands undercurrent and future climates. Bioenergy Res.,4, 165–179.

98 Schmidt, J.H. (2010) Comparative life cycleassessment of rapeseed oil and palm oil.Int. J. Life Cycle Assess., 15, 183–197.

99 Smith, D., Townsend, T., Choy, A., Hardy,I., and Sjogersten, S. (2012) Short-term soilcarbon sink potential of oil palmplantations. GCB Bioenergy, 4, 588–596.

100 Zhang, M. and Malhi, S.S. (2010)Perspectives of oilseed rape as a bioenergycrop. Biofuels, 1, 621–630.

101 Patthanaissaranukool, W. and Polprasert,C. (2011) Carbon mobilization in oil palmplantation and milling based on a carbon-balanced model – a case study in Thailand.Environ. Asia, 4, 17–26.

102 Chhetri, A.B., Tango, M.S., Budge, S.M.,and Watts, K.C., and Rafiqul Islam, M.(2008) Non-edible plant oils as new sourcesfor biodiesel production. Int. J. Mol. Sci.,9, 169–180.

103 Milazzo, M.F., Spina, F., Vinci, A., Espro,C., and Bart, J.C.J. (2013) Brassicabiodiesel: past, present and future. Renew.Sustain. Energy Rev., 18, 350–389.

104 Borrion, A.L., McManus, M.C., andHammond, G.P. (2012) Environmental lifecycle assessment of lignocellulosicconversion to ethanol: a review. Renew.Sustain. Energy Rev., 16, 4638–4650.

105 Byrt, C.S., Grof, C.P.L., and Furbank, R.T.(2011) C4 plants as biofuel feedstocks:

optimizing biomass production andfeedstock quality from a lignocellulosicperspective. J. Intergr. Plant Biol., 53,120–135.

106 Mabee, W.E., McFarlane, P.N., andSaddler, J.N. (2011) Biomass availability forlignocellulosic ethanol production. BiomassBioenergy, 35, 4519–4529.

107 Roy, P., Tokuyasu, K., Orikasa, T.,Nakamura, N., and Shiina, T. (2012) Areview of life cycle assessment (LCA) ofbioethanol from lignocellulosic biomass.Japan Agric. Res. Quart., 46, 41–57.

108 Sang, T. (2011) Toward the domesticationof lignocellulosic energy crops: learningfrom food crop domestication. J. Intergr.Plant Biol., 53, 96–104.

109 Sultana, A. and Kumar, A. (2011)Development of energy and emissionparameters for dandified form oflignocellulosic biomass. Energy, 36,2716–2732.

110 Brereton, N.J.B., Pitre, F.E., Hanley, S.J.,Ray, M.J., Karp, A., and Murphy, R.J.(2010) Quantitative trait loci mapping ofenzymatic saccharification in shortrotation coppice willow and itsindependence from biomass yield.Bioenergy Res., 3, 251–261.

111 Langeveld, H., Quist-Wessel, F.,Dimitriou, I., Aronsson, P., Baum, C. et al.(2012) Assessing environmental impacts ofshort rotation coppice (SRC) expansion:model definition and preliminary results.Bioenergy Res., 5, 621–635.

112 Weih, M. and Dimitriou, I. (2012)Environmental impacts of short rotationcoppice (SRC) grown for biomass onagricultural land. Bioenergy Res.,5, 535–536.

113 Grogan, P. and Matthews, R. (2009) Amodelling analysis of the potential for soilcarbon sequestration under short rotationcoppice willow bioenergy plantations. SoilUse Manag., 18, 175–183.

114 Matthews, R.B., Grogan, P., Bullard, M.J.,Christian, D.G., Knight, J.D. et al. (2001)Potential C-sequestration rates undershort-rotation coppiced willow andMiscanthus biomass crops: a modelingstudy. Aspects. Appl. Biol., 65, 303–312.

115 Copeland, J.E., Hardcastle, P.D., Booth, E.,Green, M., Karp, A. et al. (2008)


Environmental impacts of short rotationforestry. Aspects Appl. Biol., 90, 311–316.

116 Bouton, J.H. (2007) Molecular breeding ofswitchgrass for use as a biofuel crop. Curr.Opin. Genet. Dev., 17, 553–558.

117 Rae, A.M., Street, N.R., Robenson, K.M.,Harris, N., and Taylor, G. (2009) Five QTLhotspots for yield in short rotation coppicebioenergy poplar: the poplar biomass loci.BMC Plant Biol., 9, 23.

118 Baenziger, P.S., Russell, W.K., Graef, G.L.,and Campbell, B.T. (2006) Improving lives:50 years of crop breeding, genetics andcytology. Crop Sci., 46, 2230–2244.

119 Bouton, J.H. (2007) Molecular breeding ofswitchgrass for use as a biofuel crop. Curr.Opin. Genet. Dev., 17, 553–558.

120 Finckh, M.R. (2008) Integration ofbreeding and technology intodiversification strategies for disease controlin modern agriculture. Eur. J. Plant Pathol.,121, 399–409.

121 Lee, M. (1999) Genome projects and genepools: new germplasm for plant breeding.Proc. Natl. Acad. Sci. USA, 95, 2001–2004.

122 Jaradat, A.A. and Shahid, M. (2012) Thedwarf saltwort (Salicornia biglovii Torr.):evaluation of breeding populations. ISRNAgron., doi: 10.5402/2012/151537.

123 Johnson, T.S., Eswaran, N., and Sujatha,M. (2011) Molecular approaches toimprovement of Jatropha crucas L. as asustainable energy crop. Plant Cell Rep.,30, 1573–1591.

124 Bush, D.R. (2007) Translational genomicsfor bioenergy production: there’s roomfor more than one model. Plant Cell,19, 2971–2973.

125 Grattapaglia, D., Plomino, C., Kirst, M.,and Sederoff, RR. (2009) Genomics ofgrowth in forest trees. Curr. Opin. PlantBiol., 12, 148–156.

126 Sanderson, M.A. and Adler, P.R. (2008)Perennial forages as second generationbioenergy crops. Int. J. Mol. Sci., 9,768–788.

127 Chapotin, S.M. and Wolt, J.D. (2007)Genetically modified crops for thebioeconomy: meeting public andregulatory expectations. Transgenic Res.,16, 675–688.

128 Hallam, A., Anderson, I.C., and Buxton, D.R. (2001) Comparative economic analysis

of perennial, annual, and intercrops forbiomass production. Biomass Bioenergy,21, 407–424.

129 Ridley, C.E., Clark, C.M., LeDuc, S.D.,Bierwagen, B.G., Lin, B.B. et al. (2012)Biofuels: network analysis of the literaturereveals key environmental and economicunknowns. Environ. Sci. Technol., 46,1309–1315.

130 St€urmer, B., Schmidt, J., Schmidt, E., andSinball, F. (2013) Implications ofagricultural bioenergy crop production in aland constrained economy- the example ofAustria. Land Use Policy, 30, 570–581.

131 Bryan, B.A., King, D., and Wang, E. (2010)Biofuels agriculture: landscape-scale trade-offs between fuel, economics, carbon,energy, food, and fiber. GCB Bioenergy,2, 330–345.

132 Field, C.B., Campbell, J.E., and Lobell, D.B.(2008) Biomass energy: the scale of thepotential resource. Trends Ecol. Evol.,23, 65–72.

133 Majdalawi, M.I., El-Habbab, M.S.H.,Karablieh, E.K., and Alassaf, A. (2012)Economic and socioeconomics impact ofbiofuel production in the Arab Region. Afr.J. Agric. Res., 7, 2114–2123.

134 Tan, R.R., Aviso, K.B., Barilea, I.U.,Culaba, A.B., and Cruz, J.B. Jr. (2012) Afuzzy multi-regional input-outputoptimization model for biomassproduction and trade under resourcesand footprint constraints. Appl. Energ.,90, 154–160.

135 Frossard, E., B€unemann, E.K., Jansa, J.,Oberson, A., and Feller, C. (2009) Conceptsand practices of nutrient management inagroecosystems: Can we draw lessonsfrom history to design future sustainableagricultural production systems? DieBodenkultur, 60, 43–60.

136 Muller, A. (2009) Sustainable agricultureand the production of biomass for energyuse. Climate Change, 94, 319–331.

137 Tsao, C., Campbell, J., Mena-Carrasco, M.,Spak, S., Carmichael, G., and Chen, Y.(2012) Biofuels that cause land-use changemay have much larger non-GHG airquality emissions than fossil fuels. Environ.Sci. Technol., 46, 10835–10841.

138 Sedjo, R.E. (2011) Carbon Neutrality andBioenergy: A Zero Sum Game? RFF

References 411

Discussion Paper 11-15, RFF Press,Washington, DC.

139 Yuan, J.S., Tiller, K.H., Al-Ahmad, H.,Stewart, N.R., and Stewart, C.N. (2008)Plants to power: bioenergy to fuel thefuture. Trends Plant Sci., 13, 421–429.

140 Whitaker, J., Ludley, K.E., Rowe, R., Taylor,G., and Howard, D.C. (2010) Sources ofvariability in greenhouse gas and energybalances for biofuel production: asystematic review. GCB Bioenergy, 2,99–112.

141 Carere, C.R., Sparling, R., Cicek, N., andLevin, D.B. (2008) Third generationbiofuels via direct cellulose fermentation.Int. J. Mol. Sci., 9, 1342–1360.

142 Carpita, NC. and McCann, MC. (2008)Maize and sorghum: genetic resources forbioenergy grasses. Trends Plant Sci.,13, 415–420.

143 Cherubini, F., Bird, N.D., Cowie, A.,Jungmeier, G., Schlamadinger, B., andWoess-Gallasch, S. (2009) Energy- andgreenhouse gas-based LCA of biofuel andbioenergy systems: key issues, ranges andrecommendations. Resour. Conserv. Recy.,53, 434–447.

144 Searchinger, T., Heimlich, R., Houghton,RA., Dong, F., Elobeid, A et al. (2008) Useof U.S. croplands for biofuel increasesgreenhouse gases through emissions fromland-use change. Science, 319, 1238–1240.

145 Ducat, D.C. and Silver, P.A. (2012)Improving carbon fixation pathways. Curr.Opin. Chem. Biol., 16, 1–8.

146 Gan, Y., Liang, C., Hamel, C., Cutforth, H.,and Wang, H. (2011) Strategies forreducing carbon footprint of field crops forsemiarid areas. A review. Agron. Sustain.Dev., 31, 643–656.

147 Gillingham, K.T., Smith, S.J., and Sands,R.D. (2008) Impact of bioenergy crops in acarbon dioxide constrained world: anapplication of the MiniCAM energy-agriculture and land-use model.Mitig.Adapt. Strat. Global Change, 13, 675–701.

148 Brand~ao, M., Mil�a i Canals, L., and Clift, R.(2011) Soil organic carbon changes in thecultivation of energy crops: implicationsfor GHG balances and soil quality for usein LCA. Biomass Bioenergy, 35, 2323–2336.

149 Mishra, U., Torn, M., and Fingerman, K.(2012)Miscanthus biomass productivity

within US croplands and its potentialimpact on soil organic carbon. GCBBioenergy, 5, 391–399.

150 Jones, M.B. (2011) C-4 species as energycrops, in Advances in Photosynthesis andRespiration: C4 Photosynthesis and RelatedCO2 Concentrating Mechanisms (edsRaghavendra, A.S. and Sage, R.F.),Springer, Dordrecht, pp. 379–397.

151 Long, S.P., Zhu, X.G., Naidu, S.L., and Ort,D.R. (2006) Can improvement inphotosynthesis increase crop yields? PlantCell Environ., 29, 315–330.

152 Djomo, S.N. and Ceulemans, R. (2012) Acomparative analysis of the carbonintensity of biofuels caused byland-use changes. GCB Bioenergy,4, 392–407.

153 Thomas, A.R.C., Bond, A.J., and Hiscock,K.M. (2012) A multi-criteria based reviewof models that predict environmentalimpacts of land use-change for perennialenergy crops on water, carbon, andnitrogen cycling. GCB Bioenergy, 5,227–242.

154 Cerri, C., Bernoux, M., Cerri, C.E., andFeller, C. (2004) Carbon cycling andsequestration opportunities in SouthAmerica: the case of Brazil. Soil UseManag., 20, 248–254.

155 Fraz~ao, L.A., Paustian, K., Cerri, C.E.P.,and Cerri, C.C. (2012) Soil carbon stocksand changes after oil plam introduction inthe Brazilian Amazon. GCB Bioenergy,5, 384–390.

156 Matovic, D. (2011) Biochar as a viablecarbon sequestration options:global and Canadian perspectives. Energy,36, 2011–2016.

157 Ontl, T. and Schulte, L. (2012) Soil carbonstorage. Nat. Educ. Knowl., 3, 22–33.

158 Rosegrant, M.W., Ringler, C., Msangi, S.,Sulser, T., Zhu, T., and Cline, S. (2008)International Model for Policy Analysis ofAgricultural Commodities and Trade(IMPACT), International Food PolicyResearch Institute, Washington, DC.

159 von Braun, J. (2008) When food makesfuel: the promises and challenges ofbiofuels, presented at 13th AnnualDevelopment Conference, Canberra.

160 Hoefnagels, R., Smeets, E., and Faaij, A.(2010) Greenhouse gas footprints of


different biofuel production systems.Renew. Sustain. Energy Rev., 14,1661–1694.

161 Thelen, K.D., Fronning, B.E., Kravchenko,A., Min, D.H., and Robertson, G.P. (2010)Integrating livestock manure with a corn–soybean bioenergy cropping systemimproves short-term carbon sequestrationrates and net global warming potential.Biomass Bioenergy, 34, 960–966.

162 Borland, A.M., Griffith, H., Hartwell, J.,and Smith, J.A. (2009) Exploiting thepotential of plants with crassulaceanacid metabolism for bioenergyproduction on marginal lands. J. Exp. Bot.,60, 2879–2896.

163 Mizrachi, E., Mansfield, S.D., and Myburg,A.A. (2012) Cellulosic factories: advancingbioenergy production from forest trees.New Phytol., 194, 54–62.

164 Nair, S.S., Kang, S., Zhang, X., Miguez,F.E., Izaurralde, R.C. et al. (2012)Bioenergy crop models: descriptions, datarequirements, and future challenges. GCBBioenergy, 4, 620–633.

165 Robertson, G.P., Hamilton, S.K., DelGrosso, S.J., and Parton, W.J. (2011) Thebiogeochemistry of bioenergy landscapes:carbon, nitrogen, and waterconsiderations. Ecol. Appl., 21, 1055–1067.

166 Gerbens-Leenes, W., Hoekstra, A.Y., andvan der Meer, T.H. (2009) The waterfootprint of bioenergy. Proc. Natl. Acad. Sci.USA, 106, 10219–10223.

167 Callesen, I., Carter, M.S., and Østerga�rd,

H. (2011) Efficient use of reactive nitrogenfor cultivation of bioenergy: less is more.GCB Bioenergy, 3, 171–179.

168 Garten, C.T. Jr., Wullschleger, S.D., andClassen, A.T. (2011) Review and model-based analysis of factors influencing soilcarbon sequestration under hybrid poplar.Biomass Bioenergy, 35, 214–226.

169 Teklay, T. and Chang, S.X. (2008) Temporalchanges in soil carbon and nitrogenstorage in a hybrid poplar chronosequencein northern Alberta. Geoderma, 144,613–619.

170 Powlson, D.S., Whitmore, A.P., andGoulding, K.W.T. (2011) Soil carbonsequestration to mitigate climate change: acritical re-examination to identify the trueand the false. Eur. J. Soil Sci., 62, 42–55.

171 Sohl, T.L., Sleeter, B.M., Zhu, Z.,Sayler, K.L., Bennett, S. et al. (2012) A land-use and land-cover modeling strategy tosupport a national assessment ofcarbon stocks and fluxes. Appl. Geogr.,34, 111–124.

172 Mansfield, S.D. (2009) Solutions fordissolution – engineering cell walls fordeconstruction. Curr. Opin. Biotechnol.,20, 286–294.

173 Cuadra, S.V., Costa, M.H., Kucharik, C.J.,Da Rocha, H.R., Tatsch, J.D et al. (2012) Abiophysical model of sugarcane growth.GCB Bioenergy, 4, 36–48.

174 Lewandowski, I. and Schmidt, U. (2006)Nitrogen, energy and land use efficienciesof miscanthus, reed canary grass andtriticale as determined by the boundaryline approach. Agric. Ecosyst. Environ.,112, 335–346.

175 Peckham, S.D., Gower, S.T., andBuongiorno, J. (2012) Estimating thecarbon budget and maximizing futurecarbon uptake for a temperate forestregion in the US. Carbon BalanceManag., 7, 6.

176 Smith, J., Pearce, B.D., and Wolfe, M.S.(2011) Reconciling productivity withprotection of the environment: istemperate agroforestry the answer? Renew.Agric. Food Syst., 28, 80–92.

177 Lehtomaki, A., Viinikainen, T.A., andRintala, J.A. (2008) Screening borealenergy crops and crop residues formethane biofuel production. BiomassBioenergy, 32, 541–550.

178 Bessou, C., Ferchaud, F., Gabrielle, B., andMary, B. (2011) Biofuels, greenhouse gasesand climate change. A review. Agron.Sustain. Dev., 31, 1–79.

179 Biswas, W.K., Barton, L., and Carter, D.(2011) Biodiesel production in a semiaridenvironment: a life cycle assessmentapproach. Environ. Sci. Technol., 45,3069–3074.

180 Cherubini, F., Guest, G., and Strømman,A.H. (2012) Application of probabilitydistributions to the modeling of biogenicCO2 fluxes in life cycle assessment. GCBBioenergy, 4, 784–798.

181 Raghu, S., Spencer, J.L., Davis, A.S., andWiedenmann, R.N. (2011) Ecologicalconsiderations in the sustainable

References 413

development of terrestrial biofuel crops.Curr. Opin. Environ. Sustain., 3, 15–23.

182 Rae, A.M., Robenson, K.M., and Street,N.R. (2004) Morphological andphysiological traits infl uencing biomassprediction in short-rotation coppice poplar.Can. J. Forest. Res. , 34 , 1488–1498.

183 Ashworth, K., Folberth, G., Hewitt, C.N.,and Wild, O. (2012) Impacts of near-futurecultivation of biofuel feedstocks onatmospheric composition and local airquality. Atmos. Chem. Phys., 12, 919–939.

184 Jakob, K., Zhou, F., and Paterson, A.H.(2009) Genetic improvement of C4 grassesas cellulosic biofuel feedstocks. In VitroCell. Dev. Biol., 45, 291–305.

185 Liang, S., Xu, M., and Zhang, T. (2012)Unintended consequences of bioethanolfeedstock choice in China. Bioresour.Technol., 125, 312–317.

186 Xin, Z.G., Wang, M.L., Yuan, J.S., Qu, Y.B.,Li, S.Z., and Stewart, C.N. (2011) Sorghumas a versatile feedstock for bioenergyproduction. Biofuels, 2, 577– 588.

187 Fargione, J., Plevin, R.J., and Hill, J.D.(2010) The ecological impact of biofuels.Annu. Rev. Ecol. Syst., 41, 351–377.

188 Firbank, L.G. (2008) Assessing theecological impacts of bioenergy projects.Bioenergy Res., 1, 12–19.

189 Davis, S.C., Anderson-Teixeira, K.J., andDeLucia, E.H. (2009) Life- cycle analysisand the ecology of biofuels. Trends PlantSci., 14, 140–146.

190 Bauen, A. (2006) Future energy sourcesand systems – acting on climate changeand energy security. J. Power Sources,157, 893–901.

191 Han, F.X., King, R.L., Lindner, J.S., Yu,T.-Y., Durbha, S.S. et al. (2011) Nutrientfertilizer requirements for sustainablebiomass supply to meet U.S. bioenergygoal. Biomass Bioenergy, 35, 253–262.

192 Adler, P., Gross del, S.J., and Parton, W.J.(2007) Life-cycle assessment of netgreenhouse-gas fl ux for bioenergycropping systems. Ecol. Appl., 17, 675–691.

193 Kim, S., Dale, B.E., and Jenkins, R. (2009)Life cycle assessment of corn grain andcorn stover in the United States. Int. J. LifeCycle Assess., 14, 160–174.

194 Yuan, J.S., Tiller, K.H., Al-Ahmad, H.,Stewart, N.R., and Stewart, C.N. Jr. (2008)

Plants to power: bioenergy to fuel thefuture. Trends Plant Sci., 13, 421–429.

195 Yang, Y., Bae, J., Kim, J., and Suh, S. (2012)Replacing gasoline with corn ethanolresults in significant environmentalproblem-shifting. Environ. Sci. Technol.,46 , 3671–3678.

196 Best, G. (2006) Alternative energy crops foragricultural machinery biofuels – focus onbiodiesel. Agric. Eng. Int., 8, InvitedOverview 13.

197 Achten, W.M. and Verchot, L.V. (2011)Implications of biodiesel-induced land-usechanges for CO2 emissions: case studies intropical America, Africa, and SoutheastAsia. Ecol. Soc., 16, 14.

198 Goglio, P., Bonari, E., and Mazzonicini, M.(2012) LCA of cropping systems withdifferent external input levels forenergetic purposes. Biomass Bioenergy,42 , 33–42.

199 Patil, V., Tran, K.-Q., and HGiselrod, HR.(2008) Towards sustainable production ofbiofuels from microalgae. Int. J. Mol. Sci.,9, 1188–1195.

200 Picasso, V.D., Brummer, E.C., Liebman,M., Dixon, M.P., and Wisley, B.J. (2008)Crop species diversity affects productivityand weed suppression in perennialpolycultures under two managementstrategies. Crop Sci., 48 , 331–342.

201 Luyssaert, S., Abril, G., Andres, R.,Bastviken, D., Bellassen, V., Bergamaschi,P. et al. (2012) The European CO2 , CO,CH4, and N 2O balance between 2001 and2005. Biogeosci. Discuss., 9, 2005–20053.

202 Kendall, A., Chang, B., and Sharpe, B.(2009) Accounting for time-dependenteffects in biofuel life cycle greenhouse gasemissions calculations. Environ. Sci.Technol., 43, 7142–7147.

203 Hillier, J., Whittaker, C., Dailey, G., Aylott,M., Casella, E. et al. (2009) Greenhouse gasemissions from four bioenergy crops inEngland and Wales: integrating spatialestimates of yield and soil carbon balancein life cycle analyses. GCB Bioenergy,1, 267–281.

204 International Institute for SustainabilityAnalysis and Strategy (2013) GEMIS –

Global Emissions Model for IntegratedSystems, IINAS, Darmstadt; http://www.iinas.org/gemis-download-en.html.


http://www.iinas.org/gemis-download-en.html

http://www.iinas.org/gemis-download-en.html

205 Barrow, C.J. (2012) Biochar: potential forcountering land degradation and forimproving agriculture. Appl. Geogr.,34, 21–28.

206 Cherubini, F. and Strømman, A.H. (2011)Life cycle assessment of bioenergysystems: state of the art and futurechallenges. Bioresour. Technol., 102,437–451.

207 Dungait, J.A.J., Hopkins, D.W., Gregory, A.S., and Whitmore, A.P. (2012) Soil organicmatter turnover is governed byaccessibility not recalcitrance. GlobalChange Biol., 18, 1781–1796.

208 Stavi, L. and Lal, R. (2012) Agriculture andgreenhouse gases, a common tragedy. Areview. Agron. Sustain Dev., doi: 20.1007/s13593-012-0110-0.

209 Kirschbaum, M.U.F. (2006) Temporarycarbon sequestration cannot preventclimate change.Mitig. Adapt. Strat. GlobalChange., 11, 1151–1164.

210 Liebig, M., Schmer, M., and Vogel, K., andMitchell, R. (2008) Soil carbon storage byswitchgrass grown for bioenergy. BioenergyRes., 1, 215–222.

211 Zaehle, S., Bondeau, A., Carter, T.R.,Cramer, W., Erhard, M., Printice, I.C. et al.(2007) Projected changes in terrestrialcarbon storage in Europe under climateand land-use change, 1990–2100.Ecosystems, 10, 380–401.

212 Gutterson, N. and Zhang, J. (2009)Important issues and current status ofbioenergy crop policy for advancedbiofuels. Biofuels Bioprod. Bioref.,3, 441–447.

213 Chiu, Y.-W., Suh, S., Pfister, S., Hellweg,S., and Koehler, A. (2012) Measuringecological impact of water consumptionby bioethanol using life cycle impactassessment. Int. J. Life Cycle Assess.,17, 16–24.

214 Fingerman, K.R., Berndes, G., Orr, S.,Richter, B.D., and Vugteveen, P. (2011)Impact assessment at the bioenergy–waternexus. Biofuels Bioprod. Bioref., 5, 375–386.

215 Gheewala, S.H., Berndes, G., and Jewitt,G. (2011) The bioenergy and water nexus.Biofuels Bioprod. Bioref., 5, 353–360.

216 Heggenstaller, A.H., Anex, R.P., Liebman,M., Sundberg, D.N., and Gibson, L.R.(2008) Productivity and nutrient dynamics

in bioenergy double-cropping systems.Agron. J., 100, 1740–1748.

217 Brand~ao, M. and Mil�a i Canals, L. (2012)Global characterization factors to assessland use impacts on biotic production. Int.J. Life Cycle Assess., doi: 10.1007/s11367-012-0381-3.

218 Fargione, J., Hill, J., Tilman, D., Polasky,S., and Hawthorne, P. (2008) Land clearingand the biofuel carbon debt. Science,319, 1235–1238.

219 Kang, S., Post, W., Wang, D., Nichols, J.,Bandaru, V., and West, T. (2013)Hierarchical marginal land assessment forland use planning. Land Use Policy,30, 106–113.

220 Tang, Z., Engel, B.A., Pijanowski, B.C., andLim, K.J. (2005) Forecasting land-usechange and its environmental impact at awatershed scale. J. Environ. Manag.,76, 35–45.

221 Tilman, D., Hill, J., and Lehman, C. (2006)Carbon-negative biofuels from low-inputhigh-diversity grassland biomass. Science,314, 1598–1600.

222 Srirangan, K., Akawi, L., Moo-Young, M.,and Chou, C.P. (2012) Towardssustainable production of clean energycarriers from biomass resources. Appl.Energ., 100, 172–186.

223 Zhou, X., Wang, F., Hu, H., Yang, L., Guo,P., and Xiao, B. (2011) Assessment ofsustainable biomass resource for energyuse in China. Biomass Bioenergy,35, 1–11.

224 Fan, S., Freedman, B., and Gao, J. (2007)Potential environmental benefits fromincreased use of bioenergy in China.Environ Manag., 40, 504–515.

225 Buckeridge, M., De Souza, A.P., Arundale,R.A., Anderson-Teixira, K.J., and Delucia,E. (2012) Ethanol from sugarcane in Brazil:a ‘midway’ strategy for increasing ethanolproduction while maximizingenvironmental benefits. GCB Bioenergy,4, 119–126.

226 McKendry, P. (2002) Energy productionfrom biomass (part 1): overview ofbiomass. Bioresour. Technol., 83, 37–46.

227 Marland, G., Garten, C.T. Jr., Post, W.M.,and West, T.O. (2004) Studies onenhancing carbon sequestration in soils.Energy, 29, 1643–1650.

References 415

228 Oldenburg, C.M., Torn, M.S., DeAngelis,K.M., Ajo-Franklin, J.B., Amundson, R.G.et al. (2008) Biologically Enhanced CarbonSequestration: Research Needs andOpportunities. Report on the EnergyBiosciences Institute Workshop on BiologicallyEnhanced Carbon Sequestration, LawrenceBerkeley National Laboratory, Berkeley,CA.

229 Amichev, B.Y., Kurz, W.A., Smyth, C., andVan Rees, K.C.J. (2012) The carbonimplications of large-scale afforestation ofagriculturally marginal land and short-rotation willow in Saskatchewan. GCBBioenergy, 4, 70–87.

230 Tubiello, F.N., Soussana, J.-F., andHowden, S.M. (2007) Crop and pastureresponse to climate change. Proc. Natl.Acad. Sci. USA, 104, 19686–19690.

231 El-Nashaar, H.M., Griffith, S.M., Steiner,J.J., and Banowetz, G.M. (2009) Mineralconcentration in selected native temperategrasses with potential use as biofuelfeedstock. Biosour. Technol., 100,3526–3531.

232 Bentsen, N. and Felby, C. (2012) Biomassfor energy in the European Union – areview of bioenergy resource assessment.Biotechnol. Biofuels, 5, 25–35.

233 Birenger, T., Lucht, W., and Schaphoff, S.(2011) Bioenergy production potential ofglobal biomass plantations underenvironmental and agriculturalconstraints. GCB Bioenergy, 3, 299–312.

234 Gonz�alez-García, S., Gasol, C.M.,Gabarrell, X., Rieradevall, J., Moreira, M.T.,and Feijoo, G. (2010) Environmentalprofile of ethanol from poplar biomass astransport fuel in Southern Europe. Renew.Energy, 35, 1014–1023.

235 Schenk, P.M., Thomass-Hall, S.R.,Stephens, E., Marx, U.C., Mussgnug, H.J.et al. (2008) Second generation biofuels:high-effeciency microalgae for biodieselproduction. Bioenergy Res., 1, 20–43.

236 Zhao, Y.L., Dolat, A., Steinberger, Y., Wang,X., Osman, A., and Xie, G.H. (2009)Biomass yield and changes in chemicalcomposition of sweet sorghumcultivars grown for biofuel. Field Crops Res.,111, 55–64.

237 Vargas-Moreno, J.M., Callej�on-Ferre, A.J.,P�erez-Alonso, J., and Vel�azquez-Martí, B.

(2012) A review of the mathematicalmodels for predicting the heating value ofbiomass materials. Renew. Sustain. EnergyRev., 16, 3065–3083.

238 Hoogwijk, M., Faaij, A., Eickhout, B., Vriesde, B., and Turkenburg, W. (2009)Exploration of regional and global cost-supply curves of biomass energy fromshort-rotation crops at abandonedcropland and rest land under four IPCCSRES land-use scenarios. BiomassBioenergy, 33, 26–43.

239 Lobell, D.B., Burke, M.B., Tebaldi, C.,Mastrandera, M.D., Falcon, W.P., andNaylor, R.L. (2008) Prioritizing climatechange adaptation needs for food securityin 2030. Science, 319, 607–610.

240 Demirbas, A. (2001) Relationship betweenlignin contents and heating values ofbiomass. Energy Conserv. Manag., 42,183–188.

241 Restianti, Y.Y. and Gheewala, S.H. (2012)Environmental and life cycle costassessment of cassava ethanol inIndonesia. J. Sustain. Energy Environ.,3, 1–6.

242 Smith, K. and Searchnger, T. (2012) Crop-based biofuels and associatedenvironmental concerns. GCB Bioenergy,4, 479–484.

243 van der Hilst, F., Lesschen, J.P., van dam,J.M.C., Riksen, M., and Verweij, P.A.(2012) Spatial variation of environmentalimpacts of regional biomass chains. Renew.Sustain. Energy Rev., 16, 2053–2069.

244 Sticklen, M. (2006) Plant geneticengineering to improve biomasscharacteristics for biofuels. Curr. Opin.Biotechnol., 17, 315–319.

245 Carroll., A. and Somerville, C. (2009)Cellulosic biofuels. Annu. Rev Plant Biol.,60, 165–182.

246 Lorenz, A.J., Coors, J.G., de Leon, N.,Wolfman, E.J., Hames, B.R., Sluiter, A.D.,and Weimer, P.J. (2009) Characterization,genetic variation, and combiningability of maize traits relevant to theproduction of cellulosic ethanol. Crop Sci.,49, 85–98.

247 Scown, C.D., Nazaroff, W.W., Mishra, U.,Strogen, B., Lobscheid, A.B. et al. (2012)Corrigendum: lifecycle greenhouse gasimplications of US national scenarios for


cellulosic ethanol production. Environ. Res.Lett., 7, 014011.

248 Cornelissen, S., Koper, M., and Deng, Y.Y.(2012) The role of bioenergy in a fullysustainable global energy system. BiomassBioenergy, 41, 21–33.

249 Barney, J.N. and DiTomaso, J.M. (2011)Global climate niche estimates forbioenergy crops and invasive species ofagronomic origin: potential problems andopportunities. PLoS ONE, 6, e17222.

250 Canadell, J.G., Kirschbaum, M.U.F., Kurz,W.A., Sanz, M.-J., Schlamadinger, B., andYmagata, Y. (2007) Factoring out naturaland indirect human effects on terrestrialcarbon sources and sinks. Environ. Sci.Policy, 10, 370–384.

251 Tulbure, M.G., Wimberly, M.C., Boe, A.,and Owens, V.N. (2012) Climatic andgenetic controls of yields of swithgrass, amodel bioenergy species. Agric. Ecosyst.Environ., 146, 121–129.

252 Persson, T., Garcia, A.G., Paz, J.O., Jones,J.W., and Hoogenboom, G. (2009) Netenergy value of maize ethanol as aresponse to different climate and soilconditions in the southeastern USA.Biomass Bioenergy, 33, 1055–1064.

253 Jessup, R.W. (2009) Development andstatus of dedicated energy crops in theUnited States. In Vitro Cell. Dev. Biol.,45, 282–290.

254 Boe, A. and Lee, DK. (2007) Geneticvariation for biomass production in Prairiecordgrass and switchgrass. Crop Sci.,47, 929–934.

255 Leaky, A.D.B. (2009) Rising atmosphericcarbon dioxide concentration and thefuture of C4 crops for food and fuel.Philos. Trans. R. Soc. Lond. B, 276,2333–2343.

256 Swana, J., Yang, Y., Behnam, M., andThompson, R. (2011) An analysis of netenergy production and feedstockavailability for biobutanol and bioethanol.Bioresour. Technol., 102, 2112–2117.

257 Yang, Y., Bae, J., Kim, J., and Suh, S. (2012)Replacing gasoline with corn ethanolresults in significant environmentalproblem-shifting. Environ. Sci. Tecnol.,46, 3671–3678.

258 Blanco-Canqui, H. and Lal, R. (2009) Cornstover removal for expanded uses reduces

soil fertility and structural stability. Soil Sci.Soc. Am. J., 73, 418–426.

259 Carlyle, J.C., Charmley, E., Baldock, J.A.,Polglase, P.J., and Keating, B. (2010)Agricultural greenhouse gases andmitigation options, in Adapting agricultureto Climate Change: Preparing AustralianAgriculture, Forestry and Fisheries for theFuture (eds C.J. Stokes and S.M. Howden),CSIRO, Clayton, pp. 229–244.

260 Moreira, J.R. and Read, P. (2006) Globalbiomass energy potential.Mitig. Adapt.Strat. Global Change, 11, 313–342.

261 Wang, L.-P., Jackson, P.A., Lu, X., Fan, Y.-H., Foreman, J.W. et al. (2008) Evaluationof sugarcane�Saccharum spontaneumprogeny for biomass composition and yieldcomponents. Crop Sci., 48, 951–961.

262 Sims, R.E.H., Mabee, W., Saddler, J.N., andTaylor, M. (2010) An overview of second-generation biofuel technologies. Bioresour.Technol., 101, 1570–1580.

263 Margeot, A., Hahn-Hagerdal, B., Edlund,M., Slade, R., and Monot, F. (2009) Newimprovements for lignocellulosic ethanol.Curr. Opin. Biotechnol., 20, 372–380.

264 Wang, Y. and Yan, L. (2008) CFD studieson biomass thermochemical conversion.Int. J. Mol. Sci., 9, 1108–1130.

265 Taherzadeh, M.J. and Karimi, K. (2008)Pretreatment of linocellulosic wastes toimprove ethanol and biogas production: areview. Int. J. Mol. Sci., 9, 1621–1651.

266 McLaughlin, S.B., Kiniry, J.R., Taliaferro,C.M., and Ugarte, D. (2006) Projectingyield and utilization potential ofswitchgrass as an energy crop. Adv. Agron.,90, 267–296.

267 Vogel, K.P. and Mitchell, R.B. (2008)Heterosis in switchgrass: Biomass yield inswards. Crop Sci., 48, 2159–2164.

268 Sticklen, M. (2007) Feedstock crop geneticengineering for alcohol fuels. Crop Sci.,47, 2238–2248.

269 Fransworth, E. and Meyerson, L.A. (2003)Comparative ecophysiology of fourwetland plant species along a continuumof invasiveness.Wetlands, 23, 750–762.

270 Ram, S.G., Parthiban, K.T., Kumar, R.S.,Thiruvengadam, V., and Paramathma, M.(2008) Genetic diversity among Jatrophaspecies as revealed by RAPD markers.Genet. Resour. Crop. Evol., 55, 803–809.

References 417

271 Ranade, S.A., Srivastava, A.P., Rana, T.S.,Srivastava, J., and Tuli, R. (2008) Easyassessment of diversity in Jatropha cruca L.plants using two single-primeramplification reaction (SPAR) methods.Biomass Bioenergy, 32, 533–540.

272 Komar, R.S., Parthiban, K.T., Hemalatha,P., Kalaiselvi, T., and Rao, M.G. (2009)Investigation on cross-compatibilitybarriers in the biofuel crop Jatropha crucasL. with wild Jatropha species. Crop Sci.,49, 1667–1674.

273 Tilman, D., Socolow, R., Foley, J.A., Hill, J.,Larson, E et al. (2009) Beneficial biofuels –the food, energy, and environmenttrilemma. Science, 325, 270–271.

274 Rowe, R.L., Street, N.R., and Taylor, G.(2009) Identifying potential environmentalimpacts of large-scale deployment ofdedicated bioenergy crops in the UK.Renew. Sustain. Energy Rev., 13, 271–290.

275 Ehrlich, P.R. and Pringle, R.M. (2008)Where does biodiversity go from here? Agrim business-as-usual forecast and ahopeful portfolio of partial solutions.Proc. Natl. Acad. Sci. USA, 105,11579–11586.

276 Rubin, E.M. (2008) Genomics of cellulosicbiofuels. Nature, 454, 841–845.

277 Fraiture de, F., Giordano, M., and Liao, Y.(2008) Biofuels and implications foragricultural water use: blue impacts ofgreen energy.Water Policy, 10 (Suppl. 1),67–81.

278 Williams, C.M.J., Biswas, T.K., Black, I.,and Heading, S. (2008) Pathways toprosperity: Second generation biomasscrops for biofuels using saline lands andwastewater. Agric. Sci., 21, 34–36.

279 Jaradat, A.A. (2003) Halophytes forsustainable biosaline farming systems inthe Middle East, in Desertification in theThird Millennium (eds A.S. Alsharhan, W.W. Wood, W.S. Goudie, A. Fowler, and A.M. Abdellatif), Swets & Zeitlinger, Leiden,pp. 187–204.

280 O’Leary, J.W. (1993) Growth andphysiology of Salicornia biglovii Torr. Int. J.Plant Sci., 156, 197–205.

281 Aronson, J.A. (1989)Haloph: A Database ofSalt Tolerant Plants of the World, Office ofArid Land Studies, The University ofArizona, Tucson, AZ.

282 Dillon, S.L. and Chapter, F.M. (2007)Domestication to crop improvement:genetic resources for Sorghum andSaccharum (Andropogoneae). Ann. Bot.,100, 975–989.

283 Casler, M.D., Stendal, C.A., Kapich, L., andVogel, K.P. (2007) Genetic diversity, plantadaptation regions, and gene pools forswitchgrass. Crop Sci., 47, 2261–2273.

284 Murray, S.C., Sharma, A., Rooney, W.L.,Klein, P.E., Mullet, J.E. et al. (2008) Geneticimprovement of sorghum as a biofuelfeedstock: I. QTL for stem sugar and grainnonstructural carbohydrates. Crop Sci.,48, 2165–2179.

285 Murray, S.C., Rooney, W.L., Hamlin, M.T.,Mitchell, S.E., and Kresovich, S. (2009)Sweet sorghum genetic diversity andassociation mapping for brix and height.Plant Genome, 2, 48–62.

286 Ortiz, R. (2008) Crop genetic engineeringunder global climate change. Ann. AridZone, 47, 1–12.

287 Hattori, T. and Morita, S. (2010) Energycrops for sustainbale bioethanolproduction, which, where and how? PlantProd. Sci., 13, 221–234.

288 Gressel, J. (2008) Transgenics areimperative for biofuel crops. Plant Sci.,174, 246–263.

289 Li, X., Weng, J.-K., and Chapple, C. (2008)Improvement of biomass through ligninmodification. Plant J., 54, 569–581.

290 Youngs, H. and Somerville, C. (2012)Development of feedstocks for cellulosicbiofuels. F1000 Biol. Rep., 4, 10.

291 Casler, M.D., Vogel, K.P., Taliaferro, C.M.,Ehlke, N.J., Berdhal, J.D et al. (2007)Latitudinal and longitudinal adaptation ofswitchgrass populations. Crop Sci.,47, 2249–2260.

292 Schmer, M.R., Vogel, K.P., Mitchell, R.B.,and Perrin, R.K. (2008) Net energy ofcellulosic ethanol from switchgrass. Proc.Natl. Acad. Sci. USA, 105, 464–469.

293 Anderson, W.F., Mass, A., and Ozais-Atkins, P. (2009) Genetic variability of aforage bermudagrass core collection. CropSci., 49, 1347–1358.

294 Heaton, E.A., Dohlman, F.G., Miguez, A.F., Juvik, J.A., Lozovaya, V. et al. (2010)Miscanthus: a promising biomass crop.Adv. Bot. Res., 56, 76–137.


295 Basha, S.D. and Sujatha, M. (2007) Interand intra-population variability of Jatrophacrucas (L.) characterized by RAPD andISSR markers and development ofpopulation-specific SCAR markers.Euphytica, 156, 375–386.

296 VanLooke, A., Twine, T.E., Zeri, M., andBernacchi, C.J. (2012) A regionalcomparison of water use efficiency forMiscanthus, switchgrass and maize. Agric.Forest. Meteorol., 164, 82–95.

297 Nelson, E., Mendoza, G., Regetz, J.,Polasky, S., Tallis, H. et al. (2009) Modelingmultiple ecosystem services, biodiversityconservation, commodity production, andtradeoffs at landscape scales. Front. Ecol.Environ., 7, 4–11.

298 Murray, S.C., Rooney, W.L., Mitchell, S.E.,Sharma, S., Klein, P.E. et al. (2008) Geneticimprovement of sorghum as a biofuelfeedstock: II. QTL for stem and leafstructural carbohydrates. Crop Sci.,48, 2180–2193.

299 Sage, R.F. and Zhu, X.-G. (2011) Exploitingthe engine of C4 photosynthesis. J. Exp.Bot., 62, 2989–3000.

300 Dale, V.H., Kline, K.L., Wright, L.L.,Perlack, R.D., Downing, M., and Graham,R.L. (2011) Interactions amongbioenergy feedstock choices, landscapedynamics, and land use. Ecol. Appl.,21, 1039–1054.

301 Cantarello, E., Newton, A.C., and Hill, R.A.(2011) Potential effects of future land-usechange on regional carbon stocks in theUK. Environ. Sci. Policy, 14, 40–52.

302 Vandewalle, M., de Bello, F., Berg, M.P.,Bolger, T., Dol�edec, S., Dubs, F. et al.(2010) Functional traits as indicators ofbiodiversity response to land-use changesacross ecosystems and organisms.Biodivers. Conserv., 19, 2921–2947.

303 Tomlinson, I. (2013) Doubling foodproduction to feed 9 billion: a criticalperspective on key discourse of foodsecurity in the UK. J. Rural Stud.,29, 81–90.

304 Houghton, R.A. (2007) Balancing theglobal carbon budget. Annu. Rev. EarthPlanet Sci., 35, 313–347.

305 Searchinger, T. (2010) Biofuels and theneed for additional carbon. Environ. Res.Lett., 5, 024007.

306 Zegada-Lizarazu, W. and Monti, A. (2011)Energy crops in rotation. A review. BiomassBioenergy, 35, 12–25.

307 Zeri, M., Anderson-Teixeira, K., Hickman,G., Masters, M., DeLucia, E., andBernacchi, C.J. (2011) Carbonexchange by establishing biofuel crops incentral Illinois. Agric. Ecosyst. Environ.,144, 319–329.

308 Monti, A., Virgilio di, N., and Venturi, G.(2008) Mineral composition and ashcontent of six major energy crops. BiomassBioenergy, 32, 216–223.

309 Rosgaard, L., de Porcellinis, A.J., Jacobsen,J.H., and Frigaard, N.-U., and Sakuragi, Y.(2012) Bioengineering of carbon fixation,biofuels, and biochemicals incyanobacteria and plants. J. Biotechnol.,162, 134–147.

310 Tum, M., Strauss, F., McCallum, I.,Gunther, K., and Schmid, E. (2012) Howsensitive are estimates of carbon fixation inagriculture models to input data? CarbonBalance Manag., 7, 3.

311 Zub, H.W. and Brancourt-Hulmel, M.(2010) Agronomic and physiologicalperformances of different species ofMiscanthus, a major energycrop. A review. Agron. Sustain. Dev.,30, 201–214.

312 Lewandowski, I., Clifton-Brown, J.C.,Scurlock, J.M.O., and Huisman, W. (2000)Miscanthus: European experience with anovel energy crop. Biomass Bioenergy,19, 209–227.

313 Fernando, A.L., Duarte, M.P., Almeida, J.,Bol�eo, S., and Mendes, B. (2010)Environmental impact assessment ofenergy crops cultivation in Europe. BiofuelsBioprod. Bioref., 4, 594–604.

314 Finnan, J., Styles, D., Fitzgerald, J.,Connolly, J., and Donnelly, A. (2012) Usinga strategic environmental assessmentframework to quantify the environmentalimpact of bioenergy crops. GCB Bioenergy,4, 311–329.

315 Gonz�alez-García, S., Moreira, M.T., andFeijoo, G. (2012) Environmental aspects ofeucalyptus based ethanol production anduse. Sci. Total Environ., 438, 1–8.

316 Yates, R.A. (2006) Sugarcane, carbonsequestration and food supplies. Int. SugarJ., 113, 672–676.

References 419

317 Bhardwaj, A., Zenone, T., Jasrotia, P.,Robertson, G., Chen, J., and Hamilton, K.(2011) Water and energy footprints ofbioenergy crop production on marginallands. GCB Bioenergy, 3, 208–222.

318 Murphy, R., Woods, J., Black, M., andMcManus, M. (2011) Global developmentsin the competition for land from biofuels.Food Policy, 36, S52–S61.

319 Steffen, W. (2006) The anthropocene,global change and sleeping giants: whereon earth are we going? Carbon BalanceManag., 1, 3.

320 Hennenberg, K.J., Dragisic, C., Haye, S.,Hewson, J., Semroc, B. et al. (2009) Thepower of bioenergy-related standards toprotect biodiversity. Conserv. Biol., 24,412–423.

321 Teng, Y., Xu, Z., Lou, Y., and Reverchon, F.(2012) How do persistent organicpollutants be coupled with biogeochemicalcycles of carbon and nutrients in terrestrialecosystems under global climate change? J.Soils Sedim., 12, 411–419.

322 Yeh, S., Berndes, G., Wani, S., Neto, A.,Suh, S., Karlberg, L. et al. (2011) Evaluationof water use for bioenergy at differentscales. Biofuels Bioprod. Bioref., 5, 361–374.

323 Powers, S.E., Ascough, J.C., Nelson, R.G.,and Larocque, G.R. (2011) Modeling waterand soil quality environmental impactsassociated with bioenergy crop productionand biomass removal in the Midwest USA.Ecol. Model., 222, 2430–2447.

324 Georgescu, M., Lobell, D.B., and Field,C.B. (2011) Direct climate effects ofperennial bioenergy crops in the UnitedStates. Proc. Natl. Acad. Sci. USA,108, 4307–4312.

325 Grammelis, P., Malliopoulou, A., Basinas,P., and Danalatos, N.G. (2008) Cultivationand characterization of Cynara cardunculusfor soild biofuels production in theMediterranean region. Int. J. Mol. Sci.,9, 1241–1258.

326 Gr€unewald, H., B€ohm, C., Quinkenstein,A., Grundmann, P., Eberts, J., and vonWuhlisch, G. (2009) Robinia pseudoacaciaL.: a lesser known tree species for biomassproduction. Bioenergy Res., 2, 123–133.

327 Lewandwski, I., Scurlock, J.M.O., Lindvall,E., and Christou, M. (2003) Thedevelopment and current status ofperennial rhizomatous grasses as energycrops in the US and Europe. BiomassBioenergy, 25, 335–361.

328 Boehmel, C., Lewandowski, I., andClaupein, W. (2008) Comparing annualand perennial energy cropping systemswith different management intensities.Agric. Syst., 96, 224–236.

329 Bonin, C., Lal, R., Schmitz, M., andWullschleger, S. (2012) Soil physical andhydrological properties under three biofuelcrops in Ohio. Acta Agric. Scand. B,62, 595–603.

330 Schr€oder, P., Herzig, R., Bojinov, B.,Ruttens, A., Nehnevajova, E et al. (2008)Bioenergy to save the world: producingnovel energy plants for growth onabandoned land. Environ. Sci. Pollut. Res.Int., 15, 196–204.

331 Yang, H., Zhou, Y., and Liu, J. (2009) Landand water requirements of biofuel andimplications for food supply and theenvironment in China. Energy Policy,37, 1876–1885.


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