Renewable and Sustainable Energy Reviews 107 (2019) 250–263

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Renewable and Sustainable Energy Reviews

journal homepage: www.elsevier.com/locate/rser

Towards the implementation of sustainable biofuel production systems T

a,b,⁎ b c d
Diego F. Correa , Hawthorne L. Beyer , Joseph E. Fargione , Jason D. Hill ,
Hugh P. Possinghamb,e, Skye R. Thomas-Halla, Peer M. Schenka
a
Algae Biotechnology Laboratory, School of Agriculture and Food Sciences, The University of Queensland, Brisbane, QLD 4072, Australia
b
Centre for Biodiversity and Conservation Science (CBCS), The University of Queensland, Brisbane, QLD 4072, Australia
c
The Nature Conservancy, Minneapolis, MN 55415, USA
d
Department of Bioproducts and Biosystems Engineering, The University of Minnesota, St. Paul, MN 55108, USA
e
The Nature Conservancy, Arlington, VA 22203, USA

A R T I C LE I N FO A B S T R A C T

Keywords: Novel energy production systems are needed that not only offer reductions in greenhouse gas emissions but also
Biodiversity cause fewer overall environmental impacts. How to identify and implement more sustainable biofuel production
Biofuel alternatives, and how to overcome economic challenges for their implementation, is a matter of debate. In this
Bioenergy study, the environmental impacts of alternative approaches to biofuel production (i.e., first, second, and third
Climate change
generation biofuels), with a focus on biodiversity and ecosystem services, were contrasted to develop a set of
Microalgae
Renewable energy
criteria for guiding the identification of sustainable biofuel production alternatives (i.e., those that maximize
Ecosystem service socioeconomic and environmental benefits), as well as strategies for decreasing the economic barriers that
prevent the implementation of more sustainable biofuel production systems. The identification and im-
plementation of sustainable biofuel production alternatives should be based on rigorous assessments that in-
tegrate socioeconomic and environmental objectives at local, regional, and global scales. Further development of
environmental indicators, standardized environmental assessments, multi-objective case studies, and globally
integrated assessments, along with improved estimations of biofuel production at fine spatial scales, can enhance
the identification of more sustainable biofuel production systems. In the short term, several governmental
mandates and incentives, along with the development of financial and market-based mechanisms and applied
research partnerships, can accelerate the implementation of more sustainable biofuel production alternatives.
The set of criteria and strategies developed here can guide decision making towards the identification and
adoption of sustainable biofuel production systems.

1. Introduction × 1011 GJ consumed globally in 2016, of which 81% was derived from
coal, petroleum, and natural gas [10]. Their associated greenhouse gas
Boosting economic growth while halting environmental degradation (GHG) emissions are linked to global warming and its negative impacts
remains one of the major global challenges for humankind [1]. Current on biodiversity [11] and ecosystem services [12]. Limiting global
unsustainable use of the Earth’s finite natural capital [2] has led to a warming to well below 2 °C compared to pre-industrial levels, a goal
wide range of negative impacts on the environment [3], including in- ratified by 185 parties (i.e., on February 2019) following the 21st
creasing biodiversity losses [4], alterations in the provision and quality Conference of the Parties to the United Nations Framework Convention
of ecosystem services [5], and climate change [6]. These impacts and on Climate Change (UNFCCC) in Paris [13], is expected to require the
the decisions that society makes to reduce them, which include balan- rapid adoption of renewable energy systems for replacing fossil fuels
cing human population growth [7] and planning for solutions based on [14]. Consequently, the share of energy from renewable sources could
multiple interacting environmental pressures [8], will have profound increase from 9% of total primary energy demands in 2016 to 29% by
implications for global socioeconomic and environmental systems. 2040 [10].
How to meet increasing energy consumption demands, while re- While solar, wind and water as renewable energy sources could
versing environmental degradation, is a matter of debate [9]. Currently, provide electricity with lower environmental costs compared to fossil
the provision of energy relies primarily on fossil fuels, with around 5.8 fuels [15], liquid fuels are expected to remain necessary in the transport

⁎
Corresponding author at: Centre for Biodiversity and Conservation Science (CBCS), The University of Queensland, Brisbane, QLD 4072, Australia.
E-mail address: [email protected] (D.F. Correa).

https://doi.org/10.1016/j.rser.2019.03.005
Received 28 May 2018; Received in revised form 27 February 2019; Accepted 3 March 2019
1364-0321/ © 2019 Elsevier Ltd. All rights reserved.
D.F. Correa, et al. Renewable and Sustainable Energy Reviews 107 (2019) 250–263

Box 1
Biofuels, main production regions, and overlapping areas of high ecological importance.

Biofuel production involves the transformation of organic compounds—including cellulose, hemicellulose, lignin, starch, saccharose, and
oils—from living organisms into carbon-rich carriers (e.g., alcohols and esters) that can be used for energy generation [29]. These organic
compounds can come from a wide range of feedstocks (i.e., the range of sources from which biofuels are produced), including herbaceous
and woody plants, oilseeds, agricultural and forestry wastes, and algae [30]. Feedstocks are transformed into biofuels through various
combinations of thermochemical, biochemical, chemical and physical processes depending on feedstock properties (e.g., moisture content,
proportions of fixed carbon and volatile matter, and cellulose/lignin ratios) [31]. Different environmental impacts, including habitat loss
for native species [19], GHG emissions [20], emission of pollutants [21], and water withdrawals [32], arise from combinations of feedstock
cultivation systems and their processing technologies.
According to REN21 [34], 133 × 109 L of liquid biofuels were produced in 2015, mainly in the forms of bioethanol (98.3 × 109 L,
contributing to 74% of global biofuel production) and biodiesel (30.1 × 109 L, contributing to 23% of global biofuel production). Bioe-
thanol production was led by the USA (57% of the total global bioethanol production), followed by Brazil (29%) and the EU-28 (4%),
mostly from maize in the USA, maize and wheat in the EU-28, and sugarcane in Brazil. Biodiesel production was led by the EU-28 (38% of
the global total production), followed by the USA (16%) and Brazil (14%) [34], primarily from rapeseed in Europe, and soybean in the USA
and Brazil. Another widely used biodiesel feedstock is oil palm [35]. Cultivation of these crops overlaps with areas of high ecological
importance, and have widely replaced native ecosystems, including native grasslands in the USA [36] and Brazil [37], as well as tropical
and subtropical forests in South America [38] and Southeast Asia [39].

sector—mainly for aviation, shipping, and long-haul trucking—in spite biofuel production areas [43] as a consequence of increases in food
of an expected increase in electric vehicles [16]. In fact, some scenarios prices generated by the competition with food production (i.e., indirect
for limiting global warming to 2 °C foresee biofuel production in- land-use change) [54]. For instance, between 1990 and 2005 in
creasing from 9.7 × 106 GJ d-1 to 4.6 × 107 GJ d-1 between 2016 and Southeast Asia, more than 55% of oil palm crops—which is used for
2040, reaching 16% of total transport fuels [10], though it remains human consumption and as a source for biodiesel production—came
unclear to what degree biofuel adoption would reduce net GHG emis- from oil palm plantations on converted native forests, directly in-
sions compared to other climate change mitigation options [17]. creasing the extinction risk of thousands of species [55], while emitting
Current biofuel production is based on food crops (i.e., first gen- large amounts of CO2 into the atmosphere [20]. In Borneo, Sumatra and
eration biofuels) that compete with agricultural lands and biodiverse Peninsular Malaysia alone, it is estimated that the conversion of 6% of
landscapes (Box 1, Fig. 1). Furthermore, biofuel production has been peat-swamp forests into oil palm by the early 2000s led to direct
linked to several other environmental pressures that may, directly and emissions of more than 140 Mt of CO2 into the atmosphere plus ongoing
indirectly, impact biodiversity and the provision of ecosystem services. annual carbon losses of around 4.6 Mt as a result of peat oxidation [56].
These pressures [18] include direct and indirect land-use change [19], Conversion of peat-swamps and associated releases of CO2 are ongoing
GHG emissions [20], emission of pollutants (i.e., from pesticides, fer- [57]. The expansion of first generation biofuels has also impacted South
tilizers, biofuel production, and final use of biofuels) [21], water de- America, where soybean cultivation—used for food, animal feed, and
pletion [22], soil degradation and erosion [23], and introduction of biodiesel production—has directly replaced large areas of the biodi-
invasive species [24]. The impacts of biofuels on biodiversity and verse Cerrado savannas [37], and indirectly driven deforestation in the
ecosystem services, however, depend on the type of biofuel production Amazon forest for cattle production [38]. In North America, bioethanol
system and several factors associated with its cultivation and produc- production from maize has, directly and indirectly, promoted the re-
tion [19], including: the competing land-use and the spatial config- placement of native and planted grasslands [58]. Further cultivation of
urations of biofuel cultivation landscapes [25], their cultivation and food crops for biofuel production threatens many other biodiverse and
conversion technologies [21], their cultivation management practices carbon-rich systems, including the African savannas [59] and several
[26], their invasiveness potential [27], and the presence of co-products other suitable agricultural areas mainly in the highly productive tro-
(Box 2) [28]. pical regions [60], as well as in developing economies with high energy
How to identify and implement more sustainable biofuel production demands (e.g., China) [61].
alternatives [51], and how to overcome economic obstacles to their GHGs—including CO2, methane (CH4), nitrous oxide (N2O), and
implementation, are unresolved challenges [52]. Here, the environ- carbon monoxide (CO)—as well as air pollutants—including ammonia
mental impacts of several biofuel production alternatives (i.e., first, (NH3), volatile organic compounds (VOC), particulate matter (PM),
second, and third generation biofuels) on biodiversity and ecosystem nitrogen oxides (NOx), and sulfur oxides (SOx) [62]—are emitted
services are evaluated. This information is integrated with criteria and during the replacement of original systems [63], cultivation and pro-
avenues of research for guiding the identification and implementation cessing of feedstocks [64], transportation of biofuels to fuel stations,
of sustainable biofuel production alternatives (i.e., those that maximize and final use of biofuels [49]. For instance, the emission of N2O during
socioeconomic and environmental benefits). Finally, promising strate- the cultivation of crops with high nitrogen demands can offset CO2
gies for overcoming economic barriers to adopt more sustainable bio- savings, as its global warming potential is 296 times larger than an
fuel production systems are discussed. equal mass of CO2 [65]. Air pollution not only contributes to climate
change, but also, directly and indirectly, impact species, ecosystems,
and humans (e.g., through poisoning, acid rain, ozone layer depletion,
2. An overview of the environmental impacts of several biofuel tropospheric ozone formation, and changes in regional weather pat-
production alternatives terns) [66]. In fact, Tessum et al. [67] show that replacing conventional
gasoline with corn ethanol in USA light-duty transportation can in-
First generation biofuels, which compete with agricultural and crease environmental health impacts by 80% from increased levels of
biodiverse lands, have led to habitat loss for native species [53] and O3 and PM.
associated GHG emissions [20] (Box 3). This mainly occurs by the di- In the face of future agricultural expansion, alternatives that do not
rect replacement of biodiverse and carbon-rich original systems (i.e., compete with food production or with biodiversity, and with fewer
direct land-use change) [19], and by the agricultural expansion outside

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Fig. 1. Cultivation areas of food crops used for biofuel production globally (a) and overlapping habitat types and ecoregions (as dotted areas) [40] in North America
(b), South America (c) and South East Asia (d). Total physical cultivation area for crops is based on the Spatial Production Allocation Model (SPAM) 2005 v.2.0 at 5′
grid cells [41].

direct and indirect impacts on biodiversity and ecosystem services, are conditions, drive losses in soil carbon stocks. For instance, Strickland
needed to replace fossil fuels (Box 4, Fig. 2). Second generation bio- et al. [91] found that intercropping switchgrass within Pinus taeda
fuels, based on the transformation of the abundant lignin and cellulose plantations can reduce soil carbon during the first years following
found in non-food plants such as Miscanthus [71] and Jatropha [72,73], switchgrass planting.
as well as in organic wastes [30], could lower competition with prime While using wastes for biofuel production does not directly compete
agricultural lands used for food production, as well as decrease the use with agricultural or biodiverse lands, it could impact biodiversity and
of water, fertilizers, and pesticides [74]. The cultivation of second ecosystem services. For instance, the extraction of agricultural and
generation biofuels (e.g., willow, poplar, Eucalyptus, Miscanthus, and forestry wastes can decrease soil carbon stocks and fertility in cultiva-
switchgrass) could, however, compete with important areas for biodi- tion areas [92], negatively impact species that make use of decaying
versity conservation [75], become invasive [24], drive soil water de- biomass [93], and indirectly drive deforestation as demand for biomass
pletion in dry areas [76] (e.g., Eucalyptus plantations in Australia [77] increases [81]. On the other hand, the use of plantations of native
and Miscanthus plantations in the Midwest USA) [78]) and emit con- perennials on low-biodiversity or degraded lands could enhance the
siderable amounts of air pollutants including PM, NOx, SOx, NH3, and provision of several ecosystem services including carbon storage and
VOCs [79]. Further negative impacts on key ecosystem services (e.g., pollination [94], as well as reduce the use of fertilizers and pesticides
water availability, disease and pest control, pollination, soil and water compared to conventional crops, allow the persistence of grassland or
quality) would be expected when replacing forests and grasslands with shrubland species, and reduce competition with food crops [33].
second generation biofuels [80]. Additionally, indirect land-use Third generation biofuels are mainly based on the use of microalgae
changes would likely occur if demands for forest biomass increase, (Box 5). This technology can be optimized to produce several types of
which would create incentives for further deforestation, particularly in biofuels, including biodiesel, bioethanol, biogas, and biohydrogen [95].
tropical regions [81]. Because of high microalgal biomass productivities, microalgal systems
Intercropping biofuels in agricultural areas or timber plantations require significantly less cultivation area to meet the same amount of
would also help in reducing competition with food production [33]. energy compared to first and second generation biofuel crops (Table 1),
However, they could disturb native species that make use of the plan- particularly in areas with high solar radiation and high mean annual
tations depending on management practices [90] and, under some temperatures [18]. They do not require fertile soils, and so are not

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Box 2
Factors that modify the environmental impacts of biofuel production.

The impacts of biofuel production on biodiversity and ecosystem services are modified by:

➣ Competing land-use: Determines how much GHG will be emitted [42] and how much biodiversity will be lost [19] after the replacement of
original systems by biofuel production systems. The transformation of native ecosystems leads to fragmentation, habitat losses, and large
CO2 emissions arising from losses in biomass and soil carbon contents [28]. The competition with agricultural lands increases the potential
for indirect land-use changes [43], leading to increases in CO2 emissions, further biodiversity losses and environmental degradation outside
biofuel cultivation areas [28].
➣ Spatial configurations of cultivation landscapes: Modifies the likelihood of species persistence at local and landscapes scales, as well as the
provision of ecosystems services. For instance, a combination of intensive production areas, agroforestry systems, and forest patches (i.e.,
land-sparing) has been proposed as a way to maintain regional biodiversity and ecosystem services for oil palm cultivation [25]. Alter-
natively, biofuel cultivation areas could be managed to promote higher biodiversity (i.e., land-sharing) [44]. Jager and Kreig [45] propose
the conservation of large patches of native ecosystems and the implementation of biological corridors at landscape scales (i.e., land-
sparing), along with the reduction of production intensity at the scale of parcels (i.e., land-sharing).
➣ Biofuel cultivation and conversion technologies: Determines how much GHGs will be saved in comparison to fossil fuels, as a balance
between inputs (e.g., fertilizers, energy used for converting feedstocks into biofuels) and products (i.e., biofuels and co-products) [21].
Affects water withdrawal [46] and the amount of emitted pollutants during the cultivation and processing of feedstocks [21], as well as the
overall environmental impacts associated with biofuel production [18].
➣ Cultivation management practices: Modifies the magnitude of ongoing GHG emissions depending on how much fertilizer is used [21] and
how soil is disturbed (e.g., frequent vs. sporadic soil tillage) [47]. For instance, Qin et al. [48] found that reducing tillage in USA maize-
soybean production systems can offset GHG emissions derived from corn stover harvesting. Affects soil erosion rates, as well as pollution
potential within and outside cultivation areas as a result of pesticide and fossil fuel use [18]. Impacts the persistence of native species
within production areas [26].
➣ Invasiveness potential: Affects the local and regional persistence of native species, as well as the resilience of natural systems and their
associated ecosystems services [24].
➣ Co-products: Affects the sustainability of biofuel production systems, as well as the emission of GHGs, pollutants, and energy efficiencies
[21]. Can help in offset GHG emissions [49] and reduce external energy inputs dependent on fossil fuels [50].

expected to drive direct or indirect land-use changes within agricultural Although several potential environmental impacts of large-scale
areas or biodiverse regions [96]. Several strains can be cultivated in microalgal production systems remain unclear (e.g., carbon balances,
brackish water or seawater [97], reducing competition with freshwater, nutrient use, invasiveness potential, pollution of aquatic ecosystems)
and their dependence on environmental pollutants such as pesticides is [50], the development of more efficient cultivation and processing
lower compared to other terrestrial crops [98]. Furthermore, microalgal technologies that make use of renewable energy sources can improve
production systems can make use of residual CO2 from industries (be- the net GHG balances of microalgal production systems [101]. Fur-
cause supplementing algae production systems with CO2 increases algal thermore, the recycling of culture media [102] and biomass residues
growth) and nutrients from wastewater, helping in carbon capture [99] (e.g., after lipids are extracted for biodiesel production), can reduce the
and water remediation [100]. use of freshwater [46] and fertilizers [69], while decreasing the risk of

Box 3
The controversial GHG emissions of biofuels.

In biofuel production systems, GHGs are emitted as a result of land-use changes [20], as well as during the cultivation of feedstocks [64], their
harvesting, and their processing into biofuels (i.e., CO2 emissions through soil disturbance, heterotrophic respiration, biomass combustion, and
the use of energy-intensive processes) [68]. Further CO2 emissions occur as a result of the production and transportation of inputs required for
biofuel production (e.g., fertilizers), the transport of biofuels to fuel stations, and the final burning of biofuels for energy production [21].
Other GHGs, including CH4, N2O, and CO, are additionally emitted during the production and use of biofuels [62]. Currently, the accounting of
GHGs derived from biofuel production as well as the definitive role of biofuel in climate change mitigation remain controversial [49].
However, in relation to CO2 emissions, some consensus exists:

➣ To offset the CO2 emitted by biofuel production, the carbon uptake during cultivation should be higher than the counterfactual reference
system [42]. For instance, in Southeast Asia, it would take between 86 and 423 years to fix the CO2 emitted when lowland rainforests and
peatland rainforests are, respectively, transformed into oil palm plantations [20]. Even in systems with lower carbon stocks (e.g., grass-
lands), carbon emissions would be substantial. Searchinger et al. [59] estimate that in 99.4% of Africa’s wet savannas more than 10 years
would be needed to fix the CO2 emitted following their replacement by second generation biofuels.
➣ CO2 emissions can decrease through the use of carbon-efficient cultivation and conversion practices and technologies. This includes the use of
systems with lower fertilizer use (e.g., soybean cultivation would need fewer fertilizers than maize) [21], the avoidance of detrimental soil
management practices that drive carbon losses (e.g., reduced soil tillage) [47], and the optimization of energy-intensive processes for
feedstock harvesting and conversion into biofuels (e.g., use of anaerobic digestion for nutrient recycling and energy production in mi-
croalgal production systems) [69].
➣ Carbon can be additionally captured and sequestered in long-term geological scales, for instance, using systems of bioenergy with carbon
capture and storage (BECCS) [70].

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Box 4
Future agricultural expansion, biofuels, and biodiversity.

Current species extinction rates are estimated at between 100 [4] and 1000 times greater [3] than those found in fossil records. For
vertebrates, around 25% of mammal species, 13% of birds and 42% of amphibians are currently classified under some extinction threat
category [82], and average losses in global population abundances are calculated at 58% between 1970 and 2012 [37]. Additionally,
20–50% of the original extent of nine of the 14 world’s biomes has been transformed into croplands, with a notable loss of tropical dry
forests, temperate grasslands, temperate broadleaf forests and Mediterranean forests [83]. As biodiversity continues to be negatively
impacted by human activities—as a result of land-use change, fragmentation of native ecosystems, pollution, occurrence of invasive
species, and climate change [83]—not only will more species risk extinction, but also ecosystem resilience will decrease, affecting the
provision of multiple ecosystem services and ultimately the human wellbeing [84].
Increases in food and energy demands are expected to drive further pressures on biodiversity and ecosystem services, particularly when
using biofuels derived from food crops [18]. Currently, around 34% of global terrestrial lands are used for agriculture, including 1.6 × 109
ha of rainfed and irrigated croplands, and 3.4 × 109 ha of pastures used for animal grazing [85]. At a population projection of around 9000
million people by 2050, it is expected that food demands will increase by more than 60% from 2006 levels [86], which could lead to an
expansion of around 70 million ha for croplands, assuming that yields rise within current production systems [85]. This expansion is
expected to occur mostly in tropical developing countries, placing additional pressures on tropical ecosystems [60].
Biofuel production systems that compete with agricultural lands are not only likely to threaten food production [87], but also are
expected to magnify the environmental pressures and impacts on biodiversity and ecosystem services [88].

Drivers

Increases in food demands Increases in energy demands

Agricultural Biofuel
expansion/intensification expansion/intensification

• Land-use change (direct/indirect), land-

use intensification
• Increases in greenhouse gas emissions
Pressures • Emissions of pollutants
• Water depletion
• Soil degradation
• Introduction of invasive/genetically
modified species

• Habitat loss for native species

• Losses in richness and abundance of native species
• Increases in extinction rates and number of threatened species
Impacts • Changes in ecology and population dynamics of species
• Alteration in the supply of multiple ecosystem services (e.g.,
carbon storage, water provision, erosion control)

Fig. 2. Magnification of pressures and impacts on biodiversity and ecosystem services exerted by the combined expansion of agriculture and first generation biofuels
for meeting food and energy demands. Pressures are defined as anthropogenic factors that induce environmental impacts, based on the DPSIR framework [89].

polluting aquatic ecosystems [96], and the cultivation of microalgae identification and implementation of biofuel production systems must
with low invasiveness potential can avoid unintended ecological ensure that overall socioeconomic and environmental benefits are
changes in surrounding aquatic environments [103]. achieved (Fig. 3). Price competitiveness, affordability [114], and re-
liability in comparison to fossil fuels [115] are essential for the de-
ployment of biofuel production systems. Systems that are able to meet
3. Identifying and implementing sustainable biofuel production biofuel production targets (i.e., based on their high production levels or
alternatives the availability of feedstocks), as well as those able to meet socio-
economic targets [116] (e.g., welfare improvement in biofuel producing
If humankind is to halt further biodiversity losses and overall en- countries and local communities) [117] (Box 6), could be preferred
vironmental degradation while limiting global warming [13], the

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Box 5
Microalgal biofuel production: Higher productivities per unit area than other biofuel production crops.

Prokaryotic (i.e., cyanobacteria) and eukaryotic microalgae (e.g., green algae, red algae, and diatoms) can be cultivated for producing
biogas, bioethanol, biodiesel, and biohydrogen [104]. Other products, including biochar, high-value compounds for human consumption,
as well as fertilizer or animal feed can also be produced from microalgae [105].
Algae growth requires CO2, light, and a growing medium with inorganic salts (i.e., water with nutrients such as nitrogen, phosphorus,
iron, and silicon) [106]. Maximum productivities are achieved at high light intensities and constant high temperatures (usually between 20
and 30 °C) [106], and at a pH optimal to each microalgal strain [95]. Biomass productivities increase when supplemented with CO2 [107],
and when growth conditions are optimized to control algal grazers [108] and enhance biomass and lipid productivities [109].
Microalgae are among the most productive photosynthetic organisms on Earth [106]. Estimates on lipid productivities range from
2100 L ha-1 y-1 when cultivating Spirogyra sp. in urban wastewater ponds in India [110] to 136,900 L ha-1 y-1 if growing species with high
oil content in photobioreactors [106]. According to Lundquist et al. [111] in theoretical optimal conditions biomass yields could reach
290 t ha-1 y-1 within the continental USA (i.e., oil yields equal to 126,000 L ha-1 y-1), assuming conversion efficiencies of 10% from solar
energy into biomass, high annual irradiances (i.e., at 7500 MJ m-2 y-1 in Yuma, Arizona) and cell lipid contents at around 40%. More
conservative maximum oil yields are estimated at between 24,000 and 27,000 L ha-1 y-1, which could be achieved within tropical countries
with high solar irradiance [112]. For instance, when cultivating Scenedesmus dimorphus under subtropical conditions (Brisbane, Australia) it
is possible to produce 72 t ha-1 y-1 of dry biomass, equivalent to around 19,400 L ha-1 y-1 (based on cell lipid contents at around 25% and oil
densities at 930 kg m-3) [113]. This means that the land footprint of microalgal production systems would be substantially lower compared
to any other biofuel production system, including first generation biofuels [18].

over others. Furthermore, biofuel production systems with lower en- while maintaining ecosystems services [94].
vironmental impacts [118], or even environmental benefits, could To facilitate the identification of sustainable biofuel production
contribute to achieve targets in carbon emission reductions, biodi- systems, a number of key knowledge gaps should be addressed:
versity conservation, and provision of ecosystem services [33]. These
systems would need to provide large net GHG savings (including the (i) Development and standardization of indicators [132] for assessing
avoidance of depleting existing carbon stocks in biomass and soil) the socioeconomic and environmental impacts of biofuel produc-
[119], avoid competition with agricultural lands [33], avoid direct or tion alternatives. For biofuels, multiple indicators have been pro-
indirect land-use changes in biodiverse areas [18], have low water posed in relation to soil and water quality, GHGs, air quality, and
footprints [120], and minimize pollution [21], soil degradation [121], productivity [133], as well as in relation to social well-being, en-
and invasiveness potential [122]. Systems that maintain biodiversity ergy security, trade, profitability, and social acceptability [134].
and ecosystem services in the broader landscape (i.e., within and out- However, a more comprehensive development of some indicators,
side plantations) [25] could reduce regional biodiversity losses [123] including those related to biodiversity and ecosystem services

Table 1
Cultivation area (thousand km2) for fulfilling total transport energy demands for biggest energy consuming countries in 2016 (i.e., countries that account for 80% of
world’s total transport energy consumption), based on first (1 G), second (2 G), and third generation (3 G) biofuels. The percentage of cultivation area (%) in relation
to each country’s land area is included. See Appendix A for details on calculations and Correa et al. [18] for comparisons with other countries.
Country 1G biofuels 2G biofuels 3G biofuels

Ethanol Biodiesel Ethanol Biodiesel Biodiesel

Wheat Maize Sugarcane Soybean Rapeseed Oil palm Switchgrass Miscanthus Jatropha Microalgae

Area % Area % Area % Area % Area % Area % Area % Area % Area % Area %

United States 10,094 106 2987 31 1922 20 14,119 149 11,014 116 – – 3524 37 1153 12 4681 49 622 7
China 2905 31 2422 26 1009 11 11,515 122 4997 53 1242 13 1679 18 549 6 2229 24 353 4
Russia 2003 12 989 6 – – 5000 30 2574 15 – – 531 3 174 1 – – 157 1
India 1483 47 1624 51 306 10 5707 180 2412 76 – – – – – – 673 21 66 2
Brazil 1629 19 800 9 265 3 1934 23 2096 25 390 5 – – – – 620 7 61 1
Japan 938 251 1308 350 308 82 3019 809 1609 431 – – 408 109 133 36 – – 83 22
Canada 948 10 294 3 – – 1455 15 934 9 – – 344 3 113 1 – – 108 1
Germany 372 104 277 78 – – 1811 508 496 139 – – 322 90 105 30 – – 89 25
Mexico 503 26 751 38 174 9 2370 121 1573 80 222 11 – – – – 396 20 39 2
Indonesia – – 457 24 200 11 2228 117 – – 155 8 – – – – 353 19 36 2
Saudi Arabia 374 20 377 20 – – – – – – – – – – – – 342 18 33 2
Iran 1256 77 309 19 135 8 1388 85 798 49 – – 252 16 83 5 335 21 34 2
France 319 58 235 43 – – 1102 201 416 76 – – 248 45 81 15 – – 52 10
United Kingdom 261 107 – – – – – – 374 153 – – 231 95 76 31 – – 68 28
Italy 462 154 182 60 – – 728 242 479 159 – – 203 68 67 22 – – 35 12
South Korea 546 544 343 341 – – 1457 1450 1118 1113 – – 199 199 65 65 – – 43 43
Australia 824 11 232 3 97 1 1096 14 805 10 – – 185 2 61 1 246 3 22 0
Spain 510 101 131 26 181 36 763 151 471 93 – – 174 34 57 11 – – 27 5
Turkey 498 64 150 19 – – 451 58 246 32 – – 150 19 49 6 – – 25 3
Thailand 1246 241 280 54 83 16 1104 213 – – 76 15 – – – – 188 36 21 4
Malaysia – – 149 45 163 49 – – – – 64 19 – – – – 161 49 17 5
South Africa 281 23 192 16 69 6 766 63 443 36 – – – – – – 141 11 14 1
Egypt 146 15 117 12 39 4 399 40 – – – – 105 11 34 3 140 14 13 1

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Socioeconomic Environmental
benefits AND benefits

Is the system profitable, reliable and Does the system enhance the
able to meet socioeconomic goals? environment?

Objectives

Maximization of socioeconomic Maximization of environmental

benefits benefits

• High greenhouse gas savings

• Capability to reach price competitiveness in • No/reduced competition with suitable
comparison to fossil fuels agricultural lands
Considerations

• Affordability to consumers • Avoidance of direct/indirect land-use

• Reliability of production system changes in biodiverse areas
• Capability to meet targets in biofuel • Low water footprint
demands • Low pollution potential
• Capability to meet socioeconomic goals • Low soil degradation potential
(e.g., welfare improvement in producing • Low invasiveness potential
countries and local communities) • Maintenance of biodiversity/ecosystem
services inside/outside production areas

Fig. 3. Criteria to be considered when evaluating the socioeconomic and environmental benefits of biofuel production systems.

[135,136], would improve the understanding of the overall en- assumptions, data sources, and calculation procedures in LCA, for
vironmental impacts of biofuel production, and facilitate the as- the development of meta-analyses able to draw valid conclusions
sessment of biofuel production sustainability [137]. The standar- on the overall environmental impacts of microalgal production
dization of indicators, which simplifies their selection and use, systems.
would benefit from the participation of stakeholders (i.e., (iii) Development of case studies that consider multiple socioeconomic
academy, government, industries, non-governmental organiza- and environmental objectives (e.g., taking into account targets in
tions, and communities) [138] and the understanding of the causal energy and food production, biodiversity conservation, and pro-
relationships between indicators and biophysical, socioeconomic, vision of multiple ecosystem services) in several locations.
and governance drivers [139]. Techniques for identifying multiple objective solutions include
(ii) Development of standardized assessments on the environmental multi-criteria decision analysis (MCDA) [144], multi-agent systems
impacts exerted by biofuel production systems. This includes the (MASs) [145], and integer linear programming [146]. These stu-
development of life-cycle assessments (LCA) that make use of the dies require the participation of stakeholders for defining objec-
same system boundaries (e.g., well-to-wheel studies that consider tives, environmental indicators, criteria [147], and their weights
cultivation, biofuel production, and final use of biofuels by con- (e.g., through analytical hierarchy process AHP) [148]. Further-
sumers), impact categories, and functional units [140]. These more, they would help to identify the synergies and trade-offs
standardized assessments would facilitate objective and measur- among objectives and criteria, for instance, between land and
able comparisons between different studies, as well as the devel- water requirements [149], between biodiversity and climate
opment of meta-analysis on the environmental impacts of several change mitigation [150], or among deforestation, CO2 emissions,
biofuel production alternatives [141]. For instance, Harris et al. nitrogen losses, water withdrawals, and food prices [151]. The
[142] report that there are insufficient empirical assessments to robustness and uncertainty of models and results can be assessed
determine the impacts of second generation biofuels on GHG through the development of sensitivity analyses [152]. To date,
emissions; while Tu et al. [143] indicate the need to harmonize several frameworks have been developed to facilitate the inclusion

Box 6
The social impacts of first generation biofuels.

Biofuel production has been linked to a wide range of negative socioeconomic impacts, closely related to those exerted by large-scale
farming systems. Controversies exist on the actual benefits of agricultural and biofuel expansion in developing countries, where rural
poverty and informal land tenure are prevalent [124]. While the production of biofuels can bring economic incentives to developing
nations and help in poverty alleviation through the creation of jobs [125], it can negatively impact land rights [81], drive rises in land
prices, as well as alienate, marginalize, and displace locals [126]. Biofuels have additionally been related to increases in food prices [54],
directly affecting smallholder farmers and urban dwellers in developing economies [127] that depend on external agricultural markets for
surviving [128].
However, it has been proposed that several of the impacts attributed to biofuel production rely on the weak governance of developing
nations to protect small landholders [117]. Several governance mechanisms—including policies that promote the diversification of land
production while preventing deforestation [129], or the implementation of certification schemes aimed at increasing social welfare in local
communities [130]—can help to reduce the reported negative socioeconomic impacts of biofuel production in the developing world [131].
In the face of future increased energy and food demands, the use of non-food crops for biofuel production would be expected to reduce
these impacts.

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Box 7
Microalgal cultivation systems (open ponds and photobioreactors).

Microalgal cultivation systems include open ponds, photobioreactors, and fermenters [170]. Raceway ponds are the most widely used type
of open ponds and consist on a closed recirculation channel, built in concrete or with plastic covering the earth, usually with a depth
between 15 and 30 cm, in which algae and growth medium are mixed by paddlewheels [95]. Microalgae concentrations are low, CO2 can
be added to the water for maximal productivity, and the temperature is not controlled although evaporation helps to cool the medium
[106]. Compared to photobioreactors, this system experiences higher water losses through evaporation, is less efficient in CO2 uptake, and
is more prone to contamination by other microorganisms, which results in reduced yields [105], but is considered a more cost-effective
option for biofuel production [50].
Photobioreactors can consist of a series of plates, tubes, bags, columns or domes set in particular arrangements that maximize sunlight
uptake. Algae concentrations are usually higher than in open ponds, the light intensity can be better optimized, the temperature can be
controlled, though energy or water use increase, and CO2 can be injected at several intervals in order to ensure continuous carbon uptake,
leading to higher biomass yields than those obtained in open ponds [95]. However, setup costs may be ten times higher than those
necessary for the construction of open ponds [95], and hence are considered less cost-effective to date [50].
Hybrid systems are based on the initial growth of microalgae in photobioreactors, avoiding contamination from other microorganisms,
followed by their cultivation in open ponds [171] (Fig. 4).

of multiple objectives in biofuel decision making. For instance, biofuel production costs are achieved by first generation biofuels,
Zhang et al. [153] developed a multi-objective and spatially ex- particularly for sugarcane bioethanol in Brazil and maize bioethanol in
plicit framework for biofuel production in Michigan, based on GIS, the USA, helped in part by government subsidies [160]. High costs for
biomass yields, and trade-offs among biofuels and ecosystem ser- converting lignocellulosic feedstocks into biofuels [160] and high ca-
vices; Perimenis et al. [154] developed a support tool for helping pital and operational costs for setting up microalgal production systems
decision makers in selecting more sustainable biofuel production [161], reduce the economic competitiveness of lignocellulosic and mi-
alternatives in Germany; and Garcia and You [155] developed a croalgal biofuel production systems. While production costs for su-
framework to select the most sustainable bioethanol production garcane in Brazil and maize in the USA have been calculated at between
alternative based on global life-cycle environmental impacts (i.e., US$ 5–9 and US$ 9–20 GJ-1, respectively, estimated production costs
land-use change and GHG emissions) and production costs. Ex- for lignocellulosic feedstocks and microalgal systems (i.e., often based
panding on this work by developing detailed case studies that on assumptions about production technologies and production costs)
consider a broad range of objectives and impacts would establish can range between US$ 19–62 and US$ 13–8949 GJ-1, respectively
an evidence-base for informing policy and planning decisions. [160]. For comparison, an oil price of US$ 100 barrel-1—a price which
(iv) Improved estimation of potential biofuel production at fine spatial has only been exceeded in 20% of months in the past decade [162]—is
scales, accounting for a wide range of factors that can impact both equivalent to US$ 17.12 GJ-1 (Low Heat Value LHV). To be competitive,
feasibility and yield [156]. Biofuel production is limited by the more sustainable biofuel production alternatives must approach cost
availability of lands for the cultivation of feedstocks [157], and the equivalence with its competitors.
availability of the several resources involved in their production, The cost-effectiveness of more sustainable biofuel production al-
including freshwater [158] and nutrients (e.g., nitrogen and ternatives is expected to benefit from increased scale efficiencies and
phosphorus) [159]. For instance, potential global bioenergy pro- learning rates as biofuel production farms enlarge and production
duction from wastes, including agricultural and forestry residues, technologies evolve. Historical trends show significant cost reductions
would be lower compared to energy crops (i.e., 25–221 EJ y-1 vs. that several biofuel production systems—including bioethanol produc-
22–1272 EJ y-1) [157] and may be further constrained after taking tion from sugarcane in Brazil and from maize in the USA—have ex-
into account environmental considerations for maintaining soil perienced as the industry matured, which is also expected to occur for
fertility, carbon stocks and biodiversity associated with decaying more sustainable biofuel production alternatives [163]. For second
biomass [75]. The understanding of these limits and uncertainties generation biofuels, the development of more cost-effective conversion
can help decision makers choose biofuel production alternatives technologies based on the transformation of lignocellulosic feedstocks is
able to meet substantial amounts of fuel demands. needed [164]. For microalgal production, the cultivation of highly
(v) Development of standardized and integrated global assessments of productive microalgal strains [106] and the co-location with in-
the impacts of biofuel production considering complex socio- expensive CO2 and nutrient sources (i.e., co-locating microalgal culti-
economic and ecological systems (e.g., integrated assessment vation systems with CO2 from industries and nutrients from waste-
modeling IAM) [88]. These assessments would facilitate the un- water) improve the profitability of microalgal production systems
derstanding of the complex actual and potential impacts of biofuel [165], particularly for open ponds (Box 7) [50]. Reductions in pro-
production alternatives at multiple spatial and temporal scales. For duction costs between 35% and 86% can be achieved if CO2 from in-
instance, based on the Shared Socio-Economic Pathways (SSEPs) dustries and nutrients from wastewater are obtained for free [165].
Popp et al. [70] suggest that high levels of bioenergy production Additionally, more efficient cultivation methods (e.g., using less en-
modeled on second generation biofuels can be achieved with low ergy-intensive mixing techniques for promoting microalgal growth)
impacts on ecosystems, if future demand for agricultural com- [166], along with low-cost harvesting and de-watering methods [50]
modities remains low, if agricultural productivity increases, and if and the development of profitable co-products (e.g., animal feed and
globalized trade is maintained. biogas) [167], can increase both the profitability and sustainability of
microalgal biofuel production [168]. For instance, the defatted residues
that remain after lipids are extracted for biodiesel production can be
4. Economic profitability: a current barrier to the deployment of used as a substrate for biogas generation and for nutrient recycling (i.e.,
more sustainable biofuel production systems following anaerobic digestion) [69]; this biogas can either be sold or
used as a source of energy and CO2 for algae cultivation, reducing en-
Economic profitability is the main barrier to the deployment of ergy costs and increasing microalgal growth, while nutrient recycling
more sustainable biofuel production systems. Currently, the lowest

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Fig. 4. UQ Algae Energy Farm at Pinjarra Hills, Brisbane, Australia (Algae Biotechnology Laboratory, University of Queensland). Cultivation is based on open ponds
(a) following initial growth in sealed bags and a series of smaller ponds (b).

reduces the dependence on fertilizers [169]. (i) The introduction of biofuel blending mandates that require sus-
Several strategies can facilitate the transition of transport systems tainable biofuel production methods, following a comprehensive
based on fossil fuels and first generation biofuels to systems based on evaluation of their socioeconomic and environmental benefits
sustainable biofuels and electricity (Fig. 5) [172]. In the short term, the [176]. For instance, by 2020 the European Union aims to meet
development and commercialization of high-value products can provide 10% of total transport energy demands using renewables based on
profits and enable scaling of production. For lignocellulosic biomass, a the use of biofuels that do not drive direct or indirect land-use
biorefinery system, in which value-added products such as bio-oil, changes in biodiverse and carbon-rich regions, and that ad-
biochar, and other bio-based chemicals can be produced, is expected to ditionally deliver GHG savings of at least 35% in comparison to
increase the profitability of second generation biofuels [173]. Similarly, fossil fuels (and from 2018, of at least 60%), considering the cul-
for microalgal production systems, a biorefinery-based production tivation, processing, and transport of biofuels [177]. The devel-
model [174], in which different types of biofuels are produced (e.g., opment of these mandates should consider synergies and trade-offs
biogas and biodiesel) [69] or high-value products for food consumption among biofuel production, socioeconomic, and environmental
and animal feed (e.g., omega-3 fatty acids, pigments, proteins, and goals; for instance, among biofuel cultivation, restoration of de-
fishmeal) are produced along with biofuels [161], can increase the graded lands [178], ecosystem services [179], and biodiversity
profitability of microalgal biofuel production. conservation [180].
Several policies can be implemented to promote the deployment of (ii) The taxation or subsidizing of energy systems based on their en-
more sustainable biofuel production systems, as has already occurred vironmental impacts. This would include the elimination of fossil
for first generation biofuels in the USA, Brazil, Europe, and other fuel subsidies, the implementation of disincentives to less sus-
economies [175]. They include: tainable biofuels (e.g., through carbon taxation schemes) [181]

Short-and mid-term Long-term

• Substitution of fossil fuels and

Objectives

first generation biofuels by

• Development of cost-effective and more sustainable more sustainable biofuel
biofuel production technologies. production alternatives and by
electricity-driven transportation
systems.

• Development and commercialization of high-value

products that allow short-termeconomic profits and
Strategies

maturation of technologies.
• Development of policies for promoting the use of
sustainable biofuel production alternatives:
mandates, taxation, subsidizing, financial market-
based mechanisms, partnerships.

Fig. 5. Strategies for promoting the implementation of more sustainable biofuel production alternatives in the short and long term.

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and the subsidizing of more sustainable biofuel production alter- environmental impacts of biofuels) [190]. At the global scale, the bio-
natives while the subsidies for first generation biofuels gradually fuel industry can be supported through the development of interna-
decrease [182]. This can boost the deployment of promising more tional standards to facilitate accreditation of fuel sustainability [130],
sustainable biofuel production systems while they become eco- markets to support international trade of sustainable biofuels [191],
nomically competitive [183]. and trade agreements to ensure that pricing of sustainable biofuels re-
(iii) The implementation of financial and market-based mechanisms for mains competitive [192]. Furthermore, the development of interna-
promoting the development of sustainable biofuel production al- tional agreements based on sustainability goals (e.g., the Paris Agree-
ternatives. For instance, the use of contracts for difference (CFDs), ment, to which most countries are signatories) provides strong
in which biofuel producers enter a 10-year contract with govern- incentive and justification for fostering the growth of more sustainable
ments following reverse auctions, has been proposed as a more biofuel production systems.
cost-effective alternative for financing the setup of ultralow-carbon National energy policy is fundamental to drive the transition to
biofuels in California in comparison to capital grants [184]. Other sustainable biofuels [193]. National mandates on biofuel blends based
mechanisms include the integration of novel and more sustainable on stringent biofuel sustainability standards [194] can encourage the
biofuel production systems with carbon markets [185] and sus- implementation of sustainable biofuels. The gradual replacement of
tainability certifications schemes [130], which can increase their fossil fuels and first generation biofuels can be facilitated through: (i)
profitability based on environmental advantages (e.g., reductions National-level policies that provide disincentives to fossil fuel and un-
in GHG emissions) compared to less sustainable energy production sustainable biofuel production (e.g., through carbon taxation schemes)
alternatives. [181] and (ii) national-level incentive programs that promote sustain-
(iv) The development and strengthening of partnerships between gov- able biofuels, including the subsidizing of sustainable biofuel produc-
ernments, universities, and industries, for promoting research and tion, the development of financial and market-based mechanisms
innovation aimed at developing more profitable and sustainable mediated by governments in favor of sustainable biofuels [184], and
biofuel production alternatives [186]. the funding of applied research to develop cost-effective and sustain-
able biofuels [195].
5. Articulation of policies at the global, national, and regional Regional level policy is critical to ensure that the growth of the
level biofuel industry occurs in a strategic way, avoiding biodiversity im-
pacts, competition for agricultural land, non-sustainable use of re-
The transition to a more sustainable transport sector can be fostered sources (e.g., freshwater), and negative socioeconomic impacts [189].
through the development of strategic policies that promote the adop- Regional policy can also manage trade-offs among multiple stake-
tion of sustainable biofuel production alternatives that are able to re- holders and potential conflicts among industries [196], as well as help
duce environmental impacts and halt competition with food production to regulate the growth of biofuels and certificate sustainable biofuels
[187]. The articulation of policies at global, regional, national, and [130].
local scales is a necessary step for guiding the implementation of sus-
tainable biofuels (Fig. 6). The development of an updated global 6. Conclusions
roadmap on sustainable biofuels [188] could guide nations in im-
plementing policies in accordance with global multi-objective targets Bioenergy production is expected to increase from 9.7 × 106 to 4.6
while balancing local socioeconomic and environmental needs [189]. × 107 GJ d-1 between 2016 and 2040 [10], and how biofuels are
Because the impacts of biofuel systems are still a matter of debate, this produced will determine their overall environmental impacts. The im-
roadmap must be subject to adjustments as new evidence on the im- plementation of more sustainable biofuel production systems, which
pacts of biofuels is established (i.e., through the development of an currently include sustainably sourced wastes, native perennial crop,
adaptive framework on the global and local socioeconomic and and microalgal production systems produced on low-biodiversity or

GLOBAL SCALE

• Development of a global roadmap on sustainable biofuels.

• Development of an adaptive framework on the socioeconomic and environmental
impacts of biofuels.
• Development of international sustainability standards.
• Strengthening of markets and trade agreements for sustainable biofuels.
• Development of international sustainability agreements.

NATIONAL SCALE

• Implementation of mandates on sustainable biofuel blends.

• Taxation/subsidizing of biofuels based on their sustainability.
• Development of financial and market-based mechanisms to favor
sustainable biofuels.
• Research funding for developing cost-effective and sustainable biofuels.

REGIONAL AND LOCAL SCALE

• Management of trade-offs among industries, regulation in biofuel growth,

certification of sustainable biofuels.

Fig. 6. Articulation of policies at the global, national, regional, and local scale towards the implementation of sustainable biofuels.

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