Renewable and Sustainable Energy Reviews 46 (2015) 30–40

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews

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

A synthesis of the ecosystem services impact of second generation

bioenergy crop production
R.A. Holland a, F. Eigenbrod a, A. Muggeridge b, G. Brown b, D. Clarke a, G. Taylor a,n
a
Centre for Biological Sciences, Life Sciences Building, University of Southampton, Southampton SO17 1BJ, UK
b
Department of Earth Sciences & Engineering, Imperial College London, London SW7 2AZ, UK

art ic l e i nf o a b s t r a c t

Article history: The production of bioenergy from second generation (2G) feedstocks is being encouraged by legislation
Received 19 August 2014 targeted at addressing a number of controversial issues including carbon emissions driven by land-use change
Received in revised form and competition for crops used in food production. Here, we synthesise the implications of 2G feedstock
19 December 2014
production for a range of key ecosystem services beyond climate regulation. We consider feedstocks typical of
Accepted 1 February 2015
temperate systems (Miscanthus; short-rotation coppice, short rotation forestry) and transitions from areas of
Available online 3 March 2015
forest, marginal land and first generation (1G) feedstock production. For transitions from 1G feedstocks, studies
Keywords: suggest significant benefits may arise for a number of ecosystem services, including hazard regulation, disease
Biofuel and pest control, water and soil quality. Although less evidence is available, the conversion of marginal land to
Ecosystem services
2G production will likely deliver benefits for some services while remaining broadly neutral for others.
Miscanthus
Conversion of forest to 2G production will likely reduce the provision of a range of services due to increased
Short rotation coppice
Short rotation forestry disturbance associated with shortening of the management cycle. Most importantly, further research is needed
Land use to broaden, and deepen, our understanding of the implications of transitions to 2G feedstocks on ecosystem
services, providing empirical evidence for policy development, particularly for commercial deployment where
landscape scale effects may emerge. A programme of research that mixes both the natural and social sciences
based on an ecosystem service framework, and occurs concurrently with large scale commercial deployment
of 2G feedstocks, would address this gap, providing evidence on the effectiveness of policies to promote
production of 2G feedstocks on a wide range of ecosystem services.
& 2015 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31
3. Global overview of research and identification of knowledge gaps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32
4. Priority ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
4.1. Crops and livestock . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
4.2. Timber and forest products. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
4.3. Water availability. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
4.4. Hazard regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
4.5. Disease and pest regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
4.6. Pollination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
4.7. Soil quality regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34
4.8. Water quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35
5. Synthesis—Implications of 2G feedstock for ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36
6. Outlook—Defining a research agenda for 2G feedstocks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

n
Corresponding author at: Centre for Biological Sciences, University of Southampton, Southampton SP10 1BJ, UK. Tel.: þ44 2380592335.
E-mail address: g.taylor@soton.ac.uk (G. Taylor).

http://dx.doi.org/10.1016/j.rser.2015.02.003
1364-0321/& 2015 Elsevier Ltd. All rights reserved.
 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40 31

7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
Appendix A. Supporting information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38

1. Introduction
The importance of incorporating ecosystem services into ana-
lysis of the implications of 2G feedstock deployment stems from
Meeting the world’s growing energy demands while reducing the realisation of the value of these services to society, and the
the environmental impacts associated with energy production and concurrent understanding that many services are in decline or
use [1] is a key societal challenge for the next 50 years [2]. It is threatened [20,21]. A notable exception to this trend is crop,
within the context of environmental sustainability, alongside livestock and timber production [20,21] which has seen a dramatic
energy security, that the recent upsurge in production of bioe- increase over the last few decades due to modern production
nergy – particularly biofuel for transport – has emerged. Although techniques. This increased production has come at a cost, with
biofuels have been used in transport since the early 20th century, these resources now considered to be principal drivers of environ-
the last few decades has seen a dramatic increase in production [3] mental degradation and loss of biodiversity [23] with associated
from 314,567 barrels per day (BPD) in 2000 to 1897,202 BPD in implications for the delivery of many ecosystem services [24,25].
2011 [4]. This has been driven by a number of factors including an As trade-offs between the delivery of different ecosystem services
increase in oil price over the same time period potentially making are inherent [26–28] decisions about the deployment of energy
biofuel economically competitive, by policy commitments to technologies must be based on knowledge of implications for a
increase energy security, and as a mechanism to reduce green- broad range of services, providing policy makers and managers
house gas (GHG) emissions [5–7]. with the ability to balance competing environmental and societal
Concurrent with increased production of biofuel, a number of goals. Here we consider both the evidence available and how
significant societal and environmental issues associated with first incorporating a broad range of ecosystem services can provide
generation (1G; food and feed) based feedstocks have emerged [8– such a perspective on the implications of 2G feedstocks.
10]. First, additional demand for food and feed based crops to
produce biofuel may have contributed to increased food prices and
threatened food security through multiple pathways [11,12]. 2. Methods
Second, compared to conventional fossil fuels, relative life cycle
carbon emissions of some feedstocks have been questioned. By The aim of this synthesis is to consider the implications for
incorporating land-use change into emission calculations studies ecosystem service provision of land-use change associated with
suggests they can release as much, or more, carbon as conven- conversion to 2G feedstock production. Specifically we consider
tional fuels [13–15] leading to significant “pay-back” times before land-use change from three references states representing likely
carbon savings are realised [14]. transitions within Europe and specifically the UK: (i) arable land
In response to such emerging issues, the European Union (EU) (i.e. used in the production of crops destined for food or feed
has proposed a significant policy shift that would reduce the use of production or as 1G feedstocks), (ii) marginal land, (iii) forest (both
1G feedstocks from 10% to 5% [16]. Although implementation is plantation and natural). Our review uses the framework of the
still being debated, with a final decision due in 2015, the policy is Millennium Ecosystem Assessment [21] that divides ecosystem
intended to encourage the development of the second generation services into provisioning, regulating, supporting and cultural
(2G; dedicated lignocellulosic) feedstock industry. This is consis- categories, although for policy relevance we identify services
tent with long term roadmaps for energy production that point to representing those considered in the UK National Ecosystem
an increasing role of 2G feedstocks in the medium term, driven by Assessment [20]. This approach frames the question within a
factors such as energy security and blend mandates, coupled with context that policy makers are familiar with, although we recog-
technology innovations such as selective breeding for yield and nise that a number of alternate classification systems, such as the
biomass densification [17]. Common International Classification of Ecosystem Services (CICES)
Given the environmental and societal issues associated with [19], exist.
energy production [18], and specifically issues of food security and Searches were performed in Web of Science (WoS) during
climate regulation, the concept of ecosystem services provides a December 2014 using the ecosystem service keywords detailed
framework to examine the implications of transitions to 2G feed- in Table 1 together with ‘biofuel’, ‘biodiesel’, ‘bioethanol’, and
stock production [8]. Although a number of different classification ‘bioenergy’. In using these latter terms our aim was to capture a
schemes exist [19–21] broadly speaking ecosystem services can be representative sample of studies that examine effects of biofuel
divided into four main categories; (i) provisioning services such as feedstock production on ecosystem services. Although our focus is
crops and livestock, water availability and timber and forest on candidate feedstocks for Europe and the UK, this broad
products; (ii) regulating services such as disease and pest control, approach captures studies that consider the implications of
hazard regulation and pollination; (iii) supporting services such as analogous crops deployed in other regions of the world.
nutrient and water cycling; (iv) cultural services such as heritage Our search strategy was designed to be neutral in terms of
goods and recreational opportunities [20]. In the current study the land-use due to problems associated with terminology. While
term ecosystem services is used as a general term that encom- studies relating to transitions from arable and forest can be readily
passes the pathway from ecological processes to the delivery of identified, there is inconsistent use within the literature of the
benefits to humans [22]. However, as our synthesis does not term “marginal” land. The importance of capturing studies that
examine specifics of the social and economic systems in which consider marginal land arises from the fact that such land is stated
the ecosystem services are being provided, our discussion is as being crucial for 2G feedstock production [29–31]. A number of
concerned with the pathway to final ecosystem services [19,22] definitions of marginal land exist (see [32,33]), with the interplay
from which goods and benefits to society will flow. of a range of factors leading to its characterisation as an area that
32 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40

Table 1
Impact of second generation feedstock production on the provision of ecosystem services following transitions from reference conditions. (Blank cells indicate no returned
studies based on our selection criteria.)

Ecosystem service Keywords WoS hits Replace arable Replace marginal Replace forest

þ  N þ  N þ  N

Crops and livestock Livestock or food or fibre or pasture or forage 1422 1 3 1 1

Fisheries Fisheries or fish 166
Aquaculture Aquaculture or fish 226
Timber and forest products Timber or forest or forestry or fungi 1217 1
Honey production Bees or honey 23
Water availability Water quantity or water availability 214 4 1
Ornamental resources Flowers or horticulture 33
Climate regulation Carbon or greenhouse gas or nitrogen or evapotranspiration or albedo 5326 32 7 4 6 8 2 1 5 1
Hazard regulation Erosion or flooding 152 9 1 1
Disease and pest regulation Pests or disease 200 7
Pollination Pollination or pollinators or bees 44 5
Soil quality regulation Soil or soil cycling or nutrient cycling or carbon 4762 5 2 8 9 1 3 1
Noise regulation Noise 24
Air quality regulation Particles or ozone or ammonia or nitrogen or sulphur or air quality 2615 4 1 2 3
Water quality regulation Eutrophication or water quality 510 10 2 0 4 1 1
Soil formation Soil formation or dissolved organic carbon or DOC or weathering 171
Nutrient cycling Nitrogen cycle or nitrogen or mineralisation or phosphorous 1964 3 4 2
Water cycle river or water cycle or lake or groundwater 563 3
Primary productivity Primary productivity 60 3
Religious and spiritual National parks or protected areas or spiritual 25
Heritage goods Community or cultural or heritage 424
Landscape Landscape or national parks or protected areas 278 1
Human health Human health or health 227 5
Leisure and tourism Leisure or tourism or national parks or protected areas or recreation 181

has: (i) previously been used for agriculture then abandoned,
perhaps for social or economic reasons, (ii) could not be used for
crop production due to specific environmental constraints, or (iii)
where land is in a degraded state [30,34]. However, the use of the
term within the literature, together with the complexity of the
definition [30,34], has the potential to exclude relevant studies
from a keyword search. For this reason omitting terms relating to
land-use was considered the most appropriate strategy. Instead
returned studies were classified into relevant land-use transitions
based on a detailed examination of site descriptions within
their text.
In total the WoS search returned 20,827 references, with some
appearing across multiple categories. These were first filtered
based on the title and abstract to identify those that relate to 2G
feedstock production. Where possible the full text of the remain-
ing studies was obtained, and a second stage of filtering carried
out to identify those that considered the implications for the
identified land-use transitions. We included two different cate-
gories of study in these criteria, representing two ways that
transitions from a reference state to 2G feedstock production can
be examined. First, a true transition, where studies measured
changes over time in the provision of ecosystem services during
conversion of an area from one of our defined reference states (i.e.
arable, marginal, forest) to 2G feedstock production. Second,
studies that used a space for time substitution comparing ecosys-
tem service provision under a reference state to provision under
2G feedstock production using comparable areas in close proxi-
mity. Fig. S1 provides a decision tree that details this process (see
Supplementary online material).
For each study we captured the ecosystem service examined,
the specific feedstock, the geographic location, the land-use
transition and whether the study used empirical data collected
in the field or was based on a modelling approach. If a study
considered more than one feedstock, ecosystem service, geo-
graphic location or land use transition we disaggregated the
results to capture individual reported effects. With reference to
the land-use transition we initially classified studies based on
three categories, arable land, marginal (see discussion above) and
forest. Based on detailed site descriptions from the text we further
subdivided studies of marginal land to identify those that dealt
specifically with grassland systems.
3. Global overview of research and identification of knowledge
gaps
In total 61 unique studies met our criteria, reporting 179 effects
comparing 2G feedstock production against a reference state. As
shown in Table 1 these effects were unevenly distributed with the
majority relating to regulating services (specifically climate reg-
ulation). One hundred and twenty one effects were reported for
transitions from arable production, 45 for transitions from mar-
ginal land to 2G feedstocks, and only 13 for transitions from forest.
In terms of feedstock, switchgrass (42), Jatropha (21) and Mis-
canthus (41) dominated the research followed by a mix of other
energy grasses (38), then short-rotation coppice (SRC) and short-
rotation forestry (SRF) feedstocks (32). Geographically most
research has been carried out in the USA, a number of European
countries and in tropical and sub-tropical countries such as
Argentina, Brazil and Indonesia that have significant bioenergy
markets. As shown in Table 1 studies examining conversion from
arable to 2G feedstock production return more positive than
negative effects on ecosystem services. Across other transitions
there is a broadly equal balance between positive, negative and
neutral effects, although there are only a small number of studies
within these categories.
In the remainder of this synthesis we consider the implications
of transitions to 2G feedstocks in the UK and Europe for a number
of key ecosystem services. Our choice of service are based on those
that are priorities for legislation (e.g. water quantity and quality,
soil quality), have significant market value or costs associated with
them (e.g. crops and livestock, timber and forest products, hazard
regulation), and are priority research areas (e.g. pollination, dis-
ease and pest control). This choice is also pragmatic as such
services are readily mapped and data collected as part of environ-
mental monitoring programs. As a considerable number of reviews
 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
have examined greenhouse gas emissions [35–38] and biodiversity
[39–41] we do not consider these services further within the main
review. However, to facilitate comparison of synergies and trade-
offs between services we incorporate information from these
studies within the Supplementary online material.
We focus on the major candidate 2G feedstocks for temperate
environments such as the northern USA and Europe, including the
UK, namely Miscanthus, SRC and SRF. The 72 effects relating to
transitions to these feedstocks returned in the WoS search were
supplemented with findings from studies of analogous crops and
systems, as mechanisms identified can be used to infer effects in
different systems where there is limited or no research. For
example, studies detailing changes in water availability associated
with transitions from arable to 2G feedstocks production (e.g.
[42,43]) identify specific mechanisms relating to crop character-
istics that are likely relevant under other land-use transitions.
4. Priority ecosystem services
4.1. Crops and livestock
Of the three sets of transitions, impacts on crops and livestock
production will be most strongly associated with transitions from
arable and marginal land. Six studies described such transitions
with four considering transitions from arable [44–47], three
transitions from marginal land [48–50] and one from forest [51].
Although the production of bioenergy feedstocks fall within this
category, we restrict our consideration to other crop and livestock
production.
A series of studies in the UK suggest that utilizing marginal
land provides considerable scope for expansion of 2G feedstock
production without impacting food supplies. For example Ref. [52]
found that growing SRC on poor quality, marginal land could
release an additional 0.8 million ha of land producing 7.5 million
tons of biomass with limited impact on arable food production.
Similarly, Ref. [53] concluded that growing Miscanthus on low-
grade agricultural land in the UK would allow production of
350,000 ha without a significant impact on food crops. However,
understanding the limits within which 2G production can occur
before impacting food production is complex with around 36% of
global agriculture being located in such areas [30]. Of particular
importance is the role that marginal lands play in food production
mediated through herbivores, animals that are able to transform
low-quality plant proteins into meat and milk for human con-
sumption [54]. As Ref. [55] considers, 22.3 million ha of marginal
land will be needed to meet targets for bioenergy by 2030 in the
USA creating direct competition with traditional forage-livestock
production. Widespread conversion of marginal land for 2G feed-
stock production could therefore exert considerable pressure on
this sector of the food industry. It is suggested that such transitions
could disproportionally impact those people occupying the socio-
economic margins [48], although such impacts are likely most
relevant in developing countries.
Government incentives emerge as a key mechanism through
which land use transitions could influence crop and livestock
production, and more broadly the provision of multiple ecosystem
services [56]. For example Ref. [57] details a loss of dairy farming
in Sao Paulo state in Brazil driven by incentives for sugarcane
production from the Brazilian government. Similarly, promotion of
Jatropha production in India has led to displacement of food crop
production, which combined with low yields from the feedstock,
has negatively impacted farmers [44]. Such a scenario is predicted
to occur in the Murray–Darling area of Australia based on model-
ling the economic profitability of both food and bioenergy agri-
culture under a number of carbon pricing and climate scenarios
33
[58]. Under baseline climate scenarios, a farm subsidy designed to
promote GHG abatement through the production of bioenergy
could lead to the loss of the most productive food producing areas
as it becomes economically more favourable for farmers to
produce bioenergy feedstocks. As a principal driving force behind
adoption of 2G feedstocks is to decouple the food and bioenergy
markets, such studies raise the question of whether policy incen-
tives promoting 2G feedstocks may impact food production
through this alternate displacement pathway.
4.2. Timber and forest products
Forests are key resources that provide timber for a range of
activities such as construction and the paper and pulp industry. It
is unlikely that there will be large scale transitions of forests to
Miscanthus, particularly in Europe where policy is designed to
increase afforestation. Conversion of existing plantation forestry to
SRC and SRF for 2G feedstock production represents the most
likely pathway that will influence the provision of timber and
forest products. Here the increased intensity associated with
shorter management cycles of SRC and SRF, and the shift from
removal of only traditional products such as saw logs and pulp-
wood to a higher proportion of the forest biomass, is likely to
significantly impact forest systems [59]. Impacts will be associated
with the provision of other ecosystem services such as recreational
opportunities, hazard and climate regulation that forests provide.
More broadly, over the coming decades elevated carbon diox-
ide concentrations, longer growing seasons, together with disease
and pest outbreaks are predicted to have significant implications
for the global timber inventory [60]. As a results increasing
demand for timber (of which bioenergy feedstock production is
one component), may lead to convergence of fuelwood and
roundwood prices leading to the appropriation of resources
currently used for timber, paper and pulp production for use in
energy [61]. This in turn would drive increased extraction impact-
ing the health of forest systems and associated ecosystem services,
and reduce the availability of a primary source of household
energy of particular importance for the world’s poorest people.
Indeed, Ref. [59] considers that such global supply chain issues
will, in the absence of regulatory frameworks designed to protect
people in less developed areas, be one of the principal impacts of
increased use of forest resources for the production of bioenergy.
4.3. Water availability
Although a limited set of studies met our criteria for inclusion
[42,43,49,62,63] there is a well-developed literature that considers
the implications of 2G feedstocks on water resources. At the
landscape scale, intensity of production will have a significant
influence on water resources. Assuming uniform production across
the landscape, Ref. [63] demonstrates that replacement of 10% of
US agricultural land with Miscanthus, leading to production
capacity sufficient to meet government targets for bioenergy
production [64], would have little or no effect on the hydrological
cycle. However, such a uniform distribution is unrealistic as, for
economic and energetic reasons, production of 2G feedstocks is
likely to be clustered around biorefineries [63,65]. In this more
realistic deployment pattern conversion of 25% (in water stressed
areas) to 50% (in all remaining areas) of existing land cover
to Miscanthus would have a severe impact on the hydrological
cycle [63].
Negative impacts on water resource arise due to the crop
characteristics of 2G feedstocks such as Miscanthus, SRC and SRF.
For example, although Miscanthus has been demonstrated to
possess a water use efficiency (WUE) similar to 1G feedstocks
[42,66], it is characterised by a higher evapotranspiration rate due
34 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
to a large root system, high leaf area index, long growing season
and strong coupling with the atmosphere due to its height [67,68].
Although high WUE is desirable in conditions where water is not
limited [63], the higher absolute requirements of 2G feedstocks
mean they can have a significant negative impact in water
stressed areas.
Impacts on water resources will manifest themselves primarily
during the growing season, consistent with increased evapotran-
spiration, so are contingent on seasonal patterns of water avail-
ability within the landscape [59,69,70]. A study by Ref. [71], using
a network of 14 field trial sites across the UK, developed an
empirical yield model for Miscanthus that demonstrated a strong
link between soil available water content, precipitation and Mis-
canthus yield. The model of Ref. [71] suggests that a 40% reduction
in yield may arise if the crop is subjected to summer drought. For
this reason trade-offs between conservation of water resources
and biomass production will play an important part in determin-
ing the suitability of production in a specific area. Assessing water
resource availability should therefore be a major criteria in
determining deployment strategies [12].
4.4. Hazard regulation
Two interlinked regulating processes can be considered under
hazard regulation: first the control of erosion by wind and water,
and second flood risk regulation. Changes in erosion control arise
primarily through changes in agricultural practices [62,72] with
2G feedstocks such as Miscanthus [43,73] and SRC or SRF
[59,74,75] expected to enhance the provision of this service in
comparison to 1G feedstocks. Second generation feedstocks
require no annual tillage, provide year round soil cover (in the
case of woody feedstocks) and exert a positive influence on many
soil properties including the improvement of water fluxes result-
ing in a reduction in surface runoff [76] and changes in the size
and stability of aggregates reducing wind erosion [75,77].
Conversely, land-use change that results in a shortening of the
management cycle, such as transitions from forest to 2G feed-
stocks, would likely reduce the provision of this service [78]
although impacts will be most significant during the establish-
ment and harvesting phase [59,79]. Best practice in protecting
hazard regulating services is likely to be an approach that selects
feedstocks with longer management cycles than current land-use
and constrains production to areas not prone to erosion.
4.5. Disease and pest regulation
Our WoS search found few studies that used a reference state
approach to examine disease and pest regulation associated with
2G feedstock production [28,47,80–82]. A review of the available
literature by Ref. [83] found evidence of enhanced activity of
natural enemies associated with the presence of herbaceous and
woody habitats within the landscape, suggesting that a diverse
landscape including 2G feedstock production could be beneficial
for this service. This link was explicitly examined in a number of
studies in the USA that compared 1G feedstock production to
perennial grasslands, demonstrating enhanced pest regulations in
the latter [28,82] and distinct landscape effects. In one of the few
studies to systematically examine the effect of commercial 2G
feedstock production on biodiversity, the presence of SRC planta-
tions and perennial grasses within the landscape increased the
number of Hymenoptera and large Hemiptera species [84].
Although the authors did not explicitly examine pest regulation,
the presence of these groups would likely enhance predation,
contributing to pest control.
Placing 2G feedstocks within food crops creates a diverse range
of habitats within the landscape promoting predators and
parasitoids including arthropods, birds, mammals and microbial
pathogens [26]. More broadly the review of Dauber et al. [40]
together with a number of studies [39,85,86] suggest that conver-
sion of arable and grassland to 2G feedstock production (Mis-
canthus, SRC) can increase biodiversity of certain groups that
contribute to natural pest control. Such statements must be
qualified by considering that the relationship between biodiversity
and pest control is far from clear [83], with debate centred on the
importance of a few key species as compared to a diverse
community [87,88]. What is perhaps clearer is that the effect
could manifest itself through areas of 2G feedstocks within the
landscape providing a source for re-colonisation of food crops by
beneficial species following application of chemicals or harvesting
[89].
Of course, 2G feedstocks will harbour both pests of the feed-
stocks themselves, as well as natural enemies of such pests, with
densities of both depending on management [85]. For imported
feedstocks such as Miscanthus, associated pest species may no
longer be under control of enemies that occur in their natural
range, and so pose a threat to both the feedstock and other crops
or vegetation that the pest species can exploit [89]. Emerging
evidence of a number of parasitic nematodes [90] that could
reduce productivity of Miscanthus suggest that our assumption
of resistance to pests for 2G feedstocks may be incorrect. As the
relatively low inputs of agrochemicals associated with 2nd gen-
eration crops are responsible for many of the suggested environ-
mental benefits, these findings could undermine one of the key
arguments for 2G feedstock deployment.
4.6. Pollination
Globally it is estimated that insect-provided pollination ser-
vices are worth over $200 billion dollars per year [91]; with
around 84% of crop production in Europe [92], and 60% globally
[93] dependent on this service. Pollination is often cited as an
example of an ecosystem service that is under threat, with both
managed and wild pollinator numbers showing severe reductions
over the last 30 years [20].
For transitions from arable production the extended rotation
times, reduced tillage and increased understory vegetation asso-
ciated with 2G feedstocks should benefit pollinator species
through mechanisms such as increased diversity of nectar and
pollen sources, and provision of nesting and overwintering sites
[84,93–97]. However, as demonstrated for Miscanthus [98], rea-
lised benefits are likely to be contingent on the intensity of
feedstock production leading to a trade-off between yield and
biodiversity. Although positive benefits will most likely accrue for
transitions from arable production, at the landscape scale transi-
tions from grassland systems could deliver benefits for pollination
services by creating a diversity of habitats, both spatially and
temporally, which can act as refuges and a sources for recoloniza-
tion [28,40,81,84]. However, the lack of large scale deployment of
2G feedstocks limits our ability to examine the implications for
this service in a commercial context. A principal driver of loss of
pollinators identified in other systems is homogenisation of the
landscape [95,99], as such large scale production of 2G feedstocks
could impact pollinator species if the patterns of deployment
means that habitat diversity is lost [40,80,100,101].
4.7. Soil quality regulation
Land use transitions can exert a marked influence on levels of
SOC [102] with studies of transition to 2G feedstock production
[35,77,103–109] demonstrating changes that can be considered as
neutral to broadly positive depending on original land use, with
most benefits accruing from conversion of arable land. The need to
 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
fully account for GHG emissions from 2G feedstock production to
inform policy has led to an increasing literature that examines the
implications of such transitions on soil carbon. Indeed multisite
research projects in Ireland (e.g. [105,106]) and the UK (e.g. [104])
together with the review of Ref. [103] report changes in soil carbon
in detail and we refer the reader to these for a detailed discussion.
More broadly, compared to 1G bioenergy feedstocks, both the
common characteristics of 2G feedstocks (e.g. deep root systems,
high litter input) and the management practices (e.g. less main-
tenance, longer harvesting cycles) convey significant benefits on
soil quality. These include reduced bulk density, improved soil
porosity, improved microbial activity and biomass, improved
macro-invertebrate populations, and improved fluxes of water,
air and heat [76,110,111]. Such benefits contribute to the effective
delivery of other ecosystem services such as flood prevention,
suggesting benefits beyond SOC from the adoption of 2G feed-
stocks that should be incorporated into decisions about
deployment.
As with previous services considered, benefits accrue through
the longer management cycles associated with 2G feedstocks.
However, a number of authors note distinct temporal phases in
the relationship between 2G feedstock production and soil quality
parameters. For example during the transition phase from grass-
land to Miscanthus, Ref. [79] reported negative impacts on soil
structure associated with ploughing and lack of ground cover.
Similarly, Ref. [59] discusses a reduction in soil organic matter
associated with harvest in SRF. Such negative impacts are short
lived and only relevant at specific phases in production. Indeed
over the long term, transitions to 2G feedstocks on marginal lands
serve to improve soil quality by increasing infiltration rates,
increasing SOC and preventing erosion [76]. Indeed, at the
extreme, 2G feedstock has some potential to be used as a
phytoremediation strategy to ameliorate contamination, thereby
providing a pollution mitigation service [76]. Although recent
work has shown that growing 2G feedstock on contaminated soils
CONFIDENCE
Med.
High
Low
Positive
EFFECT
Miscanthus
Neutral
Negative
Crops and
livestock
Timber and
PRIORITY ECOSYSTEM SERVICES
forest
Water
availability
Hazard
regulation
Disease and
pest control
Pollination
Soil quality
Water quality
Fig. 1. Impact matrix of effects on priority ecosystem services of land use transitions to 2G feedstocks. Impacts are scored positive where there is an increase in the service,
negative with a decrease, and neutral where there is no significant effect reported. Confidence is assigned based on the weight of evidence as described in the main text.
35
can lead to the dis-service of increasing air pollution in the
location where it is combusted as, if not properly carried out, the
contaminants might be bound in fine particles and gaseous
compounds [112].
4.8. Water quality
Agricultural production can significantly impact water quality
through a number of different pathways including input of
agrochemicals and sedimentation. In general the lower require-
ment for fertiliser coupled with high water uptake and continuous
ground cover preventing sediment loss suggests that 2G crops
could deliver significant benefits for water quality. For example 2G
crops could be an effective management tools if deployed as buffer
strips surrounding traditional row crops [113] or in nitrate vulner-
able zones [114], with large scale changes in land use predicted to
be associated with a significant increase in water quality [81].
A key consideration for water quality is fertiliser application
rates [55]. Modelling studies of Miscanthus indicate benefits in
terms of reduction in nitrate loss to aquatic systems can be
realised at application rates of 80–100 kg-N/ha [115] however, as
rates increase impacts become comparable to those of 1G crops
[43]. For SRC, Ref. [116] reports that 87.5% of nitrate emissions can
be attributed to application of fertiliser, although losses from
forestry system such as SRC and SRF are lower than those from
arable crops [114,117,118]. From a management perspective there
are likely to be trade-offs between water quality benefits and yield
for 2G feedstocks [43,115,116] so understanding how to balance
these will be key to delivering water quality benefits.
As with other services, a number of studies report a distinct
temporal and spatial element to the benefits of 2G crops with
concentrations of agrochemical and nutrient released into aquatic
systems fluctuating through time as a function of application
timing, amount and environmental conditions [118–120]. For SRC
and SRF, establishment and harvesting have negative impacts on
ARABLE GRASSLAND FOREST
Miscanthus
Miscanthus
SRC
SRC
SRC
SRF
SRF
SRF
36 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
water quality compared to the growth phase [59,114,120], with
25% of the total eutrophication potential associated with establish-
ment and 50% with harvesting in a non-fertilised scenario [116].
5. Synthesis—Implications of 2G feedstock for ecosystem
services
Fig. 1 summarises likely consequences of different transitions
for key ecosystem services in the UK and Europe. Negative scores
indicate the transition would reduce, positive increase, and a
neutral score have little or no effect on the provision of the
service. For strength of evidence, high confidence was assigned
where there was a developed literature indicating a clear under-
standing of change resulting from the transition. A medium
confidence was assigned where there was emerging evidence to
understand the transition. Low confidence was assigned where
there is little or no evidence.
In developing the impact matrix (Fig. 1) initial scoring was
based on studies that used a reference state approach to examine
implications for ecosystem services (Table 1). For example, all the
studies of [42,43,62,63] report a negative impact on water avail-
ability associated with transitions from arable production to 2G
energy grasses. To extend the impact matrix (Fig. 1) to transitions
where the search criteria found few or no studies, we used
information available within (i) those studies that qualified under
our inclusion criteria where there were parallels in the mechan-
isms identified; (ii) those studies that did not use a reference state
approach but which were retained as part of the filtering process
(see Fig. S1) due to relevance. For example, a number of studies
highlight the crop characteristics of 2G feedstocks [42,66–68] and
deployment patterns [63,65] as key drivers of impacts on water
availability allowing us to extrapolate to other transitions that
have not been examined using a reference state approach.
The strong cross linkages that exist between different ecosys-
tem services was also used to inform the construction of the
impact matrix as mechanisms relevant for impacts on one will also
influence our understanding of impacts on the provision of other
services. For example changes in soil quality associated with land
use transitions to 2G feedstock production [76,79,110,111,121]
will also deliver benefits for the service of hazard regulation
through the control of surface runoff [76] and wind erosion
[75,77]. Contextual information was also important in developing
the impact matrix as factors such as geographic location
COMMERCIAL DEPLOYMENT
Required agrochemical inputs
Management practices
Landscape scale
deployment patterns
Land use implications
Economic feasibility given
constraints
Fig. 2. Elements of research needed to understand the implications of 2G feedstock production on ecosystem services.
[105,120,122], previous land use [105,123], and temporal
dynamics [59,114] could all influence reported effects of transi-
tions. Taking soil quality as an example, although studies that
focus on changes in soil organic carbon return a mixture of
positive and neutral impacts for transitions to 2G feedstock
production [77,103–106] reports of enhanced microbial activity
[110,124], increased porosity and litter input [79] and reduction in
wind erodability [77] under 2G feedstocks strengthen the case for
a net positive effect of this transition.
More broadly across studies, the intensity of production (both
field and landscape scale) and length of management cycle are key
factors that influence the provision of ecosystem services. As such,
and in the absence of evidence to the contrary, it would be
expected that most benefits are realised through conversion of
arable land, fewer benefits for conversion of grassland, and the
least number of benefits for conversion from forest. As reflected in
Table 1 and Fig. 1, few studies using a reference state approach
have consider transitions from grassland or forest systems to the
specific 2G feedstocks likely to be deployed in the UK and Europe.
This is reflected in the low confidence that we assign to these
effects and represents an area for future research, particularly in
relation to grassland systems that are likely key areas for 2G
feedstock deployment in the UK and Europe.
Our most complete understanding is for transitions from 1G to
2G dedicated bioenergy feedstocks. Here studies suggest signifi-
cant benefits across a broad range of ecosystem services. Research
suggests that Miscanthus and SRC would deliver benefits for
hazard regulation [43,73], disease and pest control [47,80,125],
soil [110,126,127] and water quality [46,73,119]. The mechanisms
that positively influence these services would be expected to apply
to short-rotation forestry (SRF). All three feedstocks could have a
significant negative influence on water availability [43,62,63]
through the same physiological mechanisms [42] that exert a
positive influence on other services, suggesting significant trade-
offs could arise. However, as commercial deployment of 2G feed-
stocks is only just emerging [63] there is limited empirical
evidence to understand how production at commercial scales
may influence these conclusions.
Production of 2G bioenergy crops on marginal land offers
benefits of bringing currently under-utilized areas into production,
while either enhancing or having little impact on the provision of
many of the key services considered in this review. In keeping
with our focus on production of 2G crops in the EU and specifically
the UK, the summary provided in Fig. 1 draws on studies that
ECOSYSTEM SERVICES
Temporal dynamics
between services
Scaling of impacts
Social & economic value
given local context Increase understanding of
services beyong climate
 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
explicitly consider marginal land defined as grasslands not used
for crop production, informed by other studies that raise relevant
issues. Conversion would be expected to enhance hazard regula-
tion principally through flood and erosion prevention in at-risk
areas [49]; soil quality due to increased porosity and litter input
[79]; and water quality due to decreasing inputs of fertiliser
although this will be dependent on current management practices
[43]. Livestock production could be negatively influenced [30,49]
as the importance of such areas for this activity can be
underestimated.
For transitions from forest to 2G feedstocks the majority of
services would be negatively impacted due to the increased
management intensity that the transition implies. Conversion of
existing plantations designed for harvesting and managed for
productivity [128], to SRC and SRF represent the most likely
pathway for feedstock development. Impacts will occur primarily
during establishment and harvesting, so adoption of best practice
during these portions of the management cycle could ameliorate
impacts [59].
6. Outlook—Defining a research agenda for 2G feedstocks
Tilman [129] argues that if society is to realise the potential
benefits of bioenergy a key requirement is that science-based
safeguards must be introduced to ensure that the best feedstocks
and management practices are adopted. Factoring the provision of
multiple ecosystem services, and alternate energy pathways, into
the decision making process could significantly alter our conclu-
sions about desirability [28,130], and point to different deploy-
ment strategies that enhance benefits to society [131]. Although
dependant on feedstock and land-use transition we identify path-
ways that offer potential for 2G feedstocks to deliver benefits for
ecosystem services. However, conclusions must be tempered by
acknowledging the significant knowledge gap that exists for some
land-use transitions that prevents us from fully understanding the
implications of increased production. This knowledge gap hinders
our ability to select the best feedstocks and employ the optimum
management practices to safeguard ecosystem services in
response to policy that will drive the expansion of 2G feedstock
production. As a starting point there are a number of key issues
that need to be addressed relating to scale of deployment, societal
value and trade-offs between services. These are summarised in
Fig. 2.
First, how does scaling-up of feedstock production across
landscapes influence conclusions about impacts of 2G feedstocks
on ecosystem services? As previously discussed, for economic and
energetic reasons feedstock production may not occur in a mosaic
within the landscape (a pattern analogous to experimental or
small scale deployment typical in many of the studies considered
here and one which is likely to deliver benefits for ecosystem
services [132]), but rather regions of high intensity production
clustered around biorefineries [65]. As discussed by Ref. [63] in
reference to water resources, such a pattern of deployment can
have a negative impact not associated with a less intense pattern
of feedstock production. An open question for many ecosystem
services is whether reported benefits of 2G feedstocks would still
be delivered were this pattern of deployment adopted, or whether
areas of high intensity production might negate benefits described
at smaller scales. As there is a degree of flexibility in the optimal
size of biorefinery for processing 2G feedstock material [133],
there are likely opportunities to optimise area and intensity of 2G
feedstock production to balance requirements for processing with
ecosystem service provision. This question could also be extended
to consider intensity of feedstock production at the field scale as
this will again influence the provision of services, as has been
37
demonstrated in relation to water resources [71] and biodiversity
[98].
Second, to fully understand the implication of 2G feedstock
production there is a need to explicitly link effects on ecosystem
services provision with societal values. We must consider the
social and economic context in which 2G feedstock production is
occurring in order to understand how changes in the provision of
ecosystem services will be interpreted. For example in water
stressed regions the crop characteristics of Miscanthus may make
it undesirable due to its high water use. In other regions these
same characteristics may contribute to flood prevention thus
providing a service that is of value to local inhabitants. Context
is the key, and so optimising patterns of deployment to match
societal value will be importance for wide acceptance of feedstock
production.
Third, the focus of our analysis has been on likely candidate
feedstock for the UK and Europe. As discussed in relation to crop
and livestock production, the environmental and social context in
which production occurs in other regions of the world may be
quite different [44,57] as may be the most desirable candidate
energy crops. There is the potential that implications for ecosys-
tem services elucidated in a European context could be reversed in
other regions of the world. Given our understanding of the
importance of international trade for the global economy and
how demand in one region of the world can drive impacts in
others [134], repeating such an analysis to identify implications
and knowledge gaps in other producer regions is a key step to
identifying the sustainability of 2G feedstock within the global
supply chain.
Finally, the current review examines a subset of priority
ecosystem services based on data availability and policy relevance,
excluding climate regulation and biodiversity for which major
reviews already exist (but see Supplementary online material).
While our understanding of impacts on biodiversity and climate
regulation are developing and continue to be an active area of
research, implications for other services (e.g. cultural services; see
Table 1) are not well understood. This needs to be developed to
properly assess trade-offs and synergies between feedstock pro-
duction and provision of ecosystem services [56] in order to
identify the best feedstocks and management practices given the
environmental, social and economic context.
7. Conclusion
The last decade has seen the parallel emergence of policy
designed to promote bioenergy as a route towards sustainable
energy production, and an increasing understanding of the impor-
tance of ecosystem services for human health and wellbeing.
Although our review highlights significant knowledge gaps, our
understanding of the implications of 2G bioenergy production for
landscape-scale deployment is increasing. This parallels a growing
number of initiatives that have begun to map the provision of
ecosystem services and understand human reliance on them
[135,136]. By bringing practitioners from these two communities
together there is an opportunity to address outstanding questions
with significant policy implications that transcend the service
specific impacts we identify in this review. As has been demon-
strated [137] such an integrated approach to spatial planning, that
considers both market-priced goods (e.g. feedstock crops in the
current context) and ecosystem services, can deliver benefits to
society. However, for 2G feedstock production implementation is a
significant challenge requiring us to address a series of questions
that we highlight in our review. A programme of research that
mixes both the natural and social sciences based on an ecosystem
service framework is needed to examine these questions and
38 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
understand whether changing policies promoting the production
of 2G feedstocks are likely to deliver benefits or contribute further
to the social and environmental burden of energy production.
Acknowledgements
Our thanks to Kelvin Peh for comments on an early version
of the manuscript. This work was commissioned and funded by
the Energy Technologies Institute (ETI), UK, as part of the Eco-
system Land-use Modelling & Soil Carbon GHG Flux Trial (ELUM)
project, and also funded through the UKERC project NE/J005924/1
“A global framework for quantifying the ecosystem service
impacts of oil and biofuel production”. Research on bioenergy
crops in the laboratory of GT is also funded through NERC the
Carbo-BioCrop project "Understanding processes determining soil
carbon balance under perennial bioenergy crops" (NE/H010645/1).
Appendix A. Supporting information
Supplementary data associated with this article can be found in
the online version at http://dx.doi.org/10.1016/j.rser.2015.02.003.
References
[1] Naik SN, Goud VV, Rout PK, Dalai AK. Production of first and second
generation biofuels: a comprehensive review. Renewable Sustainable Energy
Rev 2010;14:578–97. http://dx.doi.org/10.1016/j.rser.2009.10.003.
[2] Foresight. The future of food and farming. Executive summary. London: The
Government Office for Science; 2011.
[3] Nigam PS, Singh A. Production of liquid biofuels from renewable resources.
Prog Energy Combust Sci 2011;37:52–68. http://dx.doi.org/10.1016/j.
pecs.2010.01.003.
[4] U.S. Energy Information Administration. International energy statistics; 2013.
〈http://www.eia.gov/countries/data.cfm〉.
[5] Balat M. An overview of biofuels and policies in the European Union. Energy
Sources Part B—Econ Plan Policy 2007;2:167–81. http://dx.doi.org/10.1080/
15567240500402701.
[6] Sharman A, Holmes J. Evidence-based policy or policy-based evidence
gathering? Biofuels, the EU and the 10% target Environ Policy Gov
2010;20:309–21. http://dx.doi.org/10.1002/Eet.543.
[7] Bessou C, Ferchaud F, Gabrielle B, Mary B. Biofuels, greenhouse gases and
climate change: a review. Agron Sustainable Dev 2011;31:1–79. http://dx.
doi.org/10.1051/Agro/2009039.
[8] Gasparatos A, Stromberg P, Takeuchi K. Biofuels, ecosystem services and
human wellbeing: putting biofuels in the ecosystem services narrative. Agric
Ecosyst Environ 2011;142:111–28. http://dx.doi.org/10.1016/j.agee.2011.
04.020.
[9] Van der Horst D, Vermeylen S. Spatial scale and social impacts of biofuel
production. Model Environ Econ Soc Asp Assess Biofuels 2011;35:2435–43.
http://dx.doi.org/10.1016/j.biombioe.2010.11.029.
[10] Mohr A, Raman S. Lessons from first generation biofuels and implications for
the sustainability appraisal of second generation biofuels. Energy Policy
2013;63:114–22. http://dx.doi.org/10.1016/j.enpol.2013.08.033.
[11] Naylor RL, Liska AJ, Burke MB, Falcon WP, Gaskell JC, Rozelle SD, et al. The
ripple effect: biofuels, food security, and the environment. Environment
2007;49:30–43.
[12] Ajanovic A. Biofuels versus food production: does biofuels production
increase food prices? Energy 2011;36:2070–6. http://dx.doi.org/10.1016/j.
energy.2010.05.019.
[13] Fargione J, Hill J, Tilman D, Polasky S, Hawthorne P. Land clearing and the
biofuel carbon debt. Science 2008;319:1235–8. http://dx.doi.org/10.1126/
science.1152747.
[14] Searchinger T, Heimlich R, Houghton RA, Dong F, Elobeid A, Fabiosa J, et al.
Use of U.S. Croplands for biofuels increases greenhouse gases through
emissions from land-use change. Science 2008;319:1238–40. http://dx.doi.
org/10.1126/science.1151861.
[15] Smith KA, Searchinger TD. Crop-based biofuels and associated environmen-
tal concerns. Global Change Biol Bioenergy 2012;4:479–84. http://dx.doi.org/
10.1111/j.1757-1707.2012.01182.x.
[16] European Commission. Directive of the European Parliament and of the
Council amending Directive 98/70/EC relating to the quality of petrol and
diesel fuels and amending Directive 2009/28/EC on the promotion of the use
of energy from renewable sources; 2012.
[17] International Energy Agency. Technology roadmap biofuels for transport.
Paris: International Energy Agency—IEA; 2011.
[18] McBride AC, Dale VH, Baskaran LM, Downing ME, Eaton LM, Efroymson RA,
et al. Indicators to support environmental sustainability of bioenergy
systems. Ecol Indic 2011;11:1277–89. http://dx.doi.org/10.1016/j.ecolind.
2011.01.010.
[19] Haines-Young R, Potschin M. CICES version 4: response to consultation.
Centre for Environmental Management, University of Nottingham; 2012.
[20] UK NEA.. The UK National Ecosystem Assessment. Synthesis of the key
findings. UNEP-WCMC Camb 2011.
[21] Millennium Ecosystem Assessment. Ecosystems and human well-being:
synthesis. World Resource Institute; 2005.
[22] Mace GM, Norris K, Fitter AH. Biodiversity and ecosystem services: a
multilayered relationship. Trends Ecol Evol 2012;27:19–26. http://dx.doi.
org/10.1016/j.tree.2011.08.006.
[23] Vié J-C, Hilton-Taylor C, Stuart SN. Wildlife in a changing world: an analysis
of the 2008 IUCN red list of threatened species. IUCN; 2009.
[24] Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D,
et al. Quantifying the evidence for biodiversity effects on ecosystem
functioning and services. Ecol Lett 2006;9:1146–56. http://dx.doi.org/
10.1111/j.1461-0248.2006.00963.x.
[25] Flynn DF, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, et al.
Loss of functional diversity under land use intensification across multiple
taxa. Ecol Lett 2009;12:22–33. http://dx.doi.org/10.1111/j.1461-0248.2008.
01255.x.
[26] Power AG. Ecosystem services and agriculture: tradeoffs and synergies.
Philos Trans R Soc B Biol Sci 2010;365:2959–71. http://dx.doi.org/10.1098/
rstb.2010.0143.
[27] Raudsepp-Hearne C, Peterson GD, Bennett EM. Ecosystem service bundles
for analyzing tradeoffs in diverse landscapes. Proc Natl Acad Sci
2010;107:5242–7. http://dx.doi.org/10.1073/pnas.0907284107.
[28] Werling BP, Dickson TL, Isaacs R, Gaines H, Gratton C, Gross KL, et al.
Perennial grasslands enhance biodiversity and multiple ecosystem services
in bioenergy landscapes. Proc Natl Acad Sci 1652–7;2014:111. http://dx.doi.
org/10.1073/pnas.1309492111.
[29] Tilman D, Hill J, Lehman C. Carbon-negative biofuels from low-input high-
diversity grassland biomass. Science 2006;314:1598–600. http://dx.doi.org/
10.1126/science.1133306.
[30] Kang S, Post WM, Nichols JA, Wang D, West TO, Bandaru V, et al. Marginal
lands: concept, assessment and management. J Agric Sci 2013:5. http://dx.
doi.org/10.5539/jas.v5n5p129.
[31] Gallagher E. The Gallagher review of the indirect effects of biofuels produc-
tion. UK: Renewable Fuels Agency; 2008.
[32] United Nations. Glossary of environmental statistics. New York: United
Nations; 1997.
[33] UN FAO. CGIAR research priorities for Marginal Lands. Washington, DC, USA;
1999.
[34] Dauber J, Brown C, Fernando AL, Finnan J, Krasuska E, Ponitka J, et al.
Bioenergy from “surplus” land: environmental and socio-economic implica-
tions. BIORISK—Biodivers Ecosyst Risk Assess 2012;7:5–50. http://dx.doi.org/
10.3897/biorisk.7.3036.
[35] Anderson-Teixeira KJ, Davis SC, Masters MD, Delucia EH. Changes in soil
organic carbon under biofuel crops. Global Change Biol Bioenergy
2009;1:75–96. http://dx.doi.org/10.1111/j.1757-1707.2008.01001.x.
[36] Cherubini F, Bird ND, Cowie A, Jungmeier G, Schlamadinger B, Woess-
Gallasch S. Energy- and greenhouse gas-based LCA of biofuel and bioenergy
systems: key issues, ranges and recommendations. Resour Conserv Recycl
2009;53:434–47. http://dx.doi.org/10.1016/j.resconrec.2009.03.013.
[37] Hillier J, Whittaker C, Dailey G, Aylott M, Casella E, Richter GM, et al.
Greenhouse gas emissions from four bioenergy crops in England and Wales:
integrating spatial estimates of yield and soil carbon balance in life cycle
analyses. Global Change Biol Bioenergy 2009;1:267–81. http://dx.doi.org/
10.1111/j.1757-1707.2009.01021.x.
[38] Drewer J, Finch JW, Lloyd CR, Baggs EM, Skiba U. How do soil emissions of
N2O, CH4 and CO2 from perennial bioenergy crops differ from arable annual
crops? Global Change Biol Bioenergy 2012;4:408–19. http://dx.doi.org/
10.1111/j.1757-1707.2011.01136.x.
[39] Rowe RL, Street NR, Taylor G. Identifying potential environmental impacts of
large-scale deployment of dedicated bioenergy crops in the UK. Renewable
Sustainable Energy Rev 2009;13:271–90. http://dx.doi.org/10.1016/j.
rser.2007.07.008.
[40] Dauber J, Jones MB, Stout JC. The impact of biomass crop cultivation on
temperate biodiversity. Global Change Biol Bioenergy 2010;2:289–309. http:
//dx.doi.org/10.1111/j.1757-1707.2010.01058.x.
[41] Fletcher RJ, Robertson BA, Evans J, Doran PJ, Alavalapati JR,
Schemske DW. Biodiversity conservation in the era of biofuels: risks and
opportunities. Front Ecol Environ 2011;9:161–8. http://dx.doi.org/10.1890/
090091.
[42] Hickman GC, Vanloocke A, Dohleman FG, Bernacchi CJ. A comparison of
canopy evapotranspiration for maize and two perennial grasses identified as
potential bioenergy crops. Global Change Biol Bioenergy 2010;2:157–68.
http://dx.doi.org/10.1111/j.1757-1707.2010.01050.x.
[43] Wu YP, Liu SG. Impacts of biofuels production alternatives on water quantity
and quality in the Iowa River Basin. Biomass Bioenergy 2012;36:182–91.
http://dx.doi.org/10.1016/j.biombioe.2011.10.030.
[44] Ariza-Montobbio P, Lele S. Jatropha plantations for biodiesel in Tamil Nadu,
India viability, livelihood trade-offs, and latent conflict. Ecol Econom
2010;70:189–95. http://dx.doi.org/10.1016/j.ecolecon.2010.05.011.
 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
[45] Rittenburg RA, Kummel M, Perramond EP. The local climate-development
nexus: Jatropha and smallholder adaptation in Tamil Nadu, India. Clim Dev
2011;3:328–43. http://dx.doi.org/10.1080/17565529.2011.626715.
[46] Davis SC, Parton WJ, Del Grosso SJ, Keough C, Marx E, Adler PR, et al. Impact
of second-generation biofuel agriculture on greenhouse-gas emissions in the
corn-growing regions of the US. Front Ecol Environ 2012;10:69–74. http://dx.
doi.org/10.1890/110003.
[47] Werling BP, Meehan TD, Gratton C, Landis DA. Influence of habitat and
landscape perenniality on insect natural enemies in three candidate biofuel
crops. Biol Control 2011;59:304–12. http://dx.doi.org/10.1016/j.biocontrol.
2011.06.014.
[48] Findlater KM, Kandlikar M. Land use and second-generation biofuel feed-
stocks: the unconsidered impacts of Jatropha biodiesel in Rajasthan, India.
Energy Policy 2011;39:3404–13. http://dx.doi.org/10.1016/j.enpol.2011.
03.037.
[49] Garg KK, Karlberg L, Wani SP, Berndes G. Jatropha production on wastelands
in India: opportunities and trade-offs for soil and water management at the
watershed scale. Biofuels Bioprod Biorefin-Biofpr 2011;5:410–30. http://dx.
doi.org/10.1002/Bbb.312.
[50] German L, Schoneveld GC, Gumbo D. The local social and environmental
impacts of smallholder-based biofuel investments in Zambia. Ecol Soc
2011:16. http://dx.doi.org/10.5751/Es-04280-160412.
[51] Skutsch M, de los Rios E, Solis S, Riegelhaupt E, Hinojosa D, Gerfert S, et al.
Jatropha in Mexico: environmental and social impacts of an incipient biofuel
program. Ecol Soc 2011;16:11.
[52] Aylott MJ, Casella E, Farrall K, Taylor G. Estimating the supply of biomass
from short-rotation coppice in England, given social, economic and environ-
mental constraints to land availability. Biofuels Bioprod Biorefin-Biofpr
2010;5:719–27.
[53] Lovett AA, Sunnenberg GM, Richter GM, Dailey AG, Riche AB, Karp A. Land
use implications of increased biomass production identified by GIS-based
suitability and yield mapping for Miscanthus in England. Bioenergy Res
2009;2:17–28.
[54] Ceotto E. Grasslands for bioenergy production. A review. Agron Sustainable
Dev 2008;28:47–55. http://dx.doi.org/10.1051/Agro:2007034.
[55] Sanderson MA, Adler PR. Perennial forages as second generation bioenergy
crops. Int J Mol Sci 2008;9:768–88. http://dx.doi.org/10.3390/Ijms9050768.
[56] Bryan BA. Incentives, land use, and ecosystem services: synthesizing com-
plex linkages. Environ Sci Policy 2013;27:124–34. http://dx.doi.org/10.1016/j.
envsci.2012.12.010.
[57] Novo A, Jansen K, Slingerland M, Giller K. Biofuel, dairy production and beef
in Brazil: competing claims on land use in Sao Paulo state. J Peasant Stud
2010;37:769–92. http://dx.doi.org/10.1080/03066150.2010.512458.
[58] Bryan BA, Crossman ND, King D, Meyer WS. Landscape futures analysis:
assessing the impacts of environmental targets under alternative spatial
policy options and future scenarios. Environ Model Softw 2011;26:83–91.
http://dx.doi.org/10.1016/j.envsoft.2010.03.034.
[59] Lattimore B, Smith CT, Titus BD, Stupak I, Egnell G. Environmental factors in
woodfuel production: opportunities, risks, and criteria and indicators for
sustainable practices. Biomass Bioenergy 2009;33:1321–42. http://dx.doi.
org/10.1016/j.biombioe.2009.06.005.
[60] Kirilenko AP, Sedjo RA. Climate change impacts on forestry. Proc Natl Acad
Sci USA 2007;104:19697–702. http://dx.doi.org/10.1073/pnas.0701424104.
[61] Raunikar R, Buongiorno J, Turner JA, Zhu SS. Global outlook for wood and
forests with the bioenergy demand implied by scenarios of the Intergovern-
mental Panel on Climate Change. For Policy Econ 2010;12:48–56. http://dx.
doi.org/10.1016/j.forpol.2009.09.013.
[62] Brown RA, Rosenberg NJ, Hays CJ, Easterling WE, Mearns LO. Potential
production and environmental effects of switchgrass and traditional crops
under current and greenhouse-altered climate in the central United States: a
simulation study. Agric Ecosyst Environ 2000;78:31–47.
[63] Vanloocke A, Bernacchi CJ, Twine TE. The impacts of Miscanthus x giganteus
production on the Midwest US hydrologic cycle. Global Change Biol Bioenergy
2010;2:180–91. http://dx.doi.org/10.1111/j.1757-1707.2010.01053.x.
[64] Heaton EA, Dohleman FG, Long SP. Meeting US biofuel goals with less land:
the potential of Miscanthus. Global Change Biol 2008;14:2000–14.
[65] Kocoloski M, Michael Griffin W, Scott Matthews H. Impacts of facility size
and location decisions on ethanol production cost. Energy Policy
2011;39:47–56. http://dx.doi.org/10.1016/j.enpol.2010.09.003.
[66] VanLoocke A, Twine TE, Zeri M, Bernacchi CJ. A regional comparison of water
use efficiency for Miscanthus, switchgrass and maize. Agric For Meteorol
2012;164:82–95. http://dx.doi.org/10.1016/j.agrformet.2012.05.016.
[67] Finch JW, Riche AB. Interception losses from Miscanthus at a site in south-
east England—an application of the Gash model. Hydrol Processes
2010;24:2594–600. http://dx.doi.org/10.1002/hyp.7673.
[68] Le PVV, Kumar P, Drewry DT. Implications for the hydrologic cycle under
climate change due to the expansion of bioenergy crops in the Midwestern
United States. Proc Natl Acad Sci USA 2011;108:15085–90. http://dx.doi.org/
10.1073/pnas.1107177108.
[69] Oliver RJ, Finch JW, Taylor G. Second generation bioenergy crops and climate
change: a review of the effects of elevated atmospheric CO2 and drought on
water use and the implications for yield. GCB Bioenergy 2009;1:97–114.
http://dx.doi.org/10.1111/j.1757-1707.2009.01011.x.
[70] Stone KC, Hunt PG, Cantrell KB, Ro KS. The potential impacts of biomass
feedstock production on water resource availability. Bioresour Technol
2010;101:2014–25. http://dx.doi.org/10.1016/j.biortech.2009.10.037.
39
[71] Richter GM, Riche AB, Dailey AG, Gezan SA, Powlson DS. Is UK biofuel supply
from Miscanthus water-limited? Soil Use Manage 2008;24:235–45. http:
//dx.doi.org/10.1111/j.1475-2743.2008.00156.x.
[72] Boardman J, Evans R. Britain. In: Boardman J, Poesen J, editors. Soil Erosion in
Europe. Chichester, UK: John Wiley & Sons; 2006.
[73] Wilson HM, Cruse RM, Burras CL. Perennial grass management impacts on
runoff and sediment export from vegetated channels in pulse flow runoff
events. Biomass Bioenergy 2011;35:429–36. http://dx.doi.org/10.1016/j.
biombioe.2010.08.059.
[74] Updegraff K, Baughman MJ, Taff SJ. Environmental benefits of cropland conver-
sion to hybrid poplar: economic and policy considerations. Biomass Bioenergy
2004;27:411–28. http://dx.doi.org/10.1016/j.biombioe.2004.05.002.
[75] Busch G. GIS-based tools for regional assessments and planning processes
regarding potential environmental effects of poplar SRC. Bioenergy Res
2012;5:584–605. http://dx.doi.org/10.1007/s12155-012-9224-0.
[76] Blanco-Canqui H. Energy crops and their implications on soil and environ-
ment. Agron J 2010;102:403–19. http://dx.doi.org/10.2134/agronj2009.0333.
[77] Evers BJ, Blanco-Canqui H, Staggenborg SA, Tatarko J. Dedicated bioenergy
crop impacts on soil wind erodibility and organic carbon in Kansas. Agron J
2013;105:1271. http://dx.doi.org/10.2134/agronj2013.0072.
[78] Schulze ED, Korner CI, Law BE, Haberl H, Luyssaert S. Large-scale bioenergy
from additional harvest of forest biomass is neither sustainable nor green-
house gas neutral. Global Change Biol Bioenergy 2012;4:611–6. http://dx.doi.
org/10.1111/j.1757-1707.2012.01169.x.
[79] Donnelly A, Styles D, Fitzgerald J, Finnan J. A proposed framework for
determining the environmental impact of replacing agricultural grassland
with Miscanthus in Ireland. Global Change Biol Bioenergy 2011;3:247–63.
http://dx.doi.org/10.1111/j.1757-1707.2010.01086.x.
[80] Gardiner MA, Tuell JK, Isaacs R, Gibbs J, Ascher JS, Landis DA. Implications of
three biofuel crops for beneficial arthropods in agricultural landscapes.
Bioenergy Res 2010;3:6–19. http://dx.doi.org/10.1007/s12155-009-9065-7.
[81] Meehan TD, Gratton C, Diehl E, Hunt ND, Mooney DF, Ventura SJ, et al.
Ecosystem-service tradeoffs associated with switching from annual to
perennial energy crops in Riparian zones of the US Midwest. PLoS One
2013:8. http://dx.doi.org/10.1371/journal.pone.0080093.
[82] Meehan TD, Werling BP, Landis DA, Gratton C. Pest-suppression potential of
Midwestern landscapes under contrasting bioenergy scenarios. PLoS One
2012:7. http://dx.doi.org/10.1371/journal.pone.0041728.
[83] Bianchi FJJA, Booij CJH, Tscharntke T. Sustainable pest regulation in agricul-
tural landscapes: a review on landscape composition, biodiversity and
natural pest control. Proc R Soc B-Biol Sci 2006;273:1715–27.
[84] Rowe RL, Hanley ME, Goulson D, Clarke DJ, Doncaster CP, Taylor G. Potential
benefits of commercial willow Short Rotation Coppice (SRC) for farm-scale
plant and invertebrate communities in the agri-environment. Biomass
Bioenergy 2011;35:325–36. http://dx.doi.org/10.1016/j.biombioe.2010.08.
046.
[85] Sage RB. Short rotation coppice for energy: towards ecological guidelines.
Biomass Bioenergy 1998;15:39–47. http://dx.doi.org/10.1016/S0961-9534
(97)10055-1.
[86] Bourke D, Stanley D, O’Rourke E, Thompson R, Carnus T, Dauber J, et al.
Response of farmland biodiversity to the introduction of bioenergy crops:
effects of local factors and surrounding landscape context. GCB Bioenergy
2014;6:275–89. http://dx.doi.org/10.1111/gcbb.12089.
[87] Myers JH, Higgins C, Kovacs E. How many insect species are necessary for the
biological control of insects? Environ Entomol. 1989;18:541–7.
[88] Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M,
et al. Effects of biodiversity on the functioning of trophic groups and eco-
systems. Nature 2006;443:989–92. http://dx.doi.org/10.1038/nature05202.
[89] Thomson LJ, Hoffmann AA. Pest management challenges for biofuel crop
production. Curr Opin Environ Sustain 2011;3:95–9. http://dx.doi.org/
10.1016/j.cosust.2010.11.003.
[90] Mekete T, Reynolds K, Lopez-Nicora HD, Gray ME, Niblack TL. Plant-parasitic
nematodes are potential pathogens of Miscanthus  giganteus and Panicum
virgatum used for biofuels. Plant Dis 2011;95:413–8. http://dx.doi.org/
10.1094/Pdis-05-10-0335.
[91] Vaknin Y. The significance of pollination services for biodiesel feedstocks,
with special reference to Jatropha curcas L.: a review. Bioenergy Res
2012;5:32–40. http://dx.doi.org/10.1007/s12155-011-9142-6.
[92] Gallai N, Salles J-M, Settele J, Vaissière BE. Economic valuation of the
vulnerability of world agriculture confronted with pollinator decline. Ecol
Econom 2009;68:810–21. http://dx.doi.org/10.1016/j.ecolecon.2008.06.014.
[93] Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen
C, et al. Importance of pollinators in changing landscapes for world crops. Proc
Biol Sci 2007;274:303–13. http://dx.doi.org/10.1098/rspb.2006.3721.
[94] Carvell C, Meek WR, Pywell RF, Goulson D, Nowakowski M. Comparing the
efficacy of agri-environment schemes to enhance bumble bee abundance
and diversity on arable field margins. J Appl Ecol 2007;44:29–40.
[95] Holzschuh A, Steffan-Dewenter I, Kleijn D, Tscharntke T. Diversity of flower-
visiting bees in cereal fields: effects of farming system, landscape composi-
tion and regional context. J Appl Ecol 2007;44:41–9.
[96] Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley
R, et al. Pollination and other ecosystem services produced by mobile
organisms: a conceptual framework for the effects of land-use change. Ecol
Lett 2007;10:299–314.
[97] Stanley DA, Stout JC. Quantifying the impacts of bioenergy crops on
pollinating insect abundance and diversity: a field-scale evaluation reveals
40 R.A. Holland et al. / Renewable and Sustainable Energy Reviews 46 (2015) 30–40
taxon-specific responses. J Appl Ecol 2013;50:335–44. http://dx.doi.org/
10.1111/1365-2664.12060.
[98] Dauber J, Cass S, Gabriel D, Harte K, Åström S, O’Rourke E, et al. Yield-
biodiversity trade-off in patchy fields of Miscanthus  giganteus. GCB Bioe-
nergy 2014. http://dx.doi.org/10.1111/gcbb.12167.
[99] Steffan-Dewenter I, Westphal C. The interplay of pollinator diversity,
pollination services and landscape change. J Appl Ecol 2008;45:737–41.
[100] Dahms H, Mayr S, Birkhofer K, Chauvat M, Melnichnova E, Wolters V, et al.
Contrasting diversity patterns of epigeic arthropods between grasslands of
high and low agronomic potential. Basic Appl Ecol 2010;11:6–14. http://dx.
doi.org/10.1016/j.baae.2009.06.004.
[101] Robertson BA, Porter C, Landis DA, Schemske DW. Agroenergy crops
influence the diversity, biomass, and guild structure of terrestrial arthropod
communities. Bioenergy Res 2012;5:179–88. http://dx.doi.org/10.1007/
s12155-011-9161-3.
[102] Guo LB, Gifford RM. Soil carbon stocks and land use change: a meta analysis.
Global Change Biol 2002;8:345–60. http://dx.doi.org/10.1046/j.1354-
1013.2002.00486.x.
[103] Don A, Osborne B, Hastings A, Skiba U, Carter MS, Drewer J, et al. Land-use
change to bioenergy production in Europe: implications for the greenhouse
gas balance and soil carbon. GCB Bioenergy 2012;4:372–91. http://dx.doi.org/
10.1111/j.1757-1707.2011.01116.x.
[104] Keith AM, Rowe RL, Parmar K, Perks MP, Mackie E, Dondini M, et al.
Implications of land use change to Short Rotation Forestry in Great Britain
for soil and biomass carbon. GCB Bioenergy 2014. http://dx.doi.org/10.1111/
gcbb.12168.
[105] Zimmermann J, Dauber J, Jones MB. Soil carbon sequestration during the
establishment phase of Miscanthus  giganteus: a regional-scale study on
commercial farms using C-13 natural abundance. Global Change Biol Bioe-
nergy 2012;4:453–61. http://dx.doi.org/10.1111/j.1757-1707.2011.01117.x.
[106] Zimmermann J, Dondini M, Jones MB. Assessing the impacts of the establish-
ment of Miscanthus on soil organic carbon on two contrasting land-use types
in Ireland. Eur J Soil Sci 2013;64:747–56. http://dx.doi.org/10.1111/ejss.12087.
[107] Kahle P, Beuch S, Boelcke B, Leinweber P, Schulten H-R. Cropping of
Miscanthus in Central Europe: biomass production and influence on
nutrients and soil organic matter. Eur J Agron 2001;15:171–84. http://dx.
doi.org/10.1016/S1161-0301(01)00102-2.
[108] Hansen EM, Christensen BT, Jensen LS, Kristensen K. Carbon sequestration in
soil beneath long-term Miscanthus plantations as determined by 13C
abundance. Biomass Bioenergy 2004;26:97–105. http://dx.doi.org/10.1016/
S0961-9534(03)00102-8.
[109] Dowell RC, Gibbins D, Rhoads JL, Pallardy SG. Biomass production physiology
and soil carbon dynamics in short-rotation-grown Populus deltoides and P.
deltoides  P. nigra hybrids. For Ecol Manage 2009;257:134–42. http://dx.doi.
org/10.1016/j.foreco.2008.08.023.
[110] Haney RL, Kiniry JR, Johnson MVV. Soil microbial activity under different
grass species: underground impacts of biofuel cropping. Agric Ecosyst
Environ 2010;139:754–8. http://dx.doi.org/10.1016/j.agee.2010.10.003.
[111] Pellegrino E, Di Bene C, Tozzini C, Bonari E. Impact on soil quality of a 10-year-
old short-rotation coppice poplar stand compared with intensive agricultural
and uncultivated systems in a Mediterranean area. Agric Ecosyst Environ
2011;140:245–54. http://dx.doi.org/10.1016/j.agee.2010.12.011.
[112] Seidel T, Orasche J, Ruppert H, Schnelle-Kreis J, Hartmann H. Emissions of
organic and inorganic pollutants during the combustion of wood, straw and
biogas. Sustainable Bioenergy Production—An Integrated Approach. Springer;
2013. p. 387–422.
[113] Gopalakrishnan G, Negri MC, Salas W. Modeling biogeochemical impacts of
bioenergy buffers with perennial grasses for a row-crop field in Illinois.
Global Change Biol Bioenergy 2012;4:739–50. http://dx.doi.org/10.1111/
j.1757-1707.2011.01145.x.
[114] Dimitriou I, Mola-Yudego B, Aronsson P. Impact of Willow short rotation
coppice on water quality. Bioenergy Res 2012;5:537–45. http://dx.doi.org/
10.1007/s12155-012-9211-5.
[115] Ng TL, Eheart JW, Cai XM, Miguez F. Modeling Miscanthus in the soil and
water assessment tool (SWAT) to simulate its water quality effects as a
bioenergy crop. Environ Sci Technol 2010;44:7138–44. http://dx.doi.org/
10.1021/Es9039677.
[116] Gonzalez-Garcia S, Mola-Yudego B, Dimitriou I, Aronsson P, Murphy R.
Environmental assessment of energy production based on long term
commercial willow plantations in Sweden. Sci Total Environ 2012;421:210–9.
http://dx.doi.org/10.1016/j.scitotenv.2012.01.041.
[117] Callesen I, Carter MS, Ostergard H. Efficient use of reactive nitrogen for
cultivation of bioenergy: less is more. Global Change Biol Bioenergy
2011;3:171–9. http://dx.doi.org/10.1111/j.1757-1707.2010.01072.x.
[118] Syswerda SP, Basso B, Hamilton SK, Tausig JB, Robertson GP. Long-term
nitrate loss along an agricultural intensity gradient in the Upper Midwest
USA. Agric Ecosyst Environ 2012;149:10–9. http://dx.doi.org/10.1016/j.
agee.2011.12.007.
[119] Love BJ, Nejadhashemi AP. Water quality impact assessment of large-scale
biofuel crops expansion in agricultural regions of Michigan. Biomass Bioe-
nergy 2011;35:2200–16. http://dx.doi.org/10.1016/j.biombioe.2011.02.041.
[120] Palmer MM, Forrester JA, Rothstein DE, Mladenoff DJ. Conversion of open
lands to short-rotation woody biomass crops: site variability affects nitrogen
cycling and N2O fluxes in the US Northern Lake States. Global Change Biol
Bioenergy 2014;6:450–64. http://dx.doi.org/10.1111/Gcbb.12069.
[121] Börjesson P. Environmental effects of energy crop cultivation in Sweden—I:
Identification and quantification. Biomass Bioenergy 1999;16:137–54. http:
//dx.doi.org/10.1016/S0961-9534(98)00080-4.
[122] Poeplau C, Don A. Soil carbon changes under Miscanthus driven by C-4
accumulation and C-3 decompostion—toward a default sequestration func-
tion. Global Change Biol Bioenergy 2014;6:327–38. http://dx.doi.org/10.1111/
Gcbb.12043.
[123] Palmer MM, Forrester JA, Rothstein DE, Mladenoff DJ. Establishment phase
greenhouse gas emissions in short rotation woody biomass plantations in the
Northern Lake States, USA. Biomass Bioenergy 2014;62:26–36. http://dx.doi.
org/10.1016/j.biombioe.2014.01.021.
[124] Chauuat M, Perez G, Hedde M, Lamy I. Establishment of bioenergy crops on
metal contaminated soils stimulates belowground fauna. Biomass Bioenergy
2014;62:207–11. http://dx.doi.org/10.1016/j.biombioe.2014.01.042.
[125] Werling BP, Meehan TD, Robertson BA, Gratton C, Landis DA. Biocontrol
potential varies with changes in biofuel-crop plant communities and land-
scape perenniality. Global Change Biol Bioenergy 2011;3:347–59. http://dx.
doi.org/10.1111/j.1757-1707.2011.01092.x.
[126] Ma Z, Wood CW, Bransby DI. Soil management impacts on soil carbon
sequestration by switchgrass. Biomass Bioenergy 2000;18:469–77.
[127] Ma Z, Wood CW, Bransby DI. Carbon dynamics subsequent to establishment
of switchgrass. Biomass Bioenergy 2000;18:93–104.
[128] Talbot B, Ackerman PA. Renewable energy: the potential opportunities and
obligations of plantation forestry. South For 2009;71:79–83. http://dx.doi.
org/10.2989/Sf.2009.71.1.11.748.
[129] Tilman D, Socolow R, Foley JA, Hill J, Larson E, Lynd L, et al. Beneficial
biofuels—the food, energy, and environment trilemma. Science
2009;325:270–1. http://dx.doi.org/10.1126/science.1177970.
[130] Howard DC, Burgess PJ, Butler SJ, Carver SJ, Cockerill T, Coleby AM, et al.
Energyscapes: linking the energy system and ecosystem services in real
landscapes. Biomass Bioenergy 2013;55:17–26. http://dx.doi.org/10.1016/j.
biombioe.2012.05.025.
[131] Bateman IJ, Harwood AR, Mace GM, Watson RT, Abson DJ, Andrews B, et al.
Bringing ecosystem services into economic decision-making: land use in the
United Kingdom. Science 2013;341:45–50. http://dx.doi.org/10.1126/science.
1234379.
[132] Asbjornsen H, Hernandez-Santana V, Liebman M, Bayala J, Chen J, Helmers M,
et al. Targeting perennial vegetation in agricultural landscapes for enhancing
ecosystem services. Renewable Agric Food Syst 2014;29:101–25. http://dx.
doi.org/10.1017/S1742170512000385.
[133] Wright M, Brown RC. Establishing the optimal sizes of different kinds of
biorefineries. Biofuels, Bioprod Biorefin 2007;1:191–200. http://dx.doi.org/
10.1002/bbb.25.
[134] Liu J, Hull V, Batistella M, DeFries R, Dietz T, Fu F, et al. Framing sustainability
in a telecoupled world. Ecol Soc 2013:18.
[135] Crossman ND, Burkhard B, Nedkov S, Willemen L, Petz K, Palomo I, et al.
A blueprint for mapping and modelling ecosystem services. Ecosyst Serv
2013;4:4–14. http://dx.doi.org/10.1016/j.ecoser.2013.02.001.
[136] Luck GW, Chan KM, Klien CJ. Identifying spatial priorities for protecting
ecosystem services. (F1000). Research 2012:1.
[137] Bateman IJ. Bringing the real world into economic analyses of land use value:
incorporating spatial complexity. Land Use Policy 2009;26:S30–42. http://dx.
doi.org/10.1016/j.landusepol.2009.09.010.