Restoration of Biodiversity and Ecosystem Services on Agricultural Land

Abstract

Cultivation and cropping are major causes of destruction and degradation of natural ecosystems throughout the world. We face the challenge of maintaining provisioning services while conserving or enhancing other ecosystem services and biodiversity in agricultural landscapes. There is a range of possibilities within two types of intervention, namely “land sharing” and “land separation”; the former advocates the enhancement of the farmed environment, but the latter a separation between land designated for farming versus conservation. Land sharing may involve biodiversity-based agricultural practices, learning from traditional farming, changing from conventional to organic agriculture and from “simple” crops and pastures to agro-forestry systems, and restoring or creating specific elements to benefit wildlife and particular services without decreasing agricultural production. Land separation in the farmland context involves restoring or creating non-farmland habitat at the expense of field-level agricultural production—for example, woodland on arable land. Restoration by land sharing has the potential to enhance agricultural production, other ecosystem services and biodiversity at both the field and landscape scale; however, restoration by land separation would provide these benefits only at the landscape scale. Although recent debate has contrasted these approaches, we suggest they should be used in combination to maximize benefits. Furthermore, we suggest “woodland islets”, an intermediate approach between land abandonment and farmland afforestation, for ecological restoration in extensive agricultural landscapes. This approach allows reconciliation of farmland production, conservation of values linked to cultural landscapes, enhancement of biodiversity, and provision of a range of ecosystem services. Beyond academic research, restoration projects within agricultural landscapes are essential if we want to halt environmental degradation and biodiversity loss.

Full text

Restoration of Biodiversity
and Ecosystem Services
on Agricultural Land
Jose
´M. Rey Benayas
1
* and James M. Bullock
2
1
Departamento de Ecologı
´a, Universidad de Alcala
´, 28871 Alcala
´de Henares, Spain;
2
Centre for Ecology and Hydrology, Maclean
Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK
ABSTRACT
Cultivation and cropping are major causes of
destruction and degradation of natural ecosystems
throughout the world. We face the challenge of
maintaining provisioning services while conserving
or enhancing other ecosystem services and biodi-
versity in agricultural landscapes. There is a range
of possibilities within two types of intervention,
namely ‘‘land sharing’’ and ‘‘land separation’’; the
former advocates the enhancement of the farmed
environment, but the latter a separation between
land designated for farming versus conservation.
Land sharing may involve biodiversity-based agri-
cultural practices, learning from traditional farm-
ing, changing from conventional to organic
agriculture and from ‘‘simple’’ crops and pastures
to agro-forestry systems, and restoring or creating
specific elements to benefit wildlife and particular
services without decreasing agricultural produc-
tion. Land separation in the farmland context
involves restoring or creating non-farmland habitat
at the expense of field-level agricultural produc-
tion—for example, woodland on arable land.
Restoration by land sharing has the potential to
enhance agricultural production, other ecosystem
services and biodiversity at both the field and
landscape scale; however, restoration by land sep-
aration would provide these benefits only at the
landscape scale. Although recent debate has con-
trasted these approaches, we suggest they should
be used in combination to maximize benefits.
Furthermore, we suggest ‘‘woodland islets’’, an
intermediate approach between land abandonment
and farmland afforestation, for ecological restora-
tion in extensive agricultural landscapes. This
approach allows reconciliation of farmland pro-
duction, conservation of values linked to cultural
landscapes, enhancement of biodiversity, and pro-
vision of a range of ecosystem services. Beyond
academic research, restoration projects within
agricultural landscapes are essential if we want to
halt environmental degradation and biodiversity
loss.
Key words: agroforestry; financial support; land
separation; land sharing; organic agriculture; rec-
onciliation; secondary succession; tree plantations;
woodland islets.
INTRODUCTION
Currently, about 80% of the planet’s surface
shows evidence of human intervention (Ellis and
Ramankutty 2008). This implies large losses of
biodiversity (Butchart and others 2010) and of the
variety and amount of all ecosystem services (that
Received 21 September 2011; accepted 23 March 2012;
published online 19 May 2012
Author Contributions: Both authors have contributed substantially to
the work. J.M. Rey Benayas conceived the study and both J. M. Rey
Benayas and J. M. Bullock wrote the paper.
*Corresponding author; e-mail: josem.rey@uah.es
Ecosystems (2012) 15: 883–899
DOI: 10.1007/s10021-012-9552-0
2012 Springer Science+Business Media, LLC
883

is, the benefits that people obtain from ecosystems)
except certain provisioning services (MEA 2005). A
large part of such environmental degradation is due
to the expansion of the agricultural frontier in
many parts of the world together with intensifica-
tion of farming methods (BirdLife International
2008; FAO 2010; Mulitza and others 2010). For
instance, Ellis and Ramankutty (2008) indicated 14
of the world’s 21 major biome types which have
agricultural use. Predictions suggest that human-
ity’s footprint will expand in the future (Hockley
and others 2008; Pereira and others 2010; WWF
2010).
One of the most powerful approaches to coun-
tering the negative impacts of agricultural expan-
sion and intensification is ecological restoration.
Ecological restoration aims to recover the charac-
teristics of an ecosystem, such as its biodiversity
and functions, which have been degraded or
destroyed, generally as a result of human activities
(Society for Ecological Restoration International
Science and Policy Working Group 2004). Resto-
ration actions are increasingly being implemented
in response to the global biodiversity crisis, and are
supported by global agreements such as the Con-
vention for Biological Diversity (CBD) (Sutherland
and others 2009). Three major targets of the new
CBD strategic plan for 2020 arising from the
Nagoya Conference in 2010 are to eliminate sub-
sidies harmful to biodiversity, halve or bring close
to zero the rate of loss of all natural habitats, and
restore at least 15% of degraded ecosystems
(Normile 2010). Such policy initiatives are useful,
but raise questions about our ability to manage and
restore ecosystems to supply multiple ecosystem
services and biodiversity (Rey Benayas and others
2009; Bullock and others 2011).
Ecosystem management that attempts to maxi-
mize a particular ecosystem service often results in
substantial declines in the provision of other eco-
system services (Bennet and others 2009). As a
consequence, there is often a trade-off between
agricultural production versus other services and
conservation of biodiversity (Green and others
2005; Pilgrim and others 2010). Thus, we face the
challenge of increasing provisioning services such
as food production—by 70% for 2050 according to
FAO (2009)—for an expanding population while
simultaneously conserving or enhancing biodiver-
sity and the other types of ecosystem services (for
example, regulating and cultural services) in agri-
cultural systems (Kiers and others 2008). Rey
Benayas and others (2009) showed a positive
relationship between biodiversity and provision of
ecosystem services in restored versus degraded
ecosystems in a wide variety of ecosystems. How-
ever, restoration of biodiversity and of services is
not the same thing (Bullock and others 2011). For
instance, especially in agricultural land, concen-
tration on services such as carbon or water reten-
tion may be in conflict with biodiversity (Ridder
2008; Cao and others 2009; Putz and Redford
2009).
In this article, after examining the complex role of
agricultural systems in both delivering and harming
biodiversity (the ‘‘agriculture and conservation
paradox’’), we review approaches to enhance both
biodiversity and ecosystem services in agricultural
landscapes. Recent discussions of the future of
farming have contrasted ‘‘land sharing’’—some-
times called ‘‘environmental- or wildlife-friendly
farming’’—with ‘‘land separation.’’ The former
advocates the enhancement of the farmed envi-
ronment, whereas the latter advocates a separation
of land designated for farming from that for con-
servation (Green and others 2005; Fischer and
others 2008; Hodgson and others 2010; Phalan and
others 2011). Land separation is usually referred to
as ‘‘land-sparing’’ when high-yield farming is com-
bined with protecting natural habitats from con-
version to agriculture (for example, Phalan and
others 2011). We will argue that these approaches
should not be seen as alternatives, but as repre-
senting the range of actions that can be combined to
best enhance biodiversity and ecosystem services.
On one side, we will examine the potential to pro-
duce systems in which agricultural production and
conservation or enhancement of biodiversity and of
ecosystem services other than agricultural produc-
tion is in partnership rather than in conflict. We will
show an exemplary case study to illustrate examples
of existing options to achieve such a goal. Cropland
has mostly spread at the expense of forest land and
natural grassland (Foley and others 2005). Thus, on
the other side, we will focus on forest regrowth and
tree plantations on cropland as examples of land
separation by natural habitat restoration. Finally,
we will discuss the necessity of restoration projects
in the real world beyond academic research and the
key issues that must be addressed for a wide imple-
mentation of such projects.
The Agriculture and Conservation
Paradox
Few human activities are as paradoxical as agri-
culture in terms of their role for nature conserva-
tion. Agricultural activities are the major source of
884 J. M. Rey Benayas and J. M. Bullock

negative environmental impacts worldwide (Kiers
and others 2008). For instance, agriculture is the
main cause of deforestation (FAO 2010), the major
threat to bird species (BirdLife International 2008),
accounts for approximately 12% of total direct glo-
bal anthropogenic emissions of greenhouse gases
(IPCC 2007), and strongly impacts soil carbon and
nutrients (McLauchlan 2006). Cropland and grazing
land footprints accounted for approximately 24 and
7%, respectively, of the total human global footprint
in 2007 (WWF 2010). These figures vary greatly
among countries (Table 1). They are proportionally
the lowest, approximately 18 and 4%, respectively,
in the 31 OECD countries, which include the
world’s richest economies, and the highest, about 36
and 14%, respectively, in the 53 African Union
countries, which include some of the world’s poor-
est and least developed countries (WWF 2010).
Agricultural land covers over 40% of the terres-
trial surface, to the detriment of natural vegetation
cover (Foley and others 2005). At the global scale,
the conversion of natural ecosystems to agricultural
systems has currently reached a plateau (Figure 1).
However, there is great variation among countries;
agricultural land has declined in some whereas it
has increased in others—chiefly developing coun-
tries that harbor the highest amounts of biodiver-
sity (for example, Cayuela and others 2006;
Table 1).
In recent history, farming practices in many areas
have become more intensive, and increasing
amounts of water, fuel, fertilizers, pesticides, her-
bicides, and non-native species are used worldwide
to enhance production. For example, the global
area serviced by irrigation now accounts for
approximately 20% of cultivated land (FAOSTAT
2011; Figure 1). Agriculture is the major form of
human water consumption in the world and
threatens water security and habitats (Vorosmarty
and others 2010). Beyond changes in species rich-
ness, agricultural intensification has been shown to
reduce the functional diversity of plant and animal
communities, potentially imperiling the provision-
ing of ecosystem services (Flynn and others 2009).
Many studies have found negative effects of agro-
chemicals on biodiversity and ecosystem function
(for example, Rohr and others 2008; Geiger and
others 2010). Intensification of land use has
brought remnant areas of natural vegetation such
as steep hillsides, property boundaries, and track
edges into mainstream agriculture (Rey Benayas
and others 2008). Thus, agricultural expansion and
intensification have greatly increased our food
supplies at the global scale, but have damaged
biodiversity and other services.
In contrast to these negative perspectives, habi-
tats converted to agricultural activities are often
viewed positively in terms of nature conservation
due to, for example, creation of landscape mosaics
and environmental heterogeneity (Dornelas and
others 2009; Oliver and others 2010; Sitzia and
others 2010), or because they are threatened hab-
itats that support endangered species and cultural
values (Kleijn and others 2006; Lindemann-
Matthies and others 2010). In the EU-27, 31% of
Natura 2000 sites, a network of protected areas,
result from agricultural land management. Several
taxa including species of birds, insects and plants,
some of them endangered, depend on low-inten-
sity farmland for their persistence (Doxa and others
2010; Kohler and others 2011). Thus, regional
trends of common farmland birds in Europe show
negative trends (-35% since 1980) and are of
conservation concern, whereas forest birds show
positive trends due to abandonment of agricultural
land and afforestation programs (European Bird
Census Council 2010). Such declines might affect
agricultural production itself. Insects that provide
pollination and pest control services in cropland
tend to be less common in more intensive land-
scapes (Tscharntke and others 2005; Potts and
others 2010).
Agricultural intensification can have a negative
impact on the values linked to traditional agricul-
ture, but so can agricultural abandonment and,
particularly, afforestation of former cropland (Rey
Benayas and others 2007; Sitzia and others 2010).
Abandonment of agricultural land has mostly
occurred in developed countries in the last few
decades (Table 1) and it is currently happening in
developing countries with strong rural migration to
urban areas such as in Latin America (Rey Benayas
and others 2007; Grau and Aide 2008). The Euro-
pean Agrarian Policy is providing subsidies to
afforest land after vineyard extirpation in Spain, an
action that is being criticized by conservationists
due to negative impacts on esthetic and other
values. The Chinese Grain for Green project is a
major, but controversial, project related to affores-
tation of former cropland (Cao and others 2009; see
below). It seems that agriculture, woodland, and
biological conservation are in a permanent and
irreconcilable conflict, the agriculture and conser-
vation paradox (Rey Benayas and others 2008).
Enhancing Biodiversity and Ecosystem
Services in Agricultural Landscapes
There is a range of possibilities to reverse the neg-
ative environmental impacts of agriculture. Some
Restoration of Biodiversity and Ecosystem Services 885

Table 1. Statistics, for 20 Selected Countries that are Representative of Different Economies in the World, on Ecological Footprint, Percentage of
Cropland and Grassland Footprint in the Ecological Footprint, Percentage of Area of Agricultural Land, Total Forest and Forest Plantations, and their
Changes in the Last Few Decades, and Gross Per Capita Domestic Product
Country Ecological
footprint 2007
(global ha/
person)
Cropland
footprint
2007 (%)
Grassland
footprint
2007 (%)
Agricultural
area (2008,
% on land
area)
Change in
agricultural
land area
(% since 1961)
Total forest
area (2010,
% on land
area)
Forest
plantations
area (2010,
% on total
forest area)
Change in
total forest
area (% since
1990)
Change in
forest
plantation
area (%
since 1990)
Grosse per
capita domestic
product (USD)
Afghanistan 0.6 53.33 25 58.2 0.56 2 – 0.00 – 1103
Brazil 2.9 24.83 32.08 31.27 75.71 62 1 -8.86 15 10304
Canada 7.0 13.57 3.71 7.43 -3.19 34 3 0.00 586 39078
China 2.2 24.09 5 56.02 52.24 22 37 28.12 39 5971
Colombia 1.9 20.53 39.47 38.4 6.61 55 1 -2.91 356 8797
Germany 5.1 24.51 4.11 48.54 -12.66 32 48 3.12 1 35374
Guatemala 1.8 23.89 12.22 39.36 59.41 34 5 -20.61 365 4760
India 0.9 43.33 0.04 60.44 2.74 23 16 6.58 68 2946
Jamaica 1.9 27.89 5.26 42.84 -12.95 31 2 -1.93 -23 7716
Mali 1.9 38.42 43.68 32.48 25.02 10 4 -10.12 11158 1129
Mexico 3.0 27.67 10.66 52.73 4.33 33 5 -7.37 232* 14570
Nepal 3.6 10.28 1.38 29.44 19.23 25 1 -24.52 20 1104
Russia 4.4 20.23 2.27 13.16 -2.77 49 2 -0.01 28 15923
Serbia 2.4 27.92 2.5 57.22 -0.20 31 7 3.76 353 10554
Spain 5.4 26.85 5 55.90 -16.04 36 15 28.97 2 31674
United Arab Emirates 10.7 12.62 3.85 6.82 174.04 4 100 28.65 0.00 37442
Thailand 2.4 24.17 0.83 38.46 68.63 44 21 -3.10 54 8086
Togo 1.0 31 0.9 66.74 18.24 5 15 -52.32 328 830
UK 4.9 17.76 5.51 73.10 -10.69 12 77 9.79 2 35468
USA 8.0 13.50 1.75 44.95 -8.11 33 8 2.34 32 46350
*Change since 2000.
Sources: Footprint Network (http://www.footprintnetwork.org/) for ecological footprint data; FAOSTAT 2011 (http://faostat.fao.org) for percentage of area of agricultural land and its change, updated to year 2008; FAO 2011 for
percentage of area of total forest and forest plantations in 2010 and their changes as well as for GDP.
886 J. M. Rey Benayas and J. M. Bullock

of these options have the potential to enhance
biodiversity and ecosystem services including agri-
cultural production, but others may enhance bio-
diversity and ecosystem services other than
agricultural production. They can be considered
within two major approaches:
(1) Land sharing. We can classify five types of
intervention following this approach. Four involve
extensive actions on agricultural land with a focus
on productivity, that is, making agriculture more
wildlife- (and ecosystem service) friendly: (a)
adoption of biodiversity-based agricultural practices;
(b) learning from traditional farming practices; (c)
transformation of conventional agriculture into
organic agriculture; or (d) transformation of ‘‘sim-
ple’’ crops and pastures into agroforestry systems.
The fifth (e) involves restoring or creating specific
elements to benefit wildlife and particular services
without competition for agricultural land use.
In practice, these interventions may be carried
out concurrently as they are not exclusive
(Figure 2).
(2) Land separation in the farmland restoration
context involves restoring or creating non-farm-
land habitat in agricultural landscapes at the
expense of field-level agricultural production—for
example, woodland, natural grassland, wetland,
and meadow on arable land. This approach does
not necessarily imply high-yield farming of the
non-restored, remaining agricultural land.
Next, we will document some examples of these
two types of intervention to enhance biodiversity
and ecosystem services in agricultural landscapes.
Land Sharing
Adoption of Biodiversity-Based Agricultural Practices
Conservation of existing biodiversity in agricultural
landscapes and the adoption of biodiversity-based
practices have been proposed as ways of improving
the sustainability of agricultural production
through greater reliance on ecological goods and
services, and with less damaging effects on envi-
ronmental quality and biodiversity (McNeely and
Scherr 2003; Jackson and others 2007). Manage-
ment of biodiversity, that is, the biota dwelling in
agroecosystems as well as habitats and species
outside of farming systems in the landscape (Van-
dermeer and Perfecto 1995), can be used to benefit
agricultural production and enhance ecosystem
services.
Examples of agrobiodiversity functioning at dif-
ferent hierarchical levels include (Jackson and
others 2007): (1) genetic and population charac-
teristics—for example, the use of traditional varie-
ties and wild species for continuing crop and
livestock improvement for increased pest resistance,
yield, and quality (Cooper and others 2001; Tisdell
2003); (2) community assemblages or guilds that
influence agricultural production, such as pest
Figure 1. Global total agricultural area, agricultural irrigated area, organic agricultural area, total forest area, forest
plantation area, and secondary forest area in the last few decades. Sources: FAOSTAT 2011 (http://faostat.fao.org) for data
on total agricultural area and agricultural irrigated area, updated to year 2008; The World of Organic Agriculture. Statistic
and Emerging Trend 2009, IFOAM, Bonn and FiBL, Frick (http://www.ifoam.org/), for organic agricultural area; FAO
(2011) for data on forest area. The observed trends indicate a general increase in total agricultural area, which peaked in
2001, irrigated agricultural area—an indicator of agricultural intensification—, and forest plantation area, which mitigates
the loss of total forest area. The proportion of organic agricultural area is marginal.
Restoration of Biodiversity and Ecosystem Services 887

control based on toxin biosynthesis or other plant
defences against herbivore attack, crop mixtures,
release of natural enemies, and pest suppression by
a complex soil food web (Dicke and others 2004)or
increased yield following inter-cropping and crop
rotation (Chabi-Olaye and others 2005); (3) heter-
ogeneity of biota in relation to biophysical processes
within ecosystems, such as nutrient cycling and
retention or carbon accumulation (van Noordwijk
2002); and (4) landscape-level interactions between
agricultural and non-agricultural ecosystems that
enhance resources for agriculture, and potentially,
resilience during environmental change—for
example, agricultural landscapes that are composed
of a mosaic of well-connected early and late suc-
cessional habitats may be more likely to harbor
biota that contribute to regulating and supporting
services for agriculture, compared to simple
Figure 2. Sketch of a real restoration project based on a range of land sharing types and actions—that are explained in the
main text—intended to enhance the farmed environment, which is run by the Fundacio
´n Internacional para la Res-
tauracio
´n de los Ecosistemas (www.fundacionfire.org) in Valdepen
˜as (central Spain). This and similar projects have been
acknowledged as among the best 13 projects that reconcile agricultural production and biodiversity conservation in this
country. The 2-ha field mostly consists of a certified organic olive grove (type c in the text), which was established after a
1-year fallow period (type b). A row of singular fruit tree seedlings, that is, from healthy and locally adapted variety fruit
trees, of three different species is inter-cropped with the dominant olive tree crop (types a and c). The following specific
elements (type e) have been introduced in the crop system to benefit wildlife and particular services (mentioned in
parentheses): (1) a hedge row plantation consisting of approximately 1,100 seedlings of ten native species in the region (to
mitigate soil erosion, abrasion of the crop, attraction of pollinators and natural enemies, community diversification, and
seed exportation to accelerate passive restoration of nearby abandoned cropland, a means of land separation); (2) a pond
(chiefly to favor amphibians and birds, particularly game species such as the red-legged partridge Alectoris rufa, which are
an input to the local economy); (3) perch and nest boxes (enhancement of small birds of prey that are intensive rodent
consumers); (4) conditioning of stone mounds (creation of habitat and refuges for wildlife); and (5) construction of a stone
hut, a jewel of the local rural architecture (enhancement of the cultural value of this project).
888 J. M. Rey Benayas and J. M. Bullock

landscapes (Elmqvist and others 2003; Bianchi and
others 2006).
Learning from Traditional Farming Practices
Traditional farming describes practicesthat developed
through human history to produce a variety of agri-
cultural goods, largely for local use. Forms of tradi-
tional farming persist in many parts of the world,
particularly in developing countries, but also in more
developed countries, where such methods are rem-
nants or have been re-introduced to meet specific
needs (Altieri 2004; Kleyer and others 2007). Tradi-
tional farming methods are extremely diverse, by
their nature, but they often share a number of dis-
tinguishing characteristics in comparison to intensive
systems: on-farm cycling of nutrients and resources,
the development of local varieties and breeds, high
spatial and temporal structural diversity, use of local
pollination and pest control services, and effective
exploitation of local environmental heterogeneity
(Altieri 2004). Although modern, intensive farming
methods are usually better than traditional methods
at maximizing production, they do so by increasingly
using vast off-farm resources, such as inorganic
fertilizers, new crop breeds and specialized machinery
(Woods and others 2010). In comparison to these
intensive approaches, traditional farming in many
countries has been shown to have many environ-
mental and societal benefits, including enhancement
of soil carbon sequestration (Ardo and Olsson 2004)
and nutrient cycling (Badalucco and others 2010),
reduction of soil erosion (He and others 2007), more
efficient water use (Prasad and others 2004), and
maintenance of crop genetic diversity (Pujol and
others 2005; Jarvis and others 2008), as well as pro-
viding resources for endangered species (Blanco and
others 1998; Olea and Mateo-Tomas 2009).
Continuation of traditional farming is one matter
(Altieri 2004), but it is probably not possible or
desirable to ‘‘turn back the clock’’ in areas of more
intensive farming. Wholesale reversion to earlier
agricultural methods would reduce food produc-
tion massively; for example, the current UK wheat
yield per hectare is more than threefold that real-
ized in 1945 (UK National Ecosystem Assessment
2011). Furthermore, certain traditional methods,
such as swidden agriculture, may sometimes be
damaging to biodiversity and to soil and water
resources (Ziegler and others 2010). It is therefore
more appropriate to learn lessons from traditional
approaches which can be applied to modern agri-
cultural systems. Perhaps the most important idea
to borrow is to increase within- and between-farm
diversity in terms of crops, cropping systems and
land use. Such structural diversity at a variety of
scales can reduce vulnerability of crop yield to
between-year climatic variability (Reidsma and
Ewert 2008), as well as increase biodiversity and
associated ecosystem services (Benton and others
2003; Tscharntke and others 2005). Local rever-
sions to traditional management approaches are
being implemented, for example, through the
European agri-environment schemes. Options
within these include a return to traditional live-
stock grazing rates and/or seasons, which can help
weed control (Pywell and others 2010) and main-
tenance of plant and animal diversity (Redpath and
others 2010); replacement of inorganic fertilizers
with farmyard manure, with positive impacts on
soil organic matter (Hopkins and others 2011); or
re-creating traditional species-rich grasslands, in
which increased plant diversity enhances forage
production (Bullock and others 2007). More gen-
erally, there is global interest in more traditional
approaches to soil tillage involving reduced fre-
quency and depth, which can enhance soil nutri-
ent cycling and stability, and pest control, while
also reducing energy use (Roger-Estrade and others
2010; Woods and others 2010).
Transformation of Conventional Agriculture into Organic
Agriculture
There has been a considerable expansion of organic
farmland area in the world (a threefold increase
between 1999 and 2006), chiefly in developed
countries. The demand for healthy and environ-
mental-friendly food and subsidies to producers of
organic food and fiber has favored this process
(Pimentel and others 2005). However, organic
farming remains a tiny fraction of the farming
activity (Figure 1), comprising 4.1 and 0.42% of
the total agricultural area in EU27+ and the USA in
2008, respectively (FAOSTAT 2011).
The benefits of organic farming to the environ-
ment are well described, and include less contam-
ination by fertilizers, herbicides and pesticides,
increases in biodiversity (Bengtsson and others
2005; Hole and others 2005; Rundlof and others
2008; Aviron and others 2009; Danhardt and oth-
ers 2010; Gabriel and others 2010; Jose-Maria and
others 2010), enhancement of soil carbon seques-
tration and nutrients (Kimble 2002; Pimentel and
others 2005), enhancement of natural pest control
(Macfadyen and others 2009; Crowder and others
2010), and conservation of the genetic diversity of
local varieties of domestic plants and animals
(Jarvis and others 2008). Importantly, other than
benefits related to the environment and human
Restoration of Biodiversity and Ecosystem Services 889

health, it has been demonstrated that organic
farming usually produces similar or higher quan-
tities of agricultural products (Pimentel and others
2005; Crowder and others 2010) and with higher
market prices than conventional farming (Born
2004; Pimentel and others 2005), which can make
it extremely profitable (Delbridge and others
2011).
However, recent work has shown that careful
spatial planning and targeting of organic agricul-
ture will be required to maximize benefits (Gabriel
and others 2010). Meta-analyses of the effects of
organic farming on species diversity have shown
variable results among studies and taxa, with
detrimental effects of organic farming in 16%
(Bengtsson and others 2005) or 8.1% (Hole and
others 2005) of the individual studies. Bengtsson
and others (2005) also found no significant effects
of organic farming on soil microbial activity or
biomass. Organic farming uses three broad man-
agement practices (prohibition/reduced use of
chemical pesticides and inorganic fertilizers, sym-
pathetic management of non-cropped habitats, and
preservation of mixed farming) that are largely
intrinsic (but not exclusive) to organic farming, and
that are particularly beneficial for farmland wildlife
(Bengtsson and others 2005; Hole and others
2005). Thus, the role of organic farming per se in
enhancement of biodiversity and ecosystem ser-
vices is unclear. Positive effects of organic farming
on species richness might be expected in inten-
sively managed agricultural landscapes, but not in
small-scale landscapes comprising many other
biotopes as well as agricultural fields. Conse-
quently, measures to preserve and enhance biodi-
versity should be more landscape- and farm-
specific than is presently the case (Bengtsson and
others 2005; Danhardt and others 2010; Gabriel
and others 2010).
Transformation of Simple Crops and Pastures into
Agroforestry Systems
Agroforestry is the purposeful growing of trees/
shrubs with crops or pasture. These approaches offer
opportunities in both tropical and temperate regions
(Rigueiro-Rodrı´guez and others 2009; Bergmeier
and others 2010). Agroforestry can augment biodi-
versity and ecosystem services in agricultural land-
scapes, while also providing income for rural
livelihoods. It can be a management tool of buffer
zones and biological corridors to enhance landscape
connectivity and landscape-level biodiversity
(Vandermeer and Perfecto 2007; Rigueiro-
Rodrı´guez and others 2009; Lombard and others
2010). Agroforestry represents an intermediate step
between natural secondary forests (Cramer and
Hobbs 2007) and reclamation of severely degraded
land (Koch and Hobbs 2007) in terms of high versus
low provision of biodiversity and ecosystem services,
state of degradation, and time and costs of forest
restoration (Chazdon 2008). Agro-successional
restoration schemes have been proposed, which
include agro-ecological and agroforestry techniques
as a step prior to forest restoration (Vieira and others
2009).
Restoring or Creating Specific Elements to Benefit Wildlife
and Particular Services
This type of intervention encompasses highly spe-
cific actions intended to benefit wildlife and par-
ticular services such as pollination and game
production. These actions are so characterized be-
cause they occupy a tiny fraction of the agricultural
land if any at all, meaning that they hardly com-
pete for farmland use. Actions include (1) strategic
revegetation of property boundaries, field margins,
and track edges to create living fences (Noordijk
and others 2010; Pereira and Rodriguez 2010;
Poggio and others 2010); (2) planting isolated trees
to take advantage of their disproportionate positive
value for biodiversity conservation and potential
for seed dispersal (DeMars and others 2010; Fischer
and others 2010); (3) creation of pollinator-
friendly areas using plant enrichment (Kohler and
others 2008; Ricketts and others 2008; Carvalheiro
and others 2010; Hagen and Kraemer 2010); (4)
introduction of beetle banks, stone walls, stone
mounds and other strategic refuges for fauna
(MacLeod and others 2004); (5) introduction of
perches and nest boxes for birds (see example be-
low); and (6) introduction or restoration of drink-
ing troughs; (7) the reconstruction of rural
architecture is specifically intended to restore and
value cultural services. There will usually be scale
effects on biodiversity and ecosystem services
depending on how much land is affected by these
actions.
GREFA’s (http://www.grefa.org/) project for
enhancement of birds of prey for rodent control is
an outstanding example of this type of wildlife-
friendly farming. This project was motivated by
periodic field vole Microtus arvalis outbreaks, which
are often controlled using poisons that may damage
wildlife and game. Common kestrel Falco tinnun-
culus and barn owl Tyto alba are rodent predators
that have declining populations for a number of
reasons, including lack of sites for nesting in open
landscapes. Thus, more nesting sites (photo in
890 J. M. Rey Benayas and J. M. Bullock

Figure 2) should increase the populations of these
two species and contribute to place their popula-
tions at the carrying capacities. To achieve this goal,
a 2,000 ha agricultural landscape in central Spain
was seeded with nest boxes. We calculate that total
rodent consumption could be as high as around
46,250 kg y
-1
if full nest occupancy by both species
were attained, a figure that is expected to contrib-
ute to rodent damage control and the maintenance
of these birds of prey species.
Land Separation
Land separation and land sharing are sometimes
treated as alternatives (for example, Phalan and
others 2011). However, as different actions benefit
different species and ecosystem services (Brussard
and others 2010; Pilgrim and others 2010; Phalan
and others 2011), a variety of approaches would
likely be the most successful at enhancing biodi-
versity and ecosystem services. Setting aside farm-
land to restore or create non-farm habitat rarely
happens as farmers tend to use and expand into all
available land because this is usually the most
profitable choice in terms of direct use value (TEEB
2010). There are, though, some examples of habitat
restoration at the expense of farmland, including
both terrestrial (see below) and wetland ecosystems
(Thiere and others 2009; Moreno-Mateos and
others 2010). Two major contrasting approaches for
terrestrial ecosystem restoration in agricultural
landscapes are (1) passive restoration through sec-
ondary succession following abandonment of agri-
cultural land, for example, cropland and pastures
where extensive livestock farming has been
removed; and (2) active restoration, for example,
through addition of desired plant species. These
approaches have been contrasted for a variety of
ecosystem targets, including species-rich grassland
(Pywell and others 2002) and heathland (Pywell
and others 2011), but in the following we focus on
forest restoration.
The estimated global deforestation rate of
13 million ha y
-1
over the last 10 years has
resulted in a net loss of forest area of 5.2 million ha
y
-1
or 0.13% y
-1
(FAO 2011). In the past, land
abandonment and passive restoration led to the
reforestation of a larger surface area than active
restoration (e.g. 4.1 versus 3.6 million ha y
-1
,
respectively, in 2000–2005; FAO 2006). Over the
period 2000–2010, these figures reversed and they
are now 2.9 versus 4.9 million ha y
-1
, respectively
(FAO 2011). Now 36% of forest area is primary
forests, 57% is secondary forests, and 7% is forest
plantations (FAO 2010).
Passive restoration is cheap (although it may
include opportunity costs) and leads to a local
vegetation type (Myers and Harms 2009). It is
generally fast in productive environments, but slow
in low productivity environments as woody vege-
tation establishment is limited (Rey Benayas and
others 2008). The restoration capacity of woody
ecosystems depends on the magnitude and dura-
tion of ecosystem modification, that is, the ‘‘agri-
cultural legacy’’ (Dwyer and others 2010). A key
bottle-neck that hinders revegetation in vast agri-
cultural landscapes is the lack of propagules due to
absence of mother trees and shrubs (Garcia and
others 2010)
Active forest restoration basically comprises the
planting of trees and shrubs. It is needed, for
example, when abandoned land suffers continuing
degradation, local vegetation cover cannot be
recovered and secondary succession has to be
accelerated. There are differences in the biodiver-
sity and ecosystem services provided by passive
versus active restoration, and there is much debate
about the ecological benefits of tree plantations. For
instance, the mean increment of carbon in young
secondary forests of Costa Rica is 4.18 Mg ha
-1
y
-1
in the biomass (including below ground biomass)
and 1.07 Mg ha
-1
y
-1
in the soil (Fonseca and
others 2011a). These figures are higher in planta-
tions of the native tree species Vochysia guatemal-
ensis (7.07 Mg ha
-1
y
-1
in the biomass and
1.66 Mg ha
-1
y
-1
in the soil) and Hieronyma
alchorneoides (5.26 Mg ha
-1
y
-1
in the biomass and
1.27 Mg ha
-1
y
-1
in the soil) (Fonseca and others
2011b). Plantations are thus better for sequestering
carbon and for timber production than secondary
forests in this and many other case studies (for
example, Piao and others 2009; Rautiainen and
others 2010); however, they are less valuable for
non-timber forest products and biodiversity
(Newton and Tejedor 2011).
Bremer and Farley (2010) analyzed published
data on plant species richness in plantations and
paired land uses, most often representative of pre-
plantation land cover. They found that plantations
are most likely to contribute to biodiversity when
established on degraded lands rather than replacing
natural ecosystems, and when indigenous tree
species are used rather than exotic species. Simi-
larly, a meta-analysis of faunal and floral species
richness and abundance in timber plantations and
pasture lands on 36 sites across the world con-
cluded that plantations support higher species
richness or abundance than pasture land only for
particular taxonomic groups (that is, herpetofa-
una), or specific landscape features (that is, absence
Restoration of Biodiversity and Ecosystem Services 891

of remnant vegetation within pasture) (Felton and
others 2010). Zhang and others (2010) also found
higher levels of plant diversity, soil fertility, and
organic matter on land undergoing secondary
succession than on tree plantations in northwest
China.
China’s Grain to Green project and the affores-
tation of former agricultural land in southern
Europe are examples of trade-offs between differ-
ent types of ecosystem services and biodiversity.
Under the former project, which has the intention
to restore services and biodiversity (Tallis and
others 2008), activities include planting non-native
trees on agricultural land to decrease soil erosion.
This has led to decreased native vegetation cover
and increased water use, suggesting negative im-
pacts on biodiversity and water availability in arid
areas (Cao and others 2009; Chen and others
2010). Cropland afforestations in southern Europe
are mostly based on coniferous species such as
Pinus halepensis and P. pinaster, although other
species are used. The fast-growing plantations are
certainly better for carbon sequestration rates than
secondary succession of Mediterranean shrubland
and woodland (Rey Benayas and others 2010a).
However, these plantations may cause severe
damage to open habitat species, especially birds, by
replacing high quality habitat and increasing risk of
predation (Reino and others 2010). Further, they
have been shown to be suitable habitats for gen-
eralist forest birds but not for specialist forest birds,
whereas secondary succession shrubland and
woodland favor bird species that are of conserva-
tion concern in Europe (Rey Benayas and others
2010a). Navarro-Cano and others (2010) showed
that pine litter from afforestations hinders the
establishment of endemic plants in semiarid
scrubby habitats of the Natura 2000 Network.
Designing Restoration of Forest Ecosystems
on Agricultural Land
The agriculture and conservation paradox creates a
dilemma in woodland restoration projects, which
can only be resolved by considering the relative
values of biodiversity and ecosystem services asso-
ciated with woodland versus agricultural ecosys-
tems (Rey Benayas and others 2008). The
reconstruction of vegetation in a landscape
(‘‘where and when to revegetate?’’) is an issue that
deserves to become a research priority (Munro and
others 2009; Thomson and others 2009). Rey
Benayas and others (2008) suggested a new con-
cept for designing restoration of forest ecosystems
on agricultural land, which uses small-scale active
restoration as a driver for passive restoration over
much larger areas. Establishment of ‘‘woodland
islets’’ is an approach to designing restoration of
woodlands in extensive agricultural landscapes
where no remnants of native natural vegetation
exist. It involves planting a number of small, den-
sely planted, and sparse blocks of native shrubs and
trees within agricultural land that together occupy
a tiny fraction of the area (<1%) of target land to
be restored. This approach, later called ‘‘applied
nucleation’’ by Corbin and Holl (2012), allows
direction of secondary succession by establishing
small colonization foci, while using a fraction of the
resources required for large-scale reforestation.
Woodland patches provide sources of seed and
dispersing animals that can colonize adjacent hab-
itats (Cole and others 2010). If the surrounding
land is abandoned, colonists from the islets could
accelerate woodland development because dis-
persal of many woodland organisms will continue
over many years. The landscape emphasis on a
planned planting of islets maximizes benefits to
biodiversity and the potential of allowing the islets
to trigger larger-scale reforestation if the sur-
rounding land is abandoned. The islets should be
planted with a variety of native shrub and tree
species including those identified as nurse species
to take advantage of facilitation processes (Butter-
field and others 2010; Cuesta and others 2010).
Vegetation dynamics in complex landscapes
depend on interactions among environmental het-
erogeneity, disturbance, habitat fragmentation, and
seed dispersal processes. For instance, European
jays (Garrulus glandarius) are major long-distance
(500–600 m) dispersers of acorns in Mediterranean
landscapes (Go
´mez 2003). The introduction of
woodland islets planted with oaks at a distance of
1 km from each other in a deforested agricultural
landscape could facilitate acorn arrival to all points
in a given landscape (Figure 3). In heterogeneous
Mediterranean landscapes, jays disperse acorns
preferentially toward recently abandoned agricul-
tural fields, forest tracks, and pine reforestations,
while they usually avoid dense shrubland, grass-
lands, and mature holm oak forests (Go
´mez 2003;
Pons and Pausas 2007). Purves and others (2007)
found that jay-mediated directed dispersal increases
regional abundance of three native oak species.
Montoya and others (2008) indicated that animal-
dispersed tree species were less vulnerable to forest
loss than wind-dispersed species, that is, plant–
animal interactions help prevent the collapse of
forest communities suffering habitat destruction.
Accordingly, Ozinga and others (2009) concluded
that the ‘‘colonization deficit’’ of plant species due
892 J. M. Rey Benayas and J. M. Bullock

to a degraded dispersal infrastructure is equally
important in explaining plant diversity losses as
habitat quality, and called for new measures to
restore the dispersal infrastructure across entire
regions.
The woodland islets approach maintains flexi-
bility of land use, which is critical in agricultural
landscapes where land use is subject to a number of
fluctuating policy and economic drivers. It provides
a means of reconciling competing land for agricul-
ture, conservation, and woodland restoration at the
landscape scale. This could increase the economic
feasibility of large-scale restoration projects and
facilitate the involvement of local human com-
munities in the restoration process. The woodland
islets idea has similarities to other approaches
involving planting small areas of trees on farms,
such as tree clumps, woodlots, hedges, living fen-
ces, or shelterbelts and agroforestry systems (see
above). These practices provide ecological benefits
as well as supporting farm production, whereas the
woodland islets approach is primarily designed to
provide additional ecological benefits other than
agricultural production (Rey Benayas and others
2008).
Restoration of Agricultural Landscapes
in the Real World
The response of human society to halt declining
biodiversity indicators and environmental degra-
dation shows positive trends, but so far it has been
insufficient to achieve such goals (Butchart and
others 2010; Rands and others 2010). Production
Figure 3. Simulation of the large area (ca. 1.6 km
2
) that could potentially receive acorn rain following European jay
dispersal from two introduced woodland islets (as shown in the upper photograph) or living fences 1 km apart from each
other in a deforested agricultural landscape located in central Spain. The reported figure derives from an estimated
dispersion distance of 500 m from each woodland islet or living fence (Purves and others 2007). Without the introduction
of these elements, acorn rain and subsequently oak regeneration would not occur because native vegetation has been
virtually extirpated in vast areas of this region.
Restoration of Biodiversity and Ecosystem Services 893

science and conservation biology have long focused
on providing the knowledge base for intensive food
production and biodiversity conservation, respec-
tively, but the largely separate development of
these fields is counterproductive (Brussard and
others 2010). Developing and strengthening a more
interactive relationship between the science of
restoration ecology and agroecology and the prac-
tice of ecological restoration and conservation
farming has been a central but elusive goal
(Gonzalo-Turpin and others 2008; Cabin and oth-
ers 2010). Further research is needed to produce
more sustainable socio-ecosystems (Turner 2010),
but that will not be enough to reach the ultimate
objective. Restoration actions that enhance both
biodiversity and ecosystem services on agricultural
land are necessary to reverse the world’s declining
biodiversity and ecosystem services (Bullock and
others 2011; Foley and others 2011).
The adoption of environmental-friendly practices
for agriculture, however, is not solely based on
services and values that society as a whole obtains
from such functions, as individual farmers are
ultimately the agents who decide how much nat-
ural capital to conserve and utilize based on their
own objectives and needs, including the social,
economic (for example, markets and policies), and
environmental conditions in which they operate
(Jackson and others 2007). One key problem is that
the private and social values of environmental-
friendly farming differ and the markets and policies
often do not align such values properly. The pri-
vately perceived value is reflected by the financial
benefits arising from positive effects on productiv-
ity and/or the savings generated when wildlife-
friendly farming substitutes for costs of synthetic
inputs, for example, pesticides. The total or social
economic value of environmental-friendly farming
includes the value of the ecological services that it
provides to those other than farmers, for example,
through environmental quality, recreation, and
esthetic values. In general, individual farmers react
to the private use value of biodiversity and eco-
system services assigned in the marketplace and
thus typically ignore the ‘‘external’’ benefits of
conservation that accrue to wider society (Jackson
and others 2007).
Key issues for widespread ecological restoration
on agricultural land are financial support and
education to promote farmer and public awareness
and training. Land owners must be explicitly
rewarded for restoration actions occurring at their
properties in a time when society demands from
agricultural land much more than food, fiber, and
fuel production (Klimek and others 2008). The
private financial benefits arising from environ-
mental-friendly agricultural practices explained
above may actually be a reward to land owners, but
may be insufficient. To reward the total or social
value, tax deductions for land owners who imple-
ment measures to restore agricultural land and
donations to not-for-profit organizations that run
restoration projects (most restoration projects are
actually run by NGOs), payment for environmental
services and direct financing measures related to
restoration activities should be put into operation
widely. These support mechanisms are very vari-
able across countries. Incentives related to tax
deductions are more generous in the US (>90% of
the donated amount of money) than in Europe (for
example, 60–65% in France and 25% in Spain),
and non-existent in many countries.
A potentially major approach to funding resto-
rations is through payment for ecosystem services
(PES), which is designed to compensate for actions
that secure services such as water purification,
flood mitigation, or carbon sequestration (Jack and
others 2008). In recent years, many hundreds of
PES have been established worldwide for envi-
ronmental management (Farley and others 2010)
and some have focused on restoration, such as
China’s Grain to Green Program (Tallis and others
2008) and Madagascar’s Mantadia PES (Wendland
and others 2010). Globally, direct financing mea-
sures to support restoration projects have mostly to
do with afforestation measures (Bigsby 2009). In
the EU, major policy measures to support the pro-
vision of environmental public goods through
agriculture are (1) agri-environment measures (a
budget of e34 billion including co-financing for
2007–2013, 34 million ha affected); (2) Life +
Programme (a budget of e2.14 billion for the
period 2007–2013); (3) Natura 2000 (a budget of e
6.1 billion y
-1
for the period 2007–2013, with
about 15 million ha under agricultural manage-
ment); (4) Good Agricultural and Environmental
Condition standards that specify actions beyond
existing legislation focusing specifically on main-
taining landscape features, habitats, soil function-
ality or water quality; (5) aid schemes for forestry
measures in agriculture (about 1 million ha have
been afforested to date); and (6) structural funds
(projects under the heading ‘‘Preservation of the
environment in connection with land …and
landscape conservation’’).
Environmental degradation will continue to
increase while the world’s citizens do not
acknowledge the value of biodiversity and ecosys-
tem services for human well-being. For that shift in
understanding to happen, widespread education at
894 J. M. Rey Benayas and J. M. Bullock

various levels is necessary to promote public
awareness (Hall and Bauer-Armstrong 2010). Pro-
fessional training is necessary as well to build up
the capabilities to reconcile agricultural production
and the conservation or enhancement of biodi-
versity and other ecosystem services (Rey Benayas
and others 2010b). Farmers obviously play a key
role, and progress is required in engaging farmers
more fully with the concept and methods of land
management for purposes other than production
(Burton and others 2008).
CONCLUSIONS
We conclude that, although agriculture is a major
cause of environmental degradation, ecological
restoration on agricultural land offers opportunities
to reconcile agricultural production with
enhancement of biodiversity and ecosystem ser-
vices other than production. Restoration by land
sharing through environmental-friendly farming
has the potential to enhance agricultural produc-
tion, other ecosystem services and biodiversity at
both the farmed field and landscape scale. How-
ever, restoration by land separation would provide
these triple benefits only at the landscape scale as
this restoration type is at the expense of field-level
agricultural production. Beyond scientific and
technical research, an increase in such restoration
projects is needed if we want to halt environmental
degradation and biodiversity loss and meet the CBD
goals. We need widespread expansion of agricul-
tural management based on ecological knowledge:
biodiversity-based agricultural practices, organic
farming, agroforestry systems, learning from tradi-
tional practices, highly specific actions to benefit
wildlife and particular ecosystem services, and
conversion of some agricultural land into natural
ecosystems such as forests. Financial support,
public awareness, education and training, particu-
larly of farmers, are necessary to accomplish such
objectives. Restoration actions can act as an engine
of economy and a source of green employment, so
policymakers have an extra incentive to restore
degraded farmland habitat.
ACKNOWLEDGMENTS
Projects from the Spanish Ministry of Science and
Education (CGL2010-18312), the Government of
Madrid (S2009AMB-1783, REMEDINAL-2), and
the UK RELU FarmCAT project (RES-227-25-0010)
are currently providing financial support for this
body of research. We are indebted to Liliana Tovar
for her input with table and figure building. Two
anonymous reviewers and Ann Kinzig provided
valuable comments to previous versions of this
article.
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