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Title
Ecological intensification to mitigate impacts of conventional intensive land use on
pollinators and pollination.
Permalink
https://escholarship.org/uc/item/0794p97x
Journal
Ecology letters, 20(5)
ISSN
1461-023X
Authors
Kovács-Hostyánszki, Anikó
Espíndola, Anahí
Vanbergen, Adam J
et al.
Publication Date
2017-05-01
DOI
10.1111/ele.12762
Peer reviewed
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University of California
REVIEW AND
SYNTHESIS
Ecological intensification to mitigate impacts of conventional
intensive land use on pollinators and pollination
Anik
oKov
acs-Hosty
anszki,
1,2*,†
Anah
ı Esp
ındola,
3,†
Adam J.
Vanbergen,
4
Josef Settele,
5,6,7
Claire Kremen
8
and Lynn V. Dicks
9
Abstract
Worldwide, human appropriation of ecosystems is disrupting plant–pollinator communities and polli-
nation function through habitat conversion and landscape homogenisation. Conversion to agriculture
is destroying and degrading semi-natural ecosystems while conventional land-use intensification (e.g.
industrial management of large-scale monocultures with high chemical inputs) homogenises land-
scape structure and quality. Together, these anthropogenic processes reduce the connectivity of popu-
lations and erode floral and nesting resources to undermine pollinator abundance and diversity, and
ultimately pollination services. Ecological intensification of agriculture represents a strategic alterna-
tive to ameliorate these drivers of pollinator decline while supporting sustainable food production, by
promoting biodiversity beneficial to agricultural production through management practices such as
intercropping, crop rotations, farm-level diversification and reduced agrochemical use. We critically
evaluate its potential to address and reverse the land use and management trends currently degrading
pollinator communities and potentially causing widespread pollination deficits. We find that many of
the practices that constitute ecological intensification can contribute to mitigating the drivers of polli-
nator decline. Our findings support ecological intensification as a solution to pollinator declines, and
we discuss ways to promote it in agricultural policy and practice.
Keywords
Crop production, diversification, food security, grazing/mowing intensity, habitat loss, landscape
fragmentation, mass-flowering crops, wild pollinator diversity.
Ecology Letters (2017) 20: 673–689
INTRODUCTION
The interrelated growth in the global human population, eco-
nomic wealth, globalised trade and technological develop-
ments produces environmental pressures that alter pollinator
biodiversity and pollination. The multiple threats to pollina-
tors and plant pollination have been reviewed in detail else-
where (Gonz
alez-Varo et al. 2013; Vanbergen et al. 2013;
Potts et al. 2016a). Recently, the Intergovernmental Science-
Policy Platform for Biodiversity and Ecosystem Services
(IPBES) published its ‘Assessment Report on Pollinators, Pol-
lination and Food Production’ (IPBES 2016). This IPBES
report globally assessed the status of and threats to pollina-
tors and pollination. It also provided a strategic overview of
opportunities to mitigate these threats, thereby safeguarding
pollinators and pollination for the future. The IPBES
pollinators report clearly identified agriculture as both a
threat to pollinators and a potential solution to support them.
It also recognised three key complementary policy options for
safeguarding pollinators in agricultural ecosystems: adopting
ecological intensification, strengthening existing diversified
farming systems and building ecological infrastructure. The
IPBES report suggested that ‘ecological intensification’ (Bom-
marco et al. 2013; Tittonell 2014) is a key mitigation strategy,
and claimed it could transform agriculture to support pollina-
tors, pollination services and food production. Its emphasis
on managing beneficial biodiversity to maintain or enhance
agricultural productivity is particularly appropriate in the con-
text of global policy objectives to achieve greater food security
in a changing world (Dicks et al. 2016a; IPBES 2016). Here,
we examine the IPBES report’s claim in detail, critically evalu-
ating the potential of ecological intensification to mitigate the
1
MTA Centre for Ecological Research, Institute of Ecology and Botany,
Lend
€
ulet Ecosystem Services Research Group, Alkotm
any u. 2-4., 2163
V
acr
at
ot, Hungary
2
MTA Centre for Ecological Research, GINOP Sustainable Ecosystems Group,
Klebelsberg Kuno u. 3., 8237 Tihany, Hungary
3
Department of Biological Sciences, Life Sciences South 252, University of
Idaho, Moscow, ID 83844-3051, USA
4
NERC Centre for Ecology & Hydrology, Bush Estate, Penicuik, Edinburgh
EH26 0QB, UK
5
UFZ - Helmholtz Centre for Environmental Research, Dept. of Community
Ecology, Theodor-Lieser-Str. 4, 06120 Halle, Germany
6
iDiv, German Centre for Integrative Biodiversity Research, Halle-Jena-Leipzig,
Deutscher Platz 5e, 04103 Leipzig, Germany
7
Institute of Biological Sciences, College of Arts and Sciences, University of
the Philippines Los Banos, College, Laguna 4031, Philippines
8
University of California, 217 Wellman Hall Berkeley, California 94720-3114
CA, USA
9
School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ,
UK
*Correspondence: E-mail: kovacs.aniko@okologia.mta.hu
†
The authors equally contributed to this paper
© 2017 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.
Ecology Letters, (2017) 20: 673–689 doi: 10.1111/ele.12762
negative effects of conventional agricultural intensification (in-
dustrial management of large-scale monocultures with high
chemical inputs) on pollinators and pollination, at landscape
(land use) and local (land management) scales.
Human land use is the main current driver of changes in
land cover (Foley et al. 2005) on approximately 53% of the
Earth’s terrestrial surface (Klein Goldewijk et al., 2004;
Hooke & Mart
ın-Duque 2012). Globally, since the early
1960s, croplands have expanded with a consequent reduction
in forests and grasslands (Klein Goldewijk et al., 2004; FAO
2016). By 2030, the area of agricultural land is expected to
increase a further 10%, mainly in the developing world
(Haines-Young 2009). These human-induced changes in land
use shift the composition (e.g. habitat loss) and spatial config-
uration (e.g. fragmentation, isolation) of land-cover types
(Fahrig et al. 2011). Declines in wild bees and butterflies are
linked to historical landscape modification (Burkle et al. 2013;
Bommarco et al. 2014; Senapathi et al. 2015) and loss of nest-
ing and foraging sites or key floral resources (Goulson et al.
2005; Biesmeijer et al. 2006; Potts et al. 2010; Scheper et al.
2014; Baude et al. 2016). Increasing habitat loss and degrada-
tion has also lowered fruit set of insect-pollinated crops (Klein
et al. 2002, 2012) and wild plants (Aguilar et al. 2006; Bat
ary
et al. 2013; Clough et al. 2014) by eroding pollinator density
or diversity. Land-use changes can also fragment habitats,
affecting both the size and connectivity of remnant habitat
patches (Hadley & Betts 2012; Hooke & Mart
ın-Duque 2012).
This can potentially reduce pollinator gene flow, with implica-
tions for long-term population persistence (Darvill et al.
2010), and can adversely affect sexual reproduction of wild
plants, particularly of species with an obligate dependence on
pollinators (Aguilar et al. 2006).
Farm management directly affects the availability and qual-
ity of foraging and nesting resources for pollinators within
agricultural fields (Requier et al. 2015). Since the 1960s, mod-
ern agriculture has rapidly intensified, and the dominant agri-
culture in many parts of the world now uses large amounts of
chemical fertilisers, pesticides, irrigation and other technolo-
gies (Tilman et al. 2001, 2002). Compared with traditional,
low-input farming systems, conventional ‘monocultures’, dom-
inated by one or a few crops, simplify the agroecosystem and
decrease pollinator foraging resources (Kremen & Miles
2012).
Despite technological and agronomic improvements, the
benefits of conventional agricultural intensification are limited
by the available pollination services, at least in pollinator-
dependent crops for which pollination deficits are widely
observed (Deguines et al. 2014; Garibaldi et al. 2015, 2016b).
In recent decades, farming systems and techniques have been
developed to mitigate the negative impacts of intensified agri-
culture on agricultural ecosystems, for example by sustainable
intensification, organic farming and agri-environment schemes
(Morandin & Winston 2005; Andersson et al. 2012; Bat
ary
et al. 2015). Sustainable intensification originally attempted to
increase crop yield while improving ecological and social con-
ditions by the establishment of low-input ‘resource-conserving
systems’, but recently shifted towards capital and external
input intensive solutions to enhance resource-use efficiencies
(Loos et al. 2014; Garibaldi et al. 2016a). Organic farming
originated to enhance soil fertility, water storage and the bio-
logical control of crop pests and diseases. However, recently,
certified organic farming also started allowing the controlled
use of certain organic pesticides (Garibaldi et al. 2016a).
Thus, today many organic farms are high-input large-scale
operations supporting low biological diversity (Garibaldi et al.
2016a). Nevertheless, although the effects of organic farming
and other agri-environment schemes (see also below) on biodi-
versity – including pollinators – have been mixed, they have
been generally positive (Scheper et al. 2013; Bat
ary et al.
2015). Compared to these techniques, ecological intensification
describes a process fitting the original concept of sustainable
intensification, and aims to support agricultural production
through the enhancement of ecosystem services. Its goal is to
reduce reliance on anthropogenic chemical inputs in farms, a
characteristic it shares with diversified farming systems (cross-
scale diversification, integrating several crops and/or animals
in the production system to generate and regenerate ecosystem
services) (Kremen & Miles 2012; Bommarco et al. 2013; Gari-
baldi et al. 2016a).
In this paper, we outline the concept of ecological intensifi-
cation and the ecosystem and agricultural benefits arising
from its application. Then – drawing on the findings of the
recent IPBES assessment (IPBES 2016) – we consider how
land use and land management drivers affect pollinators and
pollination. For each set of drivers, we consider whether prac-
tices that constitute ecological intensification would reduce or
reverse their effects on pollinators and pollination, if widely
implemented by farmers. Finally, we discuss the viability and
policy implications of ecological intensification as an inte-
grated solution sustaining pollinator communities, pollinator-
dependent crop production and wild plant reproduction.
WHAT IS ‘ECOLOGICAL INTENSIFICATION’?
Ecological intensification, as defined by Bommarco et al.
(2013) and Tittonell (2014), involves actively managing farm-
land to increase the intensity of the ecological processes that
support production, such as biotic pest regulation, nutrient
cycling and pollination. It means making smart use of nat-
ure’s functions and services, at field and landscape scales, to
enhance agricultural productivity, and reduce reliance on
agrochemicals and the need for further land-use conversion.
We identify specific actions that farmers or land managers
may take to achieve ecological intensification (Table 1),
including actions focused on enhancing pollination or pest
regulation services delivered by mobile agents. Table 1 also
summarises the ecosystem services such actions are expected
to enhance (adapted from Kremen & Miles 2012), and the
potential for mitigating various drivers of change in pollina-
tors and pollination.
Some of the ecological intensification actions identified in
Table 1 match existing agri-environment scheme options or
general agricultural conservation measures, such as creating
flower-rich field margins, or managing hedgerows and verges
to improve habitat quality. However, the key difference from
these other, more biodiversity-focused approaches is that
under ecological intensification these actions would be
designed and located to support targeted delivery of
© 2017 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd.
674 A. Kov
acs-Hosty
anszki et al. Review and Synthesis
Table 1 Key practices in Ecological Intensification, the ecosystem services they are expected to support (adapted from Kremen & Miles 2012) and how they
relate to the main land use and land management drivers of pollinator decline identified by the IPBES pollinators report (IPBES 2016)
Practice Ecosystem services
Landscape
complexity
Landscape
connectivity
Nesting
resources
Foraging
resources
Insecticides
and herbicides
Using compost or manure Soil quality
Nutrient management
Water-holding capacity
Disease control
Energy-use efficiency
Resilience
Yield
Intercropping Soil quality
Weed control
Disease control
Pest control
Pollination
Energy-use efficiency
Resilience
Yield
+ (+) ++
Agroforestry Soil quality
Water-holding capacity
Weed control
Disease control
Pest control
Pollination
Energy-use efficiency
Resilience
Yield
+ (+) ++
Targeted flower strips Pest control
Pollination
Energy-use efficiency
Yield
(+)(+) + ()
Reduced or no-till Soil quality
Water-holding capacity
Resilience
Yield
+ (+)
Crop rotation Soil quality
Nutrient management
Weed control
Disease control
Pest control
Pollination
Energy-use efficiency
Resilience
Yield
+ (+)(+)
Cover crop or green manure Soil quality
Nutrient management
Water-holding capacity
Weed control
Disease control
Pest control
Pollination
Energy-use efficiency
Resilience
Yield
++
Fallow Soil quality
Water-holding capacity
Pest control
Pollination
Resilience
Yield
++++
Border planting (for
example, hedgerows and
wind breaks)
Nutrient management
Pest control
Pollination
Energy-use efficiency
Resilience
++++ +
(continued)
© 2017 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd.
Review and Synthesis Ecological intensification and pollination 675
ecosystem services. For example, placing flower strips can
enhance direct spill-over of pollination and/or pest regulation
services to specific crops in the locality, with their constituent
flowering plant species designed to attract and reward specific
types of insect (Blaauw & Isaacs 2014a; Tschumi et al. 2015;
Westphal et al. 2015).
LAND USE, LAND MANAGEMENT AND ECOLOGICAL
INTENSIFICATION
The IPBES pollination report (IPBES 2016) assessed the risks
and opportunities for pollinators and pollination from land
use and land management, amongst other drivers. An expert
author and reviewer team of over 70 scientists (including all
authors of this paper) critically evaluated the scientific litera-
ture, together with evidence provided by indigenous and local
knowledge holders, representing all regions of the world. This
assessment was peer-reviewed in an open, two-stage process
by both scientists and governments. It therefore represents a
thorough examination of existing global knowledge about pol-
linators and pollination up to 2016. In this paper, we build on
the IPBES report to synthesise the risks to pollinators and
pollination at the scales of land use (leading to reduced land-
scape complexity and connectivity) and land management
(leading to reduced nesting and foraging resources within the
field). For the latter, we consider arable and grassland systems
separately, as the drivers of pollinator decline differ between
these habitat types. We also consider agricultural pesticides
(insecticides and herbicides) separately because of their high
scientific and policy profile as a driver of change in pollina-
tors. For each driver, we assess whether ecological intensifica-
tion as defined above can ameliorate adverse effects on
pollinators and pollination.
LANDSCAPE COMPLEXITY AND CONNECTIVITY
Habitat loss and degradation of habitat quality can reduce
the population sizes, composition and species richness of polli-
nator communities (Steffan-Dewenter & Westphal 2008;
Kennedy et al. 2013; Ferreira et al. 2015; Nem
esio et al. 2016)
and alter the structure of plant–pollinator networks (Burkle
et al. 2013; Moreira et al. 2015), with implications for com-
munity stability and pollination processes. Specialised pollina-
tor species adapted to particular plant species, or requiring
very specific nesting resources (e.g. long-tongued bumble bees,
Bombus spp.) tend to be more vulnerable to land-cover
changes than more generalised species (Goulson et al. 2008;
€
Ockinger et al. 2010; Weiner et al. 2014; Persson et al. 2015).
Similarly, above-ground nesters seem more sensitive to habitat
loss or fragmentation than below-ground nesters (Williams
et al. 2010; Ferreira et al. 2015; Persson et al. 2015). Due to
different dispersal abilities, different pollinator groups can
also show various responses to configurational changes (Red-
head et al. 2016). For instance, small-bodied pollinators and
solitary bees are, owing to their lower dispersal ranges, more
vulnerable to effects of habitat fragmentation than larger bod-
ied and social pollinators (Ricketts et al. 2008; Bommarco
et al. 2010; Williams et al. 2010; Winfree et al. 2011). Taken
Table 1. (continued)
Practice Ecosystem services
Landscape
complexity
Landscape
connectivity
Nesting
resources
Foraging
resources
Insecticides
and herbicides
Riparian buffers Soil quality
Nutrient management
Pest control
Pollination
Energy-use efficiency
Resilience
+++(+) +
Patches of semi-natural
zones (woodland, wetland)
Soil quality
Nutrient management
Pest control
Pollination
Resilience
++++ +
Select crop varieties to
enhance recruitment of
pollinators or natural
enemies
Pollination
Pest control
+ ()
Strategies to reduce pesticide
use or exposure of
non-target organisms to
pesticides
Pollination
Pest control
+
Provide dedicated nesting or
overwintering resources for
pollinators or natural
enemies
Pollination
Pest control
(+) +
Based on the review here ‘+’ = the driver is reduced or mitigated by this action; ‘(+)’ = the driver may be reduced by this action in some circumstances;
‘’ = the driver is enhanced or added to by this action; ‘()’ = the driver may be enhanced or added to by this action in some circumstances. Blank cells
imply the driver is not affected by the action.
© 2017 The Authors. Ecology Letters published by CNRS and John Wiley & Sons Ltd.
676 A. Kov
acs-Hosty
anszki et al. Review and Synthesis