A dual role for farmlands: food security and 
pollinator conservation
Authors: Laura A. Burkle, Casey M. Delphia, and 
Kevin M. O'Neill
This is the peer reviewed version of the following article: [Burkle, Laura A. , Casey M. Delphia, 
and Kevin M. O'Neill. "A dual role for farmlands: food security and pollinator conservation." 
Journal of Ecology 105, no. 4 (July 2017): 890-899.], which has been published in final form at 
https://dx.doi.org/10.1111/1365-2745.12784. This article may be used for non-commercial 
purposes in accordance with Wiley Terms and Conditions for Self-Archiving.
Burkle, Laura A. , Casey M. Delphia, and Kevin M. O\'Neill. "A dual role for farmlands: food 
security and pollinator conservation." Journal of Ecology 105, no. 4 (July 2017): 890-899. DOI: 
10.1111/1365-2745.12784.
Made available through Montana State University’s ScholarWorks 
scholarworks.montana.edu 
A dual role for farmlands: food security and pollinator 
conservation
Laura A. Burkle*,1 , Casey M. Delphia1,2 and Kevin M. O’Neill2
1Department of Ecology, Montana State University, Bozeman, MT 59717, USA; and 2Department of Land Resources
and Environmental Sciences, Montana State University, Bozeman, MT 59717, USA
Summary
1. We briefly review current understanding of wild pollinators and pollination services on farmlands.
2. We consider how concepts in plant ecology – community assembly and functional trait diversity
– may be applied to create diverse, wild pollinator communities across scales in agroecosystems.
3. We also make recommendations for best practices to enhance pollination services and create
more sustainable food production systems under changing environmental conditions, including creat-
ing greater landscape connectivity, embracing pollinator dynamics, and providing incentives and
other motivations to support these practices.
4. Synthesis. We highlight the opportunity for agricultural lands to serve a dual role for both food
production and pollinator conservation, and conclude by posing unanswered questions and top prior-
ities for future studies.
Key-words: agroecosystems, bees, floral resources, native plants, nesting habitat, sustainability,
wild pollinators
Introduction
Wild pollinators provide essential ecosystem services to crops
(Klein et al. 2007) in agricultural landscapes. Although pri-
marily honeybees (Apis mellifera) are relied upon for crop
pollination, their recent increases in mortality highlight the
importance of wild pollinators (e.g. Allen-Wardell et al.
1998; Potts et al. 2010). Furthermore, agricultural reliance on
one managed species (i.e. the honeybee) with a prevalence of
known pathogens is risky, especially when wild bees are
often superior pollinators (Garibaldi et al. 2011, 2013).
Alone, wild bees can sufficiently pollinate certain crops (Kre-
men, Williams & Thorp 2002; Winfree et al. 2007), and their
diversity is a positive predictor of the magnitude and temporal
stability of pollination even when honeybees are also present
(Kremen, Williams & Thorp 2002; Klein 2009; Garibaldi
et al. 2011). Despite global declines in honeybee health (Potts
et al. 2010; Wilfert et al. 2016), when many colonies are
stocked locally, honeybees can usurp floral resources critical
to wild pollinators, reducing their fitness (Elbgami et al.
2014) and potentially lowering their abundance and diversity
(Cane & Tepedino 2016).
Local farm management practices (e.g. organic farming,
on-farm habitat heterogeneity; Benton, Vickery & Wilson
2003) as well as the quality and structure of the surrounding
landscape are important to the abundance and richness of wild
pollinators on farms (Kremen, Williams & Thorp 2002;
Kremen et al. 2007). Wild pollinators require floral resources
and nesting habitat that are frequently limited in agricultural
landscapes, and are often provided by adjacent or integrated
natural and semi-natural areas (Westrich 1996; Williams &
Kremen 2007). Visitation rates, richness and population sta-
bility of wild pollinators decline with increasing distance from
these habitats (Ricketts et al. 2008; Garibaldi et al. 2011), but
landscape configuration has not been shown to have strong
effects (Kennedy et al. 2013). In truly isolated agroecosys-
tems (i.e. organic farm ‘islands’ surrounded by species-poor
conventional farms), farm management practices are not able
to rescue pollinator communities or pollination services
(Brittain et al. 2010).
Given these issues, as well as other known contributors to
pollinator declines (Goulson et al. 2015), implementing man-
agement practices that increase pollinator populations and
enhance diverse community membership in agroecosystems is
paramount to maintain and ensure food security. In this
review, we (i) consider how basic concepts in plant ecology –
community assembly and functional trait diversity – can be
applied to create agricultural landscapes that support dynamic
wild pollinator communities and (ii) explore the opportunity
for agricultural lands to serve a dual role in both food*Correspondence author. E-mail: laura.burkle@montana.edu
production and pollinator conservation. Throughout, we high-
light the types of conservation goals most compatible with
feasible practices in agroecosystems and raise caveats con-
cerning circumstances in which this dual role is less likely to
succeed.
Shifting towards greater incorporation of non-managed pol-
linators in agroecosystems provides an exciting opportunity to
encourage wild pollinator conservation and restoration glob-
ally. Long-term pollinator conservation (i.e. pollinator produc-
tion) need not be seen as a goal competing with food
production. Investments in wild pollinator resources could
benefit food producers, reduce our dependence on managed
bees, and make more efficient use of available funds (Kre-
men, Williams & Thorp 2002; Blaauw & Isaacs 2014). We
develop these ideas in the context of fundamental concepts in
plant ecology, including community assembly and functional
trait diversity, which are useful frameworks for considering
the scales at which different factors restrict – or could be
manipulated to enhance – recruitment and success of diverse
pollinator communities (Fig. 1), especially with changing
environmental conditions. While the ecological understanding
of community assembly is derived mainly from research of
plant communities (reviewed in G€otzenberger et al. 2012), we
apply a similar framework to pollinators here. By combining
consideration of both community assembly and functional
trait variation, we can ‘build up’ plant assemblages such that
they contain suites of traits that will support existing, local
pollinator communities while also incorporating the functional
trait redundancy necessary to buffer against natural commu-
nity dynamics (Fig. 1). We highlight how the application of
these concepts in plant ecology can assist with food security
by supporting pollinators and pollination services in agroe-
cosystems. For our recommendations to have future longevity,
we also consider best practices in the context of global
climate change.
Consideration of community assembly and
disassembly processes
Community assembly and disassembly describe the processes
of species addition or loss, respectively, operating at differ-
ent spatiotemporal scales to form local, interacting communi-
ties (e.g. Ostfeld & LoGiudice 2003; HilleRisLambers et al.
2012). We can apply these concepts to agroecosystems to
better understand existing plant–pollinator communities as
well as manage for biodiversity conservation and sustained
pollination services. At the landscape level, agricultural
intensification has replaced once continuous, heterogeneous,
native habitat with large, often isolated, monocultures (Saun-
ders, Hobbs & Margules 1991; DeFries, Foley & Asner
2004). This reduction in and homogenization of floral diver-
sity is often accompanied by intensive pest management
practices and creates highly disturbed environments, which
can hinder the success of and disassemble resident pollinator
communities (Kevan 1999; Kremen, Williams & Thorp
2002). The resulting on-farm wild pollinator communities
are those that remain (i.e. are environmentally filtered;
HilleRisLambers et al. 2012) or have naturally recruited
since conversion to agriculture (Fig. 1). Thus, unless they
bring in honeybees or other managed bees, growers cur-
rently have little direct control over the pollinator communi-
ties in agroecosystems.
While plant community assembly in agroecosystems is
rapid (i.e. we grow the desired floral species), the speed of
pollinator community assembly is poorly understood. Pollina-
tor assembly may be slow because ample time may be needed
for pollinators to colonize from the surrounding fragmented
landscape (Aizen & Feinsinger 1994; Dorchin et al. 2013).
Alternatively, if there are flowers and other resources avail-
able in the landscape, dispersal may not be limiting and
expansion could be rapid (Lopez-Uribe et al. 2016). Both sce-
narios emphasize the potential importance of corridors or
‘stepping stones’ of floral resources and nesting habitat at the
landscape scale. There is evidence, however, that pollinators
respond consistently to the availability of floral resources after
land-use change (Winfree, Bartomeus & Cariveau 2011),
highlighting the applicability of the ‘if you build it, they will
come’ adage. On-farm management practices can therefore
help to enhance resident pollinator communities and to recruit
new, sustainable pollinator populations from surrounding nat-
ural areas. However, the degree to which these practices pro-
vide resources necessary for viable pollinator communities
(e.g. floral and nesting resources) is poorly understood
(Sardi~nas, Ponisio & Kremen 2016).
Consideration of functional trait diversity of
plants and pollinators
A main challenge facing ecologists is a better understanding
of how climate change is affecting ecological interactions
among species so that we may maintain the essential services
they provide, like pollination. To better understand mecha-
nisms by which shifts in species interactions could occur,
ecologists can quantify traits potentially involved in mediating
these interactions and examine community-wide patterns of
functional trait diversity (Diaz, Noy-Meir & Cabido 2001;
Suding et al. 2005; Sandel et al. 2010; Mouillot et al. 2013).
In particular, the originality and uniqueness of a species’ traits
relative to others in the community define its functional role
and contribution to functional diversity (Laliberte & Legendre
2010). Functional diversity often predicts ecosystem processes
more accurately than species richness (Reiss et al. 2009;
Gagic et al. 2015). Importantly for the conservation of biodi-
versity and ecosystem function, a functional trait approach
allows the ability to quantify the degree to which interactions
or ecosystem services may be maintained even if species
composition changes (Dı́az & Cabido 2001; Elmqvist et al.
2003; Laliberte et al. 2010). While functional trait approaches
have had great success in community (Weiher et al. 2011;
Spasojevic & Suding 2012) and restoration ecology (Funk
et al. 2008; Wainwright, Wolkovich & Cleland 2012; Laugh-
lin 2014), such approaches are just beginning to fully incor-
porate more than one trophic level (Sargent & Ackerly 2008;
Coux et al. 2016) and will likely provide valuable insight to
how functional diversity contributes to patterns of species
interactions across trophic levels – including plant–pollinator
interactions – and after environmental changes.
Plant species often differ in their responses to environmental
changes (e.g. Walther et al. 2002), and, taken individually,
these studies can indicate an overwhelming array of species-
specific effects with little predictive power. Perhaps even more
discouraging for the synthesis of these idiosyncratic results is
that the magnitude and direction of responses to environmental
context can be variable among plant traits being investigated.
Therefore, a functional trait approach may provide a useful per-
spective for a more immediate understanding of the effects of
environmental change on plant–pollinator interactions, via
shifts in plant traits (e.g. McGill et al. 2006).
Variation in the traits of individuals and species can
influence plant–pollinator interactions (Junker, Bl€uthgen &
Keller 2015) as well as pollinator fitness (Roulston & Cane
2002; O’Neill et al. 2011). Because farm management prac-
tices influence plant and pollinator diversity and composi-
tion, especially in intensely managed agroecosystems, these
practices also influence trait distributions (Bengtsson, Ahn-
str€om & Weibull 2005; Grass et al. 2016). By investigating
which traits of species and functional groups are most
likely to be affected (positively or negatively) by environ-
mental change and management practices in agroecosys-
tems, we can provide a framework for understanding
responses of biodiversity to these conditions. In addition,
we can extend this perspective to proactively build and
maintain agroecosystems that will be more robust to future
changes and to maintain pollination services and food
security.
PLANTS
Growers typically have a high degree of control over on-farm
plant communities, including crops themselves, weeds and
non-crop plants grown to assist beneficial organisms, like polli-
nators. Plant species can be specifically added – or ‘assembled’
– to each system to complement the utility of existing suites of
plants for pollinator forage. Selection of which non-crop spe-
cies to grow for pollinator conservation typically considers
plant traits that are important for pollinators (e.g. Tuell et al.
2008; Feltham et al. 2015; Williams et al. 2015), including
flower phenology and abundance, nectar and pollen resources,
floral morphology and petal colour, plant architecture and
perenniality (or reseeding ability), as well as those important to
farmers including ease and cost of plant propagation, plant or
seed availability, and native status (i.e. zero to low risk of inva-
sion and locally adapted to climate; Isaacs et al. 2009). Flower-
ing plants with multifunctional roles, including harvestable
commodities (e.g. sunflowers; Todd, Gardiner & Lindquist
2016), nesting substrates and materials for bees (Mader et al.
2011), services like windbreaks (Vaughn & Black 2006), and
flowering cover crops that enhance soil nitrogen (e.g. Ellis &
Barbercheck 2015) may also be used.
Selecting a suite of flower species that cover a range of
complementary traits can provide diverse pollinator communi-
ties with ample floral resources throughout the growing
Region
Agroecosystem
Farm
Field
Regional species pool of 
pollinators
Dispersal and chance
Abioc environmental filter
• Disturbance (e.g., land use, 
pescides)
• Nesng resources
Bioc interacons
• Floral resources
• Pathogens, parasites, etc.
Higher funconal trait variaon
Spaal scale Factors influencing 
pollinator communies
Plot
Fewer pollinators 
supported & lower 
redundancy 
More pollinators supported &
higher redundancy 
Flower addionNo flower addion
Lower funconal trait variaon
Fig. 1. The composition of pollinators in on-farm communities results from a series of abiotic and biotic filters, which may not be mutually
exclusive (e.g. ‘nesting resources’ may involve biotic and abiotic components). The influence of these factors on pollinator communities varies
with spatial scale. Past disturbances may have ‘disassembled’ these communities, and current communities may be a subset of this original com-
munity. Current communities may also reflect some re-assembly or novel assemblages. We can begin to assist this process of re-assembly of
diverse and highly functional communities (i.e. potential for stability of pollination services) by manipulating, in particular, floral and nesting
resources on farmlands. Because growers and managers have strong control over floral resources in agroecosystems, we illustrate examples of
potential plant–pollinator interaction networks resulting from two scenarios: with and without the addition of wildflower plantings. By taking into
account the functional trait variation of flowers being added, complementary suites of plants can be chosen to support diverse pollinator commu-
nities. Within the plant–pollinator networks, lowercase letters (a–g) and uppercase letters (H–Q) represent plant and pollinator species, respec-
tively, and the width of the black bars indicates the relative number of interactions in which that species participates. [Colour figure can be
viewed at wileyonlinelibrary.com]
season (Russo et al. 2013). A diversity-minded selection
approach can be used without advance knowledge of the
composition of the resident pollinator community or the local
pool of pollinator species that may be drawn in to the flower
plantings. Given the asymmetric and nested structure of most
plant-pollinator networks (Bascompte et al. 2003; Vazquez
et al. 2009), it seems likely that a collection of well-selected
plant species can together provide the bulk of floral resources
necessary to support the survival and reproduction of a local
pollinator community, though this has not been explicitly
tested. To establish and maintain diverse pollination systems
across the globe that are robust to environmental changes,
efforts should be made to utilize suites of native plants that
support both common, abundant pollinators (e.g. Carvell
et al. 2006; Grass et al. 2016; Todd, Gardiner & Lindquist
2016), as well as those that are less common or more special-
ized (Russo et al. 2013). However, this approach has its limi-
tations for pollinator conservation in that plant selection can
only include those species able to thrive in agricultural set-
tings, which include full sun and low water availability. For
example, in the northeastern United States (U.S.), one of the
most threatened genera is Macropis, oil-collecting bees which
can only thrive where their host plant, Lysimachia, is avail-
able (Bartomeus et al. 2013a). Maintaining this pollinator and
its plant association is not likely to be feasible specifically as
part of an agroecosystem management scheme because Lysi-
machia require moist soil conditions (i.e. wetlands, swamps
and lake margins) for growth. Thus, pollinators that need the
most specialized conservation efforts may be less likely to be
able to be supported by management compatible with agroe-
cosystems (but see Carvell et al. 2006; M’Gonigle et al.
2015).
POLL INATORS
In addition to the floral resources provided by complementary
suites of plant species, wild pollinator communities also
require a diversity of species-specific nesting substrates and
materials to survive and reproduce. For example, many soli-
tary bee species nest above-ground in tunnels left by wood-
boring beetles, in hollow plant stems, or in pithy twigs that
the bees excavate. They also require specific nest-building
materials, including leaves, pebbles, mud and tree resin, to
construct their nests (Krombein 1967; Michener 2007). While
there has been success creating artificial nesting habitat for
commercial management of some native cavity-nesting bees
in agricultural systems (e.g. Osmia lignaria; Bosch & Kemp
2002), as well as for research studies (e.g. Gathmann, Greiler
& Tscharntke 1994; Tscharntke, Gathmann & Steffan-Dewen-
ter 1998; Williams & Kremen 2007; Burkle & Irwin 2009a;
O’Neill & O’Neill 2010; MacIvor 2016), little is known about
the conditions required by ground-nesting bees and other wild
pollinators (Roulston & Goodell 2011). The relatively short
foraging and dispersal distances of many pollinator species
require that, along with food resources, nesting resources be
available within a localized area (Westrich 1996; Gathmann
& Tscharntke 2002; Zurbuchen et al. 2010). Because certain
nesting habitats may benefit some species, but not others, it is
likely that a combination of nesting habitats is needed to sus-
tain a diverse and abundant pollinator community.
Although bees are considered overall to be the most impor-
tant pollinators (Free 1993; Michener 2007), we should also
consider the contributions of non-bee floral visitors (e.g. flies,
butterflies and beetles) to pollination services (Orford,
Vaughan & Memmott 2015; Grass et al. 2016; Rader et al.
2016). Non-bee pollinators may be active at times of the day
or under weather conditions when bees are not visiting flow-
ers (e.g. McCall & Primack 1992; Cutler et al. 2012; Rader
et al. 2013). For certain plant species, some non-bee pollina-
tors can transfer pollen more efficiently and carry it further
than bees (Rader et al. 2009, 2011). Non-Hymenoptera polli-
nator taxa are also unconstrained by the need for nesting sub-
strate. All of these biological features are complementary to
those exhibited by bees, and could influence the relative
importance of non-bee taxa under the variable environmental
conditions (Burkle & Irwin 2009b; Grass et al. 2016) that
accompany climate change. Nevertheless, one would also
have to consider other requirements of non-bee taxa, such as
larval host–plant and prey availability (Holland et al. 2008),
which could also be positively or negatively affected by cli-
mate change.
Overall, we expect intraspecific and interspecific variation
in pollinator traits – including body size, mouthpart length,
foraging distances, phenology, diet breadth (generalization),
nesting and floral resource preferences, sociality, abundance,
weather conditions preferred for flight, floral constancy and
pollination efficiency, and susceptibility to pesticides and
pathogens – to be important for sustained pollination services
on farmlands over time. Syntheses of the effects of land-use
change on pollinators may provide insight into what pollinator
traits might be most affected by farm management practices.
For example, nesting habitat (i.e. above-ground) and sociality
are the traits most strongly associated with negative responses
of bee species to land-use change (Williams et al. 2010). If
different combinations of pollinator traits enable different
functional roles (e.g. morphological, physiological or pheno-
typic traits that influence pollination services; Coux et al.
2016) in agroecosystems, then practices that support redun-
dancy of pollinator species comprising trait combinations will
be important for consistency of pollination, especially in the
light of community dynamics and environmental change.
Best practices for integrating agriculture and
pollinator conservation in a changing
environment
Globally, agriculture is one of the leading types of land use
(40% of Earth’s land surface; Owen 2005). As such, the
opportunity exists for farmlands to contribute significantly to
the maintenance of biodiversity and habitat connectivity
(McIntyre 1994; Kearns, Inouye & Waser 1998). Farmlands
can have a dual role, not only providing food in the short-
term but also enhancing long-term sustainability and biodiver-
sity by acting as pollinator reserves.
CREATE GREATER LANDSCAPE CONNECTIV ITY
In the U.S., some of our ‘best’ lands (e.g. most productive,
topographically flat) are in agricultural cultivation, while our
wilderness areas are often topographically complex with low
primary productivity (Aycrigg et al. 2013; Belote & Aplet
2014). These differences bear significance in the light of cli-
mate change because environmentally dissimilar areas can be
connected across fairly short distances in topographically
complex landscapes, whereas much larger distances will
require bridging to link climatic gradients in flat areas (Loarie
et al. 2009). Thus, greater effort will likely be needed to cre-
ate and maintain connectivity for pollinators in agroecosys-
tems experiencing climate change. If floral and nesting
resources are provided on farmlands in support of their role
in pollinator conservation, this may automatically create
greater connectivity for pollinators, especially those moving
to track climate change in landscapes that need it most,
though pollinator dispersal is poorly understood. These habitat
enhancements could also aid wild pollinators deliberately
translocated from elsewhere, in the same manner in which
native biocontrol agents are moved about (see Unanswered
Questions, and the dangers of assisted migration). It is impor-
tant to note, however, that not only is pollinator dispersal
poorly understood but also that increasing connectivity does
not necessarily lead to positive ecological outcomes, as patho-
gens, invasive species, etc. may also use such corridors.
EMBRACE VARIABIL ITY IN POLL INATOR COMMUNIT IES
To encourage healthy pollinator communities in agroecosystems,
given uncertainty associated with environmental change, best
practices will likely include strategies that embrace the certainty
of inter-annual variability in pollinator composition and consider
diverse groups of pollinators. Although a few, abundant wild pol-
linator species can provide sufficient pollination services (for tar-
get crops; Winfree et al. 2015), efforts to support diverse
pollinator communities on farmlands are important in order to
avoid relying on one or a few wild species for most of our polli-
nation. Even when plants provide consistent floral resources, wild
pollinator communities are dynamic in time and space (Burkle &
Alarcon 2011), suggesting that variation in nest-site availability,
pathogens, predators, weather and other factors interact in com-
plex ways to affect populations. In particular, between-year fluc-
tuations in the identity of the dominant pollinator taxa are the
norm (Petanidou et al. 2008). In plant–pollinator networks from
wildland systems, there is evidence that core, generalist pollina-
tors are relatively stable in their central roles in the interaction net-
work over several years (Fang & Huang 2012), but some studies
suggest otherwise (Alarcon, Waser & Ollerton 2008; Petanidou
et al. 2008; Crone 2013). The specific causes of these dynamics
and the spatiotemporal scales of their occurrence are not known
for most species (see Unanswered Questions). Regardless of the
causes, these patterns emphasize the importance of species redun-
dancy in pollination systems (Fig. 1), especially in agroecosys-
tems where local communities of wild pollinators may be even
less diverse than in less-disturbed areas. For example, when dom-
inant bee species are strongly reduced in abundance or locally
extirpated, other diet generalists do not necessarily fill these roles
(Burkle, Marlin & Knight 2013). Thus, instead of attempting to
create conditions that stabilize pollinator populations and commu-
nities, a more sensible option accepts volatility and focuses on
supporting redundancy and nested network structure (Tylianakis
et al. 2010).
In the presence of pollinator population and community
dynamics, there are a number of mechanisms by which polli-
nation services might be stabilized across time or space.
These stabilizing mechanisms include the portfolio effect (ran-
dom and uncorrelated fluctuations in species abundances,
leading to lower volatility of diverse systems), density com-
pensation (negative co-variances in species abundances,
reducing likelihood of system-wide declines in pollinator spe-
cies), functional compensation (increase in the efficiencies of
individuals as total abundance declines or community compo-
sition changes), response diversity (differential response to
environmental variables among species) and cross-scale resili-
ence (response to the same environmental variable at different
scales by different species) (e.g. Kremen 2005). Thus far,
most of these stabilizing mechanisms have not been explicitly
tested for pollinator assemblages, especially in the context of
farmlands (see Winfree & Kremen 2009; Cariveau et al.
2013; Bartomeus et al. 2013b for exceptions).
PROVIDE INCENTIVES AND OTHER MOTIVATIONS FOR
GROWERS
Growers may consider this dual role radical and expensive,
especially if added profits from on-farm pollination services
do not directly outweigh costs of providing pollinator
resources at the start of a conservation programme. However,
the value of stable and diverse pollinator communities, along
with other ecosystem service benefits of habitat enhancement
(e.g. soil stability, pest control and nutrient cycling), could be
high, especially in long-term environmental and economic
analyses (Wratten et al. 2012). Costs and benefits in these
analyses can be very difficult to measure, and while there are
whole fields of study that deal with valuation from economic
and ecological perspectives (e.g. Cardinale et al. 2012), it is
beyond the scope of this review. Future valuation studies will
aid the progress of this field.
Incentives (e.g. government subsidies) could be offered to
support this dual role (Scheper et al. 2013), regardless of
whether the focal crops require insect pollinators for seed or
fruit set. First steps towards this goal that are flexible, afford-
able and feasible, relative to the cost of hedgerows, for exam-
ple (M’Gonigle et al. 2015; Morandin, Long & Kremen
2016), include wildflower plantings (Blaauw & Isaacs 2014)
and nesting habitat enhancement (e.g. MacIvor 2016). How-
ever, incentives – as the status quo – convey the idea that
governments must pay growers for the inconvenience of polli-
nator conservation. When incentives are reduced or removed,
previously supported practices are often abandoned (e.g. Hel-
lin & Schrader 2003). Thus, other methods to encourage prac-
tices that support pollinators may be more efficient in the
long term. For example, it may be more economically
profitable for growers to participate in pollinator conservation
practices for reasons other than pollination services (e.g. aes-
thetic, moral and social capital from product branding; Kleijn
et al. 2015). For example, to maximize their visibility to the
public, while also minimizing interference with combines and
other large machinery, wildflower plantings could be imple-
mented along roadways (sensu Hopwood 2008; Garibaldi
et al. 2014, 2017). Food product labelling may be leveraged
by producers to gain social capital as ‘pollinator stewards’
(e.g. http://www.cheerios.com/weneedthebees.aspx) and poten-
tially charge more for their product. For example, in the U.S.,
General Mills recently committed to plant 3300 acres of polli-
nator habitat on the farms from which it sources it oats,
which is not a pollinator-dependent crop. In the United King-
dom, through Conservation Grade, food products that come
from farms that have adopted a biodiversity-focused farming
protocol, including planting wildflowers for pollinators, are
branded ‘Fair to Nature’ (http://www.conservationgrade.org).
The sale of these products generates funds for the continued
support of increasing farmland biodiversity. While these alter-
native motivations are rarely considered and may not prove to
be adequate for continued investment in pollinator conserva-
tion, we raise them here to highlight real problems that need
to be overcome in order to effectively implement this envi-
sioned dual role of farmlands.
Unanswered questions and top priorities for
future studies
Despite many remaining uncertainties, there are particular unan-
swered questions that are primed for additional research on polli-
nation services critical to sustainable food production.
Interestingly, many of these research topics are applicable in
both natural and managed systems, and stem from basic gaps in
our understanding of pollinator biology and ecology. For exam-
ple, what factors limit pollinator populations in different regions
(reviewed in Roulston & Goodell 2011)? While floral resource
requirements of pollinators are more deeply understood than
other potential regulating factors like nesting resources or patho-
gens (Steffan-Dewenter & Schiele 2008; Dicks et al. 2015),
there is still much to learn about the quality of different plant spe-
cies as food resources (Fowler, Rotheray & Goulson 2016).
Addressing these topics will require grounding in ecological the-
ory, and we can draw on approaches used to address similar
questions in plant ecology to guide our investigations.
WHAT ARE THE DRIVERS AND SCALES OF POLL INATOR
DYNAMICS?
We lack a full understanding of the spatiotemporal scales at
which fluctuations in pollinator populations and communities
are most prominent. For example, when researchers in one
area observe low numbers of bumblebees across a growing
season, it would be useful to know whether all species of
bumblebees are similarly affected, how long this pattern lasts,
how widespread the decline is across landscapes, and whether
other pollinator taxa are fluctuating synchronously.
Documenting these patterns will help provide a better under-
standing of the underlying causes, including for example, the
degree to which region-wide climate conditions or local levels
of parasites and pathogens are influencing pollinator dynam-
ics. Regional and local drivers of floral abundance and com-
munity composition will undoubtedly directly or indirectly
also influence pollinator dynamics, though the contribution of
these drivers relative to others is unknown.
UNDER WHAT CONDIT IONS ARE NESTING HABITATS
MOST LIKELY TO BE LIMIT ING FOR DIFFERENT
POLL INATOR GROUPS?
The most effective and economical ways to enhance nesting
habitat for diverse pollinator assemblages is poorly under-
stood. Ideally, increasing nest-habitat availability could be
accomplished while minimizing the area of land removed
from production by targeting areas such as field edges, road-
ways, powerline cuts and topographically non-cultivatable
patches within fields (e.g. Hopwood 2008; Noordijk et al.
2009; Wojcik & Buchmann 2012; Hopwood, Black & Fleury
2015). Clearly, we should not assume that practices promot-
ing pollinator food resources also provide other potentially
limiting resources or that all bees have the same nest-site
requirements. For example, hedgerows aid species with
above-ground nesting requirements (Ponisio, M’Gonigle &
Kremen 2016), but do not enhance nesting for ground-nesting
bees (Sardi~nas, Ponisio & Kremen 2016).
IN WHAT CAPACITY DO FLORAL RESOURCES ACT AS
POLL INATOR PATHOGEN TRANSMISSION HUBS?
The degree to which certain flower species, whether natural
or cultivated, promote the harmful spread of bee pathogens in
agroecosystems is unclear. It is possible that we may be able
to use floral traits to predict which plant species and commu-
nities harbour the fewest pathogens and limit intra- and inter-
specific disease transmission (reviewed in McArt et al. 2014).
Although generalist plant species can provide floral resources
for numerous pollinators, these plant species may also play
key roles in pathogen transmission. Conversely, some plant
species offer nectar or pollen resources that may have ‘medic-
inal’ or protective value for some pollinators (Manson, Otter-
statter & Thomson 2010; Richardson et al. 2015; Spear et al.
2016). Understanding the roles of certain flower types in the
transmission of pathogens, protection from parasites and self-
medication will help avoid unintended management conse-
quences, limit exposure to pathogens and assist pollinators in
fighting pathogen infections.
WHAT IS THE UTIL ITY OF WILD POLL INATOR
‘TRANSPLANTS ’?
If dispersal strongly limits pollinator recruitment to new
patches across landscapes, especially those with few floral
and nesting resources, perhaps using techniques like trap-nests
to collect a diversity of regionally appropriate, locally adapted
bees from natural areas and translocating them to compatible
agroecosystems could be used to overcome some dispersal
limitation and speed pollinator restoration. Using trap-nests
would, of course, aid only cavity-nesting solitary bees, but
other techniques, similar to those developed to manage the
native alkali bee, Nomia melanderi (Stephen 1960), could be
tested for other ground-nesting bees. With any management
of this kind, it is essential to ensure that pollinator popula-
tions have access to other required resources, so that sustain-
able communities are established. There are also potential
drawbacks to such intervention, including spreading patho-
gens, predators and brood parasites (Xerces Society for Inver-
tebrate Conservation, National Resources Defense Council &
Defenders of Wildlife 2010; Graystock et al. 2016). Explor-
ing these possibilities will tell us whether we can truly
‘assemble’ pollinator communities in ways similar to how we
assemble plant communities, or whether resources are better
spent supporting existing pollinator communities that remain
after ‘disassembly’ associated with conversion of wildlands to
agriculture.
Conclusions
To support pollination services and food security on farm-
lands, we need to provide food and nesting resources that are
presently limiting to wild pollinators, while restricting condi-
tions for their natural enemies. We can use plant traits to
assemble appropriate communities of floral resources, but we
may be more limited in our ability to control and assemble
wild pollinator communities (Fig. 1). Coping with natural pol-
linator community dynamics necessitates supporting diversity
and depending upon numerous key species. One of the best
ways to do this is to restore and manage for healthy pollinator
communities at the landscape scale, with well-connected
metapopulations that support functional redundancy of inter-
actions and resilience to environmental changes (Tylianakis
et al. 2010). In areas dominated by large-scale commercial
agriculture, wild pollinator populations are estimated to have
experienced especially marked declines (Koh et al. 2016),
and these areas may also be particularly poorly positioned to
respond to climate change. Therefore, we advocate for wild
pollinator conservation that targets as much agricultural land
as possible for participation in this endeavour. Within this
context, there are numerous avenues for future research into
the potential dual role of farmlands in food production and
wild pollinator conservation.
Authors’ contributions
L.B. conceived the ideas and wrote the first draft; C.D. and K.O. contributed
significantly to writing and revising subsequent drafts and gave final approval
for publication.
Acknowledgements
We thank D. Gibson and R. Bardgett for the invitation to participate in this
Special Feature, and S. Durney, W. Glenny, M. Simanonok, A. Slominski, E.
Reese and W. Thompson for helpful discussion and feedback. D. Gibson, I.
Bartomeus and one anonymous reviewer provided valuable suggestions that
improved this mini-review.
Data accessibility
This paper does not use data.
References
Aizen, M.A. & Feinsinger, P. (1994) Habitat fragmentation, native insect polli-
nators, and feral honey-bees in Argentine Chaco Serrano. Ecological Appli-
cations, 4, 378–392.
Alarcon, R., Waser, N.M. & Ollerton, J. (2008) Year-to-year variation in the
topology of a plant-pollinator interaction network. Oikos, 117, 1796–1807.
Allen-Wardell, G., Bernhardt, P., Bitner, R. et al. (1998) The potential conse-
quences of pollinator declines on the conservation of biodiversity and stabil-
ity of food crop yields. Conservation Biology, 12, 8–17.
Aycrigg, J.L., Davidson, A., Svancara, L.K., Gergely, K.J., McKerrow, A. &
Scott, J.M. (2013) Representation of ecological systems within the protected
areas network of the continental United States. PLoS ONE, 8, e54689.
Bartomeus, I., Ascher, J.S., Gibbs, J., Danforth, B.N., Wagner, D.L., Hedtke,
S.M. & Winfree, R. (2013a) Historical changes in northeastern US bee polli-
nators related to shared ecological traits. Proceedings of the National Acad-
emy of Sciences of the United States of America, 110, 4656–4660.
Bartomeus, I., Park, M.G., Gibbs, J., Danforth, B.N., Lakso, A.N. & Winfree,
R. (2013b) Biodiversity ensures plant–pollinator phenological synchrony
against climate change. Ecology Letters, 16, 1331–1338.
Bascompte, J., Jordano, P., Melian, C.J. & Olesen, J.M. (2003) The nested
assembly of plant-animal mutualistic networks. Proceedings of the National
Academy of Sciences of the United States of America, 100, 9383–9387.
Belote, R.T. & Aplet, G.H. (2014) Land protection and timber harvesting along
productivity and diversity gradients in the Northern Rocky Mountains. Eco-
sphere, 5, art17.
Bengtsson, J., Ahnstr€om, J. & Weibull, A.N.N.C. (2005) The effects of organic
agriculture on biodiversity and abundance: a meta-analysis. Journal of
Applied Ecology, 42, 261–269.
Benton, T.G., Vickery, J.A. & Wilson, J.D. (2003) Farmland biodiversity: is
habitat heterogeneity the key? Trends in Ecology & Evolution, 18, 182–188.
Blaauw, B.R. & Isaacs, R. (2014) Flower plantings increase wild bee abun-
dance and the pollination services provided to a pollination-dependent crop.
Journal of Applied Ecology, 51, 890–898.
Bosch, J. & Kemp, W.P. (2002) Developing and establishing bee species as
crop pollinators: the example of Osmia spp. (Hymenoptera: Megachilidae)
and fruit trees. Bulletin of Entomological Research, 92, 3–16.
Brittain, C., Bommarco, R., Vighi, M., Settele, J. & Potts, S.G. (2010) Organic
farming in isolated landscapes does not benefit flower-visiting insects and
pollination. Biological Conservation, 143, 1860–1867.
Burkle, L.A. & Alarcon, R. (2011) The future of plant-pollinator diversity:
understanding interaction networks across time, space, and global change.
American Journal of Botany, 98, 528–538.
Burkle, L.A. & Irwin, R.E. (2009a) Nectar sugar limits larval growth of solitary
bees (Hymenoptera: Megachilidae). Environmental Entomology, 38, 1293–1300.
Burkle, L.A. & Irwin, R.E. (2009b) The importance of interannual variation
and bottom-up nitrogen enrichment for plant-pollinator networks. Oikos, 118,
1816–1829.
Burkle, L.A., Marlin, J.C. & Knight, T.M. (2013) Plant-pollinator interactions
over 120 years: loss of species, co-occurrence, and function. Science, 339,
1611–1615.
Cane, J.H. & Tepedino, V.J. (2016) Gauging the effect of honey bee pollen
collection on native bee communities. Conservation Letters, 10, 205–210.
Cardinale, B.J., Duffy, J.E., Gonzalez, A. et al. (2012) Biodiversity loss and its
impact on humanity. Nature, 486, 59–67.
Cariveau, D.P., Williams, N.M., Benjamin, F.E. & Winfree, R. (2013)
Response diversity to land use occurs but does not consistently stabilise
ecosystem services provided by native pollinators. Ecology Letters, 16, 903–
911.
Carvell, C., Roy, D.B., Smart, S.M., Pywell, R.F., Preston, C.D. & Goulson,
D. (2006) Declines in forage availability for bumblebees at a national scale.
Biological Conservation, 132, 481–489.
Coux, C., Rader, R., Bartomeus, I. & Tylianakis, J.M. (2016) Linking species
functional roles to their network roles. Ecology Letters, 19, 762–770.
Crone, E.E. (2013) Responses of Social and Solitary Bees to Pulsed Floral
Resources. The American Naturalist, 182, 465–473.
Cutler, G.C., Reeh, K.W., Sproule, J.M. & Ramanaidu, K. (2012) Berry unex-
pected: nocturnal pollination of lowbush blueberry. Canadian Journal of
Plant Science, 92, 707–711.
DeFries, R.S., Foley, J.A. & Asner, G.P. (2004) Land-use choices: balancing
human needs and ecosystem function. Frontiers in Ecology and the Environ-
ment, 2, 249–257.
Dı́az, S. & Cabido, M. (2001) Vive la difference: plant functional diversity
matters to ecosystem processes. Trends in Ecology & Evolution, 16, 646–
655.
Diaz, S., Noy-Meir, I. & Cabido, M. (2001) Can grazing response of herba-
ceous plants be predicted from simple vegetative traits? Journal of Applied
Ecology, 38, 497–508.
Dicks, L.V., Baude, M., Roberts, S.P., Phillips, J., Green, M. & Carvell, C.
(2015) How much flower-rich habitat is enough for wild pollinators?
Answering a key policy question with incomplete knowledge. Ecological
Entomology, 40, 22–35.
Dorchin, A., Filin, I., Izhaki, I. & Dafni, A. (2013) Movement patterns of soli-
tary bees in a threatened fragmented habitat. Apidologie, 44, 90–99.
Elbgami, T., Kunin, W.E., Hughes, W.O.H. & Biesmeijer, J.C. (2014) The
effect of proximity to a honeybee apiary on bumblebee colony fitness, devel-
opment, and performance. Apidologie, 45, 504–513.
Ellis, K.E. & Barbercheck, M.E. (2015) Management of overwintering cover
crops influences floral resources and visitation by native bees. Environmental
Entomology, 44, 999–1010.
Elmqvist, T., Folke, C., Nystr€om, M., Peterson, G., Bengtsson, J., Walker, B.
& Norberg, J. (2003) Response diversity, ecosystem change, and resilience.
Frontiers in Ecology and the Environment, 1, 488–494.
Fang, Q. & Huang, S.-Q. (2012) Relative stability of core groups in pollination
networks in a biodiversity hotspot over four years. PLoS ONE, 7, e32663.
Feltham, H., Park, K., Minderman, J. & Goulson, D. (2015) Experimental evi-
dence that wildflower strips increase pollinator visits to crops. Ecology and
Evolution, 5, 3523–3530.
Fowler, R.E., Rotheray, E.L. & Goulson, D. (2016) Floral abundance and
resource quality influence pollinator choice. Insect Conservation and Diver-
sity, 5, 3523–3530.
Free, J.B. (1993) Insect Pollination of Crops. Academic Press, New York, NY,
USA.
Funk, J.L., Cleland, E.E., Suding, K.N. & Zavaleta, E.S. (2008) Restoration
through reassembly: plant traits and invasion resistance. Trends in Ecology &
Evolution, 23, 695–703.
Gagic, V., Bartomeus, I., Jonsson, T. et al. (2015) Functional identity and
diversity of animals predict ecosystem functioning better than species-based
indices. Proceedings of the Royal Society of London B: Biological Sciences,
282, 20142620.
Garibaldi, L.A., Carvalheiro, L.G., Leonhardt, S.D. et al. (2014) From research
to action: enhancing crop yield through wild pollinators. Frontiers in Ecol-
ogy and the Environment, 12, 439–447.
Garibaldi, L.A., Gemmill-Herren, B., D’Annolfo, R., Graeub, B.E., Cunning-
ham, S.A. & Breeze, T.D. (2017) Farming Approaches for Greater Biodiver-
sity, Livelihoods, and Food Security. Trends in Ecology & Evolution, 32,
68–80.
Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C. et al. (2011) Stability of pol-
lination services decreases with isolation from natural areas despite honey
bee visits. Ecology Letters, 14, 1062–1072.
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R. et al. (2013) Wild pollinators
enhance fruit set of crops regardless of honey bee abundance. Science, 339,
1608–1611.
Gathmann, A., Greiler, H.-J. & Tscharntke, T. (1994) Trap-nesting bees and
wasps colonizing set-aside fields: succession and body size, management by
cutting and sowing. Oecologia, 98, 8–14.
Gathmann, A. & Tscharntke, T. (2002) Foraging ranges of solitary bees. Jour-
nal of Animal Ecology, 71, 757–764.
G€otzenberger, L., de Bello, F., Brathen, K.A. et al. (2012) Ecological assembly
rules in plant communities—approaches, patterns and prospects. Biological
Reviews, 87, 111–127.
Goulson, D., Nicholls, E., Botıas, C. & Rotheray, E.L. (2015) Bee declines dri-
ven by combined stress from parasites, pesticides, and lack of flowers.
Science, 347, 1255957.
Grass, I., Albrecht, J., Jauker, F., Diek€otter, T., Warzecha, D., Wolters, V. &
Farwig, N. (2016) Much more than bees—Wildflower plantings support
highly diverse flower-visitor communities from complex to structurally sim-
ple agricultural landscapes. Agriculture, Ecosystems & Environment, 225,
45–53.
Graystock, P., Blane, E.J., McFrederick, Q.S., Goulson, D. & Hughes, W.O.
(2016) Do managed bees drive parasite spread and emergence in wild
bees? International Journal for Parasitology: Parasites and Wildlife, 5, 64–
75.
Hellin, J. & Schrader, K. (2003) The case against direct incentives and the
search for alternative approaches to better land management in Central Amer-
ica. Agriculture, Ecosystems & Environment, 99, 61–81.
HilleRisLambers, J., Adler, P.B., Harpole, W.S., Levine, J.M. & Mayfield,
M.M. (2012) Rethinking community assembly through the lens of coexis-
tence theory. Annual Review of Ecology, Evolution, and Systematics, 43,
227–248.
Holland, J.M., Oaten, H., Southway, S. & Moreby, S. (2008) The effectiveness
of field margin enhancement for cereal aphid control by different natural
enemy guilds. Biological Control, 47, 71–76.
Hopwood, J.L. (2008) The contribution of roadside grassland restorations to
native bee conservation. Biological Conservation, 141, 2632–2640.
Hopwood, J., Black, S. & Fleury, S. (2015) Roadside Best Management Prac-
tices that Benefit Pollinators: Handbook for Supporting Pollinators through
Roadside Maintenance and Landscape Design. (No. FHWA-HEP-16-059).
U.S. Department of Transportation, Federal Highway Administration.
Isaacs, R., Tuell, J., Fiedler, A., Gardiner, M. & Landis, D. (2009) Maximizing
arthropod-mediated ecosystem services in agricultural landscapes: the role of
native plants. Frontiers in Ecology and the Environment, 7, 196–203.
Junker, R.R., Bl€uthgen, N. & Keller, A. (2015) Functional and phylogenetic
diversity of plant communities differently affect the structure of flower-visitor
interactions and reveal convergences in floral traits. Evolutionary Ecology,
29, 437–450.
Kearns, C.A., Inouye, D.W. & Waser, N.M. (1998) Endangered mutualisms:
the conservation of plant-pollinator interactions. Annual Review of Ecology
and Systematics, 29, 83–112.
Kennedy, C.M., Lonsdorf, E., Neel, M.C. et al. (2013) A global quantitative
synthesis of local and landscape effects on wild bee pollinators in agroe-
cosystems. Ecology Letters, 16, 584–599.
Kevan, P.G. (1999) Pollinators as bioindicators of the state of the environment:
species, activity and diversity. Agriculture Ecosystems & Environment, 74,
373–393.
Kleijn, D., Winfree, R., Bartomeus, I. et al. (2015) Delivery of crop pollination
services is an insufficient argument for wild pollinator conservation. Nature
Communications, 6, 7414.
Klein, A.M. (2009) Nearby rainforest promotes coffee pollination by increasing
spatio-temporal stability in bee species richness. Forest Ecology and Man-
agement, 258, 1838–1845.
Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham,
S.A., Kremen, C. & Tscharntke, T. (2007) Importance of pollinators in
changing landscapes for world crops. Proceedings of the Royal Society B-
Biological Sciences, 274, 303–313.
Koh, I., Lonsdorf, E.V., Williams, N.M., Brittain, C., Isaacs, R., Gibbs, J. &
Ricketts, T.H. (2016) Modeling the status, trends, and impacts of wild bee
abundance in the United States. Proceedings of the National Academy of
Sciences of the United States of America, 113, 140–145.
Kremen, C. (2005) Managing ecosystem services: what do we need to know
about their ecology? Ecology Letters, 8, 468–479.
Kremen, C., Williams, N.M., Aizen, M.A. et al. (2007) Pollination and other
ecosystem services produced by mobile organisms: a conceptual framework
for the effects of land-use change. Ecology Letters, 10, 299–314.
Kremen, C., Williams, N. & Thorp, R.W. (2002) Crop pollination from native
bees at risk from agricultural intensification. PNAS, 99, 16812–16816.
Krombein, K.V. (1967) Trap-nesting Wasps and Bees: Life Histories, Nests,
and Associates. Smithsonian Institutional Press, Washington, DC, USA.
Laliberte, E. & Legendre, P. (2010) A distance-based framework for measuring
functional diversity from multiple traits. Ecology, 91, 299–305.
Laliberte, E., Wells, J.A., DeClerck, F. et al. (2010) Land-use intensification
reduces functional redundancy and response diversity in plant communities.
Ecology Letters, 13, 76–86.
Laughlin, D.C. (2014) Applying trait-based models to achieve functional targets
for theory-driven ecological restoration. Ecology Letters, 17, 771–784.
Loarie, S.R., Duffy, P.B., Hamilton, H., Asner, G.P., Field, C.B. & Ackerly,
D.D. (2009) The velocity of climate change. Nature, 462, 1052–1055.
Lopez-Uribe, M.M., Cane, J.H., Minckley, R.L. & Danforth, B.N. (2016) Crop
domestication facilitated rapid geographical expansion of a specialist pollina-
tor, the squash bee Peponapis pruinosa. Proceedings of the Royal Society of
London B: Biological Sciences, 283, 20160443.
MacIvor, J.S. (2016) Cavity-nest boxes for solitary bees: a century of design
and research. Apidologie, 1–17.
Mader, E., Shepherd, M., Vaughn, M., Black, S.H. & LeBuhn, G. (2011)
Attracting Native Pollinators: Protecting North America’s Bees and Butter-
flies. Storey Publishing, North Adams, MA, USA.
Manson, J.S., Otterstatter, M.C. & Thomson, J.D. (2010) Consumption of a
nectar alkaloid reduces pathogen load in bumble bees. Oecologia, 162, 81–
89.
McArt, S.H., Koch, H., Irwin, R.E. & Adler, L.S. (2014) Arranging the bou-
quet of disease: floral traits and the transmission of plant and animal patho-
gens. Ecology Letters, 17, 624–636.
McCall, C. & Primack, R.B. (1992) Influence of flower characteristics, weather,
time of day, and season on insect visitation rates in three plant communities.
American Journal of Botany, 434–442.
McGill, B.J., Enquist, B.J., Weiher, E. & Westoby, M. (2006) Rebuilding com-
munity ecology from functional traits. Trends in Ecology & Evolution, 21,
178–185.
McIntyre, S. (1994) Integrating agricultural land-use and management for con-
servation of a native grassland flora in a variegated landscape. Pacific Con-
servation Biology, 1, 236–244.
M’Gonigle, L.K., Ponisio, L.C., Cutler, K. & Kremen, C. (2015) Habitat
restoration promotes pollinator persistence and colonization in intensively
managed agriculture. Ecological Applications, 25, 1557–1565.
Michener, C.D. (2007) The Bees of the World. Johns Hopkins University Press,
Baltimore, MD, USA.
Morandin, L.A., Long, R.F. & Kremen, C. (2016) Pest control and pollination
cost–benefit analysis of hedgerow restoration in a simplified agricultural land-
scape. Journal of Economic Entomology, 109, 1020–1027.
Mouillot, D., Graham, N.A.J., Villeger, S., Mason, N.W.H. & Bellwood, D.R.
(2013) A functional approach reveals community responses to disturbances.
Trends in Ecology and Evolution, 28, 167–177.
Noordijk, J., Delille, K., Schaffers, A.P. & Sỳkora, K.V. (2009) Optimizing
grassland management for flower-visiting insects in roadside verges. Biologi-
cal Conservation, 142, 2097–2103.
O’Neill, K.M. & O’Neill, J.F. (2010) Cavity-nesting wasps and bees of Central
New York state: the Montezuma wetlands complex. Northeastern Naturalist,
17, 455–472.
O’Neill, K.M., O’Neill, R.P., Kemp, W.P. & Delphia, C.M. (2011) Effect of
temperature on post-wintering development and total lipid content of alfalfa
leafcutting bees. Environmental Entomology, 40, 917–930.
Orford, K.A., Vaughan, I.P. & Memmott, J. (2015) The forgotten flies: the
importance of non-syrphid Diptera as pollinators. Proceedings of the Royal
Society of London B: Biological Sciences, 282, 20142934.
Ostfeld, R.S. & LoGiudice, K. (2003) Community disassembly, biodiversity
loss, and the erosion of an ecosystem service. Ecology, 84, 1421–1427.
Owen, J. (2005) Farming Claims Almost Half Earth’s Land, New Maps Show.
National Geographic News, 9. Available at: http://news.nationalgeographic.
com/news/2005/12/1209_051209_crops_map.html (accessed 5 November
2016).
Petanidou, T., Kallimanis, A.S., Tzanopoulos, J., Sgardelis, S.P. & Pantis, J.P.
(2008) Long-term observation of a pollination network: fluctuation in species
and interactions, relative invariance of network structure and implications for
estimates of speciation. Ecology Letters, 11, 564–575.
Ponisio, L.C., M’Gonigle, L.K. & Kremen, C. (2016) On-farm habitat restora-
tion counters biotic homogenization in intensively managed agriculture. Glo-
bal Change Biology, 22, 704–715.
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O. &
Kunin, W.E. (2010) Global pollinator declines: trends, impacts and drivers.
Trends in Ecology & Evolution, 25, 345–353.
Rader, R., Bartomeus, I., Garibaldi, L.A. et al. (2016) Non-bee insects are
important contributors to global crop pollination. Proceedings of the National
Academy of Sciences of the United States of America, 113, 146–151.
Rader, R., Edwards, W., Westcott, D.A., Cunningham, S.A. & Howlett, B.G.
(2011) Pollen transport differs among bees and flies in a human-modified
landscape. Diversity and Distributions, 17, 519–529.
Rader, R., Edwards, W., Westcott, D.A., Cunningham, S.A. & Howlett, B.G.
(2013) Diurnal effectiveness of pollination by bees and flies in agricultural
Brassica rapa: implications for ecosystem resilience. Basic and Applied
Ecology, 14, 20–27.
Rader, R., Howlett, B.G., Cunningham, S.A., Westcott, D.A., Newstrom-Lloyd,
L.E., Walker, M.K., Teulon, D.A. & Edwards, W. (2009) Alternative pollina-
tor taxa are equally efficient but not as effective as the honeybee in a mass
flowering crop. Journal of Applied Ecology, 46, 1080–1087.
Reiss, J., Bridle, J.R., Montoya, J.M. & Woodward, G. (2009) Emerging hori-
zons in biodiversity and ecosystem functioning research. Trends in Ecology
& Evolution, 24, 505–514.
Richardson, L.L., Adler, L.S., Leonard, A.S., Andicoechea, J., Regan, K.H.,
Anthony, W.E., Manson, J.S. & Irwin, R.E. (2015) Secondary metabolites in
floral nectar reduce parasite infections in bumblebees. Proceedings of the
Royal Society of London B: Biological Sciences, 282, 20142471.
Ricketts, T.H., Regetz, J., Steffan-Dewenter, I. et al. (2008) Landscape effects
on crop pollination services: are there general patterns? Ecology Letters, 11,
499–515.
Roulston, T.H. & Cane, J.H. (2002) The effect of pollen protein concentration
on body size in the sweat bee Lasioglossum zephyrum (Hymenoptera: Api-
formes). Evolutionary Ecology, 16, 49–65.
Roulston, T.H. & Goodell, K. (2011) The role of resources and risks in
regulating wild bee populations. Annual Review of Entomology, 56, 293–
312.
Russo, L., DeBarros, N., Yang, S., Shea, K. & Mortensen, D. (2013) Support-
ing crop pollinators with floral resources: network-based phenological match-
ing. Ecology and Evolution, 3, 3125–3140.
Sandel, B., Goldstein, L.J., Kraft, N.J.B., Okie, J.G., Shuldman, M.I., Ackerly,
D.D., Cleland, E.E. & Suding, K.N. (2010) Contrasting trait responses in
plant communities to experimental and geographic variation in precipitation.
New Phytologist, 188, 565–575.
Sardi~nas, H.S., Ponisio, L.C. & Kremen, C. (2016) Hedgerow presence does
not enhance indicators of nest-site habitat quality or nesting rates of ground-
nesting bees. Restoration Ecology, 24, 499–505.
Sargent, R.D. & Ackerly, D.D. (2008) Plant–pollinator interactions and the
assembly of plant communities. Trends in Ecology & Evolution, 23, 123–
130.
Saunders, D.A., Hobbs, R.J. & Margules, C.R. (1991) Biological consequences
of ecosystem fragmentation: a review. Conservation Biology, 5, 18–32.
Scheper, J., Holzschuh, A., Kuussaari, M., Potts, S.G., Rundl€of, M., Smith,
H.G. & Kleijn, D. (2013) Environmental factors driving the effectiveness of
European agri-environmental measures in mitigating pollinator loss – a meta-
analysis. Ecology Letters, 16, 912–920.
Spasojevic, M.J. & Suding, K.N. (2012) Inferring community assembly mecha-
nisms from functional diversity patterns: the importance of multiple assembly
processes. Journal of Ecology, 100, 652–661.
Spear, D.M., Silverman, S., Forrest, J.R. & McPeek, M.A. (2016) Asteraceae
pollen provisions protect Osmia mason bees (Hymenoptera: Megachilidae)
from brood parasitism. The American Naturalist, 187, 797–803.
Steffan-Dewenter, I. & Schiele, S. (2008) Do resources or natural enemies
drive bee population dynamics in fragmented habitats? Ecology, 89, 1375–
1387.
Stephen, W.P. (1960) Artificial bee beds for the propagation of the alkali bee,
Nomia melanderi. Journal of Economic Entomology, 53, 1025–1030.
Suding, K.N., Collins, S.L., Gough, L., Clark, C., Cleland, E.E., Gross, K.L.,
Milchunas, D.G. & Pennings, S. (2005) Functional- and abundance-based
mechanisms explain diversity loss due to N fertilization. Proceedings of the
National Academy of Sciences of the United States of America, 102, 4387–
4392.
Todd, K.J., Gardiner, M.M. & Lindquist, E.D. (2016) Mass flowering crops as
a conservation resource for wild pollinators (Hymenoptera: Apoidea). Journal
of the Kansas Entomological Society, 89, 158–167.
Tscharntke, T., Gathmann, A. & Steffan-Dewenter, I. (1998) Bioindication
using trap-nesting bees and wasps and their natural enemies: community
structure and interactions. Journal of Applied Ecology, 35, 708–719.
Tuell, J.K., Fiedler, A.K., Landis, D. & Isaacs, R. (2008) Visitation by wild
and managed bees (Hymenoptera: Apoidea) to eastern US native plants for
use in conservation programs. Environmental Entomology, 37, 707–718.
Tylianakis, J.M., Laliberte, E., Nielsen, A. & Bascompte, J. (2010) Conserva-
tion of species interaction networks. Biological Conservation, 143, 2270–
2279.
Vaughn, M. & Black, S.H. (2006) Agroforestry: sustaining native bee habitat
for crop pollination. USDA National Agroforestry Center, AF Note, 32, 1–4.
Vazquez, D.P., Bluthgen, N., Cagnolo, L. & Chacoff, N.P. (2009) Uniting pat-
tern and process in plant-animal mutualistic networks: a review. Annals of
Botany, 103, 1445–1457.
Wainwright, C.E., Wolkovich, E.M. & Cleland, E.E. (2012) Seasonal priority
effects: implications for invasion and restoration in a semi-arid system. Jour-
nal of Applied Ecology, 49, 234–241.
Walther, G.-R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J.C.,
Fromentin, J.-M., Hoegh-Guldberg, O. & Bairlein, F. (2002) Ecological
responses to recent climate change. Nature, 416, 389–395.
Weiher, E., Freund, D., Bunton, T., Stefanski, A., Lee, T. & Bentivenga, S.
(2011) Advances, challenges and a developing synthesis of ecological com-
munity assembly theory. Philosophical Transactions of the Royal Society of
London B: Biological Sciences, 366, 2403–2413.
Westrich, P. (1996) Habitat requirements of central European bees and prob-
lems of partial habitats. The Conservation of Bees (eds A. Matheson, S.L.
Buchmann, C. O’Toole, P. Westrich & I.H. Williams), pp. 1–16. Academic
Press, London, UK.
Wilfert, L., Long, G., Leggett, H.C., Schmid-Hempel, P., Butlin, R., Martin,
S.J.M. & Boots, M. (2016) Deformed wing virus is a recent global epidemic
in honeybees driven by Varroa mites. Science, 351, 594–597.
Williams, N.M., Crone, E.E., Minckley, R.L., Packer, L. & Potts, S.G. (2010)
Ecological and life-history traits predict bee species responses to environmen-
tal disturbances. Biological Conservation, 143, 2280–2291.
Williams, N.M. & Kremen, C. (2007) Resource distributions among habitats
determine solitary bee offspring production in a mosaic landscape. Ecological
Applications, 17, 910–921.
Williams, N.M., Ward, K.L., Pope, N. et al. (2015) Native wildflower plantings
support wild bee abundance and diversity in agricultural landscapes across
the United States. Ecological Applications, 25, 2119–2131.
Winfree, R., Bartomeus, I. & Cariveau, D.P. (2011) Native pollinators in
anthropogenic habitats. Annual Review of Ecology, Evolution, and Systemat-
ics, 42, 1–22.
Winfree, R., Fox, J.W., Williams, N.M., Reilly, J.R. & Cariveau, D.P. (2015)
Abundance of common species, not species richness, drives delivery of a
real-world ecosystem service. Ecology Letters, 18, 626–635.
Winfree, R. & Kremen, C. (2009) Are ecosystem services stabilized by differ-
ences among species? A test using crop pollination. Proceedings of the Royal
Society of London B: Biological Sciences, 276, 229–237.
Winfree, R., Williams, N.M., Dushoff, J. & Kremen, C. (2007) Native bees
provide insurance against ongoing honey bee losses. Ecology Letters, 10,
1105–1113.
Wojcik, V.A. & Buchmann, S. (2012) Pollinator conservation and management
on electrical transmission and roadside rights-of-way: a review. Journal of
Pollination Ecology, 7, 16–26.
Wratten, S.D., Gillespie, M., Decourtye, A., Mader, E. & Desneux, N. (2012)
Pollinator habitat enhancement: benefits to other ecosystem services. Agricul-
ture, Ecosystems & Environment, 159, 112–122.
Xerces Society for Invertebrate Conservation, National Resources Defense
Council & Defenders of Wildlife (2010) Petition before the United States
Department of Agriculture Animal and Plant Health Inspection Service.
Petition to regulate the movement of commercial bumble bees.
Zurbuchen, A., Landert, L., Klaiber, J., M€uller, A., Hein, S. & Dorn, S. (2010)
Maximum foraging ranges in solitary bees: only few individuals have the
capability to cover long foraging distances. Biological Conservation, 143,
669–676.
Received 14 November 2016; accepted 3 February 2017
Handling Editor: David Gibson