Mitigating the Effects of Habitat Loss on Solitary Bees in Agricultural Ecosystems

Abstract

Solitary bees and other wild pollinators provide an important ecosystem service which can benefit both the agricultural economy and the sustainability of many native ecosystems. Many solitary bees, however, are experiencing decreases in their populations and ranges, resulting in an overall loss of pollinator species richness in many areas. Several interacting factors have been implicated in this decline, including increased pesticide use, climate change, and pathogens, but habitat loss remains one of the primary drivers. The widespread conversion of natural habitats into agricultural landscapes has decreased the availability of adequate nesting sites and floral diversity for many bee species. Large monocultures with intensive production systems often cannot support the populations of wild bees (particularly species with short foraging ranges) necessary to ensure adequate pollination of animal-pollinated crops. Diversifying agricultural landscapes through the incorporation of wildflower plantings, as well as the preservation of remaining natural habitats, may offer a solution, as it has been shown to increase both bee diversity and abundance and the pollination of nearby crops. In this review article, we discuss the various effects of habitat loss on solitary bees and different ways to mitigate such effects in order to conserve bee diversity and populations in agricultural landscapes.

Full text

agriculture
Review
Mitigating the Effects of Habitat Loss on Solitary Bees
in Agricultural Ecosystems
Olivia Kline and Neelendra K. Joshi *
University of Arkansas, Department of Entomology and Plant Pathology, 217 Plant Sciences Bldg.,
Fayetteville, AR 72701, USA; okline@uark.edu
*Correspondence: nkjoshi@uark.edu or neeljoshi1005@gmail.com
Received: 23 January 2020; Accepted: 19 March 2020; Published: 5 April 2020


Abstract:
Solitary bees and other wild pollinators provide an important ecosystem service which can
benefit both the agricultural economy and the sustainability of many native ecosystems. Many solitary
bees, however, are experiencing decreases in their populations and ranges, resulting in an overall loss
of pollinator species richness in many areas. Several interacting factors have been implicated in this
decline, including increased pesticide use, climate change, and pathogens, but habitat loss remains
one of the primary drivers. The widespread conversion of natural habitats into agricultural landscapes
has decreased the availability of adequate nesting sites and floral diversity for many bee species.
Large monocultures with intensive production systems often cannot support the populations of wild
bees (particularly species with short foraging ranges) necessary to ensure adequate pollination of
animal-pollinated crops. Diversifying agricultural landscapes through the incorporation of wildflower
plantings, as well as the preservation of remaining natural habitats, may offer a solution, as it has
been shown to increase both bee diversity and abundance and the pollination of nearby crops. In this
review article, we discuss the various effects of habitat loss on solitary bees and different ways to
mitigate such effects in order to conserve bee diversity and populations in agricultural landscapes.
Keywords:
solitary bees; wild bees; native bees; pollinator; habitat loss; floral diversity; bee nutrition;
pollinator decline
1. Introduction
Animal pollinators, and in particular insect pollinators, provide an important ecosystem service,
one which globally benefits the diversity of wild plants, the human diet, agricultural production,
and the economy [
1
]. They support many native ecosystems, as around 80% of wild angiosperm
species are pollinated by animals, and the majority of these rely on pollination by different species of
bees [
2
]. Crop production, as well, often requires or at least improves with bee pollination, and this is
especially noted in certain crops, such as vegetables, fruits, and oils. Overall, around 9.5% of the total
worldwide agricultural production is due to the services provided by these insect pollinators [
3
].
The contribution to agriculture has been estimated to produce 15–30% of the human diet, both from
the pollination of food crop plants that are consumed directly by humans and from the pollination of
plants, such as alfalfa and clover, that are used to feed livestock [
4
]. Along with the improvements to
the nutrition and diversity of the human diet, there is an economic value to the pollination by bees. In
2009, 11% of the agricultural gross domestic product (GDP) came from crops pollinated by animals [
5
].
An estimated $3.07 billion annually in the United States alone comes from the plants pollinated by
wild bees, including unmanaged bumble bees and solitary bees [6].
Because of this value of pollination by bees, it is important to maintain their populations and
to therefore ensure that adequate pollination continues in both wild and cultivated flowering plants.
However, bee pollinators globally are facing problems with declining populations and reduced
Agriculture 2020,10, 115; doi:10.3390/agriculture10040115 www.mdpi.com/journal/agriculture

Agriculture 2020,10, 115 2 of 14
biodiversity [
7
–
10
]. The majority of the research on both the contributions of bee pollinators and
the bee population declines has focused on honey bees (Apis spp.), and to a lesser extent bumble bees
(Bombus spp.), but there is a lack of information on the solitary bees, which make up the majority, over
85%, of the estimated 25,000–30,000 species of bees worldwide [
11
]. In North America alone, there
are around 4000 species of native bees [
12
], 54 of which are bumble bee species and over 3900 solitary
bee species [
13
]. Western honey bees (Apis mellifera) are not a native of North America, but were
brought over in 1622 from Europe to the Americas [
12
,
14
]. There is no doubt that managed honey
bees provide valuable pollination services, but solitary bees have long been overlooked as pollinators
of wildflowers and crops. Many growers of bee-pollinated plants could benefit from encouraging
a diversity of species and families of bees, beyond just honey bees [15].
Native solitary bees can be more efficient pollinators of certain wild plants and crops than honey
bees, and have the potential to enhance crop yields with their pollination services [
16
]. Many growers
rely on solitary and wild bees for pollination in their fruit farms [
17
,
18
]. Sweet cherry orchards,
for example, had higher yields when pollinated by the blue orchard bee (Osmia lignaria) than when
pollinated by A. mellifera [
19
]. The native solitary bee, Anthophora urbana, and the bumble bee, Bombus
vosnesenskii, were both able to increase tomato production. Tomatoes are often self-pollinating plants,
but when cross-pollinated by wild bees, more tomato flowers developed into fruits [
20
]. Wild bees
may also enhance the pollination ability of honey bees, as was observed in a study on sunflower seed
production. They found that the presence of wild bees actually increased the pollination efficiency
of honey bees, measured by the number of seeds produced compared to the number of visits by bee
pollinators [21].
Native solitary bees can be more effective pollinators of certain flowers than honey bees, in
part due to their ability for sonication, the vibration of the bees’ indirect flight muscles. Sonication
can be used for multiple purposes, including defense warning and nest building, but many native
bees, such as Bombus and Xylocopa species also use it for pollen collection. Flowers that require
sonication for pollination, or “buzz-pollinated flowers” are not well pollinated by honey bees, but
rely on wild bees [
22
]. Because of these services provided by solitary bees, it is important to maintain
their populations, and to maintain a high species richness of both solitary and social bees. This
review focuses on the detrimental effects of habitat loss on wild and solitary bee populations and
on developing strategies to mitigate them. In addition, the conservation of solitary bee diversity in
agricultural landscapes and enhancement of their pollination services are both briefly discussed.
2. Recent Declines in Native Bee Populations
Many insect pollinators, including species of honey bees and native North American bees have
seen recent declines in population in different geographical regions [
9
,
23
–
28
]. Compared to other
geographical regions, in North America there has been a better documentation of population declines
and loss of species richness in the Bombus genus, though there has been evidence for solitary species as
well [
29
]. Surveys comparing the relative abundance and range of several Bombus species have found
several species to be in serious decline, and that some of the declining species formerly had broad
geographic distributions [
30
]. Some species appear to have become regionally extinct, or at the least
extremely rare, in areas where they had been previously caught. For instance, three species, Bombus
affinis, Bombus pensylvanicus, and Bombus ashtoni, were all well observed in a survey in the eastern
United States in the 1970s, but could not be found in a comparative survey in the early 2000s [24].
The decline of solitary bees, however, has been more thoroughly researched and documented in
Europe than in North America and other continents. In the Netherlands and the United Kingdom,
researchers observed a loss of diversity and evenness of unmanaged (non-Apis) bee populations,
with the pollinator populations becoming increasingly dominated by a smaller number of species.
They also noted that the species in decline tended to be specialist feeders with lower mobility [
31
].
Similar results were seen in Belgium and France, and the percentage of declining species was especially
high in the Apidae,Anthophoridae, and Megachilidae families of bees (around 58%, 55%, and 25%,

Agriculture 2020,10, 115 3 of 14
respectively) [
32
]. Ireland was estimated to have 3% of their native species regionally extinct and
41% threatened or endangered [
33
]. These trends coincide with overall losses in insect diversity and
biomass in many world regions [34,35].
Many interacting factors have been implicated in these declines. Temperature changes, which can
be brought on by climate change, have been observed to alter bee development and emergence [
36
].
Agrochemicals, including insecticides, herbicides, and fungicides, have been implicated as risk factors
to pollinators, though there is still a great deal of disagreement on the extent of this threat [
37
–
39
].
Parasites and disease can cause harm to social and solitary bees [
40
–
42
]. Of the many risk factors,
the loss of native habitats, especially when the loss is caused by urban development and to an even
greater extent, agricultural intensification, stands out among risk factors as one of the most detrimental
to bee populations [43–45].
3. Habitat Loss as a Major Contributor to Bee Population Decline
Habitat loss has become a particular cause for concern as the amount of land dedicated to
agricultural use has rapidly expanded since the 1700s, with an estimated 600% increase of the area
of grazing land alone. Managed grazing land now takes up around 25% of the terrestrial surface
of the planet Earth, which equates to over 33 million km
2
worldwide [
46
]. New grazing land for
livestock has expanded over several biomes globally, including grasslands, deciduous and evergreen
forests, and tropical forests. In North America, heavy grazing by livestock in prairie habitats can
cause the grassland to degrade, lose a portion of its floral diversity and become more like a desert [
46
].
The cultivation of grains and other crops have also undergone an intensification in the past century, in
both the yield of the crops and the area of land used to grow them [
47
]. This agricultural expansion
has coincided with, and in many cases caused, the decrease of native habitats used by solitary bees.
From 1830 to 1994, the United States experienced up to an 82% to 99% loss of unmanaged tallgrass
prairie [
48
]. Of the prairies that remain, they tend to be too small and too scarce to provide a suitable
habitat for the biodiversity they formerly supported [
49
]. The ranges of many common native bees,
both bumble bees and solitary bees, have declined in North America over the past century, as their
native habitats, such as the tallgrass prairies, have been largely taken over by land for agricultural
use [38,44,48].
3.1. Effects on Nesting Sites of Solitary Bees
Habitat loss can be detrimental to solitary bees due to their particular habitat requirements for
adequate nesting sites, floral resources, and the close proximity of these two things. There are a variety
of nesting behaviors and materials (i.e., nesting substrates) used by different solitary bee species
(Figure 1). Some, such as miner bees (Andrena spp.) and many species of sweat bees (Hymenoptera:
Halictidae), dig tunnels in the ground [
11
]. Even within these groups, there is a great deal of diversity
of nesting preferences, with different species preferring varying moisture levels, compaction, and
grain sizes of the soils [
50
]. Other solitary bees, like the mason and leafcutter bees (Hymenoptera:
Megachilidae), use natural materials, such as mud and leaves, to construct nests within pre-existing
cavities on tree trunks or branches. Still others, like the carpenter bees (Xylocopa spp.), chew their own
holes into wood [
11
]. This high diversity of nesting preferences suggests a diversity of natural habitats
is needed to support a high number of solitary bee species.
Along with adequate nesting sites, a habitat must provide floral resources in order to be suitable
for solitary bees. Müller et al. [
51
] surveyed 41 solitary bee species in Europe and found that each
female needed enough pollen to provision around 10–30 brood cells. Depending on the size and
pollen requirements of the bees, this could take from one up to hundreds of flowers for each female
bee [
51
]. Bees with a larger body size may also be more susceptible to a decrease in floral resources,
because they tend to require more food [
51
,
52
]. Modern agricultural trends have the potential to
decrease the amount of floral resources available for the bees, with the widespread use of monocultures,
especially those in uninterrupted agricultural landscapes, which may not provide adequate nutrition

Agriculture 2020,10, 115 4 of 14
to support a variety of solitary bees [
53
]. Native flower plantings provide season-long support to wild
bee communities [
54
,
55
], and their plantings in monoculture farmland could be helpful in minimizing
such effects. Certain bees are highly specialized feeders, only eating the pollen and nectar of a few
species or genera of flowers, and may have trouble finding their food source if they cannot feed on
the flower of the monoculture crop. Other species feed on a wider variety of flowers, and require
some diversity in their diet and in the nutrients they consume [
56
,
57
]. Similarly, some studies have
shown that by breaking up a purely agricultural area, adding things like hedgerows and uncultivated
natural areas, pollinator health and function can improve when compared to pollinators in a strictly
monoculture landscape [53].
Agriculture 2020, 10, x FOR PEER REVIEW 4 of 14
Figure 1. Leafcutter bees constructing nest in a drilled wood block (a) while ground-nesting solitary
bees prefer well-drained patches in bee habitat for nest construction (b). Pictures by N. Joshi.
Along with adequate nesting sites, a habitat must provide floral resources in order to be suitable
for solitary bees. Müller et al. [51] surveyed 41 solitary bee species in Europe and found that each
female needed enough pollen to provision around 10–30 brood cells. Depending on the size and
pollen requirements of the bees, this could take from one up to hundreds of flowers for each female
bee [51]. Bees with a larger body size may also be more susceptible to a decrease in floral resources,
because they tend to require more food [51,52]. Modern agricultural trends have the potential to
decrease the amount of floral resources available for the bees, with the widespread use of
monocultures, especially those in uninterrupted agricultural landscapes, which may not provide
adequate nutrition to support a variety of solitary bees [53]. Native flower plantings provide season-
long support to wild bee communities [54,55], and their plantings in monoculture farmland could be
helpful in minimizing such effects. Certain bees are highly specialized feeders, only eating the pollen
and nectar of a few species or genera of flowers, and may have trouble finding their food source if
they cannot feed on the flower of the monoculture crop. Other species feed on a wider variety of
flowers, and require some diversity in their diet and in the nutrients they consume [56,57]. Similarly,
some studies have shown that by breaking up a purely agricultural area, adding things like
hedgerows and uncultivated natural areas, pollinator health and function can improve when
compared to pollinators in a strictly monoculture landscape [53].
3.2. Role in Conserving and Propagating Solitary and Wild Bees.
Native, solitary bees require proper nesting sites and plentiful floral resources, and they need
them in close proximity to each other. There could be natural areas with all the materials needed for
nest construction, but if there are no adequate flowers within the bees’ foraging range, then the nest
site will go unused. Several studies have been done on the maximum foraging range of various
solitary bee species. Generally, they have found that solitary bees prefer to stay closer to the nest and
take shorter foraging bouts than social bees, like honey bees and bumble bees. One study, which
surveyed 16 solitary bee species, found maximum foraging distances of only 150–600 m [58]. Another
found longer foraging distances, but still only 1100–1400 m away from the nest for the three solitary
bee species in the study. However, the majority of the individual bees in the study never reached this
maximum foraging range. Most resisted traveling more than 300 m away from their nesting sites [59].
Both studies found a correlation between bee body size and foraging range, with larger species able
to travel farther than smaller species. When fewer floral resources are available, bees will take longer
Figure 1.
Leafcutter bees constructing nest in a drilled wood block (
a
) while ground-nesting solitary
bees prefer well-drained patches in bee habitat for nest construction (b). Pictures by N. Joshi.
3.2. Role in Conserving and Propagating Solitary and Wild Bees.
Native, solitary bees require proper nesting sites and plentiful floral resources, and they need
them in close proximity to each other. There could be natural areas with all the materials needed for
nest construction, but if there are no adequate flowers within the bees’ foraging range, then the nest
site will go unused. Several studies have been done on the maximum foraging range of various solitary
bee species. Generally, they have found that solitary bees prefer to stay closer to the nest and take
shorter foraging bouts than social bees, like honey bees and bumble bees. One study, which surveyed
16 solitary bee species, found maximum foraging distances of only 150–600 m [
58
]. Another found
longer foraging distances, but still only 1100–1400 m away from the nest for the three solitary bee
species in the study. However, the majority of the individual bees in the study never reached this
maximum foraging range. Most resisted traveling more than 300 m away from their nesting sites [
59
].
Both studies found a correlation between bee body size and foraging range, with larger species able to
travel farther than smaller species. When fewer floral resources are available, bees will take longer
foraging trips [
58
], but doing so can have negative effects on the larval bees. By spending more time
away from the nest and looking for food, the female bee leaves her nest more vulnerable to predators
and parasites [
11
]. Habitat loss and habitat fragmentation can make it more difficult for solitary bees
to find nesting sites and floral resources in close proximity.

Agriculture 2020,10, 115 5 of 14
4. Floral Diversity: Impacts on Solitary Bee Health
The lack of floral diversity that can occur due to habitat loss can have a detrimental effect on
solitary bee health. Solitary bees that are unable to access adequate floral resources show a drop in
fecundity and body weight. A study on the European orchard bee (Osmia cornuta) found a positive
correlation between the weight of the larval provision and the weight of the offspring, meaning that
offspring with access to more food tended to grow to a larger size [
60
]. Similarly, females of the species
with a higher provisioning rate also showed an increase in the number of offspring they had [
19
]. It is
not just the size of the pollen provision, however, but also the content of the pollen that can influence
bee health and development. When the larvae of the sweat bee, Lasioglossum zephyrum, were offered
pollen with differing protein contents, larvae that were fed protein-rich pollen grew to a larger size
than those who were fed protein-poor pollen [
61
]. In another example, larvae of the subsocial bee,
Ceratina calcarata, grew to a smaller adult size and had lower lipid stores when fed a diet with reduced
amounts of pollen and nectar [
62
]. Similar effects have been observed in social bees as well. For
instance, bumble bees have a preference for higher quality pollen, with a higher protein content, and
will visit flowers that provide this high quality pollen with greater frequency [63].
In addition to affecting body size and development, an adequate diet or lack thereof can affect
the susceptibility of many bee species to parasites and pathogens. Most of the research investigating
this relationship has focused on social bees, Apis spp. and Bombus spp., and there is little information
on the diseases of native solitary bees. In honey bees (A. mellifera), pollen content can play an important
role in immune function and detoxification. Pollen, as well as the honey and bee bread made from it,
can contain p-coumaric acid, an organic compound that can induce and upregulate honey bee genes
involved in toxicity and pathogen resistance [
64
]. Diet diversity from polyfloral pollen was shown to
increase glucose oxidase (GOX) activity in A. mellifera compared to monofloral pollen. GOX is involved
in the sterilization of food for brood, and as such is important for honey bee social immunity [
65
]. Apis
mellifera larvae fed a nutritionally poor monofloral pollen diet were more susceptible to the fungal
parasite, Aspergillus flavus than those that were fed diets supplemented by either polyfloral pollen or
dandelion pollen [
66
]. Similarly, common eastern bumble bees (Bombus impatiens) that were infected
with trypanosome parasites, Crithidia spp., had higher survival rates of the infection when fed nectar
with higher sucrose concentrations (30%) and pollen, as opposed to bumble bees fed reduced nutritional
diets [
67
]. Pollen and nectar provide protein and carbohydrates to bee diets, which can influence
health and immunity, but can also include secondary metabolites, which can also have an impact on
bee interactions with parasites and pathogens. Secondary metabolites are chemicals produced by
plants, often acting as defensive compounds to deter herbivorous feeding [
68
]. Low levels of these
compounds can also exist in nectar and can be consumed by pollinators. Some of these secondary
metabolites have been shown to reduce parasite loads in B. impatiens. This effect was most noticeable
with the alkaloid, anabasine, which is produced by Nicotiana spp. of plants. Anabasine reduced levels
of the parasite, Crithidia bombi, by 81% in one study [
69
], and in another was shown to have no negative
effect on the health of unparasitized bees [
70
]. Solitary bees can also be infected by a variety of viral and
fungal pathogens and can be affected by nest parasites, including species of blister beetles (Coleoptera:
Meloidae) and cuckoo wasps (Hymenoptera: Chrysididae) [
41
,
71
]. The relationship between their diet
and infection rates remains under-researched, however.
More research is needed on more species of solitary bees, but these initial findings suggest that
both social and solitary bees require high quality pollen that contains an adequate protein content,
as well as beneficial organic compounds, including certain plant secondary metabolites. The protein
content of bee bread, a mixture of pollen and nectar used to feed bee larvae, can differ depending
on the nest’s proximity to natural areas. Bees that were able to forage closer to wild grasslands and
forests had a higher protein content in their bee bread than those that foraged in farmland areas [
72
].
Habitat loss can cause solitary bees to be farther from these natural areas, which can lead to a decrease
in the protein content of the larval provision. This could have detrimental effects on the size and health

Agriculture 2020,10, 115 6 of 14
of the larval bees and suggests that many agricultural landscapes do not provide the adequate volume
and nutritional requirements of food for many solitary bees.
Floral Diversity Affects Community Dynamics of Solitary Bees
Overall, areas with a higher diversity of flowers, such as natural habitats, have been shown to
also have a higher diversity of bees [
73
,
74
]. Incorporating diverse floral plantings in an agricultural
landscape could enhance ecosystem services of pollinators and other beneficial insects [
75
,
76
], and
could support bee communities after the flowering period of main crops [
77
]. The drop in diversity
of solitary bees, as they move farther away from these natural habitats, like woods and prairies, is
cause for particular concern, because a higher diversity of bee species can have a positive impact on
pollination and plant yield. Inversely, a lack of bee diversity caused by the distance from natural areas
can have a negative impact on pollination, as was observed by Hoehn et al. [
78
]. In this study, a greater
diversity of bee species was shown to increase seed production in pumpkin plants. There are a few
factors that may explain this increase. Bee species differ in the times of day in which they are active, so
greater species richness would likely increase the amount of time that a flower is pollinated. Certain
bee body sizes are better suited to visit different flower shapes, flower sizes, and parts of flowers.
In addition, different species of bees are also known to have a preference for different flower colors.
Having a variety of species, and therefore a variety of body sizes, in an area can likewise increase
the number of flowers that get pollinated. Greater species richness can increase production overall of
some crop plants [
78
]. Several other studies have found that proximity to natural areas can enhance
the diversity and pollination ability of solitary bees in both North America and Europe [
38
,
79
–
82
].
For instance, in a Costa Rican study on coffee bean production, fields that were within 1 km of forest
and riparian zone habitats had a higher diversity of both solitary and social native bees, as well as
a 20% increase in yield and a reduction in misshapen coffee beans [
83
]. A similar effect had been
observed for watermelon production, where Kremen et al. found that in watermelon fields with
a greater proportion of natural habitat within 1–2.5 km, the pollen deposition by solitary bees was
enhanced when compared to fields that were farther from the natural habitats [15].
Habitat loss and fragmentation can have a negative effect on bee abundance and diversity, but
this effect was greatly ameliorated in areas where some natural habitat remained [
84
]. The enhanced
pollination ability of solitary bees and increases in crop yield due to the presence of a nearby natural
area can provide an economic benefit to many farmers of insect-pollinated crops. The conservation
of solitary bees is therefore important both for protecting wild ecosystems and agriculture [
38
,
82
,
83
].
Having a greater diversity of species can help make a community more resilient as well. The loss
of one species will not mean the loss of the entire ecosystem service, in this case pollination, when
species diversity is high [
85
]. There has been some debate over the degree of competition between
managed honey bees and wild bees in North America, and whether honey bees take resources from
wild solitary bees and bumble bees [
86
]. However, both honey bees and wild bees are able to benefit
from having an abundance and diversity of floral resources, and especially when they have access
to natural habitat and wild angiosperms. Managed honey bees may be more tolerant to areas with
poor floral availability, likely due to the intervention of beekeepers who can supplement the bee hives
with alternative food sources, but solitary bees tend to be more vulnerable [
87
]. The conservation and
management strategies for both honey bees and native bees in North America may be similar. By
providing more floral resources, the populations of both groups can benefit.
5. Recommendations and Implications
Given the detrimental effects that habitat loss can have on solitary bees, the preservation of
the remaining natural areas could also preserve the populations and species richness of the solitary
bees. For habitats such as the tallgrass prairie in the central United States, conservation is especially
important, because the tallgrass prairie has been so reduced in area over the past three centuries [
48
].
Currently temperate grasslands and savannas remain some of the least protected habitats [
88
]. Major

Agriculture 2020,10, 115 7 of 14
threats to these habitats include overgrazing by livestock, droughts, and tree encroachment [
46
].
Prevention of encroachment by wood plants and trees in grasslands and savannas would help with
their preservation [
48
]. Such habitats can provide both nesting sites and food resources for a variety of
bees, so their conservation would also help maintain the biodiversity of bees in these areas.
For areas that have already undergone a great deal of habitat loss and agricultural intensification,
landscape management can help to enhance solitary bee diversity and promote pollination [
89
].
Miniature natural habitats can be added to agricultural landscapes in the form of native flower
plantings or floral strips (Figure 2), and in other forms, such as shelterbelts, and hedgerows, which
can provide nesting sites and wind breaks when planted on the edges of crop fields and grazing
lands [87,90].
Agriculture 2020, 10, x FOR PEER REVIEW 7 of 14
Currently temperate grasslands and savannas remain some of the least protected habitats [88]. Major
threats to these habitats include overgrazing by livestock, droughts, and tree encroachment [46].
Prevention of encroachment by wood plants and trees in grasslands and savannas would help with
their preservation [48]. Such habitats can provide both nesting sites and food resources for a variety
of bees, so their conservation would also help maintain the biodiversity of bees in these areas.
For areas that have already undergone a great deal of habitat loss and agricultural
intensification, landscape management can help to enhance solitary bee diversity and promote
pollination [89]. Miniature natural habitats can be added to agricultural landscapes in the form of
native flower plantings or floral strips (Figure 2), and in other forms, such as shelterbelts, and
hedgerows, which can provide nesting sites and wind breaks when planted on the edges of crop
fields and grazing lands [87,90].
Figure 2. Establishment of floral resource plantings comprised of diverse native flowering plants for
bees and other pollinators near crop fields (a) and high tunnels (b). Pictures by N. Joshi.
Figure 2.
Establishment of floral resource plantings comprised of diverse native flowering plants for
bees and other pollinators near crop fields (a) and high tunnels (b). Pictures by N. Joshi.

Agriculture 2020,10, 115 8 of 14
The management of natural areas for ecosystem services is still poorly understood and is not
done often or well [
91
]. More information is needed to strike a balance between the land reserved
for ecosystem services like pollination and land used for agriculture, and to know how much natural
land is needed for adequate pollination [
15
]. A stable population of the pollinating bees can provide
an economic benefit, so natural habitats are worth the investment to ensure the ecosystem service
continues [
92
]. This balance between the ecological and economic benefits of adding natural habitats and
the initial financial costs of establishing native plants has been more thoroughly researched in California.
There, schemes to establish hedgerows of native trees, shrubs, grasses, sedges, and rushes, have been
shown to improve several ecosystem services, including soil erosion control, enhanced water filtration
and water quality, and increased species richness of beneficial arthropods [
93
,
94
]. These hedgerows
also have the potential to serve a great benefit for more vulnerable pollinator species, particularly those
with specialist diets, lower mobility, and specialized nesting site requirements [
95
]. Such restoration
schemes are still not often used in the United States due to the upfront costs of establishing such
habitats and the concern that such schemes will not see a financial return on investment. These
upfront costs can be high, with the estimated cost of a 300 m hedgerow in California to be $4000 [
93
].
A few years after establishment, however, natural plantings often require little upkeep [
94
], especially
when compared to conventional field edge management strategies of frequent mowing and herbicide
treatments, which can also be financially costly [
93
,
96
]. One economic cost-benefit model estimated
a return on investment within 5 to 16 years, depending on the ecosystem service requirements of
the area [
93
]. This would likely vary by region and by local landscape conditions, and is worth
investigating on a local level.
Poor nutrition is one of the main concerns of the negative effect that habitat loss can have on
solitary bees, so providing more floral resources has become an effective management strategy. In
Europe, several farms have adopted floral provisioning schemes and planted wildflowers alongside
their fields. Such schemes can provide a greater amount and variety of floral resources for the bees,
though there are several considerations to keep in mind when selecting flowers, including seed
costs, pollinator floral preferences, regional growing conditions, and bloom period [
97
–
99
]. The cost
of buying wildflower seeds is one of the major factors determining whether a floral provisioning
scheme will be implemented at all. Lower cost provisions are more likely to receive support and
can also ensure that more areas of land can potentially be planted [
97
]. Another economic concern
for wildflower plantings on field margins is the loss of land area that would have otherwise been
used for crop plantings. It is also important to select field margins that will not serve as a secondary
host of arthropod pests for the crop fields [
100
]. These plantings have been shown to improve bee
species richness in several world regions, however. Planting native, bee-preferred plants helped both
solitary and bumble bee populations in Italy [
101
]. In North America, a study that compared plots
with wildflower mixes to unmanaged weedy plots, found that the wildflower mixes in all the observed
regions (Florida, Michigan, and California) increased the abundance and species richness of wild bees
when compared to the control [
55
]. Flat monoculture landscapes are also a cause for concern, so the use
of crop diversification could help maintain bee diversity [
87
]. Aside from actively planting wildflowers,
there are some simpler and potentially more cost-effective measures, as well. Mowing less frequently
has been shown to improve pollinator abundance in residential landscapes, but may be applied to
agricultural landscapes. Common garden weeds, like dandelion and clover, can provide high quality
forage for many bees when allowed to grow longer and to flower [
102
]. Again, however, it is important
to monitor such areas for detrimental weeds and alternative host plants that may interfere with nearby
crop production. Floral plantings directly along crop field margins may offer the greatest benefit to
crop pollination, but unused areas, such as road verges and powerline easements, may also benefit
pollination if planted with wildflowers or mowed less frequently [
96
,
103
,
104
]. Finally, wildflower
provisioning can have additional benefits to local ecosystems and crop yields, besides pollination. Such
plantings can increase the population density of natural predators, such as spiders and lady beetles,
which feed on crop pests, and have been shown to reduce pest populations of soybean aphids [
75
,
105
].

Agriculture 2020,10, 115 9 of 14
Supplementing habitats with different nesting substrates could be helpful in propagation of solitary
bees in agricultural ecosystems. Different types of nest-box designs [
106
–
109
] and supplementations
are used for mason bees and leafcutter bees (Figure 3). Adding artificial habitats to an area could
attract and maintain solitary bees, particularly cavity- and tunnel-nesting bees. Many such “bee
hotels” have become available in recent years, though they are often designed to attract a variety
of native and non-native bees by including holes or tubes of varying widths [
110
]. This can raise
concerns of increasing parasite and pathogen spread among residents of the artificial nests [
111
].
Appropriate nesting substrates and nest liners for the mason bees and other tunnel-nesting bees are
important to provide protection from different pests [
112
]. Soil amendments in bee habitats could
be helpful for ground-nesting bees, as these bees construct their nests in well-drained soils [
113
])
and soils with differing textures and grain sizes [
50
]. Unlike tunnel-nesting bees, artificial nests for
ground-nesting bees may not be as effective, however, and could remain empty [
101
]. The development
of species-specific artificial nesting substrates could help in the conservation and propagation of wild
and solitary bees in different ecosystems, and future research should continue to design and develop
cost-effective and durable nest substrates for different species of solitary bees.
Agriculture 2020, 10, x FOR PEER REVIEW 9 of 14
Supplementing habitats with different nesting substrates could be helpful in propagation of
solitary bees in agricultural ecosystems. Different types of nest-box designs [106–109] and
supplementations are used for mason bees and leafcutter bees (Figure 3). Adding artificial habitats
to an area could attract and maintain solitary bees, particularly cavity- and tunnel-nesting bees. Many
such “bee hotels” have become available in recent years, though they are often designed to attract a
variety of native and non-native bees by including holes or tubes of varying widths [110]. This can
raise concerns of increasing parasite and pathogen spread among residents of the artificial nests [111].
Appropriate nesting substrates and nest liners for the mason bees and other tunnel-nesting bees are
important to provide protection from different pests [112]. Soil amendments in bee habitats could be
helpful for ground-nesting bees, as these bees construct their nests in well-drained soils [113]) and
soils with differing textures and grain sizes [50]. Unlike tunnel-nesting bees, artificial nests for
ground-nesting bees may not be as effective, however, and could remain empty [101]. The
development of species-specific artificial nesting substrates could help in the conservation and
propagation of wild and solitary bees in different ecosystems, and future research should continue
to design and develop cost-effective and durable nest substrates for different species of solitary bees.
Figure 3. Different types of nest supplementations for mason and leafcutter bees (a,b) and
deployment of a nest box (also known as Bee Hotel) in bee habitat (c). Pictures by N. Joshi.
Because much of the research on pollinators has focused heavily on the social bees, more
information is needed in order to fully understand the impact that habitat loss is having on the
solitary bees. It is clear that solitary bees have distinct and varied habitat requirements that are not
always met in heavily managed agricultural areas, and that both pollinator function and species
richness benefit from a close proximity to natural areas [15,80,83]. It would be beneficial to have more
information on the relationship between the ecosystem service provided by the bees and the amount
of natural habitat they require [15]. In addition, establishing region-specific baseline information on
wild bee diversity and abundance would be helpful in documenting the impact of habitat loss on the
communities of these bees. Wild bees are more difficult to survey than managed bees, but given the
importance of these bees to the pollination of wildflowers and crop plants, their populations are
worth monitoring and protecting. Developing and implementing coordinated research projects on
regional and global scales would be an important step in this direction.
Author Contributions: O.K. and N.K.J. conceptualized the study. O.K. prepared the manuscript draft with
contribution and guidance from N.K.J., and both authors reviewed and approved the manuscript. Opinions and
recommendations expressed in this manuscript are those of the authors.
Funding: USDA-NIFA (Project # ARK02527) and the UA System Division of Agriculture.
Conflicts of Interest: The authors declare no conflict of interest. The funders had no role in the design of the
study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to
publish the results.
Figure 3.
Different types of nest supplementations for mason and leafcutter bees (
a
,
b
) and deployment
of a nest box (also known as Bee Hotel) in bee habitat (c). Pictures by N. Joshi.
Because much of the research on pollinators has focused heavily on the social bees, more
information is needed in order to fully understand the impact that habitat loss is having on the solitary
bees. It is clear that solitary bees have distinct and varied habitat requirements that are not always met
in heavily managed agricultural areas, and that both pollinator function and species richness benefit
from a close proximity to natural areas [
15
,
80
,
83
]. It would be beneficial to have more information on
the relationship between the ecosystem service provided by the bees and the amount of natural habitat
they require [
15
]. In addition, establishing region-specific baseline information on wild bee diversity
and abundance would be helpful in documenting the impact of habitat loss on the communities of
these bees. Wild bees are more difficult to survey than managed bees, but given the importance of
these bees to the pollination of wildflowers and crop plants, their populations are worth monitoring
and protecting. Developing and implementing coordinated research projects on regional and global
scales would be an important step in this direction.
Author Contributions:
O.K. and N.K.J. conceptualized the study. O.K. prepared the manuscript draft with
contribution and guidance from N.K.J., and both authors reviewed and approved the manuscript. Opinions and
recommendations expressed in this manuscript are those of the authors. All authors have read and agreed to
the published version of the manuscript.
Funding: USDA-NIFA (Project # ARK02527) and the UA System Division of Agriculture.
Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the study;
in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish
the results.

Agriculture 2020,10, 115 10 of 14
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