ArticlePDF Available

Landscape context shifts the balance of costs and benefits from wildflower borders on multiple ecosystem services


Abstract and Figures

In the face of global biodiversity declines driven by agricultural intensification, local diversification practices are broadly promoted to support farmland biodiversity and multiple ecosystem services. The creation of flower-rich habi- tats on farmland has been subsidized in both the USA and EU to support biodiversity and promote delivery of ecosystem services. Yet, theory suggests that the landscape context in which local diversification strategies are implemented will influence their success. However, few studies have empirically evaluated this theory or assessed the ability to support multiple ecosystem services simultaneously. Here, we evaluate the impact of creating flower-rich habitats in field margins on pollination, pest control, and crop yield over 3 years using a paired design across a landscape gradient. We find general positive effects of natural habitat cover on fruit weight and that flowering borders increase yields by promoting bee visitation to adjacent crops only in landscapes with intermediate natural habitat cover. Flowering borders had little impact on biological control regardless of landscape context. Thus, knowledge of landscape context can be used to target wildflower border placement in areas where they will have the greatest likelihood for success and least potential for increasing pest populations or yield loss in nearby crops.
Content may be subject to copyright.
Cite this article: Grab H, Poveda K, Danforth
B, Loeb G. 2018 Landscape context shifts the
balance of costs and benefits from wildflower
borders on multiple ecosystem services.
Proc. R. Soc. B 285: 20181102.
Received: 17 May 2018
Accepted: 6 July 2018
Subject Category:
Global change and conservation
Subject Areas:
ecological intensification, wildflower strips,
landscape, pollination, biological control,
crop yield
Author for correspondence:
Heather Grab
Electronic supplementary material is available
online at
Landscape context shifts the balance
of costs and benefits from wildflower
borders on multiple ecosystem services
Heather Grab1, Katja Poveda1, Bryan Danforth1and Greg Loeb2
Department of Entomology, Cornell University, Ithaca, NY 14853, USA
Department of Entomology, New York State Agricultural Experiment Station, Cornell University, Geneva,
NY 14456, USA
HG, 0000-0002-1073-8805
In the face of global biodiversity declines driven by agricultural intensification,
local diversification practices are broadly promoted to support farmland
biodiversityand multiple ecosystem services. The creation of flower-rich habi-
tats on farmland has been subsidized in both the USA and EU to support
biodiversity and promote delivery of ecosystem services. Yet, theory suggests
that the landscape context in which local diversification strategies are
implemented will influence their success. However, few studies have
empirically evaluated this theory or assessed the ability to support multiple
ecosystem services simultaneously. Here, we evaluate the impact of creating
flower-rich habitats in field margins on pollination, pest control, and crop
yield over 3 years using a paired design across a landscape gradient. We
find general positive effects of natural habitat cover on fruit weight and that
flowering borders increase yields by promoting bee visitation to adjacent
crops only in landscapes with intermediate natural habitat cover. Flowering
borders had little impact on biological control regardless of landscape context.
Thus, knowledge of landscape context can be used to target wildflower border
placement in areas where they will have the greatest likelihood for success and
least potential for increasing pest populations or yield loss in nearby crops.
1. Introduction
Presently, 40% of the earth’s terrestrial surface is used for agricultural production
[1] and the continued transition of natural habitat to agricultural use is one of the
primary drivers of biodiversity loss worldwide [2]. Balancing the demand for
agricultural productivity with biodiversity conservation is one of the greatest
challenges facing global humanity. However, agricultural intensification can
undermine the very biodiversity and ecosystem services that would otherwise
benefit crop production [3– 5]. Diverse biological communities support many eco-
system services to agriculture, provide resilience to disturbances, and maintain
the capacity to adapt to future changing environments [6,7]. Agricultural intensi-
fication at both local and landscape scales reduces the spatial and temporal
availability of resources required by beneficial organisms, such as pollinators
and natural enemies [8], while crop pests often benefit from a concentration of
host plants [9].
To increase agricultural sustainability, strategies are needed that reduce
conflicts between biodiversity conservation and crop production. Ecological inten-
sification capitalizes on the biodiversity within agroecosystems to achieve
sustainable increases in crop yields by actively managing communities of ecosys-
tem service providers [10,11]. Yet, a major hurdle to the widespread adoption of
ecological intensification strategies is a framework for predicting the contexts in
which they will be successful. Variable effectiveness of these practices may be
due to the landscape context in which they are implemented [12– 14]. The inter-
mediate landscape complexity hypothesis predicts that local management
strategies will be most effective at improving biodiversity and ecosystem services
&2018 The Author(s) Published by the Royal Society. All rights reserved.
on August 2, 2018 from
when established in landscapes that are dominated by agri-
culture but with at least some natural habitat remaining
[9,12]. In landscapes with high natural habitat cover, beneficial
organisms continuously colonize agricultural habitats. Alterna-
tively, in landscapes with very little natural habitat remaining,
source populations of beneficials are too depauperate to recruit
from. However, in landscapes with intermediate amounts of
remaining natural habitat, regional source populations are pre-
sent, but agricultural habitats are not continuously colonized.
Therefore, ecological intensification in these intermediate land-
scapes is expected to produce the greatest effects and early
findings from Europe support these patterns with respect to
enhancing biodiversity [15– 19]. Whether these findings are
also reflected in the delivery of multiple ecosystem services
and crop yield remains unresolved.
Multiple ecosystem services are expected to benefit from
increases in local habitat diversity. For example, local manage-
ment with flowering strips has been shown to increase the
abundance of pollinators and natural enemies of pests in adja-
cent cropland [19–21]. However, few studies have evaluated
the effect of local habitat management on multiple services
simultaneously [22–24], and only one has evaluated their
combined effects on crop yield [25]. Consequently, our under-
standing of the potential interactions between yield-supporting
ecosystem services and ecological intensification strategies that
can simultaneously support them is limited.
Pests can also benefit from natural habitats at the local
and landscape scale [24,26,27], thus management strategies
aimed at increasing ecosystem services may fail to improve
pest control or crop yield [28]. In these cases, although bio-
diversity may be locally improved, yield gaps may trigger
the transition of natural lands to agriculture elsewhere leading
to a net loss for both biodiversity and ecosystem services.
The planting of flower-rich crop borders is subsidized by pol-
icies in both the USA and EU and many governments and
intergovernmental agencies have recently called for agricul-
tural management practices that support biodiversity and
ecosystem services on farms (White House Pollinator Protec-
tion Task Force 2016, IPBES 2017) making the need to ensure
efficient placement and effectiveness more critical than ever.
Here, we evaluate the benefits and potential costs of a
commonly implemented ecological intensification strategy,
the planting of native perennial wildflowers in field margins.
We explore the effect of wildflower borders on crop visitation
by bees, biological control, pest abundance, crop damage,
and crop yield using a paired design in strawberry plantings
with and without a wildflower border on 12 farms across a
landscape gradient. Following the predictions of the inter-
mediate landscape hypothesis, we expect that wildflower
margins will improve ecosystem services and crop production
to a greater extent when implemented in landscapes with
intermediate amounts of natural habitat cover.
2. Methods
(a) Experimental design
We identified 12 farms within the Finger Lakes region of central
New York State that varied in landscape composition (18 61%
natural land cover; electronic supplementary material, figure
S1). On each farm, we established two 10 15 m plots consisting
of five rows of strawberry (var. ‘Jewel’) in the spring of 2012.
Plots were separated by a minimum of 200 m and were randomly
assigned to either a control border or a native perennial wild-
flower border. The distance separating plots represents a
compromise between the relatively small foraging ranges of the
insect communities relevant to strawberry [29] and ensuring
that plot pairs within a farm were within the same landscape
contexts. Composition and management of control borders
were representative of field edge management practices in the
region. Control borders consisted primarily of orchard grass
and were regularly mown over the growing season. Wildflower
borders were approximately 4 m wide by 10 m long and ran
parallel with the crop border consistent with standard imple-
mentations of this management strategy in terms of size and
orientation. Plantings consisted of the following nine US native
perennial species Zizia aurea,Penstemon digitalis,Coreopsis
lanceolata,Potentilla fruticosa,Veronicastrum virginicum,Agastache
neptoides,Silphium perfoliatum,Lobelia siphilitica, and Solidago
canadensis. These species were selected based on their attractive-
ness to bees and natural enemies [13,20,30– 32] and provide
overlapping bloom periods, so that flowers are present through-
out the growing season. When possible, every effort was made to
grow plants from local ecotypes. Both border types were estab-
lished in the autumn of 2012. Plots were managed organically
or involved limited use of pesticides for weed or fungal pathogen
management. Each year, straw mulch was applied to all plots
in the autumn and raked into the row middles in the spring con-
sistent with standard horticultural practices for strawberry in
the northeast. In 2015, one wildflower strip was accidentally
destroyed leaving only 11 site replicates in that year.
At four plots, it was necessary to prevent damage from large
mammalian herbivores by erecting temporary plastic fencing.
Fence gaps were wide enough (3 3 cm) to allow access to
even the largest pollinators (H Grab 2014, personal observation).
In each case, both the control and wildflower treatment plots on
the same farm were fenced.
(b) Landscape
Landscape complexity was characterized using the National
Agricultural Statistics Service Cropland Data Layer for
New York [33] for each year of the study (2013– 2015) in ArcGIS
10.1. The region is characterized by a mix of row crops, fruits
and vegetables, orchard, dairy, old-field habitats, and forest. We
quantified the cover of natural and semi-natural habitats at four
radii from the centre of each plot (500, 750, 1 000, and 1 250 m).
Land cover values were averaged between paired plots in each
farm to generate a single landscape value for each farm in each
year. We fitted separate nonlinear models for each response vari-
able and scale and determined that 750 m was the scale at which
the cover of natural area provided the best fit to the data (based
on AICc values, see electronic supplementary material, table S1).
Previous studies of the pollinators, parasitoids, and pests in this
system have found strong responses to this landscape metric at
similar scales [29,34,35].
(c) Pollinator surveys
The community of pollinators visiting strawberry is dominated
by a diverse fauna of wild bees with honeybees comprising
only 7% of the pollinator community [29]. In the 3 years follow-
ing plot establishment (2013 2015), the visitation rate of bees to
strawberry flowers was estimated by conducting visual surveys
on four dates per plot spanning the duration of crop bloom.
Surveys were carried out between 10:00 and 15:30 on sunny
days with temperatures above 168C. Visitation rate was assessed
using standardized 10 min transects through each plot recording
each bee visit to a strawberry flower. The number of open straw-
berry flowers per square foot was estimated for each plot by
averaging counts of flowers in 1 ft
quadrats in each of the five
rows. Visitation rates per plot were calculated by dividing the Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
total number of visits recorded during the 10 min transects by
the average number of open flowers per square foot.
To better understand the relative importance of the planted
wildflower species, we monitored pollinator visitation rates to
each plant species as well as visits to flowering weeds within
the borders throughout the season in 2015. All flowering plants
within the border were observed for 10 min and total number
of visits per plant species was recorded.
(d) Pest surveys
The primary pest of strawberry in the region is Lygus lineolaris
(Hemiptera: Miridae), a generalist herbivore that feeds on the
seeds of developing strawberry fruits. From 2013 to 2015, the
abundance of L. lineolaris was estimated in each plot immediately
following strawberry flowering by tapping individual strawberry
inflorescences until a total of 24 nymphs were collected or all
inflorescences in the plot were sampled. We chose a target of
24 nymphs per sample because this number allowed us to
accurately estimate parasitism rates using the protocols described
below. Nymph densities were calculated by dividing the number
of nymphs collected by the total number of inflorescences
Because wildflower borders may harbour pest populations
that can spill over into the crop, we estimated the abundance of
L. lineolaris in the wildflower borders compared to the control bor-
ders for an entire growing season in 2015. The abundance of
L. lineolaris adults and nymphs was estimated for each flowering
species present in the wildflower borders by vacuuming (Echo
ES 230 Shred ‘n Vac, Lake Zurich, IL, USA) 25 inflorescences of
each plant species once a week from May to October. Plants
were sampled at the bud, flowering, and seed head phases, so
that our estimate for each species accurately reflected the broad
feeding preferences of L. lineolaris. After sampling a particular
species, all L. lineolaris were returned to the host plant they were
collected from to ensure that the effects of sampling in one
week had little impact on samples in the subsequent weeks.
Sampling also included any weedy flowering species that had
invaded the perennial borders. As some plant species had fewer
than 25 inflorescences on any particular sampling date, the total
number of L. lineolaris collected was divided by the number of
inflorescences vacuumed for each sample. The order of sampling
was randomized for species blooming on a given date. An equiv-
alent number of vacuum samples were obtained from the grassy
margins of control borders for each wildflower species sampled
from its paired wildflower treatment plot.
(e) Parasitism rates
In the study region, the primary natural enemies of L. lineolaris
include a complex of native and introduced parasitoid wasps
in the genus Peristenus [36]. Three species, Peristenus digoneutis
(introduced), Peristenus pallipes (native), and rarely Peristenus
relictus (introduced), are known to attack L. lineolaris; however,
parasitism rates are reduced in landscapes with a high pro-
portion of agricultural land cover [35].Diagnostic PCR assays
were used to simultaneously estimate parasitism rates and para-
sitoid species identity, as they are faster and more accurate than
rearing or dissection [37,38]. Random samples of 24 nymphs
from each sampling period at each site were selected for parasitism
assays. In some cases, fewer than 24 nymphs were collected in a
sampling period. In these cases, all collected nymphs for the
period were processed. In three instances, no nymphs were collected
on a farm in a particular year; therefore, these instances resulted in
only 32 site by year replicates. DNA from nymphs was extracted
using an abbreviated chloroform: isoamyl alcohol protocol devel-
oped by Tilmon & Hoffmann [39]. DNA extractions along with
negative controls were amplified using Peristenus species-specific
primers as in [40]. Using this method, species-specific forward
primers are combined with a genus-specific reverse primer to
amplify a region including ITS1 and ITS2.
(f) Fruit damage and yield
A typical strawberry inflorescence is comprised of a single pri-
mary fruit (king berry), a pair of secondary fruit, and four
tertiary fruit. Strawberries are an aggregate accessory fruit com-
prised of as many as 300 achenes on a primary fruit and 200 on
a secondary fruit [41]. Each achene must be fertilized for the sur-
rounding tissue to develop and an average of four visits per flower
is required to achieve full pollination [42]. Lygus lineolaris nymphs
and adults feed on developing achenes leading to developmental
failure of the surrounding tissues. Fruit weight is highly correlated
with the number of developed undamaged achenes [41]. Fruits
with a high percentage of damaged achenes, either from poorpol-
lination or L. lineolaris feeding, develop with major malformations
that reduce overall yield and marketability [43].
To measure the impact of wildflower borders on crop yield at
each site, 30 flowers were marked and the resulting fruits from
each plot were harvested when ripe and weighed. Owing to
sample processing errors, fruit data are unavailable for one site
in 2013 and one site in 2014. The percentage of poorly pollinated
and damaged achenes was estimated for each fruit. Secondary
fruits were used, as they are less prone to frost damage than
primary fruit and due to their later development are highly
susceptible to damage from L. lineolaris nymph feeding.
(g) Statistical analysis
To evaluate whether wildflower borders had differential effects
across the landscape gradient, we first pooled individual measures
for each variable (ex. pollinator visitation, L. lineolaris, parasitism,
malformations, or weights per individual fruit) by plot and year
averaging over all surveys within a plot in each year. Because the
primary objective of the study was to determine the effectiveness
of the plantings under varying landscape contexts, we calculated
an index of wildflower border effectiveness for each variable. In
this way, we are able to control for the overall variation that
occurs across the landscape gradient and isolate the variation
due to the wildflower border. Absolute values for each variable
on control and wildflower planting across the landscape gradient
are presented in electronic supplementary material, figure S2.
The effectiveness index was calculated by subtracting the average
value observed on the plots with a wildflower border minus the
control divided by the control ((Wildflower 2Control)/Control)
of each farm in each year. The effectiveness index therefore rep-
resents a quantitative measure of the relative effectiveness of the
wildflower planting. Positive values indicate an increase in the
variable of interest on the plot with a wildflower planting com-
pared to the control and negative values indicate the measured
variable was higher on control plantings. We then constructed
linear and nonlinear mixed effects models for each index
(GLMER, R package lme4 [40,44]) with Gaussian error structures.
Fixed effects in each model included year and proportion of com-
bined natural and semi-natural habitat cover as well their
interaction. We constructed linear, logistic, and polynomial
models for each variable and selected the best fit model based on
AICc values. Farm was included as a random effect in each
model to account for the paired experimental design and repeated
measures across years. Additionally, we tested whether site-level
covariates including the distance between the wildflower and con-
trol plot, the total number of flower plant species, and the total
number of native perennial species that established had an effect
on each of the index variables. Each of these site-level covariates
was evaluated in a mixed effects model that included the linear
and polynomial natural habitat cover terms with site as a
random effect. The majority of covariates did not explain a Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
significant portion of the variation in any index and were not
included in the final models.
Differences in L. lineolaris numbers and bee visits to wild-
flower and weedy flowering species within the plot margins
were assessed with generalized linear mixed effects models
with Poisson error distributions. For both variables, plant species
was included as a fixed effect and farm was included as a
random effect. For overall L. lineolaris abundance in wildflower
compared to control borders, an index was computed similar
to those described above. Fixed effects included year and pro-
portion of combined natural and semi-natural habitat cover as
well their interaction.
The contribution of L. lineolaris feeding versus poor pollination
to fruit damage was assessed using a generalized linear mixed
effects model with a Poisson error structure. Fixed effects include
year, average bee visitation, and average L. lineolaris abundance,
as well as, the two-way interactions between year and bee visits,
and year and L. lineolaris abundance. In all models, p-values and
degrees of freedom are calculated based on the Satterthwaite
approximation as implemented in the package lmerTest [45].
3. Results
Wildflowers bloomed from April to November each year begin-
ning in 2013. On average, seven of the nine wildflower species
became established at each site, but no site had fewer than six
species (electronic supplementary material, table S3). In the 3
years following establishment (2013–2015), a total of 5 684
bee visits to strawberry were recorded and 1 307 bee specimens
were collected. Wildbees were the dominant visitors, represent-
ing 95.8% of the community while managed bees (honeybees)
made up only 4.2% of recorded visits. In total, 99 species
were recorded based on net collected specimens.
Following the expectations of the intermediate landscape
hypothesis, the effect of wildflower borders on bee visitation
to the strawberry crop across the landscape gradient was best
described by a second-order polynomial function (AICc
63.86, AICc
¼73.86, AICc
¼73.89; Poly: F
p¼0.01). Wildflower borders increased bee visitation to
strawberry relative to controls only in landscapes with inter-
mediate amounts of natural habitat (figure 1a). On average,
wildflower borders had little effect on bee visitation in the
first 2 years after establishment, but had positive effects in
2015 (t
¼2.48, p¼0.02; figure 1b).
A total of 3 197 L. lineolaris nymphs were collected from
the strawberry plantings over the 3 years of the study. The
effect of wildflower borders on L. lineolaris abundance was
also influenced by the landscape according to a second-
order polynomial function (AICc
¼127.7, AICc
136.3, AICc
¼136.1; Poly: F
¼3.71, p¼0.06). Pest
abundances on plots with a wildflower border were greater
than controls in the landscapes with the least and most natu-
ral habitat cover (figure 2a). In intermediate landscapes,
wildflower borders decreased pest pressure below the levels
of control plots. The abundance of L. lineolaris on plots with
a wildflower border differed across the years (F
p¼0.003) and was greatest in 2014 (t
¼4.67, p,0.001;
electronic supplementary material, figure S3).
Parasitism assays revealed an overall parasitism rate of
18%. Three parasitoid species were detected with the intro-
duced P. digoneutis being the dominant natural enemy (96.7%
of parasitism events) and the other two species, P. pallipes
(native, 2.8%) and P. relictus (introduced, 0.05%), represented
at low levels. The effectiveness of wildflower borders across
the landscape gradient on parasitism largely mirrored the pat-
tern observed for pest abundances (figure 2b). Again a
polynomial function best fit the data (AICc
¼126.5, AICc
¼126.4; Poly: F
¼4.06, p¼
0.06). However, parasitism rates followed a pattern across
years similar to bee visitation; achieving the highest values
on wildflower plots relative to controls in 2015 (t
p¼0.02; electronic supplementary material, figure S4).
Sampling L. lineolaris within the plot margins themselves
revealed that densities of L. lineolaris were higher in wildflower
borders compared to control borders throughout the season
(WF: F
¼30.47, p¼0.0003). Although there were no differ-
ences in the number of L. lineolaris collected in control margins
between the landscape types, wildflower margins in land-
scapes with intermediate natural habitat cover supported
greater numbers of L. lineolaris relative to landscapes with
either low or high proportions of natural habitat (figure 3a,
2013 2014 2015
0.2 0.3 0.4 0.5 0.6
ortion natural habitat
effect on bee visitation to crop
Figure 1. Effectiveness of wildflower (WF) borders relative to control (C) plots ((WF 2C)/C) for bee visitation to strawberry flowers (a) in relation to the proportion
of natural land cover in a 750 m radius around each site across all 3 years of the study and (b) in each of the study years following wildflower establishment in 2012.
In (a), shaded areas represent 95% confidence intervals. Asterisk in (b) indicates values different from 0 at p,0.05 based on post hoc contrast tests. Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
¼5.42, p¼0.052). In 2015, each wildflower species in the
wildflower border was surveyed for its attractiveness to both
bees and L. lineolaris. The number of L. lineolaris supported by
different species of wildflowers varied (F
¼1.94, p¼0.03)
as did the number of bee visitors to each species (F
p¼0.0001; figure 3b). While some species supported
moderate numbers of both L. lineolaris and pollinators
(ex. Penstemon), the most attractive species were different for
pests (ex. Erigeron) and pollinators (ex. Silphium).
Both lack of pollination by bees and feeding by
L. lineolaris cause malformations to developing strawberry
fruit resulting in yield loss. The relative importance of
L. lineolaris abundance versus bee visitation in predicting
malformations varied across study years (L. lineolaris
year: F
¼36.03, p,0.001; bee year: F
¼33.26, p,
0.001). In both 2013 and 2014, L. lineolaris abundance was
the only significant predictor of fruit malformations and
increasing nymph abundance was associated with greater
malformations (2013 L. lineolaris:z¼2.98, p¼0.002, bee:
z¼0.22, p¼0.823; 2014 L. lineolaris:z¼2.17, p¼0.029,
bee: z¼20.21, p¼0.829). In 2015, both groups predicted
malformations; although, bee visitation had a stronger
effect in reducing malformations (bee: z¼22.74, p¼0.006;
L. lineolaris:z¼2.24, p¼0.025; electronic supplementary
material, figure S5) consistent with increasing positive effect
of wildflowers on bees over the 3-year study.
The difference in fruit malformations on plots with a
wildflower border compared to controls was best explained
by a polynomial response to landscape (AICc
¼72.35, AICc
¼72.58; Poly: F
¼3.48, p¼
0.07). Malformations caused by both poor pollination and
L. lineolaris feeding were greatest on plots with a wildflower
border relative to control plots in landscapes with the
least natural land cover (figure 4a). Landscapes with inter-
mediate cover of natural habitat had the greatest reduction
in malformations relative to control plots.
For fruit weight, a polynomial function also best described
the relationship between wildflower border effectiveness and
landscape (AICc
¼20.33, AICc
¼7.42, AICc
8.52; Poly: F
¼8.68, p¼0.008). In the landscapes with the
effect on L. lineolaris
0.2 0.3 0.4 0.5 0.6
proportion natural habitat
0.2 0.3 0.4 0.5 0.6
proportion natural habitat
effect on parasitism rate
Figure 2. Effectiveness of wildflower (WF) borders relative to control (C) plots ((WF 2C)/C) for (a) the number of L. lineolaris nymphs and (b) the parasitism rate
of nymphs. Shaded areas represent 95% confidence intervals.
bee visits
L. lineolaris per sample
0.2 0.3 0.4 0.5 0.6
effect on L. lineolaris in wildflowers
proportion natural habitat
Figure 3. The average number of L. lineolaris nymphs collected within the wildflower borders (a) relative to control borders and (b) on various wildflower species
(planted species with *) relative to the number of bees visiting each wildflower species. Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
least natural cover, plots with a wildflower border had lower
yields than control plots. By contrast, plots with a wildflower
border had higher yields than controls in landscapes with
intermediate amounts of natural land cover (figure 4b). This
difference between wildflower and control borders decreased
in landscapes with the most natural cover.
4. Discussion
Ecological intensification strategies including the creation of
flower-rich habitats on agricultural lands have been promoted
as a practice to support farmland biodiversity and encourage
the delivery of ecosystem services (White House Initiative,
EU Initiative, IPBES report 2016 [12,13,46– 48]). In the USA,
these practices are subsidized at a rate of $57 million per year
through the Conservation Reserve Program (CRP)and Environ-
mental Quality Incentives Program (EQIP) [49]. Yet, few studies
have evaluated the effectiveness of these practices across a
gradient of landscape contexts or on multiple ecosystem ser-
vices simultaneously, impeding our ability to effectively
implement these practices. Here, we evaluate the impact of
wildflower borders on pollination, pest control, and crop
yield across a landscape gradient and find that while flowering
crop borders can be successful in some contexts, landscapes that
are the most agriculturally intensified will require larger scale
more coordinated conservation approaches.
In terms of supporting crop pollination services, our find-
ings support the prediction of the intermediate landscape
hypothesis [9,12] with bee visitation to crop flowers increas-
ing with the addition of local wildflower borders according
to a polynomial function which peaked in landscapes with
intermediate cover of natural habitats. Interestingly, the inter-
mediate values of land cover that correspond with success of
the wildflower borders in supporting ecosystem services are
shifted strongly towards higher values of natural habitat
compared to those originally proposed by Tscharntke et al.
[12] for supporting biodiversity in European landscapes.
Tscharntke et al. proposed that wildflower borders would
have the strongest effects on biodiversity in landscapes with
1–20% non-crop habitat. In our study, wildflower habitats
were the most successful at increasing the delivery of
ecosystem services in landscapes with 25–55% natural habitat
cover. These differences in threshold values may reflect the
differences in the composition of the current dominant natural
habitat covers (grasslands in Europe, forest in the northeastern
USA) or differences in the history of large-scale agricultural
land use between the regions (thousands of years in Europe,
hundreds in the northeastern USA). Alternatively, the shift
in response curves may represent fundamentally different
landscape optima for supporting ecosystem services compared
to biodiversity with local management practices. One mechan-
ism that may lead to this shift is that flowering crop borders
continue to support increased abundance of functionally
important species past the optima at which species richness
is maximized. Delivery of ecosystem services has been shown
to be driven by the abundance of functionally important
taxa rather than community diversity [50,51]. Indeed, the
effectiveness of supplementing floral resources for enhancing
parasitism rates in California vineyards was greatest when
landscapes contained 20–60% natural habitat [52], supporting
the idea that a higher threshold of natural habitat is required for
benefits to ecosystem services. These results imply that policies
attempting to prioritize areas for either conservation or ecosys-
tem services management need to be tailored, as the response
curves may differ.
For pest pressure, the shape of the relationship between
landscape and effectiveness of flowering crop borders is also
predicted by the intermediate landscape hypothesis, yet the
curve is shifted strongly above zero. This shift indicates a cost
of wildflower borders not predicted by the intermediate land-
scape hypothesis. In landscapes with both the least and
greatest natural habitat cover, plots with a wildflower border
had greater pest abundances than those with a control border.
Although flowering borders are intended to target beneficial
insects, generalist pests like L. lineolaris are also able to take
advantage ofthese additional resources [20,24,26]. We observed
greater numbers of L. lineolaris in wildflower borders in moder-
ately agricultural landscapes compared with more complex
landscapes. This result likely reflects the lower propensity for
L. lineolaris to disperse in agriculturally dominated landscapes
[53] and may lead to increased spillover of pests from the
wildflowers to the crop in the following spring.
effect on fruit damage
0.2 0.3 0.4 0.5 0.6
ortion natural habitat
0.2 0.3 0.4 0.5 0.6
ortion natural habitat
effect on fruit weight
Figure 4. Effectiveness of wildflower (WF) borders relative to control (C) plots ((WF 2C)/C) for (a) the malformations to and (b) the weight of strawberry fruits.
Shaded areas represent 95% confidence intervals. Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
The relationship between landscape and effect ofwildflower
borders on parasitism was the opposite of our predictions based
on the intermediate landscape hypotheses. Rather, wildflower
plots with the greatest increases in parasitism relative to con-
trols were in the same landscape contexts that also had the
greatest increases in pest abundances. In this case, parasitoid
responses to wildflower borders may be obscured by density-
dependent responses to host abundance [54]. However, other
studies have found positive effects of wildflower borders on
biological control of pests [20,55], particularly when the pest
was not able to use the flowering crop border as alternative
hosts. Effects of wildflower strips on parasitism rates may
also have lagged behind effects on herbivores as L. lineolaris
had the greatest increase in plots with a wildflower border in
2014 while parasitism increased most strongly in 2015.
The lag in time between the establishment of wildflower
borders and the response of the beneficial insect community
can influence the cost–benefit ratio for farmers implementing
these borders with the goal of enhancing ecosystem services
[31]. These lags are particularly important for annual crops or
short-term perennial crops like strawberry, which are grown
in the same field for only 2– 5 years. In our study, increases in
bee visitation and parasitism rates occurred in the third year fol-
lowing establishment. Although a number of studies report
responses within the first year following establishment
[19,20,32,56], the majority of these studies report on commu-
nities within wildflower plantings rather than in adjacent crop
habitats [19,32] while others use annual plants in their borders
[56]. These results suggest that other border types may be more
appropriate for annual or rotating crops or that growers should
establish flowering borders before the crop.
Ultimately, the benefits of ecological intensification prac-
tices like flowering crop borders can be measured in terms
of increases in crop yields. Yet, while many studies evaluate
the effects of wildflower borders on bee visitation or natural
enemy communities, few assess the impact on crop damage
and the final effect on yield (but see [25,31]). Regardless of
crop border treatment, natural habitat cover had a generally
positive effect on fruit weight. When comparing border treat-
ments using the effectiveness index, wildflower borders
reduced fruit damage and increased yield most strongly in
landscapes with intermediate natural habitat cover, showing
that ecological intensification practices can successfully
improve crop productivity. However, in landscapes with
either high or low natural habitat cover, wildflower borders
tended to increase fruit damage and reduce yield. In these
same landscapes, wildflower borders had little effect on bee
visitation and increased pest abundances, suggesting that
the success of ecological intensification practices will be
dependent on the context in which they are implemented.
Although flowering crop borders had positive yield effects
at intermediate levels of landscape complexity, our study indi-
cates that wildflower border management is not without costs
imposed by increased herbivore pressure when implemented
outside of the optimal landscape window. Yet, increases in her-
bivore pressure were only observed in landscapes where
wildflower borders had the least success in improving bee
visitation. In all landscape contexts, efforts should focus on
selecting wildflower species that are not preferred by crop
pests [21,57] and on managing weedy species that support
high numbers of crop pests. Management practices that
reduce these weedy species canalso increase the establishment
rates of planted species [58]. In simple landscapes where wild-
flower borders have few benefits, efforts should focus on the
conservation of the remaining natural habitat and restoration
of larger areas of natural habitat rather than on field-scale
diversification strategies.
Because of the importance of landscape in mediating the
success of ecological intensification practices like wildflower
crop borders, we propose that landscape context should be
explicitly considered in large policy initiatives that subsidize
the creation of flowering habitats on farmlands. Ranking cri-
teria that incorporate landscape along with other site-level
criteria including slope, proximity to waterways or wetlands,
and other factors will allow land managers and conservation
practitioners to select appropriate conservation measures for
a given site. By implementing these metrics, limited resources
for establishing habitat for beneficial insect conservation can
be targeted to areas where they will have the greatest likeli-
hood for success with the least potential for increasing pest
populations or yield loss in nearby crops.
Data accessibility. Data associated with this manuscript have been depos-
ited in the Dryad Digital Repository:
dryad.425kd01 [59].
Authors’ contributions. H.G., K.P., and G.L. designed experiments. B.D.
provided materials for laboratory assays. H.G. collected data, con-
ducted analyses, and wrote the first draft of the manuscript. All
authors contributed substantially to revisions.
Competing interests. We declare we have no competing interests.
Funding. This work was supported in part by a Northeast SARE
graduate student grant to H.G. (GNE12-036).
Acknowledgements. The authors thank David Kleijn and Matthias
Albrecht for helpful comments on an earlier version of the manu-
script. Thanks to past undergraduate field assistants and to Ellie
McCabe, Alison Wentworth, and Steve Hesler for their assistance
in the field.
1. Foley JA et al. 2011 Solutions for a cultivated
planet. Nature 478, 337– 342. (doi:10.1038/
2. Newbold T et al. 2015 Global effects of land use on
local terrestrial biodiversity. Nature 520, 4550.
3. Kremen C, Williams NM, Thorp RW. 2002 Crop
pollination from native bees at risk from agricultural
intensification. Proc. Natl Acad. Sci. USA 99,
16 812–16 816. (doi:10.1073/pnas.262413599)
4. Thies C, Tscharntke T. 1999 Landscape structure and
biological control in agroecosystems. Science 285,
893895. (doi:10.1126/science.285.5429.893)
5. Rusch A et al. 2016 Agricultural landscape
simplification reduces natural pest control: a
quantitative synthesis. Agric. Ecosyst. Environ. 221,
198204. (doi:10.1016/j.agee.2016.01.039)
6. Cardinale BJ et al. 2012 Biodiversity loss and its
impact on humanity. Nature 489, 326. (doi:10.
7. Hooper DU et al. 2012 A global synthesis reveals
biodiversity loss as a major driver of ecosystem
change. Nature 486, 105– 108. (doi:10.1038/
8. Schellhorn NA, Gagic V, Bommarco R. 2015 Time
will tell: resource continuity bolsters ecosystem
services. Trends Ecol. Evol. 30, 524– 530. (doi:10.
9. Tscharntke T et al. 2012 Landscape moderation of
biodiversity patterns and processes—eight Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
hypotheses. Biol. Rev. 87, 661– 685. (doi:10.1111/j.
10. Bommarco R, Kleijn D, Potts SG. 2013 Ecological
intensification: harnessing ecosystem services for
food security. Trends Ecol. Evol. 28, 230– 238.
11. Pywell RF, Heard MS, Woodcock BA, Hinsley S,
Ridding L, Nowakowski M, Bullock JM. 2015
Wildlife-friendly farming increases crop yield:
evidence for ecological intensification. Proc. R. Soc.
B282, 20151740. (doi:10.1098/rspb.2015.1740)
12. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter
I, Thies C. 2005 Landscape perspectives on
agricultural intensification and biodiversity—
ecosystem service management. Ecol. Lett. 8,
857–874. (doi:10.1111/j.1461-0248.2005.00782.x)
13. Isaacs R, Tuell J, Fiedler A, Gardiner M, Landis D.
2009 Maximizing arthropod-mediated ecosystem
services in agricultural landscapes: the role of native
plants. Front. Ecol. Environ. 7, 196– 203. (doi:10.
14. Kleijn D, Rundlo
¨f M, Scheper J, Smith HG,
Tscharntke T. 2011 Does conservation on farmland
contribute to halting the biodiversity decline?
Trends Ecol. Evol. 26, 474– 481. (doi:10.1016/j.tree.
15. Concepcio
´n ED, Dı
´az M, Baquero RA. 2008 Effects of
landscape complexity on the ecological effectiveness
of agri-environment schemes. Landsc. Ecol. 23,
135–148. (doi:10.1007/s10980-007-9150-2)
16. Concepcio
´nEDet al. 2012 Interactive effects of
landscape context constrain the effectiveness of
local agri-environmental management. J. Appl. Ecol.
49, 695–705.
17. Batary P, Baldi A, Kleijn D, Tscharntke T. 2011
Landscape-moderated biodiversity effects of agri-
environmental management: a meta-analysis.
Proc. R. Soc. B 278, 1894– 1902. (doi:10.1098/rspb.
18. Scheper J, Holzschuh A, Kuussaari M, Potts SG,
¨f M, Smith HG, Kleijn D. 2013 Environmental
factors driving the effectiveness of European agri-
environmental measures in mitigating pollinator
loss—a meta-analysis. Ecol. Lett. 16, 912–920.
19. Scheper J et al. 2015 Local and landscape-level
floral resources explain effects of wildflower strips
on wild bees across four European countries. J. Appl.
Ecol. 52, 1165–1175. (doi:10.1111/1365-2664.
20. Blaauw BR, Isaacs R. 2015 Wildflower plantings
enhance the abundance of natural enemies and
their services in adjacent blueberry fields. Biol.
Control. 91, 94– 103. (doi:10.1016/j.biocontrol.
21. Tschumi M, Albrecht M, Collatz J, Dubsky V, Entling
MH, Najar-Rodriguez AJ, Jacot K. 2016 Tailored
flower strips promote natural enemy biodiversity
and pest control in potato crops. J. Appl. Ecol. 53,
1169–1176. (doi:10.1111/1365-2664.12653)
22. Otieno M, Woodcock BA, Wilby A, Vogiatzakis IN,
Mauchline AL, Gikungu MW, Potts SG. 2011 Local
management and landscape drivers of pollination
and biological control services in a Kenyan agro-
ecosystem. Biol. Conserv. 144, 2424– 2431. (doi:10.
23. Balzan MV, Bocci G, Moonen AC. 2016 Utilisation of
plant functional diversity in wildflower strips for the
delivery of multiple agroecosystem services.
Entomol. Exp. Appl. 158, 304319. (doi:10.1111/
24. Mccabe E, Loeb G, Grab H. 2017 Responses of crop
pests and natural enemies to wildflower borders
depends on functional group. Insects 8,18.
25. Sutter L, Albrecht M, Jeanneret P. 2017 Landscape
greening and local creation of wildflower strips and
hedgerows promote multiple ecosystem services.
J. Appl. Ecol. 55, 612 620. (doi:10.1111/1365-
26. Balzan MV, Bocci G, Moonen AC. 2014 Augmenting
flower trait diversity in wildflower strips to optimise
the conservation of arthropod functional groups for
multiple agroecosystem services. J. Insect Conserv.
18, 713728. (doi:10.1007/s10841-014-9680-2)
27. Midega CAO, Jonsson M, Khan ZR, Ekbom B. 2014
Effects of landscape complexity and habitat
management on stemborer colonization, parasitism
and damage to maize. Agric. Ecosyst. Environ. 188,
289293. (doi:10.1016/j.agee.2014.02.028)
28. Tscharntke T et al. 2016 When natural habitat fails
to enhance biological pest control—five
hypotheses. Biol. Conserv. 204, 449–458. (doi:10.
29. Connelly H, Poveda K, Loeb G. 2015 Landscape
simplification decreases wild bee pollination services
to strawberry. Agric. Ecosyst. Environ. 211, 51– 56.
30. Tuell JK, Fiedler AK, Landis D, Isaacs R, Tuell JK,
Fiedler AK, Landis D. 2008 Visitation by wild and
managed bees (Hymenoptera: Apoidea) to Eastern
U.S. Native plants for use in conservation programs.
Environ. Entomol. 37, 707–718. (doi:10.1603/0046-
31. Blaauw BR, Isaacs R. 2014 Flower plantings increase
wild bee abundance and the pollination services
provided to a pollination-dependent crop. J. Appl.
Ecol. 51, 890898. (doi:10.1111/1365-2664.12257)
32. Williams NM et al. 2015 Native wildflower plantings
support wild bee abundance and diversity in
agricultural landscapes across the United States.
Ecol. Appl. 25, 21192131. (doi:10.1890/14-
33. USDA-NASS. 2014 2013 USDA National Agricultural
Statistics Service Cropland Data Layer.
34. Renauld M, Hutchinson A, Loeb G, Poveda K,
Connelly H. 2016 Landscape simplification constrains
adult size in a native ground-nesting bee. PLoS ONE
11, e0150946.
35. Grab H, Danforth B, Poveda K, Loeb G. 2018
Landscape simplification reduces classical biological
control and crop yield. Ecol. Appl. 28, 348– 355.
36. Day WH. 1996 Evaluation of biological control of the
tarnished plant bug (Hemiptera: Miridae) in alfalfa
by the introduced parasite Peristenus digoneutis
(Hymenoptera: Braconidae). Environ. Entomol. 25,
512–518. (doi:10.1093/ee/25.2.512)
37. Tilmon KJ, Danforth BN, Day WH, Hoffmann MP.
2000 Determining parasitoid species composition in
a host population: a molecular approach.
Ann. Entomol. Soc. Am. 93, 640 647.
38. Ashfaq M, Braun L, Hegedus D, Erlandson M. 2004
Estimating parasitism levels in Lygus spp.
(Hemiptera: Miridae) field populations using
standard and molecular techniques. Biocontrol. Sci.
Technol. 14, 731– 735. (doi:10.1080/
39. Tilmon KJ, Hoffmann MP. 2003 Biological control of
Lygus lineolaris by Peristenus spp. in strawberry.
Biol. Control. 26, 287– 292. (doi:10.1016/S1049-
40. Gariepy TD, Broadbent AB, Ethier S, Kuhlmann U,
Gillott C, Erlandson M. 2008 Detection of European
Peristenus digoneutis loan in mirid populations in
southern Ontario. Biocontrol. Sci. Technol. 18,
583–590. (doi:10.1080/09583150802100197)
41. Webb RA, Purves JV, White BA. 1974 The
components of fruit size in strawberry. Sci. Hortic.
(Amsterdam) 2, 165– 174. (doi:10.1016/0304-
42. Chagnon M, Gingras J, de Oliveira D. 1989 Effect of
honey bee (Hymenoptera: Apidae) visits on the
pollination rate of strawberries. J. Econ. Entomol.
82, 1350–1353. (doi:10.1093/jee/82.5.1350)
43. Schaefers GA. 1980 Yield effects of tarnished plant
bug feeding on June-bearing strawberry varieties in
New York State. J. Econ. Entomol. 73, 721– 725.
44. Bates D, Ma
¨chler M, Bolker B, Walker S. 2014 Fitting
linear mixed-effects models using lme4. J. Stat.
Softw.,eprint arXiv:1406.5823 67, 51. (doi:10.
45. Kuznetsova A, Brockhoff PB, Christensen RHB. 2016
lmerTest: tests in linear mixed effects models.
46. Dicks LV et al. 2016 Ten policies for pollinators.
Science 354, 975–976. (doi:10.1126/science.
47. Fiedler AK, Landis DA, Wratten SD. 2008
Maximizing ecosystem services from conservation
biological control: the role of habitat management.
Biol. Control 45, 254– 271. (doi:10.1016/j.
48. Wratten SD, Gillespie M, Decourtye A, Mader E,
Desneux N. 2012 Pollinator habitat enhancement:
benefits to other ecosystem services. Agric. Ecosyst.
Environ. 159, 112– 122. (doi:10.1016/j.agee.2012.
49. USDA-FSA. 2017 Conservation Reserve Program
Monthly Summary—June 2017.
50. Kleijn D et al. 2015 Delivery of crop pollination
services is an insufficient argument for wild
pollinator conservation. Nat. Commun. 6, 7414.
51. Winfree R, Fox JW, Williams NM, Reilly JR, Cariveau
DP. 2015 Abundance of common species, not
species richness, drives delivery of a real-world Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
ecosystem service. Ecol. Lett. 18, 626– 635. (doi:10.
52. Wilson H, Miles AF, Daane KM, Altieri MA. 2017
Landscape diversity and crop vigor outweigh influence
of local diversification on biologicalcontrol of avineyard
pest. Ecosphere 8, e01736. (doi:10.1002/ecs2.1736)
53. Mazzi D, Dorn S. 2012 Movement of insect
pests in agricultural landscapes. Ann. Appl. Biol. 160,
97– 113. (doi:10.1111/j.1744-7348.2012.00533.x)
54. May RM, Hassell MP, Anderson RM, Tonkyn DW.
1981 Density dependence in host-parasitoid models.
J. Anim. Ecol. 50, 532 543.
55. Jonsson M, Straub CS, Didham RK, Buckley HL, Case
BS, Hale RJ, Gratton C, Wratten SD. 2015
Experimental evidence that the effectiveness of
conservation biological control depends on
landscape complexity. J. Appl. Ecol. 52, 1274– 1282.
56. Feltham H, Park K, Minderman J, Goulson D. 2015
Experimental evidence that wildflower strips
increase pollinator visits to crops. Ecol. Evol. 5,
3523–3530. (doi:10.1002/ece3.1444)
57. Tschumi M, Albrecht M, Entling MH, Jacot K. 2015 High
effectiveness of tailored flower strips in reducing pests
and crop plant damage. Proc. R. Soc. B 282, 20151369.
58. Benvenuti S, Bretzel F. 2017 Agro-biodiversity
restoration using wildflowers: what is the
appropriate weed management for their long-term
sustainability? Ecol. Eng. 102, 519–526. (doi:10.
59. Grab H, Poveda K, Danforth B, Loeb G. 2018 Data
from: Landscape context shifts the balance of costs
and benefits from wildflower borders on multiple
ecosystem services Dryad Digital Repository (doi:10.
5061/dryad.425kd01) Proc. R. Soc. B 285: 20181102
on August 2, 2018 from
... While leaf damage may have been lowest and flower visits highest in crops adjacent to our wildflower plots, differences were slight and our time-lapse camera work showed no clear egg-predation benefits associated with this treatment. What others have found: Other researchers have found that wildflower plantings can increase invertebrate-mediated agroecological services and/or production in adjacent crops, at least in certain landscapes, see for example, Blaauw and Isaacs (2015) working with blueberries and Grab et al. (2018) with strawberries. Lövei and Ferrante (2017) review the use of sentinel prey as a way of measuring services. ...
... Angelella et al. (2021) found that wildlife flower plantings increased crop set in strawberries and winter squash, but that these benefits were decreased in the presence of Honey Bees. Grab et al. (2018) noted improved strawberry production adjacent to wildflower plantings, but only in landscapes with intermediate levels of natural habitat. Intriguingly, Pywell et al. (2015) found that crop yields (wheat, rape, and field beans) improved relatively slowly with the most dramatic results only apparent five or more years after edge management (including wildflower additions). ...
... What others have found: Various authors have predicted and/or documented that habitat additions, such through wildflower planting, have the largest effect in landscapes with intermediate levels of semi-natural habitat (e.g., Tscharntke et al. 2005, Isaacs et al. 2009, Jonsson et al. 2015, Grab et al. 2018. Schmidt et al. (2008) and Martin et al. (2016) report estimates of the scale at which landscape composition affects various invertebrates. ...
Technical Report
Full-text available
This report details five years of work following the invertebrates of wildflower trial meadows at the Hudson Valley Farm Hub, near Hurley NY. For accompanying botanical report, please see:
... Research on supplementing natural enemies' use of pollen and nectar from flower plantings has largely been developed in parallel to the literature on flower plantings for pollinators (Fiedler et al., 2008;Wratten et al., 2012) and shown potential to improve pest control in adjacent crop fields (Albrecht et al., 2020). Only recently has the potential for multifunctional habitats that benefit both pollinators and natural enemies been explored (Balzan et al., 2016;Morandin et al., 2016;Campbell et al., 2017;Sutter et al., 2018a;Grab et al., 2018). For this reason, it remains largely unclear to what extent flower plantings targeting pollinators enhance natural enemies to crop pests and pest control services. ...
... Lace bugs are minor pests on shrubs and trees that were not found in the adjacent crops, while Lygus bugs are important pests in several field crops ( Wildflower plantings have previously been shown to harbor more Lygus bugs than control field borders (McCabe et al., 2017;Grab et al., 2018); however, those studies were in a different climatic region and landscape context. Lygus bug numbers were low in adjacent watermelon and tomato fields compared to borders irrespective of treatment and while more abundant in crop fields next to wildflower plantings, their densities were too low to be analyzed statistically. ...
Full-text available
Flower strips are advocated as a strategy to promote beneficial insects as well as the services they deliver to adjacent crops. Flower strips have, however, often been developed separately for pollinators and natural enemies and, additionally, little consideration has been given to effects on insect herbivores. We sampled insect herbi-vores, their natural enemies and parasitism of pest eggs using vacuum sampling, sticky cards and egg cards in nine pairs of bee-attractive wildflower plantings and control field borders, as well as in adjacent tomato and watermelon crop fields in Yolo County, California 2015-2016. Control field borders had a higher total number of herbivores on sticky traps than did wildflower plantings, a pattern that was driven by more aphids, hoppers, psyllids and whiteflies, whereas wildflower plantings had more lace bugs and Lygus bugs. The total number of herbivores in the adjacent crop fields did not differ between treatments, but there were more leaf beetles near (at 10 m but not 50 m from) wildflower plantings. Control field borders had a higher total number of predators, driven by more big-eyed bugs, lady beetles and minute pirate bugs, whereas spiders were more common in wildflower plantings. The total number of predators in adjacent crop fields was, however, higher in those next to wildflower plantings, which was driven by more minute pirate bugs. Parasitoid wasps were more common in wildflower plantings and at 10 m but not 50 m into adjacent crop fields. Stink bug egg parasitism rate did not differ between treatments, either in the borders or in the crop fields. In conclusion, wildflower plantings clearly affect the insect herbivore and natural enemy community, but do so in a highly taxon-specific manner, which can lead to both positive and negative outcomes for pest control as a result.
... Similarly, studies of viruses that infect bees have similarly focused on the honeybee (Daughenbaugh et al., 2021). Grab et al., 2018;Olson et al., 2021) and some from Europe (e.g., Krimmer et al., 2019;Morrison et al., 2021;Pfister et al., 2018). ...
Full-text available
Since mid-1990s, concerns have increased about a human-induced "pollination crisis." Threats have been identified to animals that act as plant pollinators, plants pollinated by these animals, and consequently human well-being. Threatening processes include loss of natural habitat, climate change, pesticide use, pathogen spread, and introduced species. However, concern has mostly been during last 10-15 years and from Europe and North America, with Australasia, known as Down-Under, receiving little attention. So perhaps Australasia has "dodged the bullet"? We systematically reviewed the published literature relating to the "pollination crisis" via Web of Science, focusing on issues amenable to this approach. Across these issues, we found a steep increase in publications over the last few decades and a major geographic bias towards Europe and North America, with relatively little attention in Australasia. While publications from Australasia are underrepresented, factors responsible elsewhere for causing the "pollination crisis" commonly occur in Australasia, so this lack of coverage probably reflects a lack of awareness rather than the absence of a problem. In other words, Australasia has not "dodged the bullet" and should take immediate action to address and mitigate its own "pollination crisis." Sensible steps would include increased tax-onomic work on suspected plant pollinators, protection for pollinator populations threatened with extinction, establishing long-term monitoring of plant-pollinator relationships , incorporating pollination into sustainable agriculture, restricting the use of various pesticides, adopting an Integrated Pest and Pollinator Management approach, and developing partnerships with First Nations peoples for research, conservation and management of plants and their pollinators. Appropriate Government policy, funding and regulation could help.
... However, we decided to include the origin treatment on the same roof following a "paired" design in order to control for differences in roof characteristics which have been shown to influence arthropod abundance in the region (Fabián et al., 2021). Moreover, paired designs are particularly useful to disentangle the effects of a categorical factor across an environmental gradient, in our case plant origin across an urbanization gradient (Grab et al., 2018). ...
... Pest control strategies against TPB mainly rely on the use of broad-spectrum insecticides [5], which threaten non-targeted beneficial organisms [6,7]. Alternatively, several biological control agents (e.g., entomopathogenic fungi, parasitoids, and predators) may contribute to the control of TPB populations [8][9][10][11][12][13]. However, the role of the natural enemies of the TPB has been mainly overlooked. ...
Full-text available
The tarnished plant bug, Lygus lineolaris, is a major strawberry pest. Only marginally effective control methods exist to manage this pest. Various predators attack L. lineolaris, but their potential is overlooked. In this study, we explore the potential of two omnivorous predators of the tarnished plant bug: the damsel bug, Nabis americoferus, and the minute pirate bug, Orius insidiosus. Firstly, the predation rate of these predators was measured in laboratory tests. Secondly, their potential release rates and release periods were determined in the field using strawberry plants. The results show that N. americoferus feeds on all nymphal stages and adults of the tarnished plant bug, while O. insidiosus attacks only smaller nymphs (up to the N2 stage). In the field, all tested densities of N. americoferus (0.25, 0.5, and 0.75 individual/plant) reduced the population of the tarnished plant bug for several weeks compared with the control treatment, but the effect of O. insidiosus alone was marginal. Additionally, for all the release periods tested, Nabis americoferus was efficient in reducing the pest population. These results demonstrate the potential of N. americoferus to control the tarnished plant bug in strawberry fields. We discuss the possible application of these results for establishing an effective and economically viable biological control strategy.
... Very few studies have sought to elucidate how natural enemies respond to both landscape effects and local management. However, we know from previous work that landscape complexity and local management interact to affect insect diversity (Batáry et al., 2010;Chaplin-Kramer et al., 2011;Tscharntke et al., 2012a;Shackelford et al., 2013) and also ecosystem services (Grab et al., 2018;Perez-Alvarez et al., 2019;Poveda et al., 2019). Within the push-pull system, previous studies have shown stemborer infestations are differentially mediated across a landscape gradient (Kebede et al., 2018), with greater damage done in simple landscapes. ...
Farmers looking to maximize ecosystem services often use diversification practices on their fields to increase abundance and diversity of insect natural enemies. These practices affect functional traits of natural enemies such as body size that can play an important role in their effectiveness as biological control agents. However, landscape features out of the control of farmers might also affect functional traits of natural enemies and their herbivores, including land use surrounding farms. There have been few studies elucidating how landscape complexity and local diversity interact to affect functional traits, and ultimately ecosystem services such as predation on herbivore pests. We examined combined effects of landscape complexity and a local management practice (push‐pull) on lady beetle size, and its consequences for egg predation of lepidopteran pests in Kenyan smallholder maize farms. Cheilomenes sulphurea (Olivier) (Coleoptera: Coccinellidae), a potential predator of the invasive fall armyworm, Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae), was collected in push‐pull and control fields along a landscape gradient. We measured beetle size and conducted feeding assays with fall armyworm eggs. We found that female beetles had larger bodies in landscapes with greater complexity. Predation rates not only increased as a response to beetle size but also in response to landscape complexity, suggesting it is not just size that determines predation. Surprisingly, we did not find any effect of the local management practice or its interaction on functional traits or predation rates. Our study suggests that landscape complexity could benefit pest control through two mechanisms: (1) increase in predator body size, leading to higher predation rates; and (2) changes in predator behavior as a function of landscape characteristics – increasing egg predation. Further studies on these mechanisms would allow deeper understanding of landscape simplification's effect on ecosystem services, as mediated by morphological and behavioral traits, and help us harness these traits to increase biological control.
... Recent syntheses suggest that on-farm wildflower plantings may be more likely than landscape-scale semi-natural habitat to enhance pest regulation services (Albrecht et al., 2020;Duarte et al., 2018;Karp et al., 2018), while the reverse is expected for pollination services (Albrecht et al., 2020;Kennedy et al., 2013;Lowe et al., 2021;Nicholson et al., 2020). Furthermore, the effectiveness of wildflower plantings may depend on the amount of semi-natural habitat in the broader landscape (Kleijn et al., 2011;Tscharntke et al., 2005), though empirical evidence for these context dependencies has been mixed (Albrecht et al., 2020;Grab et al., 2018). Our ability to resolve patterns of context-dependency and contrasting outcomes among regulating services remains limited by a lack of studies that measure both pest control and pollination services together in the same cropping system. ...
Biodiversity-friendly farming practices may create a win-win scenario for biodiversity and crop production by supporting ecosystem services to agriculture. On-farm wildflower plantings and conserving semi-natural habitat surrounding farms are two such practices that focus on the integration of non-crop components into production systems at the local and landscape scale, respectively. Here, we examine the impact of these practices on the regulating services of biological control and pollination, as well as the provisioning service of crop yield in four crops replicated across 22 farms in two US states. Wildflower plantings had no effect on pollination while their influence on pest control was both dependent on the landscape context and inconsistent across crops. In contrast, farms surrounded by higher amounts of semi-natural habitat had consistently higher marketable yields for all four crops. Our findings suggest a need to account for non-production values of wildflower plantings as they provide fewer direct production benefits than surrounding semi-natural habitats.
... In recent years, the interactive effects between local field plant diversity and landscape scale habitat diversity have drawn increased attention (Boetzl et al. 2020;Beaumelle et al. 2021). Some research has suggested that local field vegetation diversification is more effective at improving ecosystem services in simplified landscapes (Batary et al. 2011;Grab et al. 2018;Beaumelle et al. 2021). However, we found that the effects of local weed presence on H. armigera larval numbers were more apparent in diverse landscapes, where the overall levels of initial pest abundance were much lower. ...
Full-text available
Context Plant diversity can sometimes determine the distribution of pests in ecosystems, but the effects of plant diversity at local and landscape scales on the occurrence of pests on novel marginal hosts are still unknown. Objectives We explored the direct effects of plant diversity at local and landscape scales on the colonization of the marginal host walnut by Helicoverpa armigera (Lepidoptera: Noctuidae). Methods We surveyed and compared the occurrence (and damage) of H. armigera in walnut orchards embedded in simple vs. diverse landscapes, and with weeds or without weed cover. The surrounding landscape composition and weed communities in walnut orchards were also investigated to shed light on the mechanisms driving H. armigera responses. Results Diverse landscapes were associated with lower densities of overwintering adult H. armigera, first generation eggs and larvae, as well as with lower infestation rates of walnut fruits. Weed presence in walnut orchards had no significant effects on the abundance of H. armigera adults or eggs, but was associated with higher larvae densities in orchards, in both simple and diverse landscapes. The effect of within-orchard weed cover on larvae was stronger in diverse landscapes. Conclusions Our study demonstrated that landscape composition coupled with local orchard ground cover vegetation mediated the occurrence of H. armigera on a marginal host walnut. Monoculture production increases walnut’s exposure to the pest and may accelerate its evolutionary adaptation to this poor host; weed cover in individual orchards may increase larval density by providing floral resources for adults.
... Thus, Cucurbita crops pollinated by B. impatiens must be subsidized by coblooming plants that provide more nutritious or less toxic pollen as food. This finding has more general implications for the management of crops pollinated by wild bees [25]. ...
Full-text available
Concern for pollinator health often focuses on social bees and their agricultural importance at the expense of other pollinators and their ecosystem services. When pollinating herbivores use the same plants as nectar sources and larval hosts, ecological conflicts emerge for both parties, as the pollinator's services are mitigated by herbivory and its larvae are harmed by plant defences. We tracked individual-level metrics of pollinator health—growth, survivorship, fecundity—across the life cycle of a pollinating herbivore, the common hawkmoth, Hyles lineata , interacting with a rare plant, Oenothera harringtonii , that is polymorphic for the common floral volatile ( R )-(−)-linalool. Linalool had no impact on floral attraction, but its experimental addition suppressed oviposition on plants lacking linalool. Plants showed robust resistance against herbivory from leaf-disc to whole-plant scales, through poor larval growth and survivorship. Higher larval performance on other Oenothera species indicates that constitutive herbivore resistance by O. harringtonii is not a genus-wide trait. Leaf volatiles differed among populations of O. harringtonii but were not induced by larval herbivory. Similarly, elagitannins and other phenolics varied among plant tissues but were not herbivore-induced. Our findings highlight asymmetric plant–pollinator interactions and the importance of third parties, including alternative larval host plants, in maintaining pollinator health. This article is part of the theme issue ‘Natural processes influencing pollinator health: from chemistry to landscapes’.
The main aim of pollinator integrated pest management technology (PIPMT) is to integrate pollinator services in pest management strategies for enhancing productivity. Deviating from the idea of integrated pest management, we incorporate pollinators in an action process of pest management in hierarchy. We portray this new champion approach as a PIPMT hierarchy. Preference is given to enterprising actions at the foundation of a pyramid model, which are set in motion through farming, landscape, pest management, and crop pollinators. In addition to the pyramid model, procedures in the shape of responsive manipulation of biotic and abiotic factors should line up with fundamental activities. The objective of PIPMT is to keep down trade-offs, and to enhance co-benefits and collaboration between bee pollinators and pest control strategies. We assert that PIPMT has the great potential in a sustainable crop pest and bee pollination management system, as well as beneficial for the bio-ecosystem.
Full-text available
Agricultural intensification resulting in the simplification of agricultural landscapes is known to negatively impact the delivery of key ecosystem services such as the biological control of crop pests. Both conservation and classical biological control may be influenced by the landscape context in which they are deployed; yet studies examining the role of landscape structure in the establishment and success of introduced natural enemies and their interactions with native communities are lacking. In this study, we investigated the relationship between landscape simplification, classical and conservation biological control services and importantly, the outcome of these interactions for crop yield. We showed that agricultural simplification at the landscape scale is associated with an overall reduction in parasitism rates of crop pests. Additionally, only introduced parasitoids were identified, and no native parasitoids were found in crop habitat, irrespective of agricultural landscape simplification. Pest densities in the crop were lower in landscapes with greater proportions of semi-natural habitats. Furthermore, farms with less semi-natural cover in the landscape and consequently, higher pest numbers, had lower yields than farms in less agriculturally dominated landscapes. Our study demonstrates the importance of landscape scale agricultural simplification in mediating the success of biological control programs and highlights the potential risks to native natural enemies in classical biological control programs against native insects. Our results represent an important contribution to an understanding of the landscape-mediated impacts on crop yield that will be essential to implementing effective policies that simultaneously conserve biodiversity and ecosystem services.
Full-text available
Increased homogeneity of agricultural landscapes in the last century has led to a loss of biodiversity and ecosystem services. However, management practices such as wildflower borders offer supplementary resources to many beneficial arthropods. There is evidence that these borders can increase beneficial arthropod abundance, including natural enemies of many pests. However, this increase in local habitat diversity can also have effects on pest populations, and these effects are not well-studied. In this study, we investigated how wildflower borders affect both natural enemies and pests within an adjacent strawberry crop. Significantly more predators were captured in strawberry plantings with wildflower borders versus plantings without wildflowers, but this effect depended on sampling method. Overall, herbivore populations were lower in plots with a wildflower border; however, responses to wildflower borders varied across specific pest groups. Densities of Lygus lineolaris (Tarnished Plant Bug), a generalist pest, increased significantly in plots that had a border, while Stelidota geminata (Strawberry Sap Beetle) decreased in strawberry fields with a wildflower border. These results suggest that wildflower borders may support the control of some pest insects; however, if the pest is a generalist and can utilize the resources of the wildflower patch, their populations may increase within the crop.
Full-text available
1.The explicit and implicit aims of creating ecological focus areas (EFAs) and implementing greening measures in European agro-ecosystems include the promotion of regulatory ecosystem services (ES) to sustain crop production in conventional cropping systems. However, the extent to which these goals are achieved with current policy measures remains poorly explored. 2.We measured insect-mediated pollination and natural pest control service provisioning in 18 winter oilseed rape fields as a function of the independent and interactive effects of local EFA establishment ─ sown wildflower strips and hedgerows ─ and landscape-scale greening measures within a 1 km radius around focal fields and quantified their contribution to crop yield. 3.Insect pollination potential and pest predation increased on average by 10 and 13%, respectively, when landscape-scale greening measures share was increased from 6 to 26%. For pollination, the increase was stronger in fields adjoining an EFA (14%) than in fields without adjacent EFA (7%). 4.Agricultural management practices were the main drivers of crop yield. Neither insect pollination potential or natural pest control (pest predation & parasitism) nor adjacent EFAs and landscape-scale greening significantly affected crop yield in addition to agricultural management. 5.Synthesis and applications. Local establishment of perennial, species-rich wildflower strips and hedgerows, combined with landscape-scale greening measures in agricultural landscapes, can promote multiple ecosystem services (ES) in conventional production systems. Benefits may be maximized when local and landscape measures are combined. However, enhanced pollination and natural pest regulation seem to contribute relatively little to final crop yield compared to local agricultural management practices in the high-input conventional production system studied. Further research is needed to better understand how to improve the effectiveness of ecological focus areas and other greening measures in promoting regulatory ES. Potential improvements include minimising trade-offs while promoting synergies between ES provision, food production and biodiversity conservation.
Full-text available
The influence of local and landscape habitat diversification on biological control of the Western grape leafhopper (Erythroneura elegantula Osborn) by its key parasitoids Anagrus erythroneurae S. Trjapitzin & Chiappini and Anagrus daanei Triapitsyn was studied in wine grape vineyards. At the landscape scale, Anagrus rely on alternative host species in non-crop habitats outside of the vineyard to successfully overwinter, while at the local scale vineyard diversification can provide resources, such as shelter and floral nectar, which improve parasitoid performance. In a two-year experiment, plots with and without flowering cover crops were compared in vineyards representing a gradient of landscape diversity. While the cover crops did attract natural enemies, their populations were unchanged in the crop canopy and there was no difference in parasitism rate, leafhopper density, crop quality, or yield. Vineyards in diverse landscapes had higher early-season abundance of Anagrus spp., which was linked to increased parasitism and decreased late-season populations of E. elegantula. Leafhopper densities were also positively associated with crop vigor, regardless of landscape or cover crops. Flowering cover crops did increase abundance of some natural enemy species as well as parasitism rate in vineyard landscapes with intermediate levels of diversity, indicating a local × landscape interaction, although this did not lead to reductions in E. elegantula densities. These findings indicate that, in this agroecosystem, landscape diversity mediates and in many ways outweighs the influence of local diversification and that E. elegantula densities were regulated by a combination of biological control and crop vigor.
Full-text available
One of the frequent questions by users of the mixed model function lmer of the lme4 package has been: How can I get p values for the F and t tests for objects returned by lmer? The lmerTest package extends the 'lmerMod' class of the lme4 package, by overloading the anova and summary functions by providing p values for tests for fixed effects. We have implemented the Satterthwaite's method for approximating degrees of freedom for the t and F tests. We have also implemented the construction of Type I - III ANOVA tables. Furthermore, one may also obtain the summary as well as the anova table using the Kenward-Roger approximation for denominator degrees of freedom (based on the KRmodcomp function from the pbkrtest package). Some other convenient mixed model analysis tools such as a step method, that performs backward elimination of nonsignificant effects - both random and fixed, calculation of population means and multiple comparison tests together with plot facilities are provided by the package as well.
Full-text available
Ecologists and farmers often have contrasting perceptions about the value of natural habitat in agricultural production landscapes, which so far has been little acknowledged in ecology and conservation. Ecologists and conservationists often appreciate the contribution of natural habitat to biodiversity and potential ecosystem services such as biological pest control, whereas many farmers see habitat remnants as a waste of cropland or source of pests. While natural habitat has been shown to increase pest control in many systems, we here identify five hypotheses for when and why natural habitat can fail to support biological pest control, and illustrate each with case studies from the literature: (1) pest populations have no effective natural enemies in the region, (2) natural habitat is a greater source of pests than natural enemies, (3) crops provide more resources for natural enemies than does natural habitat, (4) natural habitat is insufficient in amount, proximity, composition, or configuration to provide large enough enemy populations needed for pest control, and (5) agricultural practices counteract enemy establishment and biocontrol provided by natural habitat. In conclusion, we show that the relative importance of natural habitat for biocontrol can vary dramatically depending on type of crop, pest, predator, land management, and landscape structure. This variation needs to be considered when designing measures aimed at enhancing biocontrol services through restoring or maintaining natural habitat.
Larvae of closely related parasitoid taxa often lack morphological differences that can be used for species level identification. Determining the parasitoid species present in a host population may require rearing, often a time-consuming process. To monitor field parasitism rates by several species of Peristenus wasps (Hymenoptera: Braconidae) that are natural enemies of Lygus (Heteroptera: Miridae), we have developed a two-step molecular approach. Polymerase chain reaction (PCR) of the COI gene with wasp-targeting primers is performed on DNA extracted from a Lygus nymph and the parasitoid larva (if any) therein. A positive reaction indicates parasitoid presence. A restriction digest of the PCR product then indicates which parasitoid species is present among known alternatives, and a diagnosis is achieved in days rather than weeks or months.
Wildflowers have an important environmental impact on rural biodiversity. Their chromatic and shape evolution, to attract pollinators, is the key to their dual benefit in terms of aesthetics and environmental functionality. Their scarcity and/or disappearance in conventional agro-ecosystems have led them to be considered as necessary for the restoration of the agro-environment. We compared the dynamics of wildflower-only and wildflower-weed communities, in outdoor boxes, in order to study the floristic evolution over the course of a three-year experiment. Four agronomic treatments were applied: seeding time, late winter cutting, summer harrowing, summer cutting after senescence. Our hypothesis was that the sustainability of the wildflower community was vulnerable to strong weed interference and that agronomic management is necessary for the long-term survival of wildflowers. The indicators used were: biomass, number of seeds in the seed bank, diversity indexes. Our results showed that the growth of the wildflowers was affected by the weeds, in terms of the biomass and seed bank accumulated. However, various agronomic disturbances, such as cutting and, to a greater extent, harrowing, maintained the balance of the floristic complexity in the wildflower-weed community. The plant equilibrium was confirmed by the Shannon, Simpson and Evenness indexes. We found that long-term wildflower sustainability is closely linked to the agronomic management. Further studies are needed to optimize the anthropic-dependent survival of such wildflower buffer areas, given the “greening” measures encouraged by the new European agricultural policy aimed at biodiversity conservation.
Earlier this year, the first global thematic assessment from the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) evaluated the state of knowledge about pollinators and pollination ( 1 , 2 ). It confirmed evidence of large-scale wild pollinator declines in northwest Europe and North America and identified data shortfalls and an urgent need for monitoring elsewhere in the world. With high-level political commitments to support pollinators in the United States ( 3 ), the United Kingdom ( 4 ), and France ( 5 ); encouragement from the Convention on Biological Diversity's (CBD's) scientific advice body ( 6 ); and the issue on the agenda for next month's Conference of the Parties to the CBD, we see a chance for global-scale policy change. We extend beyond the IPBES report, which we helped to write, and suggest 10 policies that governments should seriously consider to protect pollinators and secure pollination services. Our suggestions are not the only available responses but are those we consider most likely to succeed, because of synergy with international policy objectives and strategies or formulation of international policy creating opportunities for change. We make these suggestions as independent scientists and not on behalf of IPBES.