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

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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.
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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.
http://dx.doi.org/10.1098/rspb.2018.1102
Received: 17 May 2018
Accepted: 6 July 2018
Subject Category:
Global change and conservation
Subject Areas:
ecology
Keywords:
ecological intensification, wildflower strips,
landscape, pollination, biological control,
crop yield
Author for correspondence:
Heather Grab
e-mail: hlc66@cornell.edu
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.4163000.
Landscape context shifts the balance
of costs and benefits from wildflower
borders on multiple ecosystem services
Heather Grab1, Katja Poveda1, Bryan Danforth1and Greg Loeb2
1
Department of Entomology, Cornell University, Ithaca, NY 14853, USA
2
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
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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
2
quadrats in each of the five
rows. Visitation rates per plot were calculated by dividing the
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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
tapped.
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
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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
poly
¼
63.86, AICc
log
¼73.86, AICc
linear
¼73.89; Poly: F
1,21
¼7.33,
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
1,21
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
poly
¼127.7, AICc
log
¼
136.3, AICc
linear
¼136.1; Poly: F
1,18
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
2,18
¼7.88,
p¼0.003) and was greatest in 2014 (t
1,21
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
poly
¼117.7,
AICc
log
¼126.5, AICc
linear
¼126.4; Poly: F
1,16
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
1,18
¼2.48,
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
1,10
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,
–0.2
–0.1
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
2013 2014 2015
y
ear
*
–0.8
–0.6
–0.4
–0.2
0
0.2
0.4
0.6
0.8
1.0
1.2
1.4
1.6
0.2 0.3 0.4 0.5 0.6
p
ro
p
ortion natural habitat
effect on bee visitation to crop
2013
2014
2015
year
(a)(b)
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.
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F
1,10
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
12,238
¼1.94, p¼0.03)
as did the number of bee visitors to each species (F
14,86
¼8.12,
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
1,11
¼36.03, p,0.001; bee year: F
1,11
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
poly
¼65.83,
AICc
log
¼72.35, AICc
linear
¼72.58; Poly: F
1,19
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
poly
¼20.33, AICc
log
¼7.42, AICc
linear
¼
8.52; Poly: F
1,19
¼8.68, p¼0.008). In the landscapes with the
0
2
4
6
effect on L. lineolaris
–1
0
1
2
3
4
5
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
2013
2014
2015
(b)(a)
year
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.
02040
Silphium*
Symphyotrichum
Penstemon*
Solidago*
Zizea*
Lotus
Veronicastrum*
Agastache*
Cirsium
Hieracium
Lobelia*
Coreopsis*
Trifolium
Erigeron
bee visits
00.10.20.30.40.50.6
Erigeron
Solidago*
Symphyotrichum
Penstemon*
Silphium*
Achillium
Trifolium
Coreopsis*
Zizea*
Daucus
Veronicastrum*
Agastache*
Lobelia*
Hieracium
L. lineolaris per sample
–5
0
5
0.2 0.3 0.4 0.5 0.6
effect on L. lineolaris in wildflowers
proportion natural habitat
(a)(b)
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.
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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.
–0.8
0.2
1.2
2.2
effect on fruit damage
–0.7
–0.6
–0.5
–0.4
–0.3
–0.2
–0.1
0
0.1
0.2
0.3
0.2 0.3 0.4 0.5 0.6
p
ro
p
ortion natural habitat
0.2 0.3 0.4 0.5 0.6
p
ro
p
ortion natural habitat
effect on fruit weight
year
2013
2014
2015
(a)(b)
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.
rspb.royalsocietypublishing.org Proc. R. Soc. B 285: 20181102
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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: http://dx.doi.org/10.5061/
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.
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... 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: https://hvfarmscape.org/sites/default/files/native_meadow_trials_at_the_hudson_valley_farm_hub_5_year_report.pdf
... Alternatively, if wildflower plantings outcompete and draw pollinators away from nearby crops (Lander et al. 2011;Nicholson et al. 2019), then we would expect crops closest to the plantings to have the highest level of pollen limitation. Additionally, these contrasting distance effects of wildflower plantings on crop pollination are likely restricted to small spatial scales (Ganser, Mayr, Albrecht, & Knop 2018) and may vary with timing of crop and wildflower bloom (Grab et al. 2017) and with landscape context (Grab, Poveda, Danforth, & Loeb 2018) among many other factors. ...
... Because increases in crop pollination and yield may be observed only after three or more years since flower strip planting , the abundance of short-term studies may underestimate the overall value of flower strips (Albrecht et al. 2020). Additionally, the small size of our wildflower strips may have been Lastly, it is possible that the wild bee fauna on our study farms were drawn away from the squash by other crops on the farm (e.g., large patches of cucurbits present on all farms ;Cresswell & Osborne 2004), the wildflower strips (Lander et al. 2011;Nicholson et al. 2019;Peter, Hoffmann, Donath, & Diekötter 2021), or other plants in the adjacent unmanaged semi-natural habitat (Grab, Poveda, Danforth, & Loeb 2018). All farms had some type of Cucurbita species planted (e.g., summer squashes, winter squashes, gourds, and pumpkins) each year with patch size and farm placement (layout) varying each year, depending on the farm and crop rotation schedule. ...
Article
The yield of many agricultural crops depends on pollination services provided by wild and managed bees, many of which are experiencing declines due to factors such as reductions in floral resources. Thus, improving pollinator habitat on farmlands using management strategies like planting wildflower strips is vital for wild bee conservation and sustainable crop pollination. Yet, few studies have examined whether and at what spatial scales wildflower strips enhance crop pollination and yields, and most research has been conducted in large-scale commercial agriculture. Therefore, we investigated the effects of wildflower strips on crop pollination on small, diversified farms (i.e., those growing a variety of crop species) where wild bee diversity and abundance is predicted to be comparatively high. Over three years, on four diversified farms in Montana USA, we tested the hypothesis that distance (20, 60, and 180 m) of crops from native perennial wildflower strips planted alongside crop fields affected wild bee visitation, pollination, and yields of squash and sunflower crop plants. We found that distance to wildflower strips did not affect bee visitation or pollination in crops. Squash yield was pollen-limited in the growing season prior to wildflower strip establishment, and in one of the two years after wildflower strip establishment, but proximity to wildflower strips did not influence the magnitude of pollen limitation. Sunflower seed production was not pollen-limited in any year. Our findings demonstrate that even on diverse farms with wildflower strips and a demonstrated high diversity of bees, some crops do not necessarily receive maximum pollination, regardless of distance from the wildflower strips. However, the value of wildflower strips for supporting wild bee diversity, and other ecological or economic benefits, needs consideration for a full understanding of this pollinator habitat management strategy.
... B atary et al., 2011;Scheper et al., 2013Scheper et al., , 2015; but see e.g. Hoffmann et al., 2020), its validity for ecological intensification and the local delivery of crop pollination and pest control services has only just begun to be explored (Jonsson et al., 2015;Grab et al., 2018;Rundl€ of et al., 2018). ...
... The effect of adding a flower strip or hedgerow was, however, independent of landscape context. Although individual case studies (Jonsson et al., 2015;Grab et al., 2018; included in this synthesis) found support for the intermediate landscape hypothesis, enhanced ecosystem services associated with floral plantings were not generally limited to moderately complex landscape contexts, which should encourage farmers to adopt these measures irrespective of the type of landscape in which they are farming. ...
... Forest cover enhances diversity and spillover of wasps and associated pest control services in adjacent coffee plantations Hugo R. Medeiros Biology Department, Saint Mary's University, Halifax, Nova Scotia, CANADA, hugo.medeiros.r@gmail.com The overuse of agrochemicals combined with the conversion of natural ecosystems into expansive monocultures increases mortality rates of beneficial insects, reduces species diversity, and disrupts the provision of pollination and pest control services in both natural and agroecosystems (Desneux et al. 2007;Geiger et al. 2010;Grab et al. 2018). Although agricultural matrix can provide a lot of resources for beneficial insects through pest outbreaks and mass flowering, these resources are available only for short periods, and crops are periodically subjected to pesticide applications. ...
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The Sixth International Symposium on Biological Control of Arthropods, held virtually from British Columbia, Canada, continues the series of International Symposia on Biological Control of Arthropods, organized every four years. The history of the meetings is: • First ISBCA, Hawaii, USA – January 2002 • Second ISBCA, Davos, Switzerland – September 2005 • Third ISBCA, Christchurch, New Zealand – February 2009 • Fourth ISBCA: Pucón, Chile – March 2013 • Fifth ISBCA: Langkawi, Malaysia – September 2017 The goal of these symposia is to create a forum where biological control researchers and practitioners can meet and exchange information, to promote discussions of up to date issues affecting biological control, particularly pertaining the use of parasitoids and predators as biological control agents. This includes all approaches to biological control: conservation, augmentation, and importation of natural enemy species for the control of arthropod targets, as well as other transversal issues related to its implementation. To this end, 12 sessions have been organized in order to address the most relevant and current topics in the field of biological control of arthropods, delivered by invited speakers, contributed talks and poster presentations. To kick off ISBCA 2022, Dr. Martin Hill, Global President of the International Organization for Biological Control, presents an opening keynote talk on the current state of biological control. Some of the topics covered in ISBCA 2022 have remained as important issues since the first meeting, like the importance of biological control for managing invasive species, sustainable pest regulation in agricultural landscapes, the continuing challenges for biological control of forest pests, and the role of native vegetation in conservation biological control. But also, as new challenges and environmental concerns arise, some fresh topics have emerged. Among them are climate change and the disruption of biological control, stakeholder knowledge and perceptions of biological control, the use of native and exotic natural enemies for augmentative biological control, and functional diversity supporting biological control. For the first time, a workshop on biological control of ticks will be held. To show that biological control is a continuum linked to other disciplines, there will be a session on the science underpinning the successful use of pathogens in biological control. An important goal of the International Symposium on Biological Control of Arthropods is to promote early career researchers, and the first session Proceedings of ISBCA 6 – D.C. Weber, T.D. Gariepy, and W.R. Morrison III, eds. (2022) iii is organized to showcase the work of select individuals. The International Organization for Biological Control (IOBC) has sponsored these presentations. Another important goal of these meetings has been to be truly international, and this is why every conference so far has been organized in a different continent. This year we are excited in having achieved this goal despite the many world crises, by having participants from over 30 countries and all continents except Antarctica. We are particularly happy for the many works and participants from South America, a region that in the past has been poorly represented in these symposia. As a result, this meeting represents an opportunity for creating and expanding networks between researchers worldwide. Thus we expect that, despite the virtual format, the 6th International Symposium on Biological Control of Arthropods would be an important milestone in keep moving forward the research and practice on biological control of arthropods, thereby helping to improve the sustainability of managed systems as well as aiding in the protection of biodiversity on the planet.
... These factors include abiotic components such as temperature and soil nutrients as well as biotic components such as pathogens, pests, natural enemies, and pollinators (Dainese et al., 2019;Reeves, Cheng, Kovach, Kleinhenz, & Grewal, 2014;Savary et al., 2019;Tai & Val-Martin, 2017;Wortman & Lovell, 2013). To some extent, these factors can be manipulated through farming practices and management strategies that improve crop productivity (Grab, Poveda, Danforth, & Loeb, 2018;Havlin, Kissel, Maddux, Claassen, & Long, 1990;Muneret, Thi ery, Joubard, & Rusch, 2018). Our understanding of how these components influence crop yield, however, is based largely on field experimentation in rural environments and large-scale monoculture systems (Spiertz, 2013), not urban environments which typically support small to mid-sized farms with diverse polyculture plantings. ...
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While many cities have embraced urban agriculture, research examining crop productivity in urban environments is limited. Little is known about how abiotic and biotic factors affecting productivity on urban farms compare with those in rural environments. In this study, we investigated environmental factors influencing strawberry (Fragaria x ananassa) productivity for two cultivars at ten farms across a rural-urban gradient in Michigan, USA over a three-year period. We evaluated key drivers of production, namely temperature, pathogens, pests, and pollinators, which we hypothesized would be altered by urbanization. We found no direct effect of urbanization on strawberry production or fruit pathogen and pest damage. However, temperature, an environmental correlate of urbanization, significantly influenced crop productivity. In particular, cooler temperatures at rural farms and warmer temperatures at urban farms limited fruit number in the peak production year. We found no relationship between urbanization and overall abundances of arthropod pests, their predators, or pollinators. However, we found opposite effects of urbanization for two arthropod groups – Vespidae (paper wasps) and Araneae (spiders). Vespidae abundance was positively associated with increased urbanization. These omnivorous wasps are both predators of strawberry pests and pests of fruits themselves. Conversely, spiders, which are predators of strawberry pests, were negatively associated with urbanization. Greater pollinator visitation incrementally improved fruit weight, but only at low to moderate levels of pathogen and pest damage. At high levels of damage, the benefits of pollination were not apparent. Our study reveals that environmental drivers of variation in crop yield, such as pathogen and herbivore damage and pollinator visitation, can be comparable across rural-urban gradients. Some factors, however, such as temperature stress and the abundances of certain pest and beneficial organisms may be affected by urbanization.
... Such wildflower strips may benefit natural enemies that do not or rarely use floral resources, such as spiders, carabid beetles and staphylinid beetles as well because they can provide long-term stable shelters and complex vertical vegetation structures that are important for these organisms (Frank and Reichhart, 2004;Schmidt-Entling and Döbeli, 2009). However, while wildflower strips have generally been shown to benefit natural enemies (Blaauw and Isaacs, 2015;Tschumi et al., 2015), the effects of wildflower strips on ecosystem service delivery are less consistent, with studies showing positive, neutral and even negative effects on natural pest control in nearby crops (Pfiffner et al., 2009;Tscharntke et al., 2016;Tschumi et al., 2016a;Grab et al., 2018;Toivonen et al., 2018;Cahenzli et al., 2019;Albrecht et al., 2020). This makes it difficult to formulate clear recommendations that help entice farmers to integrate wildflower strips into farm management. ...
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Wildflower strips have been heralded as a promising way to enhance ecosystem services by providing organisms which may help make farming less dependent on external inputs. However, recent studies show inconsistent effects on delivery of ecosystem services and crop yield, warranting a more detailed analysis of the factors determining the effects of wildflower strips. We examined how the natural enemy groups of spider, carabid beetle and staphylinid beetle, as well as aphid pest and crop yield respond to wildflower strips. We furthermore determined whether the response of natural enemies, aphids and crop yield depends on flower cover and species richness, and how this is influenced by fertilizer and insecticide applications to the crop in 16 winter wheat fields in the Netherlands. We used an experimental approach with a nested design that included all combinations of wildflower strips (present/absent), fertilizer application (yes/no) and insecticide application (yes/no). Presence of wildflower strips did not affect ground-dwelling natural enemies, aphids or crop yield. However, flower availability across wildflower strips and control margins was positively related to the abundance of the pooled number of examined natural enemies, spiders and carabid beetles. Positive effects in the crop were observed over limited distances; up to 5 m from the edge for spiders and wheat yield. The effects of flower availability and on-field management practices on natural enemies, aphids and wheat yield did not interact suggesting that, in our study, effects of flowers were not influenced by insecticide or fertilizer applications but were mainly additive. Our study indicates that cover and richness of wildflowers in field margin habitat, rather than establishment of wildflower strips per se, drove increases in natural enemies and crop yield. This suggests that more attention should be given to the optimization of establishment success of seed mixtures and management practices enhancing wildflower cover and diversity. Furthermore, biodiversity enhancing management of the herbaceous vegetation in linear landscape elements may represent a cost-effective alternative to boost ecosystem services regulating crop production in agricultural landscapes.
Article
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’.
Thesis
La dépendance de l'agriculture aux pesticides peine à se réduire et la biodiversité dans les milieux agricoles continue de décliner. Les systèmes de culture d’aujourd’hui doivent progresser vers un renforcement des processus écologiques pour tendre vers une gestion agroécologique de la santé des cultures, ce qui nécessite d’approfondir nos connaissances sur la régulation effectuée par les prédateurs et parasitoïdes, ainsi que leurs déterminants. Par ailleurs, très peu de connaissances établies en parcelles agricoles existent sur la multifonctionnalité de systèmes de grandes cultures.La thèse a pour objectifs d'évaluer (i) comment des bandes fleuries pérennes insérées dans des systèmes de culture contrastés, modifient les communautés multitrophiques, les régulations biologiques, et les biens et services écosystémiques qui peuvent en résulter, et (ii) la multifonctionnalité des systèmes de culture adossés à une bande fleurie. À cette fin, un réseau de 31 agriculteurs qui mettent en place des systèmes de cultures en agriculture biologique, de conservation des sols (ACS) ou conventionnels, est mobilisé dans le bassin parisien. Au sein de ce réseau, nous avons comparé des couples de parcelles de grandes cultures avec et sans bande fleurie, et caractérisé la biodiversité, les services de régulation biologique sur plusieurs cultures, le service culturel et des performances agronomiques et économiques.Nos résultats montrent tout d’abord que l’effet des bandes fleuries dépend du type de système de culture dans lequel elles sont implantées et du taxon considéré. La régulation des bioagresseurs du colza est peu affectée par la présence d’une bande fleurie mais elle augmente avec les ressources trophiques fournies par les adventices dans les parcelles.Sur féverole, les ressources trophiques en bord de champ permettent d’augmenter les abondances de syrphes et de momies de pucerons verts, mais cela ne s’est pas traduit par une régulation accrue des pucerons. L’analyse du réseau trophique suggère que les oiseaux sont peu connectés aux arthropodes épigés et ne prédatent pas les prédateurs. Nos résultats indiquent aussi un rôle important des carabes dans les régulations biologiques d’insectes phytophages.Dans un second temps, une enquête auprès des citoyens sur la perception esthétique et de la biodiversité de parcelles agricoles nous a révélé une préférence marquée pour les systèmes de culture dont le sol est le plus couvert et dont la végétation, cultivée ou non, est diversifiée. Ces systèmes s’apparentent à ceux en ACS.Enfin, nous avons évalué la multifonctionnalité des systèmes de culture, dans des parcelles avec ou sans bandes fleurie. Les systèmes de culture ayant fortement recours à la biodiversité montrent un profil plus équilibré entre les biens et services fournis. Les systèmes de culture en ACS ou très diversifiés sont un peu moins performants sur le plan agronomique et économique mais sont plus performants sur le service culturel, et semblent plus favorables à la biodiversité lorsqu’ils sont associés à une bande fleurie.En conclusion, nous montrons une complémentarité entre la présence d’une bande fleurie et les différents systèmes de culture dans la fourniture de biens et services écosystémiques. Ils suggèrent que les systèmes basés sur la biodiversité, dans la parcelle et ses abords, renforcent le profil de multifonctionnalité des systèmes de culture.
Article
Farming systems maintain ecosystem services related to arthropod biodiversity, which need to be understood for its effective conservation. Some of these arthropods may also be enemies of crop pests. It has been shown that farming systems surrounded by other types of natural or semi-natural land covers/uses are less affected by pests. The abundance and richness of hymenopteran parasitoid (HP) families in olive groves were analysed along a gradient of complexity of the landscape surrounding these agroecosystems. The working hypothesis was that landscape structure is related to the abundance and richness of HP families. Through principal component analysis of samples analysed in 15 olive groves during the springs and autumns of 2015 and 2016, we found that a higher richness of HP families is associated to simple landscapes with olive grove predominance and a lower richness in landscapes with higher diversity of land uses. The most abundant families in olive-dominated landscapes were Pteromalidae, Encyrtidae and Eulophidae, and the least abundant were Elasmidae, Eupelmidae, Chrysididae, Platygastridae and Eurytomidae. In the most diverse olive grove landscapes only three families appeared: Mymaridae, the most abundant, and Diapriidae and Signiphoridae with lower abundance. Scelionidae was the most abundant family in all olive landscapes, both simple and complex. The greater richness and abundance of HP in olive-dominated landscapes does not guarantee biological control, but it does provide conservation of arthropod biodiversity as a cross-cutting ecosystem service.
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Crop Pollination by Wild and Honey Bees in Switzerland: Importance, Potential for Yield Increases and Support Measures Pollinating insects such as the domestic honey bee as well as numerous wild-bee species and other wild pollinators play an essential role in the provision of pollination services for crop production and wild plants in agroecosystems. However, pollinators are under pressure owing to the loss and fragmentation of their habitats, food scarcity, intensive agricultural management, plant-protection products, climate change, and native and introduced athogens and infectious agents, as well as the interaction of all these factors. Until recently, little data were available to the Swiss agricultural sector on the economic importance of pollination services and the role of wild pollinators and honey bees in providing these services, as well as the implications for possible pollination deficits in crops. In 2014, the Federal Council passed the Swiss Federal Action Plan for Bee Health. This report summarises the work – commissioned inter alia by the Federal Office for Agriculture – of Agroscope and its research partners aimed at improving the data situation, acquiring new knowledge on this complex of issues and determining possible measures for promoting bees and pollination services. The work shows the great economic value of the pollination services – provided mainly by honey bees and wild bees – for the Swiss agricultural sector. In 2014, the reference year, the annual direct production value alone was estimated at 341 million Swiss francs. On average, the level of pollination by insects in most of the crops studied (apples, cherries, oilseed rape, broad beans and raspberries) seems to be relatively good. Nevertheless, improved insect pollination would make in-some-cases significant production increases possible in a number of crops. This would include e.g. a 10% average increase in cherry yield, or an increase in the quality of the harvested crop (e.g. 10% larger Gala apples, fewer deformed raspberries), which is highly relevant for the producers. These results were achieved under optimal pollination conditions in 2018. In years with less-ideal conditions, considerably larger pollination-related yield limitations might be expected. The considerable variation in pollination-related yield limitation (up to 30%) between individual locations was striking. In cherry and apple crops, the variation could be explained by differences in the number of honey bees, and with cherries, mainly by the number and variety of wild bees. Wild-bee abundance was in turn influenced by the percentage of semi-natural habitats, especially of biodiversity priority areas (BPAs), in the surroundings of the orchards. In structurally poor landscapes, the yield limitations caused by the lack of wild bees were partially offset by the use of domestic pollinators. In some crops the honey bee was the most abundant pollinator species, and it was responsible on average for approx. 50% of flower visits. Crops such as apples and oilseed rape are particularly dependent on the presence of sufficiently large numbers of honey bees for optimal pollination. In addition to these, a total of more than 80 different wild bee species were identified in the relatively small number of crops and locations studied. Depending on the crop, the composition of the pollinator communities differed greatly. Whereas the honey bee usually clearly dominated in apple orchards, various groups of wild bees (e.g. Andrena sp. mining bee species, or Bombus sp. bumblebee species) played a key role for cherries and raspberries, regardless of honey bee abundance. Bumblebees were also by far the most important broad-bean pollinators, and were generally important pollinators for many crops, thanks to their usually high pollinating efficiency and their provision of pollination services even at low temperatures and during bad weather. For apple and cherry crops, which are examined in greater detail, the studies show that optimal pollination in terms of yield and quality is achieved through the complementarity of honey bees and species-and-individual-rich wild-bee communities. In cherry production, higher yields were achieved with a higher number of different wild-bee groups and greater wild-bee diversity, since this allows optimal cover of temperature niches by the pollinator communities. Robust forecasts for pollinators, pollination services or the pollination-dependent yield-increase potential of crops using spatial models are not reliably possible with the input data available and owing to the complexity of influencing factors. For honey bees, certain statements can be made on the number and distribution of the colonies and on the crops to be pollinated, but here too accurate forecasts are possible only to a very limited extent, owing to the large flight radii and the complex gathering behaviour of honey-bee colonies. For wild bees, the models have not permitted any forecasts at all, owing to the inadequate input data (e.g. regarding habitat requirements, flight radii and gathering behaviour). The low temporal and spatial resolution of available data in terms of small but potentially important food and nesting habitats and small structures also makes reliable forecasting of wild bees and their pollination performance difficult. A spatial modelling approach for monitoring pollinators, or, indirectly, pollination services, is therefore not recommended, whilst direct data surveys in the field appear to be essential for monitoring activity. The continuation and further optimisation of existing measures for the support of wild pollinators and honey bees is therefore recommended to ensure the pollination of agricultural crops in Switzerland over the long term. The flower strips for pollinators introduced over the course of the Swiss Federal Action Plan for Bee Health (2014, 2016) are used as a food source primarily by polylectic (i.e. generalist) wild bees and honey bees, and can demonstrably support the reproductive success of such wild-bee species. Endangered wild-bee species were only found in the flower strips in relatively small numbers, however. In addition, the flower strips have a spatially limited positive effect on strawberry pollination when sown next to strawberry fields. Early supplies of flower resources are important for the majority of wild-bee species, but these are difficult to achieve through annual flower strips sown in the spring. Instead, such flower strips are suitable for reducing the nectar dearth in the summer. Colony-forming bumblebees and honey bees benefit from them, but so do a range of wild-bee species with fairly late activity periods. Perennial flower strips and flower strips sown no later than the autumn of the previous year are in principle better suited to achieving an early supply of flower resources. Perennial flower strips can also offer nesting opportunities, and in doing so can help build up wild-pollinator populations over several years, thereby supporting pollination services to crops. The current composition of relatively-late-blooming plant species in perennial wildflower strips is not suited to achieving an early supply of blossom. Furthermore, a number of studies show the importance of diverse agricultural landscapes with a high proportion of different tree-and-shrub-rich semi-natural habitats such as species-rich forest margins and hedgerows together with herbaceous, blossom-rich habitats such as extensively managed meadows, wildflower strips or flower strips for pollinators. These can provide a continuous supply of blossom as well as nesting and overwintering opportunities, which are crucial for wild bees in particular. Specifically, it was shown that the extensification of meadows greatly increased the abundance and diversity of wild bees compared to those of intensively managed meadows, which could be attributed to an improved flower resource supply as well as better nesting options. This can have a positive impact on pollination services in the surrounding crops. There is a need for further research in order to better understand how existing measures can continue to be optimised, and which additional measures can contribute to the promotion of pollinators and pollination services. For example, it would make sense to further develop year-round flowering areas with nesting opportunities for wild bees in fruit, berry and arable crops. We would need to assess measures which could also support pollinators in the production area of arable crops, for instance by means of blossom-rich nurse crops (e.g. legumes in maize, cereals and sunflowers). At present, the effectiveness of shifting the cutting date for flowering temporary leys and permanent meadows with a high percentage of clover to the time after the nectar dearth in (early) summer is being evaluated. Lastly, measures for creating important nesting habitats for wild bees, e.g. by building sand heaps for ground-nesting wild bees or through the targeted support of small nesting structures, have the potential to support wild bees and their pollination services without a large spatial requirement. The two resource projects ‘Agriculture et Pollinisateurs’ and ‘Bienenfreundliche Landwirtschaft im Kanton Aargau’ investigate the influence of these and other measures on pollinator populations and their acceptance by farmers. The aim is to work with other stakeholders to further develop effective, practical and widely accepted measures for protecting, promoting and using pollinators and pollination services in Swiss agroecosystems as effectively as possible.
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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.
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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.
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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.
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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.
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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.
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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.
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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.
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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.
Article
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.