Agriculture, Ecosystems and Environment 343 (2023) 108268

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Agriculture, Ecosystems and Environment

journal homepage: www.elsevier.com/locate/agee

Intercrops as foraging habitats for bees: Bees do not prefer sole legume
crops over legume-cereal mixtures
Felix Kirsch a, 1, *, Annika L. Hass a, 2, Wolfgang Link b, 3, Catrin Westphal a, c, 4
a
Functional Agrobiodiversity, Department of Crop Sciences, University of Göttingen, Grisebachstraße 6, D-37077 Göttingen, Germany
b
Divison of Plant Breeding Methodology, Department of Crop Sciences, University of Göttingen, Carl Sprengel-Weg 1, D-37075 Göttingen, Germany
c
Centre of Biodiversity and Sustainable Land Use (CBL), University of Göttingen, Büsgenweg 1, D- 37077 Göttingen, Germany

A R T I C L E I N F O A B S T R A C T

Keywords: Enhancing crop diversity is an option to make agriculture more sustainable and biodiversity friendly. Inter­
Pollination cropping grain legumes together with cereals leads to higher crop diversity and has a broad range of agronomic
Behavior and ecological benefits. However, sole crop stands of grain legumes might be richer in floral resources than grain
Breeding
legume-cereal intercrops and thus are probably more useful to mitigate the lack of flower resources in agri­
Yield
Plant traits
cultural landscapes, which is a main driver of pollinator decline. Yet, little is known about differences between
V. faba both cropping systems and different legume genotypes in terms of attractiveness for pollinators and how these
differences moderate the pollinators’ foraging behavior and consequences for grain legume yields. In a field trial,
we analyzed the abundance of flower visiting insects, the foraging behavior of pollinators and related effects on
grain yield per plant across six different faba bean genotypes (Vicia faba L.) grown as sole crops or as intercrops
with wheat. As foraging behaviors, we considered legal flower visits (i.e. frontal visits) and illegal flower visits (i.
e. nectar robbing through bite holes). We recorded characteristics of V. faba genotypes on crop stand level
(V. faba plant height, number of V. faba inflorescences and leaf area index (LAI)). V. faba-wheat intercrops and
sole crop stands of V. faba were equally attractive foraging habitats for pollinators, implying that intercrops are
as suitable as sole crops to mitigate the lack of floral resources. Yield per V. faba plant was positively affected by
bee pollination, with this effect being determined by the number of illegal flower visits, suggesting that this
foraging strategy does not adversely affect V. faba yields and even has a positive effect. Intercrops had higher
yields per V. faba plant than sole crop stands of V. faba, indicating agronomic advantages of this farming practice.
Although V. faba genotypes differed in their plant traits, these differences could not explain shifts in the number
of flower visiting insects. However, illegal flower visits increased with a higher number of inflorescences whereas
the number of legal flower visits declined. Based on our small-scale experiment, we conclude that the use of
V. faba-wheat intercrops brings agronomic benefits while serving as a foraging habitat for pollinators that proved
to be as attractive as sole crop stands of V. faba.

1. Introduction agricultural systems more resilient (Lin, 2011) and promoting

Global challenges, such as climate warming, the increase of the
world population and biodiversity losses require urgent action to
transform agriculture in a more sustainable direction (Foley et al., 2005;
Godfray et al., 2010; Wagner et al., 2021). Crop diversification is sug­
gested as a possible strategy to address these problems by making
agro-biodiversity (Brandmeier et al., 2021; Fahrig et al., 2011; Hüber
et al., 2022; Järvinen et al., 2022; Norris et al., 2018; Sirami et al.,
2019). Higher levels of crop diversity can be achieved by intercropping,
i.e. the simultaneous cultivation of different crops on the same land
(Hufnagel et al., 2020; Vandermeer, 1992). Intercrops are considered
more complicated to manage and harvest than sole crops (Lithourgidis

* Correspondence to: University of Göttingen, Functional Agrobiodiversity, Grisebachstraße 6, D-37077 Göttingen, Germany.
E-mail address: kirsch.felix.ecology@gmail.com (F. Kirsch).
1
(ORCID: https://orcid.org/0000-0002-5645-2490)
2
(ORCID: https://orcid.org/0000-0002-3377-4622)
3
(ORCID: https://orcid.org/0000-0003-0684-6296)
4
(ORCID: https://orcid.org/0000-0002-2615-1339)

https://doi.org/10.1016/j.agee.2022.108268
Received 3 March 2022; Received in revised form 7 November 2022; Accepted 10 November 2022
Available online 18 November 2022
0167-8809/© 2022 Elsevier B.V. All rights reserved.
F. Kirsch et al.
et al., 2011), but also offer several agronomic advantages. For example,
they can help to control crop pests and diseases, reduce soil erosion and
sustain soil fertility (Dahmardeh et al., 2010; Sharma et al., 2017;
Trenbath, 1993). In addition, intercropping systems can attain higher
yields compared to sole crops due to better resource utilization through
niche complementarity, e.g. in root distribution, improved soil micro­
bial communities and nutrient mobilization (Brandmeier et al., 2021;
Brooker et al., 2015; Hauggaard-Nielsen and Jensen, 2005; Li et al.,
2014, 2006). In particular, the combination of legume and non-legume
plants has many advantages as the non-legume partner benefits directly
or indirectly from the legume’s ability of biological N-fixation (Brooker
et al., 2015; Fujita et al., 1992; White et al., 2013). This can result in
reductions of fossil-based N-fertilizer applications and thus contribute to
mitigation of climate warming (Jensen et al., 2020; Senbayram et al.,
2015). Additionally, legumes often provide floral resources for polli­
nating insects. This function is very important since the lack of floral
resources in modern agricultural landscapes is regarded as a main driver
of pollinator decline (Potts et al., 2010; Rhodes, 2018; Scheper et al.,
2014). Therefore, legume intercropping might contribute to mitigate
pollinator losses (Potts et al., 2010; Rhodes, 2018) and help to sustain
vital crop pollination services (Klein et al., 2007).
The grain legume faba bean (Vicia faba L.) has been identified as a
suitable intercropping partner for cereals like barley, maize and wheat
(Agegnehu et al., 2008, 2006; Li et al., 1999). Additionally, fields with
V. faba can serve as foraging habitats for bees (e.g. bumblebees Bombus
spp.) (Beyer et al., 2020; Veloso et al., 2016). With its flowering period in
May and June, V. faba has the potential to provide pollen and nectar for
pollinators during the so-called “June gap”, a period of especially low
flower availability during the year (Timberlake et al., 2019). Due to this
function as a forage resource, the cultivation of legumes, such as V. faba,
together with non-insect pollinated crops, such as wheat, can lead to an
increased abundance and diversity of flower-visiting insects compared
to pure stands of these crops (Bannert and Stamp, 2007; Brandmeier
et al., 2021; McGregor, 1976; Norris et al., 2018; Stoddard and Bond,
1987). However, it can be assumed that V. faba-wheat intercrops are not
as attractive to pollinators as sole crops stands of V. faba when similar
sized fields are compared with each other. The reason for this is that in
an intercropping system, unlike in a sole crop stand, V. faba cannot
occupy all the available space but has to share it with the wheat plants.
Logically, there are fewer flowering V. faba plants (Brandmeier et al.,
2021) resulting in a lower nectar and pollen density per unit area for
pollinating insects.
Additionally, the lower flower availability in V. faba-cereal in­
tercrops might change flower visitor behavior with possible conse­
quences for the pollination services provided (Beyer et al., 2022;
Marzinzig et al., 2018). To collect pollen and nectar, V. faba flowers can
be entered legally (i.e. from the front). Legal flower visits are often
conducted by long-tongued bee species, like Bombus hortorum (L.),
leading to higher seed-set and cross-fertilization (Marzinzig et al., 2018).
Through bite holes at the base of the corolla tube illegal flower visits are
carried out to exploit the nectaries. Nectar robbing is mainly done by
short-tongued bee species, such as B. terrestris (L.) or Apis mellifera (L.)
(Kirk, 2004). However, A. mellifera is usually a secondary nectar robber
that uses holes bitten by other bee species (Kirk, 2004). The impact of
illegal visits on pollination services is not well studied. High numbers of
illegal flower visits in V. faba stands could lead to fewer legal flower
visits by opportunistic secondary nectar robbers like A. mellifera (Ken­
dall and Smith, 1975) and therefore reduce seed production, as observed
for other plant species (Mackin et al., 2021). However, some studies
indicate that nectar robbing behavior causes little damage on V. faba
flowers and does not affect pollination by legal flower visitors, seed set
and pod development (Kirk, 2004; Stoddard and Bond, 1987). More­
over, V. faba is a partially autogamous crop (Brünjes and Link, 2021;
Ebmeyer, 1988) and thus illegal flower visits could still indirectly
contribute to pollination by shaking self-pollen to the stigma (Kendall
and Smith, 1975; Soper, 1952). For this reason, it is important to
2
Agriculture, Ecosystems and Environment 343 (2023) 108268
understand the effects of intercropping on pollinator densities, their
behavior and the consequences for crop yields to estimate the potential
of V. faba intercropping systems as supplementary foraging habitats and
highly productive cropping systems. So far, the effects of different
V. faba cropping systems on the foraging behavior and related yield
outcomes are not well understood.
In addition to the cropping system, visitation rates and behavior of
pollinators could also be influenced by plant traits that could be spe­
cifically taken into account in plant breeding (Irwin et al., 2004; Palmer
et al., 2009; Widrlechner and Senechal, 1992). Plant breeding mainly
focuses on producing crop genotypes suitable for intensive sole crop
systems (Barot et al., 2017). The objective of breeding is usually the
improvement of certain agronomic key traits, e.g. high quality of har­
vested plant products, tolerance of crops to pests, diseases and adverse
soil and climate conditions and high total biomass or yields (Litrico and
Violle, 2015; Priyadarshan, 2019). Crops combined in an intercropping
system should also meet these requirements and in addition complement
each other positively (Litrico and Violle, 2015). Consequently, new
plant genotypes with traits suitable for intercropping are required.
Ideally, crop varieties should be combined in a way that they provide
multiple services, including stable yields, pest and pathogen resistance
but also ecosystem services, such as climate change mitigation or
resource provision for pollinators and other organisms (Barot et al.,
2017). Nelson et al. (2021) identified an intermediate leaf area index
(LAI) and limited height of V. faba plants as important traits that mod­
erate yields of V. faba-wheat intercrops. This was related to less
competition for light between the intercropping partners and less lod­
ging (i.e. fewer plants fell over and laid on the ground) (Nelson et al.,
2021). Both plant traits could also influence the visitation rate of
pollinating insects and their foraging behavior since they presumably
improve or reduce the perceptibility of V. faba flowers (Cohen and
Shmida, 1993; Schlinkert et al., 2015). For pollinators the number of
flowers provided by different genotypes can also be an important plant
trait facilitating cross pollination (Marzinzig et al., 2018). Knowledge
about complementary traits could help to breed V. faba genotypes that
perform well in intercrops, represent attractive food resources for
pollinating insects and simultaneously enhance pollination services and
crop yields (Suso et al., 2016).
In a field trial with two different cropping systems (intercrops vs. sole
crop stands) and six genotypes of V. faba, we investigated differences in
flower visitation and foraging behavior of pollinators and the associated
effects on crop yields. Additionally, we analyzed how different V. faba
plant traits on crop stand level influenced crop yields and flower visi­
tation of the different genotypes.
We tested the following hypotheses:
1) Fewer flower visits (legal and illegal) take place in V. faba-wheat
intercrops than in sole V. faba stands due to lower numbers of in­
florescences in the intercropping systems.
2) Yields of V. faba are influenced by the number of flower visits and the
foraging behavior of pollinators:
a) An increasing number of flower visits (both legal and illegal)
leads to higher yields of V. faba.
b) V. faba yields are related to the foraging behavior of pollinators
and increase more strongly with legal than with illegal flower
visits.
3) V. faba genotypes differ in their traits on crop stand level leading to
differences in the number of flower visits and the foraging behavior
of pollinators:
a) Higher LAI per crop stand results in a lower number of flower
visits (both legal and illegal) due to decreased flower
conspicuousness.
b) The number of flower visits (both legal and illegal) increases with
the height of V. faba plants per crop stand due to increased flower
conspicuousness.
F. Kirsch et al.
c) The number of flower visits (both legal and illegal) increases with
higher numbers of V. faba inflorescences per crop stand.
2. Material and methods
2.1. Study sites and experimental design
Our study was carried out at two study sites on the experimental
farms of the University of Göttingen close to Deppoldshausen
(51◦ 34’54.8"N 9◦ 58’08.8"E) and Niedernjesa (51◦ 29’07.1"N
9◦ 55’23.3"E) (Fig. B.1, Appendix B). At both study sites, field trials were
established as part of a large interdisciplinary project addressing a va­
riety of research questions on intercropping (e.g. Bonke and Musshoff,
2020; Nelson et al., 2021; Streit et al., 2019).
At each study site, field trials consisted of four field blocks (repli­
cates) (=eight blocks in total) (hereafter referred to as block) with each
block comprising of 48 field plots (Fig. B.1, Fig. B.2, Appendix B)
(Nelson et al., 2021). During our study, we focused on a subset of 20
plots per block, including eight sole crop stands of eight different V. faba
genotypes, eight corresponding V. faba-wheat intercrops of the same
eight V. faba genotypes and the winter wheat cultivar Genius and four
sole crop stands of the winter wheat cultivar Genius (Fig. 1 (A); Table
A.1, Appendix A; Fig. B.3, Appendix B). In total, we considered 160
plots.
Each plot covered an area of 27 m2. Plots consisted of two 10.5 m2
subplots (1.5 m x 7 m) separated by a narrow path of uncultivated land.
(Fig. 1 (B)). Sowing took place at the subplot level, so that a total of
21 m2 of land was covered with crops in each plot. When variables are
given at plot level, we refer to this 21 m2 cultivated area. The sowing
density of all V. faba genotypes was 40 seeds per m2 in sole crop stands
and 20 seeds per m2 in V. faba-wheat intercrops. The winter wheat
cultivar Genius was sown with a density of 320 seed per m2 in sole crop
Graphs are generated with QGIS (QGIS.org, 2020).
3
Agriculture, Ecosystems and Environment 343 (2023) 108268
stands and 160 seeds per m2 in V. faba-wheat intercrops. Sowing took
place in rows with a between row distance of 22.5 cm (i.e. row inter­
cropping) (Vandermeer, 1992). All crops received a base application of
P, K and Mg, but no N fertilizer.
2.2. V. faba plant traits
For each plot, we recorded several plant traits and calculated crop
stand characteristics based on these measurements (hereafter termed as
V. faba plant traits). For trait measurements, we established three 1 m2
sampling plots in each plot. Each sampling plot comprised four sowing
rows, either four rows of winter wheat or V. faba in the case of sole crop
stands, or two rows of V. faba and winter wheat in the case of intercrops
(Fig. 1 (B)).
We counted the number of V. faba plants within these sampling plots.
A V. faba plant was regarded as the sum of all above-ground tillers
belonging to the same plant. Since below-ground tillering occurred
(personal observation), tillers belonging to the same plant may have
been accidentally counted as two plants if no above-ground connection
was visible. Additionally, the number of inflorescences was counted on
two V. faba plants per sampling plot (i.e. six plants per plot). Plants were
always selected from the same sowing row and from the same location
within each sampling plot to ensure comparability. By multiplying the
average number of V. faba inflorescences per V. faba plant by the sum of
all counted V. faba plants in the three 1 m2 sampling plots, we estimated
the number of V. faba inflorescences in the 3 m2 sampling plot area. In
the calculation, we rounded the average number of inflorescences per
V. faba plant to the nearest integer because we wanted to create a var­
iable representing discrete count data. Next, the estimated number of
V. faba inflorescences in the 3 m2 sampling plot area was multiplied by 7
to estimate the number of V. faba inflorescences in the cultivated area
per plot (21 m2) (hereafter termed as number of V. faba inflorescences
Fig. 1. (A) Reduced schematic representation
of a block. Each block comprised 48 plots, but
here we only show the subset of 20 plots visited
for pollinator surveys. We visited eight plots
with sole crop stands of V. faba (green), four
plots with winter wheat (orange), different
V. faba-cereal intercrop combinations (green
with orange hatching). Studied crops and crop
combinations are indicated by bold numbers.
(B) Schematic representation of a study plot.
Each plot covered a total area of 27 m2. Within
each plot, two subplots were established with
six sowing rows of either V. faba, winter wheat
or the mixture of both. Subplots were 10.5 m2
in size (1.5 m x 7 m) and separated by a narrow
path of uncultivated land. V. faba plant traits
(number of V. faba plants, number of inflores­
cence of two V. faba plants) were recorded
within three sampling plots (1 m2) which were
always located at standardized locations. All
three sampling plots included either four rows
of V. faba in case of V. faba sole crops or two
rows of winter wheat and two rows of V. faba in
V. faba-wheat intercrops. During the pollinator
surveys we walked around the two subplots at a
constant pace. The walking path is shown as a
dashed red line. The starting point of these
observation walks is marked with a red dia­
mond, the walking direction with a red arrow.
Green plant symbol is used with permission of
© BFlores (WMF), CC BY-SA 4.0 <https://cre­
ativecommons.org/licenses/by-sa/4.0 > , via
Wikimedia Commons. Modified graph is shared
via Wikimedia Commons to fulfill license terms.
F. Kirsch et al.
per plot (21 m2), Fig. 1 (B); Table A.2, Appendix A). Additionally, we
recorded flowering weed species and the number of weed flowers within
the three 1 m2 sampling plots. These plant and inflorescence measure­
ments were conducted on the same day as the surveys on pollinating
insects (2.3).
We also recorded the V. faba plant height and the LAI of the crop
stand on plot level. The LAI of each plot was recorded three times at
three growth stages of V. faba with an AccuPAR LP-80 ceptometer (i.e. at
start of flowering, during full bloom and at end of flowering) (Nelson
et al., 2021; Siebrecht-Schöll, 2018). Knowing the LAI at these devel­
opment stages, we were able to calculate daily LAI increase rates and,
thus, could estimate the LAI for each visited plot on the day of the
pollinator survey (2.3) (hereafter termed as LAI per plot (21 m2); Table
A.2, Appendix A). Likewise, plant height was measured on ten repre­
sentative V. faba plants per plot during the same three growth stages
(Nelson et al., 2021) to calculate mean height values for each plot and
growth stage. We calculated daily average height increase rates and then
could estimate the average height of V. faba plants in cm per plot
(21 m2) on the day of the pollinator survey (2.3) (Table A.2, Appendix
A).
Additionally, the start and end of the V. faba flowering period was
recorded for each plot since the flowering phenology can be an indicator
of different growth stages that are related to plant trait characteristics,
such as number of inflorescences, LAI and plant height. Flowering
phenology is represented by the number of days between the onset of
V. faba flowering and the day of the pollinator survey (hereafter termed
as days after onset of V. faba flowering; Table A.2, Appendix A).
2.3. Pollinator surveys
Pollinator surveys were conducted between the 18th of May and the
8th of June 2019 during the flowering period of V. faba. For this pur­
pose, we visited each of the 160 plots of our subset once. Study sites and
blocks as well as plots within blocks were visited in a random order.
Randomization was done by rolling a virtual dice. Surveys were carried
out between 09:30 and 18:00. Chance decided whether a plot was
visited in the morning or in the afternoon (Table A.17, Appendix A).
During surveys, the average temperature, average cloud cover (%) and
average wind speed were 27.2 ◦ C ± 5.2 (SD), 44.5 % ± 25.2 (SD) and
1.5 m/s ± 1.6 (SD), respectively. In each plot, flower-visiting insects
were recorded on V. faba and co-flowering weed species during a 6 min
period of pure observation time. During the observation time, we
walked with constant pace around both subplots (Fig. 1 (B)). We
restricted our field of vision by looking only in the direction we were
walking without turning around. In this way, we were able to observe a
strip of each subplot extending from their edges about 75 cm to their
core zones. As our perspective changed during the observation walk, we
were able to cover the whole plot (both subplots) during the observation
time. We categorized observed flower visits on V. faba as either (1) legal
(i.e. frontal flower visit) or (2) illegal visits (i.e. cases of nectar robbing)
(Fig. B.4, Appendix B). Flower visits on co-flowering weeds were
generally considered legal.
Foraging bee pollinators were identified to species level. In case of
honeybees (A. mellifera) and bumblebees (Bombus spp.), this was done
directly in the field. B. terrestris, B. lucorum (L.), B. cryptarum (F.) and
B. magnus (V.) were aggregated because they are very difficult to
distinguish in the field. Non-Bombus wild bees were caught with an in­
sect net, killed and sent to bee expert Dr. Reiner Theunert for identifi­
cation (Umwelt & Planung Dr. Theunert, D-31249, Hohenhameln,
Germany). The same procedure was applied for non-bee hymenopteran
flower visitors, which were identified by Mike Kuschereitz to family
level (Entomologische Bestimmung und Präparation, Mike Kuschereitz,
D-37077, Göttingen, Germany). Non-hymenopteran flower visitors were
recorded in the field on family (Syrphidae) or species level
(Lepidoptera).
Flower visits of non-bee pollinators on V. faba (n = 3) and on co-
4
Agriculture, Ecosystems and Environment 343 (2023) 108268
flowering weed species (n = 10) were very rare. Additionally, flower
visits in sole crop stands of winter wheat were not very common (n = 9),
and all these visits were conducted by non-bee pollinators. For that
reason, our statistical analysis was merely based on flower visits of bee
pollinators on V. faba in sole crop stand of V. faba and V. faba-wheat
intercrops. Furthermore, we had to exclude observations of sole crop
stands and intercrops of two V. faba genotypes (Diva, Cote d’ Or/1) from
our statistical analysis because the pollinator surveys did not cover their
complete flowering period.
2.4. V. faba yields
Harvesting took place between the 6th and the 8th of August 2019 at
both study sites. The central area of each plot was harvested with a
combine harvester. A total of six rows were harvested and three buffer
rows remained unharvested on both sides of the plot. The harvested area
partially covered both subplots and amounted to 10.5 m2. By doubling,
we extrapolated the yield from the harvested area to the cultivated area
per plot (21 m2), which represents the total V. faba yield per plot (g/
21 m2) (Table A.2, Appendix A).
2.5. Statistical analyses
The statistical analyses were conducted with R (R Core Team, 2018).
For each response variable, we calculated either linear mixed effects
models with the nlme package (Pinheiro et al., 2021) or generalized
linear mixed effects models with the glmmTMB package (Brooks et al.,
2017), depending on which model type had the best-fitting residuals (for
an overview of all calculated models see Table 1). Model residuals were
checked with the R base function plot (R Core Team, 2018) for linear
mixed-effects models or with the simulateResiduals function from the
DHARMa package (Hartig, 2020) for generalized linear mixed-effects
models. In addition, the performance package (Lüdecke et al., 2021)
was used to test for multicollinearity in models containing at least one
numerical variable. Following James et al. (2013) and Lüdecke et al.
(2021), we consider VIF values of less than 5 to indicate low correlation
of one predictor with other predictors. We found VIF values below 4 for
all considered variables (see Table A.18 - Table A.26, Appendix A). Mean
VIF values were 1.64 ± 0.79 (SD). Furthermore, we used the DHARMa
fuctions testDispersion and testZeroInflation (Hartig, 2020) to test for
zero inflation and over and under dispersion in case of generalized linear
mixed-effects models. Models were not zero inflated. Neither over
dispersion nor under dispersion could be detected, with one exception
(Table 1, model 7, see below). For better model fit, continuous explan­
atory variables were transformed into z-scores. Explanatory variables
were included as main effects. Each block was given a unique block ID,
which consisted of the block number and the name of the study site
where the block was located. This ensured that all blocks were treated
separately. These block IDs were added as random factors to each model.
We refrained from adding study site directly as a random factor to the
models because this variable has too few levels to be used as a random
factor (Bolker, 2015), instead study site was included as covariate in the
fixed model term. Using the AICc function from the MuMIn package
(Barton, 2018), we compared each model with its corresponding null
models.
First, we fitted generalized linear mixed effects models to analyze the
effects of the cropping systems and the V. faba genotypes on the number
of flower visits. Explanatory variables in these models were the cropping
systems (i.e. sole crop stands of V. faba vs. V. faba-wheat intercrops) and
the V. faba genotypes (Bering, S_069, S_062, Hiverna/2, Malibopop,
Augusta). Additionally, models included also the study site (i.e. Dep­
poldshausen and Niedernjesa) as co-variable. Each model was calculated
with a different response variable: We used the total number flower
visits per plot (21 m2) (i.e. sum of legal and illegal flower visits per plot)
(Table 1, model 1; Table A.2, Appendix A), the number of illegal flower
visits per plot (21 m2) (Table 1, model 2; Table A.2, Appendix A), and
F. Kirsch et al. Agriculture, Ecosystems and Environment 343 (2023) 108268

Table 1
Model terms of fitted generalized linear mixed-effects models and linear mixed-effects models calculated with the glmmTMB package (Brooks et al., 2017) and the
nlme package (Pinheiro et al., 2021).
Model number Response variable Explanatory variables (main effects) Random factor Family Package

1 Total number flower visits per plot (21 m2) Cropping system Block ID Poisson glmmTMB
2 Number of illegal flower visits per plot (21 m2) V. faba genotype
3 Number legal flower visits per plot (21 m2) Study site
4 Total number flower visits per plot (21 m2) Cropping system Block ID Poisson glmmTMB
5 Number of illegal flower visits per plot (21 m2) V. faba genotype
Study site
6 Total number flower visits per plot (21 m2) Number of V. faba inflorescences per plot (21 m2)
7 Number of V. faba inflorescence per plot (21 m2) Cropping system Block ID nbinom2 glmmTMB
V. faba genotype
Study site
Days after onset of V. faba flowering
(Days after onset of V. faba flowering)2
8 LAI per plot (21 m2) Cropping system Block ID Gaussian nlme
V. faba genotype
Study sites
Days after onset of V. faba flowering
(Days after onset of V. faba flowering)2
9 Average V. faba plant height in cm per plot (21 m2) Cropping system Block ID Gaussian nlme
V. faba genotype
Study sites
Days after onset of V. faba flowering
(Days after onset V. faba flowering)2
10 Yield per V. faba plant (g) V. faba genotype Block ID Gaussian glmmTMB
Study sites
Total number flower visits per V. faba plant
11 Yield per V. faba plant (g) V. faba genotype Block ID Gaussian glmmTMB
Study sites
Number legal flower visits per V. faba plant
Number of illegal flower visits per V. faba plant
12 Yield per V. faba plant (g) Cropping system Block ID Gaussian glmmTMB
V. faba genotypes
Study sites
Total number flower visits per V. faba plant
13 Yield per V. faba plant (g) Cropping system Block ID Gaussian glmmTMB
V. faba genotypes
Study sites
Number legal flower visits per V. faba plant
Number of illegal flower visits per V. faba plant

the number of legal flower visits per plot (21 m2) (Table 1, model 3;
Table A.2, Appendix A). In case of 16 flower visits, it was not clear
whether the observed bee was conducting a legal or an illegal flower
visit. Thus, these cases were only included in the model for the total
number flower visits per plot (21 m2). Since no sign of over or under
dispersion could be found, models were fitted with Poisson error dis­
tribution. In addition, we ran three models with the same model struc­
ture that included the number of V. faba inflorescences per plot (21 m2)
as an explanatory variable to test whether possible effects of cropping
systems and V. faba genotypes could be caused by differences in the
number of V. faba inflorescences per plot (21 m2) (Table 1, model 4,
model 5, model 6).
Secondly, three models were fitted to analyze the effects of the
cropping systems and V. faba genotypes on V. faba plant traits (i.e.
number of V. faba inflorescences per plot (21 m2), LAI per plot (21 m2)
and average V. faba plant height in cm per plot (21 m2)). The explana­
tory variables were cropping system, V. faba genotype and the co-
variable study site. Besides, we added days after onset of V. faba flow­
ering as a linear factor and as a squared factor to account for non-linear
effects of the flowering phenology. We calculated a generalized linear
mixed model for the response variable number of V. faba inflorescences
per plot (21 m2) (Table 1, model 7) that was fitted with negative bino­
mial error distribution due to over dispersion. Linear mixed effects
models were fitted for the response variables LAI per plot (21 m2)
(Table 1, model 8) and average V. faba plant height in cm per plot
(21 m2) (Table 1, model 9).
Finally, we fitted four generalized linear mixed effects models to
analyze the effects of the cropping systems, V. faba genotypes and
number of flower visits on V. faba yields. The yield per V. faba plant (g)
was used as response variable in these models. We compared V. faba
yields at the plant level rather than at the plot level as V. faba densities
were system-inherently reduced in the intercrops resulting in higher
total yields per plot (21 m2) in sole crop stands of V. faba than in V. faba-
wheat intercrops. Yield per V. faba plant (g) was calculated as follows:
We estimated the number of V. faba plants for the cultivated plot area
(21 m2) by multiplying our counts of V. faba plants in the three 1 m2
sampling plots by 7. This represents the number of V. faba plants per plot
(21 m2). Then, we calculated yields per V. faba plants (g) by dividing the
total V. faba yield per plot (g/21 m2) by the number of V. faba plants per
plot (21 m2) (Table A.2, Appendix A). We excluded one plot from the
analyses because the measured yield was exceptionally high in com­
parison to all other plots (average yield per V. faba plant = 7.4 g ± 3.1
(SD) / yield per V. faba plant (Outlier) = 55.9 g). This big difference in
yield was caused by a transmission error that could not be traced back.
In correspondence with the response variable yield per V. faba plant (g),
we converted all explanatory variables included in the yield models to
the plant level. This was the case for the total number of flower visits per
plot (21 m2), the number of illegal flower visits per plot (21 m2) and the
number of legal flower visits per plot (21 m2). We converted these
variables to the plant level by dividing them by the total number of
V. faba plants per plot (21 m2) (Table A.2, Appendix A).
The first model included the total number of flower visits per V. faba
plant as an explanatory variable to investigate the effect of flower visits
on yield per V. faba plant independent of foraging behavior.

5
F. Kirsch et al.
Additionally, V. faba genotype was considered as an explanatory vari­
able and study site as a covariate. We excluded the variable cropping
system from the model because we wanted to test the effect of flower
visits per V. faba plant on yield per V. faba plant independent of potential
yield differences due to the cropping systems (Table 1, model 10). A
second model with the same model structure included the number of
illegal flower visits per V. faba plant and the number of legal flower visits
per V. faba plant instead of the total number of flower visits per V. faba
plant to explore the importance of both foraging behaviors on yields per
V. faba plant (Table 1, model 11). Again, 16 flower visits were excluded
from the analysis because it was not clear whether they were legal or
illegal. The third model considered the total number of flower visits per
V. faba plant and V. faba genotype as explanatory variables, and the
study site as covariate. In this model, however, we also included the
cropping system as an explanatory variable (Table 1, model 12). This
was done to explore whether differences in terms of yield per V. faba
plant were related to cropping system effects. Finally, a model with the
same model structure was calculated including the number of illegal
flower visits per V. faba plant and the number of legal flower visits per
V. faba plant as explanatory variables (Table 1, model 13). Models were
fitted with Gaussian error distribution.
Using the r base function cor.test (R Core Team, 2018), we tested for
pair-wise correlation between the V. faba plant traits number of V. faba
inflorescences per plot (21 m2), LAI per plot (21 m2) and the average
V. faba plant height in cm per plot (21 m2).
We created the figures with the R package ggplot2 (Wickham, 2016).
Pairwise comparisons in boxplots were calculated with the emmeans
function of the emmeans package (Lenth, 2020). We used the Bonferroni
correction method to adjust obtained p values for multiple comparisons
(Jafari and Ansari-Pour, 2018). For a better visualization, untrans­
formed values of the response variable are presented in the figures and
predicted means and confidence intervals were back-transformed.
3. Results
We recorded a total number of 1.130 flower visits by bees on the six
considered V. faba genotypes. Illegal flower visits were conducted in the
majority of cases (57.7 %, n = 652), while legal flower visits made up
40.9 % of all visits (n = 462). We were not able to classify the foraging
behavior in 1.4 % of flower visits (n = 16). On average, we observed 4.8
± 5.3 (SD) legal flower visits and 6.8 ± 5.9 (SD) illegal flower visits per
plot (21 m2).
Most flower visits were conducted by bumblebees (Bombus spp.,
n = 801), followed by honeybees (Apis mellifera, n = 286). Non-Bombus
wild bees were the least frequent group of bee visitors (n = 43; see Table
A.3, Appendix A, for a complete list of flower visiting insects). Bum­
blebees conducted illegal flower visits in 67.3 % (n = 539) of cases.
Illegal flower visits were also regularly performed by honeybees (39.5
%, n = 113). However, legal flower visits by honeybees were more
common (59.4 %, n = 170). Bumblebees performed illegal flower visits
significantly more often than honeybees (Fig. B.5, Appendix B). No
nectar robbing was observed for non-Bombus wild bees. Co-flowering
weed species were not visited by the bees. Furthermore, no flower
visits of bees could be observed in sole crop stands of the cereal Genius. A
schematic overview of all results of our statistical analysis can be found
in Fig. 2.
3.1. Effects of cropping systems on flower visits
V. faba-wheat intercrops and sole crop stands of V. faba neither
differed in the total number of flower visits per plot (21 m2) (Table 1,
Model 1; Table A.4, Appendix A; Fig. B.6 (A), Appendix B) nor in the
number of illegal visits per plot (21 m2) (Table 1, Model 2; Table A.5,
Appendix A; Fig. B.6 (B), Appendix B) when the number of V. faba in­
florescences per plot (21 m2) was not included in the models. However,
a significant difference was found in the number of legal flower visits per
6
Agriculture, Ecosystems and Environment 343 (2023) 108268
plot (21 m2). It was 34.7% higher in sole crop stands of V. faba than in
V. faba-wheat intercrops (3.22 ± 1.54 (SE) and 2.39 ± 1.15 (SE),
respectively, Fig. 3 (A); Table 1, Model 3; Table A.6, Appendix A). In
terms of total number of flower visits per plot (21 m2) (Table 1, Model 4;
Table A.7, Appendix A) and legal flower visits per plot (21 m2) (Table 1,
Model 6; Table A.9, Appendix A), these results remained unchanged
when the number of V. faba inflorescences per plot (21 m2) was
considered in the models. However, the cropping systems also differed
slightly in terms of the number of illegal flower visits per plot (21 m2)
when the number of V. faba inflorescences per plot (21 m2) was included
in the model (Table 1, Model 5). We then observed almost one third
more cases of illegal flower visits in V. faba-wheat intercrops than in sole
crop stands of V. faba (6.42 ± 1.36 (SE) and 4.83 ± 1.03 (SE), respec­
tively, Fig. 3 (B); Table A.8, Appendix A).
Furthermore, the foraging behavior was significantly influenced by
the number of V. faba inflorescences per plot (21 m2). We found an in­
crease of the number of illegal flower visits per plot (21 m2) with an
increasing number of V. faba inflorescences per plot (21 m2) (p = 0.030,
Fig. 4 (A); Table 1, Model 5; Table A.8, Appendix A) while the number of
legal flower visits per plot (21 m2) declined slightly with increasing
number of V. faba inflorescences per plot (21 m2) (p = 0.047, Fig. 4 (B);
Table 1, Model 6; Table A.9, Appendix A). The total number of flower
visits per plot (21 m2) was not significantly influenced by the number of
V. faba inflorescences per plot (21 m2) (p = 0.905; Table 1, Model 4;
Table A.7, Appendix A).
We found a significant difference between V. faba genotypes in terms
of the total number flower visits per plot (21 m2) (Table 1, Model 1;
Table A.4, Appendix A; Fig. B.7 (A), Appendix B), the number of illegal
flower visits per plot (21 m2) (Table 1, Model 2; Table A.5, Appendix A;
Fig. B.7 (B), Appendix B) and the legal flower visits per plot (21 m2)
(Table 1, Model 3; Table A.6, Appendix A; Fig. B.7 (C), Appendix B)
when the number of V. faba inflorescences per plot (21 m2) was not
considered in the models. The highest total number of flower visits per
plot (21 m2) could be observed on the V. faba genotype Hiverna/2
(12.05 ± 3.43 (SE)). The total number of flower visits on Hiverna/2 was
almost three quarters higher than on the least frequently visited V. faba
genotype Augusta (6.97 ± 2.02 (SE)). Additionally, Hiverna/2 was also
the V. faba genotype with the highest number of illegal flower visits per
plot (21 m2) (8.16 ± 1.92 (SE)). Nearly twice as many illegal flower
visits took place on Hiverna/2 compared to the V. faba genotype Bering
which received the lowest number of illegal flower visits per plot
(21 m2) (4.21 ± 1.04 (SE)). In terms of legal flower visits per plot
(21 m2), S_062 was most often visited (3.53 ± 1.721 (SE)). This geno­
type was visited slightly more than twice as often as the genotype
Augusta (1.75 ± 0.872 (SE)) which was least frequently visited for legal
foraging.
Apart from minor variations, the differences observed between the
V. faba genotypes in terms of the total number of flower visits per plot
(21 m2) (Table 1, Model 4; Table A.7, Appendix A; Fig. B.8 (A), Ap­
pendix B), number of illegal flower visits per plot (21 m2) (Table 1,
Model 5; Table A.8, Appendix A; Fig. B.8 (B), Appendix B) and number
of legal flower visits per plot (21 m2) ( Table 1, Model 6; Table A.9,
Appendix A; Fig. B.8 (C), Appendix B) remained similar when the
number of V. faba inflorescences per plot (21 m2) was included in the
models.
3.2. Effects of cropping systems and V. faba genotypes on V. faba plant
traits
The number of V. faba inflorescences per plot (21 m2) was almost
two thirds higher in sole crop stands of V. faba (4564 ± 348 (SE))
compared to V. faba-wheat intercrops (2787 ± 215 (SE)) (Table 1,
Model 7; Table A.10, Appendix A; Fig. B.9 (A), Appendix B). Moreover,
the number of V. faba inflorescences per plot (21 m2) varied significantly
between V. faba genotypes (Table 1, Model 7; Table A.10, Appendix A;
Fig. B.9 (B), Appendix B). The highest number of V. faba inflorescences
F. Kirsch et al.
per plot (21 m2) was found in genotype S_062 (4727 ± 439 (SE)). The
number of inflorescences per plot (21 m2) was more than three quarter
higher than in Bering, the genotype with the lowest number of V. faba
inflorescences per plot (21 m2) (2583 ± 279 (SE)). With a more than
40% higher number of V. faba inflorescences per plot (21 m2) in Nie­
dernjesa than Deppoldshausen (4276 ± 425 (SE) and 2975 ± 294 (SE),
respectively), a significant difference was also found between the two
study sites (Table 1, Model 7; Table A.10, Appendix A; Fig. B.9 (C),
Appendix B). The flowering phenology (i.e. days after onset of V. faba
flowering until sampling date) had no significant influence on the
number of V. faba inflorescences per plot (21 m2), neither as a linear nor
as a squared factor (p = 0.663 and p = 0.538, respectively; Table 1,
Model 7; Table A.10, Appendix A).
The LAI per plot (21 m2) was significantly higher in sole crop stands
of V. faba than in V. faba-wheat intercrops (5.17 ± 0.23 (SE) and 4.39
± 0.23 (SE), respectively, 17.8 %; Table 1, Model 8; Table A.11, Ap­
pendix A; Fig. B.10 (A), Appendix B). In addition, significant differences
in LAI per plot (21 m2) were found between crop stands with different
V. faba genotypes varying by almost 40 % between the genotypes
7
Agriculture, Ecosystems and Environment 343 (2023) 108268
Fig. 2. Schematic summary of the statistically
significant findings, i.e. effects of different
explanatory variables on response variables at
the (A) plot level and at the (B) plant level.
Colored boxes represent explanatory variables.
White boxes represent response variables
(except the number of V. faba inflorescences per
plot (21 m2) in (A) which is both a response and
an explanatory variable). Effects of an explan­
atory variable on different response variables
are depicted as arrows of the same color. P
values are shown on the respective arrow and
plus or minus signs indicate whether the influ­
ence on the response variable is positive or
negative. If the explanatory variable is a factor
with two levels (i.e. cropping system, study
site), the p values indicate whether there is a
significant difference between factor levels.
Plus and minus signs show effects of one factor
level (indicated in brackets) compared to the
other one. Since significant differences between
factor levels cannot be summarized with a sin­
gle p value or a single plus and minus sign when
the explanatory variable is a factor with more
than two levels (e.g. V. faba genotypes), no box
with a p value and a plus and minus sign is
added to the arrows in this case. The graph is
based on the results of models 1–13 (Table 1).
Green plant symbol is used with permission of
© BFlores (WMF), CC BY-SA 4.0 <https://cre­
ativecommons.org/licenses/by-sa/4.0 > , via
Wikimedia Commons. The graph is shared via
Wikimedia Commons to fulfill license terms.
Graphs are generated with QGIS (QGIS.org,
2020).
Malibopop with the highest (5.4 ± 0.29 (SE)) and S_062 with the lowest
LAI (3.9 ± 0.27 (SE)) (Table 1, Model 8; Table A.11, Appendix A; Fig.
B.10 (B), Appendix B). We found a positive increase in LAI per plot
(21 m2) with days after onset of V. faba flowering as a linear factor
(p = 0.007; Table 1, Model 8; Table A.11, Appendix A; Fig. B.10 (C),
Appendix B).
The average V. faba plant height in cm per plot (21 m2) was signif­
icantly higher in sole crop stands of V. faba than in V. faba-wheat in­
tercrops (84.5 cm ± 3.92 (SE) and 79.0 cm ± 3.92 (SE), respectively;
Table 1, Model 9; Table A.12, Appendix A; Fig. B.11 (A), Appendix B).
However, this difference was with 7 % relatively small. V. faba geno­
types differed significantly in the average V. faba plant height in cm per
plot (21 m2) (Table 1, Model 9; Table A.12, Appendix A; Fig. B.11 (B),
Appendix B). Plants of the tallest genotype S_069 (88.6 cm ± 4.23 (SE))
were almost a quarter taller than those of the smallest genotype S_062
(71.1 cm ± 4.05 (SE)). The average V. faba plant height in cm per plot
(21 m2) increased over time (i.e. with the variable days after onset of
V. faba flowering as a linear factor, p = 0.001; Table 1, Model 9; Table
A.12, Appendix A; Fig. B.11 (C), Appendix B).
F. Kirsch et al.
Fig. 3. Effects of the cropping systems (A) on the legal number of flower visits
per plot (21 m2) and (B) on the illegal number of flower visits per plot (21 m2).
Different letters above groups indicate significant differences (significance
level: α = 0.05). Predicted means and 95 % confidence intervals are displayed
in red. The figure is based on model 3 and model 5 (Table 1).
No strong correlation between the number of V. faba inflorescences
per plot (21 m2) and the average V. faba plant height in cm per plot
(21 m2) (R2 = − 0.084, p = 0.417) and the number of V. faba in­
florescences per plot (21 m2) and the LAI per plot (21 m2) (R2 = 0.12,
p = 0.245) could be found. However, there was a strong positive cor­
relation between average V. faba plant height in cm per plot (21 m2) and
LAI per plot (21 m2) (R2 = 0.75, p = <0.00).
3.3. Effects of cropping systems, V. faba genotypes and flower visits on
yield per V. faba plant
Yield per V. faba plant (g) differed between V. faba genotypes (Fig. 5
(A); Table 1, Model 10; Table A.13, Appendix A). The highest yielding
V. faba genotype was Bering with a yield more than twice as high as the
V. faba genotype with the lowest yield S_062 (11.13 g ± 0.54 (SE) and
5.46 g ± 0.55 (SE), respectively).
We found an increase of the yield per V. faba plant (g) with an
increasing total number of flower visits per V. faba plant (p = 0.023,
Fig. 6 (A); Table A.13, Appendix A). Furthermore, the number of illegal
flower visits per V. faba plant had a positive effect on the yield per
V. faba plant (g) (p = 0.015, Fig. 6 (B), Table A.14, Appendix A),
whereas there was no significant effect of the number of legal flower
visits per V. faba plant (p = 0.951, Table A.14, Appendix A). These
positive effects of pollination were found when the variable cropping
system was not included as an explanatory variable in the models
(Table 1, Model 10, Model 11).
However, when cropping system was included as explanatory vari­
able in the models, the effects of the total number of flower visits per
V. faba plant (p = 0.774, Table A.15, Appendix A) and the number of
illegal flower visits per V. faba plant (p = 0.652, Table A.16, Appendix
A) were not significant anymore (Table 1, Model 12, Model 13). Instead,
we found significant differences in terms of yield per V. faba plant (g)
between the two cropping systems. Yield per V. faba plant (g) was 46.7%
higher in V. faba-cereal intercrops compared to sole crop stands of
V. faba (8.78 g ± 0.32 (SE) and 5.99 g ± 0.32 (SE), respectively, Fig. 5
(B); Table 1, Model 12; Table A.15, Appendix A).
8
Agriculture, Ecosystems and Environment 343 (2023) 108268
Fig. 4. Effects of the number of V. faba inflorescences per plot (21 m2) (A) on
the number of illegal flower visits per plot (21 m2) and (B) on the number of
legal flower visits per plot (21 m2). We calculated the number of V. faba in­
florescences per plot (21 m2) as follows: The inflorescences were counted on
6 V. faba plants in 3 sampling plots (1 m2) (i.e. 2 plants per sampling plot).
Additionally, all V. faba plants in the 3 sampling plots (1 m2) were counted. We
multiplied the number of V. faba inflorescences, averaged over the 6 V. faba
plants considered, by the sum of all V. faba plants counted in the sampling plots
(1 m2). The average number of V. faba inflorescences was rounded to the
nearest integer to represent discrete count data. Then the result of this calcu­
lation was multiplied by 7 to estimate the number of V. faba inflorescences
within the cultivated area per plot (21 m2) which represents the number of
V. faba inflorescences per plot. The Y-axis is sqrt-scaled for graphical reasons.
Figures are based on model 5 and model 6 (Table 1).
4. Discussion
Given the need for sustainable and biodiversity-friendly cropping
systems (Garibaldi et al., 2017), our study is the first to link potential
benefits of intercropping systems as foraging habitats for bee pollinators
compared to sole crop stands of legumes to bee foraging behavior (legal
vs. illegal visit), trait differences of genotypes and yield outcomes.
4.1. Cropping systems, number of V. faba inflorescences, flower visits and
foraging behavior
Intercrops between non-flowering and flowering plants, such as le­
gumes, can be beneficial for pollinators and other arthropods (Brand­
meier et al., 2021; Norris et al., 2018). As the visitation rate of
pollinating insects is positively affected by the density of flowers (Beyer
et al., 2022; Vrdoljak et al., 2016), we expected intercrops with V. faba
to be less attractive than sole crop stands of V. faba. Indeed, we found a
lower number of V. faba inflorescences per plot (21 m2) in intercrops
than in sole crop (see also Section 4.2). However, the number of V. faba
inflorescences per plot (21 m2) did not affect the total number of flower
visits per plot (21 m2) by bee pollinators. Furthermore, the total number
of flower visits per plot (21 m2) was also not lower in V. faba-wheat
intercrops than in sole crop stands of V. faba, suggesting that both
cropping systems are equally attractive for foraging insects. Based on
our study, it is difficult to identify the underlying mechanisms. We as­
sume that other characteristics than the number of V. faba inflorescences
per plot (21 m2) could explain our findings. For instance, V. faba-wheat
intercrops were characterized by a lower LAI per plot (21 m2) than sole
F. Kirsch et al.
Fig. 5. Effects of (A) the V. faba genotypes and (B) the cropping systems on
yield per V. faba plant (g). We calculated the yield per V. faba plant (g) as
follows: A 10.5 m2 area of each plot was harvested in August 2019. By
doubling, yield was converted from the harvested area to the cultivated area per
plot (21 m2), which represents the total V. faba yield per plot. Additionally, the
number of V. faba plants was counted in 3 sampling plots per plot (1 m2). The
number of V. faba plants in the cultivated area per plot (21 m2) was estimated
by multiplying counts of V. faba plants in the three 1 m2 sampling plots by 7,
which represents the number of V. faba plants per plot. Yield per V. faba plant
(g) was calculated by dividing the total V. faba yield per plot (g/21 m2) by the
number of V. faba plants per plot (21 m2). Different letters above groups indi­
cate significant differences (significance level: α = 0.05). The Bonferroni
correction method was used to adjust p values for multiple comparisons. Pre­
dicted means and 95 % confidence intervals are displayed in red. V. faba ge­
notypes are ordered according to the predicted means. Figures are based on
model 10 and model 12 (Table 1).
crop stands of V. faba. Thus, the lower number of V. faba inflorescences
per plot (21 m2) in intercrops could be compensated by a higher visual
perceptibility of inflorescences, resulting in a similar total number of
flower visits per plot (21 m2) (Cohen and Shmida, 1993). In some mix­
tures of plant species, above- and below-ground plant interactions have
been found to influence important floral traits that are relevant for
flower visiting insects, such as nectar quality and quantity, and thus are
likely to alter their attractiveness (Baude et al., 2011). Similar mecha­
nisms could also influence the attractiveness of V. faba plants: As LAI
was measured on crop stand level, overall lower LAI levels of
V. faba-wheat intercrops could be due to the presence of winter wheat
plants. Interspecific competition for light between V. faba plants and
winter wheat plants in intercrops could be lower than intraspecific
competition in sole crop stands of V. faba. Consequently, reduced
competition for light could allow V. faba plants in intercrops to allocate
more assimilates in rewards for pollinators (e.g. higher nectar sugar
content) at the expense of other traits which are more relevant under
light competition (e.g. plant height) (Gruntman et al., 2017). This is a
theory that we cannot confirm based on our study. However, there is
evidence that photosynthetically active radiation (PAR) and radiation
use efficiency (RUE) are higher in intercrops than in corresponding sole
crop stands, although an increase in RUE is not necessarily found in all
combined crops (Gou et al., 2017). Another explanation why there was
no difference between both cropping systems could be that the supply of
floral resources in V. faba-wheat intercrops was already sufficient to
attract the maximum number of pollinating bees in our system.
9
Agriculture, Ecosystems and Environment 343 (2023) 108268
Fig. 6. Effects of (A) the total number of flower visits per V. faba plant and (B)
of the number of illegal flower visits per V. faba on yield per V. faba plant (g).
We calculated the yield per V. faba plant (g) as follows: A 10.5 m2 area of each
plot was harvested in August 2019. By doubling, yield was converted from the
harvested area to the cultivated area per plot (21 m2), which represents the
total V. faba yield per plot. Additionally, the number of V. faba plants was
counted in 3 sampling plots per plot (1 m2). The number of V. faba plants in the
cultivated area per plot (21 m2) was estimated by multiplying counts of V. faba
plants in the three 1 m2 sampling plots by 7, which represents the number of
V. faba plants per plot. Yield per V. faba plant (g) was calculated by dividing the
total V. faba yield per plot (g/21 m2) by the number of V. faba plants per plot
(21 m2). The total number of flower visits per V. faba plant and the number of
illegal flower visits per V. faba plant were calculated by dividing the total
number of flower visits per plot (21 m2) and number of illegal flower visits per
plot (21 m2) by the number of V. faba plants per plot (21 m2). The Y-axis is sqrt-
scaled for graphical reasons. Figures are based on model 10 and model
11 (Table 1).
Consequently, an increase in inflorescences beyond a certain point
would not translate into higher number of flower visits by bees, resulting
in a similar number of visits in both cropping systems. Such diminishing
returns were observed for increases in flower cover in terms of wild bee
abundance and species richness (Alison et al., 2022). In our experiment
with rather small study plots arranged in blocks, we could not detect any
difference between sole crops stands and intercrops. However, it has
been shown that bees react differently to flowering resources depending
on the spatial scale (Veddeler et al., 2006). For this reason, future studies
are needed to investigate whether our findings can be confirmed at
larger spatial scales, e.g. at field scale.
While the number of V. faba inflorescences per plot (21 m2) did not
influence the total number of flower visits per plot (21 m2), we found a
moderation of the bees’ foraging behavior. The number of illegal flower
visits per plot (21 m2) increased with an increasing number of V. faba
inflorescences per plot (21 m2). A similar effect was reported by Mar­
zinzig et al. (2018) who observed an increase of both legal and illegal
flower visits with an increasing number of V. faba flowers. However, in
contrast to Marzinzig et al. (2018), we found a slightly decreasing
number of legal flower visits per plot (21 m2) with an increasing number
of V. faba inflorescences per plot (21 m2). There might be a short-term
increase of both foraging strategies (as Marzinzig et al., 2018 re­
ported). However in the long run, an increased number of illegal flower
visits by primary nectar robbers (B. terrestris) preferring mass-flowering
resources (Bänsch et al., 2021; Walther-Hellwig and Frankl, 2000) could
F. Kirsch et al.
result in a higher number of biting holes in the flower tubes. This could
then facilitate nectar robbing by causing shifts from legal to illegal
flower visits performed by secondary nectar robbers, such as honeybees
(Kendall and Smith, 1975; Newman and Thomson, 2005). Thus, high
numbers of V. faba inflorescences per plot (21 m2) could indirectly lead
to a decline of legal flower visits as observed in our study. In contrast,
Beyer et al. (2022) found that increasing local flower cover in faba bean
fields did not affect the nectar robbing behavior of bumblebees but
resulted in reduced nectar robbing by A. mellifera. At this point, it must
still be emphasized that the observed decrease in legal flower visits per
plot (21 m2) with increasing numbers of V. faba inflorescences per plot
(21 m2) was small. That could be related to the fact that some bee
species such as Bombus hortorum and Bombus lapidarius almost always
conduct legal flower visits (Marzinzig et al., 2018). In our study, this was
also the case (Table A.27, Appendix A): Bombus hortorum and Bombus
lapidarius were foraging legally in the vast majority of flower visits and
observed solitary wild bees (e.g. Andrena spp., Anthophora spp, Eucera
nigroaenea) always carried out legal flower visits. These legal flower
visitors were not as abundant as the typical nectar robbers such as
Bombus terrestris agg or Apis mellifera (Table A.3, Appendix A). However,
as the number of flower visits by obligate legal flower visitors probably
increased with a higher amount of flowering resources, as also observed
by Marzinzig et al. (2018), this could compensate to some extent the
increase in nectar robbing.
We also found differences between the two cropping systems in terms
of foraging behavior. Significantly more legal flower visits per plot
(21 m2) were made in sole crop stands of V. faba than in V. faba-wheat
intercrops. This is surprising, as - following our theory above - sole crop
stands are characterized by a higher number of V. faba inflorescences per
plot (21 m2) and should therefore be more dominated by illegal flower
visits. Thus, it could be that factors other than the number of V. faba
inflorescences per plot (21 m2) (e.g. other plant traits, plant stand
characteristics or abiotic and biotic factors) lead to a change in foraging
behavior of bees at the crop stand level (Baude et al., 2011; Chen et al.,
2018; Cohen and Shmida, 1993; Schlinkert et al., 2015). Also contra­
dicting our theory, a higher number of illegal flower visits per plot
(21 m2) was found in intercrops than in sole crops, even though they had
fewer V. faba inflorescences per plot (21 m2). Again, it could be argued
that this could be caused by crop characteristics other than the number
of V. faba inflorescences per plot (21 m2). However, since this effect only
occurs when the number of inflorescences per plot (21 m2) is added as
an explanatory variable to the calculated models, we assume that this
effect is somehow related to the number of V. faba inflorescences per
plot (21 m2). Unfortunately, it is very difficult to clearly identify the
underlying mechanisms based on our experimental design. Although we
found statistical differences between the intercrops and the sole crops in
terms of foraging behavior, there was also a large variability within each
cropping system. The effect sizes of the differences in foraging behavior
between the cropping systems were rather small and should therefore be
interpreted with caution.
4.2. V. faba genotypes, flower visits and foraging behavior
We found significant differences between the V. faba genotypes in
terms of the total number of flower visits per plot (21 m2), the number of
illegal flower visits per plot (21 m2) and the number of legal flower visits
per plot (21 m2). However, we could not find clear links between flower
visitation and V. faba traits such as LAI per plot (21 m2), average V. faba
plant height in cm per plot (21 m2) and number of V. faba inflorescences
per plot (21 m2) as the bees showed very heterogeneous responses. For
instance, the two V. faba genotypes with the highest total number of
flower visits per plot (21 m2), Hiverna/2 and Malibopop, were rather
different in their LAI per plot (21 m2) (second lowest vs. highest),
average V. faba plant height in cm per plot (21 m2) (third smallest vs.
second tallest) and the number of V. faba inflorescences per plot (21 m2)
(second lowest vs. second highest). Consequently, we cannot confirm
10
Agriculture, Ecosystems and Environment 343 (2023) 108268
that average V. faba plant height in cm per plot (21 m2), LAI per plot
(21 m2) and numbers of inflorescences per plot (21 m2) caused the
observed differences between V. faba genotypes in the total number of
flower visits per plot (21 m2) or in the foraging behavior of the bees. As
there is a strong positive correlation between LAI per plot (21 m2) and
average plant height in cm per plot (21 m2), improved perceptibility of
V. faba inflorescences due to higher plants was probably compensated by
a higher coverage of inflorescences with increasing LAI. Furthermore,
other factors could determine the bees’ foraging decisions that were not
recorded in our study. For instance, foraging decisions could be influ­
enced by differences between V. faba genotypes in floral rewards (e.g.
nectar quality and quantity), floral architecture and display (Bailes
et al., 2018; Suso and Maalouf, 2010).
4.3. Flower visits, cropping systems, V. faba genotypes and yields
We found a positive effect of the total number of flower visits per
V. faba plant on the yield per V. faba plant (g) when cropping system was
not included as explanatory variables in the models. This finding is in
line with other studies that reported a positive influence of insect
pollination on the yield components of V. faba (Bartomeus et al., 2014;
Beyer et al., 2022; Varis and Brax, 1990). In our study, this positive
effect seems to be due to the number of illegal flower visits per V. faba
plant, which positively influenced yield per V. faba plant (g), while no
significant effect could be found for the number of legal flower visits per
V. faba plant. Marzinzig et al. (2018) identified B. hortorum, a
bumblebee species that conducts almost exclusively legal flower visits,
as a very efficient pollinator of V. faba that increases seed set and
cross-pollination. Consequently, we expected legal flower visits to have
a positive effect on V. faba yield whereas we assumed illegal flower visits
to have a less strong or even negative impact (Mackin et al., 2021; Smith
et al., 2021). The positive effect of illegal flower visits on V. faba yields
in our study might be related to self-pollination of robbed V. faba
flowers, which could be increased despite the lack of direct pollen
transfer (Kendall and Smith, 1975; Soper, 1952).
The reason why, contrary to our expectations, we did not find an
effect of legal flower visits on the yield per V. faba plant (g) could be that
the legal flower visits were less frequent than the illegal flower visits,
both overall and on average per plot. However, this difference is not very
pronounced. Another explanation could be that the majority of legal
flower visits in our study was not done by the most efficient V. faba
pollinators (Marzinzig et al., 2018). For instance, flower visits by
B. hortorum, although an efficient pollinator even at low densities
(Marzinzig et al., 2018), may still have been too rare to make a differ­
ence (n = 23).
Although we found an effect of bee pollination on the yield per
V. faba plant (g), it must be noted that the observation time of pollinators
per plot was with six minutes relatively short and therefore may have
limited representativeness (Fijen and Kleijn, 2017). Moreover, if we
included cropping system as explanatory variable in the models there
was no such positive effect of pollination. In this case, we instead
detected significant differences between the cropping systems in terms
of yield per V. faba plant (g). Pollination might play a role in deter­
mining yield per V. faba plant, but in our study we cannot disentangle
the effects of increased numbers of illegal flower visits in V. faba-wheat
intercrops and other beneficial agronomic aspects of intercropping
systems. Therefore, it is possible that the higher yield per V. faba plant in
intercrops compared to sole crop systems could mainly be related to
favorable intercropping effects (e.g. complementary root distribution,
improved soil microbial communities and nutrient mobilization)
(Brandmeier et al., 2021; Brooker et al., 2015; Hauggaard-Nielsen and
Jensen, 2005; Li et al., 2014, 2006; Streit et al., 2019).
Finally, we found significant differences between V. faba genotypes
in terms of yield per V. faba plant (g). The best yielding V. faba genotype
was Bering which was characterized by intermediate LAI per plot
(21 m2) (third highest) and small plants (second smallest). This could be
F. Kirsch et al.
related to an reduced lodging risk and lower light competition between
intercropping components, which are important aspects that determine
the performance of V. faba-cereal intercrops in terms of yields (Nelson
et al., 2021).
5. Conclusions
In our study, we could demonstrate that V. faba-wheat intercrops
were used as foraging habitat by insect pollinators. Bumblebees and
honeybees were by far the most abundant flower visitors. Despite a
lower number of V. faba inflorescences per plot (21 m2), V. faba-wheat
intercrops had a similar number of flower visits as sole crops stands of
V. faba, indicating that both cropping systems have the same ecological
value as a foraging habitat for bees. Thus, diversification of wheat
monocultures with V. faba could be considered as a potential measure to
mitigate the loss of floral resources in intensively managed agricultural
landscapes and to bridge periods of floral scarcity. Moreover, we found
that the cropping system influenced pollinator behavior. However, the
main visitors of V. faba (i.e. honeybees and bumblebees) are very mobile
(Bänsch et al., 2020; Westphal et al., 2006) and adapt their foraging
behavior to floral resource availability within agricultural landscapes
(Bänsch et al., 2020; Beyer et al., 2022). For this reason, future studies
should broaden the spatial scope beyond this plot-scale experiment and
investigate pollinator behavior and pollination services in large fields
with V. faba-wheat intercrops and combined sole crop stands of V. faba
and wheat of the same size.
Yield per V. faba plant (g) were positively affected by bee pollination,
with this effect being determined by the number of illegal flower visits
rather than the number of legal flower visits per V. faba plant. This
suggests that illegal flower visits do not adversely affect V. faba yields
and may even have a positive effect due to self-pollination. However,
there were also differences between V. faba genotypes and cropping
systems in terms of yields per V. faba plant, showing that these aspects
are as well important to increase V. faba yields. The fact that we found
higher yields per V. faba plants in V. faba-wheat intercrops compared to
sole crop stands might be related to agronomic advantages of this
cultivation technique (Brandmeier et al., 2021; Brooker et al., 2015;
Hauggaard-Nielsen and Jensen, 2005; Li et al., 2014, 2006).
V. faba genotypes differed in three plant traits (LAI per plot (21 m2),
average V. faba plant height in cm per plot (21 m2), number of V. faba
inflorescences per plot (21 m2)), but none of these traits could be clearly
linked to higher numbers of flower visits by foraging insects. Therefore,
we conclude that other plant traits, such as flower morphology, nectar
and pollen quality and quantity (Bailes et al., 2018; Suso and Maalouf,
2010) might be more relevant to determine the attractiveness of V. faba
genotypes for flower visiting insects. More studies are needed to identify
plant traits or stand characteristics that enhance the attractiveness and
floral rewards of V. faba-wheat intercropping systems. These studies
could be integrated in future breeding programs targeting, on the one
hand, high yielding varieties that are suitable for intercropping. On the
other hand, breeding programs should also promote biodiversity and
related ecosystem services, like pollination, by enhancing floral rewards
(Bailes et al., 2018; Barot et al., 2017; Palmer et al., 2009).
CRediT authorship contribution statement
This study was conceptualized by WL and CW. Methodology was
designed by CW and FK. Data collection, statistical analysis and writing
of the manuscript were done by FK with the support and advice of WL,
ALH and CW. WL, AHL and CW reviewed and edited the manuscript.
Declaration of Competing Interest
The authors declare the following financial interests/personal re­
lationships which may be considered as potential competing interests:
Catrin Westphal reports financial support was provided by German
11
Agriculture, Ecosystems and Environment 343 (2023) 108268
Research Foundation. Felix Kirsch reports financial support was pro­
vided by German Federal Ministry of Education and Research. To create
two graphs, we (the authors) used a green plant symbol created by ©
BFlores (WMF), CC BY-SA 4.0 <https://creativecommons.org/licenses/
by-sa/4.0 > , via Wikimedia Commons. BFlores (WMF) has granted the
authors permission to use this symbol for publication in Agriculture,
Ecosystems & Environment on the condition that: -> that the original
creator is credited by the authors of the publication. -> The modified
graph is shared via Wikimedia Commons to comply with the license
conditions. Neither BFlores (WMF) nor we have any financial benefit
from this agreement. We intend to comply with these conditions and
hope that Agriculture, Ecosystems & Environment and Elsevier also
agree to the use of the symbol in our publication.
Data Availability
Data is available in the GRO-Data repository under https://doi.org/
10.25625/ISYJJE.
Acknowledgements
This study was part of the IMPAC3 project that was coordinated by
the Centre of Biodiversity and Sustainable Land Use of the University of
Göttingen, Germany. IMPAC3 was funded by the German Federal Min­
istry of Education and Research (BMBF, grant number 031A351A). We
thank the Norddeutsche Pflanzenzucht (NPZ) for the provided genetic
material. We are especially grateful for the advice and help of Dr. Horst
Henning Steinmann, Regina Martsch, Tina Tietz, Vinay Challa, Aiza
Fernanda Cantillo Rodriguez, Dr. Nicole Beyer, Dr. Reiner Theunert, Dr.
Marco Ferrante, Klara Küpers, Dr. Anjaharinony Andry Ny Aina Rako­
tomalala and Mike Kuschereitz. Moreover, we thank Dr. Petit-Michaut
and the two anonymous reviewers for their comments that helped to
improve the manuscript. CW is grateful for funding by the Deutsche
Forschungsgemeinschaft (DFG) (Project numbers 405945293 and
493487387).
Appendix A. Supporting information
Supplementary data associated with this article can be found in the
online version at doi:10.1016/j.agee.2022.108268.
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