Introduction
Stressors are biotic or abiotic variables that cause a negative response
in a taxa or community (Barrett et al., 1976; Vinebrooke et al., 2004).
For crop plants that benefit from insect pollination, insect herbivory
and a lack of pollination can be referred to as biotic stressors if they
negatively affect yield. Occasionally, compensatory responses may result
in higher yields in herbivore-attacked plants compared to un-attacked
plants (overcompensation, Poveda et al., 2010) and pollination benefits
to yield may vary from negative to positive within and between cultivars
(Bishop et al., 2020; Lundin & Raderschall, 2021). Therefore, the
characterization of herbivory and lack of pollination as crop stressors
is not clear cut, but rather a nuanced one that will depend on the
frequency, timing and quantity of herbivory/pollination as well as
modifiers such as nutrient availability and cultivar (Poveda et al.,
2010). To characterize crop stressors it is thus important to explore
such nuances (e.g. does herbivory or lack of pollination lead to yield
overcompensation?) and investigate the potential for interactions among
hypothesized stressors on crop yield (Peterson & Higley, 2000; Piggott
et al., 2015). Stressors can interact in an additive, synergistic or
antagonistic manner on plant growth and reproduction, making net effects
on crop yield challenging to predict (Supplementary material, Fig. S1A).
Empirically quantifying plant stressors and their interactions,
particularly in agroecosystems, will help guide sustainable crop
management strategies (Cote et al., 2016; Gagic et al., 2019; Saunders
et al., 2016; Sutter & Albrecht, 2016).
Lack of insect pollination and insect herbivory may independently
(additively), synergistically or antagonistically affect yield of
pollinator-dependent crops. A synergistic effect between these stressors
would result when the combined negative effect on yield, due to low
insect pollination and herbivory, is higher than the sum of their
individual effects. Alternatively, an antagonistic effect would result
when yield loss due to lack of insect pollination and herbivory is lower
than the sum of their individual effects. This may be the case if
herbivore‐induced plant overcompensation has the capacity to minimize
the negative effect of lack of pollination (Järemo et al., 1999;
Munguía-Rosas et al., 2015) or if the herbivore directly benefits plant
reproduction by acting as a pollinator (i.e. some florivores, see:
McCall & Irwin, 2006). Interactions between insect pollination and
herbivory have recently been found to influence plant trait evolution
(Ramos & Schiestl, 2019) and crop yield (Bartomeus et al., 2015; Gagic
et al., 2019; Garibaldi et al., 2018; Lundin et al., 2013; Raderschall
et al., 2021; Saunders et al., 2016; Sutter & Albrecht, 2016; Tamburini
et al., 2019). Compensatory responses of crops to herbivory, and effects
of florivorous herbivores on yield are important and under‐investigated
mechanisms as they can maintain or even increase yield of crops exposed
to pests (Gagic et al., 2016; Poveda et al., 2018). A recent
meta-analysis found that overcompensation for insect herbivory in plants
is pervasive and can increase crop yield (Garcia & Eubanks, 2019). For
example, flower abortion due to herbivory can lead damaged plants to
grow larger fruits (Sánchez & Lacasa, 2008) or produce more flowers
(Peschiutta et al., 2020) than plants without herbivory. Despite yield
increases, overcompensation due to herbivory may decrease yield quality
(Peschiutta et al., 2020) and reduce the marketable crop. These
mechanisms in interaction with pollination services can be particularly
important in crops with large compensatory potential to biotic and
abiotic stressors, such as faba bean (Vicia faba L.)
(López-Bellido et al., 2005).
Faba bean is an important nitrogen-fixating legume crop grown worldwide
(Jensen et al., 2010; Karkanis et al., 2018). Over the past 50 years,
faba bean cropping area has been declining due to yield instabilities,
associated to abiotic stress, pest and pathogen pressure (Karkanis et
al., 2018), and possibly uneven insect pollination. Faba beans are
partially dependent on insect pollinators (Bishop & Nakagawa, 2021).
While insect pollination generally increases faba bean yield and yield
stability (Suso & del Río, 2015; Suso & Maalouf, 2010), pollination
dependence within cultivars varies greatly, from -4 to 46% (loss in
yield per plant without pollination)(Bishop et al., 2020). A recent
study found that insect pollination benefit in faba bean, measured as
the increase in bean weight per plant, lessened with aphid herbivory
(Raderschall et al., 2021). This variability in pollination benefit
underlines the importance to investigate interactions between
pollinators and major pests if we want to understand factors affecting
yield variability in faba beans.
A key pest in faba bean is Bruchus rufimanus (Boh.) (Segers et
al., 2021). Adult beetles colonise the crop in spring to feed on pollen
and nectar, and start laying eggs on developing pods (Segers et al.,
2021). When the larvae hatch, they bore through the pods and develop and
feed inside the beans. We use the term ‘herbivory’ to include both
florivory by the B. rufimanus adults and seed predation by the
larvae. Larval feeding reduces seed weight and quality (Epperlein, 1992;
Roubinet, 2016; Segers et al., 2021). Adult beetles might have
additional negative effects on yield if their feeding on pollen disrupts
pollinator visitation (Ye et al., 2017), or, alternatively, positive
effects if they pollinate (Krupnick & Weis, 1999; McCall & Irwin,
2006). Interactions between pollinators and B. rufimanus on faba
bean growth and yield have so far not been investigated.
Here we evaluate the effect of herbivory by the pest B. rufimanuson faba bean yield components and ask how interactions between two
hypothesized stressors, namely lack of pollination from bumblebees, and
herbivory by B. rufimanus , affect above- and belowground
plant traits and yield of faba bean. Specifically, we investigate
whether flower visitation by pollinators changes with the inclusion of
herbivores, and/or if there is over-compensatory growth of the plant in
response to B. rufimanus damage in the presence of pollinators.