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.