The effectiveness of indirect plant defence is dependent on plant competition

Abstract

1 INTRODUCTION

To mitigate the effects of herbivory, plants may invest in a broad array of defence strategies (Agrawal, 2011). These strategies are usually divided into two categories: direct defence that affects the performance of the herbivores, for example, through the production of adverse chemicals and physical impediments (Schoonhoven et al., 2005), and indirect defence, whereby plants promote the top-down control of herbivores by recruitment of natural enemies, for example, via the production of shelters, extrafloral nectar or the release of herbivore-induced plant volatiles (Pearse et al., 2020). The evolution of plant traits that enhance the top-down control of herbivory is evident in relationships that involve resource-mediated indirect defence, such as the presence of fruit bodies or shelters to house predators (Kessler & Heil, 2011). The evolution of such plant traits often coincides with the specialization of predators such as ants, to use the housing and fruit bodies of the plant while offering strong defensive services that reduce plant fitness loss by herbivory (Heil & McKey, 2003). The evolution of information-mediated indirect defence by plant volatiles is strongly debated (Kessler & Heil, 2011). The attraction of predators and parasitoids by herbivore-induced plant volatiles is likely ubiquitous in all terrestrial ecosystems (Pearse et al., 2020; Turlings & Erb, 2018). However, only very few studies have identified a link between volatile emission, the attraction of natural enemies and plant fitness (Hare, 2011; Kergunteuil et al., 2019; Schuman et al., 2012).

One general reason for why information-mediated indirect defence may not be evident is that volatiles are used by many other community members that influence the fitness of individual plants (Poelman, 2015; Turlings & Erb, 2018). A second reason is that parasitoids, a prevalent group of natural enemies that respond to herbivore-induced plant volatiles to locate their herbivorous hosts (Godfray, 1994), do not always mitigate the impact of herbivory on plants (Cuny et al., 2021; Cuny & Poelman, 2022; Pearse et al., 2020; van der Meijden & Klinkhamer, 2000). In other words, it is unclear whether indirect defence through the release of plant volatiles evolved to specifically attract parasitoids. There are several reasons for this ongoing debate: (1) Some parasitoid species allow the host to grow until the parasitoid larvae are fully grown (Mackauer & Sequeira, 1993) and, thus, feeding damage still occurs following parasitism. Hosts parasitized by some species (mostly gregarious ones) inflict even more damage than unparasitized ones (Ode, 2006); (2) even if parasitism reduces feeding by the host, this may not affect plant fitness if plants tolerate some degree of damage and even compensate for tissue loss by regrowth (Blatt et al., 2008); and (3) parasitism may alter the herbivore's oral cues, impairing the plant's ability to mount a specific defence response (Tan et al., 2019). Only a few studies have investigated the effect of parasitoids on plant fitness using herbivores feeding on leaves (Bustos-Segura et al., 2020; Cuny et al., 2018; Hoballah & Turlings, 2001; van Loon et al., 2000), flowers (Gols et al., 2015) or seeds (Cuny et al., 2022; Gómez & Zamora, 1994). It is worth noting that while most studies have found a positive effect of parasitoids on plant fitness (Gols et al., 2015; Pearse et al., 2020; Romero & Koricheva, 2011), the impact of these interactions has often not been studied under natural conditions that include, among others, plant–plant competition or plant exposure to their full community of insects. We hypothesize that the effect of parasitoids on plant fitness is influenced by the plant's ability to tolerate herbivory, which may be reduced in environments where plants compete for resources.

Plants have to compete with other plants for access to resources, such as light, in particular when plants grow at high densities. In order to avoid being shaded, plants have evolved strategies to adapt their phenotype to the presence of neighbours (Ballaré & Pierik, 2017). The ‘shade avoidance syndrome’ refers to the phenotypic changes induced by the presence of competitors, which are triggered by the ratio of red to far-red light detected by plants (Ballaré et al., 1990). Plants experiencing this syndrome are typically taller relative to their total biomass, thinner and downregulate their direct defences (Ballaré & Pierik, 2017). However, the effect of plant competition on indirect defence responses is less clear: plant volatile emissions seem to either increase or decrease depending on several factors such as the compound class, plant species, type of damage and volatiles perceived from neighbouring plants (Kessler et al., 2023). Plant competition exerts a strong selection pressure, as it can significantly reduce the fitness of plants that are outcompeted (Züst & Agrawal, 2017). Biotic factors like herbivory can reduce plant fitness by causing early loss of photosynthetic tissue, which decreases growth and competitive ability (de Vries et al., 2018; Schädler et al., 2007). However, plants have evolved several strategies to maximize their fitness in the face of herbivory. For instance, they can compensate for, or tolerate, herbivore damage in order to maintain their fitness (Simms, 2000). Damaged plants undergo morphological and physiological changes, such as an increased photosynthetic rate or a modified plant architecture and metabolite storage pattern (Strauss & Agrawal, 1999). This allows plants to cope with tissue loss and maximize their fitness. Plant compensation of herbivore damage is a continuum that ranges from low compensation, where the damaged plant still suffers significantly in terms of fitness, to complete compensation, where there is no fitness difference between damaged and undamaged plants, and even overcompensation, where damaged plants have higher fitness than undamaged plants (Camargo, 2020).

Here, we conducted an experiment using wild Brassica nigra plants grown in an open field at two different densities to investigate the following questions: (1) how does parasitism of Pieris brassicae by the solitary parasitoid Hyposoter ebeninus affect herbivore damage and plant seed production and (2) does the level of plant–plant competition influence the effect of parasitized caterpillars on herbivore damage and plant seed production? Furthermore, we utilized a three-dimensional functional–structural plant (FSP) modelling technique (Evers, 2016; Vos et al., 2010) to further investigate questions raised by the results of our field experiment. This modelling approach allows for the testing of complex ecological scenarios and has previously been applied to our plant–herbivore system (de Vries et al., 2019; Douma et al., 2019). Specifically, we used the model presented in de Vries et al. (2018) to answer the following questions: (3) How much damage by caterpillars and what percentage of parasitism are needed to observe a significant effect on seed production of plants that are not in competition, (4) when plants are in competition, how much damage needs to be inflicted to a plant before it is being outcompeted by its close neighbours and (5) do plant density and feeding by parasitized caterpillars interact in terms of plant seed production? We discuss our results in the context of the evolution of indirect plant defence.