Direct and Indirect Chemical Defences Against Insects in a Multitrophic Framework

bs_bs_banner Plant, Cell and Environment (2014) 37, 1741–1752 doi: 10.1111/pce.12318 Review Direct and indirect chemical defences against insects in a multitrophic framework Rieta Gols Laboratory of Entomology, Department of Plant Sciences, Wageningen University, Wageningen 6708 PB, The Netherlands higher plant species (Pichersky & Lewinsohn 2011). The diversity of secondary or specialized metabolites across species is tremendous and likely exceeds 200 000 (Pichersky & Lewinsohn 2011). Primary plant metabolites, such as proteins, carbohydrates and lipids, are important for basic physiological processes in plants and are often also essential nutrients for insects (Scriber & Slansky 1981; Schoonhoven et al. 2005). ABSTRACT Plant secondary metabolites play an important role in medi- ating interactions with insect herbivores and their natural enemies. Metabolites stored in plant tissues are usually investigated in relation to herbivore behaviour and performance (direct defence), whereas volatile metabolites are often studied in relation to natural enemy attraction (indirect defence). However, so-called direct and indirect defences may also affect the behaviour and performance of the herbivore’s natural enemies and the natural enemy’s prey or hosts, respectively. This suggests that the distinction between these defence strategies may not be as black and white as is often portrayed in the literature. The ecological costs associated with direct and indirect chemical defence are often poorly understood. Chemical defence traits are often studied in two-species interactions in highly simplified experiments. However, in nature, plants and insects are often engaged in mutualistic interactions with microbes that may also affect plant secondary chemistry. Moreover, plants are challenged by threats above- and belowground and herbivory may have consequences for plant–insect multitrophic interactions in the alternative compartment mediated by changes in plant secondary chemistry. These additional associations further increase the complexity of interaction networks. Conse- quently, the effect of a putative defence trait may be under- or overestimated when other interactions are not considered. Secondary plant metabolites play an important role in plant interactions with the biotic and abiotic environment (Schoonhoven et al. 2005; Iason et al. 2012). The defence properties of these phytochemicals against a broad range of organisms such as insect herbivores and pathogens dominate the literature on plant secondary metabolites. In addition, volatile metabolites may serve as signals in the communication with other organisms in the environment. For example, herbivore-induced plant volatiles mediate interactions with neighbouring plants, herbivores, natural enemies of herbivores and pollinators (Heil & Karban 2010; Bruce & Pickett 2011; Lucas-Barbosa et al. 2011). More recently, the role of plant volatiles as a means for within-plant signalling to bypass vascular constraints has been demonstrated (Karban et al. 2006; Frost et al. 2007; Heil & Silva Bueno 2007). Plant defences against insect herbivores are often divided into direct and indirect defences. In the literature, direct plant defences, or more appropriately direct resistance, refer to traits that act upon the attacker directly, such as the presence of adverse chemical substances in plant tissues that interfere with growth and development of the consumers (Schoonhoven et al. 2005) and as a result reduce the amount of damage inflicted to the plant. Indirect defences promote the efficiency of natural enemies to control plant antagonists (Heil 2008) in order to reduce herbivory. For example, volatile plant metabolites that are produced in response to feeding by insect herbivores guide the herbivore’s natural enemies to the damaged plant (Vet & Dicke 1992). Direct and indirect defences are often studied independently. However, chemicals associated with indirect defence may also affect the behaviour of the herbivores (Bruce et al. 2005) and chemicals associated with direct defence may also have consequences for the development of the herbivore’s natural enemies mediated through the herbivore’s food plant (Ode 2006; Gols & Harvey 2009). Key-words: direct defence; herbivory; HIPV; indirect defence; insect–plant interactions; natural enemies; parasitoid; plant secondary metabolites; VOC. INTRODUCTION Plants produce an enormous array of different chemicals that are usually divided into primary and secondary metabolites. The first group of metabolites refers to chemicals that are essential for plant growth and development, and are commonly produced by most plant species. Metabolites in the second group aid plant growth and development, but are not essential for survival and often have a more restricted phylogenetic distribution. Arabidopsis thaliana L. is roughly estimated to produce up to 11 000 different metabolites of which approximately 70–80% are commonly produced by Levels of secondary metabolites associated with defence often change in response to herbivory (Karban & Baldwin 1997; Agrawal et al. 1999) and more recently epigenetic Correspondence: R. Gols. E-mail: [email protected] © 2014 John Wiley & Sons Ltd 1741 1742 R. Gols effects of insect-induced resistance have been reported (Rasmann et al. 2012).These induced changes can have longlasting consequences not only for the attacking species but also for the plant’s interactions with other members of its associated community (Poelman et al. 2008; Stam et al. in press). This suggests that the distinction between direct and indirect defences is diffuse, which is the main topic of this paper. I will further discuss potential conflicts between direct and indirect chemical defences or alternatively the potential for trade-offs between the two plant traits. I will focus on interactions among plants, insect herbivores and their natural enemies such as predators and parasitoid wasps as mediated by low molecular mass secondary plant metabolites. I will pay particular attention to the literature on plant–insect interactions in the Brassicaceae as these interactions are well studied in this plant family, which includes cabbage vegetables and mustard oil varieties. Finally, I will argue that the term ‘defence’ as described above and is used in many studies investigating the role of secondary metabolites in plant– insect interactions should be used more carefully. Berenbaum & Zangerl 2008; Ali & Agrawal 2012). As is often the case in ecology, there are examples where there is evidence for co-evolutionary processes determining plant defence chemistry levels (Zangerl & Berenbaum 2005), but there is also evidence that plants employ alternative strategies, such as tolerance, to overcome herbivory (Strauss & Agrawal 1999; Agrawal & Fishbein 2008). In addition, defence levels in natural populations may be less determined by pairwise interactions and instead are the consequence of diffuse selection involving multiple-species interactions (Strauss & Irwin 2004). Moreover, insects themselves may actively manipulate plant defences or prevent exposure to toxic plant metabolites by feeding on less toxic tissues, ‘trenching’ (Dussourd 1993), or by actively manipulating the plant’s defence response (Kahl et al. 2000). Especially phloem-feeding aphids and white flies are well known for deceiving the plant to modify the sequence of events that normally follow upon wounding by herbivores (Walling 2008).Well-adapted insects may even co-opt plant chemical defences and use them in defence against their own attackers through sequestration of these compounds from their food plants (Nishida 2002; Hartmann 2004; Zagrobelny & Moller 2011). SECONDARY METABOLITES: FROM BITROPHIC TO MULTITROPHIC INTERACTIONS Whether plant secondary plant metabolites function as defence chemicals preventing plant damage depends to a large extent on the degree of specialization of the herbivore. Moreover, plants may tolerate certain levels of herbivory without serious consequences for their performance. Traditionally, the role of secondary metabolites in defence against insects is investigated in bitrophic interactions, that is, between plants and insect herbivores. In this section, I will broaden this topic and discuss interactions with other organisms in different trophic levels that are directly or indirectly mediated by secondary plant chemistry. Herbivore-mediated effects of secondary metabolites on natural enemy interactions Plant herbivore interactions Price et al. (1980) emphasized the importance of including the third trophic level when interactions with plant and herbivores are investigated. However, when natural enemies of insect herbivores are included in studies investigating the defensive function of plant traits, their effects on the different interacting organisms may not necessarily be that straightforward. For example, morphological traits may hamper similarly sized herbivores and their natural enemies alike. In addition, exposure to ingested secondary metabolites has been shown to be toxic to natural enemies such as parasitoids (Campbell & Duffey 1981; Barbosa et al. 1991; Ode et al. 2004; Harvey et al. 2007) and predators (Nishida 2002; Hartmann 2004; Müller 2009). For an endoparasitoid, whose larval development is intimately linked to the physiology of its host, exposure to toxic compounds in the host may be difficult to avoid. The presence of high toxin concentrations underlies the ‘nasty host’ hypothesis which states that certain groups of parasitoids, for example, larval koinobiont endoparasitoids, that is, parasitoid species that allow the host to feed and grow after parasitism (Harvey 2005), are less well represented in tropical than in temperate ecosystems due to the fact that their hosts feed on plants with comparatively higher levels of secondary metabolites (Gauld et al. 1992; Quicke 2012). A large amount of studies have investigated the role of plant secondary metabolites in defence against herbivory (Schoonhoven et al. 2005). In fact, the evolution and maintenance of the enormous diversity in secondary metabolites in relation to plant–insect interactions is one of the central topics in evolutionary ecology (Iason et al. 2012). In general, insect herbivores choose their diet and adjust their food intake based on the balance between sufficient levels of nutrients and the absence or low levels of adverse metabolites (Scriber & Slansky 1981; Slansky 1993). In their seminal paper, Ehrlich & Raven (1964) developed the theory of the co-evolutionary arm’s race between plants and insects, where insects select for higher levels of toxins in plants and the insects in turn respond by developing adaptations to these adverse chemicals. Often the distribution of certain compounds is restricted to a limited number of plant families, genera or even species (Wink 2003) and specialized insect herbivores select their host plants for oviposition or feeding often based on food plant-specific secondary metabolites (Bruce et al. 2005; Schoonhoven et al. 2005; Hopkins et al. 2009). The debate whether chemical co-evolution is the mechanism underlying selection for increased levels of secondary plant metabolites persists (Bernays & Graham 1988; van der Meijden 1996; Strauss & Irwin 2004; Thompson 2005; Reduced growth of the host itself on more toxic plants may compromise growth and development of the parasitoid © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 Plant chemical defences against insects 1743 larvae developing in or on these herbivores (Harvey et al. 2005; Gols & Harvey 2009; Bukovinszky et al. 2012). Prolonged herbivore development may increase the time window that herbivores are exposed to predation and parasitism (‘slow-growth-high-mortality’ hypothesis, Benrey & Denno 1997). As most parasitoid species attack only specific developmental stages of their hosts, in contrast to predators that can consume a larger range of prey, prolongation of the vulnerable stages is predicted to affect parasitism more than predation risk. However, the limited number of studies that have empirically tested the slow-growth-high-mortality hypothesis for parasitoids shows little evidence for higher parasitism rates in hosts that grow more slowly (Benrey & Denno 1997; Williams 1999; Cornelissen & Stiling 2006). Food plant quality determined by primary and secondary metabolites may affect the immune response of herbivorous hosts to parasitism. In contrast to predation where the host is instantly killed, koinobiont parasitoids kill the host only after their larval development is completed. During this extended interaction, the host’s immune system may prevent successful parasitism by encapsulating and consecutively killing the parasitoid eggs or larvae. Plant quality may reduce the host’s immune response. For example, Bukovinszky et al. (2009) reported that hosts developing on nutritious plants with low levels of secondary metabolites encapsulated more parasitoid eggs than hosts feeding on plants containing high levels of secondary metabolites. This effect was even more pronounced in plants that were induced by previous herbivore feeding (Bukovinszky et al. 2009). In these situations, induced defence levels also enhanced the success of parasitism through suppression of the host’s immune response (Bukovinszky et al. 2009; Reudler et al. 2011). On the other hand, plant-derived components may also improve the ability to mount an immune response and prevent parasitism. For instance, the encapsulation rate of a foreign object by larvae of an Arctiid moth Parasemia plantaginis L. varied with food plant species and this ability correlated positively with antioxidant concentrations in the diet of the host (Ojala et al. 2005). Beneficial associations with microorganisms such as mycorrhizal fungi and growth-promoting rhizobacteria can further influence the plant’s nutritional and defence status. As nitrogen is a growth-limiting nutrient, insects tend to grow larger or faster with higher efficiencies of conversion on plants under high compared with low nutrient conditions (Scriber & Slansky 1981). Non-pathogenic microbial interactions belowground can enhance or prime the plant’s defence machinery against pathogen and insect attack aboveground, a process that is referred to as induced systemic resistance (ISR) (Pineda et al. 2010).These mutualistic interactions with soil microbes can impact on the behaviour and performance of associated aboveground organisms in different trophic levels through changes in plant chemistry. In general, mycorrhyzal fungi have a positive or neutral effect on the performance of phloem-feeding herbivores and specialist leaf chewers, whereas they have a negative effect on generalist chewers (Koricheva et al. 2009). Similar patterns are recognized for the interaction between insect herbivores and growth-promoting rhizobacteria (Pineda et al. 2013a) and insects and nitrogen-fixating rhizobia (Thamer et al. 2011). Little is known about the effect of beneficial soil microbes on the performance of natural enemies, or on volatile-mediated foraging behaviour (see next section) (Van der Putten et al. 2001; Hartley & Gange 2009). Plants, but also insects, may rely on beneficial interactions with microbial organisms that are able to modify secondary chemistry.These associations further increase the complexity of interactions mediated by plant primary and secondary chemistry. VOLATILE PLANT SECONDARY METABOLITES MEDIATE INTERACTIONS AMONG SPECIES IN DIFFERENT TROPHIC LEVELS So far, I have discussed the influence of secondary metabolites with low volatilities that are stored in plant tissues, though some of these compounds may also play a role in plant–insect interactions based on insect olfaction (Bruce et al. 2005) and play a role in direct defence. In this section, I will focus on insect behaviour mediated by volatile plant secondary metabolites and discuss their putative function in indirect defence. Some of these examples demonstrate that effects of secondary metabolites may not only negatively impact on the performance of the herbivore, but also on beneficial interactions with the herbivores natural enemies. The concept of ‘talking plants’ by means of volatile emissions has intrigued many ecologists over the last three decades (Baldwin & Schultz 1983; Turlings et al. 1990; Dicke & Baldwin 2010). In relation to plant–insect interactions, their role in indirect defence has been well investigated, that is, the attractiveness of herbivore-induced plant volatiles to the herbivore’s natural enemies (Dicke & Baldwin 2010; Mumm & Dicke 2010; Kessler & Heil 2011; McCormick et al. 2012). However, the function of plant organic volatiles per se (Penuelas & Llusia 2004) and their role in reducing herbivory is still controversial (van der Meijden & Klinkhamer 2000; Hare 2011; Kessler & Heil 2011). These volatile emissions do not only attract natural enemies of herbivores, but also have been reported to play a role in plant-plant communication (Karban & Shiojiri 2009; Heil & Karban 2010), in host plant Modification of plant secondary chemistry through microbial mutualistic interactions Plants may rely on other organisms to defend them against antagonists. Symbiotic endophytes, especially in grasses, produce secondary metabolites increasing the plant’s resistance to herbivores (Hartley & Gange 2009), which may move up in the food chain and negatively impact the development of parasitoids and predators consuming these hosts (Bultman et al. 1997; de Sassi et al. 2006). Conversely, symbiotic interactions with bacteria may assist herbivores in host plant utilization by suppression of the plant’s defensive response to herbivory and other physiological processes such as senescence (Kaiser et al. 2010; Frago et al. 2012; Chung et al. 2013). © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 1744 R. Gols selection by herbivores (Bruce et al. 2005) and in the foraging behaviour of hyperparasitoids (i.e. parasitoids of parasitoids) (Poelman et al. 2012). Conflicts may arise from the plant’s perspective when in response to herbivory not only natural enemies are attracted to these ‘advertising’ plants, but also the herbivores themselves (Nottingham et al. 1991; Renwick et al. 2006; Halitschke et al. 2008) as well as enemies of the natural enemies (Poelman et al. 2012). Moreover, the distinction between direct and indirect defences becomes hazy when induced volatiles also increase levels of direct defence or prepare plants to respond faster to future attacks, so-called priming (Conrath et al. 2006; Halitschke et al. 2008). the vegetation in the habitat matrix (Gols et al. 2005; Bukovinszky et al. 2007; Bezemer et al. 2010; Meiners et al. 2010; Randlkofer et al. 2010). In addition, laboratory studies often involve unnatural non-coevolved associations combining arthropods native to different biological realms. In particular, plant–insect interactions using Arabidopsis are a good example illustrating this point. Under natural condition, plants are embedded in a vegetation consisting of different plant species that may chemically and or structurally interfere with insect foraging (Gols et al. 2005; Bukovinszky et al. 2007; Bezemer et al. 2010; Meiners et al. 2010; Randlkofer et al. 2010). The arthropod community has to deal not only with this ‘noise’, but also with the spatial heterogeneity in the habitat which is usually absent in highly controlled laboratory studies as illustrated in Fig. 1. Volatile-mediated foraging behaviour of insect parasitoids and other natural enemies of insect herbivores Despite the numerous studies reporting on parasitoid attraction towards herbivore-induced plant volatiles, little is known about the identity of the compounds or about the ratio between volatile compounds that determine blend attractiveness (Pareja et al. 2009; Gols et al. 2011; Hare 2011), although several studies have demonstrated that subtle changes in volatile emissions can be perceived by natural enemies of insect herbivores (Shiojiri et al. 2006; Zhang et al. 2009; Gols et al. 2012; de Rijk et al. 2013). Moreover, parasitoids are known to be flexible in their response to these volatile blends through the process of associative learning (Vet et al. 1990; Hoedjes et al. 2011). Thus, depending on the experience status of the wasp, the response to volatile blends may vary accordingly. However, this strategy seems more beneficial to the parasitoid than to the emitting plant. If the emission of attractive blends functions as an indirect defence, what blend should the plant emit when the response to these volatiles is dynamic? Frequency-dependent selection and the degree of intimacy between the plant and the plant’s presumed mutualists determine to a large extent the defensive value of the selected trait. In other words, the importance of herbivore-induced plant volatiles as an indirect defence trait may be limited in an environment where the presence of natural enemies is highly unpredictable. This contrasts with indirect defence traits in plant–ant associations where the ants permanently inhabit the plants or when rewards are produced only when the ants are present (Kessler & Heil 2011). Alternatively, the cost of expressing these traits is limited or the function of this trait is not primarily defensive. The ecological costs of volatile emissions are often ignored and have only recently begun to be more appreciated (Ali et al. 2011; Kessler et al. 2011; Poelman et al. 2012; Robert et al. 2013). For parasitism to be successful, several sequential steps have to be accomplished (Vinson 1998). The first steps include habitat and host location, which in the case of parasitoids of herbivorous hosts are often mediated by plant volatiles, especially those emitted by the plant when damaged by the host (Vet & Dicke 1992).The question is whether natural enemies are equally attracted to plants that vary in levels of direct defence chemicals. For example, herbivores feeding on more toxic plants in the field have been shown to be less prone to parasitism (Nieminen et al. 2003; Ode et al. 2004). It is unknown in these examples whether lower parasitism is caused by the fact that the parasitoids are less attracted to these plants, whether they reject the more toxic hosts for parasitism, or whether parasitism success is compromised by enhanced parasitism immunity in hosts feeding on more toxic plants. The study of indirect defences, that is, the attraction of natural enemies through the emission of plant volatiles, relies with a few exceptions (Halitschke et al. 2008; Poelman et al. 2009; Schuman et al. 2012) on highly simplified wind tunnel or Y-tube olfactometer bioassays (Hunter 2002). In these bioassays, parasitoids or predators that are most responsive to plant volatiles (only certain age classes are used) are given the choice between two contrasting odour sources. Parasitism success is not only determined by efficient host location behaviour, in which plant volatiles play a pivotal role. The ability to overcome the host’s immune response is an important intrinsic factor and has been demonstrated to be also affected by the host food plant. In general, parasitoid attraction to herbivore-induced plant volatiles is often studied without confirming that this attraction results in increased parasitism and parasitism success. Considering that the physiological status (age, energy reserves) of parasitoids varies, their foraging behaviour in nature and their response to volatiles may vary accordingly (Steinberg et al. 1992; Winkler et al. 2006). Volatile-mediated foraging behaviour in the field may not reflect the volatilemediated decisions as they are made in simplistic laboratory bioassays. More importantly, the ability of herbivores and their natural enemies to detect and respond to volatiles may strongly depend on the identity of the physical structure of

Direct and Indirect Chemical Defences Against Insects in a Multitrophic Framework

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