Direct and Indirect Chemical Defences Against Insects in a Multitrophic Framework

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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

ABSTRACT higher plant species (Pichersky & Lewinsohn 2011). The diversity of secondary or specialized metabolites across Plant secondary metabolites play an important role in medi- species is tremendous and likely exceeds 200 000 (Pichersky ating interactions with insect herbivores and their natural & Lewinsohn 2011). Primary plant metabolites, such as pro- enemies. Metabolites stored in plant tissues are usually inves- teins, carbohydrates and lipids, are important for basic tigated in relation to herbivore behaviour and performance physiological processes in plants and are often also essential (direct defence), whereas volatile metabolites are often nutrients for insects (Scriber & Slansky 1981; Schoonhoven studied in relation to natural enemy attraction (indirect et al. 2005). defence). However, so-called direct and indirect defences Secondary plant metabolites play an important role in may also affect the behaviour and performance of the herb- plant interactions with the biotic and abiotic environment ivore’s natural enemies and the natural enemy’s prey or (Schoonhoven et al. 2005; Iason et al. 2012). The defence hosts, respectively. This suggests that the distinction between properties of these phytochemicals against a broad range of these defence strategies may not be as black and white as is organisms such as insect herbivores and pathogens dominate often portrayed in the literature. The ecological costs associ- the literature on plant secondary metabolites. In addition, ated with direct and indirect chemical defence are often volatile metabolites may serve as signals in the communica- poorly understood. Chemical defence traits are often studied tion with other organisms in the environment. For example, in two-species interactions in highly simplified experiments. herbivore-induced plant volatiles mediate interactions with However, in nature, plants and insects are often engaged in neighbouring plants, herbivores, natural enemies of herbi- mutualistic interactions with microbes that may also affect vores and pollinators (Heil & Karban 2010; Bruce & Pickett plant secondary chemistry. Moreover, plants are challenged 2011; Lucas-Barbosa et al. 2011). More recently, the role of by threats above- and belowground and herbivory may have plant volatiles as a means for within-plant signalling to consequences for plant–insect multitrophic interactions in bypass vascular constraints has been demonstrated (Karban the alternative compartment mediated by changes in plant et al. 2006; Frost et al. 2007; Heil & Silva Bueno 2007). secondary chemistry. These additional associations further Plant defences against insect herbivores are often divided increase the complexity of interaction networks. Conse- into direct and indirect defences. In the literature, direct quently, the effect of a putative defence trait may be under- plant defences, or more appropriately direct resistance, refer or overestimated when other interactions are not considered. to traits that act upon the attacker directly, such as the presence of adverse chemical substances in plant tissues that Key-words: direct defence; herbivory; HIPV; indirect interfere with growth and development of the consumers defence; insect–plant interactions; natural enemies; (Schoonhoven et al. 2005) and as a result reduce the amount parasitoid; plant secondary metabolites; VOC. 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, vola- INTRODUCTION tile plant metabolites that are produced in response to Plants produce an enormous array of different chemicals that feeding by insect herbivores guide the herbivore’s natural are usually divided into primary and secondary metabolites. enemies to the damaged plant (Vet & Dicke 1992). Direct The first group of metabolites refers to chemicals that are and indirect defences are often studied independently. essential for plant growth and development, and are com- However, chemicals associated with indirect defence may monly produced by most plant species. Metabolites in the also affect the behaviour of the herbivores (Bruce et al. 2005) second group aid plant growth and development, but are not and chemicals associated with direct defence may also have essential for survival and often have a more restricted consequences for the development of the herbivore’s natural phylogenetic distribution. Arabidopsis thaliana L. is roughly enemies mediated through the herbivore’s food plant (Ode estimated to produce up to 11 000 different metabolites of 2006; Gols & Harvey 2009). which approximately 70–80% are commonly produced by Levels of secondary metabolites associated with defence often change in response to herbivory (Karban & Baldwin Correspondence: R. Gols. E-mail: [email protected] 1997; Agrawal et al. 1999) and more recently epigenetic © 2014 John Wiley & Sons Ltd 1741 1742 R. Gols effects of insect-induced resistance have been reported Berenbaum & Zangerl 2008; Ali & Agrawal 2012). As is (Rasmann et al. 2012). These induced changes can have long- often the case in ecology, there are examples where there is lasting consequences not only for the attacking species but evidence for co-evolutionary processes determining plant also for the plant’s interactions with other members of its defence chemistry levels (Zangerl & Berenbaum 2005), but associated community (Poelman et al. 2008; Stam et al.in there is also evidence that plants employ alternative strat- press). This suggests that the distinction between direct and egies, such as tolerance, to overcome herbivory (Strauss & indirect defences is diffuse, which is the main topic of this Agrawal 1999; Agrawal & Fishbein 2008). In addition, paper. I will further discuss potential conflicts between direct defence levels in natural populations may be less determined and indirect chemical defences or alternatively the potential by pairwise interactions and instead are the consequence of for trade-offs between the two plant traits. I will focus on diffuse selection involving multiple-species interactions interactions among plants, insect herbivores and their natural (Strauss & Irwin 2004). enemies such as predators and parasitoid wasps as mediated Moreover, insects themselves may actively manipulate by low molecular mass secondary plant metabolites. I will pay plant defences or prevent exposure to toxic plant metabolites particular attention to the literature on plant–insect interac- by feeding on less toxic tissues, ‘trenching’ (Dussourd 1993), tions in the Brassicaceae as these interactions are well or by actively manipulating the plant’s defence response studied in this plant family, which includes cabbage vegeta- (Kahl et al. 2000). Especially phloem-feeding aphids and bles and mustard oil varieties. Finally, I will argue that the white flies are well known for deceiving the plant to modify term ‘defence’ as described above and is used in many studies the sequence of events that normally follow upon wounding investigating the role of secondary metabolites in plant– by herbivores (Walling 2008). Well-adapted insects may even insect interactions should be used more carefully. co-opt plant chemical defences and use them in defence against their own attackers through sequestration of these SECONDARY METABOLITES: FROM BITROPHIC compounds from their food plants (Nishida 2002; Hartmann TO MULTITROPHIC INTERACTIONS 2004; Zagrobelny & Moller 2011). Whether plant secondary plant metabolites function as Traditionally, the role of secondary metabolites in defence defence chemicals preventing plant damage depends to a against insects is investigated in bitrophic interactions, that is, large extent on the degree of specialization of the herbivore. between plants and insect herbivores. In this section, I will Moreover, plants may tolerate certain levels of herbivory broaden this topic and discuss interactions with other organ- without serious consequences for their performance. isms 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 A large amount of studies have investigated the role of plant the third trophic level when interactions with plant and her- secondary metabolites in defence against herbivory bivores are investigated. However, when natural enemies of (Schoonhoven et al. 2005). In fact, the evolution and mainte- insect herbivores are included in studies investigating the nance of the enormous diversity in secondary metabolites in defensive function of plant traits, their effects on the different relation to plant–insect interactions is one of the central interacting organisms may not necessarily be that straight- topics in evolutionary ecology (Iason et al. 2012). In general, forward. For example, morphological traits may hamper simi- insect herbivores choose their diet and adjust their food larly sized herbivores and their natural enemies alike. In intake based on the balance between sufficient levels of addition, exposure to ingested secondary metabolites has nutrients and the absence or low levels of adverse metabo- been shown to be toxic to natural enemies such as parasitoids lites (Scriber & Slansky 1981; Slansky 1993). In their seminal (Campbell & Duffey 1981; Barbosa et al. 1991; Ode et al. paper, Ehrlich & Raven (1964) developed the theory of the 2004; Harvey et al. 2007) and predators (Nishida 2002; co-evolutionary arm’s race between plants and insects, where Hartmann 2004; Müller 2009). For an endoparasitoid, whose insects select for higher levels of toxins in plants and the larval development is intimately linked to the physiology of insects in turn respond by developing adaptations to these its host, exposure to toxic compounds in the host may be adverse chemicals. Often the distribution of certain com- difficult to avoid. The presence of high toxin concentrations pounds is restricted to a limited number of plant families, underlies the ‘nasty host’ hypothesis which states that certain genera or even species (Wink 2003) and specialized insect groups of parasitoids, for example, larval koinobiont herbivores select their host plants for oviposition or feeding endoparasitoids, that is, parasitoid species that allow the host often based on food plant-specific secondary metabolites to feed and grow after parasitism (Harvey 2005), are less well (Bruce et al. 2005; Schoonhoven et al. 2005; Hopkins et al. represented in tropical than in temperate ecosystems due to 2009). the fact that their hosts feed on plants with comparatively The debate whether chemical co-evolution is the mecha- higher levels of secondary metabolites (Gauld et al. 1992; nism underlying selection for increased levels of secondary Quicke 2012). plant metabolites persists (Bernays & Graham 1988; van der Reduced growth of the host itself on more toxic plants may Meijden 1996; Strauss & Irwin 2004; Thompson 2005; 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. Beneficial associations with microorganisms such as 2005; Gols & Harvey 2009; Bukovinszky et al. 2012). Pro- mycorrhizal fungi and growth-promoting rhizobacteria can longed herbivore development may increase the time further influence the plant’s nutritional and defence status. window that herbivores are exposed to predation and para- As nitrogen is a growth-limiting nutrient, insects tend to grow sitism (‘slow-growth-high-mortality’ hypothesis, Benrey & larger or faster with higher efficiencies of conversion on Denno 1997). As most parasitoid species attack only specific plants under high compared with low nutrient conditions developmental stages of their hosts, in contrast to predators (Scriber & Slansky 1981). Non-pathogenic microbial interac- that can consume a larger range of prey, prolongation of the tions belowground can enhance or prime the plant’s defence vulnerable stages is predicted to affect parasitism more than machinery against pathogen and insect attack aboveground, predation risk. However, the limited number of studies that a process that is referred to as induced systemic resistance have empirically tested the slow-growth-high-mortality (ISR) (Pineda et al. 2010).These mutualistic interactions with hypothesis for parasitoids shows little evidence for higher soil microbes can impact on the behaviour and performance parasitism rates in hosts that grow more slowly (Benrey & of associated aboveground organisms in different trophic Denno 1997; Williams 1999; Cornelissen & Stiling 2006). levels through changes in plant chemistry. In general, Food plant quality determined by primary and secondary mycorrhyzal fungi have a positive or neutral effect on the metabolites may affect the immune response of herbivorous performance of phloem-feeding herbivores and specialist hosts to parasitism. In contrast to predation where the host is leaf chewers, whereas they have a negative effect on gener- instantly killed, koinobiont parasitoids kill the host only after alist chewers (Koricheva et al. 2009). Similar patterns are their larval development is completed. During this extended recognized for the interaction between insect herbivores and interaction, the host’s immune system may prevent successful growth-promoting rhizobacteria (Pineda et al. 2013a) and parasitism by encapsulating and consecutively killing the insects and nitrogen-fixating rhizobia (Thamer et al. 2011). parasitoid eggs or larvae. Plant quality may reduce the host’s Little is known about the effect of beneficial soil microbes on immune response. For example, Bukovinszky et al. (2009) the performance of natural enemies, or on volatile-mediated reported that hosts developing on nutritious plants with low foraging behaviour (see next section) (Van der Putten et al. levels of secondary metabolites encapsulated more 2001; Hartley & Gange 2009). parasitoid eggs than hosts feeding on plants containing high Plants, but also insects, may rely on beneficial interactions levels of secondary metabolites. This effect was even more with microbial organisms that are able to modify secondary pronounced in plants that were induced by previous herbi- chemistry.These associations further increase the complexity vore feeding (Bukovinszky et al. 2009). In these situations, of interactions mediated by plant primary and secondary induced defence levels also enhanced the success of parasit- chemistry. ism through suppression of the host’s immune response (Bukovinszky et al. 2009; Reudler et al. 2011). On the other VOLATILE PLANT SECONDARY METABOLITES hand, plant-derived components may also improve the ability MEDIATE INTERACTIONS AMONG SPECIES IN to mount an immune response and prevent parasitism. For DIFFERENT TROPHIC LEVELS instance, the encapsulation rate of a foreign object by larvae of an Arctiid moth Parasemia plantaginis L. varied with food So far, I have discussed the influence of secondary metabo- plant species and this ability correlated positively with anti- lites with low volatilities that are stored in plant tissues, oxidant concentrations in the diet of the host (Ojala et al. though some of these compounds may also play a role in 2005). plant–insect interactions based on insect olfaction (Bruce Some of these examples demonstrate that effects of sec- et al. 2005) and play a role in direct defence. In this section, I ondary metabolites may not only negatively impact on the will focus on insect behaviour mediated by volatile plant performance of the herbivore, but also on beneficial interac- secondary metabolites and discuss their putative function in tions with the herbivores natural enemies. indirect defence. The concept of ‘talking plants’ by means of volatile emis- Modification of plant secondary chemistry sions has intrigued many ecologists over the last three through microbial mutualistic interactions decades (Baldwin & Schultz 1983; Turlings et al. 1990; Dicke & Baldwin 2010). In relation to plant–insect interactions, Plants may rely on other organisms to defend them against their role in indirect defence has been well investigated, that antagonists. Symbiotic endophytes, especially in grasses, is, the attractiveness of herbivore-induced plant volatiles to produce secondary metabolites increasing the plant’s resist- the herbivore’s natural enemies (Dicke & Baldwin 2010; ance to herbivores (Hartley & Gange 2009), which may move Mumm & Dicke 2010; Kessler & Heil 2011; McCormick et al. up in the food chain and negatively impact the development 2012). However, the function of plant organic volatiles per se of parasitoids and predators consuming these hosts (Bultman (Penuelas & Llusia 2004) and their role in reducing herbivory et al. 1997; de Sassi et al. 2006). Conversely, symbiotic inter- is still controversial (van der Meijden & Klinkhamer 2000; actions with bacteria may assist herbivores in host plant uti- Hare 2011; Kessler & Heil 2011). These volatile emissions do lization by suppression of the plant’s defensive response to not only attract natural enemies of herbivores, but also have herbivory and other physiological processes such as senes- been reported to play a role in plant-plant communication cence (Kaiser et al. 2010; Frago et al. 2012; Chung et al. 2013). (Karban & Shiojiri 2009; Heil & Karban 2010), in host plant © 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 the vegetation in the habitat matrix (Gols et al. 2005; behaviour of hyperparasitoids (i.e. parasitoids of parasitoids) Bukovinszky et al. 2007; Bezemer et al. 2010; Meiners et al. (Poelman et al. 2012). Conflicts may arise from the plant’s 2010; Randlkofer et al. 2010). In addition, laboratory studies perspective when in response to herbivory not only natural often involve unnatural non-coevolved associations combin- enemies are attracted to these ‘advertising’ plants, but also ing arthropods native to different biological realms. In par- the herbivores themselves (Nottingham et al. 1991; Renwick ticular, plant–insect interactions using Arabidopsis are a et al. 2006; Halitschke et al. 2008) as well as enemies of the good example illustrating this point. Under natural condi- natural enemies (Poelman et al. 2012). Moreover, the distinction, plants are embedded in a vegetation consisting of dif- tion between direct and indirect defences becomes hazy ferent plant species that may chemically and or structurally when induced volatiles also increase levels of direct defence interfere with insect foraging (Gols et al. 2005; Bukovinszky or prepare plants to respond faster to future attacks, so-called et al. 2007; Bezemer et al. 2010; Meiners et al. 2010; priming (Conrath et al. 2006; Halitschke et al. 2008). Randlkofer et al. 2010). The arthropod community has to deal not only with this ‘noise’, but also with the spatial het- Volatile-mediated foraging behaviour of erogeneity in the habitat which is usually absent in highly insect parasitoids and other natural enemies controlled laboratory studies as illustrated in Fig. 1. of insect herbivores Despite the numerous studies reporting on parasitoid attraction towards herbivore-induced plant volatiles, little is For parasitism to be successful, several sequential steps have known about the identity of the compounds or about the to be accomplished (Vinson 1998). The first steps include ratio between volatile compounds that determine blend habitat and host location, which in the case of parasitoids of attractiveness (Pareja et al. 2009; Gols et al. 2011; Hare 2011), herbivorous hosts are often mediated by plant volatiles, espe- although several studies have demonstrated that subtle cially those emitted by the plant when damaged by the host changes in volatile emissions can be perceived by natural (Vet & Dicke 1992).The question is whether natural enemies enemies of insect herbivores (Shiojiri et al. 2006; Zhang et al. are equally attracted to plants that vary in levels of direct 2009; Gols et al. 2012; de Rijk et al. 2013). Moreover, defence chemicals. For example, herbivores feeding on more parasitoids are known to be flexible in their response to these toxic plants in the field have been shown to be less prone to volatile blends through the process of associative learning parasitism (Nieminen et al. 2003; Ode et al. 2004). It is (Vet et al. 1990; Hoedjes et al. 2011). Thus, depending on the unknown in these examples whether lower parasitism is experience status of the wasp, the response to volatile blends caused by the fact that the parasitoids are less attracted to may vary accordingly. However, this strategy seems more these plants, whether they reject the more toxic hosts for beneficial to the parasitoid than to the emitting plant. If the parasitism, or whether parasitism success is compromised by emission of attractive blends functions as an indirect defence, enhanced parasitism immunity in hosts feeding on more toxic what blend should the plant emit when the response to these plants. volatiles is dynamic? Frequency-dependent selection and the The study of indirect defences, that is, the attraction of degree of intimacy between the plant and the plant’s pre- natural enemies through the emission of plant volatiles, relies sumed mutualists determine to a large extent the defensive with a few exceptions (Halitschke et al. 2008; Poelman et al. value of the selected trait. In other words, the importance of 2009; Schuman et al. 2012) on highly simplified wind tunnel herbivore-induced plant volatiles as an indirect defence trait or Y-tube olfactometer bioassays (Hunter 2002). In these may be limited in an environment where the presence of bioassays, parasitoids or predators that are most responsive natural enemies is highly unpredictable. This contrasts with to plant volatiles (only certain age classes are used) are given indirect defence traits in plant–ant associations where the the choice between two contrasting odour sources. Parasitism ants permanently inhabit the plants or when rewards are success is not only determined by efficient host location produced only when the ants are present (Kessler & Heil behaviour, in which plant volatiles play a pivotal role. The 2011). Alternatively, the cost of expressing these traits is ability to overcome the host’s immune response is an impor- limited or the function of this trait is not primarily defensive. tant intrinsic factor and has been demonstrated to be also The ecological costs of volatile emissions are often ignored affected by the host food plant. In general, parasitoid attrac- and have only recently begun to be more appreciated (Ali tion to herbivore-induced plant volatiles is often studied et al. 2011; Kessler et al. 2011; Poelman et al. 2012; Robert without confirming that this attraction results in increased et al. 2013). parasitism and parasitism success. Considering that the physiological status (age, energy Modification of plant volatile emission through reserves) of parasitoids varies, their foraging behaviour in interactions with plant mutualists nature and their response to volatiles may vary accordingly (Steinberg et al. 1992; Winkler et al. 2006). Volatile-mediated As I discussed in the previous section, plant primary and foraging behaviour in the field may not reflect the volatile- secondary chemistry can change in response to interactions mediated decisions as they are made in simplistic laboratory with beneficial microbes. Pineda et al. (2013b) demonstrated bioassays. More importantly, the ability of herbivores and that rhizobacteria-treated A. thaliana plants infested with their natural enemies to detect and respond to volatiles may aphids were less attractive to Diaeretiella rapae parasitoids strongly depend on the identity of the physical structure of than plants without rhizobacteria. The performance of the © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 Plant chemical defences against insects 1745

Figure 1. Images of experimental set-ups, an agricultural ﬁeld, and a natural habitat illustrating the lack of ecological realism in studies investigating plant insect interactions. (a) Cabbage (Brassica oleracea) plant in a Y-tube olfactometer often used to test attractiveness of herbivore-induced plant volatiles to parasitoids and predators, (b) agricultural cabbage ﬁeld consisting of genetically similar plant with no interstitial vegetation, (c) experimental design of an experiment investigating natural colonization by arthropods using various cabbage cultivars in weeded plots in a managed landscape background, and (d) natural habitat of wild cabbage growing naturally along the coastlines of the UK (arrows indicate cabbage plants).

parasitoid on aphids feeding on control and rhizobacteria- treated plants was similar. Herbivore-induced plant responses are regulated by the activity of three key phytohormones, jasmonic acid (JA), ethylene (ET) and sali- cylic acid (SA), respectively (Heil & Ton 2008; Erb et al. 2012), and are further ﬁne-tuned by other plant hormones and crosstalk between the different signalling pathways (Pieterse et al. 2009). The reduced attractiveness of plants with rhizobacteria was attributed to increased activation of JA signalling which interfered with SA-induced signalling by the aphids (Pineda et al. 2013b). Increasing evidence points at a positive inﬂuence of mycorrhyzal fungi on natural enemy attraction (Gange et al. 2003; Guerrieri et al. 2004; Hempel et al. 2009; Wooley & Paine 2011). Moreover, mutualistic soil-borne microbes can negatively impact on volatile-mediated foraging behaviour of herbivores. For example, JA-treated Lima bean plants colo- nized by rhizobial bacteria induced a volatile blend that dif- fered quantitatively from a blend induced by non-rhizobial plants. These JA-treated non-rhizobial plants were more attractive to the Mexican bean beetle than rhizobial plants (Ballhorn et al. 2013). These examples illustrate that depending on the studied interaction, for example, plant-herbivore or plant-natural enemy, the effects of changes in secondary chemistry can be neutral, synergistic or antagonistic.

CONFLICTS AND TRADE-OFFS BETWEEN AND AMONG DIRECT AND INDIRECT PLANT DEFENCE TRAITS Investment of resources in defence can be costly, and there- fore, allocation constraints are predicted when multiple defence strategies are employed (Koricheva et al. 2004). Few studies have examined so-called direct and indirect defences simultaneously (Ballhorn et al. 2008; Gols et al. 2009; Rodriguez-Saona et al. 2011; Wei et al. 2011; Kos et al. 2012). Ballhorn et al. (2008) measured in wild and cultivated Lima bean plants (Phaseolus lunatus L.) the effect of JA treatment, which is often used to simulate herbivory by biting-chewing herbivores, and measured foliar levels of hydrogen cyanide (HCN) and volatile emissions as proxies for direct and indirect defences, respectively. The authors reported a negative correlation between the two defence traits in the secondary, but not in the primary leaves. HCN levels did not change in response to JA treatment and levels of this chemical were © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 1746 R. Gols very low in the primary leaves. In contrast, JA-induced vola- Direct and indirect defences in brassicaceous tile emissions were very high in primary leaves suggesting plant species that this trade-off is also expressed in relation to plant ontog- eny (Ballhorn et al. 2008). In the limited studies using real Conflicts and trade-offs between and among direct and indi- herbivores to determine the effects of direct and indirect rect defence traits emerge, for example, in situations where defences, little evidence has been found for conflicts: plants the associated insect community is composed of herbivores with low levels of herbivore resistance are attractive to the on which the effects of secondary metabolites are asymmet- herbivore’s natural enemies, which suggests that there is a ric. Glucosinolates are a good example of illustrating poten- trade-off between direct and indirect resistance traits (Gols tial conflicts between beneficial and adverse effects of plant & Harvey 2009; Gols et al. 2009, 2011; Kos et al. 2012; Yoneya secondary chemicals with presumed direct and indirect et al. 2012). In contrast, Rasmann et al. (2011) reported lack defence characteristics (Hopkins et al. 2009). All of a trade-off between direct and indirect defences in a field brassicaceous plant species biosynthesize glucosinolates study with milkweed (Asclepias syriaca L.). In this study, (Fahey et al. 2001). The defence machinery is compartmen- constitutive and inducible defences correlated negatively and talized and consists of relatively inactive glucosinolates and this was the case for both direct and indirect defences. Thus, myrosinase enzymes that are stored separately from the in milkweed, allocation of resources is traded off between former. Following tissue damage, myrosinase catalyses the constitutive and inducible defences and not between direct hydrolysis of the glucosinolates into biologically more active and indirect defences (Rasmann et al. 2011). isothiocyanates and other products (Halkier & Gershenzon In plant-mediated insect interactions, the effect of one 2006). Isothiocyanates, which are considered the more toxic inducing insect species on a second receiving species is tra- hydrolysis products, differ considerably in volatility and ditionally examined, whereas more recently the effect of hydrophobicity depending on the side chain structure of the multiple herbivory on species interactions has been investi- parent compound (Agerbirk & Olsen 2012) and these physi- gated demonstrating that the introduction of a second her- cal characteristics may influence their biological activity. bivore species may interfere with both direct and indirect Glucosinolates are constitutively expressed, but often defences expressed in the leaves (Ponzio et al. 2013; Stam increase in response to herbivory (Textor & Gershenzon et al. in press). Moreover, defence traits expressed in 2009). However, a range of insects have developed sophisti- belowground or aboveground tissues can affect those in the cated mechanisms to circumvent exposure (Ratzka et al. alternate compartment (Van der Putten et al. 2001; van 2002; Wittstock et al. 2004) or even sequester glucosinolates Geem et al. 2013; Soler et al. 2013) and few studies have from their food plant (Bridges et al. 2002; Müller 2009).These included the third trophic level when comparing above- and insects have often restricted their diets to plants within the belowground plant–insect interactions (Soler et al. 2005, Brassicaceae family and use glucosinolates to recognize suit- 2007a; Rasmann & Turlings 2007; Pierre et al. 2011). In these able host plants (Renwick 2002; Hopkins et al. 2009). More- studies, simultaneous below- and aboveground herbivory over, some specialized insects such as the aphids Brevicoryne tends to reduce the attractiveness of the induced volatile brassicae L. and Lipaphis erysimi Kaltenbach have copied blends to natural enemies of the herbivores in their respec- the bipartite-defence system from their host plants to protect tive compartments. them against their own antagonists. These aphids sequester White & Andow (2006) also reported reduced parasitism glucosinolates from their food plants, in addition to produc- of the aboveground-feeding corn borers Ostrinia nubilalis ing an endogenous myrosinase (Bridges et al. 2002). More Hübner in plots where corn plants were also infested with recently, it has been reported that even generalist herbivores corn rootworm larvae Diabrotica spp. belowground com- are able to divert to some extent the toxic impact of pared with plots where there were only corn borers present. isothiocyanates in the gut by metabolizing a proportion of Here, the net effects on corn borer densities were con- the ingested glucosinolates (Schramm et al. 2012). Thus, founded by positive direct effects and negative indirect glucosinolates may be relatively ineffective against specialist effects; the presence of rootworms reduced the density of herbivores and primarily affect the performance of generalist corn borers by 50%, whereas at the same time these plots herbivores (Blau et al. 1978; Giamoustaris & Mithen 1995; Li attracted less Macrocentrus grandii Goidanich, specialist et al. 2000; Gols et al. 2008a,b). A similar pattern has been parasitoids of the stem borer (White & Andow 2006). The reported for cyanogenic glucosides in non-brassicaceous authors argued that the importance of associational resist- plants, which negatively impact on the behaviour and perfor- ance (Barbosa et al. 2009) among aboveground herbivores mance of generalist and positive on that of specialist herbi- through the activity of belowground herbivores may be vores (Ballhorn et al. 2010; Zagrobelny & Moller 2011). underestimated. Whereas multiple-species herbivory on the Consequently, generalist and specialist herbivores exert aboveground plant tissues has been demonstrated to have opposing selection pressures on glucosinolate chemistry in negative, positive or neutral effects on foraging behaviour their host plants. (de Rijk et al. 2013), simultaneous herbivory on the roots and In natural stands of wild cabbage (Brassica oleracea L.) in the shoots appears to interfere with volatile-mediated forag- the UK, the insect community is dominated by specialist ing of natural enemies. In other words, indirect defences may herbivores (Moyes et al. 2000; Newton et al. 2009) suggesting be less effective when plants are challenged both above- and that defence against generalist herbivores is effective. This below ground. may explain why generalist herbivores such as Trichoplusia © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 Plant chemical defences against insects 1747 ni Hübner, Mamestra brassicae L. and Myzus percicae Sulzer larvae) reduced the performance of the herbivores and (Ahuja et al. 2010) are only serious pest species in their parasitoids in the alternate compartment (Soler et al. brassicaceous crop plants in which levels of glucosinolates 2005, 2007a). Cotesia glomerata L. females, specialized have been greatly reduced due to the process of artificial endoparasitoids of P. brassicae caterpillars feeding on the selection (Gols & Harvey 2009). However, specialists do not leaves, discriminated between volatiles emitted by undam- always perform better than generalist herbivores on plants aged and root fly-damaged plants and preferred to alight on with high levels of secondary metabolites. For example, the the former. However, the wasps did not discriminate between generalist herbivore M. brassicae performed much better plants infested with hosts alone and plants simultaneously than various species of specialist herbivores on the invasive damaged by host caterpillars and root flies (Soler et al. brassicaceous weed Bunias orientalis L., despite relatively 2007c). In a semi-field design, C. glomerata female wasps high foliar levels of the glucosinolate sinalbin (Harvey et al. foraged more efficiently in habitats that, in addition to host- 2010; Harvey & Gols 2011a).This suggests that the biological infested plants, also contained root fly-infested plants (Soler activity depends on the identity of the chemical and the et al. 2007b). The contrasting volatile blends induced by the exposed herbivore species (Gols et al. 2008b; van Leur et al. two herbivore species may guide the parasitoid to a host 2008; Harvey et al. 2010; Müller et al. 2010). plant more rapidly. Here enhanced food plant quality is reli- As discussed earlier, plant quality mediated by plant sec- ably ‘advertised’ by emitting a more attractive blend, as the ondary chemistry may not only negatively impact on the caterpillars developing on clean plants provide higher quality performance of the herbivores themselves but also on hosts (Soler et al. 2005, 2007b). Similarly, foliage feeding natural enemies that consume these herbivores and may interfered with volatile-mediated foraging of Trybliographa even compromise development of species in the fourth rapae Westwood, a parasitoid of D. radicum root fly larvae. trophic level (Harvey et al. 2003; Soler et al. 2005). Usually Female T. rapae wasps only discriminated between plant-mediated effects on the performance of the host and its uninfested Brassica rapa L. plants and those damaged by endoparasitoids are positively correlated (Gols & Harvey D. radicum hosts alone and not between singly and dually 2009). An exception to this rule is a study with M. brassicae infested plants (Pierre et al. 2011). However, in a field study, and its endoparasitoid Microplitis mediator Haliday (Harvey parasitism by T. rapae was significantly lower on plants sim- & Gols 2011a). In this study, the parasitoid was more strongly ultaneously damaged above- and belowground by affected by host plant quality on one population of P. brassicae and D. radicum, respectively, than on plants B. orientalis than the host when plants were previously infested with D. radicum alone (Pierre et al. 2011).This result induced by host caterpillars. In contrast, in a similar experi- suggests that the complete sequence of events leading to ment using wild cabbage (B. oleracea) plants, parasitoids parasitism does not solely rely on volatile cues. were able to survive on induced plants of one cabbage popu- It has been suggested that parasitoids that attack herbi- lation, whereas unparasitized hosts all died on this popula- vores that have restricted diets, such as parasitoids of herbi- tion (Harvey & Gols 2011b). These results suggest that vores that only feed on brassicaceous plant species, could plant-mediated effects on herbivore–parasitoid interactions benefit from volatile cues specifically emitted by these plant can be highly context specific. species (Vet & Dicke 1992; Gols et al. 2011). The volatile Kos et al. (2012) investigated chemical defences, both breakdown products of glucosinolates and isothiocyanates direct and indirect, in the same study system and reported a seem to be the obvious candidates to reliably reveal the positive correlation between aphid performance and levels of species identity of the food plant. The aphid parasitoid specific glucosinolates, between aphid (B. brassicae) and D. rapae McIntosch, which attacks aphid species feeding on parasitoid (D. rapae) performance, and between parasitoid brassicaceous plants, is attracted to synthetic isothiocyanates, performance and parasitoid attraction to plant volatiles. In which are also emitted by plants damaged by aphid feeding the same study, the authors also found a negative correlation (Read et al. 1970; Blande et al. 2007). Another study (Mumm between glucosinolate concentrations in the host plant of the et al. 2008) reported that in A. thaliana L. mutants aphid prey and the performance and attraction of a generalist overexpressing epithiospecifier (EPS) proteins, the hydroly- predator (Episyrphus balteatus de Geer). In both cases, the sis of glucosinolates mainly results in the production of natural enemies were attracted to the plant with host or prey nitriles instead of the more toxic isothiocyanates. These that sustained the best performance of their offspring. Thus, plants were less attractive for oviposition by the herbivore direct and indirect defences induced in the same plant– Pieris rapae L., a specialist on brassicaceous plant species, but herbivore interaction resulted in adaptive but asymmetric P. rapae damaged plants were more attractive to the responses in different natural enemies. A similar result was parasitoid of herbivore Cotesia rubecula Marshall. It is not reported for two caterpillar species and their larval known how common this diversion of hydrolysis products is endoparasitoids in wild and cultivated Brassica species (Gols in other brassicaceous plant species that are more likely to et al. 2009). interact with these insects than A. thaliana and how this Herbivory on below- or aboveground plant tissues may diversion from direct to indirect defence affects interactions interfere with plant–insect interactions in the alternative with herbivores and natural enemies under natural condi- compartment. In Brassica nigra L. plants, the effect of early tions. Moreover, for some isothiocyanates, it has been dem- herbivory on either the leaves (feeding by Pieris brassicae L. onstrated that they are used for food plant location by caterpillars) or the roots (feeding by root fly Delia radicum L. herbivores specialized on brassicaceous plant species © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 1748 R. Gols

(Nottingham & Coaker 1985; Moyes & Raybould 2001; Renwick et al. 2006), turning these compounds into ‘double- edged swords’.

SYNTHESIS AND ADDITIONAL CONSIDERATIONS REGARDING DIRECT AND INDIRECT DEFENCES Chemical defence traits in plants are often studied in two- species interactions, that is, between plants and herbivores (direct defence traits) or between plants and insect natural enemies (indirect defence traits). However, many chemical plant traits do not influence the behaviour and the performance of the herbivore and its natural enemies independently (Fig. 2). The effects of direct chemical plant defences on herbivores and by association on their natural enemies can be in the same or opposite direction and are often highly interaction and context specific. For instance, specialized insects in both the second and third trophic levels are often less affected by plant toxins than less specialized interactions, although the direction of the effect on both the herbivore and the natural enemy may be similar. In contrast, in sequestering herbivores, direct defence traits are co-opted by the herbivore with negative consequences for species in the third trophic level and the strength of the effect may differ depending on the food plant species. Similarly, volatile secondary metabolites associated with indirect defence may not only Figure 2. Overview of multitrophic interactions that are attract natural enemies but also their enemies and the herbi- mediated by chemical direct and indirect defence traits. (1) and (2) vores themselves. Thus, the distinction between direct and refer to chemical traits that are traditionally associated with direct indirect defences is not as black and white as is often por- (non-volatile plant secondary chemicals, nvPSM) and indirect defences (volatile secondary metabolites, vPSM). Red and blue trayed in the literature. lines refer to direct and indirect defences, respectively, and dashed There is a tendency towards increasing complexity in eco- lines represent potential effects of these traits on other organisms. logical studies investigating plant defence traits and their For example, direct defences may also affect the performance of effects on arthropods (Stam et al. in press). For example, the natural enemies (3), and volatile emissions may influence the effect of multiple herbivory on volatile-mediated foraging behaviour of the herbivores (4). Symbiotic bacteria can help behaviour of natural enemies of insect herbivores is receiving the herbivore to digest plant tissues and to deal with PSMs, but increasing attention (de Rijk et al. 2013) and multiple they can also (5) actively manipulate the defensive response of the plant as well as immunity against parasitism. (6) For herbivory has been reported to negatively influence the mutualistic plant–endophyte associations, it is known that they attraction of some natural enemies. Furthermore, the impor- provide the plant with anti-herbivore metabolites. Little is known tance of the belowground environment on plant–insect inter- about the effects of these symbionts associated with the plant or actions aboveground and vice versa has been acknowledged the herbivore on the production of plant volatiles and (Van der Putten et al. 2001; Bezemer & van Dam 2005; van volatile-mediated foraging of natural enemies (7) and (8). Geem et al. 2013). Examples provided in this review suggest (9) Some highly specialized herbivore species sequester nvPSMs that herbivory can interfere with direct and indirect chemical from their food plant and use them in defence against their own antagonists turning direct defences in a double-edged sword. defence traits expressed in the alternative compartment. In (10) and (11) Interactions with herbivores and microbes on addition, most, if not all organisms, host beneficial microbes belowground-plant tissues can influence the expression of direct that improve their interaction with the biotic and abiotic and indirect defences in aboveground-plant tissues and vice versa. environments. Microbial symbiotic interactions with above- and belowground plant tissues are well studied for their effects on the performance of insect herbivores, but have Given their phylogenetic and physiological constraints, received less attention with respect to interactions with plants should invest most in defence traits against threats that natural enemies.Thus,symbionts associated with organisms at present the highest risk. The benefits of these adaptations different trophic levels further increase the variation in both should at least outweigh the biosynthetic and ecological costs. the expression of defence traits in plants and the response of However, in many herbaceous plant species the risk of the consumers. By restricting the research to one specific herbivory is highly unpredictable.This may be the reason why interaction, the net effect of a plant defence trait may be over- tolerance to some level of herbivory may have evolved as an or underestimated. In general, the ecological and physiologi- alternative strategy (Strauss & Agrawal 1999).With respect to cal costs of direct and indirect defences are often unknown. the effectiveness of indirect defences, the predictability is © 2014 John Wiley & Sons Ltd, Plant, Cell and Environment, 37, 1741–1752 Plant chemical defences against insects 1749 potentially lower than for direct defences and the ecological Agrawal A.A. & Fishbein M. (2008) Phylogenetic escalation and decline of costs may be high; the plant emits these volatiles regardless of plant defense strategies. Proceedings of the National Academy of Sciences of the United States of America 105, 10057–10060. whether natural enemies are present, and other non-target Agrawal A.A., Tuzun S. & Bent E. (1999) Induced Plant Defenses against organisms, which may constitute an additional threat, can use Pathogens and Herbivores. Biochemistry, Ecology and Agriculture. APS these chemicals as well. In other words, the level of intimacy Press, St. Paul, MN, USA. between parasitoids and plants is lower than between plants Ahuja I., Rohloff J. & Bones A.M. (2010) Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for and insect herbivores.Consequently,I expect that selection by integrated pest management. A review. 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