Direct and Indirect Chemical Defences Against Insects in a Multitrophic Framework
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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 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 pres- ence 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