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- Materials and methods
- Supporting Information
In their introduced ranges, many exotic plants experience reduced herbivore regulation, especially from specialist herbivores (Keane & Crawley, 2002), which can lead to differences in defences among native and invasive populations (Blossey & Nötzold, 1995). As defence is costly (Zangerl & Rutledge, 1996; Morris et al., 2006), exotic plants may evolve to invest more resources in growth or reproduction (Blossey & Nötzold, 1995; Bossdorf et al., 2005), or less-costly defences more effective against generalists (Joshi & Vrieling, 2005; Doorduin & Vrieling, 2011). Inducible defences, which are only synthesised or mobilised in response to a stimulus, are thought to have lower costs than constitutive defences, which are always expressed in a plant. Therefore, invasive plants could change inducible defences in their invasive range due to differences in the frequency and types of herbivore attack in a way that is different than the pattern for constitutive defences.
The induction of specific defensive traits may be associated with a variety of herbivores, leading to distinct responses to specific herbivores (Karban & Myers, 1989). Some studies have reported that plants have different induced responses to specialist and generalist herbivores but it has been argued that specificity of induction may be more complex than simply generalist versus specialist defence induction (see review in Ali & Agrawal, 2012). Poelman et al. (2008a) found that damage by Pieris rapae (specialist within Brassicaceae) and Mamestra brassicae (generalist with host range extending beyond the Brassicaceae) induced higher indole glucosinolates in Brassica nigra than damage by Plutella xylostella (specialist within Brassicaceae). There are other examples showing that specialist and generalist herbivores elicit similar plant responses (Reymond et al., 2004; Poelman et al., 2008b). However, in the context of plant invasions, studies on defences of exotic plants produced in response to attack by specialist and generalist herbivores may be able to provide unique insights into understanding the evolution of plant defences due to the absence of specialists in the introduced range (Orians & Ward, 2010; Wang et al., 2012a).
Latex is an important defence against herbivores for some plants. When a plant is damaged, latex exudes from specialised canals and accumulates at the damaged points (Agrawal & Konno, 2009). There is evidence that plant latex affects herbivores by both mechanical and chemical mechanisms. First, latex exuded from the damaged point clots rapidly, and can glue the mouthparts or the whole body of insects (Dussourd & Eisner, 1987; Dussourd, 1995). Second, plant latex contains various secondary metabolites and proteins, many of which have been reported to serve as a defence against herbivores (Zalucki et al., 2001; Agrawal & Konno, 2009; Konno, 2011). Moreover, the concentrations of some substances in latex have been shown to be much higher than those in leaves (Sessa et al., 2000; Konno et al., 2004, 2006). There have been studies of latex and its chemicals that demonstrate that it is a potent plant defence against mandibulate herbivores (Agrawal & Konno, 2009). However, few studies to date have investigated latex chemicals and latex defensive functions in invasive plants, especially for responses to specialist and generalist herbivores.
Here we examine biogeographical variation in latex defences using Chinese tallow [Triadica sebifera (L.) Small = Sapium sebiferum (L.) Roxb.] as a model species. We also examined inducible latex variation among populations from invasive and native ranges. Previous studies reported that T. sebifera contains secondary chemicals such as tannins and flavonoids in leaves (Huo & Gao, 2004; Wang et al., 2012a). Tannins are known to defend leaves against insects by reducing digestibility (Salminen & Karonen, 2011), and may be particularly effective against specialist herbivores (Müller-Schärer et al., 2004). Flavonoids are primarily associated with defence against generalists (Müller-Schärer et al., 2004) but also are thought to have other functions such as protection from ultraviolet radiation, allelopathy or defence against pathogens (Harborne & Williams, 2000; Iwashina, 2003). Recent studies found that invasive populations of T. sebifera expressed higher flavonoids and lower tannins in leaves than did native populations (Huang et al., 2010; Wang et al., 2012a). No studies have examined variation in latex production in T. sebifera.
We addressed the following questions: (i) Do invasive and native populations differ in constitutive latex quantity and secondary chemical characteristics? (ii) Do latex quantity and secondary chemical characteristics vary in response to attack by different herbivores? (iii) Do invasive and native populations differ in latex quantity and secondary chemical characteristics after attack by different herbivores?
- Top of page
- Materials and methods
- Supporting Information
As a physical and chemical defence against herbivores, latex may vary in quantity and chemical composition, depending on herbivore and plant identities. In this study, we found that a specialist caterpillar induced more latex exudation than a generalist caterpillar did, and plants from invasive populations secreted more latex than those from native populations did when damaged by a specialist caterpillar. We also found latex tannin concentrations increased but flavonoid concentrations decreased when plants were damaged by a generalist but were unchanged when damaged by a specialist and that, unlike latex volume, these chemical responses did not depend on population origin.
Triadica sebifera secreted more latex when damaged by a specialist herbivore than when damaged by a generalist. Specialist herbivores have a long evolutionary history with their host plants, and so may have evolved some adaptations to plant latex. Indeed, studies have shown that specialist herbivores have physiological adaptations to plant latex (Holzinger et al., 1992; Holzinger & Wink, 1996; Labeyrie & Dobler, 2004). For instance, specialist silkworms have developed physiological and biochemical adaptations to chemicals in mulberry latex but polyphagous Lepidopteran larvae are sensitive to mulberry latex (Konno, 2011). As a response, plants may increase the volume of latex to deter specialists that are not sensitive to chemicals in latex but may be unable to counter the physical effects of large amounts of latex. In contrast, many generalist herbivores may not have adapted to chemicals in latex as specialists have and may be sensitive to even small amounts of latex. The negative correlation between latex volume and latex chemical concentrations is consistent with two defence strategies focused on physical versus chemical defence.
Invasive populations secreted more latex than native populations did when damaged by a specialist herbivore; however, invasive and native populations had similar latex responses to generalist herbivore damage. Invasive plants may evolve less costly defence strategies to cope with the lower herbivore loads in invasive ranges and reallocate more resources to growth and reproduction (Blossey & Nötzold, 1995; Cipollini et al., 2005). Because plants do not secrete latex without damage (Agrawal & Konno, 2009; Konno, 2011), latex may be less costly to maintain than other defences. Previous studies identified herbivore-derived molecules that appear to be signals of the type of herbivore damaging plants (Heil, 2009; Hilker & Meiners, 2010; Ali & Agrawal, 2012), suggesting specialist herbivores could induce distinct plant defence responses compared with generalist herbivores. In our study, a generalist herbivore induced stronger responses than a specialist herbivore, as the concentration of both tannins and flavonoids in latex changed significantly when damaged by the generalist herbivore. For tallow defence, our previous studies found that invasive populations of T. sebifera have higher tolerance to generalist herbivores and lower resistance to specialist herbivores (Huang et al., 2010), and that invasive populations have higher flavonoids and lower tannins in leaves than native populations (Wang et al., 2012a). Our study on the inducible indirect extrafloral nectar of T. sebifera also found that specialist and generalist herbivores could induce different extrafloral nectar production (Wang et al., 2013).
Plant latex contains water and a diversity of biologically active compounds (secondary metabolites) such as tannins and flavonoids, which directly defend against herbivores (Agrawal & Konno, 2009; Konno, 2011). In our study, we found latex tannin concentrations increased but flavonoid concentrations decreased when plants were damaged by a generalist but were unchanged when damaged by a specialist. Through graphical modelling (Fig. 5) we found that the combined net compound changes (flavonoids, tannins and latex exudation) from native to invasive range negatively affected the generalist but very weakly affected the specialist, indicating divergent selection on the chemical properties of latex in the introduced range where there are generalists but often lack of specialists.
Recent studies have examined secondary compounds in invasive plants, but most focused on leaf chemicals. None addressed latex exudation and chemicals, which are also important to plant defence (Agrawal & Konno, 2009). To the best of our knowledge, our study is the first to examine the amount of latex exudation and chemical composition when damaged by different herbivores and compare the induction of introduced and native plant populations. We found that invasive populations secreted more latex than native populations did when damaged by a specialist herbivore, and that there were opposite responses of latex tannins and flavonoids when damaged by generalist herbivore. Our results suggest divergent selection on the physical and chemical properties of latex in the introduced range. The quantity of latex produced was more sensitive to herbivore identity in the introduced range but the specificity of the latex chemical response was retained. Studying the expression of different defence traits in novel conditions may help to understand the ecology and evolution of plant defence and invasive mechanism.