Silicon as a plant defence against insect herbivory: response to Massey, Ennos and Hartley
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- 1Silicon (Si) has received increased attention as a nutrient capable of providing some measure of defence for plants against fungal pathogens, and insect and mammalian herbivores.
- 2On the basis of a study including two generalist insect folivores and a phloem feeder, Massey, Ennos & Hartley (2006; Journal of Animal Ecology, 75, 595–603) have drawn attention to a putative distinction between the effects of plant Si in defending against folivorous and phloem-feeding insects. On the basis of their results they imply that phloem feeders are less likely to be adversely affected by increased plant Si than folivores.
- 3However, in making this suggestion, Massey et al. have ignored many previous studies demonstrating a clear effect of plant Si on a range of phloem-feeding and some xylem-feeding insects, and that this effect stems not only from leaf mechanical properties based on opaline silica, but also from induced chemical defences seemingly mediated by soluble Si.
- 4Furthermore, Massey et al. cannot claim that their study was the first demonstration of a direct effect of Si on insect herbivore preference and performance; there have been numerous earlier studies demonstrating this from folivores, stem borers, and phloem and xylem feeders.
- 5We contend that current evidence indicates that Si is likely to be involved to a similar extent in enhancing resistance to all four insect feeding guilds and that any conclusion to the contrary is, at this stage, premature.
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The role of silicon (Si) as a nutrient enabling plants to ameliorate the effects of a range of abiotic and biotic environmental stressors, has become the subject of a burgeoning field of research (see reviews by Ma 2004; Fauteux et al. 2005; Laing, Gatarayiha & Adandonon 2006). Insect herbivores represent one class of biotic stressors that Si can provide some defence against (Laing et al. 2006); however, in comparison with plant diseases, their interaction with plant Si has been little explored. In particular, elucidation of the mechanism(s) of Si-mediated plant resistance to insect herbivores has largely addressed the dominant hypothesis of a Si barrier providing mechanical resistance to insect feeding and/or plant penetration (Hanifa, Subramaniam & Ponnaiya 1974; Bernays & Barbehenn 1987; Salim & Saxena 1992; Kvedaras & Keeping 2007).
Massey, Ennos & Hartley (2006) recently demonstrated that provision of Si increased abrasiveness of the leaves of four of five grass species studied, while changing the relative palatability of the grasses, deterring feeding, and reducing the growth rates and feeding efficiency of two generalist insect folivores, Spodoptera exempta (Lepidoptera: Noctuidae) and Schistocerca gregaria (Orthoptera: Acrididae). In contrast to the folivores, Massey et al. found that a phloem feeding insect, Sitobion avenae (Hemiptera: Aphididae), suffered no detrimental effects of increased plant Si on feeding preference or population growth performance. The authors suggest that, contrary to leaf-feeding insects, the aphid's feeding method of inserting its stylet into the leaf veins may allow it to avoid silica bodies (phytoliths) within the plant epidermis and hence any mechanical hindrance to obtaining nutriment.
Massey et al. also claim that their study was the first to demonstrate an effect of Si on insect herbivore performance (point 6 of their abstract) and on p. 596, they state that, ‘... to date there is a lack of experimental evidence on the impacts of silica on both the preference and performance of herbivores that are most likely to be affected (folivores), compared with those likely to be unaffected (phloem feeders)’.
Plant silicon and herbivore performance
With regard to the effects of Si on insect folivores there have been studies prior to that of Massey et al. also within the genus Spodoptera, which found a significant effect of Si on insect performance. Final-instar Sp. eridania (Lepidoptera: Noctuidae) larvae fed on artificial diet with powdered silicic acid at 10–20% dry weight, showed reduced ability to digest the diet, leading to increased consumption rates (Peterson, Scriber & Coors 1988). Goussain et al. (2002) found that Sp. frugiperda larvae displayed increased mortality, cannibalism and mandibular wear after feeding on corn plants fertilized with Si. Despite these studies, we are still in no position to generalize that folivores are the guild most likely to be affected by high plant Si levels, as shown in two recent studies where experimentally elevated plant Si in turfgrass species had no influence on feeding and development of Herpetogramma phaeopteralis (Lepidoptera: Pyralidae) (Korndorfer, Cherry & Nagata 2004), or on growth, survival, feeding preference and mandibular wear of Agrotis ipsilon (Lepidoptera: Noctuidae) (Redmond & Potter 2007).
Outside of the folivores, there is also a wealth of published evidence indicating or directly demonstrating the effects of increased plant Si levels on the performance of stem borers. It may serve to draw attention to a few of these studies.
Borers feeding on Si-fertilized rice or highly siliceous rice varieties showed typical effects of antibiosis, such as decreased survival, and in some cases worn mandibles indicating reduced feeding efficiency due to Si (Sasamoto 1957; Djamin & Pathak 1967; Hanifa et al. 1974; Ukwungwu & Odebiyi 1985). Sétamou et al. (1993) found that Si applied to maize reduced larval survival, percentage pupation and adult emergence in Sesamia calamistis (Lepidoptera: Noctuidae). Recently, Keeping & Meyer (2002, 2006) showed that treatment of sugarcane with Si significantly reduced survival of Eldana saccharina (Lepidoptera: Pyralidae) larvae, while further studies [albeit published subsequent to Massey et al.'s (2006) paper] found that Si treatment reduced the growth rate of individual E. saccharina larvae and delayed penetration of the sugarcane stalk by third instar larvae (Kvedaras & Keeping 2007; Kvedaras et al. 2007).
However, our main contention with Massey et al.'s paper is with their suggestion of a distinction between the effects of plant Si on folivores and phloem feeders. On p. 602, the authors somewhat dismissively state that, ‘Finally, we have found no evidence of silica affecting the growth performance or acting as a feeding deterrent on our chosen phloem feeder, although previous work has suggested that silica may [our emphasis] have detrimental effects on xylem feeders (Kim & Heinrichs 1982)’. While we agree that plant silica constitutes an important defence against certain folivores, we believe that Massey et al. have ignored work demonstrating a role for both opaline and soluble Si in enhancing plant resistance to phloem and xylem feeding insects.
For example, infestation of nitrogen-fertilized wheat plants by Sitobion avenae (the same phloem feeder studied by Massey et al.), as well as by Metopolophium dirhodum (Aphididae), was reduced through application of a 1% sodium silicate foliar spray, to below that in nitrogen-deficient control plants, apparently due to the uptake of silica in the leaves of sprayed plants (Hanisch 1981).
Work subsequent to that of Kim & Heinrichs (1982) on Sogatella furcifera (Hemiptera: Delphacidae), has found that Si decreased food intake, growth, adult longevity, fecundity and population growth of this xylem feeder on a susceptible rice variety (Salim & Saxena 1992). The inhibitory effect of silicic acid on sucking behaviour in Nilaparvata lugens (Delphacidae) (Yoshihara et al. 1979) suggests a mechanism whereby Si may impart resistance to xylem feeders.
Recent evidence for the adverse effects of plant Si on phloem feeders has come from the work of Brazilian researchers, who found that Schizaphis graminum (Aphididae) had reduced preference for, and lower longevity and fecundity on, leaves from wheat plants fertilized with sodium silicate solution (Basagli et al. 2003; Moraes et al. 2004). Reduced preference of Sc. graminum for Si-treated sorghum and of Rhopalosiphum maidis (Aphididae) for Si-treated maize was recorded by Carvalho, Moraes & Carvalho (1999) and Moraes et al. (2005), respectively. As epidermal resistance of wheat to stylet penetration and ability of Sc. graminum to reach the phloem vessels was not affected by silicon application, a mechanical barrier of opaline Si in the leaf epidermal cells was not supported (Goussain, Prado & Moraes 2005). However, Si application did induce aphids to withdraw their stylets more frequently, resulting in decreased probing time (Goussain et al. 2005).
Silicon-induced chemical defences
While increased mechanical resistance is thought to be the major mechanism whereby Si defends plants against insect attack, there is increasing evidence of an active role for soluble Si. Massey et al. citing Hochuli (1993), state (p. 596) that, ‘No previous studies have made a direct test of any mechanism by which silica may defend against herbivores, such as by increases in leaf abrasiveness’; however, they fail to note that in the 14 years since, there have been advances in this area of Si research. For example, Si-induced chemical responses by the plant may be of greater importance in resistance of wheat to Sc. graminum infestation than mechanical resistance to stylet penetration. Gomes et al. (2005) found that the plant's defence system was activated by previous infestation with aphids, Si fertilization, or both, which negatively affected green aphid preference and population increase rate, while increasing activities of three enzymes involved in induced defence responses in plants (Karban & Baldwin 1997). Indeed, Si-induced resistance to the phloem feeder Bemisia tabaci (Hemiptera: Aleyrodidae) in cucumber was identical in all parameters measured to that produced by benzothiadiazole (BTH), a synthetic analogue of the natural plant elicitor, salicylate (Correa et al. 2005).
Taken together, the above studies indicate that Si is likely to be as important in resistance to phloem (and xylem) feeding insects as in resistance to folivores (or to borers). For all four feeding guilds, it appears likely that the mechanisms of Si-mediated resistance include one or a combination of constitutive and induced mechanical and chemical defences. Hence, the emphasis placed by Massey et al. (2006) on the contrasting results they obtained between two folivores and a phloem feeder, and their suggestion that Si is likely to be of greater importance for defence against folivores (due to its effects on plant properties such as leaf abrasiveness), is premature and ignores important work, outlined above, on the likely active role of silicon in induced chemical defences against insect herbivores in general.