Delayed induced silica defences in grasses and their potential for destabilising herbivore population dynamics.

Some grass species mount a defensive response to grazing by increasing their rate of uptake of silica from the soil and depositing it as abrasive granules in their leaves. Increased plant silica levels reduce food quality for herbivores that feed on these grasses. Here we provide empirical evidence that a principal food species of an herbivorous rodent exhibits a delayed defensive response to grazing by increasing silica concentrations, and present theoretical modelling that predicts that such a response alone could lead to the population cycles observed in some herbivore populations. Experiments performed under greenhouse conditions revealed that the rate of deposition of silica defences in the grass Deschampsia caespitosa is a time-lagged, nonlinear function of grazing intensity and that, upon cessation of grazing, these defences take around one year to decay to within 5 % of control levels. Simple coupled grass-herbivore population models incorporating this functional response, and parameterised with empirical data, consistently predict population cycles for a wide range of realistic parameter values for a (Microtus) vole-grass system. Our results support the hypothesis that induced silica defences have the potential to strongly affect the population dynamics of their herbivores. Specifically, the feedback response we observed could be a driving mechanism behind the observed population cycles in graminivorous herbivores in cases where grazing levels in the field become sufficiently large and sustained to trigger an induced silica defence response.

Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores.

1. Silica in the leaves of grasses can act as a defence against both vertebrate and invertebrate herbivores. The mechanisms by which silica affects herbivore performance are not well characterized. Here we expose an insect herbivore Spodoptera exempta to high-silica diets and test two mechanisms by which silica has been proposed to act as a defence. First, that silica reduces the digestibility of leaves and second, that silica causes wear to insect mandibles, both of which could potentially impact on herbivore performance. 2. Silica reduced the efficiency with which S. exempta converted ingested food to body mass and the amount of nitrogen absorbed from their food, leading to reduced insect growth rates. The measure of how efficiently herbivores utilize digested food (ECD) was unaffected by silica. 3. These effects occurred even with short-term exposure to silica-rich diets, but they also increased markedly with the duration of exposure and affected late instars more than early instar larvae. This appears to be due to the progressive impacts of silica with longer exposure times and suggests that herbivores cannot adapt to silica defences, nor do they develop a tolerance for silica with age. 4. Exposure to silica-rich diets caused increased mandible wear in S. exempta. This effect was extremely rapid, occurring within a single instar, further reducing feeding efficiency and growth rates. These effects on insect growth and feeding efficiency are nonreversible, persisting after the herbivore has switched diets. Up to a third of this residual impact can be explained by the degree of mandible wear caused by previous silica-rich diets. 5. The impacts of silica on S. exempta larvae were progressive with exposure time and could not be compensated for, even by switching to a different diet. Thus, herbivores cannot easily adapt to physical defences such as silica, suggesting this defence will have major implications for herbivore fitness.

Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates.

The impact of plant-based factors on the population dynamics of mammalian herbivores has been the subject of much debate in ecology, but the role of antiherbivore defences in grasses has received relatively little attention. Silica has been proposed as the primary defence in grasses and is thought to lead to increased abrasiveness of foliage so deterring feeding, as well as reducing foliage digestibility and herbivore performance. However, at present there is little direct experimental evidence to support these ideas. In this study, we tested the effects of manipulating silica levels on the abrasiveness of grasses and on the feeding preference and growth performance of field voles, specialist grass-feeding herbivores. Elevated silica levels did increase the abrasiveness of grasses and deterred feeding by voles. We also demonstrated, for the first time, that silica reduced the growth rates of both juvenile and mature female voles by reducing the nitrogen they could absorb from the foliage. Furthermore, we found that vole feeding leads to increased levels of silica in leaves, suggesting a dynamic feedback between grasses and their herbivores. We propose that silica induction due to vole grazing reduces vole performance and hence could contribute to cyclic dynamics in vole populations.

Herbivore specific induction of silica-based plant defences.

Induced plant responses to herbivory have major impacts on herbivore feeding behaviour, performance and population dynamics. These effects are well established for chemical defences, but induction of physical defences remains far less studied. However, for many plants, it is physical defences that play the major role in regulating the levels of herbivore damage sustained. We provide evidence that, in grasses, induction of physical defences is both specific to herbivore feeding, as opposed to mechanical damage, and may be dependant on the amount of damage imposed. Furthermore, we show that the magnitude of the induction response is sufficient to deter further damage and affect herbivore performance. We compared silica induction in two grass species in response to vertebrate and invertebrate damage, and to mechanical defoliation. Induction was assessed at two levels of damage over 16 months. Foliar silica content did not increase in response to mechanical defoliation, but damage by either voles or locusts resulted in increases in silica content of over 400%. This increase deterred feeding by both voles and locusts. Silica induction in grasses due to repeated damage events over a prolonged period suggests a possible role for silica defence in the cyclical population fluctuations observed in many grass-feeding herbivores.

Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder.

1. Silica, deposited as opaline phytoliths in the leaves of grasses, constitutes 2-5% of dry leaf mass, yet its function remains unclear. It has been proposed that silica may act as an antiherbivore defence by increasing the abrasiveness and reducing the digestibility of grass leaves, although there is little direct experimental evidence to support this. 2. We investigated the effects of manipulated silica levels on the abrasiveness of the leaves of five grass species. We also examined the effects of silica levels on the feeding preferences, growth performance and digestion efficiency of two folivorous insects and one phloem-feeding insect. 3. Silica addition resulted in increases to leaf abrasiveness in four of the five grass species studied. Silica addition also deterred feeding by both folivores and reduced their growth rates and digestion efficiency. 4. These effects resulted in lower pupal mass of the lepidopteron larvae Spodoptera exempta and compensatory feeding by the orthopteran, Schistocerca gregaria. In contrast, silica had no effects on the feeding preference or the population growth of the phloem feeder, Sitobion avenae. 5. Our results demonstrate that silica is an effective defence against folivorous insects, both as a feeding deterrent, possibly mediated by increased abrasiveness, and as a digestibility reducer. The effects of silica on pupal mass and development time may impact on herbivore fitness and exposure to natural enemies. 6. These results are the first demonstration of a direct effect of silica on the abrasiveness of grasses and the adverse impact of silica on herbivore preference and performance.