Do silica-based defences drive plant-herbivore dynamics?

Lead Research Organisation: University of Aberdeen
Department Name: Inst of Biological and Environmental Sci

Abstract

Understanding the factors that drive changes in the abundance of animal populations is fundamental to ecology. Many herbivore populations show regular oscillations in abundance, known as cycles, and these are usually thought to be due to matched oscillations in the abundance of predators rather than any changes in the herbivore's food plants. Food quality is not thought to respond to herbivory in a way which could lead to cycles, but we have discovered a novel way in which changes in plant quality could cause cycles in herbivore populations. This mechanism has not been considered before but it could apply to wide range of plant-herbivore systems. Our new idea is called the silica induction hypothesis. Periods of sustained heavy grazing lead to an increase in the levels of silica in grasses, so herbivores subsequently experience reduced availability of nutrients. This reduces their growth and reproductive rate and hence slows down the rate of population growth in the following year. Eventually populations fall to a level where there is only low grazing on the grasses, so the levels of silica in the leaves also fall because less well-defended leaves are produced. Herbivores are once again able to access nutrients in the grasses and their growth and reproduction increase again. We believe this mechanism can operate in many plant-herbivore systems, particularly ones based on grasses and other plants that contain high levels of silica. Silicon is the second most abundant mineral on earth and present in significant amounts in all plants, so the mechanism we propose is of wide relevance and significance. We already have some evidence from laboratory experiments and observations in the field that support our idea. In this project we aim to test this potential mechanism for the first time in large-scale field experiments. Firstly, we will determine the silica levels in grasses in areas where vole populations are high and compare them with those in areas where vole populations are low. If our ideas are correct, silica levels should be declining in areas where vole populations are increasing and vice versa. We will then set up an experiment to measure the rate and magnitude of the increase in silica at different levels of grazing and we will also measure how quickly the levels of silica defences decrease. Then we will test our ideas by moving voles into areas where we have induced high silica levels previously and see how feeding in these areas affects their growth and reproduction. These experiments will assess whether changes in plant defences can cause changes in herbivore abundance and help us develop a better understanding of the interactions between grasses and their herbivores. There are many important grassland systems that support a wide range of herbivores, including both rare species and livestock, so this project will be useful to both conservation and sustainable agriculture.
 
Description 1. 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.
2. Experiments 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 1 year to decay to within 5% of control levels.
3. Simple coupled grass-herbivore population models incorporating this functional response, and parameterized with empirical data, consistently predict population cycles for a wide range of realistic parameter values for a (Microtus) vole-grass system.
4. 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.

Grazing-induced changes in plant quality have been suggested to drive the negative delayed density-dependence exhibited by many herbivore species, but little field evidence exists to support this hypothesis. We tested a key premise of the hypothesis that reciprocal feedback between vole grazing pressure and the induction of anti-herbivore silicon defences in grasses drives observed population cycles in a large-scale field experiment in northern England. We repeatedly reduced population densities of field voles (Microtus agrestis) on replicated 1 ha grassland plots at Kielder Forest over one year. Subsequently, we tested for the impact of past density on vole life history traits in spring, and whether these effects were driven by induced silicon defences in the voles' major over-winter food, the grass Deschampsia caespitosa. We predicted that female voles on sites with previously high density, and consequently higher grass silicon concentrations, would be slower to gain weight and so would enter reproduction later in spring than those on sites with previously low density. After several months of density manipulation, leaf silicon concentrations diverged and averaged 22% lower on sites where vole density had been reduced, but this difference did not persist beyond the period of the density manipulations. Contrary to our predictions, there were no significant effects of our density manipulations on either vole mass or mean date for the onset of spring reproduction the following year. These findings show that grazing by field voles does induce increased silicon defences in grasses on a landscape-scale, but at the vole densities encountered, levels of plant damage appear to be below those needed to induce changes in silicon levels large and persistent enough to affect vole performance, confirming the threshold effects we observed in lab-based studies. Reducing vole densities did not have the positive impacts on vole performance we expected, suggesting that plant defence-induced negative density dependence may only operate once populations exceed a certain density. We thus reject our nutritional hypothesis for observed vole population cycles in northern England, at least over the range of vole densities that now prevail here.
Exploitation Route none at this stage
Sectors Environment
 
Description Other colleagues, notably in Poland Norway and Sweden have been inspired by our work to test similar mechanisms in other ecosystem and find mix support.
First Year Of Impact 2013
Sector Environment
Impact Types Societal