Do silica-based defences drive plant-herbivore dynamics

Project: Research project (funded)Research

Project Details


Cyclic dynamics are common in herbivore populations and have traditionally been thought to reflect interactions with higher trophic levels, rather than being driven by plant-based factors. This project aims to radically reassess this view by testing a novel mechanism by which changes in plant quality can drive herbivore population dynamics. Our long-term data sets on vole populations, together with our recent work on the impacts of induced silica-based defences on vole performance, have suggested a that changes in these defences could lead to cyclic dynamics in voles, and indeed in other grass-feeding herbivores. We propose that the silica-based defences are induced in response to heavy grazing when vole populations are high. We know that high levels of silica reduce the growth rates of voles and hence delay the time they begin to breed in spring. Once populations begin to fall and silica defences relax, plant quality recovers and vole populations begin to increase again. We have evidence to support these ideas from lab work on a range of grass species and preliminary field observations, and we now seek to test them fully, at the field scale.
Our experiments will test the following hypotheses:
(i) that foliar silica content of D. caespitosa varies primarily in response to past vole population density (Hypothesis1 /assessed using large-scale field survey)
(ii) that silica induction is a) a linear function with damage levels or b) a step function requiring a specific damage threshold to be induced (Hypothesis 2 / tested by grazing enclosure experiment)
(iii) that induction in response to spring grazing levels has a sufficient lag and amplitude to account for the variation in onset of breeding observed in demographic data (Hypothesis 3 / tested by grazing enclosure experiment)
(iv) that population-level experimental manipulation of vole density translates, in the future, into changes in grass quality, timing of onset of vole reproduction and population growth rates commensurate with those observed in cyclical populations (Hypothesis 4 / tested by large-scale field manipulation)
(v) that models which include seasonal forcing and our measured magnitude and time scale of silica-based defence induction provide a quantitatively robust explanation for population cycles in voles (Hypothesis 5 / tested by model development)
This project will generate a new understanding of the role of plant-based factors in herbivore population dynamics and hence has wide significance for the study of trophic interactions in ecology.

Layman's description

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 that 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 some evidence from laboratory experiments and some fieldwork that supports 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.

Key findings

A large enclosure experiment involving was established in early 2009 with replicated treatments of 6 different vole densities. The impact on Silicon (Si) levels in the voles’ major over-winter food species, the grass Deschampsia caespitosae was measured until spring the following year and demonstrated that a) induction of Si was proportional to vole densities and positively related to damage levels; b) there is a threshold to induction in that no significant induction occurs unless vole densities exceed ~200voles/ha; c) there is a seasonal component to both Si content and plant responses, with maximum induction occurring in response to damage in spring when plants are actively growing; d) there is a lag of ~9months to maximum induction and the increases in Si are similar to those causing significant impacts on vole performance in lab experiments.
We also manipulated population densities of field voles on approximately 1 ha grassland plots in Northern England over one year. Subsequently, we tested for the impact of past density on vole life history traits in spring, and whether these effects are driven by the induction Si. We predicted that female voles on sites with previously high density, and consequently high grass Si concentrations, would be slower to gain weight and so would enter reproduction later in spring than conspecifics on sites with previously low density. Several months after commencing the population density manipulations, leaf silicon concentrations diverged and were on average 22% lower on plots where vole densities had been reduced. However, these effects did not persist beyond the period of the density manipulations. Contrary to our predictions, for every additional 100 voles/ha in the previous spring and early summer, vole mass in spring increased by 2.4g and the mean date for the onset of spring reproduction was advanced by ~20 days. These findings show that grazing by field voles can induce increased silicon defences in grasses on a landscape-scale, but that the effect is relatively transient and thus unlikely to drive the multi-annual population cycles of field voles in Northern England. Unusually this study found that reducing vole densities had a negative rather than the expected positive impact on vole performance the following spring, suggesting that negative density dependent processes may only operate once vole populations have exceeded a certain density threshold.
In addition to this field work, we have carried out some initial modelling work, based on our measured magnitude and time-scale of silica-based defence induction, which did provide a quantitatively robust explanation for population cycles in voles (Reynolds et al 2012).
We have also collaborated with researchers in Norway to investigate Si -herbivore interactions in the sub-arctic (Soininen et al 2012), developed a new analytical method for Si measurement (Reidinger et al 2012) and examined the impact of Si defences on plant competition (Garbuzov et al 2011).
Effective start/end date1/11/105/07/12