Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?

Most plant species have a range of traits that deter herbivores. However, understanding of how different defences are related to one another is surprisingly weak. Many authors argue that defence traits trade off against one another, while others argue that they form coordinated defence syndromes. We collected a dataset of unprecedented taxonomic and geographic scope (261 species spanning 80 families, from 75 sites across the globe) to investigate relationships among four chemical and six physical defences. Five of the 45 pairwise correlations between defence traits were significant and three of these were tradeoffs. The relationship between species' overall chemical and physical defence levels was marginally nonsignificant (P = 0.08), and remained nonsignificant after accounting for phylogeny, growth form and abundance. Neither categorical principal component analysis (PCA) nor hierarchical cluster analysis supported the idea that species displayed defence syndromes. Our results do not support arguments for tradeoffs or for coordinated defence syndromes. Rather, plants display a range of combinations of defence traits. We suggest this lack of consistent defence syndromes may be adaptive, resulting from selective pressure to deploy a different combination of defences to coexisting species.

A faecal index of diet quality that predicts reproductive success in a marsupial folivore.

Estimating the nutritional value of a herbivore's diet is difficult because it requires knowing what the animal eats, the relative quality of each component and how these components interact in relation to animal physiology. Current methods are cumbersome and rely on many assumptions that are hard to evaluate. We describe a new method for estimating relative diet quality directly from faeces that avoids the problems inherent in other methods. We combine this method with near infrared reflectance spectroscopy (NIRS) to analyse many samples and thus provide a technique with immense value in ecological studies. The method stems from the correlation between the concentrations of dietary and faecal nitrogen in herbivores eating a tannin-free diet, but a weaker relationship in browsers that ingest substantial amounts of tannins, which form complexes with proteins. These complexes reduce the availability of nitrogen and may increase faecal nitrogen concentrations. Using the tannin-binding compound, polyethylene glycol, we showed that tannin-bound nitrogen is a significant and variable part of faecal nitrogen in wild common brushtail possums (Trichosurus vulpecula). We developed a technique to measure faecal available nitrogen and found that it predicted the reproductive success of female brushtail possums in northern Australia. Faecal available nitrogen combined with NIRS provides a powerful tool for estimating the relative nutritional value of the diets of browsing herbivores in many ecological systems. It is a better indicator of diet quality than other commonly used single-nutrient measures such as faecal nitrogen and foliage analysis paired with observed feeding behaviour.

The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal.

Plants contain a variety of chemical defenses that strongly affect feeding rates in captive mammals, but their effects on the fitness of wild herbivores are largely unknown. This is because the complexity of defensive compounds, and herbivores' counteradaptations to them, make their effects in the wild difficult to measure. We show how tannins interact with protein to produce spatial variation in the nutritional quality of eucalypt foliage, which is related to demography in a wild population of a marsupial folivore, the common brushtail possum (Trichosurus vulpecula Kerr). Tannins reduced the digestibility of nitrogen (N) in vitro, creating variation in available N concentrations among the home ranges of individual possums in an otherwise homogeneous habitat. This was strongly correlated with reproductive success: females with better quality trees in their home range reproduced more often and had faster-growing offspring. These results demonstrate a powerful mechanism by which spatial variation in plant chemistry may control herbivore population dynamics in nature.

Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites.

Plant secondary metabolites (PSMs) strongly influence diet selection by mammalian herbivores. Concentrations of PSMs vary within and among plant species, and across landscapes. Therefore, local adaptations may cause different populations of herbivores to differ in their ability to tolerate PSMs. Here, we tested the food intake responses of three populations of a marsupial folivore, the common brushtail possum (Trichosurus vulpecula Kerr), from different latitudes and habitat types, to four types of PSMs. We found clear variation in the responses of northern and southern Australian possums to PSMs. Brushtail possums from southern Australia showed marked decreases in food intake in response to all four PSMs, while the two populations from northern Australia were not as sensitive and their responses did not differ from one another. These results were unexpected, based on our understanding of the experiences of these populations with PSMs in the wild. Our results suggest that geographically separated populations of possums may have evolved differing abilities to cope with PSMs, as a result of local adaptation to their natural environments. Our results provide the basis for future studies to investigate the mechanisms by which populations of mammalian species differ in their ability to tolerate PSMs.

Population-level manipulations of field vole densities induce subsequent changes in plant quality but no impacts on vole demography.

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 defenses 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, northern England, over a period of 1 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 defenses in the voles' major over-winter food, the grass Deschampsia caespitosa. 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. There were no significant effects of our density manipulations on vole body mass, spring population growth rate, or mean date for the onset of spring reproduction the following year. These findings show that grazing by field voles does induce increased silicon defenses in grasses at a landscape scale. However, 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 have previously observed in laboratory-based studies. Our findings do not support the plant quality hypothesis for observed vole population cycles in northern England, at least over the range of vole densities that now prevail here.

Male-biased predation and its effect on paternity skew and life history in a population of common brushtail possums (Trichosurus vulpecula).

Differences in predation risk may exert strong selective pressures on life history strategies of populations. We investigated the potential for predation to shape male mating strategies in an arboreal folivore, the common brushtail possum (Trichosurus vulpecula Kerr). We predicted that possums in a tropical population exposed to high natural levels of predation would grow faster and reproduce earlier compared to those in temperate populations with lower predation. We trapped a population of possums in eucalypt woodland in northern Australia each month to measure life history traits and used microsatellites to genotype all individuals and assign paternity to all offspring. We observed very high levels of male-biased predation, with almost 60% of marked male possums being eaten by pythons, presumably as a result of their greater mobility due to mate-searching. Male reproductive success was also highly skewed, with younger, larger males fathering significantly more offspring. This result contrasts with previous studies of temperate populations experiencing low levels of predation, where older males were larger and the most reproductively successful. Our results suggest that in populations exposed to high levels of predation, male possums invest in increased growth earlier in life, in order to maximise their mating potential. This strategy is feasible because predation limits competition from older males and means that delaying reproduction carries a risk of failing to reproduce at all. Our results show that life histories are variable traits that can match regional predation environments in mammal species with widespread distributions.

A simple, integrative assay to quantify nutritional quality of browses for herbivores.

Many regard the concentrations of nitrogen (N), tannins and plant cell wall constituents (fibre) as key indicators of food quality and habitat suitability for browsing herbivores; yet there is no method for measuring their combined effects. We have developed a simple in vitro assay for measuring the effects of tannins and fibre on N availability in browse. We determined the effects of tannins by measuring the polyethylene glycol (PEG)-binding capacity (PEG-BC) of Eucalyptus leaf samples, followed by a two-stage in vitro digestion with pepsin and cellulase to determine the digestibility of dry matter and N. There was a significant relationship between concentrations of digestible N and the PEG-BC of the leaves. Furthermore, adding PEG significantly improved the digestibility of N. Our results concur with in vivo observations from several mammalian species. This suggests that our method is effective for measuring the nutritional quality of browse and the benefits of adding PEG, providing some index of the detrimental effects of tannins. We further simplified the assay by removing the PEG step, allowing us to quickly analyse samples in bulk. Nevertheless, this simplified method is still not practical for analysing the many samples necessary to compare the nutritional values of different tracts of forest. We used near-infrared reflectance spectroscopy to produce calibration equations and predicted total and digestible N in 322 trees at eleven sites. Both within and between sites, we found a wide variation in concentrations of digestible N but a much lower variation in total N, with either no relationship or poor relationships between the two measures. This confirms the variability in the nutritional quality of eucalypt forests, which may explain the distribution and abundance of mammalian herbivores. Thus, our assay provides a useful tool for understanding how food resources influence herbivore populations at different scales.