Gordon D. Sanson

Gross vs. net income: How plant toughness affects performance of an insect herbivore

Leaf biomechanical properties are thought to impose a significant obstacle to herbivores and as such influence patterns of herbivory more than leaf chemistry. However, evidence for the role of structural traits in influencing herbivore food choice and performance has come from correlative studies, whereas the underlying mechanisms have been given little attention. By manipulating the biomechanical properties of a host grass species through a combination of lyophilization and milling, and providing water separately, we were able to compare behavioral, physiological, and developmental responses of the Australian plague locust, Chortoicetes terminifera, to the biomechanical properties of plant food (exemplified by toughness) independently of the foods macronutrient content and the insects demand for water. Increasing leaf toughness was associated with reduced rates of locust growth and prolonged development, with potential ecological consequences. Poorer performance on the tougher foods was primarily a consequence of a reduced rate of nutrient supply, which occurred as a result of (1) smaller meals being eaten more slowly, (2) slowed gut passage rates, which limited how quickly the next meal could be taken, and (3) reduced efficiency of assimilation of nutrients from food in the gut. In addition, there were deleterious changes in the ratio of protein to carbohydrate assimilated from the gut. Prolonged development time was associated with increased total nutrient demands throughout the extended developmental period. Because these demands could not be met by increased consumption, there was a decreased efficiency of conversion of assimilated nutrients to growth. By disentangling the effects of biomechanical properties from macronutrient and water content we have shown that leaf biomechanical traits can influence chewing herbivores independently of leaf chemical traits.

The biomechanics of browsing and grazing

Terrestrial plant leaves are complex structures of composite materials. Resistance to fracture is achieved by a number of mechanisms, which operate at the molecular, cell, tissue, and structural levels. Leaves of dicots have different venation patterns and cell wall volume fractions from those of grasses, and consequently, they potentially resist fracture in different ways. Animals mechanically process plants in order to rupture the cell wall in preparation for enzymic hydrolysis, for which the imperative is to maximize new surface area and/or to expedite access to cell contents, ideally by promoting elastic fracture. The two different plant types are fed on by two different groups of organisms of very different sizes, digestive physiologies, mechanical processing abilities and properties, and nutritional requirements. Small insects can feed in or on parts of leaves, while larger mammals generally have to feed on the whole leaf. The scale of feeding also differs for the two groups of herbivores, but how this interacts with the scale of the mechanical properties of the leaf is not well understood. Plant leaves are attacked at all scales and probably can only produce generalized responses to specialized herbivores. In addition, the opportunities that these different scales of interactions open for the different herbivores remain unexplored.

Characterising sclerophylly: some mechanical properties of leaves from heath and forest

Abstract Although sclerophylly is widespread through the world and is often the dominant leaf-form in mediterranean climates, the mechanical properties of sclerophyllous leaves are poorly understood. The term ”sclerophyllous” means hard-leaved, but biologists also use terms such as tough, stiff and leathery to describe sclerophyllous leaves. The latter term has no precise definition that allows quantification. However, each of the former terms is well-defined in materials engineering, although they may be difficult or sometimes inappropriate to measure in leaves because of their size, shape or composite and anisotropic nature. Two of the most appropriate and practically applicable mechanical properties of sclerophyllous leaves are ”strength” and ”toughness”, which in this study were applied using punching, tearing and shearing tests to 19 species of tree and shrub at Wilson’s Promontory, Australia. The results of these tests were compared with leaf specific mass (LSM) and a sclerophylly index derived from botanists’ ranks. Principal components analysis was used to reduce the set of mechanical properties to major axes of variation. Component 1 correlated strongly with the botanists’ ranks. Overall, leaves ranked as sclerophyllous by botanists were both tough and strong in terms of punching and tearing tests. In addition, tough and strong leaves typically had high toughness and strength per unit leaf thickness. There was also a significant correlation between component 1 and LSM. Although more detailed surveys are required, we argue that sclerophylly should be defined in terms of properties that have precise meanings and are measurable, such as toughness and strength, and that relate directly to mechanical properties as implicit in the term.

The effect of tooth wear on the feeding behaviour of free‐ranging koalas (Phascolarctos cinereus, Goldfuss)

The free-ranging feeding behaviours of five adult koalas Phascolarctos cinereus with varying degrees of tooth wear were investigated using acoustically sensitive radio telemetry. An increase in tooth wear was found to be associated with a significant increase in the average amount of time spent feeding, average number of leaves consumed and the average number of daily chews. This suggests that koalas compensate for tooth wear by increasing food intake. Furthermore, there was a significant increase in the average number of chews per leaf and average chew rate, suggesting a greater investment in processing each leaf.

Biomechanical properties of insects in relation to insectivory: cuticle thickness as an indicator of insect 'hardness' and 'intractability'

The concept of ‘hardness’ has long been used to describe the biomechanical properties of the diet of many animals. However, due to the lack of a consistent definition, and the multitude of uses to which the term has been put, the use of the term ‘intractability’ has been advocated here to represent the extent to which the structural strength, stiffness and toughness are increased in a foodstuff. The thickness of the cuticle of an insect was a good measure of the intractability of cuticle. The tremendous advantage of the use of cuticle thickness as a measure of the biomechanical properties of invertebrates means that the dietary properties of a living insectivore can be directly quantified according to the thickness of the cuticle in its faeces. The quantitative measurement of intractability obtained through this technique can be used in correlations with adaptations of the masticatory apparatus, including tooth and skull morphology, as well as more general considerations of ecology. This is a major advance on previous measures of the biomechanical properties of insectivore diets, and may represent the best technique of any dietary group in assessing the properties of its diet.

Leaf Mechanical Properties in Sclerophyll Woodland and Shrubland on Contrasting Soils

Sclerophylly is a common feature of vegetation on infertile soils, and its adaptive significance has been linked to nutrient-use efficiency by protection of leaves to maximise carbon gain. However, there has been little investigation of how the leaf mechanical properties that contribute to the phenomenon of sclerophylly vary along nutrient gradients. In this paper, we investigate how leaf mechanical properties vary among plants on three contrasting soil types (grey sand, laterite soil, and soil overlying dolerite) in a Mediterranean climate in southwestern Australia. Most species were sclerophyllous, but there was 5-fold variation in leaf mass per unit area (LMA) and 17- to 473-fold variation in mechanical properties among species. Species growing on laterite and/or sand (low-nutrient soils) had higher punch strength, work (a measure of toughness) to punch, specific (per unit leaf thickness) work to punch, work to shear, specific work to shear, and flexural stiffness (EIW) than those on dolerite soils (higher in nutrients). There were few differences in mean values of leaf mechanical properties between the two low-nutrient soils, possibly because the lower concentration of nutrients in the sand is balanced by the greater soil volume than the laterite soil (higher concentration of nutrients, but shallower). There were also few differences in leaf properties between plants of the same species growing on contrasting soil types. There was some variation among sclerophyllous species in their mechanical characteristics, but overall, EIW provided the strongest contribution to sclerophylly, explaining up to 81% of the variation in LMA. There was no evidence of differences among soil types in the relationships of mechanical properties with LMA, and therefore, no evidence of variation in the mechanical constitution of sclerophylly among soil types.

Indigestibility of plant cell wall by the Australian plague locust, Chortoicetes terminifera

The plant cell wall may play an important role in defence against herbivores since it can be both a barrier to, and nutrient diluter of, the easily digested cell contents. The aim of this study was to investigate the digestibility of the cell wall of three grasses, Triticum aestivum L., Dactyloctenium radulans (R. Br.) Beauv., and Astrebla lappacea (Lindl.) Domin, by the Australian plague locust, Chortoicetes terminifera Walker (Orthoptera: Acrididae, Acridinae) as determined by the Van Soest method [ Van Soest PJ, Robertson JB & Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74: 3583–3597]. Determination of plant cell wall digestion by locusts required a precise methodological procedure to determine both the exact intake and the concentration of cell wall in the diet and the faeces. Plant cell wall determination is affected by the particle size distribution of the dried plant material. All three grasses differed in the percentage of cell wall per gram dry matter and the proportions of hemicellulose, cellulose, and acid‐detergent sulphuric lignin within the cell wall. The locust was unable to digest the cell wall of any of the grasses. Thus, plant cell walls are a mechanical barrier hindering locusts assimilating nutrients. That is, access, rather than nutrient concentration per se, may be limiting nutrient factor.

How do soil nutrients affect within-plant patterns of herbivory in seedlings of Eucalyptus nitens?

This study assessed how the palatability of leaves of different age classes (young, intermediate and older) of Eucalyptus nitens seedlings varied with plant nutrient status, based on captive feeding trials with two mammalian herbivores, red-bellied pademelons (Thylogale billardierii), and common brushtail possums (Trichosurus vulpecula). Seedlings were grown under three nutrient treatments (low, medium and high), and we determined how palatability was related to chemical and physical characteristics of the leaves. Pademelons ate more older leaves than young and intermediate leaves for all treatments. This pattern was best explained by sideroxylonals (formylated phloroglucinol compounds known to deter herbivory by other marsupials), and/or essential oil compounds that were present in lower concentrations in older leaves. In the low-nutrient treatment, possums also ate more of the older leaves. However, in the medium- and high-nutrient treatments, possums ate more intermediate leaves than older leaves and showed a behavioural preference for young leaves (consuming younger leaves first) over intermediate and older leaves, in spite of high levels of sideroxylonals and essential oils. The young leaves did, however, have the highest nitrogen concentration of all the leaf age classes. Thus, either sideroxylonals and essential oils provided little or no deterrent to possums, or the deterrent was outweighed by other factors such as high nitrogen. This study indicates that mammalian herbivores show different levels of relative use and damage to leaf age classes at varying levels of plant nutrient status and, therefore, their impact on plant fitness may vary with environment.

Changes in resource concentration and defence during leaf development in a tough-leaved (Nothofagus moorei) and soft-leaved (Toona ciliata) species

Developing leaves that are soft, with high concentrations of resources, can be particularly vulnerable to herbivore damage. Since a developing leaf cannot be very tough, given the constraints of cell expansion, the major form of protection is likely to be chemical defence. We investigated changes in concentration of herbivore resources (protein, carbohydrates and water) and putative defences (total phenolics, tannin activity, cyanogenic glycosides, alkaloids, cell wall, and leaf mechanics) across five leaf development stages of the soft-leaved Toona ciliata M. Roem. and the tough-leaved Nothofagus moorei (F. Muell.) Krasser. Chemical defences were predicted to be more highly developed in young than expanded leaves of both species, and to decline more in expanded leaves of N. moorei, which become tough and strong at maturity, than in the softer expanded leaves of T. ciliata. Resources and defences were dynamic within the developing leaves. Highest concentrations of protein were recorded in young leaves in both species, and highest levels of non-structural carbohydrate were recorded in young leaves of T. ciliata. Allocation to defence varied in both amount and type across leaf stages. In T. ciliata, there was an increase in chemical defence in expanded leaves (tannin activity, alkaloids). However, in N. moorei, increasing strength and toughness of developing leaves coincided with decreasing chemical defence, consistent with our hypothesis. For phenolics, this decrease was partly due to dilution by cell wall, but cyanogenic glycosides were present in young leaves and absent in fully mature leaves. These results are consistent with leaf toughness acting as an effective anti-herbivore defence, thereby reducing the need for investment in chemical defence.

The potential contribution of biomechanical properties to anti-herbivore defence in seedlings of six Australian rainforest trees

Biomechanical properties of leaves, such as strength and toughness, may contribute to anti-herbivore defence by making it physically difficult or energetically costly for animals to eat them. We investigated leaf strength and toughness in seedlings of six rainforest trees from eastern Australia and their potential contribution to defence. Strength and toughness (work to fracture) were measured at the scale of the whole leaf and of different leaf parts. Resources for herbivores (water and nitrogen) and potential chemical defences (phenolics, alkaloids and cyanogenic glycosides) were also investigated. Leaves of Nothofagus moorei (F.Muell.) Krasser, Ceratopetalum apetalum D.Don and Doryphora sassafras Endl. were generally the toughest and strongest of those studied. Toona ciliata M.Roemer showed high concentrations of nutritive resources and little investment in the defences investigated, consistent with its shorter leaf lifespan and higher growth rate. There were no significant correlations of mechanical properties with palatability, but the softest leaf (T. ciliata) was associated with high levels of leaf damage in bioassay trials. There was also evidence that some leaves that are well-defended mechanically (involving carbon-rich cell wall) may invest less in competing carbon-based chemical defences, such as phenolics.