Evergrowing incisors of diprotodont marsupials record age and life history.

OBJECTIVE: Tooth growth and wear are commonly used tools for determining the age of mammals. The most speciose order of marsupials, Diprotodontia, is characterised by a pair of procumbent incisors within the lower jaw. This study examines the growth and wear of these incisors to understand their relationship with age and sex. DESIGN: Measurements of mandibular incisor crown and root length were made for two sister species of macropodid (kangaroos and wallabies); Macropus giganteus and Macropus fuliginosus. Histological analysis examined patterns of dentine and cementum deposition within these teeth. Broader generalisability within Diprotodontia was tested using dentally reduced Tarsipes rostratus - a species disparate in body size and incisor function to the studied macropodids. RESULTS: In the macropodid sample it is demonstrated that the hypsodont nature of these incisors makes measurements of their growth (root length) and wear (crown length) accurate indicators of age and sex. Model fitting finds that root growth proceeds according to a logarithmic function across the lifespan, while crown wear follows a pattern of exponential reduction for both macropodid species. Histological results find that secondary dentine deposition and cementum layering are further indicators of age. Incisor measurements are shown to correlate with age in the sample of T. rostratus. CONCLUSIONS: The diprotodontian incisor is a useful tool for examining chronological age and sex, both morphologically and microstructurally. This finding has implications for population ecology, palaeontology and marsupial evolution.

Which leaf mechanical traits correlate with insect herbivory among feeding guilds?

BACKGROUND AND AIMS: There is abundant evidence that leaf mechanical traits deter feeding by insect herbivores, but little is known about which particular traits contribute to defence across feeding guilds. We investigated the contribution of multiple mechanical traits from shear, punch and tear tests to herbivore deterrence across feeding guilds. METHODS: Visible damage from miners and external chewers was measured and sucker feeding density estimated in mature leaves of 20 species of forest shrubs and small trees. Cafeteria trials were undertaken using a generalist chewer (larvae of Epiphyas postvittana, Lepidoptera). Damage was compared with leaf mechanical traits and associated nutrient and chemical defence traits. KEY RESULTS: Damage by external chewers in the field and by E. postvittana correlated negatively with mechanical traits. Hierarchical partitioning analysis indicated that the strongest independent contribution to chewing damage was by the material trait of specific work to shear, with 68 % of total variance explained by the combination of specific work to shear (alone explaining 54 %) and tannin activity in a regression model. Mining damage did not correlate with mechanical traits, probably because miners can avoid tissues that generate high strength and toughness in mature leaves. Mechanical traits correlated more strongly with chewing damage in the field than chemical defences (total phenolics and tannin activity) and nutrients (nitrogen and water), but nutrients correlated strongly with diet selection in the cafeteria trial. Surprisingly, sucker feeding density correlated positively with mechanical traits and negatively with nutrients. CONCLUSIONS: Mechanical traits of mature leaves influenced insect feeding guilds differentially, reflecting differences in life history and feeding modes. For external chewers, energy (work) to fracture in shearing tests, at both structural and material levels, was strongly predictive of damage. Knowing which leaf mechanical traits influence insect feeding, and in which guilds, is important to our wider understanding of plant-herbivore interactions.

Wood properties and trunk allometry of co-occurring rainforest canopy trees in a cyclone-prone environment.

PREMISE OF STUDY: New Caledonia commonly experiences cyclones, so trees there are expected to have enhanced wood traits and trunk allometry that confer resistance to wind damage. We ask whether there is evidence of a trade-off between these traits and growth rate among species. METHODS: Wood traits, including density, microfibril angle (MFA), and modulus of elasticity (MOE), ratio of tree height to stem diameter, and growth rate were investigated in mature trees of 15 co-occurring canopy species in a New Caledonian rainforest. KEY RESULTS: In contrast to some studies, wood density did not correlate negatively with growth increment. Among angiosperms, wood density and MOE correlated positively with diameter-adjusted tree height, and MOE correlated positively with stem-diameter growth increment. Tall slender trees achieved high stiffness with high efficiency with respect to wood density, in part by low MFA, and with a higher diameter growth increment but a lower buckling safety factor. However, some tree species of a similar niche differed in whole-tree resistance to wind damage and achieved wood stiffness in different ways. CONCLUSIONS: There was no evidence of a growth-safety trade-off in these trees. In forests that regularly experience cyclones, there may be stronger selection for high wood density and/or stiffness in fast-growing trees of the upper canopy, with the potential growth trade-off amortized by access to the upper canopy and by other plant traits. Furthermore, decreasing wood density does not necessarily decrease resistance to wind damage, resistance being influenced by other characteristics including cell-level traits (e.g., MFA) and whole-plant architecture.

Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia.

BACKGROUND AND AIMS: Plants are likely to invest in multiple defences, given the variety of sources of biotic and abiotic damage to which they are exposed. However, little is known about syndromes of defence across plant species and how these differ in contrasting environments. Here an investigation is made into the association between carbon-based chemical and mechanical defences, predicting that species that invest heavily in mechanical defence of leaves will invest less in chemical defence. METHODS: A combination of published and unpublished data is used to test whether species with tougher leaves have lower concentrations of phenolics, using 125 species from four regions of Australia and the Pacific island of New Caledonia, in evergreen vegetation ranging from temperate shrubland and woodland to tropical shrubland and rainforest. Foliar toughness was measured as work-to-shear and specific work-to-shear (work-to-shear per unit leaf thickness). Phenolics were measured as 'total phenolics' and by protein precipitation (an estimate of tannin activity) per leaf dry mass. KEY RESULTS: Contrary to prediction, phenolic concentrations were not negatively correlated with either measure of leaf toughness when examined across all species, within regions or within any plant community. Instead, measures of toughness (particularly work-to-shear) and phenolics were often positively correlated in shrubland and rainforest (but not dry forest) in New Caledonia, with a similar trend suggested for shrubland in south-western Australia. The common feature of these sites was low concentrations of soil nutrients, with evidence of P limitation. CONCLUSIONS: Positive correlations between toughness and phenolics in vegetation on infertile soils suggest that additive investment in carbon-based mechanical and chemical defences is advantageous and cost-effective in these nutrient-deficient environments where carbohydrate may be in surplus.

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 food's macronutrient content and the insect's 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.

Mass flowering and parental death in the regeneration of Cerberiopsis candelabra (Apocynaceae), a long-lived monocarpic tree in New Caledonia1.

Monocarpy is rare among forest trees, and the selective conditions allowing this life history to evolve are poorly known. Here we examined the regeneration dynamics of a New Caledonian monocarpic tree species, Cerberiopsis candelabra, to better understand how postreproductive mortality and mass flowering might contribute to the success of this strategy. We investigated population size structures and seedling establishment patterns in 18 stands following the 2003 flowering event. We found little evidence of recent recruitment. Instead, population size structures suggested a history of one or more substantial recruitment events followed by recruitment failure, despite multiple flowering events in most populations. The canopy gap created by death of an individual parent appeared generally insufficient to allow seedling establishment, but mass flowering and consequent death of many adults appeared to enhance seedling recruitment by opening more of the canopy. Site means of seedling density below dead parents correlated strongly with light availability and with the proportional density of flowering trees. Therefore, we suggest that mass flowering and gregariousness may have been necessary preconditions for the evolution of monocarpy in this species. However, the degree to which regeneration relies on synchronous flowering and gregariousness vs. infrequent catastrophic disturbances remains uncertain.

Age-size plasticity for reproduction in monocarpic plants.

Empirical and theoretical investigations of monocarpy have usually addressed the question of minimum or threshold sizes for reproduction. However, the range of flowering sizes observed in many monocarpic species is extraordinarily large (well beyond what can be called a "threshold"), and the sizes of flowering and nonflowering plants may overlap greatly. We attempt to explain these reproductive patterns in terms of optimal reaction norms predicted by simple deterministic life history models. We assume that individuals differ in their growth trajectories due to the heterogeneous quality of microsites and ask how the optimal age and size at flowering varies with environmental variation in growth and for different assumptions about fecundity and mortality. Under two very different growth functions (one with no age- or size-related decline in growth rate and another with such a decline as size approaches an asymptote), the optimal reaction norms imply considerable plasticity for size at reproduction, particularly when poor growth is associated with higher mortality or lower asymptotic size. Deterministic models such as these may be more applicable to long-lived than to short-lived monocarps, because fitness potential should be less affected by stochastic variability in yearly growing condition in the former than in the latter. We consider the case of a tropical monocarpic and masting tree species, Cerberiopsis candelabra (Apocynaceae), and show that our model results can account for wide ranges of reproductive size and overlap in size of flowering and nonflowering plants, in accord with observation. We suggest that empirical attention to norms of reaction across growth environments will be a more profitable approach than investigation of size thresholds per se.

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.

Spatial and functional modeling of carnivore and insectivore molariform teeth.

The interaction between the two main competing geometric determinants of teeth (the geometry of function and the geometry of occlusion) were investigated through the construction of three-dimensional spatial models of several mammalian tooth forms (carnassial, insectivore premolar, zalambdodont, dilambdodont, and tribosphenic). These models aim to emulate the shape and function of mammalian teeth. The geometric principles of occlusion relating to single- and double-crested teeth are reviewed. Function was considered using engineering principles that relate tooth shape to function. Substantial similarity between the models and mammalian teeth were achieved. Differences between the two indicate the influence of tooth strength, geometric relations between upper and lower teeth (including the presence of the protocone), and wear on tooth morphology. The concept of "autocclusion" is expanded to include any morphological features that ensure proper alignment of cusps on the same tooth and other teeth in the tooth row. It is concluded that the tooth forms examined are auto-aligning, and do not require additional morphological guides for correct alignment. The model of therian molars constructed by Crompton and Sita-Lumsden ([1970] Nature 227:197-199) is reconstructed in 3D space to show that their hypothesis of crest geometry is erroneous, and that their model is a special case of a more general class of models.

Sclerophylly in two contrasting tropical environments: low nutrients vs. low rainfall.

The defining characteristics of sclerophylly are mechanical (e.g., hardness, toughness, stiffness), but little is known about how they vary in contrasting environments and contribute to the adaptiveness of sclerophylly. Here we investigate how the degree and nature of sclerophylly in terms of leaf mechanics differ between vegetation of two contrasting stressful environments, maquis on nutrient-deficient, moist sites and dry forest on moderate-nutrient, drier sites. We measured toughness, strength, and stiffness at the level of the whole leaf ("structural") and per unit thickness ("material"). Leaves of maquis plants were on average structurally stiffer, stronger, and tougher than those in dry forest. There was little difference in material properties between habitats, and leaf thickness was the main contributor to differences in structural mechanical properties between habitats. Flexural stiffness varied most among species and habitats, correlating strongly with leaf mass per area and thickness. We suggest that having thicker leaves allows efficient packaging of biomass to reduce branching costs in sunny but stressful environments, with subsequent impacts on structural mechanical properties. Sclerophylly is probably a complex phenomenon, however, with its mechanical constitution arising from both evolved mechanical properties that confer protection or resistance to stress and nonadaptive mechanical consequences of adaptation to stressful environments.

Characterizing sclerophylly: the mechanical properties of a diverse range of leaf types.

• Although sclerophylly is defined by textural properties, its adaptive significance has been debated without a strong base of mechanical data. We measured a wide range of mechanical properties across a diverse range of species and leaf forms, including highly scleromorphic leaves, and compared these with sclerophylly indices to determine the mechanical properties of sclerophylls. • Fracture and flexure tests were used to determine leaf strength, toughness (work to fracture) and flexural stiffness ('structural' properties), and specific strength, specific toughness and Young's modulus of elasticity ('material' properties, i.e. normalized per unit leaf thickness). • Leaves varied considerably in all properties tested, and in the way they combined various 'structural' and 'material' properties. However, on average, highly scleromorphic leaves were stronger, tougher and stiffer than soft leaves. 'Structural' properties correlated more strongly with sclerophylly than 'material' properties, and the ratio of stiffness to strength and toughness increased in sclerophyllous species. • Of the structural properties, strength, toughness and flexural stiffness each made substantial independent contributions to the variation in sclerophylly indices, but the best individual explanators were flexural stiffness and strength, with the best predictive model being a combination of these two properties. This model should now be tested on leaves from contrasting environments.