Clare McArthur

Global patterns of leaf mechanical properties

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

PREDICTING DIGESTIBLE PROTEIN AND DIGESTIBLE DRY MATTER IN TANNIN-CONTAINING FORAGES CONSUMED BY RUMINANTS'

Equations for predicting digestible protein and digestible dry matter on the basis of laboratory analytical techniques (Robbins et al. 1987a, b) were tested with in vivo digestion trials using black-tailed deer (Odocoileus hemionus sitkensis). Leaves of seven natural, tannin-containing forages and twigs from one browse species were fed fresh in total collection digestion trials. The equation for estimating digestible protein was based on the plants crude protein content and a measure of the tannins protein-precipitating capacity. The equation for estimating digestible dry matter was based on a measure of tannin astringency and the concentrations of neutral detergent fiber, lignin, cutin, and biogenic silica. Both equations predicted in vivo results accurately, although a slight mod- ification of the laboratory technique was recommended for determining neutral detergent fiber. Sodium sulfite should be used when analyzing tannin-containing forb and shrub leaves and omitted for relatively tannin-free forages. The equations provide useful measures of both the ecological effectiveness of tannins as digestion-reducing agents and the nutri- tional value of the ingested plant matter for the animal.

Salivary proline-rich proteins in mammals: roles in oral homeostasis and counteracting dietary tannin

We review information on the structure of proline-rich proteins (PRPs), their various functions related to oral homeostasis and dietary tannin, and the structural basis of these functions. Consideration of the multifunctional nature of these salivary proteins helps explain both the subtle and large variations found in structure and secretion rates both within individuals and between species. We propose that the ancestral function of PRPs is in maintaining oral homeostasis and that counteracting dietary tannins by binding with them is a derived function. PRPs are effective in oral homeostasis at low secretion levels, whereas counteracting tannin depends on high secretion levels. In the dietary habits ranging from carnivores through omnivores to exclusively planteaters, the dietary nitrogen level is progressively reduced, and plant allelochemical intake, including tannins, increases. We suggest that during this evolution from meat-eater to plant-eater, there was some point in omnivory at which selective pressure from nitrogen limitations, arising from a low nitrogen/high tannin diet, became sufficiently great for the evolution of increased secretion level and diversification of PRPs for dealing with tannin. If this hypothesis is correct, carnivorous mammals should secrete low levels of PRPs for oral homeostasis, but should never secrete high levels, unless they are secondarily carnivorous. Omnivores consuming a diet of very little animal tissue but higher levels of tannin-containing foliage or fruit should generally have the capacity to produce high levels of salivary PRPs. Browsers and frugivores should also produce high levels of PRPs, but grazers may have reduced secretion rates depending on the antiquity of the dietary habit. This hypothesis is consistent with the limited information available on the abundance, type, and distribution of PRPs in mammals. Studies are suggested which would test the functional and evolutionary arguments presented.

Effects of Two Plant Secondary Metabolites, Cineole and Gallic Acid, on Nightly Feeding Patterns of the Common Brushtail Possum

We investigated effects of two plant secondary metabolites (PSMs), cineole and gallic acid, on the nightly feeding behavior of the common brushtail possum (Trichosurus vulpecula), a generalist folivore. We tested whether possums altered their feeding behavior in response to increasing levels of cineole, a dietary terpene. Possums were fed artificial diets containing three levels of cineole; zero (basal diet), medium (6.8% of total dry matter, DM), and high (15.3% DM). In another experiment, we introduced gallic acid, a dietary phenolic, into the diets. Possums were offered a Choice PSM diet (cineole and gallic acid diets simultaneously) or a No-Choice PSM diet (containing either cineole or gallic acid). Detoxification products of cineole and gallic acid were examined in urine to determine that different detoxification pathways were utilized in the elimination of each compound. With increasing cineole levels, possums ate less, had smaller feeding bouts, and had a lower rate of intake, but did not extend their total nightly feeding time. Possums offered the Choice PSM diet, compared with the No-Choice diets, ate more, had larger feeding bouts, and tended to increase their rate of intake. Results from the urinary analysis indicated that gallic acid and cineole were not involved in competing detoxification pathways in brushtail possums. There was also a significant sex effect: females ate more overall, ate more per feeding bout, and ate at a higher rate than males. These results indicate that PSMs not only constrain overall intake, but that possums alter their feeding behavior in response to them. Altered feeding patterns may reduce the negative influence of PSMs on intake.

Genetic variation in resistance of Eucalyptus globulus to marsupial browsers

The evolution of plant defensive traits in response to selection pressures imposed by herbivores is central to co-evolutionary theory. To demonstrate the role of herbivores as selective agents on plant resistance there must be variability in plant resistance to herbivores within a plant population. This variability must be under genetic control, and the variability in plant resistant traits and consequently herbivore damage to plants must reflect variability in plant fitness. We used a common eucalypt species, Eucalyptus globulus, and two major mammalian herbivores, the common brushtail possum (Trichosurus vulpecula) and the red-bellied pademelon (Thylogale billardierii), as a system to investigate intraspecific variation in plant resistance to mammalian herbivores and to investigate if this variation has a genetic basis. We measured mammalian browsing damage on 2,302 individual trees of E. globulus, from 563 families derived from range-wide native stand seed collections of known pedigree and grown in a common environment field trial. Using a selection of trees from the field trial we then conducted a feeding trial with captive herbivores to assess if the genetic variation in plant resistance in the field was reflected in feeding preferences of captive animals, as measured by relative intake. Results from the field trial showed significant genetic variation in plant resistance amongst races, localities and amongst different families. These results were consolidated in the captive trial with similar trends in genetic variation among E. globulus localities. Dry matter intake of foliage by Trichosurus vulpecula was consistently greater than that by Thylogale billardierii; however, the intraspecific preferences of the two herbivores were significantly correlated.

PHOTOINHIBITION: A LINK BETWEEN EFFECTS OF THE ENVIRONMENT ON EUCALYPT LEAF CHEMISTRY AND HERBIVORY

We investigated effects of light and nutrients on whole plant growth, ecophysiology, and leaf chemistry of Eucalyptus nitens seedlings, and the effect of these characteristics on herbivory by common brushtail possums (Trichosurus vulpecula) and red-bellied pademelons (Thylogale billardierii). We compared results of the response of plant secondary chemistry to changes in environmental conditions against two contrasting hypotheses: (1) the carbon:nutrient balance hypothesis (CNBH) and (2) the photoinhibition hypothesis. Nutrient and light levels affected relative growth rate and leaf area ratio of seedlings. Electron transport rates and optimum photochemical efficiencies indicated different rates of carbon fixation between treatments, consistent with levels of chlorophyll and xanthophyll pigments. Nonphotochemical quenching and xanthophylls per unit chlorophyll were negatively correlated with total chlorophyll content. Consistent with the photoinhibition hypothesis, levels of leaf phenolics (flavonols, hydrolyzable tannins, and sideroxylonals) per unit chlorophyll were also negatively correlated with total chlorophyll content. In contrast, phenolic levels on a dry-mass basis were not consistent with predictions of the CNBH; they were better explained as a response to severity of photoinhibition than by reallocation of resources from growth to defense. Total essential oil and cineole levels were positively correlated with nitrogen levels, but there was an interaction in their response to nutrients and light. Thus, levels of essential oils were not well predicted by the CNBH. Sideroxylonal and cineole levels were not correlated, and we hypothesize that different processes and requirements drive their production. Intake of seedlings by possums and pademelons was not directly negatively correlated with levels of hydrolyzable tannins, sideroxylonals, or essential oils. An interaction of the costs of these compounds against benefits of nitrogen levels may explain patterns in intake. We suggest that, while environmentally induced levels of carbon-based plant secondary metabolites have consequences for herbivory, photoinhibition may drive the adjustment of levels of leaf phenolics in response to variation in light and nutrients. This contrasts with the view that these adjustments represent a trade-off in resource allocation between growth and defense.

Effects of nutrient variability on the genetic-based resistance of Eucalyptus globulus to a mammalian herbivore and on plant defensive chemistry

Plant resistance to herbivores can be influenced not only by the independent effects of plant genotype and environmental variation, but by interactions between the two. The main aim of this study was to assess the effects of environmental variability (nutrient treatment) on the known genetic-based expression of resistance and defensive chemistry of Eucalyptus globulus to browsing by the generalist mammalian herbivore Trichosurus vulpecula. In a captive feeding trial, we measured intake of seedlings from one relatively resistant (Blue Gum Hill) and one relatively susceptible (St Helens) population of E. globulus grown under two nutrient treatments (no fertiliser, plus fertiliser). There was a significant genotype×fertiliser interaction effect on intake of E. globulus foliage by T. vulpecula, and the predicted genetic-based resistance of the two populations was expressed only for the non-fertilised treatment. Expression of resistance largely reflected the combined and inverse effects of nitrogen and condensed tannin concentrations. The expression of plant secondary metabolite concentration differed between compounds, but in all cases the effects of plant genotype and fertiliser treatment were independent. The formylated phloroglucinol compounds differed significantly between genotypes but not between fertiliser treatments. In contrast, the effect of plant genotype on the expression of condensed tannins was weak but they were significantly reduced by fertiliser. Essential oils were influenced by both plant genotype and fertiliser treatment and were significantly higher in the fertilised seedlings than in the non-fertilised seedlings. This study highlights interactive effects of plant genotype and environment in influencing the phenotypic expression of resistance in a eucalypt species to a mammalian browser. It also demonstrates that this interactive effect is the net result of independent effects of genotype and environment on plant chemistry and finally, that different groups of compounds within a plant can respond very differently to variation in environmental conditions.

Preferences, selection and damage to seedlings under changing availability by two marsupial herbivores

Preferences for and damage to seedlings used in commercial forestry in Tasmania, Australia, by brushtail possums (Trichosurus vulpecula) and Tasmanian pademelons (Thylogale billardierii) were measured in paired-species feeding trials with captive animals. Both possums and pademelons consistently ate foliage more than stem for all seedling species examined. Possums showed significant interspecific foliage preferences more often than pademelons and they often had opposite preferences to pademelons. For possums, Eucalyptus nitens was one of the most preferred species, whereas for pademelons, Acacia melanoxylon and Pinus radiata were preferred. At low damage levels, possums ate the apical bud of seedlings more frequently than pademelons. A non-linear regression model was developed that describes the depletion of two food types by herbivores. A conditional selection index comparing two plant types was derived from the model, allowing selection to be quantified at any stage in the resource depletion process. Results are discussed in relation to the per capita impact of the two herbivore species, the development of non-lethal methods for managing browsing damage and the use of indicator plant species for triggering management options.

A practical guide to avoid giving up on giving-up densities

The giving-up density (GUD) framework provides a powerful experimental approach with a strong theoretical underpinning to quantify foraging outcomes in heterogeneous landscapes. Since its inception, the GUD approach has been applied successfully to a vast range of foraging species and foraging scenarios. However, its application is not simple, as anyone who has tried to use it for the first time might attest. Limitations of the technique were noted at its conception, yet only the artificiality of the patches, the appropriateness of the food resource, and the possibility of multiple visiting foragers were identified. Here we show the current uses of GUD and outline the practical benefits as well as the often overlooked limitations of the technique. We define seven major points that need to be addressed when applying this methodology: (1) the curvilinearity between harvest rate and energy, (2) the energetic state of the forager, (3) the effect of group foraging, (4) food quality and substrate properties, (5) the predictability of the patch, (6) behavioral traits of the forager, and (7) nontarget species. We also suggest how GUD experiments can be enhanced by incorporating complementary methods (such as cameras) to better understand the foraging processes involved in the GUD itself. We conclude that the benefits of using GUD outweigh the costs, but that its limitations should not be ignored. Incorporating new methods when using GUD can potentially offer novel and important insights into the study of foraging behavior.

Inheritance Of Resistance to Mammalian Herbivores and of Plant Defensive Chemistry in an Eucalyptus Species

Hybridization in plants provides an opportunity to investigate the patterns of inheritance of hybrid resistance to herbivores, and of the plant mechanisms conferring this resistance such as plant secondary metabolites. We investigated how inter-race differences in resistance of Eucalyptus globulus to a generalist mammalian herbivore, Trichosurus vulpecula, are inherited in their F1 hybrids. We assessed browsing damage of 3-year-old trees in a common environment field trial on four hybrid types of known progeny. The progeny were artificial intra-race crosses and reciprocal inter-race F1 hybrids of two geographically distinct populations (races) of E. globulus north-eastern Tasmania and south-eastern Tasmania. Populations of trees from north-eastern Tasmania are relatively susceptible to browsing by T. vulpecula, while populations from south-eastern Tasmania are more resistant. We assessed the preferences of these trees in a series of paired feeding trials with captive animals to test the field trial results and also investigated the patterns of inheritance of plant secondary metabolites. Our results demonstrated that the phenotypic expression of resistance of the inter-race F1 hybrids supported the additive pattern of inheritance, as these hybrids were intermediate in resistance compared to the pure parental hybrids. The expression of plant secondary metabolites in the F1 hybrids varied among major groups of individual compounds. The most common pattern supported was dominance towards one of the parental types. Together, condensed tannins and essential oils appeared to explain the observed patterns of resistance among the four hybrid types. While both chemical groups were inherited in a dominant manner in the inter-race F1 hybrids, the direction of dominance was opposite. Their combined concentration, however, was inherited in an additive manner, consistent with the phenotypic differences in browsing.