Ian R. Wallis

Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes

• It has long been believed that plant species from the tropics have higher levels of traits associated with resistance to herbivores than do species from higher latitudes. A meta-analysis recently showed that the published literature does not support this theory. However, the idea has never been tested using data gathered with consistent methods from a wide range of latitudes. • We quantified the relationship between latitude and a broad range of chemical and physical traits across 301 species from 75 sites world-wide. • Six putative resistance traits, including tannins, the concentration of lipids (an indicator of oils, waxes and resins), and leaf toughness were greater in high-latitude species. Six traits, including cyanide production and the presence of spines, were unrelated to latitude. Only ash content (an indicator of inorganic substances such as calcium oxalates and phytoliths) and the properties of species with delayed greening were higher in the tropics. • Our results do not support the hypothesis that tropical plants have higher levels of resistance traits than do plants from higher latitudes. If anything, plants have higher resistance toward the poles. The greater resistance traits of high-latitude species might be explained by the greater cost of losing a given amount of leaf tissue in low-productivity environments.

The detoxification limitation hypothesis : Where did it come from and where is it going?

The detoxification limitation hypothesis is firmly entrenched in the literature to explain various aspects of the interaction between herbivores and plant toxins. These include explanations for the existence of specialist and generalist herbivores and for the prevalence of each of these. The hypothesis suggests that the ability of mammalian herbivores to eliminate plant secondary metabolites (PSMs) largely determines which plants, and how much, they can eat. The value of the hypothesis is that it provides a clear framework for understanding how plant toxins might limit diet breadth. Thus, it is surprising, given its popularity, that there are few studies that provide experimental support either for or against the detoxification limitation hypothesis. There are two likely reasons for this. First, Freeland and Janzen did not formally propose the hypothesis, although it is implicit in their paper. Second, it is a difficult hypothesis to test, requiring an understanding of the metabolic pathways that lead to toxin elimination. Recent attempts to test the hypothesis appear promising. Results suggest that herbivores can recognize mounting saturation of a detoxification pathway and adjust their feeding accordingly to avoid intoxication. One strategy they use is to ingest a food containing a toxin that is metabolized by a different pathway. This demonstrates that careful selection of food plants is a key to existing in a chemically complex environment. As more studies characterize the detoxification products of PSMs, we will better understand how widespread this phenomenon is.

Conflicting demands on detoxification pathways influence how common brushtail possums choose their diets

Most herbivores eat more and survive better when they have access to a variety of foods. One explanation involves the detoxification of plant secondary metabolites (PSMs). By feeding from a variety of plants that contain different classes of PSMs, animals can use multiple detoxification pathways and presumably consume more food. Although popular, this theory is difficult to test because it requires knowledge of the detoxification pathways of each PSM in the diet. We established that common brushtail possums (Trichosurus vulpecula) use various combinations of oxidation, hydrolysis, and conjugation with glucuronic acid (GA) or glycine to detoxify six PSMs. Compared to their ingestion of a single PSM, possums ate more when offered a choice between two diets containing PSMs that require apparently independent detoxification pathways (benzoate and 1,8-cineole, benzoate and p-cymene, benzoate and orcinol, benzoate and salicin, or orcinol and 1,8-cineole). However, possums still did not eat as much of these diets as they did of a basal diet free of PSMs. This suggests that detoxification pathways are never independent, but are separated instead by degrees. In contrast, possums offered a choice of two PSMs that require competing detoxification pathways (1,8-cineole and p-cymene, 1,8-cineole and salicin, or orcinol and salicin) ate no more than when offered diets containing one of the compounds. There was an exception: even though both rutin and orcinol are detoxified via conjugation with GA, the feeding behavior of possums did not suggest competition for detoxification pathways. This implies that the supply of GA is not limiting. This study provides the first convincing evidence that herbivorous mammals can eat more by selecting mixed diets with a diversity of PSMs that make full use of their detoxification potential. It also emphasizes that other behavioral and physiological factors, such as transient food aversions, influence feeding behavior.

Eucalyptus foliar chemistry explains selective feeding by koalas.

The koala is the quintessential specialist herbivore, feeding almost exclusively on Eucalyptus foliage. Consequently, the limitations imposed on the koalas diet by plant defences indicate the extent to which evolutionary adaptations allow mammalian herbivores to circumvent such defences. We tested whether a recently discovered group of plant secondary metabolites, the formylated phloroglucinol compounds (FPCs), deters koalas from feeding on some eucalypt foliage. We found that captive koalas ate less foliage in a single night from trees with high FPC concentrations. Individual trees also differ in the types of FPC they possess, but for a given eucalypt species, most FPCs were similarly effective deterrents. Two closely related and sympatric eucalypt species could be clearly separated by the amounts that koalas ate from each; however, this difference could not be explained by total FPC concentrations alone. We suggest, that in this case, the presence of a distinct type of FPC deters koala herbivory on the less palatable species, and may have facilitated the evolutionary divergence of these species. We conclude that plant defences probably play an important role in determining the distribution and abundance of koalas.

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.

Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula)

The effect of two plant secondary metabolites, tannins and formylated phloroglucinol compounds (FPCs), on the intake of Eucalyptus foliage by common ringtail (Pseudocheirus peregrinus) and common brushtail possums (Trichosurus vulpecula) was studied. We manipulated the amount of tannin that was free to bind with protein by coating foliage with polyethylene glycol 4000 (PEG) and relied on natural intraspecific variation in FPC concentrations. In contrast to ringtail possums, brushtail possums showed a greater tolerance to FPCs and ate more foliage when it was coated with PEG, suggesting that tannins limited their food intake. Brushtails detected the effects of tannins through immediate oral sensations rather than through systemic effects. Ringtail possums appeared highly tolerant of foliar tannins yet susceptible to low concentrations of FPCs. We could not detect any interaction between tannins and FPCs that affected the intake of Eucalyptus foliage by either species of possum. Although ringtail and brushtail possums are widely regarded as specialist and generalist folivores, respectively, their differential susceptibility to co-occurring secondary metabolites suggests greater complexity. Each possum species appears to be a specialist in its own right, which leads to a partitioning of available foliage. Brushtails avoid tannins and ringtails avoid FPCs.

Palatability mapping: a koala's eye view of spatial variation in habitat quality

Ecologists trying to understand the value of habitat to animals must first describe the value of resources contained in the habitat to animals and, second, they must describe spatial variation in resource quality at a resolution relevant to individual animal foraging. We addressed these issues in a study of koalas (Phascolarctos cinereus) in a Eucalyptus woodland. We measured beneficial and deterrent chemical characteristics as well as the palatability of trees using a near-infrared spectroscopic model based on direct feeding experiments. Tree use by koalas was influenced by tree size and foliar quality but was also context-dependent: trees were more likely to be visited if they were surrounded by small, unpalatable trees or by large, palatable trees. Spatial autocorrelation analysis and several mapping approaches demonstrated that foliar quality is spatially structured in the woodland at a scale relevant to foraging decisions by koalas and that the spatial structure is an important component of habitat quality.

Nutritional Ecology of Ateles chamek in lowland Bolivia: How Macronutrient Balancing Influences Food Choices

All free-living animals must make choices regarding which foods to eat, with the choices influencing their health and fitness. An important goal in nutritional ecology is therefore to understand what governs animals’ diet selection. Despite large variation in the availability of different food items, Peruvian spider monkeys (Ateles chamek) maintain a relatively stable daily protein intake, but allow total energy intake to vary as a function of the composition of available food items. This is referred to as protein-dominated macronutrient balancing. Here we assess the influence of this nutritional strategy on daily and seasonal nutritional intakes, estimate the nutritional value of different foods, and interpret unusual food choices. We conducted continuous all-day observations of focal spider monkeys inhabiting a semideciduous forest in Bolivia. We recorded feeding events, collected foods, and analyzed their nutrient content. By using the Geometric Framework for nutrition, we show that individuals reached their daily end-point in nutrient space —balance between protein and nonprotein energy intake— by consuming nutritionally balanced foods or by alternating between nutritionally complementary foods. The macronutritionally balanced figs of Ficus boliviana were their primary staple food and therefore dominated their overall nutritional intake. Our results also demonstrate that spider monkeys consumed a diverse array of ripe fruits to overcome periods of fig scarcity rather than vice versa; they could obtain sufficient protein on a diet of pure fruit; and unripe figs constituted a nutritionally rewarding and reliable food resource. We hope that the approaches taken and the conclusions reached in this study will catalyze further inquiries into the nutritional ecology of frugivorous primates.

Marker-Based Quantitative Genetics in the Wild?: The Heritability and Genetic Correlation of Chemical Defenses in Eucalyptus

Marker-based methods for estimating heritability and genetic correlation in the wild have attracted interest because traditional methods may be impractical or introduce bias via G × E effects, mating system variation, and sampling effects. However, they have not been widely used, especially in plants. A regression-based approach, which uses a continuous measure of genetic relatedness, promises to be particularly appropriate for use in plants with mixed-mating systems and overlapping generations. Using this method, we found significant narrow-sense heritability of foliar defense chemicals in a natural population of Eucalyptus melliodora. We also demonstrated a genetic basis for the phenotypic correlation underlying an ecological example of conditioned flavor aversion involving different biosynthetic pathways. Our results revealed that heritability estimates depend on the spatial scale of the analysis in a way that offers insight into the distribution of genetic and environmental variance. This study is the first to successfully use a marker-based method to measure quantitative genetic parameters in a tree. We suggest that this method will prove to be a useful tool in other studies and offer some recommendations for future applications of the method.

Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum

We studied the influence of a group of plant secondary compounds, the sideroxylonals, on feeding by the common brushtail possum (Trichosurus vulpecula), a generalist herbivore. Possums were offered synthetic diets either with or without sideroxylonals or, in separate experiments, foliage from 28 individual Eucalyptus melliodora trees. Possums ate less of the synthetic diet at sideroxylonal concentrations of 4 and 7 mg g–1 when offered a choice or no choice, respectively. Possums fed foliage in no-choice protocols ate 12–61 g of dry matter per day. Sideroxylonal concentration was an essential determinant of feeding on foliage but the wide variation, particularly at intermediate sideroxylonal concentrations, suggests that other secondary plant chemicals, e.g. tannins, are important also. The normal distribution of sideroxylonal concentrations (mean = 27.7, s.d. = 7.85 mg sideroxylonals per g dry leaf) in a natural population of 150 E. melliodora trees shows that brushtail possums will rarely encounter highly palatable trees ( 40 mg sideroxylonals per g dry leaf). When foraging on E. melliodora, brushtail possums must contend with intermediate sideroxylonal concentrations (20–30 mg per g dry leaf), where variability in food intake is most noticeable.