Jane L. DeGabriel

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.

The effect of plant secondary metabolites on the interplay between the internal and external environments of marsupial folivores

Most woody plants contain a diverse array of plant secondary metabolites (PSMs) that deter vertebrate herbivores. However, mammalian folivores have evolved a complex of physiological and behavioural strategies to counter these compounds, leading to the development of an “evolutionary arms race”. Marsupial folivores are ideal models to investigate the role of PSMs in the interaction between the external foraging environment and the digestive physiology of mammalian herbivores, as we have a very strong understanding of the diversity and modes of action of PSMs in Eucalyptus, as well as the mechanisms by which animals overcome the effects of these compounds. Studies of marsupial folivores have benefited from the facts that: these herbivores subsist on relatively poor quality diets; they include feeding types from specialist species such as the koala, to generalists; and life history factors such as maternal investment in reproduction can be measured more easily than in eutherians. Here, we describe patterns of spatial variation in the types and distributions of plant secondary metabolites in Australian forests and discuss how this variation influences foraging behaviour, habitat selection and life history strategies in arboreal, folivorous marsupials. We also provide a summary of our understanding of the mechanisms by which marsupials detect and regulate their intake of toxic compounds. While our examples are drawn largely from studies of the interaction between marsupials and Eucalyptus, this knowledge is applicable to advancing our understanding of interactions in plant–mammal systems more broadly. We also identify and discuss key areas that should be the focus of future research.

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.

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.

The effect of excesses and deficiencies in amino acids on the feeding behaviour of the common brushtail possum ( Trichosurus vulpecula )

Abstract. In this study of the amino acid nutrition of a marsupial we tested three hypotheses: (a) that brushtail possums eat less when diets contain excesses or deficiencies in essential amino acids, (b) that brushtail possums choose diets that do not contain amino acid excesses, and (c) that amino acid consumption is mediated partly by the 5HT3 receptor. Possums ate less when 0.2–1.0% methionine (wet matter) was added to the diet, but similar concentrations of lysine and threonine had little effect. However, when given a choice, possums always selected the basal ration over one with added lysine, methionine or threonine at concentrations between 0.05% and 0.9%. In contrast to the experiments with excess amino acids, possums did not eat less of a diet almost devoid of an essential amino acid. Instead, the possums ate less when their diets contained synthetic amino acids rather than similar amounts and proportions of amino acids as casein. Contrary to the third hypothesis, the 5HT3 receptor antagonist, ondansetron, did not affect feeding by possums given a diet containing 0.8% methionine, suggesting that post-ingestive feedback, via the 5HT3 receptor, does not regulate amino acid intake when diets contain amino acid excesses.

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.

Diversity and specificity of sap-feeding herbivores and their parasitoids on Australian fig trees

The ecology, diversity, and parasitoid complex of plant–sap feeding insects of the family Homotomidae (Hemiptera: Psylloidea) specialised on fig trees (Ficus) have so far received little research attention. They are ecologically important, however, as occasional outbreaks of the homotomid Mycopsylla fici may cause complete defoliation of its host plant, the Moreton Bay fig (Ficus macrophylla). Mycopsylla proxima, the only other species reported from Australia, feeds on F. rubiginosa without any recorded outbreaks. We searched for homotomids and their parasitoids on eight Ficus species on the east coast of Australia, Lord Howe Island (LHI), and in Auckland, New Zealand, and detected them on three Ficus species. Using mitochondrial and nuclear DNA sequences, we delimited three Mycopsylla species, including a putative new species on F. watkinsiana. We also characterised six (including one previously described) parasitoid species of the genus Psyllaephagus (Hymenoptera: Encyrtidae) based on congruent morphological characters and molecular data. Each of the homotomid species was highly host specific to a single fig species, whereas parasitoid species varied in host specificity: three host specific to M. fici and three host generalists. Geographic distribution varied among parasitoid species; e.g. one host‐specific species was found on both the mainland and LHI, but a second species only on LHI. Our study revealed previously unrecognised diversity in fig homotomids and especially in their parasitoids. The herbivores and parasitoids showed contrasting patterns of host specificity. Interestingly, M. fici, the only outbreak species, had the highest diversity of associated parasitoid species and was the only species with host‐specific parasitoids.

Local coexistence and genetic isolation of three pollinator species on the same fig tree species

Molecular tools increasingly reveal cryptic lineages and species that were previously unnoticed by traditional taxonomy. The discovery of cryptic species in sympatry prompts the question of how they coexist in the apparent absence of ecological divergence. However, this assumes first that the molecular taxonomy used to identify cryptic lineages delimits species boundaries accurately. This issue is important, because many diversity studies rely heavily or solely on data from mitochondrial DNA sequences for species delimitation, and several factors may lead to poor identification of species boundaries. We used a multilocus population genetics approach to show that three mtDNA-defined cryptic lineages of the fig wasp Pleistodontes imperialis Saunders, which pollinate Port Jackson figs (Ficus rubiginosa) in north-eastern Australia, represent reproductively isolated species. These species coexist locally, with about 13% of figs (where mating occurs) containing wasps from two or three species. However, there was no evidence for gene flow between them. Confirmed cases of coexisting cryptic species provide excellent opportunities for future studies of the ecological and evolutionary forces shaping both species coexistence and fig/pollinator coevolution.

Silicon-induced root nodulation and synthesis of essential amino acids in a legume is associated with higher herbivore abundance

Summary Ecologists have become increasingly aware that silicon uptake by plants, especially the Poaceae, can have beneficial effects on both plant growth and herbivore defence. The effects of silicon on other plant functional groups, such as nitrogen-fixing legumes, have been less well studied. Silicon could, however, indirectly promote herbivore performance in this group if reported increases in N2-fixation caused improvements in host plant quality for herbivores. We tested how silicon supplementation in the legume Medico sativa affected plant growth rates, root nodulation and foliage quality (silicon content and amino acid profiles) for an insect herbivore (Acyrthosiphon pisum). Plants supplemented with silicon (Si+) grew three times as quickly as those without supplementation (Si-), almost entirely in shoot mass. While root growth was unaffected by silicon uptake, root nodules containing nitrogen-fixing bacteria were 44% more abundant on Si+ plants. Aphid abundance was twice as high on Si+ plants compared to Si- plants and was positively correlated with silicon-stimulated plant growth. Si+ plants accumulated more than twice as much silicon as Si- plants, but did not have higher silicon concentrations because of dilution effects linked to the rapid growth of Si+ plants. Si+ plants showed a 65% increase in synthesis of essential foliar amino acids, probably due to increased levels of root nodulation. These results suggest that increased silicon supply makes M. sativa more susceptible to A. pisum, mainly because of increased plant growth and resource availability (i.e. essential amino acids). While silicon augmentation of the Poaceae frequently improves herbivore defence, the current study illustrates that this cannot be assumed for other plant families where the beneficial effects of silicon on plant growth and nutrition may promote herbivore performance in some instances. This article is protected by copyright. All rights reserved.

Editorial: Plant Silicon Interactions between Organisms and the Implications for Ecosystems

Silicon (Si) is a beneficial, if not essential, plant nutrient (Epstein, 1994). As the second most abundant element in the Earths crust it has a global cycling budget similar to that of carbon (Conley, 2002). Some ecological roles of Si are characterized (Cooke and Leishman, 2011), but recent technological advances mean unprecedented understanding of functions at multiple scales, and recognition of its importance to global biogeochemical cycling and food security. We present eight original research papers and an opinion article highlighting the novelty and diversity of recent research. New methods, fresh approaches in both applied and fundamental Si research, innovative herbivore defense experiments, ecosystem-scale field measurements, and Si changes under climate change are investigated. The diversity of topics reveals the complexity of plant responses in terms of Si accumulation, distribution, and function, which are contingent on genotype, biotic interactions, and environmental conditions.