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 Earth's 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

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.This work was supported by the Australian Research Council http://www.arc.gov.au/ Grant number DP0449621 to CNJ, DP0449544 to WJF. JLD was supported by an Australian National University Graduate School Scholarship

Population-level manipulations of field vole densities induce subsequent changes in plant quality but no impacts on vole demography

Grazing-induced changes in plant quality have been suggested to drive the negative delayed density-dependence exhibited by many herbivore species, but little field evidence exists to support this hypothesis. We tested a key premise of the hypothesis that reciprocal feedback between vole grazing pressure and the induction of anti-herbivore silicon defences in grasses drives observed population cycles in a large-scale field experiment in northern England. We repeatedly reduced population densities of field voles (Microtus agrestis) on replicated 1-ha grassland plots at Kielder Forest, northern England, over a period of one year. Subsequently, we tested for the impact of past density on vole life history traits in spring, and whether these effects were driven by induced silicon defences in the voles’ major over-winter food, the grass Deschampsia caespitosa. After several months of density manipulation, leaf silicon concentrations diverged and averaged 22% lower on sites where vole density had been reduced, but this difference did not persist beyond the period of the density manipulations. There were no significant effects of our density manipulations on vole body mass, spring population growth rate, or mean date for the onset of spring reproduction the following year. These findings show that grazing by field voles does induce increased silicon defences in grasses at a landscape-scale. However, at the vole densities encountered, levels of plant damage appear to be below those needed to induce changes in silicon levels large and persistent enough to affect vole performance, confirming the threshold effects we have previously observed in lab-based studies. Our findings do not support the plant quality hypothesis for observed vole population cycles in northern England, at least over the range of vole densities that now prevail here

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

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 (Medicago 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

Plant Silicon Interactions between Organisms and the Implications for Ecosystems

In this Frontiers topic, we explore how the functions and fates of plant silicon interact with other organisms and ecosystem processes. By bringing together new data from multiple disciplines and scales, we present a cross-section of novel explorations into how plants use silicon and the implications for agriculture and ecosystems. Key aims in this field are to understand the determinants of plant silicon uptake and cycling, and the benefits that silicon uptake confers on plants, including reducing the impacts of stresses such as herbivory. Current research explores inter-specific interactions, including co-evolutionary relationships between plant silicon and animals, particularly morphological adaptations, behavioural responses and the potential for plant silicon to regulate mammal populations. Another emerging area of research is understanding silicon fluxes in soils and vegetation communities and scaling this up to better understand the global silicon cycle. New methods for measuring plant silicon are contributing to progress in this field. Silicon could help plants mitigate some effects of climate change through alleviation of biotic and abiotic stress and silicon is a component of some carbon sinks. Therefore, understanding the role of plant silicon across ecological, agricultural and biogeochemical disciplines is increasingly important in the context of global environmental change

Data from: The ecology of herbivore-induced silicon defences in grasses

Silicon as a defence against herbivory in grasses has gained increasing recognition and has now been studied in a wide range of species, at scales from individual plants in pots to plant communities in the field. The impacts of these defences have been assessed on herbivores ranging from insects to rodents to ungulates. Here, we review current knowledge of silicon mediation of plant–herbivore interactions in an ecological context. The production of silicon defences by grasses is affected by both abiotic and biotic factors and by their interactions. Climate, soil type and water availability all influence levels of silicon uptake, as does plant phenology and previous herbivory. The type of defoliation matters and artificial clipping does not appear to have the same impact on silicon defence induction as herbivory which includes the presence of saliva. Induction of silicon defences has been demonstrated to require a threshold level of damage, both in the laboratory and in the field. In recent studies of vole–plant interactions, the patterns of induction were found to be quantitatively similar in glasshouse compared with field experiments, in terms of both the threshold required for induction and timing of the induction response. The impacts of silicon defences differ between different classes of herbivore, possibly reflecting differences in body size, feeding behaviour and digestive physiology. General patterns are hard to discern however, and a greater number of studies on wild mammalian herbivores are required to elucidate these, particularly with an inclusion of major groups for which there are currently no data, one such example being marsupials. We highlight new research areas to address what still remains unclear about the role of silicon as a plant defence, particularly in relation to plant–herbivore interactions in the field, where the effects of grazing on defence induction are harder to measure. We discuss the obstacles inherent in scaling up laboratory work to landscape-scale studies, the most ecologically relevant but most difficult to carry out, which is the next challenge in silicon ecology

Integrating the effects of PSMs on vertebrate herbivores across spatial and temporal scales

Since Fraenkel (1959) proposed a leading role for plant secondary metabolites (PSMs) in the interactions between plants and herbivores, science has achieved broad insight into the diversity of PSMs and herbivores’ counter-adaptations to them (Freeland & Janzen, 1974; Foley et al., 1999; Foley & Moore, 2005). However, the more we learn about the distributions and functions of PSMs in natural systems, the sharper the limitations of our understanding become. In countless plant–herbivore interactions, ecologists have identified PSMs that act as feeding deterrents, toxins, digestibility reducers, feeding or oviposition cues, and signals for communicating to neighbouring plants and natural enemies of herbivores. However, most studies focus on the interaction between single species of herbivore and plant, usually with observations of captive animals fed diets containing PSMs under highly simplified conditions. Although such approaches are a necessary first step in isolating and characterising the actions of PSMs, they greatly oversimplify the complex interactions that occur between wild herbivores and plants. The next challenge for ecologists is to ‘scale up’ the roles of PSMs in plant–herbivore interactions, as we understand them from controlled experiments at small temporal scales, to predict ecological interactions at greater temporal and spatial extents. A captive herbivore may commonly eat less as PSM concentrations in its food increase, but can this predict the foraging decisions of a wild animal within its home range, or, ultimately the distributions and abundances of plant and herbivore species and genotypes? Scaling up has an obvious spatial component, because wild animals forage more extensively than do captive animals, but it also has a temporal component. Experiments usually describe plant–herbivore interactions over very short time intervals, but in nature they are continuous and the effects of PSMs can be long-lasting (Cheeke, 1998). Animal feeding preferences are dynamic and often change with season or reproductive state, or through the ongoing process of refinement of conditioned flavour aversions (Provenza, 1996). With increasing spatial extent and finer spatial grain size comes greater complexity in the interactions between plants and animals; PSMs are rarely distributed evenly throughout landscapes, and understanding how this influences plant–animal interactions requires approaches adopted from resource ecology, foraging theory and spatial ecology and often an extensive, high-resolution picture of the foodscapes within which animals forage (van Langevelde & Prins, 2008)

Koalas and Climate Change : Hungry for CO2 Cuts

Koalas are iconic animals native to Australia. They are true habitat and food specialists, only ever inhabiting forests and woodlands where Eucalyptus trees are present. Increasing atmospheric CO2 levels will reduce the nutritional quality of Eucalyptus leaves, causing nutrient shortages in the species that forage on them. As a result, Koalas may no longer be able to meet their nutritional demands, resulting in malnutrition and starvation. Increasing frequency and intensity of droughts can force Koalas to descend from trees in search of water or new habitats. This makes them particularly vulnerable to wild and domestic predators, as well as to road traffic, often resulting in death. Koala populations are reported to be declining probably due to malnutrition, the sexually-transmitted disease chlamydia, and habitat destruction. Koalas have very limited capability to adapt to rapid, human-induced climate change, making them very vulnerable to its negative impacts

Data from: 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

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