Summary
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.
Lay Summary
The functional ecology of plant silicon Cooke, Julia; DeGabriel, Jane L.; Hartley, Susan E.
Functional ecology,
08/2016, Volume:
30, Issue:
8
Journal Article
Plants contain a variety of chemical defenses that strongly affect feeding rates in captive mammals, but their effects on the fitness of wild herbivores are largely unknown. This is because the ...complexity of defensive compounds, and herbivores' counteradaptations to them, make their effects in the wild difficult to measure. We show how tannins interact with protein to produce spatial variation in the nutritional quality of eucalypt foliage, which is related to demography in a wild population of a marsupial folivore, the common brushtail possum (Trichosurus vulpecula Kerr). Tannins reduced the digestibility of nitrogen (N) in vitro, creating variation in available N concentrations among the home ranges of individual possums in an otherwise homogeneous habitat. This was strongly correlated with reproductive success: females with better quality trees in their home range reproduced more often and had faster-growing offspring. These results demonstrate a powerful mechanism by which spatial variation in plant chemistry may control herbivore population dynamics in nature.
1. Mutualisms may be particularly vulnerable to climate change as interacting species are likely to respond differently, which could destabilise interactions.
2. Temperate zone insects typically ...experience mean temperatures below their thermal optima, making them less vulnerable than tropical insects to small increases in mean temperature. However, they are likely to experience a higher frequency of extreme heat events, putting mutualism persistence in jeopardy.
3. This study investigated the potential impacts of climate change on
Pleistodontes imperialis
, a temperate Australian fig wasp that pollinates Port Jackson figs (
Ficus rubiginosa
). Wasp emergence and longevity were measured at temperatures ranging from those commonly experienced in nature (25 °C) to high values (> 40 °C) that are currently infrequent, but which are becoming more common with climate change.
4. Wasp emergence was unaffected by temperatures up to 39 °C, but it declined drastically above 39 °C. Adult longevity was unaffected by temperatures up to 30 °C, but decreased at 35 °C and above. Low humidity reduced wasp longevity across all temperatures.
5. Fitness reductions were observed at temperatures ∼5 °C above the summer daily mean maximum, suggesting that
P. imperialis
has a high thermal tolerance, but is vulnerable to extreme heat. Figs located in the shade may provide protected microhabitats under hot conditions.
6. Tropical pollinators may be threatened by small increases in mean temperature. In contrast, it is shown here that temperate pollinators may face a different primary threat from climate change – the increasing frequency of extreme heat events – despite their higher thermal tolerances.
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 defenses 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 1 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 defenses 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 defenses 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 laboratory‐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.
Our manipulative experiment of natural grass‐eating vole populations induced changes in plant quality, but these changes were clearly insufficient in both magnitude and duration to elicit effects on vole demography the following year. 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.
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 (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.
A lay summary is available for this article.
Lay Summary
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.
A central goal of nutritional ecology is to understand how variation in food quality limits the persistence of wild animal populations. Habitat suitability for browsing mammals is strongly affected ...by concentrations of nutrients and plant secondary metabolites (PSMs), but our understanding of this is based mostly on short‐term experiments of diet selection involving captive animals. In the wild, browsers forage in biologically, chemically and spatially‐complex environments, and foraging decisions in response to varying food quality will be correspondingly complicated. We have identified four steps that must be achieved in order to translate our understanding from laboratory experiments to populations of mammalian browsers: 1) knowing what foods and how much of these wild browsers eat, as well as what they avoid eating; 2) knowing the relevant aspects of plant nutritional and defensive chemistry to measure in a given system and how to measure them; 3) understanding the spatial distribution of nutrients and PSMs in plant communities, the costs they impose on foraging and the effects on animals’ distributions; and 4) having appropriate statistical tools to analyse the data. We discuss prospects for each of these prerequisites for extending laboratory studies of nutritional quality, and review recent developments that may offer solutions for field studies. We also provide a synthesis of how to use this nutritional knowledge to link food quality to population regulation in wild mammals and describe examples that have successfully achieved this aim.
Insect herbivores and their parasitoids make up a large proportion of biodiversity, but studies of their communities rarely involve geographic comparisons. If the community on a host plant varies ...geographically, insect diversity will be underestimated by ignoring this. In addition, community functional structure may vary geographically due to differential abundance of functional groups.
To address these issues, we compared the composition and structure of the fig wasp community associated with Ficus rubiginosa between temperate (Sydney) and tropical (Townsville) regions of eastern Australia. We sampled figs from four sites per region, twice a year for 2 years, resulting in about 14,000 wasps from 11 genera and 19 sub‐generic taxa. Since two of these taxa each comprise two cryptic species, we refer to taxonomic diversity below, but this is largely at species level.
Taxonomic richness (14) was the same in both regions and nine taxa were shared across regions. However, 10 taxa were found in only one of the two regions, driving a significant difference in the taxonomic composition of the tropical and temperate communities, and increasing overall diversity in the system.
The wasps belong to five functional groups – pollinators, small and large gallers, and small and large parasitoids. In contrast to taxonomic composition and diversity, community functional structure did not differ significantly between regions.
Our results highlight that there can be broad latitudinal conservation of functional community structure across regions, despite considerable regional differences in taxonomic composition.
The taxonomic composition of the fig wasp community associated with fruits of Ficus rubiginosa changes substantially between tropical and temperate regions in Australia.
However, the wasp functional group structure is not significantly different between these tropical and temperate sites separated by 2500 km.
These contrasting patterns reflect the outcome of ‘like‐for‐like’ geographic turnover of species between regions, involving both morphologically differentiated and cryptic species.
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