Root Foraging Increases Performance of the Clonal Plant Potentilla reptans in Heterogeneous Nutrient Environments

Background Plastic root-foraging responses have been widely recognized as an important strategy for plants to explore heterogeneously distributed resources. However, the benefits and costs of root foraging have received little attention. Methodology/Principal Findings In a greenhouse experiment, we grew pairs of connected ramets of 22 genotypes of the stoloniferous plant Potentilla reptans in paired pots, between which the contrast in nutrient availability was set as null, medium and high, but with the total nutrient amount kept the same. We calculated root-foraging intensity of each individual ramet pair as the difference in root mass between paired ramets divided by the total root mass. For each genotype, we then calculated root-foraging ability as the slope of the regression of root-foraging intensity against patch contrast. For all genotypes, root-foraging intensity increased with patch contrast and the total biomass and number of offspring ramets were lowest at high patch contrast. Among genotypes, root-foraging intensity was positively related to production of offspring ramets and biomass in the high patch-contrast treatment, which indicates an evolutionary benefit of root foraging in heterogeneous environments. However, we found no significant evidence that the ability of plastic foraging imposes costs under homogeneous conditions (i.e. when foraging is not needed). Conclusions/Significance Our results show that plants of P. reptans adjust their root-foraging intensity according to patch contrast. Moreover, the results show that the root foraging has an evolutionary advantage in heterogeneous environments, while costs of having the ability of plastic root foraging were absent or very small.

Invasive clonal plant species have a greater root-foraging plasticity than non-invasive ones

Clonality is frequently positively correlated with plant invasiveness, but which aspects of clonality make some clonal species more invasive than others is not known. Due to their spreading growth form, clonal plants are likely to experience spatial heterogeneity in nutrient availability. Plasticity in allocation of biomass to clonal growth organs and roots may allow these plants to forage for high-nutrient patches. We investigated whether this foraging response is stronger in species that have become invasive than in species that have not. We used six confamilial pairs of native European clonal plant species differing in invasion success in the USA. We grew all species in large pots under homogeneous or heterogeneous nutrient conditions in a greenhouse, and compared their nutrient-foraging response and performance. Neither invasive nor non-invasive species showed significant foraging responses to heterogeneity in clonal growth organ biomass or in aboveground biomass of clonal offspring. Invasive species had, however, a greater positive foraging response in terms of root and belowground biomass than non-invasive species. Invasive species also produced more total biomass. Our results suggest that the ability for strong root foraging is among the characteristics promoting invasiveness in clonal plants.

Interactive effects of mycorrhizae and a root hemiparasite on plant community productivity and diversity

Plant communities can be affected both by arbuscular mycorrhizal fungi (AMF) and hemiparasitic plants. However, little is known about the interactive effects of these two biotic factors on the productivity and diversity of plant communities. To address this question, we set up a greenhouse study in which different AMF inocula and a hemiparasitic plant (Rhinanthus minor) were added to experimental grassland communities in a fully factorial design. In addition, single plants of each species in the grassland community were grown with the same treatments to distinguish direct AMF effects from indirect effects via plant competition. We found that AMF changed plant community structure by influencing the plant species differently. At the community level, AMF decreased the productivity by 15-24%, depending on the particular AMF treatment, mainly because two dominant species, Holcus lanatus and Plantago lanceolata, showed a negative mycorrhizal dependency. Concomitantly, plant diversity increased due to AMF inoculation and was highest in the treatment with a combination of two commercial AM strains. AMF had a positive effect on growth of the hemiparasite, and thereby induced a negative impact of the hemiparasite on host plant biomass which was not found in non-inoculated communities. However, the hemiparasite did not increase plant diversity. Our results highlight the importance of interactions with soil microbes for plant community structure and that these indirect effects can vary among AMF treatments. We conclude that mutualistic interactions with AMF, but not antagonistic interactions with a root hemiparasite, promote plant diversity in this grassland community.

Herbaceous plant species invading natural areas tend to have stronger adaptive root foraging than other naturalized species

Although plastic root-foraging responses are thought to be adaptive, as they may optimize nutrient capture of plants, this has rarely been tested. We investigated whether nutrient-foraging responses are adaptive, and whether they pre-adapt alien species to become natural-area invaders. We grew 12 pairs of congeneric species (i.e., 24 species) native to Europe in heterogeneous and homogeneous nutrient environments, and compared their foraging responses and performance. One species in each pair is a USA natural-area invader, and the other one is not. Within species, individuals with strong foraging responses, measured as plasticity in root diameter and specific root length, had a higher biomass. Among species, the ones with strong foraging responses, measured as plasticity in root length and root biomass, had a higher biomass. Our results therefore suggest that root foraging is an adaptive trait. Invasive species showed significantly stronger root-foraging responses than non-invasive species when measured as root diameter. Biomass accumulation was decreased in the heterogeneous vs. the homogeneous environment. In aboveground, but not belowground and total biomass, this decrease was smaller in invasive than in non-invasive species. Our results show that strong plastic root-foraging responses are adaptive, and suggest that it might aid in pre-adapting species to becoming natural-area invaders.

The Role of Plant Primary and Secondary Metabolites in Root-Herbivore Behaviour, Nutrition and Physiology

Many insect herbivores feed on belowground plant tissues. In this chapter, we discuss how they have adapted to deal with root primary and secondary metabolites. It is becoming evident that root herbivores can use root volatiles and exudates for host location and foraging. Their complex sensory apparatus suggests a sophisticated recognition and signal transduction system. Furthermore, endogenous metabolites trigger attractive or repellent responses in root feeders, indicating that they may specifically fine-tune food uptake to meet their dietary needs. Little evidence for direct toxic effects of root secondary metabolites has accumulated so far, indicating high prevalence of tolerance mechanisms. Root herbivores furthermore facilitate the entry of soil microbes into the roots, which may influence root nutritional quality. Investigating the role of plant metabolites in an ecologically and physiologically relevant context will be crucial to refine our current models on root-herbivore physiology and behaviour in the future.

Herbivore-induced plant volatiles mediate host selection by a root herbivore

In response to herbivore attack, plants mobilize chemical defenses and release distinct bouquets of volatiles. Aboveground herbivores are known to use changes in leaf volatile patterns to make foraging decisions, but it remains unclear whether belowground herbivores also use volatiles to select suitable host plants. We therefore investigated how above- and belowground infestation affects the performance of the root feeder Diabrotica virgifera virgifera, and whether the larvae of this specialized beetle are able to use volatile cues to assess from a distance whether a potential host plant is already under herbivore attack. Diabrotica virgifera larvae showed stronger growth on roots previously attacked by conspecific larvae, but performed more poorly on roots of plants whose leaves had been attacked by larvae of the moth Spodoptera littoralis. Fittingly, D. virgifera larvae were attracted to plants that were infested with conspecifics, whereas they avoided plants that were attacked by S. littoralis. We identified (E)-β-caryophyllene, which is induced by D. virgifera, and ethylene, which is suppressed by S. littoralis, as two signals used by D. virgifera larvae to locate plants that are most suitable for their development. Our study demonstrates that soil-dwelling insects can use herbivore-induced changes in root volatile emissions to identify suitable host plants.

A specialist root herbivore reduces plant resistance and uses an induced plant volatile to aggregate in a density-dependent manner

1.Leaf-herbivore attack often triggers induced resistance in plants. However, certain specialist herbivores can also take advantage of the induced metabolic changes. In some cases, they even manipulate plant resistance, leading to a phenomenon called induced susceptibility. Compared to above-ground plant-insect interactions, little is known about the prevalence and consequences of induced responses below-ground. 2.A recent study suggested that feeding by the specialist root herbivore Diabrotica virgifera virgifera makes maize roots more susceptible to conspecifics. To better understand this phenomenon, we conducted a series of experiments to study the behavioural responses and elucidate the underlying biochemical mechanisms. 3.We found that D. virgifera benefitted from feeding on a root system in groups of intermediate size (3–9 larvae/plant in the laboratory), whereas its performance was reduced in large groups (12 larvae/plant). Interestingly, the herbivore was able to select host plants with a suitable density of conspecifics by using the induced plant volatile (E)-β-caryophyllene in a dose-dependent manner. Using a split root experiment, we show that the plant-induced susceptibility is systemic and, therefore, plant mediated. Chemical analyses on plant resource reallocation and defences upon herbivory showed that the systemic induced-susceptibility is likely to stem from a combination of (i) increased free amino acid concentrations and (ii) relaxation of defence inducibility. 4.These findings show that herbivores can use induced plant volatiles in a density-dependent manner to aggregate on a host plant and change its metabolism to their own benefit. Our study furthermore helps to explain the remarkable ecological success of D. virgifera in maize fields around the world.

A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack

Plants produce large amounts of secondary metabolites in their shoots and roots and store them in specialized secretory structures. Although secondary metabolites and their secretory structures are commonly assumed to have a defensive function, evidence that they benefit plant fitness under herbivore attack is scarce, especially below ground. Here, we tested whether latex secondary metabolites produced by the common dandelion (Taraxacum officinale agg.) decrease the performance of its major native insect root herbivore, the larvae of the common cockchafer (Melolontha melolontha), and benefit plant vegetative and reproductive fitness under M. melolontha attack. Across 17 T. officinale genotypes screened by gas and liquid chromatography, latex concentrations of the sesquiterpene lactone taraxinic acid β-D-glucopyranosyl ester (TA-G) were negatively associated with M. melolontha larval growth. Adding purified TA-G to artificial diet at ecologically relevant concentrations reduced larval feeding. Silencing the germacrene A synthase ToGAS1, an enzyme that was identified to catalyze the first committed step of TA-G biosynthesis, resulted in a 90% reduction of TA-G levels and a pronounced increase in M. melolontha feeding. Transgenic, TA-G-deficient lines were preferred by M. melolontha and suffered three times more root biomass reduction than control lines. In a common garden experiment involving over 2,000 T. officinale individuals belonging to 17 different genotypes, high TA-G concentrations were associated with the maintenance of high vegetative and reproductive fitness under M. melolontha attack. Taken together, our study demonstrates that a latex secondary metabolite benefits plants under herbivore attack, a result that provides a mechanistic framework for root herbivore driven natural selection and evolution of plant defenses below ground.

A below-ground herbivore shapes root defensive chemistry in natural plant populations

Plants display extensive intraspecific variation in secondary metabolites. However, the selective forces shaping this diversity remain often unknown, especially below ground. Using Taraxacum officinale and its major native insect root herbivore Melolontha melolontha, we tested whether below-ground herbivores drive intraspecific variation in root secondary metabolites. We found that high M. melolontha infestation levels over recent decades are associated with high concentrations of major root latex secondary metabolites across 21 central European T. officinale field populations. By cultivating offspring of these populations, we show that both heritable variation and phenotypic plasticity contribute to the observed differences. Furthermore, we demonstrate that the production of the sesquiterpene lactone taraxinic acid β-d-glucopyranosyl ester (TA-G) is costly in the absence, but beneficial in the presence of M. melolontha, resulting in divergent selection of TA-G. Our results highlight the role of soil-dwelling insects for the evolution of plant defences in nature.

Epigenetic variation creates potential for evolution of plant phenotypic plasticity

Heritable variation in plant phenotypes, and thus potential for evolutionary change, can in principle not only be caused by variation in DNA sequence, but also by underlying epigenetic variation. However, the potential scope of such phenotypic effects and their evolutionary significance are largely unexplored. Here, we conducted a glasshouse experiment in which we tested the response of a large number of epigenetic recombinant inbred lines (epiRILs) of Arabidopsis thaliana – lines that are nearly isogenic but highly variable at the level of DNA methylation – to drought and increased nutrient conditions. We found significant heritable variation among epiRILs both in the means of several ecologically important plant traits and in their plasticities to drought and nutrients. Significant selection gradients, that is, fitness correlations, of several mean traits and plasticities suggest that selection could act on this epigenetically based phenotypic variation. Our study provides evidence that variation in DNA methylation can cause substantial heritable variation of ecologically important plant traits, including root allocation, drought tolerance and nutrient plasticity, and that rapid evolution based on epigenetic variation alone should thus be possible.

Sequence of arrival determines plant-mediated interactions between herbivores

Induced changes in plant quality can mediate indirect interactions between herbivores. Although the sequence of attack by different herbivores has been shown to influence plant responses, little is known about how this affects the herbivores themselves. We therefore investigated how induction by the leaf herbivore Spodoptera frugiperda influences resistance of teosinte (Zea mays mexicana) and cultivated maize (Zea mays mays) against root-feeding larvae of Diabrotica virgifera virgifera. The importance of the sequence of arrival was tested in the field and laboratory. Spodoptera frugiperda infestation had a significant negative effect on colonization by D. virgifera larvae in the field and weight gain in the laboratory, but only when S. frugiperda arrived on the plant before the root herbivore. When S. frugiperda arrived after the root herbivore had established, no negative effects on larval performance were detected. Yet, adult emergence of D. virgifera was reduced even when the root feeder had established first, indicating that the negative effects were not entirely absent in this treatment. The defoliation of the plants was not a decisive factor for the negative effects on root herbivore development, as both minor and major leaf damage resulted in an increase in root resistance and the extent of biomass removal was not correlated with root-herbivore growth. We propose that leaf-herbivore-induced increases in feeding-deterrent and/or toxic secondary metabolites may account for the sequence-specific reduction in root-herbivore performance. Synthesis. Our results demonstrate that the sequence of arrival can be an important determinant of plant-mediated interactions between insect herbivores in both wild and cultivated plants. Arriving early on a plant may be an important strategy of insects to avoid competition with other herbivores. To fully understand plant-mediated interactions between insect herbivores, the sequence of arrival should be taken into account. © 2011 The Authors. Journal of Ecology © 2011 British Ecological Society.

Factors controlling decomposition rates of fine root litter in temperate forests and grasslands

Background and aims Fine root decomposition contributes significantly to element cycling in terrestrial ecosystems. However, studies on root decomposition rates and on the factors that potentially influence them are fewer than those on leaf litter decomposition. To study the effects of region and land use intensity on fine root decomposition, we established a large scale study in three German regions with different climate regimes and soil properties. Methods In 150 forest and 150 grassland sites we deployed litterbags (100 μm mesh size) with standardized litter consisting of fine roots from European beech in forests and from a lowland mesophilous hay meadow in grasslands. In the central study region, we compared decomposition rates of this standardized litter with root litter collected on-site to separate the effect of litter quality from environmental factors. Results Standardized herbaceous roots in grassland soils decomposed on average significantly faster (24 ± 6 % mass loss after 12 months, mean ± SD) than beech roots in forest soils (12 ± 4 %; p < 0.001). Fine root decomposition varied among the three study regions. Land use intensity, in particular N addition, decreased fine root decomposition in grasslands. The initial lignin:N ratio explained 15 % of the variance in grasslands and 11 % in forests. Soil moisture, soil temperature, and C:N ratios of soils together explained 34 % of the variance of the fine root mass loss in grasslands, and 24 % in forests. Conclusions Grasslands, which have higher fine root biomass and root turnover compared to forests, also have higher rates of root decomposition. Our results further show that at the regional scale fine root decomposition is influenced by environmental variables such as soil moisture, soil temperature and soil nutrient content. Additional variation is explained by root litter quality.