While shoot herbivores reduce, root herbivores increase nutrient enrichment's impact on diversity in a grassland model.

Nutrient enrichment is widespread throughout grassland systems and expected to increase during the Anthropocene. Trophic interactions, like aboveground herbivory, have been shown to mitigate its effect on plant diversity. Belowground herbivory may also impact these habitats' response to nutrient enrichment, but its influence is much less understood, and likely to depend on factors such as the herbivores' preference for dominant species and the symmetry of belowground competition. If preferential toward the dominant, fastest growing species, root herbivores may reduce these species' relative fitness and support diversity during nutrient enrichment. However, as plant competition belowground is commonly considered to be symmetric, root herbivores may be less impactful than shoot herbivores because they do not reduce any competitive asymmetry between the dominant and subordinate plants. To better understand this system, we used an established, two-layer, grassland community model to run a full-factorially designed simulation experiment, crossing the complete removal of aboveground herbivores and belowground herbivores with nutrient enrichment. After 100 yr of simulation, we analyzed communities' diversity, competition on the individual level, as well as their resistance and recovery. The model reproduced both observed general effects of nutrient enrichment in grasslands and the short-term trends of specific experiments. We found that belowground herbivores exacerbate the negative influence of nutrient enrichment on Shannon diversity within our model grasslands, while aboveground herbivores mitigate its effect. Indeed, data on individuals' above- and belowground resource uptake reveals that root herbivory reduces resource limitation belowground. As with nutrient enrichment, this shifts competition aboveground. Since shoot competition is asymmetric, with larger, taller individuals gathering disproportionate resources compared to their smaller, shorter counterparts, this shift promotes the exclusion of the smallest species. While increasing the root herbivores' preferences toward dominant species lessens their negative impact, at best they are only mildly advantageous, and they do very little reduce the negative consequences of nutrient enrichment. Because our model's belowground competition is symmetric, we hypothesize that root herbivores may be beneficial when root competition is asymmetric. Future research into belowground herbivory should account for the nature of competition belowground to better understand the herbivores' true influence.

Grazing exclusion by fencing non-linearly restored the degraded alpine grasslands on the Tibetan Plateau.

Resilience is an important aspect of the non-linear restoration of disturbed ecosystems. Fenced grassland patches on the northern Tibetan Plateau can be used to examine the resistance and resilience of degraded alpine grasslands to grazing and to a changing climate. To examine the non-linearity of restoration, we used moderate resolution imaging spectroradiometer (MODIS) normalized difference vegetation index (NDVI) as a proxy for productivity during a ten-year restoration by fencing. Degraded alpine grasslands exhibited three restoration trajectories: an equilibrium in meadows, a non-linear increase across steppes, and an abrupt impulse in desert-steppes following a slight increase in productivity. Combined with weather conditions, the ten-year grazing exclusion has successfully enhanced the NDVI on the most degraded steppes, but did not do so efficiently on either meadows or desert-steppes. Warming favors the NDVI enhancement of degraded meadows, but higher temperatures limited the restoration of degraded steppes and desert-steppes. Precipitation is necessary to restore degraded alpine grasslands, but more precipitation might be useless for meadows due to lower temperatures and for desert-steppes due to limitations caused by the small species pool. We suggest that detailed field observations of community compositional changes are necessary to better understand the mechanisms behind such non-linear ecological restorations.

Fear of predation alters clone-specific performance in phloem-feeding prey.

Fear of predation has been shown to affect prey fitness and behaviour, however, to date little is known about the underlying genetics of responses to predator-associated risk. In an effort to fill this gap we exposed four naïve clones of green peach aphid (Myzus persicae), maintained on the model crop Brassica oleracea, to different types of cues from aphid lion (Chrysoperla carnea). The respective predation risks, we termed Fear Factors, were either lethal (consumption by predator), or non-lethal (non-consumptive predator-associated cues: plant-tethered predator cadavers and homogenised shoot-sprayed or soil-infused blends of predator remains). Our results show that the non-lethal risk cues differentially impeded prey reproductive success that varied by clone, suggesting genotype-specific response to fear of predation. Furthermore, whether plants were perceived as being safe or risky influenced prey responses as avoidance behaviour in prey depended on clone type. Our findings highlight that intra-specific genetic variation underlies prey responses to consumptive and non-consumptive effects of predation. This allows selection to act on anti-predator responses to fear of predation that may ramify and influence higher trophic levels in model agroecosystems.

Sequential above- and belowground herbivory modifies plant responses depending on herbivore identity.

BACKGROUND: Herbivore-induced changes in plant traits can cause indirect interactions between spatially and/or temporally separated herbivores that share the same host plant. Feeding modes of the herbivores is one of the major factors that influence the outcome of such interactions. Here, we tested whether the effects of transient aboveground herbivory for seven days by herbivores of different feeding guilds on tomato plants (Solanum lycopersicum) alters their interaction with spatially as well as temporally separated belowground herbivores. RESULTS: The transient aboveground herbivory by both chewing caterpillars (Spodoptera exigua) and sucking aphids (Myzus persicae) had significant impacts on plant traits such as plant growth, resource allocation and phytohormone contents. While the changes in plant traits did not affect the overall performance of the root-knot nematodes (Meloidogyne incognita) in terms of total number of galls, we found that the consequences of aboveground herbivory for the plants can be altered by the subsequent nematode herbivory. For example, plants that had hosted aphids showed compensatory growth when they were later challenged by nematodes, which was not apparent in plants that had hosted only aphids. In contrast, plants that had been fed by S. exigua larvae did not show such compensatory growth even when challenged by nematodes. CONCLUSION: The results suggest that the earlier aboveground herbivory can modify plant responses to subsequent herbivores, and such modifications may depend upon identity and/or feeding modes of the aboveground herbivores.

Land-use type and intensity differentially filter traits in above- and below-ground arthropod communities.

Along with the global decline of species richness goes a loss of ecological traits. Associated biotic homogenization of animal communities and narrowing of trait diversity threaten ecosystem functioning and human well-being. High management intensity is regarded as an important ecological filter, eliminating species that lack suitable adaptations. Below-ground arthropods are assumed to be less sensitive to such effects than above-ground arthropods. Here, we compared the impact of management intensity between (grassland vs. forest) and within land-use types (local management intensity) on the trait diversity and composition in below- and above-ground arthropod communities. We used data on 722 arthropod species living above-ground (Auchenorrhyncha and Heteroptera), primarily in soil (Chilopoda and Oribatida) or at the interface (Araneae and Carabidae). Our results show that trait diversity of arthropod communities is not primarily reduced by intense local land use, but is rather affected by differences between land-use types. Communities of Auchenorrhyncha and Chilopoda had significantly lower trait diversity in grassland habitats as compared to forests. Carabidae showed the opposite pattern with higher trait diversity in grasslands. Grasslands had a lower proportion of large Auchenorrhyncha and Carabidae individuals, whereas Chilopoda and Heteroptera individuals were larger in grasslands. Body size decreased with land-use intensity across taxa, but only in grasslands. The proportion of individuals with low mobility declined with land-use intensity in Araneae and Auchenorrhyncha, but increased in Chilopoda and grassland Heteroptera. The proportion of carnivorous individuals increased with land-use intensity in Heteroptera in forests and in Oribatida and Carabidae in grasslands. Our results suggest that gradients in management intensity across land-use types will not generally reduce trait diversity in multiple taxa, but will exert strong trait filtering within individual taxa. The observed patterns for trait filtering in individual taxa are not related to major classifications into above- and below-ground species. Instead, ecologically different taxa resembled each other in their trait diversity and compositional responses to land-use differences. These previously undescribed patterns offer an opportunity to develop management strategies for the conservation of trait diversity across taxonomic groups in permanent grassland and forest habitats.

Land-use intensification causes multitrophic homogenization of grassland communities.

Land-use intensification is a major driver of biodiversity loss. Alongside reductions in local species diversity, biotic homogenization at larger spatial scales is of great concern for conservation. Biotic homogenization means a decrease in ß-diversity (the compositional dissimilarity between sites). Most studies have investigated losses in local (α)-diversity and neglected biodiversity loss at larger spatial scales. Studies addressing ß-diversity have focused on single or a few organism groups (for example, ref. 4), and it is thus unknown whether land-use intensification homogenizes communities at different trophic levels, above- and belowground. Here we show that even moderate increases in local land-use intensity (LUI) cause biotic homogenization across microbial, plant and animal groups, both above- and belowground, and that this is largely independent of changes in α-diversity. We analysed a unique grassland biodiversity dataset, with abundances of more than 4,000 species belonging to 12 trophic groups. LUI, and, in particular, high mowing intensity, had consistent effects on ß-diversity across groups, causing a homogenization of soil microbial, fungal pathogen, plant and arthropod communities. These effects were nonlinear and the strongest declines in ß-diversity occurred in the transition from extensively managed to intermediate intensity grassland. LUI tended to reduce local α-diversity in aboveground groups, whereas the α-diversity increased in belowground groups. Correlations between the ß-diversity of different groups, particularly between plants and their consumers, became weaker at high LUI. This suggests a loss of specialist species and is further evidence for biotic homogenization. The consistently negative effects of LUI on landscape-scale biodiversity underscore the high value of extensively managed grasslands for conserving multitrophic biodiversity and ecosystem service provision. Indeed, biotic homogenization rather than local diversity loss could prove to be the most substantial consequence of land-use intensification.

Plant functional trait diversity regulates the nonlinear response of productivity to regional climate change in Tibetan alpine grasslands.

The biodiversity-productivity relationship is still under debate for alpine grasslands on the Tibetan Plateau. We know little about direct and indirect effects of biotic and abiotic drivers on this relationship, especially in regard to plant functional trait diversity. Here, we examine how aboveground net primary productivity (ANPP) and precipitation use efficiency (PUE) respond to climate, soil and community structure across alpine grasslands on the Northern Tibetan Plateau. We found that both ANPP and PUE showed nonlinear patterns along water availability and site altitude variation, which together accounted for 80.3% and 68.8% of variation in ANPP and PUE, respectively, by optimal generalized additive models. Functional trait divergence (FTD) and community weighted mean (CWM) of plant functional traits were as important as plant species diversity (PSD) for explaining the nonlinear productivity-climate relationship. These findings were confirmed by results from principal component analyses and structural equation models. We also found that FTD was negatively correlated with PSD across different alpine grasslands. Our results implicate: first, the combinatorial influences of temperature and precipitation gradients are important for predicting alpine grassland dynamics; second, the convergence and divergence of plant functional traits may have the potential to elucidate the effect of plant diversity on ecosystem functionality.

Shoot- and root-borne cytokinin influences arbuscular mycorrhizal symbiosis.

The arbuscular mycorrhizal (AM) symbiosis is functionally important for the nutrition and growth of most terrestrial plants. Nearly all phytohormones are employed by plants to regulate the symbiosis with AM fungi, but the regulatory role of cytokinin (CK) is not well understood. Here, we used transgenic tobacco (Nicotiana tabacum) with a root-specific or constitutive expression of CK-degrading CKX genes and the corresponding wild-type to investigate whether a lowered content of CK in roots or in both roots and shoots influences the interaction with the AM fungus Rhizophagus irregularis. Our data indicates that shoot CK has a positive impact on AM fungal development in roots and on the root transcript level of an AM-responsive phosphate transporter gene (NtPT4). A reduced CK content in roots caused shoot and root growth depression following AM colonization, while neither the uptake of phosphorus or nitrogen nor the root transcript levels of NtPT4 were significantly affected. This suggests that root CK may restrict the C availability from the roots to the fungus thus averting parasitism by AM fungi. Taken together, our study indicates that shoot- and root-borne CK have distinct roles in AM symbiosis. We propose a model illustrating how plants may employ CK to regulate nutrient exchange with the ubiquitous AM fungi.

A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling.

Plant-microbe mutualisms can improve plant defense, but the impact of root endophytes on below-ground herbivore interactions remains unknown. We investigated the effects of the root endophyte Piriformospora indica on interactions between rice (Oryza sativa) plants and its root herbivore rice water weevil (RWW; Lissorhoptrus oryzophilus), and how plant jasmonic acid (JA) and GA regulate this tripartite interaction. Glasshouse experiments with wild-type rice and coi1-18 and Eui1-OX mutants combined with nutrient, jasmonate and gene expression analyses were used to test: whether RWW adult herbivory above ground influences subsequent damage caused by larval herbivory below ground; whether P. indica protects plants against RWW; and whether GA and JA signaling mediate these interactions. The endophyte induced plant tolerance to root herbivory. RWW adults and larvae acted synergistically via JA signaling to reduce root growth, while endophyte-elicited GA biosynthesis suppressed the herbivore-induced JA in roots and recovered plant growth. Our study shows for the first time the impact of a root endophyte on plant defense against below-ground herbivores, adds to growing evidence that induced tolerance may be an important root defense, and implicates GA as a signal component of inducible plant tolerance against biotic stress.

Priming and memory of stress responses in organisms lacking a nervous system.

Experience and memory of environmental stimuli that indicate future stress can prepare (prime) organismic stress responses even in species lacking a nervous system. The process through which such organisms prepare their phenotype for an improved response to future stress has been termed 'priming'. However, other terms are also used for this phenomenon, especially when considering priming in different types of organisms and when referring to different stressors. Here we propose a conceptual framework for priming of stress responses in bacteria, fungi and plants which allows comparison of priming with other terms, e.g. adaptation, acclimation, induction, acquired resistance and cross protection. We address spatial and temporal aspects of priming and highlight current knowledge about the mechanisms necessary for information storage which range from epigenetic marks to the accumulation of (dormant) signalling molecules. Furthermore, we outline possible patterns of primed stress responses. Finally, we link the ability of organisms to become primed for stress responses (their 'primability') with evolutionary ecology aspects and discuss which properties of an organism and its environment may favour the evolution of priming of stress responses.

Community-Weighted Mean Plant Traits Predict Small Scale Distribution of Insect Root Herbivore Abundance.

Small scale distribution of insect root herbivores may promote plant species diversity by creating patches of different herbivore pressure. However, determinants of small scale distribution of insect root herbivores, and impact of land use intensity on their small scale distribution are largely unknown. We sampled insect root herbivores and measured vegetation parameters and soil water content along transects in grasslands of different management intensity in three regions in Germany. We calculated community-weighted mean plant traits to test whether the functional plant community composition determines the small scale distribution of insect root herbivores. To analyze spatial patterns in plant species and trait composition and insect root herbivore abundance we computed Mantel correlograms. Insect root herbivores mainly comprised click beetle (Coleoptera, Elateridae) larvae (43%) in the investigated grasslands. Total insect root herbivore numbers were positively related to community-weighted mean traits indicating high plant growth rates and biomass (specific leaf area, reproductive- and vegetative plant height), and negatively related to plant traits indicating poor tissue quality (leaf C/N ratio). Generalist Elaterid larvae, when analyzed independently, were also positively related to high plant growth rates and furthermore to root dry mass, but were not related to tissue quality. Insect root herbivore numbers were not related to plant cover, plant species richness and soil water content. Plant species composition and to a lesser extent plant trait composition displayed spatial autocorrelation, which was not influenced by land use intensity. Insect root herbivore abundance was not spatially autocorrelated. We conclude that in semi-natural grasslands with a high share of generalist insect root herbivores, insect root herbivores affiliate with large, fast growing plants, presumably because of availability of high quantities of food. Affiliation of insect root herbivores with large, fast growing plants may counteract dominance of those species, thus promoting plant diversity.

Choosing and using diversity indices: insights for ecological applications from the German Biodiversity Exploratories.

Biodiversity, a multidimensional property of natural systems, is difficult to quantify partly because of the multitude of indices proposed for this purpose. Indices aim to describe general properties of communities that allow us to compare different regions, taxa, and trophic levels. Therefore, they are of fundamental importance for environmental monitoring and conservation, although there is no consensus about which indices are more appropriate and informative. We tested several common diversity indices in a range of simple to complex statistical analyses in order to determine whether some were better suited for certain analyses than others. We used data collected around the focal plant Plantago lanceolata on 60 temperate grassland plots embedded in an agricultural landscape to explore relationships between the common diversity indices of species richness (S), Shannon's diversity (H'), Simpson's diversity (D1), Simpson's dominance (D2), Simpson's evenness (E), and Berger-Parker dominance (BP). We calculated each of these indices for herbaceous plants, arbuscular mycorrhizal fungi, aboveground arthropods, belowground insect larvae, and P. lanceolata molecular and chemical diversity. Including these trait-based measures of diversity allowed us to test whether or not they behaved similarly to the better studied species diversity. We used path analysis to determine whether compound indices detected more relationships between diversities of different organisms and traits than more basic indices. In the path models, more paths were significant when using H', even though all models except that with E were equally reliable. This demonstrates that while common diversity indices may appear interchangeable in simple analyses, when considering complex interactions, the choice of index can profoundly alter the interpretation of results. Data mining in order to identify the index producing the most significant results should be avoided, but simultaneously considering analyses using multiple indices can provide greater insight into the interactions in a system.

Using a multi-trait approach to manipulate plant functional diversity in a biodiversity-ecosystem function experiment.

A frequent pattern emerging from biodiversity-ecosystem function studies is that functional group richness enhances ecosystem functions such as primary productivity. However, the manipulation of functional group richness goes along with major disadvantages like the transformation of functional trait data into categories or the exclusion of functional differences between organisms in the same group. In a mesocosm study we manipulated plant functional diversity based on the multi-trait Functional Diversity (FD)-approach of Petchey and Gaston by using database data of seven functional traits and information on the origin of the species in terms of being native or exotic. Along a gradient ranging from low to high FD we planted 40 randomly selected eight-species mixtures under controlled conditions. We found a significant positive linear correlation of FD with aboveground productivity and a negative correlation with invasibility of the plant communities. Based on community-weighted mean calculations for each functional trait, we figured out that the traits N-fixation and species origin, i.e. being native or exotic, played the most important role for community productivity. Our results suggest that the identification of the impact of functional trait diversity and the relative contributions of relevant traits is essential for a mechanistic understanding of the role of biodiversity for ecosystem functions such as aboveground biomass production and resistance against invasion.

Arbuscular mycorrhizal fungi affect glucosinolate and mineral element composition in leaves of Moringa oleifera.

Moringa is a mycorrhizal crop cultivated in the tropics and subtropics and appreciated for its nutritive and health-promoting value. As well as improving plant mineral nutrition, arbuscular mycorrhizal fungi (AMF) can affect plant synthesis of compounds bioactive against chronic diseases in humans. Rhizophagus intraradices and Funneliformis mosseae were used in a full factorial experiment to investigate the impact of AMF on the accumulation of glucosinolates, flavonoids, phenolic acids, carotenoids, and mineral elements in moringa leaves. Levels of glucosinolates were enhanced, flavonoids and phenolic acids were not affected, levels of carotenoids (including provitamin A) were species-specifically reduced, and mineral elements were affected differently, with only Cu and Zn being increased by the AMF. This study presents novel results on AMF effects on glucosinolates in leaves and supports conclusions that the impacts of these fungi on microelement concentrations in edible plants are species dependent. The nonspecific positive effects on glucosinolates and the species-specific negative effects on carotenoids encourage research on other AMF species to achieve general benefits on bioactive compounds in moringa.

Genetic Variation of the Host Plant Species Matters for Interactions with Above- and Belowground Herbivores.

Plants are challenged by both above- and belowground herbivores which may indirectly interact with each other via herbivore-induced changes in plant traits; however, little is known about how genetic variation of the host plant shapes such interactions. We used two genotypes (M4 and E9) of Solanum dulcamara (Solanaceae) with or without previous experience of aboveground herbivory by Spodoptera exigua (Noctuidae) to quantify its effects on subsequent root herbivory by Agriotes spp. (Elateridae). In the genotype M4, due to the aboveground herbivory, shoot and root biomass was significantly decreased, roots had a lower C/N ratio and contained significantly higher levels of proteins, while the genotype E9 was not affected. However, aboveground herbivory had no effects on weight gain or mortality of the belowground herbivores. Root herbivory by Agriotes increased the nitrogen concentration in the roots of M4 plants leading to a higher weight gain of conspecific larvae. Also, in feeding bioassays, Agriotes larvae tended to prefer roots of M4 over E9, irrespective of the aboveground herbivore treatment. Fourier-Transform Infrared Spectroscopy (FT-IR) documented differences in metabolic profiles of the two plant genotypes and of the roots of M4 plants after aboveground herbivory. Together, these results demonstrate that previous aboveground herbivory can have genotype-specific effects on quantitative and qualitative root traits. This may have consequences for belowground interactions, although generalist root herbivores might not be affected when the root biomass offered is still sufficient for growth and survival.

Plant-mediated links between detritivores and aboveground herbivores.

Most studies on plant-mediated above-belowground interactions focus on soil biota with direct trophic links to plant roots such as root herbivores, pathogens, and symbionts. Detritivorous soil fauna, though ubiquitous and present in high abundances and biomasses in soil, are under-represented in those studies. Understanding of their impact on plants is mainly restricted to growth and nutrient uptake parameters. Detritivores have been shown to affect secondary metabolites and defense gene expression in aboveground parts of plants, with potential impacts on aboveground plant-herbivore interactions. The proposed mechanisms range from nutrient mobilization effects and impacts on soil microorganisms to defense induction by passive or active ingestion of roots. Since their negative effects (disruption or direct feeding of roots) may be counterbalanced by their overall beneficial effects (nutrient mobilization), detritivores may not harm, but rather enable plants to respond to aboveground herbivore attacks in a more efficient way. Both more mechanistic and holistic approaches are needed to better understand the involvement of detritivores in plant-mediated above-belowground interactions and their potential for sustainable agriculture.

The root herbivore history of the soil affects the productivity of a grassland plant community and determines plant response to new root herbivore attack.

Insect root herbivores can alter plant community structure by affecting the competitive ability of single plants. However, their effects can be modified by the soil environment. Root herbivory itself may induce changes in the soil biota community, and it has recently been shown that these changes can affect plant growth in a subsequent season or plant generation. However, so far it is not known whether these root herbivore history effects (i) are detectable at the plant community level and/or (ii) also determine plant species and plant community responses to new root herbivore attack. The present greenhouse study determined root herbivore history effects of click beetle larvae (Elateridae, Coleoptera, genus Agriotes) in a model grassland plant community consisting of six common species (Achillea millefolium, Plantago lanceolata, Taraxacum officinale, Holcus lanatus, Poa pratensis, Trifolium repens). Root herbivore history effects were generated in a first phase of the experiment by growing the plant community in soil with or without Agriotes larvae, and investigated in a second phase by growing it again in the soils that were either Agriotes trained or not. The root herbivore history of the soil affected plant community productivity (but not composition), with communities growing in root herbivore trained soil producing more biomass than those growing in untrained soil. Additionally, it influenced the response of certain plant species to new root herbivore attack. Effects may partly be explained by herbivore-induced shifts in the community of arbuscular mycorrhizal fungi. The root herbivore history of the soil proved to be a stronger driver of plant growth on the community level than an actual root herbivore attack which did not affect plant community parameters. History effects have to be taken into account when predicting the impact of root herbivores on grasslands.

Effect of arbuscular mycorrhizal fungi (Glomus intraradices) on the oviposition of rice water weevil (Lissorhoptrus oryzophilus).

Root-feeding insects are important drivers in ecosystems, and links between aboveground oviposition preference and belowground larval performance have been suggested. The root-colonizing arbuscular mycorrhizal fungi (AMF) play a central role in plant nutrition and are known to change host quality for root-feeding insects. However, it is not known if and how AMF affect the aboveground oviposition of insects whose offspring feed on roots. According to the preference-performance hypothesis, insect herbivores oviposit on plants that will maximize offspring performance. In a greenhouse experiment with rice (Oryza sativa), we investigated the effects of AMF (Glomus intraradices) on aboveground oviposition of rice water weevil (Lissorhoptrus oryzophilus), the larvae of which feed belowground on the roots. Oviposition (i.e., the numbers of eggs laid by weevil females in leaf sheaths) was enhanced when the plants were colonized by AMF. However, the leaf area consumed by adult weevils was not affected. Although AMF reduced plant biomass, it increased nitrogen (N) and phosphorus concentrations in leaves and N in roots. The results suggest that rice water weevil females are able to discriminate plants for oviposition depending on their mycorrhizal status. The discrimination is probably related to AMF-mediated changes in plant quality, i.e., the females choose to oviposit more on plants with higher nutrient concentrations to potentially optimize offspring performance. AMF-mediated change in plant host choice for chewing insect oviposition is a novel aspect of below- and aboveground interactions.

Intraspecific variation in plant defense alters effects of root herbivores on leaf chemistry and aboveground herbivore damage.

Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether root-feeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the "high-IG line" contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the "low-IG line," whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of "low-IG line" plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of "high-IG line" plants decreased. In contrast, glucose concentrations in roots of "low-IG" plants decreased, while they increased in "high-IG" plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced "low-IG" plants and lower in wireworm-induced compared to noninduced "high-IG" plants, despite induction of catalpol in leaves of the "low-IG" plants and reduction in "high-IG" plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.

Earthworms and litter distribution affect plant-defensive chemistry.

Studies on plant-defensive chemistry have mainly focused on plants in direct interaction with aboveground and occasionally belowground herbivores and pathogens. Here we investigate whether decomposers and the spatial distribution of organic residues in soil affect plant-defensive chemistry. Litter concentrated in a patch (vs. homogeneously mixed into the soil) led to an increase in the aucubin content in shoots of Plantago lanceolata. Earthworms increased total phytosterol content of shoots, but only when the litter was mixed homogeneously into the soil. The phytosterol content increased and aphid reproduction decreased with increasing N concentration of the shoots. This study documents for the first time that earthworms and the spatial distribution of litter may change plant-defensive chemistry against herbivores.