Evolutionary responses to environmental change: trophic interactions affect adaptation and persistence

According to recent reviews, the question of how trophic interactions may affect evolutionary responses to climate change remains unanswered. In this modelling study, we explore the evolutionary dynamics of thermal and plant–herbivore interaction traits in a warming environment. We find the herbivore usually reduces adaptation speed and persistence time of the plant by reducing biomass. However, if the plant interaction trait and thermal trait are correlated, herbivores can create different coevolutionary attractors. One attractor has a warmer plant thermal optimum, and the other a colder one compared with the environment. A warmer plant thermal strategy is given a head start under warming, the only case where herbivores can increase plant persistence under warming. Persistence time of the plant under warming is maximal at small or large thermal niche width. This study shows that considering trophic interactions is necessary and feasible for understanding how ecosystems respond to climate change.     

Herbivore regulation of plant abundance in aquatic ecosystems

Herbivory is a fundamental process that controls primary producer abundance and regulates energy and nutrient flows to higher trophic levels. Despite the recent proliferation of small‐scale studies on herbivore effects on aquatic plants, there remains limited understanding of the factors that control consumer regulation of vascular plants in aquatic ecosystems. Our current knowledge of the regulation of primary producers has hindered efforts to understand the structure and functioning of aquatic ecosystems, and to manage such ecosystems effectively. We conducted a global meta‐analysis of the outcomes of plant–herbivore interactions using a data set comprised of 326 values from 163 studies, in order to test two mechanistic hypotheses: first, that greater negative changes in plant abundance would be associated with higher herbivore biomass densities; second, that the magnitude of changes in plant abundance would vary with herbivore taxonomic identity. We found evidence that plant abundance declined with increased herbivore density, with plants eliminated at high densities. Significant between‐taxa differences in impact were detected, with insects associated with smaller reductions in plant abundance than all other taxa. Similarly, birds caused smaller reductions in plant abundance than echinoderms, fish, or molluscs. Furthermore, larger reductions in plant abundance were detected for fish relative to crustaceans. We found a positive relationship between herbivore species richness and change in plant abundance, with the strongest reductions in plant abundance reported for low herbivore species richness, suggesting that greater herbivore diversity may protect against large reductions in plant abundance. Finally, we found that herbivore–plant nativeness was a key factor affecting the magnitude of herbivore impacts on plant abundance across a wide range of species assemblages. Assemblages comprised of invasive herbivores and native plant assemblages were associated with greater reductions in plant abundance compared with invasive herbivores and invasive plants, native herbivores and invasive plants, native herbivores and mixed‐nativeness plants, and native herbivores and native plants. By contrast, assemblages comprised of native herbivores and invasive plants were associated with lower reductions in plant abundance compared with both mixed‐nativeness herbivores and native plants, and native herbivores and native plants. However, the effects of herbivore–plant nativeness on changes in plant abundance were reduced at high herbivore densities. Our mean reductions in aquatic plant abundance are greater than those reported in the literature for terrestrial plants, but lower than aquatic algae. Our findings highlight the need for a substantial shift in how biologists incorporate plant–herbivore interactions into theories of aquatic ecosystem structure and functioning. Currently, the failure to incorporate top‐down effects continues to hinder our capacity to understand and manage the ecological dynamics of habitats that contain aquatic plants.     

Not all droughts are created equal? The effects of stress severity on insect herbivore abundance

Predicting interactions between drought and plant–insect interactions has been a challenge. Currently, we are unable to accurately predict herbivore abundance on stressed plants despite over 500 publications and half a dozen formal hypotheses. With drought predicted to increase in severity with climate change, determining herbivore abundance on stressed plants is critical for continued agricultural and natural system management. During drought, plants increase concentrations of nutrients and also suffer from water loss. Many empirical studies test drought on plants using severe continuous stress, but studies suggest drought may benefit herbivores when it is intermittent (pulsed). In our study, we tested intermittent and severe stress on herbivore and arthropod abundance in a cotton agro-ecosystem. Our goal was to determine how these types of drought influence herbivore abundance on stressed plants and the relationship between herbivore abundance and stress-related nutrients. We found that intermittent and severe water-deficit stress had different effects on insect herbivores, signifying that drought severity influences herbivore abundance. Piercing–sucking herbivores such as thrips, stink bugs, and leafhoppers were more abundant on intermittently stressed plants than on severely stressed plants. Drought did not significantly affect chewing herbivores, and their abundance was inconsistent on stressed and well-watered plants. Furthermore, nutrient concentrations were similar between stressed and unstressed plants, but herbivore abundance was greater on intermittently stressed plants, suggesting that other physiological characteristics of stressed plants and herbivore feeding ecology must be considered. Our study suggests that the drought severity must be considered when predicting herbivore abundance on stressed plants.     

Drought impacts on above–belowground interactions: Do effects differ between annual and perennial host species?

Root herbivores can have a positive or negative effect on the abundance and/or performance of foliar phytophages. In addition, abiotic factors such as drought can either strengthen or weaken this effect, depending on the system under investigation. One explanation for these varying responses lies in differences in the physiological response of host plants to drought and root herbivores. Here, the impacts of root phytophages on a leaf-mining species feeding on annual and perennial plant species (four Sonchus species) were compared. The responses of plants and leaf-miners to drought and root herbivore treatments were not related to whether the host plant was an annual or perennial. However, where root feeders did affect foliar phytophage performance, this occurred only under a drought treatment, demonstrating the potential for climate change to alter the outcome of plant-mediated interactions.     

Testing the Paradox of Enrichment along a Land Use Gradient in a Multitrophic Aboveground and Belowground Community

In the light of ongoing land use changes, it is important to understand how multitrophic communities perform at different land use intensities. The paradox of enrichment predicts that fertilization leads to destabilization and extinction of predator-prey systems. We tested this prediction for a land use intensity gradient from natural to highly fertilized agricultural ecosystems. We included multiple aboveground and belowground trophic levels and land use-dependent searching efficiencies of insects. To overcome logistic constraints of field experiments, we used a successfully validated simulation model to investigate plant responses to removal of herbivores and their enemies. Consistent with our predictions, instability measured by herbivore-induced plant mortality increased with increasing land use intensity. Simultaneously, the balance between herbivores and natural enemies turned increasingly towards herbivore dominance and natural enemy failure. Under natural conditions, there were more frequently significant effects of belowground herbivores and their natural enemies on plant performance, whereas there were more aboveground effects in agroecosystems. This result was partly due to the “boom-bust” behavior of the shoot herbivore population. Plant responses to herbivore or natural enemy removal were much more abrupt than the imposed smooth land use intensity gradient. This may be due to the presence of multiple trophic levels aboveground and belowground. Our model suggests that destabilization and extinction are more likely to occur in agroecosystems than in natural communities, but the shape of the relationship is nonlinear under the influence of multiple trophic interactions.     

Integration of ecosystem engineering and trophic effects of herbivores

Herbivores affect vegetation in a variety of ways, involving both trophic and ecosystem engineering interactions, but the study of these different interaction types has rarely been integrated. The aim of this study was to investigate both the trophic and engineering effects of herbivores on plant communities in the Negev desert, Israel, and to promote an integrative approach to the study of herbivore effects in ecosystems. First, we summarise previous studies of the Indian crested porcupine (Hystrix indica), which show that in digging for food, porcupines excavate soil pits, which accumulate resources and seeds resulting in marked changes in plant species richness, density and biomass. By contrast, their trophic effect, via consumption of bulbs, has little impact on populations of perennial plants. Second, we present an empirical study of the trophic and ecosystem engineering effects of harvester ants (Messor spp.). An exclusion experiment, using barriers to restrict ant access, failed to reveal any significant effect of seed collection by harvester ants on plant species incidence (proportional occurrence in samples) or abundance (number of individuals). However, we show that vegetation on nest mounds of M. ebeninus differs in plant density, species richness and biomass from that on undisturbed soil. An analysis of incidence and abundance responses of individual plant species suggests that the observed differences in vegetation resulted from multiple interacting mechanisms.
The case studies highlight that many interactions between herbivores and plant communities can occur simultaneously, and that ecosystem engineering and trophic processes can be closely associated, resulting from single actions of herbivores. We propose a conceptual framework that classifies the range of possible trophic and engineering interactions between herbivores and plant communities with respect to the level of association between trophic and engineering effects. The framework is presented as an aid to the design and interpretation of studies of interactions between herbivores and plant communities, and promotes integrative research into the roles of herbivores in ecosystems.     

Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores

Drought events are predicted to increase due to climate change, yet consequences for plant–insect interactions are only partially understood. Drought‐mediated interactions between herbivores and their host plants are affected by a combination of factors, including characteristics of the affected plant, its associated herbivore and of the prevailing drought. Studying the effect of these factors in combination may provide important insight into plant and herbivore responses to drought. We studied drought effects on plant resistance to two leaf‐chewing herbivores by considering differing growth conditions, plant chemistry and insect responses in concert. We exposed Alliaria petiolata plants from several wild populations to different intensities of intermittent drought stress and quantified drought‐mediated changes in plant chemistry. Simultaneously, we assessed behavior (feeding preference) and performance of two lepidopteran herbivores: Pieris brassicae, a specialist, and Spodoptera littoralis, a generalist. Drought led to lowest concentrations of secondary defense compounds in severely stressed plants, without affecting total nitrogen content. Additionally, drought evoked opposite patterns in feeding preferences (plant palatability) between the herbivore species. Pieris brassicae consumed most of well‐watered plants, while S. littoralis preferred severely drought‐stressed plants. Hence, feeding preferences of S. littoralis reflected changes in plant secondary chemistry. Contrary to their feeding preference, P. brassicae performed better on drought‐stressed than on well‐watered plants, with faster development and higher attained pupal mass (plant suitability). Spodoptera littoralis showed retarded development in all treatments. In conclusion, drought caused plant secondary defense compounds to decrease consistently across all studied plant populations, which evoked contrasting feeding preferences of two herbivore species of the same feeding guild. These results suggest herbivore specificity as a possible explanation for herbivore responses to drought and emphasize the importance of herbivore characteristics such as feeding specialization in understanding and predicting consequences of future drought events.     

Potential impacts of climate change on patterns of insect herbivory on understorey plant species: A transplant experiment

Species‐specific responses to climate change will lead to changes in species interactions across multiple trophic levels. Interactions between plants and their insect herbivores, in particular, may become increasingly disrupted if mobile herbivores respond more rapidly to climatic change than their associated host plants. We present a multispecies transplant experiment aimed at assessing potential climatic impacts on patterns of leaf herbivory. Four shrubby understorey plant species were transplanted outside their native range into a climate 2.5°C warmer in annual mean temperature. After 12 months, we assessed the types and amount of herbivore leaf damage, compared with plants transplanted to a control site within their native range. The overall amount of foliage loss to herbivores ranged from approximately 3–10% across species and sites, a range consistent with most estimates of leaf loss in other studies. The most common types of leaf damage were sucking and chewing and this pattern was consistent for all four plant species at all sites. There were no significant differences in levels and patterns of herbivory between control and warm sites for three out of four plant species. This suggests that with moderate climate warming, most herbivory will continue to be dominated by chewers and suckers, and that the overall level of foliage loss will be similar to that experienced presently.     

Drought and Root Herbivory Interact to Alter the Response of Above-Ground Parasitoids to Aphid Infested Plants and Associated Plant Volatile Signals

Multitrophic interactions are likely to be altered by climate change but there is little empirical evidence relating the responses of herbivores and parasitoids to abiotic factors. Here we investigated the effects of drought on an above/below-ground system comprising a generalist and a specialist aphid species (foliar herbivores), their parasitoids, and a dipteran species (root herbivore).We tested the hypotheses that: (1) high levels of drought stress and below-ground herbivory interact to reduce the performance of parasitoids developing in aphids; (2) drought stress and root herbivory change the profile of volatile organic chemicals (VOCs) emitted by the host plant; (3) parasitoids avoid ovipositing in aphids feeding on plants under drought stress and root herbivory. We examined the effect of drought, with and without root herbivory, on the olfactory response of parasitoids (preference), plant volatile emissions, parasitism success (performance), and the effect of drought on root herbivory. Under drought, percentage parasitism of aphids was reduced by about 40–55% compared with well watered plants. There was a significant interaction between drought and root herbivory on the efficacy of the two parasitoid species, drought stress partially reversing the negative effect of root herbivory on percent parasitism. In the absence of drought, root herbivory significantly reduced the performance (e.g. fecundity) of both parasitoid species developing in foliar herbivores. Plant emissions of VOCs were reduced by drought and root herbivores, and in olfactometer experiments parasitoids preferred the odour from well-watered plants compared with other treatments. The present work demonstrates that drought stress can change the outcome of interactions between herbivores feeding above- and below-ground and their parasitoids, mediated by changes in the chemical signals from plants to parasitoids. This provides a new insight into how the structure of terrestrial communities may be affected by drought.     

Preference and Performance in Plant–Herbivore Interactions across Latitude–A Study in U.S. Atlantic Salt Marshes

High-latitude plants are often more palatable to herbivores than low-latitude conspecifics. Does increased plant palatability lead to better herbivore performance? Our field and laboratory work investigated (A) whether high-latitude plants have traits indicating that they should be higher-quality foods for herbivores; (B) whether geographic differences in plant quality are more important than local adaptation of herbivores. We studied 3 plant species and 6 invertebrate herbivores in U.S. Atlantic Coast. Past studies had shown high-latitude individuals of these plants are more palatable than low-latitude conspecifics. We documented plant traits and herbivore performance (body size) in the field across latitude. We collected individuals from different latitudes for factorial (plant region x herbivore region) laboratory experiments, examining how herbivore performance was affected by plant region, herbivore region, and their interaction (i.e., local adaptation). Field surveys suggested high-latitude plants were likely of higher quality to herbivores. Leaf nitrogen content in all plant species increased toward high latitudes, consistent with lower leaf C/N and higher leaf chlorophyll content at high latitudes. Furthermore, leaf toughness decreased toward higher latitudes in 1 species. The body size of 4 herbivore species increased with latitude, consistent with high-latitude leaves being of higher quality, while 2 grasshopper species showed the opposite pattern, likely due to life-history constraints. In the laboratory, high-latitude plants supported better performance in 4 herbivore species (marginal in the 5th). The geographic region where herbivores were collected affected herbivore performance in all 6 species; however, the pattern was mixed, indicating a lack of local adaptation by herbivores to plants from their own geographic region. Our results suggest that more-palatable plants at high latitudes support better herbivore growth. Given that geographic origin of either plants or herbivores can affect herbivore performance, the nature of plant-herbivore interactions is likely to change if climate change “reshuffles” plant and herbivore populations across latitude.     

Trophic and non‐trophic interactions influence the mechanisms underlying biodiversity–ecosystem functioning relationships under different abiotic conditions

Plant diversity effects on ecosystem functioning usually have been studied from a plant perspective. However, the mechanisms underlying biodiversity–ecosystem functioning relationships may also depend on positive or negative interactions between plants and other biotic and abiotic factors, which remain poorly understood. Here we assessed whether plant–herbivore and/or plant–detritivore interactions modify the biodiversity–ecosystem functioning relationship and the mechanisms underlying biodiversity effects, including complementarity and selection effects, biomass allocation, vertical distribution of roots, and plant survival using a microcosm experiment. We also evaluated to what extent trophic and non‐trophic interactions are affected by abiotic conditions by studying drought effects. Our results show that biotic and abiotic conditions influence the shape of the biodiversity–ecosystem function relationship, varying from hump‐shaped to linear. For instance, total biomass increased linearly with plant richness in the presence of detritivores, but not in the absence of detritivores. Moreover, detritivore effects on belowground plant productivity were highly context dependent, varying in the presence of herbivores. Plant interactions with soil biota, especially with herbivores, influenced the mechanisms underlying diversity effects. Herbivores increased plant complementarity and modified biomass allocation and vertical distribution of roots. Furthermore, biotic–abiotic interactions influenced plant productivity differently across plant functional groups. Our findings emphasize the importance of complex biotic interactions underlying biodiversity effects, and that these biotic interactions may change with abiotic conditions. Despite minor changes in productivity in the short‐term, soil biota‐induced changes in plant–plant interactions and plant survival are likely to have significant long‐term consequences for ecosystem functioning. Considering the context‐dependency of multichannel interactions may contribute to reconciling differences among observed patterns in biodiversity studies. Further, abiotic conditions modified the effects of biotic interactions, suggesting that changes in environmental conditions may not only affect ecosystems directly, but also change the biotic composition of and dynamics within ecosystems.     

Responses of plants and invertebrate trophic groups to contrasting herbicide regimes in the Farm Scale Evaluations of genetically modified herbicide-tolerant crops

Effects of genetically modified herbicide-tolerant (GMHT) and conventional crop management on invertebrate trophic groups (herbivores, detritivores, pollinators, predators and parasitoids) were compared in beet, maize and spring oilseed rape sites throughout the UK. These trophic groups were influenced by season, crop species and GMHT management. Many groups increased twofold to fivefold in abundance between early and late summer, and differed up to 10-fold between crop species. GMHT management superimposed relatively small (less than twofold), but consistent, shifts in plant and insect abundance, the extent and direction of these effects being dependent on the relative efficacies of comparable conventional herbicide regimes. In general, the biomass of weeds was reduced under GMHT management in beet and spring oilseed rape and increased in maize compared with conventional treatments. This change in resource availability had knock-on effects on higher trophic levels except in spring oilseed rape where herbivore resource was greatest. Herbivores, pollinators and natural enemies changed in abundance in the same directions as their resources, and detritivores increased in abundance under GMHT management across all crops. The result of the later herbicide application in GMHT treatments was a shift in resource from the herbivore food web to the detritivore food web. The Farm Scale Evaluations have demonstrated over 3 years and throughout the UK that herbivores, detritivores and many of their predators and parasitoids in arable systems are sensitive to the changes in weed communities that result from the introduction of new herbicide regimes.     

Parasitic wasp‐associated symbiont affects plant‐mediated species interactions between herbivores

Microbial mutualistic symbiosis is increasingly recognised as a hidden driving force in the ecology of plant–insect interactions. Although plant‐associated and herbivore‐associated symbionts clearly affect interactions between plants and herbivores, the effects of symbionts associated with higher trophic levels has been largely overlooked. At the third‐trophic level, parasitic wasps are a common group of insects that can inject symbiotic viruses (polydnaviruses) and venom into their herbivorous hosts to support parasitoid offspring development. Here, we show that such third‐trophic level symbionts act in combination with venom to affect plant‐mediated interactions by reducing colonisation of subsequent herbivore species. This ecological effect correlated with changes induced by polydnaviruses and venom in caterpillar salivary glands and in plant defence responses to herbivory. Because thousands of parasitoid species are associated with mutualistic symbiotic viruses in an intimate, specific relationship, our findings may represent a novel and widespread ecological phenomenon in plant–insect interactions.     

Water stress in grasslands: dynamic responses of plants and insect herbivores

Global climate change is altering precipitation patterns. The effect of water stress on plant–herbivore interactions is poorly understood even though this is a primary ecological interaction that will be altered by climate change. This is especially true for grasslands where water is often limiting. In this study we manipulated water inputs in open grassland plots (1 m²) during a severe drought and assessed plant and insect herbivore responses. There were two watering treatments: ambient and supplemented. Supplemented plots received water weekly in amounts that mimicked average seasonal rainfall. For plants, we were interested in how water input affected protein and digestible carbohydrate content; previous studies predicted water stress would increase the concentration of these two nutrients. Grasshoppers are the dominant insect herbivores in grasslands and we assessed their responses to water inputs by measuring abundance and diversity. Previous studies suggested grasshoppers would prefer water‐stressed plots. Protein and carbohydrate content in bulk grass and forb samples, plus plant biomass and diversity, were measured monthly (May–August). Immediately prior to harvesting plant tissue, we counted and identified individual grasshoppers in each plot. Grass biomass was reduced with water stress, but macronutrient content and species diversity were unaffected. After three months water‐stressed forbs were less protein biased, and diverse, relative to watered forbs; forb biomass was indistinguishable between treatments. Grasshopper abundance and diversity were lower in water‐stressed plots as the season progressed. However, grasshopper‐feeding biology mattered: densities of mixed‐feeders and grass‐feeders, but not forb‐specialists, decreased over time in water‐stressed plots, but not in water supplemented plots. Our results demonstrate the importance of focusing on plant and insect herbivore functional groups and provide valuable new data that can be incorporated into models to explore the effects of global climate change in greater detail.     

Are Tree Species Diversity and Genotypic Diversity Effects on Insect Herbivores Mediated by Ants?

Plant diversity can influence predators and omnivores and such effects may in turn influence herbivores and plants. However, evidence for these ecological feedbacks is rare. We evaluated if the effects of tree species (SD) and genotypic diversity (GD) on the abundance of different guilds of insect herbivores associated with big-leaf mahogany (Swietenia macrophylla) were contingent upon the protective effects of ants tending extra-floral nectaries of this species. This study was conducted within a larger experiment consisting of mahogany monocultures and species polycultures of four species and –within each of these two plot types– mahogany was represented by either one or four maternal families. We selected 24 plots spanning these treatment combinations, 10 mahogany plants/plot, and within each plot experimentally reduced ant abundance on half of the selected plants, and surveyed ant and herbivore abundance. There were positive effects of SD on generalist leaf-chewers and sap-feeders, but for the latter group this effect depended on the ant reduction treatment: SD positively influenced sap-feeders under ambient ant abundance but had no effect when ant abundance was reduced; at the same time, ants had negative effects on sap feeders in monoculture but no effect in polyculture. In contrast, SD did not influence specialist stem-borers or leaf-miners and this effect was not contingent upon ant reduction. Finally, GD did not influence any of the herbivore guilds studied, and such effects did not depend on the ant treatment. Overall, we show that tree species diversity influenced interactions between a focal plant species (mahogany) and ants, and that such effects in turn mediated plant diversity effects on some (sap-feeders) but not all the herbivores guilds studied. Our results suggest that the observed patterns are dependent on the combined effects of herbivore identity, diet breadth, and the source of plant diversity.     

Drought alters interactions between root and foliar herbivores

Drought can alter plant quality and the strength of trophic interactions between herbivore groups, and is likely to increase in occurrence and severity under climate change. We hypothesized that changes in plant chemistry due to root herbivory and drought stress would affect the performance of a generalist and a specialist aphid species feeding on a Brassica plant. High drought stress increased the negative effect of root herbivory on the performance of both aphid species (30 % decrease in fecundity and 15 % reduction in intrinsic rate of increase). Aphid performance was greatest at moderate drought stress, though the two species differed in which treatment combination maximized performance. Nitrogen concentration was greatest in high and moderately drought-stressed plants without root herbivores and moderately drought-stressed plants under low root herbivore density, and correlated positively with aphid fecundity for both species. Glucosinolate concentrations increased 62 % under combined drought stress and root herbivory, and were positively correlated with extended aphid development time. Root herbivory did not influence relative water content and foliar biomass under normal water regimes but they decreased 24 and 63 %, respectively, under high drought stress. This study shows that drought can alter the strength of interactions between foliar and root herbivores, and that plant chemistry is key in mediating such interactions. The two aphid species responded in a broadly similar way to root herbivore and drought-stress treatments, which suggests that generalized predictions of the effects of abiotic factors on interactions between above- and below-ground species may be possible.     

Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism

The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the field of ecology of multitrophic interactions. Scarcely studied aspects include the effects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the effects of constitutive and herbivore-induced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as first instars were low and did not differ among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed differences in encapsulation rates between plant populations could not be explained exclusively by differences in host growth on the different Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the first study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, affecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of fitness costs and benefits of herbivore diet on the third trophic level.     

Plant defence as a complex and changing phenotype throughout ontogeny

Background and Aims Ontogenetic changes in anti-herbivore defences are common and result from variation in resource availability and herbivore damage throughout plant development. However, little is known about the simultaneous changes of multiple defences across the entire development of plants, and how such changes affect plant damage in the field. The aim of this study was to assess if changes in the major types of plant resistance and tolerance can explain natural herbivore damage throughout plant ontogeny.Methods An assessment was made of how six defensive traits, including physical, chemical and biotic resistance, simultaneously change across the major transitions of plant development, from seedlings to reproductive stages of Turnera velutina growing in the greenhouse. In addition, an experiment was performed to assess how plant tolerance to artificial damage to leaves changed throughout ontogeny. Finally, leaf damage by herbivores was evaluated in a natural population.Key Results The observed ontogenetic trajectories of all defences were significantly different, sometimes showing opposite directions of change. Whereas trichome density, leaf toughness, extrafloral nectary abundance and nectar production increased, hydrogen cyanide and compensatory responses decreased throughout plant development, from seedlings to reproductive plants. Only water content was higher at the intermediate juvenile ontogenetic stages. Surveys in a natural population over 3 years showed that herbivores consumed more tissue from juvenile plants than from younger seedlings or older reproductive plants. This is consistent with the fact that juvenile plants were the least defended stage.Conclusions The results suggest that defensive trajectories are a mixed result of predictions by the Optimal Defence Theory and the Growth–Differentiation Balance Hypothesis. The study emphasizes the importance of incorporating multiple defences and plant ontogeny into further studies for a more comprehensive understanding of plant defence evolution.     

Responses of belowground communities to large aboveground herbivores: Meta‐analysis reveals biome‐dependent patterns and critical research gaps

The importance of herbivore–plant and soil biota–plant interactions in terrestrial ecosystems is amply recognized, but the effects of aboveground herbivores on soil biota remain challenging to predict. To find global patterns in belowground responses to vertebrate herbivores, we performed a meta‐analysis of studies that had measured abundance or activity of soil organisms inside and outside field exclosures (areas that excluded herbivores). Responses were often controlled by climate, ecosystem type, and dominant herbivore identity. Soil microfauna and especially root‐feeding nematodes were negatively affected by herbivores in subarctic sites. In arid ecosystems, herbivore presence tended to reduce microbial biomass and nitrogen mineralization. Herbivores decreased soil respiration in subarctic ecosystems and increased it in temperate ecosystems, but had no net effect on microbial biomass or nitrogen mineralization in those ecosystems. Responses of soil fauna, microbial biomass, and nitrogen mineralization shifted from neutral to negative with increasing herbivore body size. Responses of animal decomposers tended to switch from negative to positive with increasing precipitation, but also differed among taxa, for instance Oribatida responded negatively to herbivores, whereas Collembola did not. Our findings imply that losses and gains of aboveground herbivores will interact with climate and land use changes, inducing functional shifts in soil communities. To conceptualize the mechanisms behind our findings and link them with previous theoretical frameworks, we propose two complementary approaches to predict soil biological responses to vertebrate herbivores, one focused on an herbivore body size gradient, and the other on a climate severity gradient. Major research gaps were revealed, with tropical biomes, protists, and soil macrofauna being especially overlooked.     

Plant genotypic diversity reduces the rate of consumer resource utilization

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore—the Japanese beetle (Popillia japonica)—increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose (Oenothera biennis). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.