Induced resistance to herbivory and the intelligent plant.

Plant induced responses to environmental stressors are increasingly studied in a behavioral ecology context. This is particularly true for plant induced responses to herbivory that mediate direct and indirect defenses, and tolerance. These seemingly adaptive alterations of plant defense phenotypes in the context of other environmental conditions have led to the discussion of such responses as intelligent behavior. Here we consider the concept of plant intelligence and some of its predictions for chemical information transfer in plant interaction with other organisms. Within this framework, the flow, perception, integration, and storage of environmental information are considered tunable dials that allow plants to respond adaptively to attacking herbivores while integrating past experiences and environmental cues that are predictive of future conditions. The predictive value of environmental information and the costs of acting on false information are important drivers of the evolution of plant responses to herbivory. We identify integrative priming of defense responses as a mechanism that allows plants to mitigate potential costs associated with acting on false information. The priming mechanisms provide short- and long-term memory that facilitates the integration of environmental cues without imposing significant costs. Finally, we discuss the ecological and evolutionary prediction of the plant intelligence hypothesis.

Associational Effects of Desmodium Intercropping on Maize Resistance and Secondary Metabolism.

Intercropping is drawing increasing attention as a strategy to increase crop yields and manage pest pressure, however the mechanisms of associational resistance in diversified cropping systems remain controversial. We conducted a controlled experiment to assess the impact of co-planting with silverleaf Desmodium (Desmodium uncinatum) on maize secondary metabolism and resistance to herbivory by the spotted stemborer (Chilo partellus). Maize plants were grown either in the same pot with a Desmodium plant or adjacent to it in a separate pot. Our findings indicate that co-planting with Desmodium influences maize secondary metabolism and herbivore resistance through both above and below-ground mechanisms. Maize growing in the same pot with a Desmodium neighbor was less attractive for oviposition by spotted stemborer adults. However, maize exposed only to above-ground Desmodium cues generally showed increased susceptibility to spotted stemborer herbivory (through both increased oviposition and larval consumption). VOC emissions and tissue secondary metabolite titers were also altered in maize plants exposed to Desmodium cues, with stronger effects being observed when maize and Desmodium shared the same pot. Specifically, benzoxazinoids were strongly suppressed in maize roots by direct contact with a Desmodium neighbor while headspace emissions of short-chain aldehydes and alkylbenzenes were increased. These results imply that direct root contact or soil-borne cues play an important role in mediating associational effects on plant resistance in this system.

Volatile-mediated plant-plant communication and higher-level ecological dynamics.

Volatile organic compounds (VOCs) in general and herbivory-induced plant volatiles (HIPVs) in particular are increasingly understood as major mediators of information transfer between plant tissues. Recent findings have moved the field of plant communication closer to a detailed understanding of how plants emit and perceive VOCs and seem to converge on a model that juxtaposes perception and emission mechanisms. These new mechanistic insights help to explain how plants can integrate different types of information and how environmental noise can affect the transmission of information. At the same time, ever-new functions of VOC-mediated plant-plant interactions are being revealed. Chemical information transfer between plants is now known to fundamentally affect plant organismal interactions and, additionally, population, community, and ecosystem dynamics. One of the most exciting new developments places plant-plant interactions along a behavioral continuum with an eavesdropping strategy at one end and mutually beneficial information-sharing among plants within a population at the other. Most importantly and based on recent findings as well as theoretical models, plant populations can be predicted to evolve different communication strategies depending on their interaction environment. We use recent studies from ecological model systems to illustrate this context dependency of plant communication. Moreover, we review recent key findings about the mechanisms and functions of HIPV-mediated information transfer and suggest conceptual links, such as to information theory and behavioral game theory, as valuable tools for a deeper understanding of how plant-plant communication affects ecological and evolutionary dynamics.

Herbivory selects for tolerance and constitutive defence across stages of community succession.

Plants defend themselves from herbivory by either reducing damage (resistance) or minimizing its negative fitness effects with compensatory growth (tolerance). Herbivore pressure can fluctuate from year to year in an early secondary successional community, which can create temporal variation in selection for defence traits. We manipulated insect herbivory and successional age of the community as agents of natural selection in replicated common gardens with the perennial herb Solidago altissima. In these genotypic selection experiments, herbivory consistently selected for better defended plants in both successional communities. Herbivore suppression increased plant survival and the probability of flowering only in mid-succession. Despite these substantial differences in the effects of herbivory between early and mid-succession, the selection on defence traits did not change. Succession affected selection only on aboveground biomass, with positive selection in early but not mid-succession, suggesting an important role of competition in the selective environment. These results demonstrate that changes in the community that affect key life-history traits in an individual species can occur over very short timescales in a dynamic secondary successional environment. The resulting community context-driven variation in natural selection may be an important, yet overlooked, contributor to adaptive mosaics across populations.

Defensive functions and potential ecological conflicts of floral stickiness.

Stickiness of vegetative tissues has evolved multiple times in different plant families but is rare and understudied in flowers. While stickiness in general is thought to function primarily as a defense against herbivores, it may compromise mutualistic interactions (such as those with pollinators) in reproductive tissues. Here, we test the hypothesis that stickiness on flower petals of the High-Andean plant, Bejaria resinosa (Ericaceae), functions as a defense against florivores. We address ecological consequences and discuss potential trade-offs associated with a repellant trait expressed in flowers that mediate mutualistic interactions. In surveys and manipulative experiments, we assess florivory and resulting fitness effects on plants with sticky and non-sticky flowers in different native populations of B. resinosa in Colombia. In addition, we analyze the volatile and non-volatile components in sticky and non-sticky flower morphs to understand the chemical information context within which stickiness is expressed. We demonstrate that fruit set is strongly affected by floral stickiness but also varies with population. While identifying floral stickiness as a major defensive function, our data also suggest that the context-dependency of chemical defense functionality likely arises from differential availability of primary pollinators and potential trade-offs between chemical defense with different modes of action.

Metabolic Integration of Spectral and Chemical Cues Mediating Plant Responses to Competitors and Herbivores.

Light quality and chemicals in a plant's environment can provide crucial information about the presence and nature of antagonists, such as competitors and herbivores. Here, we evaluate the roles of three sources of information-shifts in the red:far red (R:FR) ratio of light reflected off of potentially competing neighbors, induced metabolic changes to damage by insect herbivores, and induced changes to volatile organic compounds emitted from herbivore-damaged neighboring plants-to affect metabolic responses in the tall goldenrod, Solidago altissima. We address the hypothesis that plants integrate the information available about competitors and herbivory to optimize metabolic responses to interacting stressors by exposing plants to the different types of environmental information in isolation and combination. We found strong interactions between the exposure to decreased R:FR light ratios and damage on the induction of secondary metabolites (volatile and non-volatile) in plants. Similarly, the perception of VOCs emitted from neighboring plants was altered by the simultaneous exposure to spectral cues from neighbors. These results suggest that plants integrate spectral and chemical environmental cues to change the production and perception of volatile and non-volatile compounds and highlight the role of plant context-dependent metabolic responses in mediating population and community dynamics.

Interaction diversity explains the maintenance of phytochemical diversity.

The production of complex mixtures of secondary metabolites is a ubiquitous feature of plants. Several evolutionary hypotheses seek to explain how phytochemical diversity is maintained, including the synergy hypothesis, the interaction diversity hypothesis, and the screening hypothesis. We experimentally tested a set of predictions derived from these hypotheses by manipulating the richness and structural diversity of phenolic metabolites in the diets of eight plant consumers. Across 3940 total bioassays, there was clear support for the interaction diversity hypothesis over the synergy or screening hypotheses. The number of consumers affected by a particular phenolic composition increased with increasing richness and structural diversity of compounds. Furthermore, the bioactivity of phenolics was consumer-specific. All compounds tested reduced the performance of at least one consumer, but no compounds affected all consumers. These results show how phytochemical diversity may be maintained in nature by a complex selective landscape exerted by diverse communities of plant consumers.

Predictability of Biotic Stress Structures Plant Defence Evolution.

To achieve ecological and reproductive success, plants need to mitigate a multitude of stressors. The stressors encountered by plants are highly dynamic but typically vary predictably due to seasonality or correlations among stressors. As plants face physiological and ecological constraints in responses to stress, it can be beneficial for plants to evolve the ability to incorporate predictable patterns of stress in their life histories. Here, we discuss how plants predict adverse conditions, which plant strategies integrate predictability of biotic stress, and how such strategies can evolve. We propose that plants commonly optimise responses to correlated sequences or combinations of herbivores and pathogens, and that the predictability of these patterns is a key factor governing plant strategies in dynamic environments.

Soil Microbiomes From Fallow Fields Have Species-Specific Effects on Crop Growth and Pest Resistance.

Communities of microorganisms in the soil can affect plants' growth and interactions with aboveground herbivores. Thus, there is growing interest in utilizing soil microbiomes to improve plant performance in agriculture (e.g., for pest control), but little is known about the phenotypic responses of various crop species to different microbiomes. In this study, we inoculated four crop species from different botanical families, maize (Zea mays, Poaceae), cucumber (Cucumis sativus, Cucurbitaceae), tomato (Solanum lycopersicum, Solanaceae), and lettuce (Lactuca sativa, Asteraceae), with diverse soil microbiomes originating from actively-managed agricultural fields or fallow fields under varying stages of succession (1, 3, and 16-years post-agriculture) sourced from a large-scale field experiment. We compared the crops' responses to these different microbiomes by assessing their growth and resistance to two generalist insect pests, cabbage looper (Trichoplusia ni) and fall armyworm (Spodoptera frugiperda). These different microbiomes affected both plant growth and resistance, but the effects were species-specific. For instance, lettuce produced the largest leaves when inoculated with a 3-year fallow microbiome, the microbiome in which cucumber performed worst. Plants were generally more resistant to T. ni when inoculated with the later succession microbiomes, particularly in contrast to those treated with agricultural microbiomes. However, for tomato plants, the opposite pattern was observed with regard to S. frugiperda resistance. Collectively, these results indicate that plant responses to microbiomes are species-specific and emphasize the need to characterize the responses of taxonomically diverse plant species to different microbiomes.

The ecological consequences of herbivore-induced plant responses on plant-pollinator interactions.

Plant induced responses to herbivory have long been found to function as plant direct and indirect defenses and to be major drivers of herbivore community and population dynamics. While induced defenses are generally understood as cost-saving strategies that allow plants to allocate valuable resources into defense expression, it recently became clear that, in particular, induced metabolic changes can come with significant ecological costs. In particular, interactions with mutualist pollinators can be significantly compromised by herbivore-induced changes in floral morphology and metabolism. We review recent findings on the evidence for ecological conflict between defending against herbivores and attracting pollinators while using similar modes of information transfer (e.g. visual, olfactory, tactile). Specifically, we discuss plant traits and mechanisms through which plants mediate interactions between antagonists and mutualist and present functional hypotheses for how plants can overcome the resulting conflicts.

Soil organic matter attenuates the efficacy of flavonoid-based plant-microbe communication.

Plant-microbe interactions are mediated by signaling compounds that control vital plant functions, such as nodulation, defense, and allelopathy. While interruption of signaling is typically attributed to biological processes, potential abiotic controls remain less studied. Here, we show that higher organic carbon (OC) contents in soils repress flavonoid signals by up to 70%. Furthermore, the magnitude of repression is differentially dependent on the chemical structure of the signaling molecule, the availability of metal ions, and the source of the plant-derived OC. Up to 63% of the signaling repression occurs between dissolved OC and flavonoids rather than through flavonoid sorption to particulate OC. In plant experiments, OC interrupts the signaling between a legume and a nitrogen-fixing microbial symbiont, resulting in a 75% decrease in nodule formation. Our results suggest that soil OC decreases the lifetime of flavonoids underlying plant-microbe interactions.

Pollen defenses negatively impact foraging and fitness in a generalist bee (Bombus impatiens: Apidae).

Plants may benefit from limiting the community of generalist floral visitors if the species that remain are more effective pollinators and less effective pollenivores. Plants can reduce access to pollen through altered floral cues or morphological structures, but can also reduce consumption through direct pollen defenses. We observed that Eucera (Peponapis) pruinosa, a specialist bee on Cucurbita plants, collected pure loads of pollen while generalist honey bees and bumble bees collected negligible amounts of cucurbit pollen, even though all groups of bees visited these flowers. Cucurbit flowers have no morphological adaptations to limit pollen collection by bees, thus we assessed their potential for physical, nutritional, and chemical pollen traits that might act as defenses to limit pollen loss to generalist pollinators. Bumble bee (Bombus impatiens) microcolonies experienced reduced pollen consumption, mortality, and reproduction as well as increased stress responses when exposed to nutritional and mechanical pollen defenses. These bees also experienced physiological effects of these defenses in the form of hindgut expansion and gut melanization. Chemical defenses alone increased the area of gut melanization in larger bees and induced possible compensatory feeding. Together, these results suggest that generalist bumble bees avoid collecting cucurbit pollen due to the physiological costs of physical and chemical pollen defenses.

Shifts in plant-microbe interactions over community succession and their effects on plant resistance to herbivores.

Soil microorganisms can influence the development of complex plant phenotypes, including resistance to herbivores. This microbiome-mediated plasticity may be particularly important for plant species that persist in environments with drastically changing herbivore pressure, for example over community succession. We established a 15-yr gradient of old-field succession to examine the herbivore resistance and rhizosphere microbial communities of Solidago altissima plants in a large-scale field experiment. To assess the functional effects of these successional microbial shifts, we inoculated S. altissima plants with microbiomes from the 2nd , 6th and 15th successional years in a glasshouse and compared their herbivore resistance. The resistance of S. altissima plants to herbivores changed over succession, with concomitant shifts in the rhizosphere microbiome. Late succession microbiomes conferred the strongest herbivore resistance to S. altissima plants in a glasshouse experiment, paralleling the low levels of herbivory observed in the oldest communities in the field. While many factors change over succession and may contribute to the shifts in rhizosphere communities and herbivore resistance we observed, our results indicated that soil microbial shifts alone can alter plants' interactions with herbivores. Our findings suggest that changes in soil microbial communities over succession can play an important role in enhancing plant resistance to herbivores.

Human-Mediated Land Use Change Drives Intraspecific Plant Trait Variation.

In the Anthropocene, more than three quarters of ice-free land has experienced some form of human-driven habitat modification, with agriculture dominating 40% of the Earth's surface. This land use change alters the quality, availability, and configuration of habitat resources, affecting the community composition of plants and insects, as well as their interactions with each other. Landscapes dominated by agriculture are known to support a lower abundance and diversity of pollinators and frequently larger populations of key herbivore pests. In turn, insect communities subsidized by agriculture may spill into remaining natural habitats with consequences for wild plants persisting in (semi) natural habitats. Adaptive responses by wild plants may allow them to persist in highly modified landscapes; yet how landscape-mediated variation in insect communities affects wild plant traits related to reproduction and defense remains largely unknown. We synthesize the evidence for plant trait changes across land use gradients and propose potential mechanisms by which landscape-mediated changes in insect communities may be driving these trait changes. Further, we present results from a common garden experiment on three wild Brassica species demonstrating variation in both defensive and reproductive traits along an agricultural land use gradient. Our framework illustrates the potential for plant adaptation under land use change and predicts how defense and reproduction trait expression may shift in low diversity landscapes. We highlight areas of future research into plant population and community effects of land use change.

Insect Herbivory Selects for Volatile-Mediated Plant-Plant Communication.

Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1-3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6-9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10-12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage. We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.

High levels of abiotic noise in volatile organic compounds released by a desert perennial: implications for the evolution and ecology of airborne chemical communication.

Plants release airborne volatile organic compounds (VOCs) in response to abiotic and biotic stimuli, including herbivory. These chemicals are used by insect parasitoids as sources of information that aid in finding hosts. It is unclear how biotic and abiotic factors interact to affect blend composition and the ability of insects to interpret signals. Here, we present a novel stimulus-space model, and use it to examine patterns of VOC emission. In field experiments, we manipulated herbivory levels and collected VOCs in a population of wild Datura wrightii, while simultaneously measuring key abiotic factors. We mirrored field experiments under controlled conditions in the lab, and used both sets of data to test predictions made by our proposed model. VOC blends were structured mainly by variation in abiotic factors, not herbivory. However, linear discriminant analysis showed that it is possible to distinguish different herbivory levels. We show that most compounds produced by D. wrightii are invariant, or respond solely to environmental variation or herbivory. Our results suggest that blend composition may be under selection for noise reduction, to maximize responses from potential receivers, and that abiotic variation can act as potentially strong sources of noise in chemical communication displays.

Phenolic root exudate and tissue compounds vary widely among temperate forest tree species and have contrasting effects on soil microbial respiration.

Root-soil interactions fundamentally affect the terrestrial carbon (C) cycle and thereby ecosystem feedbacks to climate change. This study addressed the question of whether the secondary metabolism of different temperate forest tree species can affect soil microbial respiration. We hypothesized that phenolics can both increase and decrease respiration depending on their function as food source, mobilizer of other soil resources, signaling compound, or toxin. We analyzed the phenolic compounds from root exudates and root tissue extracts of six tree species grown in a glasshouse using high-performance liquid chromatography. We then tested the effect of individual phenolic compounds, representing the major identified phenylpropanoid compound classes, on microbial respiration through a 5-d soil incubation. Phenolic root profiles were highly species-specific. Of the eight classes identified, flavonoids were the most abundant, with flavanols being the predominating sub-class. Phenolic effects on microbial respiration ranged from a 26% decrease to a 46% increase, with reduced respiration occurring in the presence of compounds possessing a catechol ring. Tree species variation in root phenolic composition influences the magnitude and direction of root effects on microbial respiration. Our data support the hypothesis that functional group rather than biosynthetic class determines the root phenolic effect on soil C cycling.