Aboveground Herbivores Research Articles

Dual nematode infection in Brassica nigra affects shoot metabolome and aphid survival in distinct contrast to single-species infection.

Previous studies showed that aphid performance was compromised on Brassica nigra infected by root-lesion nematodes (Pratylenchus penetrans, Pp), but less, or positively influenced by root-knot nematode (Meloidogyne spp., Mi) infection. These experiments were on single-nematode infections, while naturally, roots are infected with several nematode species simultaneously. We performed greenhouse assays to assess the effects of single (Mi, Pp) and concurrent (MP)-nematode infections on aphid performance. Using targeted and untargeted profiling of leaf and phloem metabolomes, we examined how single- and concurrent-nematode infections affect shoot metabolomes, and elucidated the possible consequences on aphid performance. We found that the metabolic response towards double-infection is different from single-species infections. Moreover, Mi- and Pp-infections triggered discrete changes in B. nigra leaf and phloem metabolic profiles. Both Pp and MP-infections reduced aphid survival, suggesting that the biological effect could primarily be dominated by Pp-induced changes. This concurred with increased indole glucosinolates and hydroxycinnamic acid levels in the leaves, in particular the putative involvement of salicylic acid-2-O-β-D-glucoside. This study provides evidence that concurrent infection by different nematode species, as is common in natural environments, is associated with distinct changes in aboveground plant metabolomes, which are linked to differences in the survival of an aboveground herbivore.

Constitutive Level of Specialized Secondary Metabolites Affects Plant Phytohormone Response to Above- and Belowground Herbivores

Plants defend themselves chemically against herbivory through secondary metabolites and phytohormones. Few studies have investigated how constitutive variation in secondary metabolites contributes to systemic herbivory response. We hypothesized that plants with lower constitutive defenses would induce a stronger phytohormone response to spatially separated herbivory than plants with high constitutive defense. We used growth chamber bioassays to investigate how aboveground herbivory by Colorado potato beetle (Leptinotarsa decemlineata, CPB) and belowground herbivory by northern root-knot nematode (Meloidogyne hapla, RKN) altered phytohormones and glycoalkaloids in roots and shoots of two lines of wild potato (Solanum chacoense). These lines had different constitutive levels of chemical defense, particularly leptine glycoalkaloids, which are only present in aboveground tissues. We also determined how these differences influenced the preference and performance of CPB. The susceptible wild potato line responded to aboveground damage by CPB through induction of jasmonic acid (JA) and OPDA. However, when challenged by both RKN and CPB, the susceptible line retained high levels of JA, but not OPDA. Beetles gained more mass after feeding on the susceptible line compared to the resistant line, but were not affected by nematode presence. Belowground, JA, JA-Isoleucine, and OPDA were higher in the resistant line compared to the susceptible line, and some compounds demonstrated response to local herbivory. In contrast, the susceptible line did not induce phytohormone defenses belowground. These findings allow us to predict that constitutive level of defense may influence the threshold of herbivory that may lead to plant-mediated effects on spatially separated herbivores.

The multiple-mechanisms hypothesis of biodiversity–stability relationships

Long-term research in grassland biodiversity experiments has provided empirical evidence that ecological and evolutionary processes are intertwined in determining both biodiversity–ecosystem functioning (BEF) and biodiversity–stability relationships. Focusing on plant diversity, we hypothesize that multifunctional stability is highest in high-diversity plant communities and that biodiversity–stability relationships increase over time due to a variety of forms of ecological complementarity including the interaction with other biota above and below ground. We introduce the multiple-mechanisms hypothesis of biodiversity–stability relationships suggesting that it is not an individual mechanism that drives long-term biodiversity effects on ecosystem functioning and stability but that several intertwined processes produce increasingly positive ecosystem effects. The following six mechanisms are important. Low-diversity plant communities accumulate more plant antagonists over time (1), and use resources less efficiently and have more open, leaky nutrient cycles (2). Conversely, high-diversity plant communities support a greater diversity and activity of beneficial interaction partners across trophic levels (3); diversify in their traits over time and space, within and across species, to optimize temporal (intra- and interannual) and spatial complementarity (4), create a more stable microclimate (5), and foster higher top-down control of aboveground and belowground herbivores by predators (6). In line with the observation that different species play unique roles in ecosystems that are dynamic and multifaceted, the particular mechanism contributing most to the higher performance and stability of diverse plant communities might differ across ecosystem functions, years, locations, and environmental change scenarios. This indicates “between-context insurance” or “across-context complementarity” of different mechanisms. We introduce examples of experiments that will be conducted to test our hypotheses and which might inspire additional work.

Cultivar-Specific Defense Responses in Wild and Cultivated Squash Induced by Belowground and Aboveground Herbivory.

Plant domestication often alters plant traits, including chemical and physical defenses against herbivores. In squash, domestication leads to reduced levels of cucurbitacins and leaf trichomes, influencing interactions with insects. However, the impact of domestication on inducible defenses in squash remains poorly understood. Here, we investigated the chemical and physical defensive traits of wild and domesticated squash (Cucurbita argyrosperma), and compared their responses to belowground and aboveground infestation by the root-feeding larvae and the leaf-chewing adults of the banded cucumber beetle Diabrotica balteata (Coleoptera: Chrysomelidae). Wild populations contained cucurbitacins in roots and cotyledons but not in leaves, whereas domesticated varieties lacked cucurbitacins in all tissues. Belowground infestation by D. balteata larvae did not increase cucurbitacin levels in the roots but triggered the expression of cucurbitacin biosynthetic genes, irrespective of domestication status, although the response varied among different varieties. Conversely, whereas wild squash had more leaf trichomes than domesticated varieties, the induction of leaf trichomes in response to herbivory was greater in domesticated plants. Leaf herbivory varied among varieties but there was a trend of higher leaf damage on wild squash than domesticated varieties. Overall, squash plants responded to both belowground and aboveground herbivory by activating chemical defense-associated gene expression in roots and upregulating their physical defense in leaves, respectively. While domestication suppressed both chemical and physical defenses, our findings suggest that it may enhance inducible defense mechanisms by increasing trichome induction in response to herbivory.

Salinity stress alters plant-mediated interactions between above- and below-ground herbivores

Below-ground herbivory impacts plant development and often induces systemic responses in plants that affect the performance and feeding behavior of above-ground herbivores. Meanwhile, pest-damaged root tissue can enhance a plant's susceptibility to abiotic stress such as salinity. Yet, the extent to which herbivore-induced plant defenses are modulated by such abiotic stress has rarely been studied. In this study, we examine whether root feeding by larvae of the turnip moth, Agrotis segetum (Lepidoptera: Noctuidae) affects the performance of the above-ground, sap-feeding aphid Aphis gossypii (Hemiptera: Aphididae) on cotton, and assess whether those interactions are modulated by salinity stress. In the absence of salinity stress, A. segetum root feeding does not affect A. gossypii development. On the other hand, under intense salinity stress (i.e., 600 mM NaCl), A. segetum root feeding decreases aphid development time by 16.1 % and enhances fecundity by 72.0 %. Transcriptome, metabolome and bioassay trials showed that root feeding and salinity stress jointly trigger the biosynthesis of amino acids in cotton leaves. Specifically, increased titers of valine in leaf tissue relate to an enhanced performance of A. gossypii. Taken together, salinity stress alters the interaction between above- and below-ground feeders by changing amino acid accumulation. Our findings advance our understanding of how plants cope with concurrent biotic and abiotic stressors, and may help tailor plant protection strategies to varying production contexts.

Jasmonic acid and heat stress induce high volatile organic compound emissions in Picea abies from needles, but not from roots.

Plants emit diverse volatile organic compounds (VOCs) from their leaves and roots for protection against biotic and abiotic stress. An important signaling cascade activated by aboveground herbivory is the jasmonic acid (JA) pathway that stimulates the production of VOCs. So far it remains unclear if the activation of this pathway also leads to enhanced VOC emissions from conifer roots, and how the interplay of above- and belowground defenses in plants are affected by multiple stressors. Therefore, we simultaneously analyzed needle and root VOC emissions of Picea abies saplings, as well as CO2 and H2O fluxes in response to aboveground JA treatment, heat stress and their interaction in a controlled climate chamber experiment. Continuous online VOC measurements by PTR-TOF-MS showed an inverse pattern of total needle and root VOC emissions, when plants were treated with JA and heat. While needle sesquiterpene emissions increased nine-fold one day after JA application, total root VOC emissions decreased. This was mainly due to reduced emissions of acetone and monoterpenes by roots. In response to aboveground JA treatment, root total carbon emitted as VOCs decreased from 31% to only 4%. While VOC emissions aboveground increased, net CO2 assimilation strongly declined due to JA treatment, resulting in net respiration during the day. Interestingly, root respiration was not affected by aboveground JA application. Under heat the effect of JA on VOC emissions of needles and roots was less pronounced. The buffering effect of heat on VOC emissions following JA treatment points towards an impaired defense reaction of the plants under multiple stress. Our results indicate efficient resource allocation within the plant to protect threatened tissues by a rather local VOC release. Roots may only be affected indirectly by reduced belowground carbon allocation, but are not involved directly in the JA-induced stress response.

Contrasting plant transcriptome responses between a pierce-sucking and a chewing herbivore go beyond the infestation site

BackgroundPlants have acquired a repertoire of mechanisms to combat biotic stressors, which may vary depending on the feeding strategies of herbivores and the plant species. Hormonal regulation crucially modulates this malleable defense response. Jasmonic acid (JA) and salicylic acid (SA) stand out as pivotal regulators of defense, while other hormones like abscisic acid (ABA), ethylene (ET), gibberellic acid (GA) or auxin also play a role in modulating plant-pest interactions. The plant defense response has been described to elicit effects in distal tissues, whereby aboveground herbivory can influence belowground response, and vice versa. This impact on distal tissues may be contingent upon the feeding guild, even affecting both the recovery of infested tissues and those that have not suffered active infestation.ResultsTo study how phytophagous with distinct feeding strategies may differently trigger the plant defense response during and after infestation in both infested and distal tissues, Arabidopsis thaliana L. rosettes were infested separately with the chewing herbivore Pieris brassicae L. and the piercing-sucker Tetranychus urticae Koch. Moderate infestation conditions were selected for both pests, though no quantitative control of damage levels was carried out. Feeding mode did distinctly influence the transcriptomic response of the plant under these conditions. Though overall affected processes were similar under either infestation, their magnitude differed significantly. Plants infested with P. brassicae exhibited a short-term response, involving stress-related genes, JA and ABA regulation and suppressing growth-related genes. In contrast, T. urticae elicited a longer transcriptomic response in plants, albeit with a lower degree of differential expression, in particular influencing SA regulation. These distinct defense responses transcended beyond infestation and through the roots, where hormonal response, flavonoid regulation or cell wall reorganization were differentially affected.ConclusionThese outcomes confirm that the existent divergent transcriptomic responses elicited by herbivores employing distinct feeding strategies possess the capacity to extend beyond infestation and even affect tissues that have not been directly infested. This remarks the importance of considering the entire plant’s response to localized biotic stresses.

Soil arthropod communities collected from agricultural soils influence wheat growth and modify phytohormone responses to aboveground herbivory in a microcosm experiment

Soil arthropods can affect plant growth and aboveground interactions directly via root herbivory and indirectly through nutrient cycling and interactions with soil microorganisms. Research on these effects of soil arthropods has focused on a few taxa within natural systems, largely neglecting agroecosystems and arthropod community-level effects. This study investigated the effects of soil arthropod communities from cereal-based agroecosystems on wheat plant growth and above-belowground interactions. Nutrient cycling and wheat growth were measured in a greenhouse microcosm experiment using field-collected agricultural soils from two rotational schemes with and without their soil arthropod communities. The effects of soil arthropods on aboveground phytohormones and colony growth of an aphid [Metopolophium festucae cerealium (Stroyan)] infesting the plants were measured. Wheat grown in soils with arthropod communities had significantly greater root (+ Arth mean: 0.15 ± 0.01 g; − Arth mean: 0.06 ± 0.01 g; F1,54 = 72.34, p < 0.001) and shoot biomass (+ Arth mean: 0.39 ± 0.03 g; − Arth mean: 0.24 ± 0.03 g; F1,54 = 17.61, p < 0.001), greater soil nitrate concentrations (+ Arth mean: 62.18 ± 4.76 mg NO3− - N kg−1 soil; − Arth mean: 13.06 ± 0.61 mg NO3− - N kg−1 soil; F1,54 = 99.89, p < 0.001), and altered root architecture compared to controls. Soil arthropod communities collected from the two rotational schemes differed significantly in abundance and diversity, but affected wheat growth similarly. Aphid colony growth (+ Arth mean: 30.50 ± 4.06; − Arth mean: 22.13 ± 3.36; χ21,27 = 21.19, p < 0.001), but not plant damage by aphids (+ Arth mean: 2.72 ± 0.17, − Arth mean: 2.69 ± 0.16; F1,27 = 0.02, p > 0.05), was significantly greater on wheat grown in soils with arthropods. Aphids, in turn, modified the effects of soil arthropods on root architecture and increased the abundance of soil arthropods. Wheat grown in soils with arthropods had increased levels of stress- and defense-related phytohormones in response to aphid herbivory, while phytohormones of wheat plants grown in soils without arthropods did not differ with aphid presence. Soil arthropod communities may help plants defend against herbivores aboveground by facilitating phytohormone induction while offsetting costs by increasing soil nutrients and modifying plant growth. By using taxonomically diverse field-collected soil arthropod communities from agroecosystems, this study showed that community-level effects on plant growth are more complex and dynamic than the effects of any single taxon, such as Collembola, illustrating that interactions within communities can produce emergent properties that alter the net effect of soil arthropods on plant growth. The results indicate that community-level effects of soil organisms should be considered as part of sustainable plant production and protection strategies.

Invasive earthworms modulate native plant trait expression and competition

Biological invasions have major impacts on a variety of ecosystems and threaten native biodiversity. Earthworms have been absent from northern parts of North America since the last ice age, but non‐native earthworms were recently introduced there and are now being spread by human activities. While past work has shown that plant communities in earthworm‐invaded areas change towards a lower diversity mainly dominated by grasses, the underlying mechanisms related to changes in the biotic interactions of the plants are not well understood. Here, we used a trait‐based approach to study the effect of earthworms on interspecific plant competition and aboveground herbivory. We conducted a microcosm experiment in a growth chamber with a full‐factorial design using three plant species native to northern North American deciduous forests, Poa palustris (grass), Symphyotrichum laeve (herb) and Vicia americana (legume), either growing in monoculture or in a mixture of three. These plant community treatments were crossed with earthworm (presence or absence) and herbivore (presence or absence) treatments. Eight out of the fourteen above‐ and belowground plant functional traits studied were significantly affected by earthworms, either by a general effect or in interaction with plant species identity, plant diversity level and/or herbivore presence. Earthworms increased the aboveground productivity and the number of inflorescences of the grass P. palustris. Further, earthworms and herbivores together affected root tissue density of P. palustris and the specific leaf area of V. americana. In this study, earthworm presence gave a competitive advantage to the grass species P. palustris by inducing changes in plant functional traits. Our results suggest that invasive earthworms can alter competitive and multitrophic interactions of plants, shedding light on some of the mechanisms behind invasive earthworm‐induced plant community changes in northern North America forests.

Combined effects of aboveground herbivores and belowground microorganisms on dynamics of soil nematode communities in grassland mesocosms

Nematodes are the most abundant animals in soil. They are active in all trophic levels and functionally important for plant growth and plant diversity. Nematode community structure not only can be directly influenced by other belowground organisms such as soil microbes via trophic interactions, but also indirectly by aboveground organisms like herbivores through plant-mediated aboveground-belowground linkages. In the current study, by introducing foliar-feeding aphids (Rhopalosiphum padi) and soil microbial suspensions to mesocosms planted with 12 grassland plant species and where an identical nematode community was introduced in all mesocosms, we aimed to investigate the individual and combined effects of soil microbes and foliar herbivores on the dynamics of plant and the soil nematode community. Introduction of aphids reduced shoot and root biomass of the plant community, and in particular decreased the proportional biomass of the dominant plant species Anthoxanthum odoratum, resulting in a higher diversity of the plant community but without affecting the nematode communities. In contrast, the inoculation of soil microbes did not significantly alter plant composition structure, but it reduced the total nematode abundance and enhanced nematode diversity by increasing the abundance of carnivorous nematodes and decreasing the abundance of plant-feeding nematodes. There were no significant aboveground-belowground interactions in the current study via effects of aphids on the soil nematode communities or via soil microbes and nematodes on the plant communities. Collectively, our study indicates that soil nematode communities in grasslands can be strongly steered by soil microbial inoculations but weakly influenced by aboveground herbivory despite its resulting changes in plant communities, notwithstanding that these effects appeared to be largely independent.

Two-way plant-mediated interactions between a plant parasitic nematode and a foliar herbivore arthropod

Interactions between belowground and aboveground heterotrophic communities with no direct physical contact can be connected by the plant as a mediator. Plants respond to the attack of herbivores by producing a suite of defensive compounds that can affect the choice and performance of other herbivores. The aim of this study was to determine the impact of one herbivore's activity on the acceptability of that plant to another species of herbivore. Two herbivores were tested; root-knot nematode, Meloidogyne incognita (RKN), a belowground plant-parasitic nematode, and the two-spotted spider mite, Tetranychus urticae (TSSM), an aboveground folivore. We conducted herbivore preference and performance tests on Lima bean (LB) (Phaseolus lunatus cv. Henderson) as an optimal host for TSSM, and tomato (Solanum lycopersicum cv. Rutgers) which is a sub-optimal host for TSSM but optimal host for RKN. We used two-choice glass olfactometers to measure the response of RKN to plants that were exposed to TSSM versus a clean LB plant. RKN infected the clean plants at a significantly greater rate than the TSSM exposed plants. TSSM preference was measured, using leaf discs and two-choice olfactometers containing a RKN infected plant versus a clean plant at different days post-inoculation (DPI) of the RKN. TSSM preferred the clean plants to those with 25-day old RKN infections on LB, but preferred RKN infected tomato plants at 1 DPI. We also tested the effect of the inoculation (1 DPI) of the entomopathogenic nematode (EPN) Steinernema carpocapsae on tomato plants and TSSM preferred the EPN inoculated plants. We carried out a non-choice performance test for TSSM on both LB and tomato on plants inoculated with RKN versus clean plants and observed no effect of RKN exposure on TSSM performance. This research shows that plants can mediate interactions between below and aboveground herbivores that share the same plant.

Effects of simulated psyllid herbivory on the root development of Japanese knotweed.

Japanese knotweed (Reynoutria japonica) is a notoriously invasive riparian plant species which spreads primarily through detachment and dispersal of rhizomes. Currently management options are limited, and there are no biological counters to its spread across the country besides one species. Aphalara itadori, a psyllid native to East Asia has recently been approved by the USDA to be released in the United States to control the spread of Japanese knotweed. This psyllid feeds by piercing aboveground tissues and sucking phloem from the stems and leaves. We investigated the potential role of aboveground herbivory by A. itdori on root system development and rhizome mass in a simulated herbivory experiment. We hypothesized that simulated herbivory would induce the plants to allocate more resources to aboveground tissues for defense or regrowth, potentially limiting root development and reducing rhizome mass. We conducted an experiment with 84 young Japanese knotweed plants divided into two treatment groups: control and simulated herbivory. The simulated herbivory treatment was applied weekly, and plants were harvested weekly to assess changes in rhizome mass and root system development via high resolution root scanning using WinRhizo software. We found that simulated herbivory does affect the root system, though results were inconsistent between weeks. Simulated herbivory decreased root length in week 5 and reduced rhizome mass in weeks 3 and 6. While results were idiosyncratic, they highlight that simulated herbivory may negatively impact root system development in Japanese knotweed, with potential benefits for limiting the spread of knotweed invasion.

Simulated aboveground herbivory is not a source of context dependence in plant-soil feedbacks for individually-grown native and invasive woodland plants

Simulated aboveground herbivory is not a source of context dependence in plant-soil feedbacks for individually-grown native and invasive woodland plants

Density-Dependent Effects of Simultaneous Root and Floral Herbivory on Plant Fitness and Defense

Plants are attacked by multiple herbivores, and depend on a precise regulation of responses to cope with a wide range of antagonists. Simultaneous herbivory can occur in different plant compartments, which may pose a serious threat to plant growth and reproduction. In particular, plants often face co-occurring root and floral herbivory, but few studies have focused on such interactions. Here, we investigated in the field the combined density-dependent effects of root-chewing cebrionid beetle larvae and flower-chewing pierid caterpillars on the fitness and defense of a semiarid Brassicaceae herb. We found that the fitness impact of both herbivore groups was independent and density-dependent. Increasing root herbivore density non-significantly reduced plant fitness, while the relationship between increasing floral herbivore density and the reduction they caused in both seed number and seedling emergence was non-linear. The plant defensive response was non-additive with regard to the different densities of root and floral herbivores; high floral herbivore density provoked compensatory investment in reproduction, and this tolerance response was combined with aboveground chemical defense induction when also root herbivore density was high. Plants may thus prioritize specific trait combinations in response to varying combined below- and aboveground herbivore densities to minimize negative impacts on fitness.

Current and legacy effects of neighborhood communities on plant growth and aboveground herbivory

Current and legacy effects can greatly affect the growth of a focal plant and its interactions with herbivores and such effects can be mediated by above- and belowground effects. However, determining the relative importance of current and legacy above- and belowground effects in natural conditions is a major challenge. In a long-term grassland experiment, we examined the relative importance of the current and legacy above- and belowground effects of plant communities on the growth and aboveground herbivore damage on a focal plant, Leucanthemum vulgare. Focal plants were planted into tubes with soil collected from different plant communities and placed back into the plant communities. Weekly, plant growth and damage were recorded and after 12 weeks plant biomass was measured. We analyzed how well aboveground and belowground characteristics of the current and legacy plots explained plant growth and herbivory. We found both current plant communities and legacy plant communities significantly affected plant growth (shoot biomass and the number of leaves) and herbivory. Root biomass of the focal plants was influenced by current plant communities only. Current and legacy above- and belowground characteristics explained 12% and 11% of the variation in shoot biomass. Root biomass was mainly explained by current above- and belowground characteristics with a total explained variation of 10%, while legacy effects explained 3%. Legacy effects explained most variation in the number of leaves during the first two weeks of measurements, and the effect remained present during the growth season. In contrast, characteristics of the current community explained most of the variation in herbivory throughout the growth period, with on average 6% explained variance aboveground vs. 5% belowground. Our grassland field study highlights that both current and legacy effects influence plant growth, but herbivory on focal plants is caused by current neighborhood effects only and not by legacy effects.

Aboveground herbivory does not affect mycorrhiza-dependent nitrogen acquisition from soil but inhibits mycorrhizal network-mediated nitrogen interplant transfer in maize.

Arbuscular mycorrhizal fungi (AMF) are considered biofertilizers for sustainable agriculture due to their ability to facilitate plant uptake of important mineral elements, such as nitrogen (N). However, plant mycorrhiza-dependent N uptake and interplant transfer may be highly context-dependent, and whether it is affected by aboveground herbivory remains largely unknown. Here, we used 15N labeling and tracking to examine the effect of aboveground insect herbivory by Spodoptera frugiperda on mycorrhiza-dependent N uptake in maize (Zea mays L.). To minimize consumption differences and 15N loss due to insect chewing, insect herbivory was simulated by mechanical wounding and oral secretion of S. frugiperda larvae. Inoculation with Rhizophagus irregularis (Rir) significantly improved maize growth, and N/P uptake. The 15N labeling experiment showed that maize plants absorbed N from soils via the extraradical mycelium of mycorrhizal fungi and from neighboring plants transferred by common mycorrhizal networks (CMNs). Simulated aboveground leaf herbivory did not affect mycorrhiza-mediated N acquisition from soil. However, CMN-mediated N transfer from neighboring plants was blocked by leaf simulated herbivory. Our findings suggest that aboveground herbivory inhibits CMN-mediated N transfer between plants but does not affect N acquisition from soil solutions via extraradical mycorrhizal mycelium.

Undercover operation: Belowground insect herbivory modifies systemic plant defense and repels aboveground foraging insect herbivores

Plants attacked by insects may induce defenses locally in attacked plant tissues and/or systemically in non-attacked tissues, such as aboveground herbivory affecting belowground roots or belowground herbivory modifying aboveground tissues (i.e., cross-compartment systemic defense). Through induced systemic plant defenses, above-and belowground insect herbivores indirectly interact when feeding on a shared host plant. However, determining the systemic effects of herbivory on cross-compartment plant tissues and cascading consequences for herbivore communities remains underexplored. The goal of this study was to determine how belowground striped cucumber beetle (Acalymma vittatum) larval herbivory alters aboveground zucchini squash (Cucurbita pepo subsp. pepo) defenses and interactions with herbivores, including adult cucumber beetles and squash bugs (Anasa tristis). To explore this question, field and laboratory experiments were conducted to compare responses of aboveground herbivores to belowground larvae-damaged plants and non-damaged control plants. We also characterized changes in defensive chemicals and nutritional content of aboveground plant structures following belowground herbivory. We discovered belowground herbivory enhanced aboveground plant resistance and deterred aboveground foraging herbivores. We also found that larvae-damaged plants emitted higher amounts of a key volatile compound, (E)-β-ocimene, compared to non-damaged controls. Further investigation suggests that other mechanisms, such as plant nutrient content, may additionally contribute to aboveground herbivore foraging decisions. Collectively, our findings underscore connections between above-and belowground herbivore communities as mediated through induced systemic defenses of a shared host plant. Specifically, these findings indicate that belowground larval herbivory systemically enhances plant defenses and deters a suite of aboveground herbivores, suggesting larvae may manipulate aboveground plant defenses for their own benefit, while plants may benefit from enhanced systemic defenses against multi-herbivore attack.

Aboveground herbivory can promote exotic plant invasion through intra- and interspecific aboveground-belowground interactions.

Aboveground herbivores and soil biota profoundly affect plant invasions. However, how they interactively affect plant invasions through plant-soil feedbacks (PSFs) remains unclear. To explore how herbivory by the introduced beetle Agasicles hygrophila affects Alternanthera philoxeroides invasions in China, we integrated multiyear field surveys and a 2-yr PSF experiment, in which we examined how herbivory affects PSFs on the performance of native and invasive plants and the introduced beetles. Despite increased herbivory from A.hygrophila, A.philoxeroides dominance over co-occurring congeneric native Alternanthera sessilis remained constant from 2014 to 2019. While occurring at lower abundances, A.sessilis experienced similar herbivore damage, suggesting apparent competitive effects. Our experiments revealed that herbivory on A.philoxeroides altered soil microbial communities, prolonged its negative PSF on A.sessilis, and decreased A.hygrophila larvae performance on the next-generation invasive plants. Consequently, A.hygrophila larvae performed better on leaves of natives than those of invasives when grown in soils conditioned by invasive plants defoliated by the introduced beetles. Our findings suggest that aboveground herbivory might promote rather than suppress A.philoxeroides invasion by enhancing its soil-mediated self-reinforcement, providing a novel mechanistic understanding of plant invasions. These findings highlight the need to incorporate an aboveground-belowground perspective during the assessment of potential biocontrol agents.

Herbivory modifies plant symbiont number and impact on host plant performance in the field.

Species interactions are a unifying theme in ecology and evolution. Both fields are currently moving beyond their historical focus on isolated pairwise relationships to understand how ecological communities affect focal interactions. Additional species can modify both the number of interactions and the fitness consequences of each interaction (i.e., selection). Although only selection affects the evolution of the focal interaction, the two are often conflated, limiting our understanding of the evolution of multispecies interactions. We manipulated aboveground herbivory on the legume Medicago lupulina in the field and quantified its effect on number of symbionts and the per-symbiont impact on plant performance in two belowground symbioses: mutualistic rhizobia bacteria (Ensifer meliloti) and parasitic root-knot nematodes (Meloidogyne hapla). We found that herbivores modified the number of rhizobia nodules, as well as the benefit per nodule. However, each effect was specific to a distinct herbivory regime: natural herbivory affected nodule number, whereas leafhoppers (Cicadellidae) weakened the per nodule benefit. We did not detect any effect of herbivory on nematode gall number or the cost of infection. Our data demonstrate that distinguishing between symbiont number from the fitness consequences of symbiosis is crucial to accurately infer how pairwise interactions will evolve in a community.

Characterizing rhizosphere microbial communities associated with tolerance to aboveground herbivory in wild and domesticated tomatoes.

Root-associated microbial communities are well known for their ability to prime and augment plant defenses that reduce herbivore survival or alter behavior (i.e., resistance). In contrast, the role root microbes play in plant tolerance to herbivory, an evolutionarily sustainable alternative to resistance, is overlooked. In this study, we aimed to expand our limited understanding of what role rhizosphere microbial communities play in supporting tolerance to insect damage. Using domesticated tomatoes and their wild ancestors (Solanum spp.), we first documented how tobacco hornworm (Manduca sexta) herbivory impacted tomato fruit production in order to quantify plant tolerance. We then characterized the bacterial and fungal rhizosphere communities harbored by high and low tolerance plants. Wild tomatoes excelled at tolerating hornworm herbivory, experiencing no significant yield loss despite 50% leaf area removal. Their domesticated counterparts, on the other hand, suffered 26% yield losses under hornworm herbivory, indicating low tolerance. Ontogeny (i.e., mid- vs. late-season sampling) explained the most variation in rhizosphere community structure, with tomato line, tolerance, and domestication status also shaping rhizosphere communities. Fungal and bacterial community traits that associated with the high tolerance line include (1) high species richness, (2) relatively stable community composition under herbivory, and (3) the relative abundance of taxa belonging to Stenotrophomonas, Sphingobacterium, and Sphingomonas. Characterizing tolerance-associating microbiomes may open new avenues through which plant defenses are amended in pest management, such as plant breeding efforts that enhance crop recruitment of beneficial microbiomes.