Multitrophic and Multilevel Interactions Mediated by Volatile Organic Compounds.

Plants communicate with insects and other organisms through the release of volatile organic compounds (VOCs). Using Boolean operators, we retrieved 1093 articles from the Web of Science and Scopus databases, selecting 406 for detailed analysis, with approximately 50% focusing on herbivore-induced plant volatiles (HIPVs). This review examines the roles of VOCs in direct and indirect plant defense mechanisms and their influence on complex communication networks within ecosystems. Our research reveals significant functions of VOCs in four principal areas: activating insect antennae, attracting adult insects, attracting female insects, and attracting natural enemies. Terpenoids like α-pinene and ß-myrcene significantly alter pest behavior by attracting natural enemies. ß-ocimene and ß-caryophyllene are crucial in regulating aboveground and belowground interactions. We emphasize the potential applications of VOCs in agriculture for developing novel pest control strategies and enhancing crop resilience. Additionally, we identify research gaps and propose new directions, stressing the importance of comparative studies across ecosystems and long-term observational research to better understand VOCs dynamics. In conclusion, we provide insights into the multifunctionality of VOCs in natural ecosystems, their potential for future research and applications, and their role in advancing sustainable agricultural and ecological practices, contributing to a deeper understanding of their mechanisms and ecological functions.

Insect-microbe interactions and their influence on organisms and ecosystems.

Microorganisms are important associates of insect and arthropod species. Insect-associated microbes, including bacteria, fungi, and viruses, can drastically impact host physiology, ecology, and fitness, while many microbes still have no known role. Over the past decade, we have increased our knowledge of the taxonomic composition and functional roles of insect-associated microbiomes and viromes. There has been a more recent shift toward examining the complexity of microbial communities, including how they vary in response to different factors (e.g., host genome, microbial strain, environment, and time), and the consequences of this variation for the host and the wider ecological community. We provide an overview of insect-microbe interactions, the variety of associated microbial functions, and the evolutionary ecology of these relationships. We explore the influence of the environment and the interactive effects of insects and their microbiomes across trophic levels. Additionally, we discuss the potential for subsequent synergistic and reciprocal impacts on the associated microbiomes, ecological interactions, and communities. Lastly, we discuss some potential avenues for the future of insect-microbe interactions that include the modification of existing microbial symbionts as well as the construction of synthetic microbial communities.

From a local descriptive to a generic predictive model of cereal aphid regulation by predators.

The temporal dynamics of insect populations in agroecosystems are influenced by numerous biotic and abiotic interactions, including trophic interactions in complex food webs. Predicting the regulation of herbivorous insect pests by arthropod predators and parasitoids would allow for rendering crop production less dependent on chemical pesticides. Curtsdotter et al. (2019) developed a food-web model simulating the influences of naturally occurring arthropod predators on aphid population dynamics in cereal crop fields. The use of an allometric hypothesis based on the relative body masses of the prey and various predator guilds reduced the number of estimated parameters to just five, albeit field-specific. Here, we extend this model and test its applicability and predictive capacity. We first parameterized the original model with a dataset with the dynamic arthropod community compositions in 54 fields in six regions in France. We then integrated three additional biological functions to the model: parasitism, aphid carrying capacity and suboptimal high temperatures that reduce aphid growth rates. We developed a multi-field calibration approach to estimate a single set of generic allometric parameters for a given group of fields, which would increase model generality needed for predictions. The original and revised models, when using field-specific parameterization, achieved quantitatively good fits to observed aphid population dynamics for 59% and 53% of the fields, respectively, with pseudo-R2 up to 0.99. But the multi-field calibration showed that increased model generality came at the cost of reduced model reliability (goodness-of-fit). Our study highlights the need to further improve our understanding of how body size and other traits affect trophic interactions in food webs. It also points up the need to acquire high-resolution data to use this type of modelling approach. We propose that a hypothesis-driven strategy of model improvement based on the integration of additional biological functions and additional functional traits beyond body size (e.g., predator space search or prey defences) into the food-web matrix can improve model reliability.

Rhizobia-legume symbiosis mediates direct and indirect interactions between plants, herbivores and their parasitoids.

Microorganisms associated with plant roots significantly impact the quality and quantity of plant defences. However, the bottom-up effects of soil microbes on the aboveground multitrophic interactions remain largely under studied. To address this gap, we investigated the chemically-mediated effects of nitrogen-fixing rhizobia on legume-herbivore-parasitoid multitrophic interactions. To address this, we initially examined the cascading effects of the rhizobia bean association on herbivore caterpillars, their parasitoids, and subsequently investigated how rhizobia influence on plant volatiles and extrafloral nectar. Our goal was to understand how these plant-mediated effects can affect parasitoids. Lima bean plants (Phaseoulus lunatus) inoculated with rhizobia exhibited better growth, and the number of root nodules positively correlated with defensive cyanogenic compounds. Despite increase of these chemical defences, Spodoptera latifascia caterpillars preferred to feed and grew faster on rhizobia-inoculated plants. Moreover, the emission of plant volatiles after leaf damage showed distinct patterns between inoculation treatments, with inoculated plants producing more sesquiterpenes and benzyl nitrile than non-inoculated plants. Despite these differences, Euplectrus platyhypenae parasitoid wasps were similarly attracted to rhizobia- or no rhizobia-treated plants. Yet, the oviposition and offspring development of E. platyhypenae was better on caterpillars fed with rhizobia-inoculated plants. We additionally show that rhizobia-inoculated common bean plants (Phaseolus vulgaris) produced more extrafloral nectar, with higher hydrocarbon concentration, than non-inoculated plants. Consequently, parasitoids performed better when fed with extrafloral nectar from rhizobia-inoculated plants. While the overall effects of bean-rhizobia symbiosis on caterpillars were positive, rhizobia also indirectly benefited parasitoids through the caterpillar host, and directly through the improved production of high quality extrafloral nectar. This study underscores the importance of exploring diverse facets and chemical mechanisms that influence the dynamics between herbivores and predators. This knowledge is crucial for gaining a comprehensive understanding of the ecological implications of rhizobia symbiosis on these interactions.

Multitrophic Higher-Order Interactions Modulate Species Persistence.

AbstractEcologists increasingly recognize that interactions between two species can be affected by the density of a third species. How these higher-order interactions (HOIs) affect species persistence remains poorly understood. To explore the effect of HOIs stemming from multiple trophic layers on a plant community composition, we experimentally built a mesocosm with three plants and three pollinator species arranged in a fully nested and modified network structure. We estimated pairwise interactions among plants and between plants and pollinators, as well as HOIs initiated by a plant or a pollinator affecting plant species pairs. Using a structuralist approach, we evaluated the consequences of the statistically supported HOIs on the persistence probability of each of the three competing plant species and their combinations. HOIs substantially redistribute the strength and sign of pairwise interactions between plant species, promoting the opportunities for multispecies communities to persist compared with a non-HOI scenario. However, the physical elimination of a plant-pollinator link in the modified network structure promotes changes in per capita pairwise interactions and HOIs, resulting in a single-species community. Our study provides empirical evidence of the joint importance of HOIs and network structure in determining species persistence within diverse communities.

Aphidius colemani Behavior Changes Depending on Volatile Organic Compounds Emitted by Plants Infected with Viruses with Different Modes of Transmission.

Natural enemies are an additional component that may interact directly with the plant-virus-vector association, affecting viral dispersion. In our study, we conducted olfactometry assays to explore how single and mixed infections with CMV or/and CABYV modify the attractiveness of A. colemani to aphid-free and aphid-infested melon plants using two melon genotypes. Subsequently, we investigated the influence of CABYV-infected plants infested by A. gossypii on the parasitism rate and emergence of A. colemani in a dual-choice assay under greenhouse conditions. Our study demonstrates that males showed no preference for either infected or non-infected plants. Female parasitoids exhibit a preference for volatiles emitted by CMV and mixed-infected melon plants over clean air but not over mock-inoculated plants, suggesting a response influenced by plant genotype. Female parasitoid responses to CABYV and its interactions with aphids revealed a preference for mock-inoculated plants over CABYV-infected plants and a parasitism rate slightly higher (7.12%) on non-infected plants. Our study revealed that (1) parasitoids may reject olfactory cues from CABYV-infected plants, potentially interfering with the plant's "cry for help" response; (2) in the case of CMV, whether in single or mixed infections, non-infected plants are as attractive as infected ones to parasitoids. Our findings suggest that persistent viruses manipulate aphid parasitoid behavior to their advantage, promoting virus disease in melon crops.

Toward an Integrated Understanding of the Lepidoptera Microbiome.

Research over the past 30 years has led to a widespread acceptance that insects establish widespread and diverse associations with microorganisms. More recently, microbiome research has been accelerating in lepidopteran systems, leading to a greater understanding of both endosymbiont and gut microorganisms and how they contribute to integral aspects of the host. Lepidoptera are associated with a robust assemblage of microorganisms, some of which may be stable and routinely detected in larval and adult hosts, while others are ephemeral and transient. Certain microorganisms that populate Lepidoptera can contribute significantly to the hosts' performance and fitness, while others are inconsequential. We emphasize the context-dependent nature of the interactions between players. While our review discusses the contemporary literature, there are major avenues yet to be explored to determine both the fundamental aspects of host-microbe interactions and potential applications for the lepidopteran microbiome; we describe these avenues after our synthesis.

Linking Anthropogenic Landscape Perturbation to Herbivory and Pathogen Leaf Damage in Tropical Tree Communities.

Anthropogenic disturbance of tropical humid forests leads to habitat loss, biodiversity decline, landscape fragmentation, altered nutrient cycling and carbon sequestration, soil erosion, pest/pathogen outbreaks, among others. Nevertheless, the impact of these alterations in multitrophic interactions, including host-pathogen and vector-pathogen dynamics, is still not well understood in wild plants. This study aimed to provide insights into the main drivers for the incidence of herbivory and plant pathogen damage, specifically, into how vegetation traits at the local and landscape scale modulate such interactions. For this purpose, in the tropical forest of Calakmul (Campeche, Mexico), we characterised the foliar damage caused by herbivores and pathogens in woody vegetation of 13 sampling sites representing a gradient of forest disturbance and fragmentation in an anthropogenic landscape from well preserved to highly disturbed and fragmented areas. We also evaluated how the incidence of such damage was modulated by the vegetation and landscape attributes. We found that the incidence of damage caused by larger, mobile, generalist herbivores, was more sensitive to changes in landscape configuration, while the incidence of damage caused by small and specialised herbivores with low dispersal capacity was more influenced by vegetation and landscape composition. In relation to pathogen symptoms, the herbivore-induced foliar damage seems to be the main factor related to their incidence, indicating the enormous importance of herbivorous insects in the modulation of disease dynamics across tropical vegetation, as they could be acting as vectors and/or facilitating the entry of pathogens by breaking the foliar tissue and the plant defensive barriers. The incidence of pathogen damage also responded to vegetation structure and landscape configuration; the incidence of anthracnose, black spot, and chlorosis, for example, were favoured in sites surrounded by smaller patches and a higher edge density, as well as those with a greater aggregation of semi-evergreen forest patches. Fungal pathogens were shown to be an important cause of foliar damage for many woody species. Our results indicate that an increasing transformation and fragmentation of the tropical forest of southern Mexico could reduce the degree of specialisation in plant-herbivore interactions and enhance the proliferation of generalist herbivores (chewers and scrapers) and of mobile leaf suckers, and consequently, the proliferation of some symptoms associated with fungal pathogens such as fungus black spots and anthracnose. The symptoms associated with viral and bacterial diseases and to nutrient deficiency, such as chlorosis, could also increase in the vegetation in fragmented landscapes with important consequences in the health and productivity of wild and cultivated plant species. This is a pioneering study evaluating the effect of disturbances on multitrophic interactions, offering key insights on the main drivers of the changes in herbivory interactions and incidence of plant pathogens in tropical forests.

Birds and bats enhance cacao yield despite suppressing arthropod mesopredation.

Bird- and bat-mediated biocontrol benefits the productivity of tropical commodity crops such as cacao, but the ecological interactions driving these ecosystem services remain poorly understood. Whereas birds and bats prey on herbivorous arthropods, they may also prey on arthropod mesopredators such as ants, with poorly understood consequences for pest biocontrol. We used a full-factorial experiment excluding birds, bats, and ants to assess their effects on (a) the abundance of multiple arthropod groups; (b) predation pressure on arthropods evaluated through artificial sentinel caterpillars; and (c) cacao yield over 1 year in shaded agroforestry systems of native cacao varieties in Peru. Birds and bats increased cacao yield by 118%, which translates in smallholder benefits of ca. US $959 ha-1 year-1 . Birds and bats decreased predation by ants and other arthropods, but contributed to the control of phytophagous taxa such as aphids and mealybugs. By contrast, ant presence increased the abundance of these sap-sucking insects, with negative impacts for cacao yield. Notably, high abundances of the dominant ant Nylanderia sp., known to attend sap-sucking insects, were associated with lower cacao yield along a distance gradient from the closest forest edge. According to these results, arthropod predation by birds and bats, rather than mesopredation by arthropods, was most responsible for increases in cacao yield. Moving forward, detailed research about their trophic interactions will be necessary to identify the cause of such benefits. Retaining and restoring the large benefits of birds and bats as well as minimizing disservices by other taxa in cacao agroforests can benefit from management schemes that prioritize preservation of shade trees and adjacent forests within agroforestry landscapes.

Early damage enhances compensatory responses to herbivory in wild lima bean.

Damage by herbivores can induce various defensive responses. Induced resistance comprises traits that can reduced the damage, while compensatory responses reduce the negative effects of damage on plant fitness. Timing of damage may be essential in determining the patterns of induced defenses. Here, we tested how timing and frequency of leaf damage affect compensatory responses in wild lima bean plants in terms of growth and seed output, as well as their effects on induced resistance to seed beetles. To this end, we applied mechanical damage to plants at different ontogenetical stages, at one time point (juvenile stage only) or two time points (seedling and juvenile stage or juvenile and reproductive stage). We found that plants damaged at the seedling/juvenile stage showed higher compensatory growth, and seed output compared to plants damaged only at the juvenile stage or juvenile/reproductive stage. Seeds from plants damaged at the juvenile and juvenile/reproductive stages had fewer beetles than seeds from undamaged plants, however this was driven by a density dependent effect of seed abundance rather than a direct effect of damage treatments. We did not find differences in parasitism rate by parasitoid wasps on seed beetles among plant treatments. Our results show that damage at the seedling stage triggers compensatory responses which implies that tolerance to herbivory is enhanced or primed by early damage. Herbivory often occurs at several time points throughout plant development and this study illustrates that, for a full understanding of the factors associated with plant induced responses in a dynamic biotic environment, it is important to determine the multitrophic consequences of damage at more than one ontogenetical stage.

Olfactometer Responses of Convergent Lady Beetles Hippodamia convergens (Coleoptera: Coccinellidae) to Odor Cues from Aphid-Infested Cotton Plants Treated with Plant-Associated Fungi.

Microbes have the potential to affect multitrophic plant-insect-predator interactions. We examined whether cotton plants treated with potentially beneficial fungi affect interactions between cotton aphids Aphis gossypii and predatory lady beetles Hippodamia convergens. We used Y-tube olfactometer assays to test lady beetle behavioral responses to stimuli emitted by aphid-infested and non-infested cotton plants grown from seeds treated with either Phialemonium inflatum (TAMU490) or Chaetomium globosum (TAMU520) versus untreated control plants. We tested a total of 960 lady beetles (480 males and 480 females) that had been deprived of food for approximately 24 h. In the absence of any fungal treatments, males preferred stimuli from aphid-infested plants, and females spent more time associated with stimuli from aphid-infested versus non-infested plants. When fungal treatments were added, we observed that lady beetles preferred non-aphid-infested P. inflatum plants, and males responded slower to plants treated with P. inflatum in the absence of aphids. We found some evidence to suggest that lady beetle behavioral responses to plants might vary according to the fungal treatment but not strongly impact their use as part of an insect pest management strategy.

Genomic and Biological Characterization of Ralstonia solanacearum Inovirus Brazil 1, an Inovirus that Alters the Pathogenicity of the Phytopathogen Ralstonia pseudosolanacearum.

Filamentous bacteriophages contain a single-stranded DNA genome and have a peculiar lifestyle, since they do not cause host cell lysis, but establish a persistent association with the host, often causing behavioral changes, with effects on bacterial ecology. Over the years, a gradual reduction in the incidence of bacterial wilt has been observed in some fields from Brazil. This event, which has been associated with the loss of pathogenicity of Rasltonia spp. isolates due to infection by filamentous viruses of the inovirus group, is widely reported for Ralstonia spp. Asian isolates infected by inoviruses. In an attempt to elucidate which factors are associated with the phenomenon reported in Brazil, we investigated one isolate of R. solanacearum (UB-2014), with unusual characteristics for R. solanacearum, obtained from eggplant with mild wilt symptoms. To verify if the presence of filamentous bacteriophage was related to this phenotype, we performed viral purification and nucleic acid extraction. The phage genome was sequenced, and phylogenetic analyses demonstrated that the virus belongs to the family Inoviridae and was named as Ralstonia solanacerarum inovirus Brazil 1 (RSIBR1). RSIBR1 was transmitted to R. pseudosolanacearum GMI1000, and the virus-infected GMI1000 (GMI1000 VI) isolate showed alterations in phenotypic characteristics, as well as loss of pathogenicity, similarly to that observed in R. solanacearum isolate UB-2014. The presence of virus-infected UB-2014 and GMI1000 VI plants without symptoms, after 3 months, confirms that the infected isolates can colonize the plant without causing disease, which demonstrates that the phage infection changed the behavior of these pathogens.

Beneficial worm allies warn plants of parasite attack below-ground and reduce above-ground herbivore preference and performance.

Antagonistic interactions among different functional guilds of nematodes have been recognized for quite some time, but the underlying explanatory mechanisms are unclear. We investigated responses of tomato (Solanum lycopersicum) to two functional guilds of nematodes-plant parasite (Meloidogyne javanica) and entomopathogens (Heterorhabditis bacteriophora, Steinernema feltiae below-ground, and S. carpocapsae)-as well as a leaf mining insect (Tuta absoluta) above-ground. Our results indicate that entomopathogenic nematodes (EPNs): (1) reduced root knot nematode (RKN) infestation below-ground, (2) reduced herbivore (T. absoluta) host preference and performance above-ground, and (3) induced overlapping plant defence responses by rapidly activating polyphenol oxidase and guaiacol peroxidase activity in roots, but simultaneously suppressing this activity in above-ground tissues. Concurrently, we investigated potential plant signalling mechanisms underlying these interactions using transcriptome analyses. We found that both entomopathogens and plant parasites triggered immune responses in plant roots with shared gene expression. Secondary metabolite transcripts induced in response to the two nematode functional guilds were generally overlapping and showed an analogous profile of regulation. Likewise, we show that EPNs modulate plant defence against RKN invasion, in part, by suppressing active expression of antioxidant enzymes. Inoculations of roots with EPN triggered an immune response in tomato via upregulated phenylpropanoid metabolism and synthesis of protease inhibitors in plant tissues, which may explain decreased egg laying and developmental performance exhibited by herbivores on EPN-inoculated plants. Furthermore, changes induced in the volatile organic compound-related transcriptome indicated that M. javanica and/or S. carpocapsae inoculation of plants triggered both direct and indirect defences. Our results support the hypothesis that plants "mistake" subterranean EPNs for parasites, and these otherwise beneficial worms activate a battery of plant defences associated with systemic acquired resistance and/or induced systemic resistance with concomitant antagonistic effects on temporally co-occurring subterranean plant pathogenic nematodes and terrestrial herbivores.

The Ecology of Hyperparasitoids.

Hyperparasitoids are some of the most diverse members of insect food webs. True hyperparasitoids parasitize the larvae of other parasitoids, reaching these larvae with their ovipositor through the herbivore that hosts the parasitoid larva. During pupation, primary parasitoids also may be attacked by pseudohyperparasitoids that lay their eggs on the parasitoid (pre)pupae. By attacking primary parasitoids, hyperparasitoids may affect herbivore population dynamics, and they have been identified as a major challenge in biological control. Over the past decades, research, especially on aphid- and caterpillar-associated hyperparasitoids, has revealed that hyperparasitoids challenge rules on nutrient use efficiency in trophic chains, account for herbivore outbreaks, or stabilize competitive interactions in lower trophic levels, and they may use cues derived from complex interaction networks to locate their hosts. This review focuses on the fascinating ecology of hyperparasitoids related to how they exploit and locate their often inconspicuous hosts and the insect community processes in which hyperparasitoids are prominent players.

Community structure and specialization in fig wasps (Hymenoptera: Chalcidoidea) in a region of Cerrado

ABSTRACT Ficus inflorescences host a species-rich chalcid wasp community, including pollinating fig wasps (Agaonidae: Tetrapusinae, Kradibiinae, and Agaoninae) and several species of non-pollinating fig wasps (NPFW), that show several life-history strategies, including gall-inducers, kleptoparasites (i. e. inquilines), and parasitoids. We analyzed the structure and degree of specialization of the fig wasp community associated with Ficus inflorescences in urbanized areas, agroecosystems, and on the edge of forest fragments in the state of Goiás (Brazil). We sampled 34 wasp species in four native Ficus tree species, from which four wasp species occurred in more than one host. Neotropical fig pollinators (Pegoscapus and Tetrapus) were the most abundant species, and they were host-specific, although two pollinator species were associated with Ficus obtusifolia. The Jaccard similarity index was higher in samples of fig wasps collected in the same host, indicating that the community composition was specific to each host species. Community structure indices indicate a specialized structure with low connectance, high bidimensional Shannon H2' and low partner diversity. The communities present a modular web structure in which modules were represented by each host and its associated insect species. These results indicate that the fig wasp communities analyzed are highly specialized, despite a few not strictly host-specific species.

Climate Change Modulates Multitrophic Interactions Between Maize, A Root Herbivore, and Its Enemies.

How climate change will modify belowground tritrophic interactions is poorly understood, despite their importance for agricultural productivity. Here, we manipulated the three major abiotic factors associated with climate change (atmospheric CO2, temperature, and soil moisture) and investigated their individual and joint effects on the interaction between maize, the banded cucumber beetle (Diabrotica balteata), and the entomopathogenic nematode (EPN) Heterorhabditis bacteriophora. Changes in individual abiotic parameters had a strong influence on plant biomass, leaf wilting, sugar concentrations, protein levels, and benzoxazinoid contents. Yet, when combined to simulate a predicted climate scenario (Representative Concentration Pathway 8.5, RCP 8.5), their effects mostly counter-balanced each other. Only the sharp negative impact of drought on leaf wilting was not fully compensated. In both current and predicted scenarios, root damage resulted in increased leaf wilting, reduced root biomass, and reconfigured the plant sugar metabolism. Single climatic variables modulated the herbivore performance and survival in an additive manner, although slight interactions were also observed. Increased temperature and CO2 levels both enhanced the performance of the insect, but elevated temperature also decreased its survival. Elevated temperatures and CO2 further directly impeded the EPN infectivity potential, while lower moisture levels improved it through plant- and/or herbivore-mediated changes. In the RCP 8.5 scenario, temperature and CO2 showed interactive effects on EPN infectivity, which was overall decreased by 40%. We conclude that root pest problems may worsen with climate change due to increased herbivore performance and reduced top-down control by biological control agents.

Great tits (Parus major) flexibly learn that herbivore-induced plant volatiles indicate prey location: An experimental evidence with two tree species.

When searching for food, great tits (Parus major) can use herbivore-induced plant volatiles (HIPVs) as an indicator of arthropod presence. Their ability to detect HIPVs was shown to be learned, and not innate, yet the flexibility and generalization of learning remain unclear.We studied if, and if so how, naïve and trained great tits (Parus major) discriminate between herbivore-induced and noninduced saplings of Scotch elm (Ulmus glabra) and cattley guava (Psidium cattleyanum). We chemically analyzed the used plants and showed that their HIPVs differed significantly and overlapped only in a few compounds.Birds trained to discriminate between herbivore-induced and noninduced saplings preferred the herbivore-induced saplings of the plant species they were trained to. Naïve birds did not show any preferences. Our results indicate that the attraction of great tits to herbivore-induced plants is not innate, rather it is a skill that can be acquired through learning, one tree species at a time.We demonstrate that the ability to learn to associate HIPVs with food reward is flexible, expressed to both tested plant species, even if the plant species has not coevolved with the bird species (i.e., guava). Our results imply that the birds are not capable of generalizing HIPVs among tree species but suggest that they either learn to detect individual compounds or associate whole bouquets with food rewards.

Shared friends counterbalance shared enemies in old forests.

Mycorrhizal mutualisms are nearly ubiquitous across plant communities. Yet, it is still unknown whether facilitation among plants arises primarily from these mycorrhizal networks or from physical and ecological attributes of plants themselves. Here, we tested the relative contributions of mycorrhizae and plants to both positive and negative biotic interactions to determine whether plant-soil feedbacks with mycorrhizae neutralize competition and enemies within multitrophic forest community networks. We used Bayesian hierarchical generalized linear modeling to examine mycorrhizal-guild-specific and mortality-cause-specific woody plant survival compiled from a spatially and temporally explicit data set comprising 101,096 woody plants from three mixed-conifer forests across western North America. We found positive plant-soil feedbacks for large-diameter trees: species-rich woody plant communities indirectly promoted large tree survival when connected via mycorrhizal networks. Shared mycorrhizae primarily counterbalanced apparent competition mediated by tree enemies (e.g., bark beetles, soil pathogens) rather than diffuse competition between plants. We did not find the same survival benefits for small trees or shrubs. Our findings suggest that lower large-diameter tree mortality susceptibility in species-rich temperate forests resulted from greater access to shared mycorrhizal networks. The interrelated importance of aboveground and belowground biodiversity to large tree survival may be critical for counteracting increasing pathogen, bark beetle, and density threats.

Microbiota, pathogens, and parasites as mediators of tritrophic interactions between insect herbivores, plants, and pollinators.

Insect-associated microbes, including pathogens, parasites, and symbionts, influence the interactions of herbivorous insects and pollinators with their host plants. Moreover, herbivory-induced changes in plant resource allocation and defensive chemistry can influence pollinator behavior. This suggests that the outcomes of interactions between herbivores, their microbes and host plants could have implications for pollinators. As epizootic diseases occur at high population densities, pathogen and parasite-mediated effects on plants could have landscape-level impacts on foraging pollinators. The goal of this minireview is to highlight the potential for an herbivore's multitrophic interactions to trigger plant-mediated effects on the immunity and health of pollinators. We highlight the importance of plant quality and gut microbiomes in bee health, and how caterpillars as model herbivores interact with pathogens, parasites, and symbionts to affect plant quality, which forms the centerpiece of multitrophic interactions between herbivores and pollinators. We also discuss the impacts of other herbivore-associated factors, such as agricultural inputs aimed at decreasing herbivorous pests, on pollinator microbiomes.