Herbivore Host Research Articles

Traits across trophic levels interact to influence parasitoid establishment in biological control releases.

A central goal in ecology is to predict what governs a species’ ability to establish in a new environment. One mechanism driving establishment success is individual species’ traits, but the role of trait combinations among interacting species across different trophic levels is less clear. Deliberate or accidental species additions to existing communities provide opportunities to study larger scale patterns of establishment success. Biological control introductions are especially valuable because they contain data on both the successfully established and unestablished species. Here, we used a recent dataset of importation biological control introductions to explore how life‐history traits of 132 parasitoid species and their herbivorous hosts interact to affect parasitoid establishment. We find that of five parasitoid and herbivore traits investigated, one parasitoid trait—host range—weakly predicts parasitoid establishment; parasitoids with higher levels of phylogenetic specialization have higher establishment success, though the effect is marginal. In addition, parasitoids are more likely to establish when their herbivore host has had a shorter residence time. Interestingly, we do not corroborate earlier findings that gregarious parasitoids and endoparasitoids are more likely to establish. Most importantly, we find that life‐history traits of the parasitoid species and their hosts can interact to influence establishment. Specifically, parasitoids with broader host ranges are more likely to establish when the herbivore they have been released to control is also more of a generalist. These results provide insight into how multiple species’ traits and their interactions, both within and across trophic levels, can influence establishment of species of higher trophic levels.

Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore.

Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly, Euphydryas phaeton (Nymphalidae), have recently incorporated an exotic plant, Plantago lanceolata (Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus, Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using either P. lanceolata or a native plant, Chelone glabra (Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.

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.

Manduca sexta experience high parasitoid pressures in the field but minor fitness costs of consuming plant secondary compounds.

Plant‐herbivore coevolutionary interactions have led to a range of plant defenses that minimize insect damage and a suite of counter adaptations that allow herbivores to feed on defended plants. Consuming plant secondary compounds results in herbivore growth and developmental costs but can have beneficial effects such as deterrence or harm of parasitoid enemies. Therefore, the role of secondary compounds on herbivore fitness must be considered in the context of the abundance and level of harm from natural enemies and the costs herbivores incur feeding on plant secondary compounds.In this study, I combined field measurements of Cotesia congregata wasp parasitism pressure with detailed measurements of the costs of plant secondary compounds across developmental stages in the herbivore host, Manduca sexta.I show that C. congregata parasitoids exert large negative selective pressures, killing 31%–57% of M. sexta larvae in the field. Manduca sexta developed fastest during instars most at risk for parasitoid oviposition but growth was slowed by consumption of plant secondary compounds. The negative effects of consuming plant secondary compounds as larvae influenced adult size traits but there were no immune, survival, or fecundity costs.These results suggest that developmental costs experienced by M. sexta herbivores consuming defensive compounds are minor in comparison to the strong negative survival pressures from abundant parasitoid enemies.

Plant-phenotypic changes induced by parasitoid ichnoviruses enhance the performance of both unparasitized and parasitized caterpillars.

There is increasing awareness that interactions between plants and insects can be mediated by microbial symbionts. Nonetheless, evidence showing that symbionts associated with organisms beyond the second trophic level affect plant‐insect interactions are restricted to a few cases belonging to parasitoid‐associated bracoviruses. Insect parasitoids harbour a wide array of symbionts which, like bracoviruses, can be injected into their herbivorous hosts to manipulate their physiology and behaviour. Yet, the function of these symbionts in plant‐based trophic webs remains largely overlooked. Here, we provide the first evidence of a parasitoid‐associated symbiont belonging to the group of ichnoviruses which affects the strength of plant‐insect interactions. A comparative proteomic analysis shows that, upon parasitoid injection of calyx fluid containing ichnovirus particles, the composition of salivary glands of caterpillars changes both qualitatively (presence of two viral‐encoded proteins) and quantitatively (abundance of several caterpillar‐resident enzymes, including elicitors such as glucose oxidase). In turn, plant phenotypic changes triggered by the altered composition of caterpillar oral secretions affect the performance of herbivores. Ichnovirus manipulation of plant responses to herbivory leads to benefits for their parasitoid partners in terms of reduced developmental time within the parasitized caterpillar. Interestingly, plant‐mediated ichnovirus‐induced effects also enhance the performances of unparasitized herbivores which in natural conditions may feed alongside parasitized ones. We discuss these findings in the context of ecological costs imposed to the plant by the viral symbiont of the parasitoid. Our results provide intriguing novel findings about the role played by carnivore‐associated symbionts on plant‐insect‐parasitoid systems and underline the importance of placing mutualistic associations in an ecological perspective.

Feeding guild determines strength of top-down forces in multitrophic system experiencing bottom-up constraints

Nitrogen (N) and water are crucial in crop production but increasingly scarce environmental resources. Reducing their inputs can affect the whole plant-arthropod community including biocontrol agents. In a multitrophic system, we studied the interaction of the bottom-up effects of moderately reduced N concentration and/or water supply as well as the top-down effects of pests of different feeding guilds on plant nutritional quality (N and carbon concentration), direct defense (alkaloids and phenolics), and indirect defense (plant volatile organic compounds); on herbivore performance and host quality (N and carbon) to parasitoids and the latter's performance. Studied organisms were tomato plants, the sap feeders Macrosiphum euphorbiae and Bemisia tabaci, the leaf chewers Tuta absoluta and Spodoptera littoralis, and the parasitic wasps Aphelinus abdominalis and Necremnus tutae. Resource limitation affected plant quality, triggering bottom-up effects on herbivore and parasitoid performance, except for T. absoluta and N. tutae. Feeding guild had a major influence: bottom-up effects were stronger on sap feeders; N effects were stronger on sap feeders while water effects were stronger with leaf chewers (S. littoralis). Top-down effects of leaf chewer herbivory partly attenuated bottom-up effects and partly suppressed plant defenses. Bottom-up effects weakened when cascading up trophic levels. In summary, the interaction between plants, pests, and beneficial insects was modulated by abiotic factors, affecting insect performance. Simultaneous abiotic and biotic impact shaped plant biochemistry depending on the feeding guild: the biotic top-down effect of leaf chewer herbivory attenuated the bottom-up effects of plant nutrition and hence dominated the plant biochemical profile whereas in sap feeder infested leaves, it corresponded to the abiotic impact. This study highlights the plant's finely tuned regulatory system facilitating response prioritization. It offers perspectives on how smart manipulation of plant nutrient solutions might save resources while maintaining efficient biocontrol in crop production.

Influence of parasitoid-associated viral symbionts on plant-insect interactions and biological control.

Insect parasitoids have evolved symbiotic interactions with several viruses and thousands of parasitoid species have established mutualistic associations with polydnaviruses (PDVs). While PDVs have often been described as virulence factors allowing development of immature parasitoids inside their herbivore hosts, there is increasing awareness that PDVs can affect plant-insect interactions. We review recent literature showing that PDVs alter not only host physiology, but also feeding patterns and composition of herbivore's oral secretions. In turn PDV-induced changes in herbivore phenotype affect plant responses to herbivory with consequences ranging from differential expression of plant defense-related genes to wider ecological effects across multiple trophic levels. In this opinion paper we also highlight important missing gaps to fully understand the role of PDVs and other parasitoid-associated viral symbionts in a plant-insect interaction perspective. Because PDVs negatively impact performance and survival of herbivore pests, we conclude arguing that PDV genomes offer potential opportunities for biological control.

Aversive responses of Queensland fruit flies towards larval-infested fruits are modified by fruit quality and prior experience

For frugivorous fruit flies, the decision whether to accept or reject a host fruit for oviposition is influenced by a variety of fruit quality factors. Additionally, ovipositing flies may be influenced by the presence of eggs or larvae already within the host fruit. Species of the genus Bactrocera have been shown to avoid ovipositing into larval-infested fruits. However, the observed oviposition aversion in Bactrocera is variable, with some studies showing that deterrence to infested fruits may not always occur, but what may influence such variation is unknown. Using the polyphagous fruit fly Bactrocera tryoni (Froggatt), we tested if the quality of host fruit for offspring survival was a factor in influencing a female fly’s decision whether to oviposit or not into larval-infested fruits. In both small cages and field cages, ovipositing B. tryoni did not discriminate between infested and non-infested high-quality fruits. However, when given a choice between poor-quality infested and non-infested fruits, significantly more flies selected and oviposited in non-infested fruits. For example, B. tryoni did not discriminate between infested and non-infested guava (a fruit in which there is high offspring survival), but more flies selected and oviposited on non-infested than on infested green apples (a fruit in which there is poor offspring survival). Small cage experiments also showed that prior oviposition experience on a larval-infested host negated the previously observed aversive response for that particular infested host fruit. The results are discussed in the light of a long recognised, but often ignored fact that herbivore host choice is about the sum of both the positive and negative cues received from the host.

Walk this way, fly that way: Goniozus jacintae attunes flight and foraging behaviour to leafroller host instar

AbstractParasitoids exhibit distinct behaviours while foraging for their herbivorous hosts. Some are specialised with respect to the host stage they can utilise and even the age of individuals within a single stage. Observing the behavioural response of parasitoids to hosts of varying age may provide more practical understanding of potential biocontrol agents. A wind tunnel experiment was conducted to test for host‐stage dependent foraging behaviour in Goniozus jacintae Farrugia (Hymenoptera: Bethylidae), a common but understudied parasitoid of the light brown apple moth (LBAM), Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae), which is a pest of grapevine, Vitis vinifera L. (Vitaceae), and other crops in Australia. Goniozus jacintae was already known to parasitise instars 3‐6 of LBAM, but most readily parasitises the later instars. Later instars are larger and have a higher rate of feeding, producing more faeces and silk deposits than earlier instars, and are likely to also produce more volatile cues that may be detected by parasitoids. We found that the timing, frequency, and duration of foraging behaviours of G. jacintae varied significantly among host instars. Flight duration was shortest when females were exposed to leaves infested by fifth instars. The profile of behaviours exhibited was different during pre‐ and post‐flight foraging, with the newly described slow walking behaviour only exhibited in close proximity to a potential host. These results contribute to the understanding of bethylid foraging, a relatively unexplored aspect of bethylid reproductive behaviour, and towards enhancing the efficacy of utilising G. jacintae in the control of leafroller pests.

The Role of Trialeurodes vaporariorum-Infested Tomato Plant Volatiles in the Attraction of Encarsia formosa (Hymenoptera: Aphelinidae).

Natural enemies locate their herbivorous host and prey through kairomones emitted by host plants and herbivores. These kairomones could be exploited to attract and retain natural enemies in crop fields for insect pest control. The parasitoid Encarsia formosa preferentially parasitises its whitefly host, Trialeurodes vaporariorum, a major pest of tomato Solanum lycopersicum, thus offering an effective way to improve whitefly control. However, little is known about the chemical interactions that occur in E. formosa-T. vaporariorum-S. lycopersicum tritrophic system. Using behavioural assays and chemical analyses, we investigated the kairomones mediating attraction of the parasitoid to host-infested tomato plants. In Y-tube olfactometer bioassays, unlike volatiles of healthy tomato plants, those of T. vaporariorum-infested tomato plants attracted E. formosa, and this response varied with host infestation density. Coupled gas chromatography/mass spectrometric analyses revealed that host infestation densities induced varying qualitative and quantitative differences in volatile compositions between healthy and T. vaporariorum adult-infested tomato plants. Bioassays using synthetic chemicals revealed the attractiveness of 3-carene, β-ocimene, β-myrcene and α-phellandrene to the parasitoid, and the blend of the four compounds elicited the greatest attraction. Our results suggest that these terpenes could be used as an attractant lure to recruit the parasitoid E. formosa for the control of whiteflies in tomato crop fields.

Host quality does not matter to native or invasive cactus moth larvae: grave implications for North American prickly pears

1. Relationships between prickly pear cactus (Cactaceae: Opuntia) and specialist moth larvae (Lepidoptera: Pyralidae) are exemplar of exclusive interactions between herbivorous insects and host plants.2. We measured nutritional and defensive factors indicative of Opuntia quality to native and invasive host‐specialised moth larvae. Our goals were to investigate whether host qualities varied among and within Opuntia species, use that information to test whether host quality axes predicted occupancy by larvae in two focal O. engelmannii populations, and draw conclusions about whether these herbivores were resource limited.3. There were minimal differences in protein, carbohydrate, fatty acid, fibre, water, and cuticular thickness, among four Opuntia species distributed throughout Texas. Macronutrient content did not differ between most species. Mucilage exudation was an induced response to herbivory. Field experiments compared pairs of O. engelmannii in which one individual hosted native Melitara doddalis or invasive Cactoblastis cactorum larvae, and the other did not; host quality and nutritional space did not predict herbivore occupancy. Moreover, ordination of host quality traits did not reveal spatial aggregation of cacti with and without herbivores.4. These results demonstrated that neither moth species was resource limited. An overall lack of variation among and within Texas Opuntia indicate that these species were suitable resources to invasive C. cactorum that recently established in Texas.5. Outcomes of this study have serious implications for Opuntia, native moths, and associated food webs, that will soon interact with an expanding C. cactorum population as it spreads inland from the Texas Gulf Coast.

Bottom-up Effects on Tri-trophic Interactions: Plant Fertilization Enhances the Fitness of a Primary Parasitoid Mediated by Its Herbivore Host.

Plants play a pivotal role in interactions involving herbivores and their natural enemies. Variation in plant primary and secondary metabolites not only affects herbivores but, directly and indirectly, also their natural enemies. Here, we used a commercial NPK fertilizer to test the impact of three fertilizer, namely 50, 100, and 200 ppm nitrogen, and one control (i.e., water) treatments, on the weight of the nymphs of the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Subsequently, the whitefly parasitoid Eretmocerus mundus Mercet (Hymenoptera: Aphelinidae) was reared on the different groups of whitefly nymphs and upon parasitoid emergence, the number of oocytes was determined as a measure of reproductive capacity. Trials were done on tomato and tobacco plants. The level of nitrogen concentration in tobacco leaves was directly correlated with the fertilizer applications, thus confirming the effect of our fertilizer treatments. Both in tomato and tobacco plants, healthy as well as parasitized whitefly nymphs, were heaviest in the 200 ppm nitrogen treatment. The highest number of oocytes per female parasitoid was recorded in the 200 ppm nitrogen treatment in tomato (31% more oocytes as compared with the control) and in the 100 and 200 ppm nitrogen treatments in tobacco (200% more oocytes). We suggest that the increase in oocytes was the result of the enhanced size (food quantity) and/or nutritional quality of the whitefly host. The practical implications of these results for the mass rearing of whitefly parasitoids and for biological pest control are discussed.

Do plant volatiles confuse rather than guide foraging behavior of the aphid hyperparasitoid Dendrocerus aphidum?

Many species of parasitoid wasps use plant volatiles to locate their herbivorous hosts. These volatiles are reliable indicators of host presence when their emission in plants is induced by herbivory. Hyperparasitoids may also use information from lower trophic levels to locate their parasitoid hosts but little is known about the role of volatiles from the plant–host complex in the foraging behavior of hyperparasitoids. Here, we studied how Dendrocerus aphidum (Megaspilidae) responds to plant and host volatiles in a series of experiments. This hyperparasitoid uses aphid mummies as its host and hampers biological control of aphids by parasitoids in greenhouse horticulture. We found that D. aphidum females were strongly attracted to volatiles from mummy-infested sweet pepper plants, but only when clean air was offered as an alternative odor source in the Y-tube olfactometer. Hyperparasitoid females did not have a preference for mummy-infested plants when volatiles from aphid-infested or healthy pepper plants were presented as an alternative. These olfactory responses of D. aphidum were mostly independent of prior experience. Volatiles from the host itself were also highly attractive to D. aphidum, but again hyperparasitoid females only had a preference in the absence of plant volatiles. Our findings suggest that plant volatiles may confuse, rather than guide the foraging behavior of D. aphidum. Mummy hyperparasitoids, such as D. aphidum, can use a wide variety of mummies and are thus extreme generalists at the lower trophic levels, which may explain the limited role of (induced) plant volatiles in their host searching behavior.

Fungus-growing insects host a distinctive microbiota apparently adapted to the fungiculture environment

Some lineages of ants, termites, and beetles independently evolved a symbiotic association with lignocellulolytic fungi cultivated for food, in a lifestyle known as fungiculture. Fungus-growing insects’ symbiosis also hosts a bacterial community thought to integrate their physiology. Similarities in taxonomic composition support the microbiota of fungus-growing insects as convergent, despite differences in fungus-rearing by these insects. Here, by comparing fungus-growing insects to several hosts ranging diverse dietary patterns, we investigate whether the microbiota taxonomic and functional profiles are characteristic of the fungiculture environment. Compared to other hosts, the microbiota associated with fungus-growing insects presents a distinctive taxonomic profile, dominated by Gammaproteobacteria at class level and by Pseudomonas at genera level. Even with a functional profile presenting similarities with the gut microbiota of herbivorous and omnivorous hosts, some differentially abundant features codified by the microbiota of fungus-growing insects suggest these communities occupying microhabitats that are characteristic of fungiculture. These features include metabolic pathways involved in lignocellulose breakdown, detoxification of plant secondary metabolites, metabolism of simple sugars, fungal cell wall deconstruction, biofilm formation, antimicrobials biosynthesis, and metabolism of diverse nutrients. Our results suggest that the microbiota could be functionally adapted to the fungiculture environment, codifying metabolic pathways potentially relevant to the fungus-growing insects’ ecosystems functioning.

Asymmetric Responses to Climate Change: Temperature Differentially Alters Herbivore Salivary Elicitor and Host Plant Responses to Herbivory

The effect of temperature on insect-plant interactions in the face of changing climate is complex as the plant, its herbivores and their interactions are usually affected differentially leading to an asymmetry in response. Using experimental warming and a combination of biochemical and herbivory bioassays, the effects of elevated temperatures and herbivore damage (Helicoverpa zea) on resistance and tolerance traits of Solanum lycopersicum var. Better boy (tomato), as well as herbivory performance and salivary defense elicitors were examined. Insects and plants were differentially sensitive towards warming within the experimental temperature range. Herbivore growth rate increased with temperature, whereas plants growth as well as the ability to tolerate stress measured by photosynthesis recovery and regrowth ability were compromised at the highest temperature regime. In particular, temperature influenced the caterpillars’ capacity to induce plant defenses due to changes in the amount of a salivary defense elicitor, glucose oxidase (GOX). This was further complexed by the temperature effects on plant inducibility, which was significantly enhanced at an above-optimum temperature; this paralleled with an increased plants resistance to herbivory but significantly varied between previously damaged and undamaged leaves. Elevated temperatures produced asymmetry in species’ responses and changes in the relationship among species, indicating a more complicated response under a climate change scenario.

The gut bacterial community affects immunity but not metabolism in a specialist herbivorous butterfly.

Plant tissues often lack essential nutritive elements and may contain a range of secondary toxic compounds. As nutritional imbalance in food intake may affect the performances of herbivores, the latter have evolved a variety of physiological mechanisms to cope with the challenges of digesting their plant‐based diet. Some of these strategies involve living in association with symbiotic microbes that promote the digestion and detoxification of plant compounds or supply their host with essential nutrients missing from the plant diet. In Lepidoptera, a growing body of evidence has, however, recently challenged the idea that herbivores are nutritionally dependent on their gut microbial community. It is suggested that many of the herbivorous Lepidopteran species may not host a resident microbial community, but rather a transient one, acquired from their environment and diet. Studies directly testing these hypotheses are however scarce and come from an even more limited number of species.By coupling comparative metabarcoding, immune gene expression, and metabolomics analyses with experimental manipulation of the gut microbial community of prediapause larvae of the Glanville fritillary butterfly (Melitaea cinxia, L.), we tested whether the gut microbial community supports early larval growth and survival, or modulates metabolism or immunity during early stages of development.We successfully altered this microbiota through antibiotic treatments and consecutively restored it through fecal transplants from conspecifics. Our study suggests that although the microbiota is involved in the up‐regulation of an antimicrobial peptide, it did not affect the life history traits or the metabolism of early instars larvae.This study confirms the poor impact of the microbiota on diverse life history traits of yet another Lepidoptera species. However, it also suggests that potential eco‐evolutionary host‐symbiont strategies that take place in the gut of herbivorous butterfly hosts might have been disregarded, particularly how the microbiota may affect the host immune system homeostasis.

Host functional and phylogenetic composition rather than host diversity structure plant-herbivore networks.

Declining plant diversity alters ecological networks, such as plant-herbivore interactions. However, our knowledge of the potential mechanisms underlying effects of plant species loss on plant-herbivore network structure is still limited. We used DNA barcoding to identify herbivore-host plant associations along declining levels of tree diversity in a large-scale, subtropical biodiversity experiment. We tested for effects of tree species richness, host functional and phylogenetic diversity, and host functional (leaf trait) and phylogenetic composition on species, phylogenetic and network composition of herbivore communities. We found that phylogenetic host composition and related palatability/defence traits but not tree species richness significantly affected herbivore communities and interaction network complexity at both the species and community levels. Our study indicates that evolutionary dependencies and functional traits of host plants determine the composition of higher trophic levels and corresponding interaction networks in species-rich ecosystems. Our findings highlight that characteristics of the species lost have effects on ecosystem structure and functioning across trophic levels that cannot be predicted from mere reductions in species richness.

Symbiont Digestive Range Reflects Host Plant Breadth in Herbivorous Beetles

Numerous adaptations are gained in light of a symbiotic lifestyle. Here, we investigated the obligate partnership between tortoise leaf beetles (Chrysomelidae: Cassidinae) and their pectinolytic Stammera symbionts to detail how changes to the bacterium's streamlined metabolic range can shape the digestive physiology and ecological opportunity of its herbivorous host. Comparative genomics of 13 Stammera strains revealed high functional conservation, highlighted by the universal presence of polygalacturonase, a primary pectinase targeting nature's most abundant pectic class, homogalacturonan (HG). Despite this conservation, we unexpectedly discovered a disparate distribution for rhamnogalacturonan lyase, a secondary pectinase hydrolyzing the pectic heteropolymer, rhamnogalacturonan I (RG-I). Consistent with the annotation of rhamnogalacturonan lyase in Stammera, cassidines are able to depolymerize RG-I relative to beetles whose symbionts lack the gene. Given the omnipresence of HG and RG-I in foliage, Stammera that encode pectinases targeting both substrates allow their hosts to overcome a greater diversity of plant cell wall polysaccharides and maximize access to the nutritionally rich cytosol. Possibly facilitated by their symbionts' expanded digestive range, cassidines additionally endowed with rhamnogalacturonan lyase appear to utilize a broader diversity of angiosperms than those beetles whose symbionts solely supplement polygalacturonase. Our findings highlight how symbiont metabolic diversity, in concert with host adaptations, may serve as a potential source of evolutionary innovations for herbivorous lineages.

Varying responses to combined water-stress and herbivory in maize for spider mite species that differ in host specialization

Water-stress commonly affects crops grown in arid and semi-arid regions. Apart from the direct impact of this abiotic stress on yield, a diverse community of herbivores can outbreak under these conditions, and plant responses to abiotic stress may alter plant defense responses that deter herbivores. Outbreaks of both generalist and specialist spider mites are strongly associated with hot and dry conditions in the field settings. To understand how water-stress impacts maize responses to spider mites, we conducted parallel greenhouse and field experiments with maize plants (B73 inbred line) subjected to optimal irrigation and water-stress conditions (50-60% and 5-10% volumetric water content (VWC), and 25-32% and 10-15% VWC, in the greenhouse and field, respectively). In addition to recording B73 responses to water-stress alone, we measured the population growth of the generalist twospotted spider mite (Tetranychus urticae, TSM) and the specialist Banks grass mite (Oligonychus pratensis, BGM) on optimally watered and water-stressed plants. We also measured plant defense protein activities (peroxidase (POD), polyphenol oxidase (PPO), chitinase (CHI) and trypsin inhibitor (TI)) at 1, 3, and 7 days post mite introduction for each irrigation treatment. For B73 plants exposed to water-stress, we observed increases in leaf temperature, leaf water potential, POD activity, as well as decreases in stomatal conductance and stem height. Populations of both mite species increased more rapidly on water-stressed B73 plants. While optimally irrigated B73 plants responded with similar plant defense activity to both mite species, combinations of plant water-stress and TSM herbivory resulted in increases in CHI and TI activity that were not observed for the respective treatments with BGM. Collectively, our results highlight a role for species-specific factors, possibly associated with herbivore host plant breadth, in impacting plant responses to herbivory in combination with an abiotic stress.

Intraguild predation decreases predator fitness with potentially varying effects on pathogen transmission in a herbivore host

Predators and pathogens often regulate the population dynamics of their prey or hosts. When species interact with both their predators and their pathogens, understanding each interaction in isolation may not capture the system's dynamics. For instance, predators can influence pathogen transmission via consumptive effects, such as feeding on infected prey, or non-consumptive effects, such as changing the prey's susceptibility to infection. A prey species' infection status can, in turn, influence predator's choice of prey and have negative fitness consequences for the predator. To test how intraguild predation (IGP), when predator and pathogen share the same prey/host, affects pathogen transmission, predator preference, and predator fitness, we conducted a series of experiments using a crop pest (Pseudoplusia includens), a generalist predator (Podisus maculiventris), and a generalist pathogen (Autographa californica multicapsid nuclear polyhedrovirus, AcMNPV). Using a field experiment, we quantified the effects of consumptive and non-consumptive predators on pathogen transmission. We found that a number of models provided similar fits to the data. These models included null models showing no effects of predation and models that included a predation effect. We also found that predators consumed infected prey more often when choosing between live infected or live healthy prey. Infected prey also reduced predator fitness. Developmental times of predators fed infected prey increased by 20% and longevity decreased by 45%, compared with those that consumed an equivalent number of non-infected prey. While this research shows an effect of the pathogen on intraguild predator fitness, we found no support that predators affected pathogen transmission.