Thomas S. Davis

Microbial Volatile Emissions as Insect Semiochemicals

We provide a synthesis of the literature describing biochemical interactions between microorganisms and insects by way of microbial volatile organic compound (MVOC) production. We evaluated the functionality and ecological context of MVOC signals, and explored important metabolic pathways involved in MVOC production. The cosmopolitan distribution of microorganisms creates a context for frequent, and frequently overlooked, insect responses to microbial emissions. There are numerous instances of MVOCs being closely associated with insect feeding behaviors, but some MVOCs are also powerful repellants. Emissions from microorganisms in situ may signal aspects of habitat suitability or potential exposure to entomopathogens. In some ecosystems, bacterial or fungal volatiles can also incite insect aggregations, or MVOCs can resemble sexual pheromones that elicit mating and oviposition behaviors from responding insects. A single microorganism or MVOC can have different effects on insect behaviors, especially across species, ontogenies, and habitats. There appears to be a multipartite basis for insect responses to MVOCs, and complex tritrophic interactions can result from the production of MVOCs. Many biochemical pathways for behaviorally active volatile production by microbial species are conserved across large taxonomic groupings of microorganisms. In addition, there is substantial functional redundancy in MVOCs: fungal tissues commonly produce polyketides and short-chain alcohols, whereas bacterial tissues tend to be more commonly associated with amines and pyrazines. We hypothesize that insect olfactory responses to emissions from microorganisms inhabiting their sensory environment are much more common than currently recognized, and that these signals represent evolutionarily reliable infochemicals. Insect chemoreception of microbial volatiles may contribute to the formation of neutral, beneficial, or even harmful symbioses and provide considerable insight into the evolution of insect behavioral responses to volatile compounds.

Environmentally dependent host–pathogen and vector–pathogen interactions in the Barley yellow dwarf virus pathosystem

Summary Understanding environmentally dependent variation in interspecific interactions is needed for evaluating how agroecosystems respond to abiotic stressors, including climate change. Both biotic and abiotic conditions shape crop responses to stress events, but interactions between environmental conditions and insect borne plant pathogens remain poorly understood. We tested the hypothesis that drought stress, as applied by experimental water deprivation, drives conditional outcomes in host–pathogen and host–vector interactions using a cereal–aphid–virus association and greenhouse experiments. Under conditions of ample water supply, infection of wheat plants with Barley yellow dwarf virus (BYDV) resulted in reduced above-ground growth, seed set, seed yields and seed germination compared with plants exposed only to non-infected (non-viruliferous) aphids or control plants not subjected to aphid infestation. However, when water was chronically limiting, infection with Barley yellow dwarf virus did not significantly affect plant performance. When wheat was subjected to acute drought stress, plants infected with Barley yellow dwarf virus surpassed both control plants and plants exposed to non-infected aphids in all measured performance traits. Feeding experiments with aphid vectors (Rhopalosiphum padi) and subsequent life table analysis revealed that aphid fecundity improved by 47% when feeding on Barley yellow dwarf virus-infected plants when water inputs were chronically low. However, when plants received ample water, aphid fecundity was enhanced by only 23% from feeding on BYDV-infected plants. Synthesis and applications. Collectively, our experiments suggest that wheat– Barley yellow dwarf virus interactions shift along gradients of water stress severity and duration. When Barley yellow dwarf virus infection preceded water deprivation, plant performance was not reduced from virus infection, and infected plants recovered from severe stress events more readily than non-infected plants. However, vector–pathogen mutualism resulting in enhanced reproduction of aphids on virus-infected plants is likely to amplify direct plant injury from herbivory in the field. Our findings indicate that during periods of drought, management of Barley yellow dwarf virus infection may not be needed and infection could benefit wheat under conditions of acute water stress.

The Ecology of Yeasts in the Bark Beetle Holobiont: A Century of Research Revisited

Yeasts are extremely common associates of scolytine bark beetles, yet the basic ecology of yeasts in the bark beetle holobiont remains poorly understood. Yeasts are present in all beetle life stages and consistently isolated from adult, larval, and pupal integuments and mycangial structures, but yeasts are also found in oviposition galleries, pupal chambers, larval and adult digestive tracts, as well as phloem and xylem tissues. Yeasts in the Saccharomycetaceae family are the most prevalent associates, and most individual beetles are associated with only one or several yeast species. Kuraishia capsulata and Ogataea pini are the most commonly encountered yeast species in surveys of Dendroctonus and Ips beetles; most beetles that have been surveyed are vectors for one or both yeasts. Yeasts have significant but often overlooked functional roles in bark beetle ecology. Infochemicals resulting from volatile production by yeast have wide-ranging bioactivity for arthropods: Yeast emissions attract beetles at low concentrations but repel beetles at high concentrations, and yeast emissions can also serve as cues to predators and parasites of bark beetles. In some cases, yeasts can modify tree chemistry over time or metabolize toxic terpenoids, though potential consequences for beetle performance or the growth of nutritional fungi remain to be demonstrated. Also, the presence of yeast species can restrict or promote the establishment and growth of filamentous fungi, including mutualists, entomopathogens, and opportunistic saprophytes. The role of yeasts as nutritional symbionts has received mixed support, though a nutritional hypothesis has not been extensively tested. Continued research on the functional ecology of bark beetle–yeast associations is needed to better understand the emergent properties of these complex symbiont assemblages.

Symbiotic Associations of Bark Beetles

A vast community of organisms occurs on and within bark beetles and bark beetle-infested trees. The large diversity of symbiotic species covers a breadth of functional roles that are often redundant or substitutable. Symbiotic associations can be facultative or obligatory, and vary from antagonistic to mutualistic depending on the context at which the interactions occurs. Most symbiotic organisms are phoretic, and thus are transferred from tree to tree by bark beetles or other arthropods. Symbionts influence bark beetle communication, reproduction, nutrition and population dynamics, as well as tri-trophic interactions, competition among species, and host-tree utilization by bark beetles. Taxa considered symbiotic with bark beetles include fungi, bacteria, viruses, algae, mites, protozoa, and nematodes, among others. Interactions among symbionts are often mediated by host plant chemistry, abiotic factors such as temperature, or other phoretic organisms. Some of the symbionts, such as fungi, amplify our view of bark beetles as pests, as they may be tree pathogens or influence the coloration and texture of wood or plant products. However, some symbionts may also provide a solution to bark beetle population outbreaks and range expansion, as some symbiotic species are harmful to bark beetles and could be used as biological control agents.

Aphid behavioral responses to virus-infected plants are similar despite divergent fitness effects

We compared the settling preferences and reproductive potential of an oligophagous herbivore, the pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), in response to pea plants, Pisum sativum L. cv. ‘Aragorn’ (Fabaceae), infected with two persistently transmitted viruses, Pea enation mosaic virus (PEMV) and Bean leaf roll virus (BLRV), that differ in their distribution within an infected plant. Aphids preferentially oriented toward and settled on plants infected with PEMV or BLRV in comparison with sham‐inoculated plants (plants exposed to herbivory by uninfected aphids), but aphids did not discriminate between plants infected with the two viruses. Analysis of plant volatiles indicated that plants inoculated with either virus had significantly higher green leaf volatile‐to‐monoterpene ratios. Time until reproductive maturity was marginally influenced by plant infection status, with a trend toward earlier nymph production on infected plants. There were consistent age‐specific effects of plant infection status on aphid fecundity: reproduction was significantly enhanced for aphids on BLRV‐infected plants across most time intervals, though mean aphid fecundity did not differ between sham and PEMV‐infected plants. There was no clear pattern of age‐specific survivorship; however, mean aphid lifespan was reduced on plants infected with PEMV. Our results are consistent with predictions of the host manipulation hypothesis, extended to include plant viruses: non‐viruliferous A. pisum preferentially orient to virus‐infected host plants, potentially facilitating pathogen transmission. These studies extend the scope of the host manipulation hypothesis by demonstrating that divergent fitness effects on vectors arise relative to the mode of virus transmission.

Evidence for additive effects of virus infection and water availability on phytohormone induction in a staple crop

Infection with phytoviruses influences plant responses to environmental stress, but the biochemical mechanisms underlying these interactions are unknown. Infection of wheat (Triticum aestivum) with a cereal virus (Barley yellow dwarf virus, BYDV) has context-dependent effects on plant productivity and survival conditional to water stress, and we hypothesized this was due to phythormone induction resulting from virus infection. We tested whether BYDV infection and water availability interact to influence hormone profiles in wheat across multiple time periods. Wheat plants were inoculated with BYDV by exposing them to infectious aphids (Rhopalosiphum padi). Concentrations of five hormones (abscisic acid, jasmonic acid, methyl jasmonate, methyl salicylate [MS], and salicylic acid [SA]) in leaf tissues were compared to concentrations in plants exposed to noninfectious aphids (sham treatment) and nondamaged control plants for five time-since-infection periods (0, 8, 16, 24, and 32 d) and two levels of water availability (0.2 and 0.8 g H20/g soil). Three important findings emerged: (1) total hormone concentrations in BYDV-infected plants exceeded concentrations in sham-treated and control plants up to 16 d following infection, after which nondamaged plants exhibited the highest concentrations of hormones; compared with nondamaged and BYDV-infected plants, hormone levels were reduced in sham-treated plants; (2) inoculation treatment affected concentrations of MS and SA: SA concentrations were increased in BYDV-infected plants, but control plants exhibited higher MS concentrations than either BYDV-infected or sham-treated plants irrespective of watering treatments and across all time periods; and (3) correlation analysis revealed no evidence of hormonal cross-inhibition. This study provides the first evidence that BYDV infection elevates both total phytohormone levels and SA in wheat in a time-sensitive manner, suggesting a potential biochemical basis for virus-induced hormonal responses that alter plant responses to environmental stress.

Attraction of the Orange Mint Moth and False Celery Leaftier Moth (Lepidoptera: Crambidae) to Floral Chemical Lures

ABSTRACT Orange mint moths, Pyrausta orphisalis (Walker) (Crambidae), were initially trapped in a study of noctuid moth attraction to floral volatiles. A subsequent series of trapping experiments in commercial mint fields determined that phenylacetaldehyde and 4-oxoisophorone were attractive to P. orphisalis, whereas benzyl acetate, eugenol, cis-jasmone, limonene, linalool, methyl-2-methoxybenzoate, methyl salicylate, &bgr;-myrcene, and 2-phenylethanol were not. When used in combination with phenylacetaldehyde, 4-oxoisophorone and methyl-2-methoxybenzoate increased catches of P. orphisalis in traps by ∼50%, and &bgr;-myrcene tripled the trap catch. A second crambid species, the false celery leaftier moth, Udea profundalis Packard, was also attracted to phenylacetaldehyde, but was not attracted to any other single-chemical lure. Cis-jasmone, limonene, and 4-oxoisophorone increased catches of U. profundalis by &bgr;50% when presented in traps with phenylacetaldehyde, while linalool increased the catch 2.5-fold, and &bgr;-myrcene tripled the trap catch. Both sexes of each species were similarly attracted to most of these lures. These findings provide chemical lures for trapping males and females of both P. orphisalis and U. profundalis.

Differing contributions of density dependence and climate to the population dynamics of three eruptive herbivores

1. Although both endogenous and exogenous processes regulate populations, the current understanding of the contributions from density dependence and climate to the population dynamics of eruptive herbivores remains limited.

Insect-Borne Plant Pathogens and Their Vectors: Ecology, Evolution, and Complex Interactions

The transmission of insect-borne plant pathogens, including viruses, bacteria, phytoplasmas, and fungi depends upon the abundance and behavior of their vectors. These pathogens should therefore be selected to influence their vectors to enhance their transmission, either indirectly, through the infected host plant, or directly, after acquisition of the pathogen by the vector. Accumulating evidence provides partial support for the occurrence of vector manipulation by plant pathogens, especially for plant viruses, for which a theoretical framework can explain patterns in the specific effects on vector behavior and performance depending on their modes of transmission. The variability in effects of pathogens on their vectors, however, suggests inconsistency in the occurrence of vector manipulation but also may reflect incomplete information about these systems. For example, manipulation can occur through combinations of specific effects, including direct and indirect effects on performance and behavior, and dynamics in those effects with disease progression or pathogen acquisition that together constitute syndromes that promote pathogen spread. Deciphering the prevalence and forms of vector manipulation by plant pathogens remains a compelling field of inquiry, but gaps and opportunities to advance it remain. A proposed research agenda includes examining vector manipulation syndromes comprehensively within pathosystems, expanding the taxonomic and genetic breadth of the systems studied, evaluating dynamic effects that occur during disease progression, incorporating the influence of biotic and abiotic environmental factors, evaluating the effectiveness of putative manipulation syndromes under field conditions, deciphering chemical and molecular mechanisms whereby pathogens can influence vectors, expanding the use of evolutionary and epidemiological models, and seeking opportunities to exploit these effects to improve management of insect-borne, economically important plant pathogens. We expect this field to remain vibrant and productive in its own right and as part of a wider inquiry concerning host and vector manipulation by plant and animal pathogens and parasites.

The Effects of Bean Leafroll Virus on Life History Traits and Host Selection Behavior of Specialized Pea Aphid (Acyrthosiphon pisum, Hemiptera: Aphididae) Genotypes

Abstract Intraspecific specialization by insect herbivores on different host plant species contributes to the formation of genetically distinct “host races,” but the effects of plant virus infection on interactions between specialized herbivores and their host plants have barely been investigated. Using three genetically and phenotypically divergent pea aphid clones (Acyrthosiphon pisum L.) adapted to either pea (Pisum sativum L.) or alfalfa (Medicago sativa L.), we tested how infection of these hosts by an insect-borne phytovirus (Bean leafroll virus; BLRV) affects aphid performance and preference. Four important findings emerged: 1) mean aphid survival rate and intrinsic rate of population growth (R m ) were increased by 15% and 14%, respectively, for aphids feeding on plants infected with BLRV; 2) 34% of variance in survival rate was attributable to clone × host plant interactions; 3) a three-way aphid clone × host plant species × virus treatment significantly affected intrinsic rates of population growth; and 4) each clone exhibited a preference for either pea or alfalfa when choosing between noninfected host plants, but for two of the three clones tested these preferences were modestly reduced when selecting among virus-infected host plants. Our studies show that colonizing BLRV-infected hosts increased A. pisum survival and rates of population growth, confirming that the virus benefits A. pisum. BLRV transmission affected aphid discrimination of host plant species in a genotype-specific fashion, and we detected three unique “virus-association phenotypes,” with potential consequences for patterns of host plant use by aphid populations and crop virus epidemiology.