Paul J. Ode

Plant chemical defenses are known to influence herbivore performance, yet their effects on herbivore immunity are poorly understood. In this study, we manipulated both the mean and variance of the concentration of a plant toxin in an artificial diet to assess the effects on herbivore immune function and survival. Our results revealed a biphasic immune response across increasing mean toxin concentrations, with exposure to low toxin concentrations enhancing immune function, creating a ‘window of enhanced immunity’, and exposure to higher concentrations suppressing it relative to toxin-free diets. Encountering variable toxin levels may alter this relationship by mixing toxin levels from within and outside this window. Importantly, we found that when the mean toxin concentration is just outside of the window of enhanced immunity, exposure to low variability in toxin concentrations enhanced herbivore immunocompetence compared to when they were exposed to high or no variation. Elevated immunity correlated with increased survival under pathogen challenge.

In the years immediately following its introduction in 1986, the Russian wheat aphid Diuraphis noxia (Kurdjumov) became a significant pest of wheat in the western United States. In recent years, however, there have been few reports of economically damaging populations and lower numbers of Russian wheat aphid collected in suction traps. Here, we present evidence that the existing natural enemy complex may significantly reduce Russian wheat aphid populations even if no single species can be shown to be highly effective. In this study, we used 3 exclusion cage treatments (fully caged, partially caged, and uncaged plots) to explore the effects of the existing natural enemy complex on Russian wheat aphid populations in winter wheat in 3 fields across a north–south gradient in eastern Colorado: Fort Collins (northeastern Colorado), Akron (eastern Colorado), and Lamar (southeastern Colorado). Natural enemies were collected and identified. Fewer aphids and symptomatic wheat tillers were found in the uncaged treatment and partially caged treatments than in the caged treatment, which excluded the possibility of natural enemy attack on aphids, suggesting that natural enemies were responsible for suppressing Russian aphid populations in the open cage treatments. Predators were collected on both early and later growth stages of wheat, whereas parasitoids were found only on the later growth stage. Together, these findings suggest that the natural enemy complex is responsible for reducing Russian wheat aphid abundance among different dryland agroecosystems and climatic conditions.

Many parasitoids increase plant fitness by decreasing herbivore feeding damage. Solitary parasitoids (where only one individual completes development per host) generally cause their hosts to feed less than unparasitized herbivores, reducing pressure on plants to induce chemical defense production. However, gregarious parasitoids (where more than one individual develops per host) can cause their hosts to feed more than unparasitized herbivores, which should then also induce greater defense chemistry. Yet, it is unclear whether differential induction effects are primarily due to differences in feeding amount or parasitoid identity. We explored the relationship between plant defense induction and caterpillars parasitized by a solitary versus a gregarious parasitoid. We wanted to determine whether: 1) caterpillars parasitized by a gregarious parasitoid induced higher concentrations of chemical defense and 2) differential responses to feeding by herbivores parasitized by different parasitoids were based on differences in the amount of feeding damage or the identity of parasitoids developing within the parasitized caterpillars. We measured the induction of glucosinolate defenses in Brassica rapa using Pieris rapae caterpillars of equivalent size and development stage parasitized by either a solitary ( Cotesia rubecula ) or a gregarious ( C. glomerata ) parasitoid. We demonstrate that C. glomerata ‐parasitized P. rapae elicit an increase in glucosinolate production independent of the amount of feeding damage, suggesting qualitative rather than quantitative differences in feeding damage are responsible for the observed patterns. Furthermore, gregarious parasitoid broods were reduced when their hosts fed on plants with higher glucosinolate concentrations, indicating the potential of glucosinolates to reduce brood size and potentially feeding damage by the host. Our results indicate that plants can differentially induce chemical defenses in response to the identity of a parasitoid inside an herbivore and demonstrate the importance of parasitoid identity in determining plant defense expression.

Patterns of phytochemistry localisation in plant tissues are diverse within and across leaves. These spatial heterogeneities are important to the fitness of herbivores, but their effects on herbivore foraging and dietary experience remain elusive. We manipulated the spatial variance and clusteredness of a plant toxin in a synthetic diet landscape on which individual caterpillars fed. We monitored caterpillars with cameras across most of their larval development. Caterpillars that fed on diets with a lower spatial variance and more clustered arrangement of toxins had overall worse performance, mostly because those caterpillars ate less, moved more, ingested more toxin, or failed to physiologically acclimate. Using empirically parameterised individual‐based models, we found that differences in movement away from, not towards, less toxic food drove a body size‐dependent effect of clusteredness. Hence, the spatial pattern of phytochemicals itself, beyond mean concentration, can have important consequences for herbivores through complex interactions with herbivore foraging.

Parasitoid wasp larvae engage in intense interspecific competition when sharing a host insect, with lethal consequences for the losers. Larval parasitoid competition is generally thought to be resolved by physical traits, such as enlarged mandibles. Although solitary parasitoid larvae are typically superior competitors against gregarious larvae, such physical traits are unlikely to be effective against large numbers of competitors. Larval competition may instead be mediated by maternal factors that increase the survival of offspring facing interspecific competition, thus increasing parental fitness. When laying eggs inside a host, many female parasitoids also inject oviposition fluids that are known to suppress host immune responses, permitting successful offspring development. We explored whether the oviposition fluids of two wasp species in the genus Cotesia ( Cotesia rubecula, a strong competitor that almost always wins interspecific competition against a weaker competitor, Cotesia glomerata ) might also represent maternal factors that improve the interspecific competitive ability of their offspring. We demonstrate that injections of both venom and calyx fluid from C. rubecula can inhibit egg hatching and larval development of C. glomerata . Venom from C. rubecula decreased C. glomerata egg development by 2.7 times, and calyx fluid injections caused deformities in 23% of developing C. glomerata. In contrast, reciprocal injections of the oviposition fluids from C. glomerata did not inhibit the development of C. rubecula . Our results show that maternal factors can improve the interspecific competitive ability of parasitoid larvae, challenging the previous assumptions that larval competition was resolved primarily through physical combat or larval secretions.

Insect herbivores frequently encounter plant defense molecules, but the physiological and ecological consequences for their immune systems are not fully understood. The majority of studies attempting to relate levels of plant defensive chemistry to herbivore immune responses have used natural population or species-level variation in plant defensive chemistry. Yet, this potentially confounds the effects of plant defense chemistry with other potential plant trait differences that may affect the expression of herbivore immunity. We used an artificial diet containing known quantities of a plant toxin (4-methylsulfinylbutyl isothiocyanate; 4MSOB-ITC or ITC, a breakdown product of the glucosinolate glucoraphanin upon herbivory) to explicitly explore the effects of a plant toxin on the cellular and humoral immune responses of the generalist herbivore Trichoplusia ni (Lepidoptera: Noctuidae) that frequently feeds on glucosinolate-containing plants. Caterpillars feeding on diets with high concentrations of ITC experienced reduced survivorship and growth rates. High concentrations of ITC suppressed the appearance of several types of hemocytes and melanization activity, which are critical defenses against parasitic Hymenoptera and microbial pathogens. In terms of T. ni humoral immunity, only the antimicrobial peptide (AMP) genes lebocin and gallerimycin were significantly upregulated in caterpillars fed on diets containing high levels of ITC relative to caterpillars that were provided with ITC-free diet. Surprisingly, challenging caterpillars with a non-pathogenic strain of Escherichia coli resulted in the upregulation of the AMP gene cecropin. Feeding on high concentrations of plant toxins hindered caterpillar development, decreased cellular immunity, but conferred mixed effects on humoral immunity. Our findings provide novel insights into the effects of herbivore diet composition on insect performance demonstrating the role of specific plant defense toxins that shape herbivore immunity and trophic interactions.