Indirect plant-mediated interactions between heterospecific parasitoids that develop in different caterpillar species.

Parasitoids induce physiological changes in their herbivorous hosts that affect how plants respond to herbivory. The signature of parasitoids on induced plant responses to feeding by parasitized herbivores indirectly impacts insect communities interacting with the plant. The effect may extend to parasitoids and cause indirect interaction between parasitoids that develop inside different herbivore hosts sharing the food plant. However, this type of interactions among parasitoid larvae has received very little attention. In this study, we investigated sequential and simultaneous plant-mediated interactions among two host-parasitoid systems feeding on Brassica oleracea plants: Mamestra brassicae parasitized by Microplitis mediator and Pieris rapae parasitized by Cotesia rubecula. We measured the mortality, development time, and weight of unparasitized herbivores and performance of parasitoids that had developed inside the two herbivore species when sharing the food plant either simultaneously or sequentially. Plant induction by parasitized or unparasitized hosts had no significant effect on the performance of the two herbivore host species. In contrast, the two parasitoid species had asymmetrical indirect plant-mediated effects on each other's performance. Cotesia rubecula weight was 15% higher on plants induced by M. mediator-parasitized hosts, compared to control plants. In addition, M. mediator development time was reduced by 30% on plants induced by conspecific but not heterospecific parasitoids, compared to plants induced by its unparasitized host. Contrary to sequential feeding, parasitoids had no effect on each other's performance when feeding simultaneously. These results reveal that indirect plant-mediated interactions among parasitoid larvae could involve any parasitoid species whose hosts share a food plant.

Bringing Fundamental Insights of Induced Resistance to Agricultural Management of Herbivore Pests.

In response to herbivory, most plant species adjust their chemical and morphological phenotype to acquire induced resistance to the attacking herbivore. Induced resistance may be an optimal defence strategy that allows plants to reduce metabolic costs of resistance in the absence of herbivores, allocate resistance to the most valuable plant tissues and tailor its response to the pattern of attack by multiple herbivore species. Moreover, plasticity in resistance decreases the potential that herbivores adapt to specific plant resistance traits and need to deal with a moving target of variable plant quality. Induced resistance additionally allows plants to provide information to other community members to attract natural enemies of its herbivore attacker or inform related neighbouring plants of pending herbivore attack. Despite the clear evolutionary benefits of induced resistance in plants, crop protection strategies to herbivore pests have not exploited the full potential of induced resistance for agriculture. Here, we present evidence that induced resistance offers strong potential to enhance resistance and resilience of crops to (multi-) herbivore attack. Specifically, induced resistance promotes plant plasticity to cope with multiple herbivore species by plasticity in growth and resistance, maximizes biological control by attracting natural enemies and, enhances associational resistance of the plant stand in favour of yield. Induced resistance may be further harnessed by soil quality, microbial communities and associational resistance offered by crop mixtures. In the transition to more sustainable ecology-based cropping systems that have strongly reduced pesticide and fertilizer input, induced resistance may prove to be an invaluable trait in breeding for crop resilience.

Role of cyanogenic glycosides in the seeds of wild lima bean, Phaseolus lunatus: defense, plant nutrition or both?

MAIN CONCLUSION: Cyanogenic glycosides present in the seeds of wild lima bean plants are associated with seedling defense but do not affect seed germination and seedling growth. Wild lima bean plants contain cyanogenic glycosides (CNGs) that are known to defend the plant against leaf herbivores. However, seed feeders appear to be unaffected despite the high levels of CNGs in the seeds. We investigated a possible role of CNGs in seeds as nitrogen storage compounds that influence plant growth, as well as seedling resistance to herbivores. Using seeds from four different wild lima bean natural populations that are known to vary in CNG levels, we tested two non-mutually exclusive hypotheses: (1) seeds with higher levels of CNGs produce seedlings that are more resistant against generalist herbivores and, (2) seeds with higher levels of CNGs germinate faster and produce plants that exhibit better growth. Levels of CNGs in the seeds were negatively correlated with germination rates and not correlated with seedling growth. However, levels of CNGs increased significantly soon after germination and seeds with the highest CNG levels produced seedlings with higher CNG levels in cotyledons. Moreover, the growth rate of the generalist herbivore Spodoptera littoralis was lower in cotyledons with high-CNG levels. We conclude that CNGs in lima bean seeds do not play a role in seed germination and seedling growth, but are associated with seedling defense. Our results provide insight into the potential dual function of plant secondary metabolites as defense compounds and storage molecules for growth and development.

Changes in plant growth and seed production in wild lima bean in response to herbivory are attenuated by parasitoids.

Lima bean plants (Phaseolus lunatus) exhibit compensatory growth responses to herbivory. Among the various factors that have been identified to affect plant compensatory growth are the extent and type of tissue damage, the herbivore's feeding mode and the time of damage. Another factor that can greatly impact plant responses to herbivory, but has been largely ignored in previous studies, is the action of parasitoids. In most cases, parasitoids halt or slow down the development of herbivorous hosts, which, can result in decreased leaf damage, thereby affecting plant responses and ultimately plant fitness. Here, we investigated the effects of two koinobiont parasitoids on the amount of leaf damage inflicted by the Southern armyworm Spodoptera latifascia to wild lima bean, and the consequences of this for plant growth and seed production in the field. We specifically tested the hypothesis that the action of parasitoids will reduce plant damage and that this reduction will alter plant growth responses and seed production. Indeed, we found that in the presence of parasitoids plants suffered less damage than plants with only herbivores. As a consequence, compensatory growth was reduced and more and heavier seeds were produced earlier in the season, compared to plants exposed to only herbivores.

Specificity of induced defenses, growth, and reproduction in lima bean (Phaseolus lunatus) in response to multispecies herbivory.

UNLABELLED: • PREMISE OF THE STUDY: Following herbivore attack, plants can either reduce damage by inducing defenses or mitigate herbivory effects through compensatory growth and reproduction. It is increasingly recognized that such induced defenses in plants are herbivore-specific, but less is known about the specificity of compensatory responses. Damage by multiple herbivores may also lead to synergistic effects on induction and plant fitness that differ from those caused by a single herbivore species. Although largely unstudied, the order of arrival and damage by different herbivore species might also play an important role in the impacts of herbivory on plants.• METHODS: We investigated the specificity of defense induction (phenolics) and effects on growth (number of stems and leaves) and reproduction (number of seeds, seed mass, and germination rate) from feeding by two generalist leaf-chewing herbivores (Spodoptera eridania and Diabrotica balteata) on Phaseolus lunatus plants and evaluated whether simultaneous attack by both herbivores and their order of arrival influenced such dynamics.• KEY RESULTS: Herbivory increased levels of leaf phenolics, but such effects were not herbivore-specific. In contrast, herbivory enhanced seed germination in an herbivore-specific manner. For all variables measured, the combined effects of both herbivore species did not differ from their individual effects. Finally, the order of herbivore arrival did not influence defense induction, plant growth, or seed number but did influence seed mass and germination.• CONCLUSIONS: Overall, this study highlights novel aspects of the specificity of plant responses induced by damage from multiple species of herbivores and uniquely associates such effects with plant lifetime fitness.

Evolution of koinobiont parasitoid host regulation and consequences for indirect plant defence.

Tritrophic interactions among plants, herbivorous insects and their parasitoids have been well studied in the past four decades. Recently, a new angle has been uncovered: koinobiont parasitoids, that allow their host to keep feeding on the plant for a certain amount of time after parasitism, indirectly alter plant responses against herbivory via the many physiological changes induced in their herbivorous hosts. By affecting plant responses, parasitoids may indirectly affect the whole community of insects interacting with plants induced by parasitized herbivores and have extended effects on plant fitness. These important findings have renewed research interests on parasitoid manipulation of their host development. Parasitoids typically arrest their host development before the last instar, resulting in a lower final weight compared to unparasitized hosts. Yet, some parasitoids prolong their host development, leading to larger herbivores that consume more plant material than unparasitized ones. Furthermore, parasitoid host regulation is plastic and one parasitoid species may arrest or promote its host growth depending on the number of eggs laid, host developmental stage and species as well as environmental conditions. The consequences of plasticity in parasitoid host regulation for plant-insect interactions have received very little attention over the last two decades, particularly concerning parasitoids that promote their host growth. In this review, we first synthesize the mechanisms used by parasitoids to regulate host growth and food consumption. Then, we identify the evolutionary and environmental factors that influence the direction of parasitoid host regulation in terms of arrestment or promotion of host growth. In addition, we discuss the implication of different host regulation types for the parasitoid's role as agent of plant indirect defence. Finally, we argue that the recent research interests about parasitoid plant-mediated interactions would strongly benefit from revival of research on the mechanisms, ecology and evolution of host regulation in parasitoids.

Host density and parasitoid presence interact and shape the outcome of a tritrophic interaction on seeds of wild lima bean.

The interaction between the seed beetle Zabrotes subfasciatus and its parasitoid Stenocorse bruchivora, was investigated on seeds of two populations of wild lima bean, Phaseolus lunatus. By manipulating the number of beetle larvae per seed and the presence of parasitoids, we determined how factors related to beetle larvae density, the seed in which they feed and the parasitoid, may interact and affect host and parasitoid survival. Results showed that an increase in larval beetle density had a negative impact on beetle performance. This effect cascaded up to parasitoids, high larval density strongly reduced parasitoid emergence. Also, parasitoid presence resulted in faster beetle development and lower female weight. An interactive effect between larval host density and parasitoid presence affected the number of insects that emerged from the seeds. Beetle performance was better in the bean population with the largest seeds, while parasitoid emergence was the lowest in these seeds. This study shows that the impact of parasitoids on seed beetles is contingent on the interaction between density-mediated (direct mortality) and trait-mediated (e.g. non-consumptive) effects. Indirect trait-mediated effects of natural enemies are likely prevalent across insect communities, understanding their role in driving host-parasitoid interactions can have important implications for biological control.