Chemical ecology in conservation biocontrol: new perspectives for plant protection.

Threats to food security require novel sustainable agriculture practices to manage insect pests. One strategy is conservation biological control (CBC), which relies on pest control services provided by local populations of arthropod natural enemies. Research has explored manipulative use of chemical information from plants and insects that act as attractant cues for natural enemies (predators and parasitoids) and repellents of pests. In this review, we reflect on past strategies using chemical ecology in CBC, such as herbivore-induced plant volatiles and the push-pull technique, and propose future directions, including leveraging induced plant defenses in crop plants, repellent insect-based signaling, and genetically engineered crops. Further, we discuss how climate change may disrupt CBC and stress the importance of context dependency and yield outcomes.

Deciphering Plant-Insect-Microorganism Signals for Sustainable Crop Production.

Agricultural crop productivity relies on the application of chemical pesticides to reduce pest and pathogen damage. However, chemical pesticides also pose a range of ecological, environmental and economic penalties. This includes the development of pesticide resistance by insect pests and pathogens, rendering pesticides less effective. Alternative sustainable crop protection tools should therefore be considered. Semiochemicals are signalling molecules produced by organisms, including plants, microbes, and animals, which cause behavioural or developmental changes in receiving organisms. Manipulating semiochemicals could provide a more sustainable approach to the management of insect pests and pathogens across crops. Here, we review the role of semiochemicals in the interaction between plants, insects and microbes, including examples of how they have been applied to agricultural systems. We highlight future research priorities to be considered for semiochemicals to be credible alternatives to the application of chemical pesticides.

Water availability and plant-herbivore interactions.

Water is essential to plant growth and drives plant evolution and interactions with other organisms such as herbivores. However, water availability fluctuates, and these fluctuations are intensified by climate change. How plant water availability influences plant-herbivore interactions in the future is an important question in basic and applied ecology. Here we summarize and synthesize the recent discoveries on the impact of water availability on plant antiherbivore defense ecology and the underlying physiological processes. Water deficit tends to enhance plant resistance and escape traits (i.e. early phenology) against herbivory but negatively affects other defense strategies, including indirect defense and tolerance. However, exceptions are sometimes observed in specific plant-herbivore species pairs. We discuss the effect of water availability on species interactions associated with plants and herbivores from individual to community levels and how these interactions drive plant evolution. Although water stress and many other abiotic stresses are predicted to increase in intensity and frequency due to climate change, we identify a significant lack of study on the interactive impact of additional abiotic stressors on water-plant-herbivore interactions. This review summarizes critical knowledge gaps and informs possible future research directions in water-plant-herbivore interactions.

Effects of Plant Stress on Aphid-Parasitoid Interactions: Drought Improves Aphid Suppression.

Drought events have the potential to mediate tri-trophic interactions. Changes in plant quality influence herbivore performance, which affects prey availability and quality for natural enemies. Parasitoid wasps are particularly vulnerable to these changes since their development is inextricably linked to that of their prey. However, we know little about the indirect effects of plant water limitation on parasitoid performance, especially the consequences of mild water limitation. This study investigated the ability of a parasitoid wasp (Aphidius colemani Viereck (Hymenoptera: Braconidae)) to suppress aphid (Rhopalosiphum padi L. (Hemiptera: Aphididae)) populations on well-watered, mildly stressed, or highly stressed wheat (Triticum aestivum L. (Poales: Poaceae)). We then investigated the role that aphid body size and behavioral interactions might play in wasp acceptance of aphid hosts. We found improved aphid suppression under mild and high-water limitation, but the underlying mechanisms were different. Mild-stress appeared to maximize parasitoid performance, as indicated by the highest mummy production. Aphids were larger when feeding on mildly stressed plants than on any other treatment, which suggests improved aphid quality for parasitoids. Improved aphid suppression under high-stress may have been driven by enhanced nonconsumptive effects. Despite improved aphid suppression, mummy formation was lowest on highly stressed plants. High-stress conditions have been shown to negatively affect aphid performance, so improved aphid suppression may be driven by poor aphid performance exacerbating the cost of interactions with parasitoids, such as stinging. No differences were observed in parasitoid foraging behaviors such as antennation or stinging across any treatments. This study highlights the importance of plant water stress intensity in affecting outcomes of parasitoid-host interactions.

Primacy of plants in driving the response of arthropod communities to drought.

Drought threatens arthropod communities worldwide. Water limitation affects the quantity and quality of plants available to herbivores as food, and can also affect higher trophic-level consumers through variability in prey quality and reduced availability of suitable habitats. Our study assessed the response of an arthropod community to water limited wheat (Triticum aestivum L.) in a field setting. We used rainout shelters to exclude precipitation, irrigated raised bed plots to create three levels of water availability, and monitored arthropod community development over 8 weeks. First, we compared arthropod communities in habitats with different levels of water limitation and found that community composition was reliant on the magnitude of the water stress. This difference was largely due to the loss of piercing-sucking herbivores and predators in high-stress environments. Next, we focused on aphids and their natural enemies to investigate the underlying mechanisms driving community responses using structural equation modeling (SEM). Aphid abundance was negatively affected by water limitation, and this response was primarily associated with stress-induced plant physiological changes and not plant biomass or natural enemy abundance. Natural enemy abundance was also reduced in water-limited habitats, but natural enemies responded to plant biomass and not prey availability. These effects were exacerbated as water stress increased. The absence of natural enemy effects on aphids indicates that top-down predation effects were dampened by strong bottom-up effects of plant water limitation. This study revealed the importance of considering water stress intensity when predicting outcomes of droughts for arthropod communities.

Diurnal feeding as a potential mechanism of osmoregulation in aphids.

Diurnal variation in phloem sap composition has a strong influence on aphid performance. The sugar-rich phloem sap serves as the sole diet for aphids and a suite of physiological mechanisms and behaviors allow them to tolerate the high osmotic stress. Here, we tested the hypothesis that night-time feeding by aphids is a behavior that takes advantage of the low sugar diet in the night to compensate for osmotic stress incurred while feeding on high sugar diet during the day. Using the electrical penetration graph (EPG) technique, we examined the effects of diurnal rhythm on feeding behaviors of bird cherry-oat aphid (Rhopalosiphum padi L.) on wheat. A strong diurnal rhythm in aphids as indicated by the presence of a cyclical pattern of expression in a core clock gene did not impact aphid feeding and similar feeding behaviors were observed during day and night. The major difference observed between day and night feeding was that aphids spent significantly longer time in phloem salivation during the night compared to the day. In contrast, aphid hydration was reduced at the end of the day-time feeding compared to end of the night-time feeding. Gene expression analysis of R. padi osmoregulatory genes indicated that sugar breakdown and water transport into the aphid gut was reduced at night. These data suggest that while diurnal variation occurs in phloem sap composition, aphids use night-time feeding to overcome the high osmotic stress incurred while feeding on sugar-rich phloem sap during the day.