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.

Both consumptive and non-consumptive effects of predators impact mosquito populations and have implications for disease transmission.

Predator-prey interactions influence prey traits through both consumptive and non-consumptive effects, and variation in these traits can shape vector-borne disease dynamics. Meta-analysis methods were employed to generate predation effect sizes by different categories of predators and mosquito prey. This analysis showed that multiple families of aquatic predators are effective in consumptively reducing mosquito survival, and that the survival of Aedes, Anopheles, and Culex mosquitoes is negatively impacted by consumptive effects of predators. Mosquito larval size was found to play a more important role in explaining the heterogeneity of consumptive effects from predators than mosquito genus. Mosquito survival and body size were reduced by non-consumptive effects of predators, but development time was not significantly impacted. In addition, Culex vectors demonstrated predator avoidance behavior during oviposition. The results of this meta-analysis suggest that predators limit disease transmission by reducing both vector survival and vector size, and that associations between drought and human West Nile virus cases could be driven by the vector behavior of predator avoidance during oviposition. These findings are likely to be useful to infectious disease modelers who rely on vector traits as predictors of transmission.

Mosquitoes are often referred to as the deadliest animals on earth because some species spread malaria, West Nile virus or other dangerous diseases when they bite humans and other animals. Adult mosquitoes fly to streams, ponds and other freshwater environments to lay their eggs. When the eggs hatch, the young mosquitoes live in the water until they are ready to grow wings and transform into adults. In the water, the young mosquitoes are particularly vulnerable to being eaten by dragonfly larvae, fish and other predators. When adult females are choosing where to lay their eggs, they can use their sense of smell to detect these predators and attempt to avoid them. Along with eating the mosquitoes, the predators may also reduce mosquito populations in other ways. For example, predators can disrupt feeding among young mosquitoes, which may affect the time that it takes for them to grow into adults or the size of their bodies once they reach the adult stage. Although the impacts of different predators have been tested separately in multiple settings, the overall effects of predators on the ability of mosquitoes to spread diseases to humans remain unclear. To address this question, Russell, Herzog et al. used an approach called meta-analysis on data from previous studies. The analysis found that along with increasing the death rates of mosquitoes, the presence of predators also leads to a reduction in the body size of those mosquitoes that survive, causing them to have shorter lifespans and fewer offspring. Russell, Herzog et al. found that one type of mosquito known as Culex ­ which carries West Nile virus ­ avoided laying its eggs near predators. During droughts, increased predation in streams, ponds and other aquatic environments may lead adult female Culex mosquitoes to lay their eggs closer to residential areas with fewer predators. Russell, Herzog et al. propose that this may be one reason why outbreaks of West Nile virus in humans are more likely to occur during droughts. In the future, these findings may help researchers to predict outbreaks of West Nile virus, malaria and other diseases carried by mosquitoes more accurately. Furthermore, the work of Russell, Herzog et al. provides examples of mosquito predators that could be used as biocontrol agents to decrease numbers of mosquitoes in certain regions.

Predation risk differentially affects aphid morphotypes: impacts on prey behavior, fecundity and transgenerational dispersal morphology.

To avoid predation, prey initiate anti-predator defenses such as altered behavior, physiology and/or morphology. Prey trait changes in response to perceived predation risk can influence several aspects of prey biology that collectively contribute to individual success and thus population growth. However, studies often focus on single trait changes in a discrete life stage or morphotype. We assessed how predation risk by Harmonia axyridis affects several important traits in the aphid, Myzus persicae: host plant preference, fecundity and investment in dispersal. Importantly, we examined whether these traits changed in a similar way between winged (alate) and wingless (apterous) adult aphid morphotypes, which differ in morphology, but also in life-history characteristics important for reproduction and dispersal. Host plant preference was influenced by the presence of H.axyridis odors in choice tests; wingless aphids were deterred by the odor of plants with H.axyridis whereas winged aphids preferred plants with H.axyridis present. Wingless aphids reared in the presence of ladybeetle cues produced fewer offspring in the short-term, but significantly more when reared with exposure to predator cues for multiple generations. However, winged aphid fecundity was unaffected by H.axyridis cues. Lastly, transgenerational plasticity was demonstrated in response to predation risk via increased formation of winged aphid morphotypes in the offspring of predator cue-exposed wingless mothers. Importantly, we found that responses to risk differ across aphid polyphenism and that plasticity in aphid morphology occurs in response to predation risk. Together our results highlight the importance of considering how predation risk affects multiple life stages and morphotypes.

Predators of monarch butterfly eggs and neonate larvae are more diverse than previously recognised.

Conserving threatened organisms requires knowledge of the factors impacting their populations. The Eastern monarch butterfly (Danaus plexippus L.) has declined by as much as 80% in the past two decades and conservation biologists are actively seeking to understand and reverse this decline. While it is well known that most monarchs die as eggs and young larvae, few studies have focused on identifying what arthropod taxa contribute to these losses. The aim of our study was to identify previously undocumented predators of immature monarchs in their summer breeding range in the United States. Using no-choice feeding assays augmented with field observations, we evaluated 75 arthropod taxa commonly found on the primary host plant for their propensity to consume immature monarchs. Here we report 36 previously unreported monarch predators, including representatives from 4 new orders (Orthoptera, Dermaptera, Lepidoptera and Opiliones) and 11 taxa (Acrididae, Gryllidae, Tettigoniidae, Forficulidae, Anthocoridae, Geocoridae, Lygaeidae, Miridae, Nabidae, Erebidae and Opilliones). Surprisingly, several putative herbivores were found to readily consume immature monarchs, both in a targeted fashion or incidentally as a result of herbivory. This work expands our understanding of the monarch predator community and highlights the importance of unrecognized predation on insects of conservation concern.

The effect of predator presence on the behavioral sequence from host selection to reproduction in an invulnerable stage of insect prey.

Predator-prey interactions primarily focus on prey life-stages that are consumed. However, animals in less vulnerable life-stages might also be influenced by the presence of a predator, making our understanding of predation-related impacts across all life-stages of prey essential. It has been previously demonstrated that Podisus maculiventris is a voracious predator of eggs and larvae of Leptinotarsa decemlineata, and that larvae will alter their behavior to avoid predation. However, the adult beetles are not readily consumed by P. maculiventris, raising the question of whether they will respond to predators to protect themselves or their offspring. Here, we examine the effect of predation risk by P. maculiventris, on three adult behaviors of L. decemlineata; colonization, oviposition, and feeding, and the resulting impact on host plant damage. In an open-field test, there was no difference in natural beetle colonization between plots with predation risk and control treatments. However, subsequent host plant damage by adult beetles was 63.9% less in predation risk treatments. Over the lifetime of adult beetles in field mesocosms, per capita feeding was 23% less in the predation risk treatment. Beetle oviposition was 37% less in the presence of predators in a short-term, greenhouse assay, and marginally reduced in longer term field mesocosms. Our results indicate that predation risk can drive relatively invulnerable adult herbivores to adjust behaviors that affect themselves (feeding) and their offspring (oviposition). Thus, the full impact of predator presence must be considered across the prey life cycle.

Scaling up our understanding of non-consumptive effects in insect systems.

Non-consumptive effects (NCEs) of predators on prey is an important topic in insect ecology with potential applications for pest management. NCEs are changes in prey behavior and physiology that aid in predation avoidance. While NCEs can have positive outcomes for prey survival there may also be negative consequences including increased stress and reduced growth. These effects can cascade through trophic systems influencing ecosystem function. Most NCEs have been studied at small spatial and temporal scales. However, recent studies show promise for the potential to manipulate NCEs for pest management. We suggest the next frontier for NCE studies includes manipulating the landscape of fear to improve pest control, which requires scaling-up to field and landscape levels, over ecologically relevant time frames.

Thermally moderated firefly activity is delayed by precipitation extremes.

The timing of events in the life history of temperate insects is most typically primarily cued by one of two drivers: photoperiod or temperature accumulation over the growing season. However, an insect's phenology can also be moderated by other drivers like rainfall or the phenology of its host plants. When multiple drivers of phenology interact, there is greater potential for phenological asynchronies to arise between an organism and those with which it interacts. We examined the phenological patterns of a highly seasonal group of fireflies (Photinus spp., predominantly P. pyralis) over a 12-year period (2004-2015) across 10 plant communities to determine whether interacting drivers could explain the variability observed in the adult flight activity density (i.e. mating season) of this species. We found that temperature accumulation was the primary driver of phenology, with activity peaks usually occurring at a temperature accumulation of approximately 800 degree days (base 10°C); however, our model found this peak varied by nearly 180 degree-day units among years. This variation could be explained by a quadratic relationship with the accumulation of precipitation in the growing season; in years with either high or low precipitation extremes at our study site, flight activity was delayed. More fireflies were captured in general in herbaceous plant communities with minimal soil disturbance (alfalfa and no-till field crop rotations), but only weak interactions occurred between within-season responses to climatic variables and plant community. The interaction we observed between temperature and precipitation accumulation suggests that, although climate warming has the potential to disrupt phenology of many organisms, changes to regional precipitation patterns can magnify these disruptions.

Host genetic determinants of microbiota-dependent nutrition revealed by genome-wide analysis of Drosophila melanogaster.

Animals bear communities of gut microorganisms with substantial effects on animal nutrition, but the host genetic basis of these effects is unknown. Here we use Drosophila to demonstrate substantial among-genotype variation in the effects of eliminating the gut microbiota on five host nutritional indices (weight, protein, lipid, glucose and glycogen contents); this includes variation in both the magnitude and direction of microbiota-dependent effects. Genome-wide association studies to identify the genetic basis of the microbiota-dependent variation reveal polymorphisms in largely non-overlapping sets of genes associated with variation in the nutritional traits, including strong representation of conserved genes functioning in signalling. Key genes identified by the GWA study are validated by loss-of-function mutations that altered microbiota-dependent nutritional effects. We conclude that the microbiota interacts with the animal at multiple points in the signalling and regulatory networks that determine animal nutrition. These interactions with the microbiota are probably conserved across animals, including humans.

Prey perception of predation risk: volatile chemical cues mediate non-consumptive effects of a predator on a herbivorous insect.

Predators can affect prey in two ways-by reducing their density (consumptive effects) or by changing their behavior, physiology or other phenotypic traits (non-consumptive effects). Understanding the cues and sensory modalities prey use to detect predators is critical for predicting the strength of non-consumptive effects and the outcome of predator-prey encounters. While predator-associated cues have been well studied in aquatic systems, less is known about how terrestrial prey, particularly insect larvae, detect their predators. We evaluated how Colorado potato beetle, Leptinotarsa decemlineata, larvae perceive predation risk by isolating cues from its stink bug predator, the spined soldier bug, Podisus maculiventris. When exposed to male "risk" predators that were surgically manipulated so they could hunt but not kill, beetles reduced feeding 29% compared to controls. Exposure to risk females caused an intermediate response. Beetles ate 24% less on leaves pre-exposed to predators compared to leaves never exposed to predators, indicating that tactile and visual cues are not required for the prey's response. Volatile odor cues from predators reduced beetle feeding by 10% overall, although male predators caused a stronger reduction than females. Finally, visual cues from the predator had a weak effect on beetle feeding. Because multiple cues appear to be involved in prey perception of risk, and because male and female predators have differential effects, beetle larvae likely experience tremendous variation in the information about risk from their local environment.

Induced release of a plant-defense volatile 'deceptively' attracts insect vectors to plants infected with a bacterial pathogen.

Transmission of plant pathogens by insect vectors is a complex biological process involving interactions between the plant, insect, and pathogen. Pathogen-induced plant responses can include changes in volatile and nonvolatile secondary metabolites as well as major plant nutrients. Experiments were conducted to understand how a plant pathogenic bacterium, Candidatus Liberibacter asiaticus (Las), affects host preference behavior of its psyllid (Diaphorina citri Kuwayama) vector. D. citri were attracted to volatiles from pathogen-infected plants more than to those from non-infected counterparts. Las-infected plants were more attractive to D. citri adults than non-infected plants initially; however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Experiments with Las-infected and non-infected plants under complete darkness yielded similar results to those recorded under light. The behavior of psyllids in response to infected versus non-infected plants was not influenced by whether or not they were carriers of the pathogen. Quantification of volatile release from non-infected and infected plants supported the hypothesis that odorants mediate psyllid preference. Significantly more methyl salicylate, yet less methyl anthranilate and D-limonene, was released by infected than non-infected plants. Methyl salicylate was attractive to psyllids, while methyl anthranilate did not affect their behavior. Feeding on citrus by D. citri adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants. Infected plants were characterized by lower levels of nitrogen, phosphorus, sulfur, zinc, and iron, as well as, higher levels of potassium and boron than non-infected plants. Collectively, our results suggest that host selection behavior of D. citri may be modified by bacterial infection of plants, which alters release of specific headspace volatiles and plant nutritional contents. Furthermore, we show in a laboratory setting that this apparent pathogen-mediated manipulation of vector behavior may facilitate pathogen spread.

Sexual transmission of a plant pathogenic bacterium, Candidatus Liberibacter asiaticus, between conspecific insect vectors during mating.

Candidatus Liberibacter asiaticus is a fastidious, phloem-inhabiting, gram-negative bacterium transmitted by Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae). The bacterium is the presumed causal agent of huanglongbing (HLB), one of the most destructive and economically important diseases of citrus. We investigated whether Las is transmitted between infected and uninfected D. citri adults during courtship. Our results indicate that Las was sexually transmitted from Las-infected male D. citri to uninfected females at a low rate (<4%) during mating. Sexual transmission was not observed following mating of infected females and uninfected males or among adult pairs of the same sex. Las was detected in genitalia of both sexes and also in eggs of infected females. A latent period of 7 days or more was required to detect the bacterium in recipient females. Rod shaped as well as spherical structures resembling Las were observed in ovaries of Las-infected females with transmission electron microscopy, but were absent in ovaries from uninfected D. citri females. The size of the rod shaped structures varied from 0.39 to 0.67 µm in length and 0.19 to 0.39 µm in width. The spherical structures measured from 0.61 to 0.80 µm in diameter. This investigation provides convincing evidence that a plant pathogenic bacterium is sexually transmitted from male to female insects during courtship and established evidence that bacteria persist in reproductive organs. Moreover, these findings provide an alternative sexually horizontal mechanism for the spread of Las within populations of D. citri, even in the absence of infected host trees.