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Dermanyssus gallinae (De Geer 1778), commonly named the poultry red mite (PRM), is considered to be the most harmful ectoparasite in poultry farms in Europe. This species feeds on the blood of laying hens, but spends most of its time hidden in cracks and crevices around hen nests. To control PRM populations in poultry houses, chemical pesticides are currently used; however, concern is growing regarding the harmful residues found in eggs and hens, along with the increased resistance of mites against several compounds. Alternatives to synthetic compounds are now being explored, including vaccines, biological control, physical control and semiochemical control based on the chemical ecology of PRM. This review focused on the different volatile organic compounds (VOCs) identified from D. gallinae and other mite species that have been discovered to control them. Pheromones (aggregation pheromone, sex pheromone and alarm pheromone) and kairomones promoting attraction behaviour in D. gallinae and other mite species are presented, while VOCs from essential oils and plant extracts with repellent properties are also explored. Finally, devices using VOCs on PRM in the field are described, with devices that have been tested on other Acari species being mentioned as potential directions for the future control of PRM.

(E)-β-Farnesene (EβF) is the predominant constituent of the alarm pheromone of most aphid pest species. Moreover, natural enemies of aphids use EβF to locate their aphid prey. Some plant species emit EβF, potentially as a defense against aphids, but field demonstrations are lacking. Here, we present field and laboratory studies of flower defense showing that ladybird beetles are predominantly attracted to young stage-2 pyrethrum flowers that emitted the highest and purest levels of EβF. By contrast, aphids were repelled by EβF emitted by S2 pyrethrum flowers. Although peach aphids can adapt to pyrethrum plants in the laboratory, aphids were not recorded in the field. Pyrethrum’s (E)-β-farnesene synthase (EβFS) gene is strongly expressed in inner cortex tissue surrounding the vascular system of the aphid-preferred flower receptacle and peduncle, leading to elongated cells filled with EβF. Aphids that probe these tissues during settlement encounter and ingest plant EβF, as evidenced by the release in honeydew. These EβF concentrations in honeydew induce aphid alarm responses, suggesting an extra layer of this defense. Collectively, our data elucidate a defensive mimicry in pyrethrum flowers: the developmentally regulated and tissue-specific EβF accumulation and emission both prevents attack by aphids and recruits aphid predators as bodyguards.

Animals use learning and memory to recognise cues that predict rewards or punishments, allowing flexible decision-making. When facing new stimuli, they often generalise – responding similarly to different but related cues – enabling adaptive behaviour despite natural variation. Pheromones, chemical signals central to social interactions, are known to affect learning and memory, but their role in generalisation is unknown. This study explores how formic acid, an alarm pheromone in Camponotus aethiops ants, influences odour discrimination and generalisation in an appetitive olfactory discrimination learning task. Using controlled conditioning, we found that formic acid affected learning asymmetrically: it enhanced discrimination when octanal was rewarded and hexanal punished but not when hexanal was rewarded and octanal punished, suggesting a shift in learning priorities. Unexpectedly, formic acid also increased responses to conditioned stimuli and novel odours but only when octanal was the rewarded stimulus. These findings suggest that formic acid modulates associative learning and generalisation in a context-dependent way. Rather than acting solely as an arousal trigger, formic acid appears to reshape cognitive processing by altering stimulus discrimination and odour sensitivity. This highlights a novel role for alarm pheromones in modulating cognition, with broader implications for understanding chemical communication in social insects and beyond.

Aphids are destructive pests, and alarm pheromones play a key role in their chemical ecology. Here, we conducted a detailed analysis of terpenoids in the vetch aphid, Megoura viciae, and its host plant Pisum sativum using gas chromatography/mass spectrometry. Four major components, (-)-β-pinene (49.74%), (E)-β-farnesene (32.64%), (-)-α-pinene (9.42%) and ( +)-limonene (5.24%), along with trace amounts of ( +)-sabinene, camphene and α-terpineol) (3.14%) were found in the aphid. In contrast, few terpenoids were found in the host plant, consisting mainly of squalene (66.13%) and its analog 2,3-epoxysqualene (31.59%). Quantitative analysis of the four major terpenes in different developmental stages of the aphid showed that amounts of the monoterpenes increased with increasing stage, while the sesquiterpene amount peaked in the 3rd instar. (-)-β-Pinene was the most abundant terpene at all developmental stages. Behavioral assays using a three-compartment olfactometer revealed that the repellency of single compounds varied in a concentration-dependent manner, but two mixtures [(-)-α-pinene: (-)-β-pinene: (E)-β-farnesene: ( +)-limonene = 1:44.4:6.5:2.2 or 1:18.4:1.3:0.8], were repellent at all concentrations tested. Our results suggest that (-)-α-pinene and (-)-β-pinene are the major active components of the alarm pheromone of M. viciae, but that mixtures play a key role in the alarm response. Our study contributes to the understanding of the chemical ecology of aphids and may help design new control strategies against this aphid pest.

Herbivores assess predation risk in their environment by identifying visual, chemical, and tactile predator cues. Detection of predator cues can induce risk-avoidance behaviors in herbivores that affect feeding, dispersal, and host selection in ways that minimize mortality and reproductive costs. For herbivores that transmit plant pathogens, including many aphids, changes in herbivore behavior in response to predator cues may also affect pathogen spread. However, few studies have assessed how aphid behavioral responses to different types of predator cues affect pathogen transmission. Here, we conducted greenhouse experiments to assess whether responses of pea aphids (Acyrthosiphon pisum) to predation risk and alarm pheromone (E-β-Farnesene), an aphid alarm signal released in response to predation risk, affected transmission of Pea enation mosaic virus (PEMV). We exposed A. pisum individuals to risk cues, and quantified viral titer in aphids and pea (Pisum sativum) host plants across several time periods. We also assessed how A. pisum responses to risk cues affected aphid nutrition, reproduction, and host selection. We show that exposure to predator cues and alarm pheromone significantly reduced PEMV acquisition and inoculation. Although vectors avoided hosts with predator cues, predator cues did not alter vector reproduction or reduce nutrient acquisition. Overall, these results suggest that non-consumptive effects of predators may indirectly decrease the spread of plant pathogens by altering vector behavior in ways that reduce vector competence and pathogen transmission efficiency.

Abstract Ants communicate via an arsenal of different pheromones produced in a variety of exocrine glands. For example, ants release alarm pheromones in response to danger to alert their nestmates and to trigger behavioral alarm responses. Here we characterize the alarm pheromone and the alarm response of the clonal raider ant Ooceraea biroi, a species that is amenable to laboratory studies but for which no pheromones have been identified. During an alarm response, ants quickly become unsettled, leave their nest pile, and are sometimes initially attracted to the source of alarm, but ultimately move away from it. We find that the alarm pheromone is released from the head of the ant and identify the putative alarm pheromone as a blend of two compounds found in the head, 4-methyl-3-heptanone and 4-methyl-3-heptanol. These compounds are sufficient to induce alarm behavior alone and in combination. They elicit similar, though slightly different behavioral features of the alarm response, with 4-methyl-3-heptanone being immediately repulsive and 4-methyl-3-heptanol being initially attractive before causing ants to move away. The behavioral response to these compounds in combination is dose-dependent, with ants becoming unsettled and attracted to the source of alarm pheromone at low concentrations and repulsed at high concentrations. While 4-methyl-3-heptanone and 4-methyl-3-heptanol are known alarm pheromones in other more distantly related ant species, this is the first report of the chemical identity of a pheromone in O. biroi, and the first alarm pheromone identified in the genus Ooceraea. Identification of a pheromone that triggers a robust, consistent, and conserved behavior, like the alarm pheromone, provides an avenue to dissect the behavioral and neuronal mechanisms underpinning chemical communication.

The major component of aphid alarm pheromone is ( E )-β-farnesene (EβF), but the molecular mechanisms of EβF synthesis are poorly understood. Here we established a biological model to study the modulation of EβF synthesis in the bird cherry-oat aphid Rhopalosiphum padi by using quantitative polymerase chain reaction, gas chromatography/mass spectrometry and RNA interference. Our results showed that the rearing conditions significantly affected the weight of adult and modulated EβF synthesis in a transgenerational manner. Specifically, the quantity of EβF per milligram of aphid was significantly reduced in the individually reared adult or 1st-instar nymphs derived from 1-day-old adult reared individually, but EβF in the nymph derived from 2-day-old adult that experienced collective conditions returned to normal. Further study revealed that the production of EβF started in embryo and was extended to early nymphal stage, which was modulated by farnesyl diphosphate synthase genes ( RpFPPS1 and RpFPPS2 ) and rearing conditions. Knockdown of RpFPPS1 and RpFPPS2 confirmed the role played by FPPS in the biosynthesis of aphid alarm pheromone. Our results suggested that the production of EβF starts at the embryo stage and is modulated by FPPS and rearing conditions in R . padi , which sheds lights on the modulatory mechanisms of EβF in the aphid.

Aphids use an alarm pheromone, E-β farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not , a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.

Main conclusionIn flowers multiple secretory systems cooperate to deliver specialized metabolites to support specific roles in defence and pollination. The collective roles of cell types, enzymes, and transporters are discussed.The interplay between reproductive strategies and defense mechanisms in flowering plants has long been recognized, with trade-offs between investment in defense and reproduction predicted. Glandular trichomes and secretory cavities or ducts, which are epidermal and internal structures, play a pivotal role in the secretion, accumulation, and transport of specialized secondary metabolites, and contribute significantly to defense and pollination. Recent investigations have revealed an intricate connection between these two structures, whereby specialized volatile and non-volatile metabolites are exchanged, collectively shaping their respective ecological functions. However, a comprehensive understanding of this profound integration remains largely elusive. In this review, we explore the secretory systems and associated secondary metabolism primarily in Asteraceous species to propose potential shared mechanisms facilitating the directional translocation of these metabolites to diverse destinations. We summarize recent advances in our understanding of the cooperativity between epidermal and internal secretory structures in the biosynthesis, secretion, accumulation, and emission of terpenes, providing specific well-documented examples from pyrethrum (Tanacetum cinerariifolium). Pyrethrum is renowned for its natural pyrethrin insecticides, which accumulate in the flower head, and more recently, for emitting an aphid alarm pheromone. These examples highlight the diverse specializations of secondary metabolism in pyrethrum and raise intriguing questions regarding the regulation of production and translocation of these compounds within and between its various epidermal and internal secretory systems, spanning multiple tissues, to serve distinct ecological purposes. By discussing the cooperative nature of secretory structures in flowering plants, this review sheds light on the intricate mechanisms underlying the ecological roles of terpenes in defense and pollination.

Environmental stressors can be key drivers of phenotypes, including reproductive strategies and morphological traits. The response to stress may be altered by the presence of microbial associates. For example, in aphids, facultative (secondary) bacterial symbionts can provide protection against natural enemies and stress induced by elevated temperatures. Furthermore, aphids exhibit phenotypic plasticity, producing winged (rather than wingless) progeny that may be better able to escape danger, and the combination of these factors improves the response to stress. How symbionts and phenotypic plasticity, both of which shape aphids’ stress response, influence one another, and together influence host fitness, remains unclear. In this study, we investigate how environmental stressors drive shifts in fecundity and winged/wingless offspring production, and how secondary symbionts influence the process. We induced production of winged offspring through distinct environmental stressors, including exposure to aphid alarm pheromone and crowding, and, in one experiment, we assessed whether the aphid response is influenced by host plant. In the winged morph, energy needed for wing maintenance may lead to trade‐offs with other traits, such as reproduction or symbiont maintenance. Potential trade‐offs between symbiont maintenance and fitness have been proposed but have not been tested. Thus, beyond studying the production of offspring of alternative morphs, we also explore the influence of symbionts across wing/wingless polyphenism as well as symbiont interaction with cross‐generational impacts of environmental stress on reproductive output. All environmental stressors resulted in increased production of winged offspring and shifts in fecundity rates. Additionally, in some cases, aphid host‐by‐symbiont interactions influenced fecundity. Stress on first‐generation aphids had cross‐generational impacts on second‐generation adults, and the impact on fecundity was further influenced by the presence of secondary symbionts and presence/absence of wings. Our study suggests a complex interaction between beneficial symbionts and environmental stressors. Winged aphids have the advantage of being able to migrate out of danger with more ease, but energy needed for wing production and maintenance may come with reproductive costs for their mothers and for themselves, where in certain cases, these costs are altered by secondary symbionts. The authors’ work sheds new light on the interaction between environmental stressors and beneficial symbionts, and how these factors act as drivers in pea aphid life‐history characteristics. Organisms need to adapt to ever‐changing environments, and this study shows how beneficial symbionts influence shifts in response to distinct types of environmental stress.