Gustatory polymorphism mediates a new adaptive courtship strategy.

Human-imposed selection can lead to adaptive changes in sensory traits. However, rapid evolution of the sensory system can interfere with other behaviours, and animals must overcome such sensory conflicts. In response to intense selection by insecticide baits that contain glucose, German cockroaches evolved glucose-aversion (GA), which confers behavioural resistance against baits. During courtship the male offers the female a nuptial gift that contains maltose, which expediates copulation. However, the female's saliva rapidly hydrolyses maltose into glucose, which causes GA females to dismount the courting male, thus reducing their mating success. Comparative analysis revealed two adaptive traits in GA males. They produce more maltotriose, which is more resilient to salivary glucosidases, and they initiate copulation faster than wild-type males, before GA females interrupt their nuptial feeding and dismount the male. Recombinant lines of the two strains showed that the two emergent traits of GA males were not genetically associated with the GA trait. Results suggest that the two courtship traits emerged in response to the altered sexual behaviour of GA females and independently of the male's GA trait. Although rapid adaptive evolution generates sexual mismatches that lower fitness, compensatory behavioural evolution can correct these sensory discrepancies.

Nonanal, a new fall armyworm sex pheromone component, significantly increases the efficacy of pheromone lures.

BACKGROUND: The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith), is a global pest that feeds on >350 plant species and severely limits production of cultivated grasses, vegetable crops and cotton. An efficient way to detect new invasions at early stages, and monitor and quantify the status of established infestations of this pest is to deploy traps baited with species-specific synthetic sex pheromone lures. RESULTS: We re-examined the compounds in the sex pheromone glands of FAW females by gas chromatography-electroantennogram detector (GC-EAD), GC-mass spectrometry (MS), behavioral and field assays. A new bioactive compound from pheromone gland extracts was detected in low amounts (3.0% relative to (Z)-9-tetradecenyl acetate (Z9-14:OAc), the main pheromone component), and identified as nonanal. This aldehyde significantly increased attraction of male moths to a mix of Z9-14:OAc and (Z)-7-dodecenyl acetate in olfactometer assays. Adding nonanal to this two-component mix also doubled male trap catches relative to the two-component mix alone in cotton fields, whereas nonanal alone did not attract any moths. The addition of nonanal to each of three commercial pheromone lures also increased male catches by 53-135% in sorghum and cotton fields. CONCLUSION: The addition of nonanal to pheromone lures should improve surveillance, monitoring and control of FAW populations. © 2023 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Nutritional condition affects tergal gland secretion and courtship success of male cockroaches.

An integral part of the courtship sequence of the German cockroach (Blattella germanica) involves the male raising his wings to expose tergal glands on his dorsum. When a female cockroach feeds on the secretion of these glands, she is optimally positioned for mating. Core chemical components have been identified, but the effect of male diet on the quality of the tergal gland secretion remains unexplored. After validating the pivotal role of tergal feeding in mating, we starved or fed reproductively mature males for one week. We then paired each male with a sexually receptive female and observed their interactions through an infrared-sensitive camera. While starvation had no effect on male courtship behavior, it did influence the duration of female tergal feeding and mating outcomes. Females fed longer on the gland secretion of fed males, and fed males experienced greater mating success than starved males (73.9% vs. 48.3%, respectively). These results suggest that the quality of the tergal gland secretions, and by association mating success, are dependent on the nutritional condition of the male.

Rapid evolution of an adaptive taste polymorphism disrupts courtship behavior.

The evolution of adaptive behavior often requires changes in sensory systems. However, rapid adaptive changes in sensory traits can adversely affect other fitness-related behaviors. In the German cockroach, a gustatory polymorphism, 'glucose-aversion (GA)', supports greater survivorship under selection with glucose-containing insecticide baits and promotes the evolution of behavioral resistance. Yet, sugars are prominent components of the male's nuptial gift and play an essential role in courtship. Behavioral and chemical analyses revealed that the saliva of GA females rapidly degrades nuptial gift sugars into glucose, and the inversion of a tasty nuptial gift to an aversive stimulus often causes GA females to reject courting males. Thus, the rapid emergence of an adaptive change in the gustatory system supports foraging, but it interferes with courtship. The trade-off between natural and sexual selection under human-imposed selection can lead to directional selection on courtship behavior that favors the GA genotype.

Comparison of Diet Preferences of Laboratory-Reared and Apartment-Collected German Cockroaches.

The German cockroach, Blattella germanica (L.) (Blattodea: Ectobiidae), is a common pest of human-built structures worldwide. German cockroaches are generalist omnivores able to survive on a wide variety of foods. A number of studies have concluded that laboratory-reared B. germanica self-select diets with an approximate 1P:3C (protein-to-carbohydrate) ratio. We predicted that field-collected insects would exhibit more variable dietary preferences, related to the wide-ranging quality, quantity, and patchiness of foods available to them. We compared diet self-selection of B. germanica within apartments and in the laboratory by offering them a choice of two complementary diets with 1P:1C and 1P:11C ratios. We observed high variation in the population-level self-selection of these diets among individual apartment sites as well as among various life stages tested in laboratory-based assays. Significant differences between populations in various apartments as well as between populations maintained in the laboratory suggested that factors beyond temporary food scarcity influence diet choice. Nevertheless, we found significant correlations between the amounts of diets ingested by cockroaches in apartments and cockroaches from the same populations assayed in the laboratory, as well as between males, females, and nymphs from these populations. These findings suggest that females, males, and nymphs within apartments adapt to the local conditions and convergently prefer similar amounts of food of similar dietary protein content.

Detrimental effects of pyriproxyfen on the detoxification and abilities of Belostoma anurum to prey upon Aedes aegypti larvae.

Despite being effective in controlling mosquito larvae and a few other target organisms, the application of insecticides into aquatic systems may cause unintended alterations to the physiology or behavioral responses of several aquatic non-target organisms, which can ultimately lead to their death. Here, we firstly evaluated whether the susceptibility of the giant water bug, Belostoma anurum (Hemiptera: Belostomatidae), a predator of mosquito larvae, to pyriproxyfen would be similar to that of its potential prey, larvae of Aedes aegypti (Diptera: Culicidae). Secondly, we recorded the nominal concentrations of pyriproxyfen in water and evaluated whether sublethal exposures would lead to physiological or behavioral alterations on the B. anurum nymphs. We characterized the activities of three major families of detoxification enzymes (i.e., cytochrome P450 monooxygenases, glutathione-S-transferase, and general esterases) and further evaluated the abilities of pyriproxyfen sublethally-exposed B. anurum to prey upon A. aegypti larvae at different prey densities. Our findings revealed that nominal pyriproxyfen concentration significantly decreased (approximately 50%) over the first 24 h. Furthermore, when applied at the concentration of 10 µg a.i./L, pyriproxyfen was approximately four times more toxic to A. aegypti larvae (LT50 = 48 h) than to B. anurum nymphs (LT50 = 192 h). Interestingly, the pyriproxyfen sublethally-exposed (2.5 µg a.i./L) B. anurum nymphs exhibited reduced enzyme activities (cytochrome P450 monooxygenases) involved in detoxication processes and preyed significantly less on A. aegypti larvae when compared to unexposed predators. Collectively, our findings demonstrate that mortality-based pyriproxyfen risk assessments are not always protective of aquatic non-target organisms.

Aphid alarm pheromone alters larval behaviour of the predatory gall midge, Aphidoletes aphidimyza and decreases intraguild predation by anthocorid bug, Orius laevigatus.

Intraguild predation is the killing and consuming of a heterospecific competitor that uses similar resources as the prey, and also benefit from preying on each other. We investigated the foraging behaviour of the gallmidge, Aphidoletes aphidimyza, a predator of aphids used for biological control that is also the intraguild prey for most other aphid natural enemies. We focus on how aphid alarm pheromone can alter the behaviour of the gallmidge, and predation by the anthocorid bug Orius laevigatus (O. laevigatus). We hypothesised that gallmidges would respond to the presence of (E)-ß-farnesene (EBF) by leaving the host plant. Since feeding by Aphidoletes gallmidge larvae does not induce EBF emission by aphids, this emission indicates the presence of an intraguild predator. We found that gallmidge larvae reduced their foraging activities and left the plant earlier when exposed to EBF, particularly when aphids were also present. Contrastingly, gallmidge females did not change the time visiting plants when exposed to EBF, but lay more eggs on plants that had a higher aphid density. Lastly, EBF reduced the number of attacks of the intraguild predator, O. laevigatus, on gallmidge larvae, potentially because more gallmidges stopped aphid feeding and moved off the plant at which point O. laevigatus predated on aphids. Our work highlights the importance of understanding how intraguild predation can influence the behaviour of potential biological control agents and the impact on pest control services when other natural enemies are also present.

The egg and larval pheromone dodecanoic acid mediates density-dependent oviposition of Phlebotomus papatasi.

BACKGROUND: Gravid females assess the conditions of oviposition sites to secure the growth and survival of their offspring. Conspecific-occupied sites may signal suitable oviposition sites but may also impose risk due to competition or cannibalism at high population density or heterogeneous larval stage structure, respectively. Chemicals in the habitat, including chemicals emitted from other organisms, serve as cues for females to assess habitat conditions. Here, we investigated the attraction and oviposition preference of the Old World cutaneous leishmaniasis vector, Phlebotomus papatasi, to young and old conspecific stages, including eggs and evaluated the effect of a semiochemical associated with eggs and neonate larvae. METHODS: Attraction and oviposition preference of Ph. papatasi to each of various life stages (eggs, first-, second-, third-, fourth-instar larvae, pupae and male and female adults) was investigated using cage and oviposition jar behavioral assays. Identification of organic chemical compounds extracted from eggs was performed using GC-MS and chemicals were tested in the same behavioral assays in a dose-response manner. Behavioral responses were statistically analyzed using logistic models. RESULTS: Gravid Ph. papatasi females were significantly attracted to and preferred to oviposit on medium containing young life stages (eggs and first instars). This preference decreased towards older life stages. Dose effect of eggs indicated a hump-shaped response with respect to attraction but a concave-up pattern with respect to oviposition. Chemical analysis of semiochemicals from eggs and first-instar larvae revealed the presence of dodecanoic acid (DA) and isovaleric acid. Sand flies were attracted to and laid more eggs at the lowest DA dose tested followed by a negative dose-response. CONCLUSIONS: Findings corroborated our hypothesis that gravid sand flies should prefer early colonized oviposition sites as indicators of site suitability but avoid sites containing older stages as indicators of potential competition. Findings also supported the predictions of our hump-shaped oviposition regulation (HSR) model, with attraction to conspecific eggs at low-medium densities and switching to repellence at high egg densities. This oviposition behavior is mediated by DA that was identified from surface extracts of both eggs and first-instar larvae. Isovaleric acid was also found in extracts of both stages.

Environmental decomposition of olefinic cuticular hydrocarbons of Periplaneta americana generates a volatile pheromone that guides social behaviour.

Once emitted, semiochemicals are exposed to reactive environmental factors that may alter them, thus disrupting chemical communication. Some species, however, might have adapted to detect environmentally mediated breakdown products of their natural chemicals as semiochemicals. We demonstrate that air, water vapour and ultraviolet (UV) radiation break down unsaturated cuticular hydrocarbons (CHCs) of Periplaneta americana (American cockroach), resulting in the emission of volatile organic compounds (VOCs). In behavioural assays, nymphs strongly avoided aggregating in shelters exposed to the breakdown VOCs from cuticular alkenes. The three treatments (air, water vapour, UV) produced the same VOCs, but at different time-courses and ratios. Fourteen VOCs from UV-exposed CHCs elicited electrophysiological responses in nymph antennae; 10 were identified as 2-nonanone, 1-pentanol, 1-octanol, 1-nonanol, tetradecanal, acetic acid, propanoic acid, butanoic acid, pentanoic acid and hexanoic acid. When short-chain fatty acids were tested as a mix and a blend of the alcohols and aldehyde was tested as a second mix, nymphs exhibited no preference for control or treated shelters. However, nymphs avoided shelters that were exposed to VOCs from the complete 10-compound mix. Conditioned shelters (occupied by cockroaches with faeces and CHCs deposited on the shelters), which are normally highly attractive to nymphs, were also avoided after UV exposure, confirming that breakdown products from deposited metabolites, including CHCs, mediate this behaviour. Our results demonstrate that common environmental agents degrade CHCs into behaviourally active volatile compounds that potentially may serve as necromones or epideictic pheromones, mediating group dissolution.

Diel periodicity and visual cues guide oviposition behavior in Phlebotomus papatasi, vector of old-world cutaneous leishmaniasis.

BACKGROUND: Phlebotomine sand flies are vectors of human leishmaniases, important neglected tropical diseases. In this study, we investigated diel patterns of oviposition behavior, effects of visual cues on oviposition-site selection, and whether these affect the attraction of gravid Phlebotomus papatasi (Scopoli), the vector of old-world cutaneous leishmaniasis, to olfactory cues from oviposition sites. METHODOLOGY/PRINCIPAL FINDINGS: To evaluate these questions, we conducted a series of experiments using attraction and oviposition assays within free-flight test chambers containing gravid females entrained under a 14:10 hrs light:dark photoperiod. By replacing sticky-screens or moist filter papers every three hours, we showed that oviposition site search occurs mainly in the latest part of the night whereas peak oviposition occurs during the early part of the night. Behavioral responses to olfactory oviposition cues are regulated by time-of-day and can be disrupted by transient exposure to a constant darkness photoperiod. Gravid females, but not any other stage, age, or sex, were attracted to dark, round oviposition jars, possibly resembling rodent burrow openings. This visual attraction disappeared in the absence of an illumination source. Egg deposition rate was not affected by jar color. Olfactory cues had the strongest effect when the visual cues were minimal. CONCLUSION AND SIGNIFICANCE: Our study showed, for the first time, that visual cues in the form of oviposition-site color, lighting level, and photoperiod are important in guiding the oviposition behavior of phlebotomine sand flies. Furthermore, such visual cues could modify the flies' sensitivity to olfactory oviposition cues. Our results suggest that chemosensory and visual cues are complementary, with visual cues used to orient gravid females towards oviposition sites, possibly at long- to medium-ranges during crepuscular periods, while olfactory cues are used to approach the burrow in darkness and assess its suitability at close-range. Implications to sand fly control are discussed.

Comparison of Techniques for Sampling Adult Necrophilous Insects From Pig Carcasses.

Studies of the pre-colonization interval and mechanisms driving necrophilous insect ecological succession depend on effective sampling of adult insects and knowledge of their diel and successional activity patterns. The number of insects trapped, their diversity, and diel periodicity were compared with four sampling methods on neonate pigs. Sampling method, time of day and decomposition age of the pigs significantly affected the number of insects sampled from pigs. We also found significant interactions of sampling method and decomposition day, time of sampling and decomposition day. No single method was superior to the other methods during all three decomposition days. Sampling times after noon yielded the largest samples during the first 2 d of decomposition. On day 3 of decomposition however, all sampling times were equally effective. Therefore, to maximize insect collections from neonate pigs, the method used to sample must vary by decomposition day. The suction trap collected the most species-rich samples, but sticky trap samples were the most diverse, when both species richness and evenness were factored into a Shannon diversity index. Repeated sampling during the noon to 18:00 hours period was most effective to obtain the maximum diversity of trapped insects. The integration of multiple sampling techniques would most effectively sample the necrophilous insect community. However, because all four tested methods were deficient at sampling beetle species, future work should focus on optimizing the most promising methods, alone or in combinations, and incorporate hand-collections of beetles.

Hedgehog Signaling Regulates the Ciliary Transport of Odorant Receptors in Drosophila.

Hedgehog (Hh) signaling is a key regulatory pathway during development and also has a functional role in mature neurons. Here, we show that Hh signaling regulates the odor response in adult Drosophila olfactory sensory neurons (OSNs). We demonstrate that this is achieved by regulating odorant receptor (OR) transport to and within the primary cilium in OSN neurons. Regulation relies on ciliary localization of the Hh signal transducer Smoothened (Smo). We further demonstrate that the Hh- and Smo-dependent regulation of the kinesin-like protein Cos2 acts in parallel to the intraflagellar transport system (IFT) to localize ORs within the cilium compartment. These findings expand our knowledge of Hh signaling to encompass chemosensory modulation and receptor trafficking.

A herbivore-induced plant volatile interferes with host plant and mate location in moths through suppression of olfactory signalling pathways.

BACKGROUND: Plants under herbivore attack release volatiles that attract natural enemies, and herbivores in turn avoid such plants. Whilst herbivore-induced plant volatile blends appeared to reduce the attractiveness of host plants to herbivores, the volatiles that are key in this process and particularly the way in which deterrence is coded in the olfactory system are largely unknown. Here we demonstrate that herbivore-induced cotton volatiles suppress orientation of the moth Spodoptera littoralis to host plants and mates. RESULTS: We found that (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), an induced volatile, is key in herbivore deterrence: DMNT suppressed plant odour- and pheromone-induced behaviours. We then dissected the neurophysiological basis of this interaction. DMNT-responding glomeruli were also activated by other plant compounds, suggesting that S. littoralis possesses no segregated olfactory circuit dedicated exclusively to DMNT. Instead, DMNT suppressed responses to the main pheromone component, (Z)-9-(E)-11-tetradecenyl acetate, and primarily to (Z)-3-hexenyl acetate, a host plant attractant. CONCLUSION: Our study shows that olfactory sensory inhibition, which has previously been reported without reference to an animal's ecology, can be at the core of coding of ecologically relevant odours. As DMNT attracts natural enemies and deters herbivores, it may be useful in the development or enhancement of push-pull strategies for sustainable agriculture.

Modulation of aphid alarm pheromone emission of pea aphid prey by predators.

Recent studies on animal alarm signaling have shown that alarm calls generally are not uniform, but may vary depending on the type and intensity of threat. While alarm call variability has been studied intensively in birds and mammals, little is known about such variation in insects. We investigated variability in alarm signaling in aphids, group-living insect herbivores. Under attack, aphids release droplets containing a volatile alarm pheromone, (E)-ß-farnesene (EBF), that induces specific escape behavior in conspecifics. We used a handheld gas chromatograph (zNose™), which allows real-time volatile analysis, to measure EBF emission by pea aphids, Acyrthosiphon pisum, under attack from different predators, lacewing or ladybird larvae. We demonstrate that aphid alarm signaling is affected by the predator species attacking. Ladybirds generally elicited smaller EBF emission peaks and consumed aphids more quickly, resulting in lower total EBF emission compared to lacewing attacks. In 52 % of the replicates with lacewings and 23 % with ladybirds, no EBF was detectable in the headspace, although aphids secreted cornicle droplets after attack. We, therefore, examined EBF amounts contained in these droplets and the aphid body. While all aphid bodies always contained EBF, many secreted droplets did not. Our experiments show that alarm signaling in insects can be variable, and both the attacker as well as the attacked may affect alarm signal variation. While underlying mechanisms of such variation in aphid-predator interactions need to be investigated in more detail, we argue that at least part of this variation may be adaptive for the predator and the aphid.

Aphid wing induction and ecological costs of alarm pheromone emission under field conditions.

The pea aphid, Acyrthosiphon pisum Harris, (Homoptera: Aphididae) releases the volatile sesquiterpene (E)-beta-farnesene (EBF) when attacked by a predator, triggering escape responses in the aphid colony. Recently, it was shown that this alarm pheromone also mediates the production of the winged dispersal morph under laboratory conditions. The present work tested the wing-inducing effect of EBF under field conditions. Aphid colonies were exposed to two treatments (control and EBF) and tested in two different environmental conditions (field and laboratory). As in previous experiments aphids produced higher proportion of winged morphs among their offspring when exposed to EBF in the laboratory but even under field conditions the proportion of winged offspring was higher after EBF application (6.84+/-0.98%) compared to the hexane control (1.54+/-0.25%). In the field, the proportion of adult aphids found on the plant at the end of the experiment was lower in the EBF treatment (58.1+/-5.5%) than in the control (66.9+/-4.6%), in contrast to the climate chamber test where the numbers of adult aphids found on the plant at the end of the experiment were, in both treatments, similar to the numbers put on the plant initially. Our results show that the role of EBF in aphid wing induction is also apparent under field conditions and they may indicate a potential cost of EBF emission. They also emphasize the importance of investigating the ecological role of induced defences under field conditions.

Do aphid colonies amplify their emission of alarm pheromone?

When aphids are attacked by natural enemies, they emit alarm pheromone to alert conspecifics. For most aphids tested, (E)-beta-farnesene (EBF) is the main, or only, constituent of the alarm pheromone. In response to alarm pheromone, alerted aphids drop off the plant, walk away, or attempt to elude predators. However, under natural conditions, EBF concentration might be low due to the low amounts emitted, to rapid air movement, or to oxidative degradation. To ensure that conspecifics are warned, aphids might conceivably amplify the alarm signal by emitting EBF in response to EBF emitted by other aphids. To examine whether such amplification occurs, we synthesized deuterated EBF (DEBF), which allowed us to differentiate between applied and aphid-derived chemical. Colonies of Acyrthosiphon pisum were treated with DEBF, and headspace volatiles were collected and analyzed for evidence of aphid-derived EBF. No aphid-derived EBF was detected, suggesting that amplification of the alarm signal does not occur. We discuss the disadvantages of alarm signal reinforcement.

Occurrence of Pyemotes sp. on Tuta absoluta (Meyrick)

The aim of this work was to study the population reduction of the tomato leafminer moth, Tuta absoluta (Meyrick), by Pyemotes sp. in the laboratory. The mite became greenish when fed on caterpillars, pupae, and adults of T. absoluta. The caterpillars and adults of T. absoluta were quickly paralyzed by the mite venom. A single T. absoluta could host many Pyemotes sp, physogastric females, which were allowed to grow on the moth. Pyemotes sp. can be a new alternative for the biological control of T. absoluta. However, this possibility must be better understood before it could be recommended, because Pyemotes sp. could also cause dermatitis in the humans.

O ácaro Pyemotes sp. (Acari: Pyemotidae) é um parasita de várias espécies de insetos e exibe o processo de fisogastria na reprodução. É registrada a ocorrência de Pyemotes sp. sobre a traça-do-tomateiro, Tuta absoluta (Meyrick), que sofreu redução considerável de suas populações em condições de laboratório. Este ácaro foi observado parasitando larvas, pupas e adultos de T. absoluta e suas fêmeas fisogástricas apresentaram coloração esverdeada. As larvas e adultos de T. absoluta atacados por Pyemotes sp. exibiram paralisia em poucos minutos, devido à injeção de toxinas por parte do ácaro. Observou-se que um único indivíduo de T. absoluta pode suportar muitas fêmeas fisogástricas de Pyemotes sp., permitindo que outra geração do ácaro continuasse a se reproduzir. O ácaro Pyemotes sp. surge como uma possibilidade para o controle biológico de T. absoluta, mas sua utilização deve ser melhor avaliada já que é uma espécie causadora de dermatites em humanos.

Isolation and structure elucidation of Peronosporomycetes hyphal branching-inducing factors produced by Pseudomonas jessenii EC-S101.

Pseudomonas jessenii EC-S101 produced hyphal branching-inducing and mitosis-accelerating factors active towards Peronosporomycetes, Aphanomyces cochlioides hyphae. In searching for the active substances, EtOAc-solubles extracted from EC-S101-cultured solid medium were fractionated under the guidance of a paper disc assay using an A. cochlioides mycelium. Two active substances were subsequently isolated and the structure was elucidated by spectroscopic analysis to be (+)-4,5-didehydroacaterin (1) and 3-[(1R)-hydroxyhexyl]-5-methylene-2(5H)-furanone (2), both of which accelerated the mitotic process of A. cochlioides hyphae along with excessive branching at 1.0 microg per disc. These compounds are likely to affect the morphophysiological development of certain eukaryotic organisms in the terrestrial ecosystem.