@article{wada-katsumata_hatano_schal_2023, title={Gustatory polymorphism mediates a new adaptive courtship strategy}, volume={290}, ISSN={["1471-2954"]}, url={https://doi.org/10.1098/rspb.2022.2337}, DOI={10.1098/rspb.2022.2337}, abstractNote={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.}, number={1995}, journal={PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES}, author={Wada-Katsumata, Ayako and Hatano, Eduardo and Schal, Coby}, year={2023}, month={Mar} }
 @article{saveer_hatano_wada-katsumata_meagher_schal_2023, title={Nonanal, a new fall armyworm sex pheromone component, significantly increases the efficacy of pheromone lures}, volume={4}, ISSN={["1526-4998"]}, url={https://doi.org/10.1002/ps.7460}, DOI={10.1002/ps.7460}, abstractNote={AbstractBackgroundThe 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.ResultsWe 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.ConclusionThe 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.}, journal={PEST MANAGEMENT SCIENCE}, author={Saveer, Ahmed M. and Hatano, Eduardo and Wada-Katsumata, Ayako and Meagher, Robert L. and Schal, Coby}, year={2023}, month={Apr} }
 @article{mcpherson_wada-katsumata_hatano_silverman_schal_2022, title={Nutritional condition affects tergal gland secretion and courtship success of male cockroaches}, volume={17}, ISSN={["1932-6203"]}, url={https://doi.org/10.1371/journal.pone.0271344}, DOI={10.1371/journal.pone.0271344}, abstractNote={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.}, number={8}, journal={PLOS ONE}, author={McPherson, Samantha and Wada-Katsumata, Ayako and Hatano, Eduardo and Silverman, Jules and Schal, Coby}, editor={Borges, Renee M.Editor}, year={2022} }
 @article{wada-katsumata_hatano_mcpherson_silverman_schal_2022, title={Rapid evolution of an adaptive taste polymorphism disrupts courtship behavior}, volume={5}, ISSN={["2399-3642"]}, url={https://doi.org/10.1038/s42003-022-03415-8}, DOI={10.1038/s42003-022-03415-8}, abstractNote={AbstractThe 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.}, number={1}, journal={COMMUNICATIONS BIOLOGY}, author={Wada-Katsumata, Ayako and Hatano, Eduardo and McPherson, Samantha and Silverman, Jules and Schal, Coby}, year={2022}, month={May} }
 @article{hosseini_mehrparvar_zytynska_hatano_weisser_2021, title={Aphid alarm pheromone alters larval behaviour of the predatory gall midge, Aphidoletes aphidimyza and decreases intraguild predation by anthocorid bug, Orius laevigatus}, volume={111}, ISSN={["1475-2670"]}, DOI={10.1017/S0007485321000122}, abstractNote={AbstractIntraguild 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)-β-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.}, number={4}, journal={BULLETIN OF ENTOMOLOGICAL RESEARCH}, author={Hosseini, Mojtaba and Mehrparvar, Mohsen and Zytynska, Sharon E. and Hatano, Eduardo and Weisser, Wolfgang W.}, year={2021}, month={Aug}, pages={445–453} }
 @article{mcpherson_wada-katsumata_hatano_silverman_schal_2021, title={Comparison of Diet Preferences of Laboratory-Reared and Apartment-Collected German Cockroaches}, volume={114}, ISSN={["1938-291X"]}, url={https://doi.org/10.1093/jee/toab139}, DOI={10.1093/jee/toab139}, abstractNote={AbstractThe 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.}, number={5}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, publisher={Oxford University Press (OUP)}, author={McPherson, Samantha and Wada-Katsumata, Ayako and Hatano, Eduardo and Silverman, Jules and Schal, Coby}, editor={Appel, ArthurEditor}, year={2021}, month={Oct}, pages={2189–2197} }
 @article{valbon_hatano_oliveira_ataide_correa_gomes_martins_haddi_alvarenga_oliveira_2021, title={Detrimental effects of pyriproxyfen on the detoxification and abilities of Belostoma anurum to prey upon Aedes aegypti larvae}, volume={284}, ISSN={["1873-6424"]}, DOI={10.1016/j.envpol.2021.117130}, abstractNote={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.}, journal={ENVIRONMENTAL POLLUTION}, author={Valbon, Wilson R. and Hatano, Eduardo and Oliveira, Nadylla R. X. and Ataide, Alvaro D. and Correa, Maria Julia M. and Gomes, Sabriny F. and Martins, Gustavo F. and Haddi, Khalid and Alvarenga, Elson S. and Oliveira, Eugenio E.}, year={2021}, month={Sep} }
 @article{shymanovich_faw_hajhashemi_teague_schal_ponnusamy_apperson_hatano_wasserberg_2019, title={Diel periodicity and visual cues guide oviposition behavior in Phlebotomus papatasi, vector of old-world cutaneous leishmaniasis}, volume={13}, ISSN={1935-2735}, url={http://dx.doi.org/10.1371/journal.pntd.0007165}, DOI={10.1371/journal.pntd.0007165}, abstractNote={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.}, number={3}, journal={PLOS Neglected Tropical Diseases}, publisher={Public Library of Science (PLoS)}, author={Shymanovich, Tatsiana and Faw, Lindsey and Hajhashemi, Nima and Teague, Jimmie and Schal, Coby and Ponnusamy, Loganathan and Apperson, Charles S. and Hatano, Eduardo and Wasserberg, Gideon}, editor={Oliveira, FabianoEditor}, year={2019}, month={Mar}, pages={e0007165} }
 @article{cruise_hatano_watson_schal_2018, title={Comparison of Techniques for Sampling Adult Necrophilous Insects From Pig Carcasses}, volume={55}, ISSN={0022-2585 1938-2928}, url={http://dx.doi.org/10.1093/jme/tjx255}, DOI={10.1093/jme/tjx255}, abstractNote={Abstract 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.}, number={4}, journal={Journal of Medical Entomology}, publisher={Oxford University Press (OUP)}, author={Cruise, Angela and Hatano, Eduardo and Watson, David W and Schal, Coby}, year={2018}, month={Feb}, pages={947–954} }