@article{gonzalez-morales_thomson_yeatts_enomoto_haija_santangelo_petritz_crespo_schal_baynes_2023, title={Pharmacokinetics of fluralaner as a systemic drug to control infestations of the common bed bug, Cimex lectularius, in poultry facilities}, volume={16}, ISSN={["1756-3305"]}, url={https://doi.org/10.1186/s13071-023-05962-3}, DOI={10.1186/s13071-023-05962-3}, abstractNote={Abstract Background Bed bug infestations are re-emerging in the poultry industry throughout the USA. Although the impacts of bed bugs on birds’ health and welfare are poorly understood, adverse outcomes are expected, including stress, anemia, infections and lower production rates. Worker welfare is also an important consideration in commercial poultry farms. A limited number of insecticides are available for use in the complex spatial environment of commercial farms. Systemic drugs have the potential to overcome the limitations of existing pest management tactics. A recent study showed that fluralaner administered to chickens caused high levels of mortality in bed bugs. Methods To further understand the efficacy of this approach, we evaluated the pharmacokinetics of an oral solid formulation of fluralaner in 11 chickens and quantified its plasma concentration in chickens using UPLC/MS. We administered fluralaner to chickens with two doses of Bravecto® (each 0.5 mg/kg body mass) via gavage 1 week apart and evaluated its efficacy on bed bugs that fed on medicated chickens for up to 28 days post-treatment. Results Bed bugs that fed on fluralaner-treated chickens experienced > 50% mortality within 30 min of the administration of Bravecto and 100% mortality 2 days post-treatment. Mortality slowly declined to 66.6% by day 28. Fluralaner was quantifiable in the hens’ plasma for at least 28 days post-treatment. The treatment resulted in maximal plasma concentrations (Cmax) of 106.4 ng/ml around day 9.0 (Tmax), substantially higher than the LC90, the concentration needed to kill 90% of the bed bugs. Conclusions Fluralaner appears to be a promising candidate for bed bug control in poultry farms, with a treatment effect lasting at least 28 days. Graphical Abstract }, number={1}, journal={PARASITES & VECTORS}, author={Gonzalez-Morales, Maria A. and Thomson, Andrea E. and Yeatts, James and Enomoto, Hiroko and Haija, Ahmed and Santangelo, Richard G. and Petritz, Olivia A. and Crespo, Rocio and Schal, Coby and Baynes, Ronald}, year={2023}, month={Sep} } @article{gordon_santangelo_gonzalez-morales_menechella_schal_devries_2023, title={Spatial distribution of histamine in bed bug-infested homes}, volume={880}, ISSN={["1879-1026"]}, DOI={10.1016/j.scitotenv.2023.163180}, abstractNote={Histamine is a component of the bed bug aggregation pheromone. It was recently identified as an environmental contaminant in homes with active bed bug infestations, posing a potential health risk to humans via skin contact or inhalation. It remains unclear how histamine is distributed in homes and if histamine can become airborne. In the present study, histamine levels in household dust were quantified from multiple locations within bed bug infested and uninfested apartments. Bed bug population levels were quantified using both traps and visual counts. The amount of histamine detected varied significantly with respect to sampling location, with the highest concentration of histamine quantified from bedding material. Infestation severity did not have a significant effect on histamine quantified at any location. Our results indicate that the bedroom should be the primary focus of histamine mitigation efforts, although histamine can be found throughout the home. Histamine quantified from homes without active bed bug infestations suggests that histamine from previous infestations can persist following pest eradication. These findings highlight the importance of histamine as a potential insect allergen and will be important for the development of targeted mitigation strategies of bed bug histamine.}, journal={SCIENCE OF THE TOTAL ENVIRONMENT}, author={Gordon, Johnalyn M. and Santangelo, Richard G. and Gonzalez-Morales, Maria A. and Menechella, Mark and Schal, Coby and DeVries, Zachary C.}, year={2023}, month={Jul} } @article{gonzalez-morales_devries_santangelo_kakumanu_schal_2022, title={Multiple Mechanisms Confer Fipronil Resistance in the German Cockroach: Enhanced Detoxification and Rdl Mutation}, volume={8}, ISSN={["1938-2928"]}, url={https://doi.org/10.1093/jme/tjac100}, DOI={10.1093/jme/tjac100}, abstractNote={Abstract Populations of Blattella germanica (L.) (German cockroach) have been documented worldwide to be resistant to a wide variety of insecticides with multiple modes of action. The phenylpyrazole insecticide fipronil has been used extensively to control German cockroach populations, exclusively in baits, yet the highest reported fipronil resistance is 38-fold in a single population. We evaluated five populations of German cockroaches, collected in 2018–2019 in apartments in North Carolina and assayed in 2019, to determine the status of fipronil resistance in the state. Resistance ratios in field-collected strains ranged from 22.4 to 37.2, indicating little change in fipronil resistance over the past 20 yr. In contrast, resistance to pyrethroids continues to escalate. We also assessed the roles of detoxification enzymes in fipronil resistance with four synergists previously shown to diminish metabolic resistance to various insecticides in German cockroaches—piperonyl butoxide, S,S,S-tributyl phosphorotrithioate, diethyl maleate, and triphenyl phosphate. These enzymes appear to play a variable role in fipronil resistance. We also sequenced a fragment of the Rdl (resistant to dieldrin) gene that encodes a subunit of the GABA receptor. Our findings showed that all field-collected strains are homozygous for a mutation that substitutes serine for an alanine (A302S) in Rdl, and confers low resistance to fipronil. Understanding why cockroaches rapidly evolve high levels of resistance to some insecticides and not others, despite intensive selection pressure, will contribute to more efficacious pest management.}, journal={JOURNAL OF MEDICAL ENTOMOLOGY}, author={Gonzalez-Morales, Maria A. and DeVries, Zachary C. and Santangelo, Richard G. and Kakumanu, Madhavi L. and Schal, Coby}, editor={Booth, WarrenEditor}, year={2022}, month={Aug} } @article{gonzalez-morales_thomson_petritz_crespo_haija_santangelo_schal_2022, title={Systemic veterinary drugs for control of the common bed bug, Cimex lectularius, in poultry farms}, volume={15}, ISSN={["1756-3305"]}, DOI={10.1186/s13071-022-05555-6}, abstractNote={AbstractBackgroundThe common bed bug,CimexlectulariusL., is a hematophagous ectoparasite that was a common pest in poultry farms through the 1960s. Dichlorodiphenyltrichloroethane (DDT) and organophosphates eradicated most infestations, but concurrent with their global resurgence as human ectoparasites, infestations of bed bugs have been reappearing in poultry farms. Although the impact of bed bugs on chicken health has not been quantified, frequent biting and blood-feeding are expected to cause stress, infections and even anemia in birds. Bed bug control options are limited due to the sensitive nature of the poultry environment, limited products labeled for bed bug control and resistance of bed bug populations to a broad spectrum of active ingredients. Veterinary drugs are commonly used to control endo- and ectoparasites in animals. In this study, we evaluated the effects of two common veterinary drugs on bed bugs by treating the host with systemic antiparasitic drugs.MethodsWe conducted dose–response studies of ivermectin and fluralaner against several bed bug strains using a membrane feeding system. Also, different doses of these drugs were given to chickens and two delivery methods (topical treatment and ingestion) were used to evaluate the efficacy of ivermectin and fluralaner on bed bug mortality.ResultsUsing an artificial feeding system, both ivermectin and fluralaner caused high mortality in insecticide-susceptible bed bugs, and fluralaner was found to be effective on pyrethroid- and fipronil-resistant bed bugs. Ivermectin was ineffective in chickens either by the topical treatment or ingestion, whereas bed bugs that fed on chickens which had ingested fluralaner suffered high mortality when feeding on these chickens for up to 28 days post treatment.ConclusionsThese findings suggest that systemic ectoparasitic drugs have great potential for practical use to control bed bug infestations in poultry farms. These findings also demonstrate the efficacy of fluralaner (and potentially other isoxazolines) as a potent new active ingredient for bed bug control.Graphical Abstract}, number={1}, journal={PARASITES & VECTORS}, author={Gonzalez-Morales, Maria A. and Thomson, Andrea E. and Petritz, Olivia A. and Crespo, Rocio and Haija, Ahmed and Santangelo, Richard G. and Schal, Coby}, year={2022}, month={Nov} } @article{gaire_devries_mick_santangelo_bottillo_camera_schal_2021, title={Human skin triglycerides prevent bed bug (Cimex lectularius L.) arrestment}, volume={11}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-021-01981-1}, abstractNote={AbstractBed bugs (Cimex lectularius) have proliferated globally and have become one of the most challenging pests to control indoors. They are nocturnal and use multiple sensory cues to detect and orient towards their human hosts. After feeding, usually on a sleeping human, they return to a shelter on or around the sleeping surface, but not directly on the host. We hypothesized that although human skin odors attract hungry bed bugs, human skin compounds may also prevent arrestment on hosts. We used arrestment assays to test human skin swabs, extracts from human skin swabs, and pure compounds identified from human skin swabs. When given a choice, bed bugs preferred to arrest on substrates not previously conditioned by humans. These responses were consistent among laboratory-reared and apartment-collected bed bugs. The compounds responsible for this behavior were found to be extractable in hexane, and bed bugs responded to such extracts in a dose-dependent manner. Bioassay-guided fractionation paired with thin-layer chromatography, GC–MS, and LC–MS analyses suggested that triglycerides (TAGs), common compounds found on human skin, were preventing arrestment on shelters. Bed bugs universally avoided sheltering in TAG-treated shelters, which was independent of the number of carbons or the number of double bonds in the TAG. These results provide strong evidence that the complex of human skin compounds serve as multifunctional semiochemicals for bed bugs, with some odorants attracting host-seeking stages, and others (TAGs and possibly other compounds) preventing bed bug arrestment. Host chemistry, environmental conditions and the physiological state of bed bugs likely influence the dual nature behavioral responses of bed bugs to human skin compounds.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Gaire, Sudip and DeVries, Zachary C. and Mick, Russell and Santangelo, Richard G. and Bottillo, Grazia and Camera, Emanuela and Schal, Coby}, year={2021}, month={Dec} } @article{saveer_devries_santangelo_schal_2021, title={Mating and starvation modulate feeding and host-seeking responses in female bed bugs, Cimex lectularius}, volume={11}, ISSN={["2045-2322"]}, url={https://doi.org/10.1038/s41598-021-81271-y}, DOI={10.1038/s41598-021-81271-y}, abstractNote={AbstractReproductive fitness and survival are enhanced by adaptive behaviors that are modulated by internal physiological states and external social contexts. The common bed bug,Cimex lectularius, is an obligate hematophagous ectoparasite that requires host blood for growth, development, and reproduction. We investigated how mating, starvation and social interactions affect host-seeking, blood feeding, oviposition, and survival of female bed bugs. The percentage of females that fed and the amount of blood they ingested were greater in mated females (90–100%) than in unmated females (48–60%). Mating state also modulated the female’s orientation towards human skin odor in an olfactometer; more mated (69%) than unmated (23%) females responded to human odors. The response rate of unmated females (60%) to skin odor increased with longer starvation period, while the opposite pattern was observed in mated females (20%). Although fecundity after a single blood meal was unaffected by long or short residence and interaction with males, females subjected to frequent copulation attempts had lower survivorship and lifespan than females housed with males for only 24 h. Taken together, these results indicate that by adaptively and coordinately expressing behaviors based on the internal physiological state, females maximize their survival and reproductive fitness.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Saveer, Ahmed M. and DeVries, Zachary C. and Santangelo, Richard G. and Schal, Coby}, year={2021}, month={Jan} } @article{gonzalez-morales_devries_sierras_santangelo_kakumanu_schal_2021, title={Resistance to Fipronil in the Common Bed Bug (Hemiptera: Cimicidae)}, volume={58}, ISSN={["1938-2928"]}, url={https://doi.org/10.1093/jme/tjab040}, DOI={10.1093/jme/tjab040}, abstractNote={AbstractCimex lectularius L. populations have been documented worldwide to be resistant to pyrethroids and neonicotinoids, insecticides that have been widely used to control bed bugs. There is an urgent need to discover new active ingredients with different modes of action to control bed bug populations. Fipronil, a phenylpyrazole that targets the GABA receptor, has been shown to be highly effective on bed bugs. However, because fipronil shares the same target site with dieldrin, we investigated the potential of fipronil resistance in bed bugs. Resistance ratios in eight North American populations and one European population ranged from 1.4- to >985-fold, with highly resistant populations on both continents. We evaluated metabolic resistance mechanisms mediated by cytochrome P450s, esterases, carboxylesterases, and glutathione S-transferases using synergists and a combination of synergists. All four detoxification enzyme classes play significant but variable roles in bed bug resistance to fipronil. Suppression of P450s and esterases with synergists eliminated resistance to fipronil in highly resistant bed bugs. Target-site insensitivity was evaluated by sequencing a fragment of the Rdl gene to detect the A302S mutation, known to confer resistance to dieldrin and fipronil in other species. All nine populations were homozygous for the wild-type genotype (susceptible phenotype). Highly resistant populations were also highly resistant to deltamethrin, suggesting that metabolic enzymes that are responsible for pyrethroid detoxification might also metabolize fipronil. It is imperative to understand the origins of fipronil resistance in the development or adoption of new active ingredients and implementation of integrated pest management programs.}, number={4}, journal={JOURNAL OF MEDICAL ENTOMOLOGY}, publisher={Oxford University Press (OUP)}, author={Gonzalez-Morales, Maria A. and DeVries, Zachary and Sierras, Angela and Santangelo, Richard G. and Kakumanu, Madhavi L. and Schal, Coby}, editor={Hribar, LawrenceEditor}, year={2021}, month={Jul}, pages={1798–1807} } @article{devries_santangelo_crissman_mick_schal_2019, title={Exposure risks and ineffectiveness of total release foggers (TRFs) used for cockroach control in residential settings}, volume={19}, ISSN={1471-2458}, url={http://dx.doi.org/10.1186/s12889-018-6371-z}, DOI={10.1186/s12889-018-6371-z}, abstractNote={The German cockroach, Blattella germanica, is one of the most challenging pests to eradicate from indoor environments. Professional pest control is often prohibitively expensive, prompting low-income residents to turn to over-the-counter consumer products, including total release foggers (TRFs, "bug bombs"). Despite their widespread use, little is known regarding either the associated pesticide exposure risks or the efficacy of TRFs.Cockroach-infested homes were recruited into the study. Wipe samples were collected from various surfaces before TRFs were discharged, immediately after, and one month later to determine pesticide exposure risks in 20 homes (divided equally among four different TRF products). Simultaneously, cockroach populations were monitored in all homes to assess the efficacy of TRFs. In parallel, 10 homes were treated with gel baits (divided equally between two bait products), to compare TRFs to a more targeted, low-risk, do-it-yourself intervention strategy.TRFs failed to reduce cockroach populations, whereas similarly priced gel baits caused significant declines in the cockroach populations. Use of TRFs resulted in significant pesticide deposits throughout the kitchen. Across all products, pesticides, and horizontal kitchen surfaces, pesticide residues following TRF discharge were 603-times (SEM ±184) higher than baseline, with a median increase of 85 times.The high risks of pesticide exposure associated with TRFs combined with their ineffectiveness in controlling German cockroach infestations call into question their utility in the marketplace, especially because similarly priced and much safer bait products are highly effective in the indoor environment.}, number={1}, journal={BMC Public Health}, publisher={Springer Science and Business Media LLC}, author={DeVries, Zachary C. and Santangelo, Richard G. and Crissman, Jonathan and Mick, Russell and Schal, Coby}, year={2019}, month={Jan} } @article{devries_santangelo_crissman_suazo_kakumanu_schal_2019, title={Pervasive Resistance to Pyrethroids in German Cockroaches (Blattodea: Ectobiidae) Related to Lack of Efficacy of Total Release Foggers}, volume={112}, ISSN={0022-0493 1938-291X}, url={http://dx.doi.org/10.1093/jee/toz120}, DOI={10.1093/jee/toz120}, abstractNote={Abstract Despite limited efficacy data, do-it-yourself (DIY) insecticide products often promise low-cost alternatives to professional pest control. Total release foggers (TRFs, ‘bug bombs’), which are prominent DIY products, were recently shown to be ineffective at reducing German cockroach (Blattella germanica L.) infestations, in contrast to highly effective baits. However, the reason(s) for TRF failure remain unknown. Therefore, we investigated insecticide resistance of apartment-collected cockroaches from homes where TRFs failed. In topical (direct) application assays, resistance to cypermethrin (a common active ingredient in TRFs) was 202 ± 33 times that of a laboratory insecticide-susceptible population (based on LD50 ratios), while resistance to fipronil, a common bait active ingredient, was considerably lower at 14 ± 2 times that of the laboratory insecticide-susceptible population. The addition of PBO, a P450 inhibitor that synergizes pyrethroids, enhanced the efficacy of cypermethrin, but only at high doses of cypermethrin. Additionally, >96% of screened cockroaches possessed at least one copy of the L993F mutation in the voltage-gated sodium channel, known to confer resistance to pyrethroids (knockdown resistance, kdr). Because TRF treatments killed insecticide-susceptible sentinel cockroaches but failed to kill apartment-collected cockroaches, these results suggest that pyrethroid resistance is a major factor contributing to the failure of TRFs. Multiple mechanisms of resistance, including metabolic detoxification of the pyrethroids and kdr mutations that confer target-site insensitivity, suggest that TRFs would lack efficacy against German cockroaches in residential settings, where high levels of pyrethroid resistance have been documented globally.}, number={5}, journal={Journal of Economic Entomology}, publisher={Oxford University Press (OUP)}, author={DeVries, Zachary C and Santangelo, Richard G and Crissman, Jonathan and Suazo, Alonso and Kakumanu, Madhavi L and Schal, Coby}, editor={Rust, MichaelEditor}, year={2019}, month={May}, pages={2295–2301} } @article{devries_santangelo_barbarin_schal_2018, title={Histamine as an emergent indoor contaminant: Accumulation and persistence in bed bug infested homes}, volume={13}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0192462}, DOI={10.1371/journal.pone.0192462}, abstractNote={Histamine is used in bronchial and dermal provocation, but it is rarely considered an environmental risk factor in allergic disease. Because bed bugs defecate large amounts of histamine as a component of their aggregation pheromone, we sought to determine if histamine accumulates in household dust in bed bug infested homes, and the effects of bed bug eradication with spatial heat on histamine levels in dust. We collected dust in homes and analyzed for histamine before, and up to three months after bed bug eradication. Histamine levels in bed bug infested homes were remarkably high (mean = 54.6±18.9 μg/100 mg of sieved household dust) and significantly higher than in control homes not infested with bed bugs (mean < 2.5±1.9 μg/100 mg of sieved household dust). Heat treatments that eradicated the bed bug infestations failed to reduce histamine levels, even three months after treatment. We report a clear association between histamine levels in household dust and bed bug infestations. The high concentrations, persistence, and proximity to humans during sleep suggest that bed bug-produced histamine may represent an emergent contaminant and pose a serious health risk in the indoor environment.}, number={2}, journal={PLOS ONE}, publisher={Public Library of Science (PLoS)}, author={DeVries, Zachary C. and Santangelo, Richard G. and Barbarin, Alexis M. and Schal, Coby}, editor={Benoit, Joshua B.Editor}, year={2018}, month={Feb}, pages={e0192462} } @article{vargo_crissman_booth_santangelo_mukha_schal_2014, title={Hierarchical Genetic Analysis of German Cockroach (Blattella germanica) Populations from within Buildings to across Continents}, volume={9}, ISSN={1932-6203}, url={http://dx.doi.org/10.1371/journal.pone.0102321}, DOI={10.1371/journal.pone.0102321}, abstractNote={Understanding the population structure of species that disperse primarily by human transport is essential to predicting and controlling human-mediated spread of invasive species. The German cockroach (Blattella germanica) is a widespread urban invader that can actively disperse within buildings but is spread solely by human-mediated dispersal over longer distances; however, its population structure is poorly understood. Using microsatellite markers we investigated population structure at several spatial scales, from populations within single apartment buildings to populations from several cities across the U.S. and Eurasia. Both traditional measures of genetic differentiation and Bayesian clustering methods revealed increasing levels of genetic differentiation at greater geographic scales. Our results are consistent with active dispersal of cockroaches largely limited to movement within a building. Their low levels of genetic differentiation, yet limited active spread between buildings, suggests a greater likelihood of human-mediated dispersal at more local scales (within a city) than at larger spatial scales (within and between continents). About half the populations from across the U.S. clustered together with other U.S. populations, and isolation by distance was evident across the U.S. Levels of genetic differentiation among Eurasian cities were greater than those in the U.S. and greater than those between the U.S. and Eurasia, but no clear pattern of structure at the continent level was detected. MtDNA sequence variation was low and failed to reveal any geographical structure. The weak genetic structure detected here is likely due to a combination of historical admixture among populations and periodic population bottlenecks and founder events, but more extensive studies are needed to determine whether signatures of global movement may be present in this species.}, number={7}, journal={PLoS ONE}, publisher={Public Library of Science (PLoS)}, author={Vargo, Edward L. and Crissman, Jonathan R. and Booth, Warren and Santangelo, Richard G. and Mukha, Dmitry V. and Schal, Coby}, editor={Adelman, Zach N.Editor}, year={2014}, month={Jul}, pages={e102321} } @article{groot_schöfl_inglis_donnerhacke_classen_schmalz_santangelo_emerson_gould_schal_et al._2014, title={Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences}, volume={281}, ISSN={0962-8452 1471-2954}, url={http://dx.doi.org/10.1098/rspb.2013.3054}, DOI={10.1098/rspb.2013.3054}, abstractNote={Evolutionary diversification of sexual communication systems in moths is perplexing because signal and response are under stabilizing selection in many species, and this is expected to constrain evolutionary change. In the mothHeliothis virescens, we consistently found high phenotypic variability in the female sex pheromone blend within each of four geographically distant populations. Here, we assess the heritability, genetic basis and behavioural consequences of this variation. Artificial selection with field-collected moths dramatically increased the relative amount of the saturated compound 16:Ald and decreased its unsaturated counterpart Z11–16:Ald, the major sex pheromone component (high line). In a cross between the high- and low-selected lines, one quantitative trait locus (QTL) explained 11–21% of the phenotypic variance in the 16:Ald/Z11–16:Ald ratio. Because changes in activity of desaturase enzymes could affect this ratio, we measured their expression levels in pheromone glands and mapped desaturase genes onto our linkage map. A delta-11-desaturase had lower expression in females producing less Z11–16:Ald; however, this gene mapped to a different chromosome than the QTL. A model in which the QTL is a trans-acting repressor of delta-11 desaturase expression explains many features of the data. Selection favouring heterozygotes which produce more unsaturated components could maintain a polymorphism at this locus.}, number={1779}, journal={Proceedings of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Groot, Astrid T. and Schöfl, Gerhard and Inglis, Ollie and Donnerhacke, Susanne and Classen, Alice and Schmalz, Antje and Santangelo, Richard G. and Emerson, Jennifer and Gould, Fred and Schal, Coby and et al.}, year={2014}, month={Mar}, pages={20133054} } @article{groot_staudacher_barthel_inglis_schöfl_santangelo_gebauer‐jung_vogel_emerson_schal_et al._2013, title={One quantitative trait locus for intra‐ and interspecific variation in a sex pheromone}, volume={22}, ISSN={0962-1083 1365-294X}, url={http://dx.doi.org/10.1111/mec.12171}, DOI={10.1111/mec.12171}, abstractNote={AbstractEven though premating isolation is hypothesized to be a major driving force in speciation, its genetic basis is poorly known. In the noctuid moth Heliothis subflexa, one group of sex pheromone components, the acetates, emitted by the female, plays a crucial isolating role in preventing interspecific matings to males of the closely related Heliothis virescens, in which females do not produce acetates and males are repelled by them. We previously found intraspecific variation in acetates in H. subflexa: females in eastern North America contain significantly more acetates than females in Western Mexico. Here we describe the persistence of this intraspecific variation in laboratory‐reared strains and the identification of one major quantitative trait locus (QTL), explaining 40% of the variance in acetate amounts. We homologized this intraspecific QTL to our previously identified interspecific QTL using restriction‐associated DNA (RAD) tags. We found that a major intraspecific QTL overlaps with one of the two major interspecific QTL. To identify candidate genes underlying the acetate variation, we investigated a number of gene families with known or suspected acetyl‐ or acyltransferase activity. The most likely candidate genes did not map to our QTL, so that we currently hypothesize that a transcription factor underlies this QTL. Finding a single, large QTL that impacts variation in pheromone blends between and within species is, to our knowledge, the first such example for traits that have been demonstrated to affect premating isolation.}, number={4}, journal={Molecular Ecology}, publisher={Wiley}, author={Groot, A. T. and Staudacher, H. and Barthel, A. and Inglis, O. and Schöfl, G. and Santangelo, R. G. and Gebauer‐Jung, S. and Vogel, H. and Emerson, J. and Schal, C. and et al.}, year={2013}, month={Jan}, pages={1065–1080} } @article{booth_saenz_santangelo_wang_schal_vargo_2012, title={Molecular Markers Reveal Infestation Dynamics of the Bed Bug (Hemiptera: Cimicidae) Within Apartment Buildings}, volume={49}, ISSN={0022-2585 1938-2928}, url={http://dx.doi.org/10.1603/ME11256}, DOI={10.1603/me11256}, abstractNote={ABSTRACT The bed bug, Cimex lectularius L. (Hemiptera: Cimicidae), has experienced an extraordinary global resurgence in recent years, the reasons for which remain poorly understood. Once considered a pest of lower socioeconomic classes, bed bugs are now found extensively across all residential settings, with widespread infestations established in multiapartment buildings. Within such buildings, understanding the population genetic structure and patterns of dispersal may prove critical to the development of effective control strategies. Here, we describe the development of 24 high-resolution microsatellite markers through next generation 454 pyrosequencing and their application to elucidate infestation dynamics within three multistory apartment buildings in the United States. Results reveal contrasting characteristics potentially representative of geographic or locale differences. In Raleigh, NC, an infestation within an apartment building seemed to have started from a single introduction followed by extensive spread. In Jersey City, NJ, two or more introductions followed by spread are evident in two buildings. Populations within single apartments in all buildings were characterized by high levels of relatedness and low levels of diversity, indicative of foundation from small, genetically depauperate propagules. Regardless of the number of unique introductions, genetic data indicate that spread within buildings is extensive, supporting both active and human-mediated dispersal within and between adjacent rooms or apartments spanning multiple floors.}, number={3}, journal={Journal of Medical Entomology}, publisher={Oxford University Press (OUP)}, author={Booth, Warren and Saenz, Virna L. and Santangelo, Richard G. and Wang, Changlu and Schal, Coby and Vargo, Edward L.}, year={2012}, month={May}, pages={535–546} } @article{eliyahu_nojima_santangelo_carpenter_webster_kiemle_gemeno_leal_schal_2011, title={Unusual macrocyclic lactone sex pheromone of Parcoblatta lata, a primary food source of the endangered red-cockaded woodpecker}, volume={109}, ISSN={0027-8424 1091-6490}, url={http://dx.doi.org/10.1073/pnas.1111748109}, DOI={10.1073/pnas.1111748109}, abstractNote={ Wood cockroaches in the genus Parcoblatta , comprising 12 species endemic to North America, are highly abundant in southeastern pine forests and represent an important prey of the endangered red-cockaded woodpecker, Picoides borealis . The broad wood cockroach, Parcoblatta lata , is among the largest and most abundant of the wood cockroaches, constituting >50% of the biomass of the woodpecker's diet. Because reproduction in red-cockaded woodpeckers is affected dramatically by seasonal and spatial changes in arthropod availability, monitoring P. lata populations could serve as a useful index of habitat suitability for woodpecker conservation and forest management efforts. Female P. lata emit a volatile, long-distance sex pheromone, which, once identified and synthesized, could be deployed for monitoring cockroach populations. We describe here the identification, synthesis, and confirmation of the chemical structure of this pheromone as (4 Z ,11 Z )-oxacyclotrideca-4,11-dien-2-one [= (3 Z ,10 Z )-dodecadienolide; herein referred to as “parcoblattalactone”]. This macrocyclic lactone is a previously unidentified natural product and a previously unknown pheromonal structure for cockroaches, highlighting the great chemical diversity that characterizes olfactory communication in cockroaches: Each long-range sex pheromone identified to date from different genera belongs to a different chemical class. Parcoblattalactone was biologically active in electrophysiological assays and attracted not only P. lata but also several other Parcoblatta species in pine forests, underscoring its utility in monitoring several endemic wood cockroach species in red-cockaded woodpecker habitats. }, number={8}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Eliyahu, D. and Nojima, S. and Santangelo, R. G. and Carpenter, S. and Webster, F. X. and Kiemle, D. J. and Gemeno, C. and Leal, W. S. and Schal, C.}, year={2011}, month={Dec}, pages={E490–E496} } @article{booth_santangelo_vargo_mukha_schal_2011, title={Population Genetic Structure in German Cockroaches (Blattella Germanica): Differentiated Islands in an Agricultural Landscape}, volume={102}, ISSN={0022-1503 1465-7333}, url={http://dx.doi.org/10.1093/jhered/esq108}, DOI={10.1093/jhered/esq108}, abstractNote={Although a number of species live syanthropically with humans, few rely entirely on humans for their survival and distribution. Unlike other cosmopolitan human commensals, the German cockroach (Blattella germanica), an insect of both public and livestock health concern, is considered incapable of dispersal outside human dwellings. Patterns of genetic association are therefore constrained and may not be associated with distance. Analogies with other human-commensal species are therefore impossible to draw with any degree of accuracy. In the past 2 decades, B. germanica has become a prominent pest within the US swine production system. Swine production is mainly carried out through contracted producers, each associated with a management company. It has been hypothesized that cockroach populations will be genetically structured based on association to a specific management company. Here, we tested this hypothesis using microsatellite genotypes (8 polymorphic loci) from 626 individual cockroaches collected from 22 farms in southeastern North Carolina representing 3 management companies. Significant genetic differentiation was detected (F(ST) = 0.171), most of which was partitioned among the 22 farms rather than the 3 management groups. All pair-wise population comparisons yielded F(ST) values significantly greater than zero. Our results reveal that structure does not correspond to management company of origin, but instead it may be regional and influenced strongly by the unintentional movement of cockroaches by farm workers.}, number={2}, journal={Journal of Heredity}, publisher={Oxford University Press (OUP)}, author={Booth, W. and Santangelo, R. G. and Vargo, E. L. and Mukha, D. V. and Schal, C.}, year={2011}, month={Mar}, pages={175–183} } @article{crissman_booth_santangelo_mukha_vargo_schal_2010, title={Population genetic structure of the German cockroach (Blattodea: Blattellidae) in apartment buildings}, volume={47}, DOI={10.1603/me09036}, abstractNote={The German cockroach, Blattella germanica (L.) (Blattodea: Blattellidae), is a major residential pest with the potential to vector various pathogens and produce and disseminate household allergens. Understanding population genetic structure and differentiation of this important pest is critical to efforts to eradicate infestations, yet little is known in this regard. Using highly polymorphic microsatellite markers, we investigated patterns of genetic diversity and differentiation within and among 18 apartments from six apartment complexes located in Raleigh, NC. No departure from panmixia was found between rooms within apartments, indicating that active dispersal resulting in gene flow may occur among rooms within apartment units. Alternatively, aggregations within apartments may exist in relative isolation under a metapopulation framework, derived from a recent, common source. Thus, in the event of population control practices leading to incomplete cockroach eradication within an apartment, recolonization of shelters and rooms is likely to occur from a genetically similar aggregation. A pattern of isolation-by-distance across the six apartment complexes indicated that dispersal was more common within complexes than among them, and F statistics suggested greater genetic similarity between apartments in a single building than between separate buildings of an apartment complex. Similarly, neighbor-joining tree and Bayesian clustering analyses were able to cluster only those apartments that were within a single building, indicating higher dispersal with associated gene flow within buildings than between them. The lack of any broader connectivity, as indicated by significant FST and G-tests suggests that human-mediated dispersal of B. germanica between buildings of an apartment complex or between complexes occurs infrequently enough to have negligible effects on gene flow.}, number={4}, journal={Journal of Medical Entomology}, author={Crissman, J. R. and Booth, W. and Santangelo, R. G. and Mukha, D. V. and Vargo, E. L. and Schal, Coby}, year={2010}, pages={553–564} } @article{groot_blanco_classen_inglis_santangelo_lopez_heckel_schal_2010, title={Variation in Sexual Communication of the Tobacco Budworm, Heliothis virescens}, volume={35}, ISSN={["2162-2647"]}, DOI={10.3958/059.035.0317}, abstractNote={Abstract. Females of the tobacco budworm, Heliothis virescens (F.), exhibit distinct geographical and temporal variation in sex pheromone composition, but the causes and significance of this variation are largely unexplored. Here we assessed whether 1) female pheromone variation was related to the host plants of origin, and 2) pheromone lures with varying amounts of Z9–14:Ald or 16:Ald were differentially attractive to males. Variation in female pheromone did not seem to be related to the host plants from which the eggs or larvae were collected, which may be because field-collected larvae were reared for three to five larval stages on artificial diet. By varying the concentration of Z9–14:Ald within the range in the female pheromone gland, we found males were more attracted as the amount increased from 1 to 10% relative to Z11–16:Ald, but significantly less with the highest concentration of 25%. In contrast, with 16:Ald, similar numbers of tobacco budworm males were caught in all traps where 16:Ald ranged from 0 to 200%. These results show that variation in Z9–14:Ald but not 16:Ald is evolutionary significant and likely subject to stabilizing selection in the field.}, number={3}, journal={SOUTHWESTERN ENTOMOLOGIST}, author={Groot, Astrid T. and Blanco, Carlos A. and Classen, Alice and Inglis, Ollie and Santangelo, Richard G. and Lopez, Juan and Heckel, David G. and Schal, Coby}, year={2010}, month={Sep}, pages={367–372} } @misc{groot_inglis_bowdridge_santangelo_blanco_lopez_teran vargas_gould_schal_2009, title={GEOGRAPHIC AND TEMPORAL VARIATION IN MOTH CHEMICAL COMMUNICATION}, volume={63}, ISSN={["1558-5646"]}, DOI={10.1111/j.1558-5646.2009.00702.x}, abstractNote={In moth pheromone communication signals, both quantitative and qualitative intraspecific differences have been found across geographic regions. Such variation has generally been hypothesized to be due to selection, but evidence of genetic control of these differences is largely lacking. To explore the patterns of variation in pheromone signals, we quantified variation in the female sex pheromone blend and male responses of two closely related noctuid moth species in five different geographic regions for 2–3 consecutive years. We found significant variation in the ratios of sex pheromone blend components as well as in male response, not only between geographic regions but also within a region between consecutive years. The temporal variation was of a similar magnitude as the geographic variation. As far as we know, this is the first study reporting such temporal variation in moth chemical communication systems. The geographic variation seems to at least partly be controlled by genetic factors, and to be correlated with the quality of the local chemical environment. However, the pattern of temporal variation within populations suggests that optimization of the pheromonal signal also may be driven by within-generation physiological adjustments by the moths in response to their experience of the local chemical environment.}, number={8}, journal={EVOLUTION}, author={Groot, Astrid T. and Inglis, Olive and Bowdridge, Scott and Santangelo, Richard G. and Blanco, Carlos and Lopez, Juan D., Jr. and Teran Vargas, Antonio and Gould, Fred and Schal, Coby}, year={2009}, month={Aug}, pages={1987–2003} } @article{groot_estock_horovitz_hamilton_santangelo_schal_gould_2009, title={QTL analysis of sex pheromone blend differences between two closely related moths: Insights into divergence in biosynthetic pathways}, volume={39}, ISSN={["1879-0240"]}, DOI={10.1016/j.ibmb.2009.05.002}, abstractNote={To understand the evolution of premating signals in moths, it is important to know the genetic basis of these signals. We conducted Quantitative Trait Locus (QTL) analysis by hybridizing two noctuid moth species, Heliothis virescens (Hv) and Heliothis subflexa (Hs), and backcrossing the F(1) females to males of both parental species. One of these backcrosses (F(1) x Hs) was a biological replicate of our previous study (Sheck et al., 2006) and served to test the robustness of our previous findings. The backcross to Hv was designed to reveal QTL with recessive inheritance of the Hv character state. This study confirms previously discovered QTL, but also reports new QTL. Most importantly, we found relatively large QTL affecting Z9-16:Ald, the critical sex pheromone component of Hs. For Z9-14:Ald, the critical sex pheromone component of Hv, as well as for the minor pheromone compound 14:Ald, we found QTL in which the change in pheromone ratio was opposite-to-expected. Linking QTL to the biosynthetic pathways of the pheromone compounds of Hv and Hs implicates several candidate genes in the divergence of these premating signals, the most important of which are acetyl transferase, one or more desaturase(s), and a fatty acyl reductase or alcohol oxidase.}, number={8}, journal={INSECT BIOCHEMISTRY AND MOLECULAR BIOLOGY}, author={Groot, Astrid T. and Estock, Marie L. and Horovitz, Joy L. and Hamilton, Jennifer and Santangelo, Richard G. and Schal, Coby and Gould, Fred}, year={2009}, month={Aug}, pages={568–577} } @article{sever_arbes_gore_santangelo_vaughn_mitchell_schal_zeldin_2007, title={Cockroach allergen reduction by cockroach control alone in low-income urban homes: A randomized control trial}, volume={120}, ISSN={0091-6749}, url={http://dx.doi.org/10.1016/j.jaci.2007.07.003}, DOI={10.1016/j.jaci.2007.07.003}, abstractNote={BackgroundWe previously reported significant reductions in cockroach allergen concentrations in urban homes by reducing cockroach infestations.ObjectiveTo determine the effectiveness of pest control performed by professional entomologists, compared with commercial companies, in reducing cockroach allergen.MethodsThis 3-arm randomized controlled trial enrolled 60 cockroach-infested homes in North Carolina. Homes were randomly assigned to a control group or 1 of 2 treatment groups. Treatment 1 had insecticide baits placed by entomologists from North Carolina State University. Treatment 2 received pest control from a randomly assigned commercial company. Vacuumed dust sampling and cockroach trapping were conducted at 0, 6, and 12 months. Dust samples were analyzed by ELISA.ResultsIn treatment 1 homes, there were significant reductions in geometric mean trap counts compared with control and treatment 2 homes at 12 months. Relative to control, significant 12-month reductions in Bla g 1 were evident in treatment 1 homes at all sampled sites, except bedroom floor. From baseline to month 12, geometric mean Bla g 1 concentrations (U/g) decreased from 64.2 to 5.6 in kitchen, 10.6 to 1.1 in living room, 10.7 to 1.9 on bedroom floor, and 3.6 to 2.3 in bed. Treatment 2 homes showed no significant 12-month allergen reductions versus control.ConclusionReductions in Bla g 1 in cockroach-infested homes can be achieved by reducing infestations; however, the magnitude of allergen reduction is dependent on the thoroughness and effectiveness of cockroach eradication efforts.Clinical implicationsElimination of cockroaches is an effective method for reducing exposure to cockroach allergen. We previously reported significant reductions in cockroach allergen concentrations in urban homes by reducing cockroach infestations. To determine the effectiveness of pest control performed by professional entomologists, compared with commercial companies, in reducing cockroach allergen. This 3-arm randomized controlled trial enrolled 60 cockroach-infested homes in North Carolina. Homes were randomly assigned to a control group or 1 of 2 treatment groups. Treatment 1 had insecticide baits placed by entomologists from North Carolina State University. Treatment 2 received pest control from a randomly assigned commercial company. Vacuumed dust sampling and cockroach trapping were conducted at 0, 6, and 12 months. Dust samples were analyzed by ELISA. In treatment 1 homes, there were significant reductions in geometric mean trap counts compared with control and treatment 2 homes at 12 months. Relative to control, significant 12-month reductions in Bla g 1 were evident in treatment 1 homes at all sampled sites, except bedroom floor. From baseline to month 12, geometric mean Bla g 1 concentrations (U/g) decreased from 64.2 to 5.6 in kitchen, 10.6 to 1.1 in living room, 10.7 to 1.9 on bedroom floor, and 3.6 to 2.3 in bed. Treatment 2 homes showed no significant 12-month allergen reductions versus control. Reductions in Bla g 1 in cockroach-infested homes can be achieved by reducing infestations; however, the magnitude of allergen reduction is dependent on the thoroughness and effectiveness of cockroach eradication efforts.}, number={4}, journal={Journal of Allergy and Clinical Immunology}, publisher={Elsevier BV}, author={Sever, Michelle L. and Arbes, Samuel J., Jr. and Gore, J. Chad and Santangelo, Richard G. and Vaughn, Ben and Mitchell, Herman and Schal, Coby and Zeldin, Darryl C.}, year={2007}, month={Oct}, pages={849–855} } @article{groot_santangelo_ricci_brownie_gould_schal_2007, title={Differential attraction of Heliothis subflexa males to synthetic pheromone lures in eastern US and western Mexico}, volume={33}, ISSN={["1573-1561"]}, DOI={10.1007/s10886-006-9233-6}, abstractNote={The mate attraction signal of Heliothis subflexa (Hs) females consists of a multicomponent sex pheromone blend. In this study, we assessed the intraspecific importance of three groups of compounds found in Hs pheromone glands: three acetate esters (Z7-16:OAc, Z9-16:OAc, and Z11-16:OAc), two 14-carbon aldehydes (14:Ald and Z9-14:Ald), and one 16-carbon alcohol (Z11-16:OH). Because the relative importance of pheromone components may vary in different regions, we conducted experiments in Eastern US (North Carolina) and Western Mexico (Jalisco). Our experiments in Eastern US showed that when the acetates were omitted from a 7-component blend in rubber septa, fewer males were caught in cone traps. Subsequent experiments conducted both in Eastern US and Western Mexico indicated that the addition of Z9-16:OAc alone does not increase attraction of male Hs, while Z11-16:OAc does. The Hs male response to Z7-16:OAc differed between the two regions. In Eastern US, significantly more males were attracted to a minimal three-component blend to which Z7-16:OAc was added, but this was not the case in Western Mexico. The two 14-carbon aldehydes also showed differential attraction between the two regions. 14:Ald and Z9-14:Ald appeared not to play any role in the sexual communication of Hs in Eastern US, but reduced trap catches in Western Mexico. The alcohol Z11-16:OH was tested in two concurrent dose-response studies with Hs males in Western Mexico, one using a minimal blend and one using a complete blend. The minimal three-component blend provided a more discriminating tool for delineating dose-response effects of Z11-16:OH than the seven-component blend. In the minimal blend, the optimal dose of Z11-16:OH was 1%, while in the complete blend similar numbers of males were caught when the alcohol ranged from 1 to 25%.}, number={2}, journal={JOURNAL OF CHEMICAL ECOLOGY}, author={Groot, A. T. and Santangelo, R. G. and Ricci, E. and Brownie, C. and Gould, F. and Schal, Coby}, year={2007}, month={Feb}, pages={353–368} } @article{groot_horovitz_hamilton_santangelo_schal_gould_2006, title={Experimental evidence for interspecific directional selection on moth pheromone communication}, volume={103}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.0508609103}, abstractNote={The chemical composition of the sexual communication signals of female moths is thought to be under strong stabilizing selection, because females that produce atypical pheromone blends suffer lower success in finding mates. This intraspecific selection pressure cannot explain the high diversity of moth pheromone blends found in nature. We conducted experiments to determine whether communication interference from males of closely related species could exert strong enough directional selection to cause evolution of these signals. Attraction and mating success ofHeliothis subflexa(Hs) females with a normal quantitative trait locus for production of acetate pheromone components (norm-OAc) were compared with Hs females with an introgressed quantitative trait locus fromHeliothis virescens(Hv) that dramatically decreased the amount of acetate esters in their pheromone glands (low-OAc). In field experiments with natural Hv and Hs populations, 10 times more Hv males were captured in traps baited with live low-OAc Hs females than in traps with norm-OAc Hs females. This pattern was confirmed in mate-choice assays in cages. Hybrids resulting from Hv–Hs matings have effectively zero fitness in the field. Combining our results with the extensive data set gathered in the past 40 years on the reproductive biology of Hv, we can quantitatively estimate that the directional selection exerted by Hv males on Hs females to produce relatively high amounts (>5%) of acetates can range from 0.135 to 0.231. Such intense interspecific selection may counteract intraspecific stabilizing selection that impedes evolutionary changes in pheromone blends and could lead to diversification of sexual signals.}, number={15}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Groot, AT and Horovitz, JL and Hamilton, J and Santangelo, RG and Schal, C and Gould, F}, year={2006}, month={Apr}, pages={5858–5863} } @article{groot_ward_wang_pokrzywa_o’brien_bennett_kelly_santangelo_schal_gould_2004, title={Introgressing pheromone QTL between species: Towards an evolutionary understanding of differentiation in sexual communication}, volume={30}, ISSN={["1573-1561"]}, DOI={10.1007/s10886-004-7946-y}, abstractNote={As a first step toward understanding how noctuid moths evolve species-specific pheromone communication systems, we hybridized and backcrossed two closely related moth species, Heliothis virescens (Hv) and H. subflexa (Hs), which differ qualitatively and quantitatively in their multi-component sex pheromone blends. We used amplified fragment length polymorphism (AFLP) marker-based mapping of backcross families to determine which of the 30 autosomes in these moths contained quantitative trait loci (QTL) controlling the percentages of specific chemical components in the pheromone blends. In two previous backcrosses to Hs, we found a strong depressive effect of Hv-chromosome 22 on the percentage of three acetate components in the pheromone gland. These acetates are present in Hs and absent in Hv. Here, we describe how we introgressed Hv-chromosome 22 into the genomic background of Hs. Selection for Hv-chromosome 22 started from backcross 3 (BC3) females. All females that had Hv-chromosome 22 and a low percentage of acetates (< 3% of the total amount of pheromone components present) were backcrossed to Hs males. In BC5 to BC8, we determined whether Hv-chromosome 22 was present by a) running only the primer pairs that would yield the markers for that chromosome, and/or b) determining the relative percentages of acetates in the pheromone glands. Either or both genotype and phenotype were used as a criterion to continue to backcross these females to Hs males. In BC9, we confirmed the isolation of Hv-chromosome 22 in the Hs genomic background, and backcrossed the males to Hs females to eliminate the Hv-sex chromosome as well as mitochondrial DNA. The pheromone composition was determined in BC3, BC5, and BC11 females with and without Hv-chromosome 22. All backcross females with Hv-chromosome 22 contained significantly less acetates than females without this chromosome. In addition, BC3 females with Hv-chromosome 22 contained significantly more Z11-16:OH than BC3 females without Hv-chromosome 22. However, in BC5 and BC11 females, the correlation between Z11-16:OH and Hv-chromosome 22 was lost, suggesting that there are separate QTL for the acetates and for Z11-16:OH, and that the relative amount of the alcohol component is only affected in epistasis with other (minor) QTL. Now that we have succeeded in isolating the chromosome that has a major effect on acetate production, we can test in behavioral experiments whether the presence of acetates may have been a driving force for a shift in pheromone composition. Such tests are necessary to move towards an evolutionary understanding of the differentiation in sexual communication in Heliothis spp. moths.}, number={12}, journal={Journal of Chemical Ecology}, author={Groot, A.T. and Ward, C. and Wang, J. and Pokrzywa, A. and O’Brien, J. and Bennett, J. and Kelly, J. and Santangelo, R.G. and Schal, C. and Gould, F.}, year={2004}, pages={2495–2514} } @article{gore_zurek_santangelo_stringham_watson_schal_2004, title={Water solutions of boric acid and sugar for management of German cockroach populations in livestock production systems}, volume={97}, ISSN={["1938-291X"]}, DOI={10.1603/0022-0493-97.2.715}, abstractNote={Pest management in conÞnement swine production relies primarily on calendar-based applications of broad-spectrum insecticides. However, regulatory restrictions imposed by the U.S. Food Quality Protection Act of 1996, the large Þnancial obligation of pesticide registration, and development of insecticide resistance have led to a renewed search for alternative control methods. Boric acid dust has long served as an insecticide in urban pest management and has been shown an effective alternative for use in sensitive environments such as swine production. However, dust formulations are difÞcult to apply and require specialized equipment. The purpose of this study was to evaluate the efÞcacy of liquid baits containing boric acid for the control of German cockroaches in a commercial swine nursery. Bait, consisting of 1 or 2% boric acid and 0.5 M sucrose, was deployed in 21 bait delivery tubes per room. Results of a 2-yr study showed signiÞcant reductions in cockroach populations. When baits were withdrawn in the summer, the cockroach population increased signiÞcantly faster than when the baits were removed during the winter. These data indicate that liquid formulations of boric acid effectively reduce the burden of cockroach infestation in swine production. This approach should have applications in structures in other urban and agricultural environments.}, number={2}, journal={JOURNAL OF ECONOMIC ENTOMOLOGY}, author={Gore, JC and Zurek, L and Santangelo, RG and Stringham, SM and Watson, DW and Schal, C}, year={2004}, month={Apr}, pages={715–720} }