BIOLOGY, PHYSIOLOGY, AND MANAGEMENT OF URBAN ARTHROPOD PESTS IN ALABAMA

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 1017844
• Project Start Date: Oct 18, 2018
• Project End Date: Sep 30, 2023
• Program Code: [(N/A)]- (N/A)

Recipient Organization
AUBURN UNIVERSITY
108 M. WHITE SMITH HALL
AUBURN,AL 36849

Performing Department
Entomology

Non Technical Summary
This project focuses on understanding the biology and physiology of urban arthropod pests that live in and around our homes. The structural pest control industry in the U.S. generated an estimated $8.6 billion in total service revenue in 2017 and is increasing at approximately 5% per year. In addition, homeowners purchase >$2 billion in over the counter insecticide products to control household pests. The goal of this project is to develop and implement safe, biologically based, and cost-effective integrated pest management (IPM) systems for control of urban arthropod pests. Specific objectives are to: 1) Determine the effects of insecticides, relative humidity, and temperature on the energetics, respiration patterns, and water relations of urban arthropod pests, 2) Develop and validate laboratory bioassays that estimate field efficacy of insecticides, repellents, and environmental modifications used to control urban arthropod pests, and 3) Develop integrated control systems for urban arthropod pests. This project addresses the goals of the USDA-NIFA and the National IPM Roadmap, and will identify low inputIPM tactics that will reduce pesticide use in and around homes, reduce human health risks, and minimize adverse effects of toxic conventional insecticides on urban ecosystems and wildlife.

Animal Health Component

30%

Research Effort Categories

Basic

70%

Applied

30%

Developmental

0%

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
721	3199	1130	50%
216	5220	1020	50%

Knowledge Area
216 - Integrated Pest Management Systems; 721 - Insects and Other Pests Affecting Humans;

Subject Of Investigation
3199 - Invertebrates, general/other; 5220 - Pesticides;

Field Of Science
1130 - Entomology and acarology; 1020 - Physiology;

Keywords

urban pest management

insect physiology

house and landscape characteristics

Goals / Objectives
The overall goal of this project is to identify key aspects of the biology, physiology, and ecology of urban arthropod pests that can be used to develop IPM systems for their management. Specific objectives include 1) determining the effects of insecticides, relative humidity, and temperature on the energetics, respiration patterns, and water relations of urban arthropod pests, 2) developing and validating laboratory bioassays that estimate field efficacy of insecticides, repellents, and environmental modifications used to control urban arthropod pests, and 3) developing integrated control systems for urban arthropod pests.

Project Methods
Objective 1.Determine the effects of insecticides, relative humidity, and temperature on the energetics, respiration patterns, and water relations of urban arthropod pests.Closed-system RespirometryOxygen consumption and CO2 production will be measured using a closed-system method described by Lighton (1991). Respirometers will be placed into temperature controlled environmental chambers (10-40°C at 5°C intervals). Arthropods will be examined periodically during incubation and only data from inactive individuals (for standard metabolic rate) will be included.Flow-through RespirometryAn individual arthropod will be confined in 50 ml glass respirometer chambers. Dry, CO2-free outside air will be pulled through the respirometer at 100 ml min-1 and O2 , CO2, and water vapor concentrations in the excurrent air stream will be recorded at 1-2 sec intervals and converted to STP-corrected VO2 (ml g-1 h-1), andVO2 (mg/h) using ExpeData software. The effects of insecticides on arthropod respiration and water loss will be determined by confining individuals to insecticide treated surfaces within flow-through respirometers or by dosing individuals with insecticide diluted in acetone.Calculations and Statistical AnalysisSummary statistics and analysis will be performed with SAS (SAS Institute, 1985) or SigmaStat (Jandel Scientific 1994). Regression will also be used to relate incubation temperature to log-transformed VO2 and VCO2 (ml g-1 h-1). The proportional increase in VO2 and VCO2 over a 10°C increase in temperature or Q10 will be calculated. Analysis of variance will be used to compare RQ's among temperatures.Objective 2.Develop and validate laboratory bioassays that estimate field efficacy of insecticides, repellents, and environmental modifications used to control urban arthropod pests.The repellency of various insecticides, repellents, temperatures, relative humidities, and mulches to arthropod pests will be evaluated in Ebeling choice boxes (Ebeling et al. 1966, 1968). The choice box is a square wooden box divided into two equal compartments one compartment is maintained in darkness, and the other is exposed to a photoperiod. Pests can move between the compartments; a treatment (insecticide, repellent, or environmental modification) will be placed in the dark compartment and living pests found in the illuminated compartment during the photophase are considered to be repelled.Randomized complete block designs with a factorial arrangement of treatments will be used. Treatments will include selected combinations of insecticides, temperatures, humidities, and mulches. Temperatures and humidities will encompass the range of microclimates in mulches used in the southern region. A minimum of six replicates each containing 10-20 cockroaches will be used for each treatment.A performance index (PI) (Rust and Reierson 1978) will be calculated from choice box data as an estimate of potential field performance of insecticides and environmental conditions. The PI is expressed as a unit less number between -100 and 100. The mean daily PI of each treatment and a control will be plotted over time. The change in PI over time will be estimated by nonlinear regression (SAS Institute 1985). A rectangular hyperbolic model of the form:PI = (PIMax · Day)/(t PI/2 + Day)where PIMax is the horizontal asymptote (maximum PI) and t PI/2 is the day at which 50% of the PIMax is reached will be used. Because this function begins at the point [0, 0], data will be coded accordingly. Estimates and standard errors of PIMax and t PI/2 will be generated and compared by overlap of the estimates ± 2SE.Field tests will be conducted in and around arthropod infested apartments and homes. Taylor's power law analysis will provide the distribution pattern parameters to calculate the number of apartments needed to compare IPM strategies reliably and determine the efficacy of new insecticides. The effectiveness of various treatments in reducing target pest trap catch will be determined relative to untreated control units using ANOVA of log or square root transformed trap catch.Objective 3.Develop integrated control systems for urban arthropod pests.IPM strategies such as debris removal and mulch management, and new insecticides will be evaluated in and around infested homes using the trapping methods described earlier. Sticky traps will be used to monitor cockroach populations. Five to 20 traps will be placed in the kitchen of each apartment and evaluated before treatment and 1, 2, 4, 8, and 12 weeks after treatment. Following the trapping before treatment, treatments will be randomly assigned to individual apartments with catches >10 cockroaches per apartment so that the initial cockroach population size and distribution will be equivalent among treatments. Because trap count data are not usually normally distributed, counts will be converted to percentage reduction for each apartment. Percentage reductions will be ranked for each week of each field trial and ranks will be analyzed by Wilcoxon's Signed-ranks Test.The correlation between perimeter pest abundance and diversity, and house and landscape characteristics will be examined at 40 homes in Auburn-Opelika, AL. Perimeter pest abundance will be measured biweekly from May through October (Smith et al. 1995a,b). Wide-mouth glass jars will be used to measure cockroach abundance; ant abundance will be measured using honey and hotdog baited traps, and termites will be captured in wood-baited bucket traps. Twelve traps will be positioned at selected locations on the outside of homes against walls and near potential hiding places. Traps will be placed against a vertical surface such a fence, tree, or shrub to maximize catch. Catch will be counted in situ and the age class of individuals recorded (Benson 1988, Brenner 1988).The following house and landscape characteristics will be recorded at each home:Trees: species, diameter at breast height, diameter of canopy cover, presence and number of tree holes, distance from house, light intensity under canopies measured under standardized conditions.Shrubs: species, volume, distance from house.Mulches: specific type of mulch, area covered, average thickness, distance from house.Objects: type of object (woodpile, masonry grill, outbuilding, etc.), area covered, volume, distance from house.Lawn cover: area, percent coverage of total area.Cardinal direction relative to the house will also be noted for each of the above as will GPS coordinates; southern and eastern exposures increase the favorability of mulches to cockroaches next to simulated houses (Smith et al. 1993). Multivariate techniques will be used (principal components analysis and detrended correspondence analysis) to reduce complexity of the data. The techniques produce linear combinations of variables and combinations that best describe perimeter pest habitat (i.e., correlations between cockroach abundance and environment) will be added to a predictive model. The refined model will be validated with jackknife bias correction methods and bootstrap confidence intervals. Of the 40 homes to be included in the study, 10 will be selected randomly for model validation.The refined model will identify additional house and landscape characteristics that alter abundance of perimeter pests. It will also rank these characteristics for each of the 40 homes based on their effect on abundance. Average values of individual characteristics will be input into the model to calculate their relative importance. This method will reveal which characteristics influence abundance and diversity of perimeter pests the most. The sensitivity of the model to changes in each landscape characteristic will also be analyzed. For example, will removing an outbuilding decrease abundance of perimeter pests more or less than filling in tree holes?

Progress 10/01/20 to 09/30/21

Outputs
Target Audience:The target audience for this research includes both undergraduate and graduate students (for classroom lectures and discussions), pest management professionals (PMPs), and other professional urban entomologists, insect physiologists, and insect behaviorists. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Results from this research have been presented to pest management professionals as well as undergraduate and graduate students. How have the results been disseminated to communities of interest?Results have been presented to pest management professionals at the Alabama Pest Control Association winter and summer meetings and at meetings of the Entomological Society of America. What do you plan to do during the next reporting period to accomplish the goals?Continued studies on the toxicity and repellency of conventional insecticides and essential oil products are planned for the next reporting period.

Impacts
What was accomplished under these goals? Effective control of domestic and peridomestic cockroaches requires integrated approaches that emphasize concurrent use of chemicals with alternative control tactics. An integrated pest management (IPM) approach is particularly justified in environments where satisfactory cockroach control cannot be achieved due to multiple factors including the development of insecticide aversion and resistance in some cockroach species, and poor sanitation or structural issues that foster infestations. While a flurry of research efforts have been devoted to studying alternative tactics for cockroach control, only a few of them have been evaluated in the context of IPM programs. This review focuses on examining studies on alternative tactics that are proven efficacious, economical, and logistically feasible for their inclusion in IPM programs for important domestic and peridomestic cockroaches in the USA. Management programs that educate the public on cockroach biology, behavior, and the importance of sanitation; use of traps to monitor infestation levels; apply targeted low impact insecticides such as baits, have demonstrated a greater success for effective and sustainable control of cockroaches when compared to an insecticide-only approach. Incorporation of other alternative control methods into IPM programs will require more applied research that validates their use in real-world scenarios and demonstrates their cost-effectiveness.

Publications

• Type: Book Chapters Status: Published Year Published: 2021 Citation: Appel, A. G. 2021. Biology, nutrition, and physiology. pp. 53-74. In Changlu Wang, Chow-Yang Lee, and Michael K. Rust (eds.), Biology and Management of the German Cockroach. CSIRO Publishing, Australia.
• Type: Book Chapters Status: Published Year Published: 2021 Citation: Appel, A. G. and M. K. Rust. 2021. German cockroach management using baits. pp. 213-230. In Changlu Wang, Chow-Yang Lee, and Michael K. Rust (eds.), Biology and Management of the German Cockroach. CSIRO Publishing, Australia.
• Type: Journal Articles Status: Published Year Published: 2021 Citation: Gondhalekar, A. D., A. G. Appel, G. M. Thomas, and A. Romero. 2021. A Review of Alternative Management Tactics Employed for the Control of Various Cockroach Species (Order: Blattodea) in the USA. Insects. 12(6), 550; https://doi.org/10.3390/insects12060550
• Type: Journal Articles Status: Accepted Year Published: 2021 Citation: Appel, A.G., B. N. Dingha, M. J. Eva, and L. E. N. Jackai. 2021. Toxicity, repellency, and laboratory performance of consumer bait products for German cockroach (Blattodea: Ectobiidae) management. Florida Entomologist.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:Target audience for this research includes both undergraduate and graduate students (for classroom lectures and discussions), pest management professionals (PMPs), and other professional urban entomologists, insect physiologists, and insect behaviorists Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Results from this research have been presented to pest management professionals as well as undergraduate and graduate students. How have the results been disseminated to communities of interest?Results have been presented to pest management professionals at the Alabama Pest Control Association winter and summer meetings and at meetings of the Entomological Society of America. What do you plan to do during the next reporting period to accomplish the goals?Continued studies on the toxicity and repellency of conventional insecticides and essential oil products are planned for the next reporting period.

Impacts
What was accomplished under these goals? The high surface area to volume ratio of terrestrial insects makes them highly susceptible to desiccation mainly through the cuticle. Cuticular permeability (CP) is usually the most important factor limiting water loss in terrestrial insects. Water loss rate, percentage of total body water (%TBW) content, CP, and desiccation tolerance were investigated in workers of four Solenopsis species in the southeastern USA. We hypothesized that tropical/subtropical ants (S. invicta and S.geminata) will have lower CP values and tolerate higher levels of desiccation than temperate ants(S. richteri and S. invicta × S. richteri). The %TBW content was similar among species. Solenopsis invicta had a 1.3-fold and 1.1-fold lower CP value than S. invicta × S. richteri and S. richteri, respectively. Solenopsis geminata had a 1.3-fold lower CP value than S. invicta × S. richteri, and a 1.2-fold lower CP value than S. richteri. The LT50 values (lethal time to kill 50% of the population) ranged from 1.5 h (small S. geminata) to 8.5 h (large S. invicta). Desiccation tolerance ranged between 36 and 50 %TBW lost at death and was not related to a species' location of origin. This study is the first report of water relations of S. invicta × S. richteri. It demonstrates that desiccation stress differentially can affect the survival of different Solenopsis species and implies that environmental stress can affect the distribution of these species in the southeastern USA. Water loss rate, percentage total body water content (%TBW), cuticular permeability (CP), and desiccation tolerance were investigated in adult and immature stages of the invasive kudzu bug, Megacopta cribraria (Fab.) (Hemiptera: Plataspidae), a serious soybean pest and an urban nuisance. Adults and all five nymphal instars were weighed prior to and 2, 4, 6, 8, 10, and 24 h after desiccated at 30 ± 1°C and 0-2% RH. Both % initial mass and %TBW loss increased linearly with time of desiccation. Rates of loss ranged from approximately 1-7%/h. Mortality occurred at 10 h after desiccation. Desiccation tolerance (%TBW lost at death) ranged between 25.6% for first-generation adult females and 75% for first-generation fifth-instar nymphs. First-generation first-instar nymphs had significantly greater %TBW (88.9%) than the other generations and instars, whereas second-generation fifth instars had the lowest %TBW (62.4%). The CP value of first-generation adult females (12.3 ± 1.6 µg cm-1 h-1 mmHg-1) was the greatest across generations. First-generation first instars had the greatest mass loss (111.11 mg/g) among all instars and generations, whereas overwintered second-generation adult females had the lowest mass loss (18.39) across generations. This study demonstrated that desiccation stress differentially affected the survival of adult and nymphal kudzu bugs and may imply that environmental stress can affect the relative abundance of this species in the fields and around homes. The use of essential oil components (EOCs) against the German cockroach, Blattella germanica (L.), has increasingly received attention from researchers. However, the determination of lethal doses/concentrations alone does not provide enough information on the range of biological effects of these EOCs. To improve our understanding of the potential effects of EOCs, we examined the biological parameters of B. germanica exposed to sublethal EOCs formulated in gels. This study employed superabsorbent polymer (SAP) gel to prolong bioavailability of limonene, carvacrol, and β-thujaplicin and evaluated how these EOCs shape biological parameters of B. germanica. Overall, median survival days ranged from 57 to 69.5 d for males and 73 to 99 d for females. The survival day ranking for the EOCs was limonene > β-thujaplicin > carvacrol. Carvacrol and β-thujaplicin gels reduced male longevity by at least 34 and 39%, respectively, while limonene had no effect. The longevity of females was reduced by limonene, but not by carvacrol and β-thujaplicin gels. EOCs significantly suppressed overall adult females' reproductive period, oothecal hatchability, reduced fecundity, and interoothecal period, but not the number of oothecae formed and egg incubation period. The preoviposition period (mean: 2-25 d) ranking was limonene < carvacrol < β-thujaplicin. Based on these results, limonene, carvacrol, and β-thujaplicin in SAP gels show promising potential to reduce adult male survival/longevity, suppress egg hatchability and female fecundity, and delay the interoothecal period. These findings may represent the basis for the practical use of EOCs as a tactic in integrated pest management systems for B. germanica.

Publications

• Type: Journal Articles Status: Published Year Published: 2020 Citation: Benk, G., P. J. Thompson, X. P. Hu, and A. G. Appel. 2020. Water loss and desiccation tolerance of the two yearly generations of adult and nymphal Kudzu bugs, Megacopta cribraria (Hemiptera: Plataspidae). Environ. Entomol. 49: 651-659.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Gardner, S. T., V. R. Assis, K. M. Smith, A. G. Appel, and M. T. Mendon�a. 2020. Innate immunity of Florida cane toads: how dispersal has affected physiological responses to LPS. Journal of Comparative Physiology B. 190: 317-327.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Ajayi, O. S., A. G. Appel, L. Chen, and H. Y. Fadamiro. 2020. Comparative cutaneous water loss and desiccation tolerance of four Solenopsis spp. (Hymenoptera: Formicidae) in the southeastern United States: implications for distribution patterns. Insects. 2020, 11, 418; doi:10.3390/insects11070418
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Oladipupo, S. O., X. P. Hu, and A. G. Appel. 2020. Topical toxicity profiles of some aliphatic and aromatic essential oil components against insecticide-susceptible and resistant strains of German cockroach (Blattodea: Ectobiidae). J. Econ Entomol. 113: 896-904.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Oladipupo, S. O., X. P. Hu, and A. G. Appel. 2020. Essential oil components in superabsorbent polymer gel modify reproduction of Blattella germanica (L.) (Blattodea: Ectobiidae). J. Econ. Entomol. 113: 2436-2447.

Progress 10/18/18 to 09/30/19

Outputs
Target Audience:Target audience for this research includes both undergraduate and graduate students (for classroom lectures and discussions), pest management professionals (PMPs), and other professional urban entomologists, insect physiologists, and insect behaviorists. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Results from this research have been presented to pest management professionals as well as undergraduate and graduate students. How have the results been disseminated to communities of interest?Results have been presented to pest management professionals at the Alabama Pest Control Association winter and summer meetings and at meetings of the Entomological Society of America. What do you plan to do during the next reporting period to accomplish the goals?Continued studies on the toxicity and repellency of conventional insecticides and essential oil products are planned for the next reporting period.

Impacts
What was accomplished under these goals? These results provide better understanding of how insecticides work against termites at different temperatures and concentrations that are relevant to homeowners and pest control professionals. Insecticides cause predictable changes in termite behavior before they kill. These behaviors are important to enable the spread of insecticide through a colony and kill it. If insecticides work too quickly, they cannot be transferred. If they work too slowly, they can be diluted and become ineffective. Understanding the biology and development of insects helps to develop accurate methods of predicting insect population growth and ultimately models that will help the timing of insecticide applications for superior control. We estimated the number of developmental stages (instars) of the invasive Asian cockroach and determined that it can have 2-3 generations per year in Alabama. We determined the toxicity of several essential oils against German cockroaches. Essential oils are popular and relatively safe compounds that are also used in perfume, cleaning agents, and as spices. These compounds can be toxic to German cockroaches, the most important insect pest in homes and apartments. Many essential oils are toxic and some are toxic to cockroaches that are resistant to conventional insecticides. Some of these essential oils however are detoxified by the same mechanisms as conventional inesticides. Behavioral symptoms and mortality associated with intoxication with the insecticides fipronil and indoxacarb were determined in field-collected eastern subterranean termites, Reticulitermes flavipes (Kollar), and Formosan subterranean termites, Coptotermes formosanus Shiraki. These termites are major economic pests throughout the southeastern United States and many other locations worldwide. Behaviors and mortality were evaluated at three temperatures (16, 22, and 28°C) and three concentrations of fipronil (0.5, 1, and 5 ppm) and indoxacarb (50, 75, and 100 ppm). LT50 (median lethal time to kill 50% of the termites) values declined with increasing concentrations and temperatures for both fipronil-exposed eastern and Formosan subterranean termites, whereas these values were not always the highest at 16°C for indoxacarb-treated termites. The greatest change (reduction) in LT50 values occurred for both species between 16 and 22°C at the lowest concentration of each insecticide. Intoxication and moribundity were the most frequently observed behaviors for fipronil-exposed termites, whereas intoxication, ataxia, and moribundity were observed for most concentration and temperature combinations for indoxacarb-exposed termites. The inherent toxicity of fipronil was higher than that of indoxacarb. The higher presence and duration of intoxication behaviors may positively affect the performance of indoxacarb against subterranean termite colonies. The Asian cockroach, Blattella asahinai Mizukubo, has expanded its range throughout the southeastern United States since its introduction into Florida. Unlike its closest relative, the German cockroach, Blattella germanica (L.), B. asahinai lives outdoors and can fly. There is little information on the biology and development of B. asahinai, including the number of instars during nymphal development. To estimate the number of instars of B. asahinai nymphs were photographed, sexed, and the lengths and widths of their pronota were measured digitally. The number of instars of B. asahinai was estimated using Gaussian mixture models with the pronotal data. The most probable model and its clusters were selected to assign individuals to an instar. Instars were also determined by counting the number of cercal annuli of nymphs. Both clustering and cercal annuli indicated that B. asahinai most frequently had six instars when reared at 30°C. Growth did not strictly follow the Brooks-Dyar Rule, because nymphs had different numbers of instars and different growth patterns. Although Gaussian mixture models are not efficient for field sampling experiments, digital measurements may provide a way to estimate instars with live specimens in development studies without handling the animals in a way that may alter growth. Toxicity profiles of four aliphatic (α-pinene, cyclononanone, limonene, nerolidol), four aromatic (β-thujaplicin, carvacrol, eugenol, tropolone) essential oil components (EOCs), and permethrin were investigated against three strains of German cockroach, Blattella germanica (L.). The strains include a susceptible strain (S), and two multi-resistant strains - strains D and E. Also, a synergism bioassay, using piperonyl butoxide (PBO) was conducted. The most toxic EOCs were aromatic EOCs carvacrol, eugenol, and tropolone, followed by aliphatic EOC limonene; all had LD50 values of <0.7 mg/μl. Four of the EOCs were equally toxic against all the strains, with carvacrol being the most toxic, followed by eugenol, tropolone, and α-pinene. The other four EOCs were more toxic against strain S than against the two resistant strains. Permethrin was significantly more toxic to strain S (LD50 = 0.056 μg/μl) compared with the resistant strains (D = 2.138 μg/μl, E = 1.730 μg/μl). Toxicity of aliphatic EOCs correlated positively with their molecular weight against strain E only, whereas both molecular weight and vapor pressure of aromatic EOCs correlated significantly with toxicity in all strains. Strain D exhibited the greatest resistance (RR of 6.7) to EOCs, and synergism to the aliphatic EOC cyclononanone. Clear synergism with PBO was observed in permethrin against resistant strains, but not in all of the EOCs, suggesting multiple resistance mechanisms in the resistant cockroaches. These findings give insight on the potential of EOCs to be incorporated as parts of an IPM approach to managing insecticide resistant German cockroaches

Publications

• Type: Journal Articles Status: Published Year Published: 2019 Citation: Quarcoo, F. Y., X. P. Hu, and A. G. Appel. 2019. Temperature-mediated variations in behavior and mortality caused by non-repellent insecticides in subterranean termites (Blattodea: Rhinotermitidae). Insects 10 (2), 37; 1-14.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Peterson, M. K., A. G. Appel, and X. P. Hu. 2019. Instar determination of Blattella asahinai (Blattodea: Ectobiidae) from digital measurements of the pronotum using Gaussian mixture modeling and the number of cercal annuli. J. Entomol. Sci. 19: 5; 1-14.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Oladipupo, S. O., X. P. Hu, and A. G. Appel. 2019. Topical toxicity profiles of some aliphatic and aromatic essential oil components against insecticide-susceptible and resistant strains of German cockroach (Blattodea: Ectobiidae). J. Econ Entomol. toz323, https://doi.org/10.1093/jee/toz323.