Recent attention focused on the risks associated with Zika virus and mosquito vectors, combined with demonstrated customer satisfaction for PMP mosquito service offerings, likely will increase the number of PMP barrier treatments applied in the U.S. suburban landscape (Grard et al. 2014, PCT 2015, Zanluca et al. 2015, Armstrong et al. 2016).
We, researchers at the University of Georgia, undertook three complementary studies examining PMP barrier treatments in suburban landscapes. Mosquitoes were sampled before and after treatments in field trials, including properties serviced by PMPs and research personnel. We also treated hedgerows in a nonresidential setting for further evaluation of efficacy related to residual activity. We hypothesized mosquito barrier treatments using backpack sprayers would result in a lower number of adult mosquitoes compared to untreated controls.
MATERIALS & METHODS. Our research was comprised of a variety of methodologies.
Property Owner Survey. A total of 53 property owners were given a survey inquiring about the time of day they were most likely to be outside, the amount of time they spent outside and their tolerance for mosquitoes. The survey results divided properties into categories with homeowners who reported a low tolerance for mosquitoes in their yard and those who had a higher tolerance.
Mosquito Sampling. There were three field experiments. Mosquito collection in all trials was conducted using a hand-held, commercially available vacuum device. The device was a LSWV36 Black & Decker 36V Lithium Hard Surface Sweeper Vac modified with a collection sleeve (60-cm x 60-cm; Mosquito Curtains Heavy Mosquito Curtain Netting) held in place with a rubber band (88-mm x 6-mm). The vacuum was slowly moved in and around all foliage from ground level to 6 feet in height on each property. All insects collected were confined in a collection sleeve, labeled by property and date, and the sleeve placed on ice. Upon return to the laboratory, samples were placed in a -20°C freezer for 15 minutes and emptied onto a white VERSI-DRY lab soaker paper (100-cm x 100-cm). Adult mosquitoes were identified to species and gender using dichotomous keys (Darsie and Ward 2005, Burkett-Cadena 2013).
Barrier Treatment Shadowing Study (PMP). We sampled 47 residences in this portion of the study, including 23 PMP-treated properties and 24 (2014 and 2015 respectively) control, untreated properties in the same neighborhoods. Solicitation of participants included a permission letter explaining the study. Properties were included only after obtaining a signed consent form. All residences were sampled twice a month for adult mosquitoes using the vacuum device along with visual examination of larval breeding sites and presence of larvae from July-October 2014 and May-October 2015.
We sampled mosquitoes on residential properties serviced by two pest management firms; one in Atlanta and one in Athens, Ga. Company 1 used bifenthrin and one technician treated all their residential properties sampled in 2014-15. Company 2 used a mixture of esfenvalerate, prallethrin, piperonyl butoxide and pyriproxyfen in 2014, while they used bifenthrin and a different technician to service the shadowed accounts in 2015.
Barrier treatments were applied monthly using a backpack mist blower (Stihl Model #SR420, Stihl Corp., Virginia Beach, Va.) according to protocols established by each company. Both companies applied 1.5% methoprene to obvious mosquito breeding sites including: catch basins, temporary pools and flower pot saucers. The amount of pesticide applied, property dimensions and weather data were recorded by treatment date for each company — and are available upon request from the authors.
Residential Treatments Conducted by Research Program Laboratory. We conducted a field trial complementing the PMP study. The previously described PMP-shadowing sampling protocol was employed at 9 and 15 residential structures in 2014 and 2015, respectively. Treatments in 2014 were replicated three times. They included a water-only control and two pyrethroid formulations, bifenthrin and deltamethrin, applied at the highest label rate (7.81mL/L and 11.72 mL/L per 92.9 m2, respectively). In 2015, two 25b products: one containing garlic oil and one containing an oil blend, were added to the list of treatments. Treatments were conducted using separate backpack mist blowers (Stihl Model # SR450, Stihl Corp., Virginia Beach, Va., or Solo Model #451, Solo Corp., Newport News, Va.) for each treatment. Pretreatment sampling was performed starting in July 2014 and May 2015. Treatments were applied in August. Post-treatment sampling was conducted one day after treatment and twice a month until November of both years.
Non-Residential Treatments Conducted by the Household and Structural Entomology Research Program Laboratory (hedgerow). The residual efficacy of foliar applications was further tested in experiments using 21 hedgerow sites bordering parking areas on the University of Georgia, Athens, campus. Artificial breeding sites consisting of black plastic oil pans filled three-fourths full of hay infusion were set out in April, inspected, refilled and the amount of larvae was recorded on a weekly basis. We sampled a greater number of replicates in 2015, thus, a greater amount of mosquitoes were caught that year. The five treatments included bifenthrin, deltamethrin, solutions of two 25b products — sodium lauryl sulfate, soybean oil and corn oil (oil blend), and garlic oil — plus a water-only control.
RESULTS. Researchers caught a variety of mosquitoes at a variety of sites.
Survey. The survey showed the outdoor activities of property owners were similar between the treated and untreated households (T-test P > 0.05). The majority stated they were outside in the evening (97% and 79%, treated and controls respectively) and spent more than two hours outdoors on a daily basis. Homeowners of treated properties expressed a significantly lower tolerance of mosquitoes (T-test P > 0.01) than control property owners. The majority of the treatment group (90%) stated zero mosquito bites was their tolerance limit, while 42% of the controls stated a limit of 100 bites and 46% stated greater than 20 bites. Ten percent of the treated property owners stated they will always have their yard treated, while 13% of control property owners stated they would never have their yard treated.
Barrier Treatment Shadowing Study (PMP). One hundred sixty-four mosquitoes were caught at residences during the two-year PMP shadowing study. Eighty mosquitoes were caught in 2014, with five Culex pipiens complex, one Culex restuans and 74 Aedes albopictus. All 84 mosquitoes caught in 2015 were Ae. albopictus. August provided the peak number of mosquitoes; 34 and 29, in 2014 and 2015, respectively.
The number of residences with potential mosquito breeding sites varied by year because, for example, three properties completed landscape changes in late 2014 that removed breeding sites. We caught mosquitoes at most control houses where we identified breeding sites. There were 47 control properties, if we consider each year separately, and 12 had visible breeding sites. We consistently caught mosquitoes at 13 structures in that timeframe. Therefore, 100% of properties with visible breeding sites provided adult mosquitoes, while one property without a visible breeding site provided adults. In 2014, we caught mosquitoes at eight control properties as opposed to 2015 when we caught mosquitoes at five controls. The data illustrate adult mosquitoes were usually found where larval breeding sites were present, and the amount of adults present decreased after the sites were treated.
Residential Treatments Conducted by the Household and Structural Entomology Research Program Laboratory (HSERP). We caught 162 mosquitoes at 18 properties over a two year-study period, with 113 mosquitoes in 2014 from nine properties with (98%) representing Ae. albopictus (n=111), 1 Cx. pipiens complex and 1 Cx. restuans. Despite the addition of six properties, the number of mosquitoes collected in 2015 was lower (n=45) with Ae. albopictus representing 91% and the remaining 9% were Aedes vexans (n=4).
These experiments and the PMP shadowing study showed two general trends. First, properties where we caught mosquitoes were likely to have mosquitoes on additional sampling dates, and a greater number of mosquitoes were caught in 2014 than 2015. Properties we treated with bifenthrin had fewer mosquitoes than properties with the other treatments (see Table 2). The bifenthrin and deltamethrin treatments also provided significantly fewer mosquitoes than the control, garlic oil and oil blend treatments (Nguyen 2016).
Non-Residential Treatments Conducted by the Household and Structural Entomology Research Program Laboratory (hedgerow). We caught 426 mosquitoes during the two-year study with Ae. albopictus comprising more than 93% of all mosquitoes caught in both years. We also caught three Cx. pipiens complex and two Cx. restuans in 2014, and 17 Ae. vexans and 2 Aedes j. japonicus in 2015.
The hedgerow data is indicative of the clumped distribution of Ae. albopictus populations we sampled throughout these trials. Despite providing and not treating larval breeding sites in this study, only 13 of 21 sites consistently provided adult mosquitoes. Three control sites had mosquitoes the day after treatment; the garlic oil and oil blend (25b) treatments had one day of no mosquitoes, while deltamethrin sites provided at least one week and bifenthrin two weeks.
DISCUSSION. Ae. albopictus, a potential vector of several human diseases, made up most of the mosquitoes caught in the three field trials and are the main human-biting pest species found in the Georgia Piedmont (Farajollahi and Nelder 2009, Sawabe et al. 2010, Faraji et al. 2014). We, however, also collected two other potential vectors: Cx. pipiens complex and Cx. restuans (Kilpatrick et al. 2005, Ciota and Kramer 2013). The sampling data highlight and validate concerns that often drive property owners to secure PMP mosquito control services, but this work has applicability only to backpack mist blower applied barrier treatments against Asian Tiger mosquito in a suburban setting (PCT 2015). The property owner survey clearly shows that the industry services customers who have a very low tolerance to being bitten by mosquitoes while people with a high tolerance will never contract for such service.
Barrier treatments as a PMP service offering for residential accounts have a reputation for customer satisfaction (PCT 2015). Data from our field trials indicate barrier sprays with pyrethroid insecticides impact the number of adult mosquitoes on residential properties (see Table 2 and Table 3). The PMP shadowing study showed properties that hired a monthly professional service using pyrethroid insecticide barrier treatments combined with insect growth regulator (IGR) applications to potential breeding sites were less likely to have adult mosquitoes than nearby properties without such service (see Table 3). A single adulticide application to hedgerows provided support for two to four weeks’ residual efficacy for the two pyrethroid products, but not the 25b products we tested. The hedgerow and residential properties treated by the research personnel did not provide evidence for more than one-week relief from adult mosquitoes because larval breeding sites were not treated (see Table 2).
Barrier spray treatments target adult mosquitoes. We purposely did not treat known larval breeding sites at the properties or hedgerows sprayed by the research personnel where we caught mosquitoes within a week of treatment (see Table 2 and Table 3). Those data reflect the two PMP-treated properties where we caught mosquitoes in 2014, but not in 2015 when serviced by a different technician (T-V Nguyen Personal Communication). Our data convey the importance of an Integrated Pest Management (IPM) approach to residential mosquito control, especially the need to identify the mosquito species and target potential larval mosquito breeding sites with appropriate interventions (American Mosquito Control Association 2009). Our data on potential breeding sites showed treatment and control properties had similar numbers, but we caught more adult mosquitoes at control than treatment properties. This supports recommendations that interventions involving breeding sites in addition to adulticiding are essential for effective control of Ae. albopictus that do not fly great distances (Pant 1979, Laird and Miles 1983, Bonizzoni et al. 2013).
An unexpected theme in our data was the proportion of residences where no mosquitoes were caught. The PMP-treated properties provided the highest proportion of 97% (58/60) properties with no mosquitoes over the course of the two-year study. The proportion of not-treated single-family suburban properties with no mosquitoes over the same time frame was 72% (34/47). Sixty-two percent of the properties treated by the research program did not have mosquitoes. In contrast, 29% of the hedgerows provided with breeding sites did not have mosquitoes. This point has implications for designing and evaluating residential mosquito management practices. We can state 60% of suburban residential properties in north Georgia do not have significant Ae. albopictus populations, with the caveat that our sampling technique was suitable to identify pestiferous mosquito populations (Nguyen 2016).
Our work supports previous studies showing barrier treatments with bifenthrin can significantly reduce adult Ae. albopictus populations and lends support to employing an IPM approach to backyard mosquito management (Cilek and Hallmon 2006, Doyle et al. 2009, Faraji et al. 2014). Technicians should inspect, identify and treat breeding sites on each visit followed by monthly monitoring for adult mosquitoes with a vacuum device. Adulticide barrier sprays should be performed on an as-needed basis, when sampling is positive or when the homeowner reports mosquitoes. Vacuum sampling is a consistent, real-time way of assessing the presence or absence of resting mosquitoes, and can be an integral part in validating an insecticide spray program. A best practices protocol using inspections and interventions aimed at reducing on-property breeding sites combined with a vacuum sampling regime to determine the need for foliar sprays on a presence/absence action threshold would allow PMPs to address their customers’ concerns, assuage environmental concerns about pesticide over-use and perhaps reduce costs by lowering insecticide use and time on site.
American Mosquito Control Association. 2009. Best Management Practices for Integrated Mosquito Managements.
Armstrong, P., M. Hennessey, M. Adams, C. Cherry, S. Chiu, A. Harrist, N. Kwit, L. Lewis, D. O. McGuire, T. Oduyebo, K. Russell, P. Talley, M. Tanner, and C. Williams. 2016. Travel-Associated Zika Virus Disease Cases Among U.S. Residents - United States, January 2015-February 2016. MMWR: Morbidity & Mortality Weekly Report 65: 286-289.
Bonizzoni, M., Gasperi, G., Chen, X., & James, A. A. (2013). The invasive mosquito species Aedes albopictus: current knowledge and future perspectives. Trends in Parasitology.
Burkett-Cadena, N. D. 2013. Mosquitoes of the southeastern United States, University of Alabama Press.
Cilek, J. E., and C. F. Hallmon. 2006. Residual effectiveness of pyrethroid-treated foliage against adult Aedes albopictus and Culex quinquefasciatus in screened field cages. Journal Of The American Mosquito Control Association 22: 725-731.
Ciota, A. T., and L. D. Kramer. 2013. Vector-Virus Interactions and Transmission Dynamics of West Nile Virus. Viruses (1999-4915) 5: 3021-3047.
Darsie, R. F., and R. A. Ward. 2005. Identification and Geographical Distribution of the mosquitoes of North America, North of Mexico, University Press of Florida.
Doyle, M. A., D. L. Kline, S. A. Allan, and P. E. Kaufman. 2009. Efficacy of residual bifenthrin applied to landscape vegetation against Aedes albopictus. Journal of the American Mosquito Control Association 25: 179-183.
Faraji, A., A. Egizi, D. M. Fonseca, I. Unlu, T. Crepeau, S. P. Healy, and R. Gaugler. 2014. Comparative Host Feeding Patterns of the Asian Tiger Mosquito, Aedes albopictus, in Urban and Suburban Northeastern USA and Implications for Disease Transmission. PLoS Neglected Tropical Diseases 8: 1-11.
Farajollahi, A., and M. P. Nelder. 2009. Changes in Aedes albopictus (Diptera: Culicidae) Populations in New Jersey and Implications for Arbovirus Transmission [electronic resource]. Journal of medical entomology 46: 1220-1224.
Grard, G., M. Caron, I. M. Mombo, D. Nkoghe, S. M. Ondo, D. Jiolle, D. Fontenille, C. Paupy, and E. M. Leroy. 2014. Zika virus in Gabon (Central Africa) - 2007: a new threat from Aedes albopictus? PLoS Neglected Tropical Diseases 8: e2681-e2681.
Kilpatrick, A. M., L. D. Kramer, S. R. Campbell, E. O. Alleyne, A. P. Dobson, and P. Daszak. 2005. West Nile Virus Risk Assessment and the Bridge Vector Paradigm. Emerging Infectious Diseases 11: 425-429.
Laird, M., and J. W. Miles. 1983. Residual Insecticides in Vector Control, pp. 49-81, Integrated mosquito control methodologies. Vol. 1. Academic Press Inc.(London) Ltd.
Pant, C. 1979. Control of vectors of Japanese encephalitis. WHOIVBCI79 733.
PCT. 2015. State of the Mosquito Market Survey, pp. 1-12, Pest Control Technology. GIE Media Inc., Cleveland; USA.
Sawabe, K., I. Nishiumi, Y. Tsuda, N. Hisai, M. Kobayashi, S. Hamao, S. Kasai, K. Hoshino, H. Isawa, T. Sasaki, Y. Higa, and S. Roychoudhury. 2010. Host-Feeding Habits of Culex pipiens and Aedes albopictus (Diptera: Culicidae) Collected at the Urban and Suburban Residential Areas of Japan [electronic resource]. Journal of medical entomology 47: 442-450.
Zanluca, C., V. C. A. d. Melo, A. L. P. Mosimann, G. I. V. d. Santos, C. N. D. d. Santos, and K. Luz. 2015. First report of autochthonous transmission of Zika virus in Brazil. Memórias do Instituto Oswaldo Cruz 110: 569-572.
Nguyen is an entomologist with the Georgia Department of Public Health’s Vector-Borne & Zoonotic Diseases team. Mayes is an undergraduate entomology research associate at the University of Georgia. Forschler is an entomology professor at the University of Georgia.