Sean P. Healy

Field efficacy of BG-Sentinel and industry-standard traps for Aedes albopictus (Diptera: Culicidae) and West Nile virus surveillance.

ABSTRACT Standard surveillance traps in North America for adult Aedes albopictus (Skuse) (Diptera: Culicidae), an invasive mosquito with public health implications, are currently ineffective. We compared the efficacy of the BG-Sentinel trap (BGS) with and without lures (BG-lure, octenol, and CO2), the Centers for Disease Control and Prevention light trap (CDC) with and without lures, and the gravid trap (GT) for Ae. albopictus collection in two urban sites in New Jersey. The BGS with or without lures collected more Ae. albopictus compared with other trap configurations and was more specific for Ae. albopictus. In Camden County, the BGS with lures collected three times more Ae. albopictus than the CDC (with CO2 only) and five times more than the GT. In Mercer County, BGS with lures collected the most mosquitoes, with 3 times more Ae. albopictus than the CDC with all lures and 50 times more than the GT. The BGS collected more male Ae. albopictus than other traps in both counties, providing further population monitoring. The GT and BGS provided a relative measure of the enzootic activity of West Nile virus in Culex spp. and the potential epidemic activity of WNV in Ae. albopictus. The BGS provides effective chemical and visual cues for host-seeking Ae. albopictus and should be used as a part of existing surveillance programs and new initiatives targeting this mosquito.

Larval Mosquito Habitat Utilization and Community Dynamics of Aedes albopictus and Aedes japonicus (Diptera: Culicidae)

ABSTRACT Aedes albopictus (Skuse) and Ae. japonicus (Theobald) are important container-inhabiting mosquitoes that transmit disease agents, outcompete native species, and continue to expand their range in the United States. Both species deposit eggs in natural and artificial containers and thrive in peridomestic environments. The goal of our study was to examine the types and characteristics of containers that are most productive for these species in the northeastern United States. In total, 306 containers were sampled in urban, suburban, and rural areas of New Jersey. Multiple biotic and abiotic factors were recorded in an attempt to identify variables associated with the productivity of each species. Based on pupal abundance and density of container types, results showed that tires, trash cans, and planter dishes were the most important containers for Ae. albopictus, while planter dishes were the most important containers for Ae. japonicus. Container color (black and gray), material (rubber), and type (tires) were correlated with species presence for Ae. albopictus and Ae. japonicus. These factors may play a role in the selection of oviposition sites by female mosquitoes or in the survival of their progeny. Differences in species composition and abundance were detected between areas classified as urban, suburban, and rural. In urban and suburban areas, Ae. albopictus was more abundant in container habitats than Ae. japonicus; however, Ae. japonicus was more abundant in rural areas, and when water temperatures were below 14°C Our results suggest many variables can influence the presence of Ae. albopictus and Ae. japonicus in container habitats in northeastern United States.

Insecticide resistance status of United States populations of Aedes albopictus and mechanisms involved.

Aedes albopictus (Skuse) is an invasive mosquito that has become an important vector of chikungunya and dengue viruses. Immature Ae. albopictus thrive in backyard household containers that require treatment with larvicides and when adult populations reach pest levels or disease transmission is ongoing, adulticiding is often required. To assess the feasibility of control of USA populations, we tested the susceptibility of Ae. albopictus to chemicals representing the main insecticide classes with different modes of action: organochlorines, organophosphates, carbamates, pyrethroids, insect growth regulators (IGR), naturalytes, and biolarvicides. We characterized a susceptible reference strain of Ae. albopictus, ATM95, and tested the susceptibility of eight USA populations to five adulticides and six larvicides. We found that USA populations are broadly susceptible to currently available larvicides and adulticides. Unexpectedly, however, we found significant resistance to dichlorodiphenyltrichloroethane (DDT) in two Florida populations and in a New Jersey population. We also found resistance to malathion, an organophosphate, in Florida and New Jersey and reduced susceptibility to the IGRs pyriproxyfen and methoprene. All populations tested were fully susceptible to pyrethroids. Biochemical assays revealed a significant up-regulation of GSTs in DDT-resistant populations in both larval and adult stages. Also, β-esterases were up-regulated in the populations with suspected resistance to malathion. Of note, we identified a previously unknown amino acid polymorphism (Phe → Leu) in domain III of the VGSC, in a location known to be associated with pyrethroid resistance in another container-inhabiting mosquito, Aedes aegypti L. The observed DDT resistance in populations from Florida may indicate multiple introductions of this species into the USA, possibly from tropical populations. In addition, the mechanisms underlying DDT resistance often result in pyrethroid resistance, which would undermine a remaining tool for the control of Ae. albopictus. Continued monitoring of the insecticide resistance status of this species is imperative.

Area-wide management of Aedes albopictus: choice of study sites based on geospatial characteristics, socioeconomic factors and mosquito populations†

BACKGROUND Aedes (Stegomyia) albopictus (Skuse), the Asian tiger mosquito, is an introduced invasive species in the United States that is responsible for a significant proportion of service requests to local mosquito control programs. This container-utilizing mosquito is refractory to standard mosquito abatement measures in the United States. This study is part of a USDA-ARS project to develop an area-wide management strategy for Ae. albopictus. The goal was to identify three study sites, similar in socioeconomic parameters, geography and Ae. albopictus abundance, in urban and suburban areas in Mercer and Monmouth counties in New Jersey. Prior service requests and light trap counts and also detailed county maps were used to chose nine preliminary sites (four in Mercer and five in Monmouth) where weekly surveillance for Ae. albopictus was performed throughout the 2008 active season. RESULTS Although outliers were detected, socioeconomic variables in the study sites within each county were fairly consistent. Ae. albopictus abundance was associated with poverty levels and had the highest maxima in Mercer, although average mosquito abundance was similar in urban Mercer and suburban Monmouth. CONCLUSION Three study sites in each county were identified for future studies. The summer-long surveillance also revealed socioeconomic variables critical for the development of integrated mosquito management.

Comparative Host Feeding Patterns of the Asian Tiger Mosquito, Aedes albopictus, in Urban and Suburban Northeastern USA and Implications for Disease Transmission

Background Aedes albopictus is an invasive species which continues expanding its geographic range and involvement in mosquito-borne diseases such as chikungunya and dengue. Host selection patterns by invasive mosquitoes are critically important because they increase endemic disease transmission and drive outbreaks of exotic pathogens. Traditionally, Ae. albopictus has been characterized as an opportunistic feeder, primarily feeding on mammalian hosts but occasionally acquiring blood from avian sources as well. However, limited information is available on their feeding patterns in temperate regions of their expanded range. Because of the increasing expansion and abundance of Ae. albopictus and the escalating diagnoses of exotic pathogens in travelers returning from endemic areas, we investigated the host feeding patterns of this species in newly invaded areas to further shed light on its role in disease ecology and assess the public health threat of an exotic arbovirus outbreak. Methodology/Principal Findings We identified the vertebrate source of 165 blood meals in Ae. albopictus collected between 2008 and 2011 from urban and suburban areas in northeastern USA. We used a network of Biogents Sentinel traps, which enhance Ae. albopictus capture counts, to conduct our collections of blooded mosquitoes. We also analyzed blooded Culex mosquitoes collected alongside Ae. albopictus in order to examine the composition of the community of blood sources. We found no evidence of bias since as expected Culex blood meals were predominantly from birds (n = 149, 93.7%) with only a small proportion feeding on mammals (n = 10, 6.3%). In contrast, Aedes albopictus fed exclusively on mammalian hosts with over 90% of their blood meals derived from humans (n = 96, 58.2%) and domesticated pets (n = 38, 23.0% cats; and n = 24, 14.6% dogs). Aedes albopictus fed from humans significantly more often in suburban than in urban areas (χ2, p = 0.004) and cat-derived blood meals were greater in urban habitats (χ2, p = 0.022). Avian-derived blood meals were not detected in any of the Ae. albopictus tested. Conclusions/Significance The high mammalian affinity of Ae. albopictus suggests that this species will be an efficient vector of mammal- and human-driven zoonoses such as La Crosse, dengue, and chikungunya viruses. The lack of blood meals obtained from birds by Ae. albopictus suggest that this species may have limited exposure to endemic avian zoonoses such as St. Louis encephalitis and West Nile virus, which already circulate in the USA. However, growing populations of Ae. albopictus in major metropolitan urban and suburban centers, make a large autochthonous outbreak of an arbovirus such as chikungunya or dengue viruses a clear and present danger. Given the difficulties of Ae. albopictus suppression, we recommend that public health practitioners and policy makers install proactive measures for the imminent mitigation of an exotic pathogen outbreak.

Genetic analysis of invasive Aedes albopictus populations in Los Angeles County, California and its potential public health impact.

The Asian tiger mosquito, Aedes albopictus, is an anthropophilic aggressive daytime-biting nuisance and an efficient vector of certain arboviruses and filarial nematodes. Over the last 30 years, this species has spread rapidly through human travel and commerce from its native tropical forests of Asia to every continent except Antarctica. In 2011, a population of Asian tiger mosquito (Aedes albopictus) was discovered in Los Angeles (LA) County, California. To determine the probable origin of this invasive species, the genetic structure of the population was compared against 11 populations from the United States and abroad, as well as preserved specimens from a 2001 introduction into California using the mitochondrial cytochrome c oxidase 1 (CO1) gene. A total of 66 haplotypes were detected among samples and were divided into three main groups. Aedes albopictus collected in 2001 and 2011 from LA County were genetically related and similar to those from Asia but distinct from those collected in the eastern and southeastern United States. In view of the high genetic similarities between the 2001 and 2011 LA samples, it is possible that the 2011 population represents in part the descendants of the 2001 introduction. There remains an imperative need for improved surveillance and control strategies for this species.

Source Reduction Behavior as an Independent Measurement of the Impact of a Public Health Education Campaign in an Integrated Vector Management Program for the Asian Tiger Mosquito

The goal of this study was to evaluate the effectiveness of a public health educational campaign to reduce backyard mosquito-larval habitats. Three communities each, within two New Jersey counties, were randomly selected to receive: (1) both education and mosquito control, (2) education only, and (3) no education or mosquito control. Four separate educational events included a 5-day elementary school curriculum in the spring, and three door to door distributions of educational brochures. Before and after each educational event, the numbers of mosquito-larval container habitats were counted in 50 randomly selected homes per study area. Container surveys allowed us to measure source reduction behavior. Although we saw reductions in container habitats in sites receiving education, they were not significantly different from the control. Our results suggest that traditional passive means of public education, which were often considered the gold standard for mosquito control programs, are not sufficient to motivate residents to reduce backyard mosquito-larval habitats.

Integrated Use of 4-Poster Passive Topical Treatment Devices for Deer, Targeted Acaricide Applications, and Maxforce TMS Bait Boxes to Rapidly Suppress Populations of Ixodes scapularis (Acari: Ixodidae) in a Residential Landscape

Abstract In fall 2003, we began testing an integrated control strategy to rapidly achieve and sustain reduced numbers of Ixodes scapularis Say (Acari: Ixodidae) in a residential area. We combined two host-targeted technologies in conjunction with single, barrier acaricide applications to sequentially attack each postembryonic life stage of the tick. Granular deltamethrin applied to the lawn–forest interface of participant properties resulted in 100% control of host-seeking nymphs. Nymphal and larval tick burdens on targeted small mammal hosts at treated properties were reduced by 92.7 and 95.4%, respectively, after the first year (2004) of combined interventions. Over the same period, populations of host-seeking nymphs, larvae, and adults were reduced by 58.5, 24.8, and 77.8%, respectively. After interventions in 2005, tick burdens on small mammals were maintained at similar levels, whereas control of host-seeking nymphs, larvae, and adults increased to 94.3, 90.6, and 87.3%, respectively. Prospects for widespread use of these technologies to protect the public’s health are discussed.

Effects of Biogents Sentinel Trap Field Placement on Capture Rates of Adult Asian Tiger Mosquitoes, Aedes albopictus

The Biogents® Sentinel (BGS) trap is the standard tool to monitor adult Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae), the Asian tiger mosquito. BGS traps are commonly placed in residential properties during surveillance operations, but locations within properties may have significant differences in ambient light, temperature, and humidity (e.g. between a sunlit lawn and shady underbrush). We examined the effect of BGS trap placement on Ae. albopictus capture rates in three residential properties in Monmouth County, New Jersey, USA. In each property we visually selected locations as shade, partial shade, and sun. Traps in “partial shade” locations were under vegetation and were exposed to filtered sunlight during some parts of the day while “shaded” locations were never exposed to direct sunlight. Locations defined as “sun” were exposed to direct sunlight for large parts of the day. We placed a BGS trap in each of the three location types and used small data loggers to measure temperature, relative humidity, and light exposure at each trap during a 24-hour deployment. To address temporal variability, we made seven separate measurements from 31 August to 22 September 2010. We found that “partial shade” and “full shade” locations did not differ but that “full sun” locations had significantly higher light exposure, higher temperature, and lower humidity. Importantly, Ae. albopictus catches (males, females, or both) were consistently and significantly over 3 times higher in traps located in shaded locations. To further investigate the effects of local temperature and humidity on surveillance we examined Ae. albopictus collections from 37 BGS traps fitted with data loggers and deployed weekly from August through mid October, during the 2009 season, in three urban sites in Mercer County, NJ. We confirmed that local climate influences capture rates and that Ae. albopictus surveillance projects need to monitor trap placement carefully for maximum efficiency.

Suppressing Aedes albopictus, an emerging vector of dengue and chikungunya viruses, by a novel combination of a monomolecular film and an insect-growth regulator.

The Asian tiger mosquito Aedes albopictus (Skuse) is rapidly increasing its global range and importance in transmission of chikungunya and dengue viruses. We tested pellet formulations of a monomolecular film (Agnique) and (S)-methoprene (Altosid) under laboratory and field conditions. In the laboratory, Agnique provided 80% control for 20 days, whereas Altosid, in combination with Agnique, provided 80% control for > 60 days. During field trials, the 1:1 pellet ratio of combined products provided > 95% control for at least 32 days and 50% control for at least 50 days. Altosid remained effective after a 107-day laboratory-induced drought, suggesting that the product serves as a means of control during drought conditions and against spring broods in temperate regions. Agnique and Altosid, when used in tandem for cryptic, difficult-to-treat locations, can provide long-term control of Ae. albopictus larvae and pupae. The possible additive or synergistic effects of the combined products deserve further investigation.