Ary Faraji

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.

Area-wide ground applications of Bacillus thuringiensis var. israelensis for the control of Aedes albopictus in residential neighborhoods: from optimization to operation.

The increasing range of Aedes albopictus, the Asian tiger mosquito, in the USA and the threat of chikungunya and dengue outbreaks vectored by this species have necessitated novel approaches to control this peridomestic mosquito. Conventional methods such as adulticiding provide temporary relief, but fail to manage this pest on a sustained basis. We explored the use of cold aerosol foggers and misting machines for area-wide applications of Bacillus thuringiensis var. israelensis (VectoBac WDG) as a larvicide targeting Aedes albopictus. During 2010–2013 we performed initially open field trials and then 19 operational area-wide applications in urban and suburban residential areas in northeastern USA to test three truck-mounted sprayers at two application rates. Area-wide applications of WDG in open field conditions at 400 and 800 g/ha killed on average 87% of tested larvae. Once techniques were optimized in residential areas, applications with a Buffalo Turbine Mist Sprayer at a rate of 800 g/ha, the best combination, consistently provided over 90% mortality. Importantly, there was no significant decrease in efficacy with distance from the spray line even in blocks of row homes with trees and bushes in the backyards. Under laboratory conditions Bti deposition in bioassay cups during the operational trials resulted in over 6 weeks of residual control. Our results demonstrate that area-wide truck mounted applications of WDG can effectively suppress Ae. albopictus larvae and should be used in integrated mosquito management approaches to control this nuisance pest and disease vector.

The Eye of the Tiger, the Thrill of the Fight: Effective Larval and Adult Control Measures Against the Asian Tiger Mosquito, Aedes albopictus (Diptera: Culicidae), in North America

Abstract The Asian tiger mosquito, Aedes albopictus (Skuse), is a highly invasive container-inhabiting species with a global distribution. This mosquito, similar to other Stegomyia species such as Aedes aegypti (L.), is highly adapted to urban and suburban areas, and commonly oviposits in artificial containers, which are ubiquitous in these peridomestic environments. The increase in speed and amount of international travel and commerce, coupled with global climate change, have aided in the resurgence and expansion of Stegomyia species into new areas of North America. In many parts of their range, both species are implicated as significant vectors of emerging and re-emerging arboviruses such as dengue, chikungunya, and now Zika. Although rapid and major advances have been made in the field of biology, ecology, genetics, taxonomy, and virology, relatively little has changed in the field of mosquito control in recent decades. This is particularly discouraging in regards to container-inhabiting mosquitoes, because traditional integrated mosquito management (IMM) approaches have not been effective against these species. Many mosquito control programs simply do not possess the man-power or necessary financial resources needed to suppress Ae. albopictus effectively. Therefore, control of mosquito larvae, which is the foundation of IMM approaches, is exceptionally difficult over large areas. This review paper addresses larval habitats, use of geographic information systems for habitat preference detection, door-to-door control efforts, source reduction, direct application of larvicides, biological control agents, area-wide low-volume application of larvicides, hot spot treatments, autodissemination stations, public education, adult traps, attractive–toxic sugar bait methods, lethal ovitraps, barrier–residual adulticides, hand-held ultra-low-volume adulticides, area-wide adulticides applied by ground or air, and genetic control methods. The review concludes with future recommendations for practitioners, researchers, private industry, and policy makers.

The hidden world of Asian tiger mosquitoes: immature Aedes albopictus (Skuse) dominate in rainwater corrugated extension spouts

BACKGROUND The primary sources of Aedes albopictus (Skuse) in its exotic range in North America are artificial containers in backyards, which vary widely in accessibility. In this study we examined their prevalence in two container types that are difficult to inspect: catch basins and corrugated extension spouts (CES), the latter used to divert rainwater in downspouts away from house foundations. METHODS We conducted larval and pupal surveys in catch basins, CES and open containers such as buckets and plant saucers in three urban locations in Mercer County, New Jersey, USA. RESULTS We found that Ae. albopictus were rare in catch basins but prevalent in CES, and were often the only species collected in CES. Specific characteristics of the CES were not significantly associated with the presence or number of Ae. albopictus in them, but those longer and closer to the ground were significantly more likely to contain water, and therefore mosquitoes. During peak season (July-August), the abundance of immature Ae. albopictus was significantly higher in CES than open containers. CONCLUSIONS We found that CES are an important source of Ae. albopictus in our region and propose that effective control strategies should be implemented to minimize mosquito populations from these cryptic habitats.

Anthropogenic impacts on mosquito populations in North America over the past century

The recent emergence and spread of vector-borne viruses including Zika, chikungunya and dengue has raised concerns that climate change may cause mosquito vectors of these diseases to expand into more temperate regions. However, the long-term impact of other anthropogenic factors on mosquito abundance and distributions is less studied. Here, we show that anthropogenic chemical use (DDT; dichlorodiphenyltrichloroethane) and increasing urbanization were the strongest drivers of changes in mosquito populations over the last eight decades in areas on both coasts of North America. Mosquito populations have increased as much as tenfold, and mosquito communities have become two- to fourfold richer over the last five decades. These increases are correlated with the decay in residual environmental DDT concentrations and growing human populations, but not with temperature. These results illustrate the far-reaching impacts of multiple anthropogenic disturbances on animal communities and suggest that interactions between land use and chemical use may have unforeseen consequences on ecosystems.

Field Comparisons of the Gravid Aedes Trap (GAT) and BG-Sentinel Trap for Monitoring Aedes albopictus (Diptera: Culicidae) Populations and Notes on Indoor GAT Collections in Vietnam

Abstract We report on the use of the Gravid Aedes Trap (GAT) as a surveillance device for Aedes albopictus (Skuse) relative to the BG-Sentinel (BGS) trap in field studies conducted in Trenton, NJ, and on Hammond Island, Queensland, Australia. A parallel study conducted in Nha Trang, Vietnam, assessed the use of the GAT as an indoor surveillance device as well as the use of canola oil as a noninsecticide killing agent. In Trenton and Hammond Island, the GAT collected fewer male (0.40 ± 0.12 and 0.43 ± 0.30, respectively) and female (3.05 ± 0.67 and 2.7 ± 2.3, respectively) Ae. albopictus than the BGS trap (males: 3.54 ± 1.26 and 3.75 ± 0.83; females: 4.66 ± 1.18 and 3.9 ± 0.23) over their respective sampling periods (i.e., 24 h for the BGS and 1 wk for the GAT). Despite differences in capture rates, the percentage of traps positive for female Ae. albopictus was similar between the BGS and GAT (Trenton: 60.1 ± 6.3% and 64.4 ± 4.1%; Hammond: 87.5 ± 6.9% and 80.0 ± 8.2%). In Nha Trang, the GAT was equally effective indoors and outdoors with (10 g hay or 3 g fish food) and without (water or empty) infusion. Additionally, no significant decrease in collections was observed between GATs set with canola oil or long-lasting insecticidal net. In summary, both traps were successful in monitoring female Ae. albopictus over their respective trapping intervals, but would be best used to complement each other to monitor both sexes and all physiological stages of female Ae. albopictus. However, the versatility and low-cost of the GAT makes it an attractive alternative to the more expensive BGS trap.

Droplet Characterization and Penetration of an Ultra-Low Volume Mosquito Adulticide Spray Targeting the Asian Tiger Mosquito, Aedes albopictus, within Urban and Suburban Environments of Northeastern USA

Adult control of Aedes albopictus via ultra-low volume is difficult because this species occurs primarily in peridomestic habitats where obstacles such as buildings and vegetation can disrupt spray plumes and droplet dispersion. We determined droplet penetration and characterization of a pyrethroid adulticide applied from the ground at mid (46.77 ml/ha) and maximum (93.53 ml/ha) label rates within cryptic habitats of urban and suburban environments. Droplets were collected from all habitats, with no significant differences detected between locations within the same application rate or collection method. No differences were detected in droplet densities (drops per mm2) between rates within urban environments, but more droplets were collected in urban (149.93 ± 11.07 SE) than suburban sites (114.37 ± 11.32) at the maximum label rate (P = 0.003). The excellent penetration of aerosols into cryptic habitats of an urban site was likely due to the shorter spray paths afforded by our network of roads and alleys. Mid label rates displayed similar droplet density values as maximum label rates in urban areas, indicating that lower rates may be used effectively to reduce costs, lessen non-target effects, and increase environmental stewardship. Advances in formulations and technology are driving changes in adulticide applications, leading to use of the minimum effective dose for maximum efficacy, precision, and accountability.

Reduced performance of a PVC-coated Biogents Sentinel prototype in comparison to the original Biogents Sentinel for monitoring the Asian tiger mosquito, Aedes albopictus, in temperate North America

Aedes albopictus is a major nuisance pest and also a public health concern because of the role it plays in the transmission of arboviruses. There is a continuing demand for effective surveillance tools for this species. The first generation of Biogents Sentinel (BGS1) traps have proven to be an effective tool for surveillance of Ae. albopictus throughout its range, however, some defects in construction led to the eventual development of the next generation. We compared the performance of the new generation prototype trap (BGS2P) to the original. Studies were conducted in suburban and urban areas in Florida, Louisiana, New Jersey, and Virginia, USA in the summer of 2014 (July-October). BGS1 traps collected significantly more Ae. albopictus when compared to the BGS2P with or without CO2 in all locations (P<0.05). When a white cloth was wrapped around the BGS2P traps, efficiency did not change in Louisiana, New Jersey, and Virginia; however, numbers of adult Ae. albopictus collected from the BGS2P and the BGS1 were significantly different based on lure type (P< 0.0001). Results from Florida showed that BGS1with the BG lure and CO2 collected significantly higher adult numbers compared to BGS2P with a three component cartridge lure and CO2 (P< 0.0001). Overall, our results indicate that despite improvements in construction and durability of the BGS2P, this newer trap type did not increase the capture rates of Ae. albopictus in North America. Biogents modified BGS2P based on the data collected from the current study and updated as Biogents Sentinel 2 is now commercially available and its efficacy in comparison to the original will require further study.

TrapTech R-Octenol Lure Does Not Improve the Capture Rates of Aedes albopictus (Diptera: Culicidae) and Other Container-Inhabiting Species in Biogents Sentinel Traps

Abstract Aedes albopictus (Skuse) and other container-inhabiting species have become important public health concerns due to the transmission of dengue, chikungunya, and Zika viruses. Effective surveillance is dependent on the ability to collect a sufficient number of mosquitoes for population monitoring and pathogen isolation. The Biogents Sentinel (BGS) trap supplied with a proprietary human skin lure has become the standard tool for container-inhabiting Aedes species collections worldwide. Recently, R-octenol, a single isomer of the well characterized mosquito attractant octenol, was shown to greatly improve the capture rate of some Aedes species when utilized with the Center for Disease Control and Prevention (CDC) light traps and Mosquito Magnet traps. This study evaluated the effectiveness of the TrapTech lure (TT lure), containing R-octenol, alone or in combination with the human skin lure in a BGS trap to capture Ae. albopictus and other species. BGS traps with human skin lures or a combination of the two lures collected approximately twice as many Ae. albopictus females compared to those with TT lures. Unlike previous studies, baiting BGS traps with TT lures did not result in increased diversity of mosquito species, or in higher numbers of other container-inhabiting Aedes species. Although human skin lures were clearly superior to TT R-octenol lures in BGS traps, R-octenol lures are more widely available and might still be used as an alternative lure, especially when Ae. albopictus populations are high.

Vertical Oviposition Preferences of the Asian Tiger Mosquito, Aedes albopictus, In Temperate North America.

Abstract As a hyperaggressive mosquito that is also a public health threat, Aedes albopictus (Skuse), the Asian tiger mosquito, is a major priority for control efforts. We examine one aspect of Ae. albopictus biology: oviposition height. Field-based research in an urban habitat was conducted to determine if a height preference exists for this species. Larval and egg counts showed a significant preference for oviposition at ground level (0 m) compared to heights of 1, 2, 3, or 4 m (P < 0.01). An experiment conducted under semi–field conditions supported our conclusion of oviposition preference at ground level (P < 0.001), and further defines the search image needed by mosquito control personnel when dealing with this invasive species.