Ary Farajollahi

Host Feeding Patterns of Established and Potential Mosquito Vectors of West Nile Virus in the Eastern United States

An important variable in determining the vectorial capacity of mosquito species for arthropod-borne infections is the degree of contact of the vector and the vertebrate reservoir. This parameter can be estimated by examining the host-feeding habits of vectors. Serological and polymerase chain reaction based methods have been used to study the host-feedings patterns of 21 mosquito species from New York, New Jersey, and Tennessee, 19 of which previously have been found infected with West Nile virus. Mammalophilic mosquito species in New Jersey and New York fed primarily upon white-tailed deer, while those from Memphis, Tennessee, fed mainly upon domestic dogs. A total of 24 different avian host species were detected among the avian-derived blood meals. American Robin, Northern Cardinal, Northern Mockingbird, Tufted Titmouse, and Brown-headed Cowbird were common avian hosts, while blood meals derived from the American Crow were relatively rare. Although the majority of common host species were potentially among the most abundant birds at each location, the proportion of blood meals from the most commonly fed upon avian species was greater than was predicted based upon the likely abundance of these species alone. These findings suggest that vector species for West Nile virus may preferentially feed upon certain avian hosts.

''Bird biting'' mosquitoes and human disease: A review of the role of Culex pipiens complex mosquitoes in epidemiology

The transmission of vector-borne pathogens is greatly influenced by the ecology of their vector, which is in turn shaped by genetic ancestry, the environment, and the hosts that are fed on. One group of vectors, the mosquitoes in the Culex pipiens complex, play key roles in the transmission of a range of pathogens including several viruses such as West Nile and St. Louis encephalitis viruses, avian malaria (Plasmodium spp.), and filarial worms. The Cx. pipiens complex includes Culex pipiens pipiens with two forms, pipiens and molestus, Culex pipiens pallens, Culex quinquefasciatus, Culex australicus, and Culex globocoxitus. While several members of the complex have limited geographic distributions, Cx. pipienspipiens and Cx. quinquefasciatus are found in all known urban and sub-urban temperate and tropical regions, respectively, across the world, where they are often principal disease vectors. In addition, hybrids are common in areas of overlap. Although gaps in our knowledge still remain, the advent of genetic tools has greatly enhanced our understanding of the history of speciation, domestication, dispersal, and hybridization. We review the taxonomy, genetics, evolution, behavior, and ecology of members of the Cx. pipiens complex and their role in the transmission of medically important pathogens. The adaptation of Cx. pipiens complex mosquitoes to human-altered environments led to their global distribution through dispersal via humans and, combined with their mixed feeding patterns on birds and mammals (including humans), increased the transmission of several avian pathogens to humans. We highlight several unanswered questions that will increase our ability to control diseases transmitted by these mosquitoes.

Climate Change and Range Expansion of the Asian Tiger Mosquito (Aedes albopictus) in Northeastern USA: Implications for Public Health Practitioners

The Asian tiger mosquito, Aedes albopictus (Skuse), is an invasive species with substantial biting activity, high disease vector potential, and a global distribution that continues to expand. New Jersey, southern New York, and Pennsylvania are currently the northernmost boundary of established Ae. albopictus populations in the eastern United States. Using positive geographic locations from these areas, we modeled the potential future range expansion of Ae. albopictus in northeastern USA under two climate change scenarios. The land area with environmental conditions suitable for Ae. albopictus populations is expected to increase from the current 5% to 16% in the next two decades and to 43%–49% by the end of the century. Presently, about one-third of the total human population of 55 million in northeastern USA reside in urban areas where Ae. albopictus is present. This number is predicted to double to about 60% by the end of the century, encompassing all major urban centers and placing over 30 million people under the threat of dense Ae. albopictus infestations. This mosquito species presents unique challenges to public health agencies and has already strained the resources available to mosquito control programs within its current range. As it continues to expand into areas with fewer resources and limited organized mosquito control, these challenges will be further exacerbated. Anticipating areas of potential establishment, while planning ahead and gathering sufficient resources will be the key for successful public health campaigns. A broad effort in community sanitation and education at all levels of government and the private sector will be required until new control techniques are developed that can be applied efficiently and effectively at reasonable cost to very large areas.

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.

Detection of West Nile viral RNA from an overwintering pool of Culex pipens pipiens (Diptera: Culicidae) in New Jersey, 2003.

Abstract In total, 1,324 Culex pipiens pipiens L. female mosquitoes were collected at Ft. Hancock, Monmouth County, New Jersey, from January to March 2001–2003. Mosquitoes were held in an insectary at 27°C and a photoperiod of 16:8 (L:D) h for 6 to 21 d after which they were tested in 34 pools. West Nile viral RNA was detected in one pool by a TaqMan reverse transcription-polymerase chain reaction assay; however, infectious virus could not be isolated using either Vero cell plaque assay or C6/36 mosquito cells. Twenty females dissected in January and March 2003 confirmed ovarian diapause status. We suggest that the mode of infection in this pool of overwintering females may have been due to vertical (transgenerational) transmission.

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.

Changes in Aedes albopictus (Diptera: Culicidae) Populations in New Jersey and Implications for Arbovirus Transmission

ABSTRACT The Asian tiger mosquito Aedes albopictus (Skuse) was first detected in New Jersey in 1995 during mosquito surveillance operations in Monmouth County. We tracked statewide changes in populations of the Asian tiger mosquito and its association with West Nile virus from 2003 to 2007. Ae. albopictus population abundance has increased in New Jersey since 2003, primarily along the urban corridor between New York City and Philadelphia, and they are now expanding their range further into suburban and rural areas of the state. Ae. albopictus has invaded all counties of New Jersey except for two northwest rural counties (Sussex and Warren). West Nile virus was detected in Ae. albopictus throughout several foci in New Jersey during the study, underscoring the public health significance of this mosquito.

Crouching Tiger, Hidden Trouble: Urban Sources of Aedes albopictus (Diptera: Culicidae) Refractory to Source-Reduction

Our ultimate objective is to design cost-effective control strategies for Aedes albopictus, the Asian tiger mosquito, an important urban nuisance and disease vector that expanded worldwide during the last 40 years. We conducted mosquito larval surveys from May through October 2009 in the City of Trenton, New Jersey, USA, while performing intensive monthly source-reduction campaigns that involved removing, emptying, or treating all accessible containers with larvicides and pupicides. We examined patterns of occurrence of Ae. albopictus and Culex pipiens, another urban mosquito, among different container types by comparing observed and expected number of positive containers of each type. Expected use was based on the relative frequency of each container type in the environment. Aedes albopictus larvae and pupae were found significantly more often than expected in medium volumes of water in buckets and plant saucers but were rarely collected in small volumes of water found in trash items such as discarded cups and cans. They were also absent from large volumes of water such as in abandoned swimming pools and catch basins, although we consistently collected Cx. pipiens from those habitats. The frequency of Ae. albopictus in tires indicated rapid and extensive use of these ubiquitous urban containers. Standard larval-based indices did not correlate with adult catches in BG-Sentinel traps, but when based only on Ae. albopictus key containers (buckets, plant saucers, equipment with pockets of water, and tires) they did. Although we found that only 1.2% of the 20,039 water-holding containers examined contained immature Ae. albopictus (5.3% if only key containers were counted), adult populations were still above nuisance action thresholds six times during the 2009 mosquito season. We conclude that in urban New Jersey, effective source reduction for Ae. albopictus control will require scrupulous and repeated cleaning or treatment of everyday use containers and extensive homeowner collaboration.