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Effects of Sublethal Pyrethroid Exposure on the Hostseeking Vol. 36, no. 2 Journal of Vector Ecology 395 Effects of sublethal pyrethroid exposure on the host-seeking behavior of female mosquitoes Lee W. Cohnstaedt and Sandra A. Allan* USDA-ARS-CMAVE, 1600 SW 23rd Drive, Gainesville, FL 32608, U.S.A., [email protected] Received 7 April 2011; Accepted 7 September 2011 ABSTRACT: A common method of adult mosquito control consists of residual application on surfaces and aerial spraying often using pyrethroids. However, not all insects that contact insecticides are killed. Sublethal exposure to neurotoxic compounds can negatively affect sensory organs and reduce efficiency of host location. Flight tracks of host-seeking female Culex quinquefasciatus, Anopheles albimanus, and Aedes aegypti in a wind tunnel were video-recorded to compare activation of host-seeking and patterns of flight orientation to host odors. During host-seeking flights, all three mosquito species differed significantly in flight duration, velocity, turn angle, and angular velocity. Mosquitoes were then exposed to sublethal levels (LD25) of pyrethroid insecticides to evaluate the effects of the neurotoxicants 24 hours post-exposure. Significant reductions in time of activation to flight and flight direction were observed in mosquitoes exposed to deltamethrin and permethrin. Additionally, pesticide-treated Cx. quinquefasciatus mosquitoes flew significantly slower, spent more time in flight, and turned more frequently than untreated controls. Journal of Vector Ecology 36 (2): 395-403. 2011. Keyword Index: Culex quinquefasciatus, Aedes aegypti, Anopheles albimanus, pesticide exposure, host orientation. INTRODUCTION the insect nervous system. They prevent sodium channels from closing which leads to trembling or paralysis usually In a public health setting, pyrethroid-based insecticides followed by death (Vijverberg and van den Bercken 1990). are most often used for adult mosquito control programs. Pyrethroids are more stable synthetic analogs of pyrethrin Adult mosquito populations are often reduced by aerial and are preferred in public health settings because of their sprays and residual treatments and, although effective at high arthropod specificity, a low mammalian toxicity, preventing disease transmission by repelling or killing and a rapid degradation (reviewed by Vijverberg and van mosquitoes, not all mosquitoes that contact the pesticides den Bercken 1990). Modifications to basic pyrethroid will die from contact with the aerial droplets or landing on structure has increased the effectiveness of the pyrethroids treated surfaces. Some mosquitoes may be pesticide-resistant while changing their properties and uses (Carter 2006). and others may receive a sublethal dosage of pesticide. The Permethrin, a type I pyrethroid without a cyano moiety in sublethal effects of pesticides on adult mosquitoes is not the alpha position, generally affects the peripheral nerves, well reported, although considerable research has been whereas deltamethrin, a type II pyrethroid with the cyano conducted on larval mosquitoes (reviewed in Elliott et group, affects the entire nervous system (reviewed in al. 1978, Robert and Olson 1989), non-target organisms Soderlund and Bloomquist 1989). Permethrin is used for (Newsom 1967) and beneficial insects (Delpuech et al. 2001, intradomestic residual spraying and as a treatment for Desneux et al. 2003, Thompson 2003, Prasifka et al. 2007). clothing and bednets to prevent mosquito bites (Schreck The predominantly nocturnal biting Culex and Kline 1989). Deltamethrin applications primarily quinquefasciatus (Say) is an important vector of West Nile consist of intradomestic residual spraying, aerial spraying and St. Louis encephalitis viruses in the United States (Clayton and Sander 2002), and as a long-lasting insecticide (Foster and Walker 2002, Turell et al. 2001) and lymphatic on the bed-net Permanet®3 (Westergaard-Frandsen). filariasis globally. Another nocturnally biting mosquito, During host-seeking, mosquitoes may encounter sublethal Anopheles albimanus (Wiedemann), is the principal doses of neurotoxic compounds from contact with treated vector of malaria in Central America (Breeland 1972). The substrates or aerosolized insecticides (ultralow volume daytime biting Aedes aegypti (L) is the principal disease sprays or insecticide fogging). While most pesticide vector of dengue and yellow fever (Foster and Walker 2002). applications are evaluated for their direct killing potential, Although mosquito behavioral patterns, such as being pyrethroid applications may also be detrimental to nocturnally active, strong fliers, and preferred host-seeking neurological pathways necessary for host-seeking behavior. heights, are broadly reported (Foster and Walker 2002), Pyrethroid exposure may result in excitation or repellent there has not been a detailed comparison of the differences responses similar to those for several repellents (Greico et in host-seeking behaviors. Behavioral differences may affect al. 2007, Cooperband et al. 2010, Miller et al. 2009), but the the optimal delivery of pesticides applied for control of effect of this on subsequent host-feeding remains unclear. If mosquito populations. sublethal pyrethroid exposure does cause reduced olfactory Pyrethroid insecticides function by interfering with detection, altered behavior, learning inhibition, and 396 Journal of Vector Ecology December 2011 changes in feeding patterns (Haynes 1988), then a reduction LD25 for each species and pyrethroid was based on a dose in longevity, host-seeking efficiency, biting behavior, and a response curve calculated by probit analysis using Polo change in time flying will reduce the mosquito’s probability Plus software (LeOra Software, Berkeley, CA). Preliminary of transmitting disease based on mathematical modeling, testing indicated that LD25 was the highest dose of pesticide such as for malaria using the classic Ross-MacDonald that knocked down all mosquitoes but caused minimal equation for vectorial capacity (Klempner et al. 2007), West external damage (e.g., leg autonomization) to the 75% of Nile virus (Wonham et al. 2006), and dengue virus (Newton the mosquitoes which survived 24 h later. and Reiter 1992). The current study examines the effects of Females of Cx. quinquefasciatus and Ae. aegypti a sublethal exposure to the pyrethroids, permethrin and received a dose of 1.6 ng/µl and 1.4 ng/µl, respectively, of deltamethrin, on host-seeking activation and orientation of permethrin and deltamethrin to obtain an average mortality Cx. quinquefasciatus, An. albimanus, and Ae. aegypti. of 25% (LD25) at 24 h. Females of Anopheles albimanus were the most susceptible and required a dose of 0.15 ng/µl of MATERIALS AND METHODS permethrin and deltamethrin to obtain the LD25 at 24 h. Cold-immobilized mosquitoes in the control groups had no Insect rearing mortality or less than one per 30 mosquitoes. The replicates Culex quinquefasciatus, An. albimanus, and Ae. aegypti were limited to <28 individuals because of the laborious were raised at the USDA Center for Medical, Agricultural, nature of hand treating three species of mosquitoes with and Veterinary Entomology in Gainesville, FL, following three treatments to insure uniform exposure during protocols of Gerberg et al. (1994). The mosquitoes used in treatment. trials were non-blood-fed females, seven to ten days of age, maintained on a 10% sucrose solution (w/w). The colonies Flight activation and orientation were provided with blood meals in the form of heated For host-seeking behavioral trials, treated mosquitoes blood sausages which consisted of a lamb skin membrane were released individually 24 h after treatment into a containing defibrinated bovine blood. Adult mosquitoes wind tunnel flight chamber between 09:00-13:00, which were maintained at 28° C and a 14:10 (L:D) photoperiod. corresponded to the lighted phase for the day-biting Larvae were provided ad libitum with an abundance of food mosquitoes and the dark phase for the photoperiod-adjusted while in the colony and during the 24 h post-treatment. mosquito colony. Mosquito releases were conducted over Environmental conditions were maintained between 25 to a one-month period to insure uniform environmental 27° C and 52-82% relative humidity. conditions. The Plexiglas wind tunnel measured 121.9 cm long x 29.2 cm wide x 30.5 cm high with laminar air flow at Pesticide treatment 3.6 m/sec as described by Cooperband et al. (2010) (Figure Prior to behavioral studies, the optimal sublethal 1). Carbon dioxide as a flight stimulant (Gillies 1980), doses were determined for each pesticide. Adult female was released into the middle of the air stream at 50ml/ mosquitoes were topically treated with technical grade min. Additionally, a mixture of host-associated chemicals, permethrin (98% pure, ChemService, West Chester, PA) known to be attractants for mosquitoes and sand flies, was or deltamethrin (99% pure, ChemService, West Chester, used to provide a consistent attractive source (Mann et al. PA) serially diluted in acetone (99% pure, Acros Organics, 2009). This chemo-attractant mixture consisted of 2.5% Morris Plains, NJ). Pesticide was delivered by pipeting 1 1-octen-3-ol (98% pure, Sigma-Aldrich, St. Louis, MO), µl of acetone containing the insecticide onto the thorax 2.5% 1-hexen-3-ol (98% pure, Acros Organics, Morris of individual mosquitoes immobilized by chilling (4° C). Plains, NJ) and 95% acetone (99% pure, Acros Organics, Controls consisted of acetone treatment without pesticide. Morris Plains, NJ). Odor delivery
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