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      Oviposition Site Selection by the Dengue Vector Aedes aegypti and Its Implications for Dengue Control

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          Abstract

          Background

          Because no dengue vaccine or antiviral therapy is commercially available, controlling the primary mosquito vector, Aedes aegypti, is currently the only means to prevent dengue outbreaks. Traditional models of Ae. aegypti assume that population dynamics are regulated by density-dependent larval competition for food and little affected by oviposition behavior. Due to direct impacts on offspring survival and development, however, mosquito choice in oviposition site can have important consequences for population regulation that should be taken into account when designing vector control programs.

          Methodology/Principal Findings

          We examined oviposition patterns by Ae. aegypti among 591 naturally occurring containers and a set of experimental containers in Iquitos, Peru. Using larval starvation bioassays as an indirect measure of container food content, we assessed whether females select containers with the most food for their offspring. Our data indicate that choice of egg-laying site is influenced by conspecific larvae and pupae, container fill method, container size, lid, and sun exposure. Although larval food positively influenced oviposition, our results did not support the hypothesis that females act primarily to maximize food for larvae. Females were most strongly attracted to sites containing immature conspecifics, even when potential competitors for their progeny were present in abundance.

          Conclusion/Significance

          Due to strong conspecific attraction, egg-laying behavior may contribute more to regulating Ae. aegypti populations than previously thought. If highly infested containers are targeted for removal or larvicide application, females that would have preferentially oviposited in those sites may instead distribute their eggs among other suitable, previously unoccupied containers. Strategies that kill mosquitoes late in their development (i.e., insect growth regulators that kill pupae rather than larvae) will enhance vector control by creating “egg sinks,” treated sites that exploit conspecific attraction of ovipositing females, but reduce emergence of adult mosquitoes via density-dependent larval competition and late acting insecticide.

          Author Summary

          Controlling the mosquito Aedes aegypti is of public health importance because, at present, it is the only means to stop dengue virus transmission. Implementing successful mosquito control programs requires understanding what factors regulate population abundance, as well as anticipating how mosquitoes may adapt to control measures. In some species of mosquitoes, females choose egg-laying sites to improve the survival and growth of their offspring, a behavior that ultimately influences population distribution and abundance. In the current study, we tested whether Ae. aegypti actively choose the containers in which they lay their eggs and determined what cues are most relevant to that process. We also explored whether females select containers that provide the most food for their larval progeny. Surprisingly, egg-laying females were most attracted to sites containing other immature Ae. aegypti, rather than to sites containing the most food. We propose that this behavior may contribute to density-dependent competition for food among larvae and play a larger role than previously thought in regulating Ae. aegypti populations. We recommend that accounting for, and even taking advantage of, this natural behavior will lead to more effective strategies for dengue prevention.

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          Most cited references119

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          Conspecific Attraction and Aggregation in Territorial Species

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            Effects of temperature and larval diet on development rates and survival of the dengue vector Aedes aegypti in north Queensland, Australia.

            Immature development times, survival rates and adult size (wing-lengths) of the mosquito Aedes aegypti (L.) (Diptera: Culicidae) were studied in the laboratory at temperatures of 10-40 degrees C. The duration of development from egg eclosion (hatching of the first instar) to adult was inversely related to temperature, ranging from 7.2 +/- 0.2 days at 35 degrees C to 39.7 +/- 2.3 days at 15 degrees C. The minimum temperature threshold for development (t) was determined as 8.3 +/- 3.6 degrees C and the thermal constant (K) was 181.2 +/- 36.1 day-degrees above the threshold. Maximum survival rates of 88-93% were obtained between 20 and 30 degrees C. Wing-length was inversely related to temperature. The sex ratio (female:male) was 1:1 at all temperatures tested (15, 20, 25 and 35 degrees C) except 30 degrees C (4:3). Under field conditions at Townsville and Charters Towers, north Queensland, the duration of immature development varied according to the container position (i.e. shaded or exposed) and the availability of food resources, as well as inversely with temperature. These data indicate that containers with an abundance of organic matter (e.g. those used for striking plant cuttings) or those amongst foliage or under trees (e.g. discarded plastic tubs and tyres) tended to produce the largest adult Ae. aegypti, which had faster development and better immature survival. As such progeny have been linked to a greater risk of dengue transmission, it would seem important to focus on control of such containers.
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              Dynamic life table model for Aedes aegypti (Diptera: Culicidae): analysis of the literature and model development.

              The container-inhabiting mosquito simulation model (CIMSiM) is a weather-driven, dynamic life table simulation model of Aedes aegypti (L.). It is designed to provide a framework for related models of similar mosquitoes which inhibit artificial and natural containers. CIMSiM is an attempt to provide a mechanistic, comprehensive, and dynamic accounting of the multitude of relationships known to play a role in the life history of these mosquitoes. Development rates of eggs, larvae, pupae, and the gonotrophic cycle are based on temperature using an enzyme kinetics approach. Larval weight gain and food depletion are based on the differential equations of Gilpin & McClelland compensated for temperature. Survivals are a function of weather, habitat, and other factors. The heterogeneity of the larval habitat is depicted by modeling the immature cohorts within up to nine different containers, each of which represents an important type of mosquito-producing container in the field. The model provides estimates of the age-specific density of each life stage within a representative 1-ha area. CIMSiM is interactive and runs on IBM-compatible personal computers. The user specifies a region of the world of interest; the model responds with lists of countries and associated cities where historical data on weather, larval habitat, and human densities are available. Each location is tied to an environmental file containing a description of the significant mosquito-producing containers in the area and their characteristics. In addition to weather and environmental information, CIMSiM uses biological files that include species-specific values for each of the parameters used in the model. Within CIMSiM, it is possible to create new environmental and biological files or modify existing ones to allow simulations to be tailored to particular locations or to parameter sensitivity studies. The model also may be used to evaluate any number and combination of standard and novel control methods.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                April 2011
                12 April 2011
                : 5
                : 4
                : e1015
                Affiliations
                [1 ]Department of Entomology, University of California Davis, Davis, California, United States of America
                [2 ]Naval Medical Research Center Unit-6, Lima, Peru
                Colorado State University, United States of America
                Author notes

                Conceived and designed the experiments: JW ACM TWS. Performed the experiments: JW HA. Analyzed the data: JW STS. Wrote the paper: JW. Edited the manuscript: STS ACM TWS.

                Article
                PNTD-D-10-00187
                10.1371/journal.pntd.0001015
                3075222
                21532736
                9cc43f7f-9af7-4676-9ae1-1392c9863cc8
                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
                History
                : 15 November 2010
                : 9 February 2011
                Page count
                Pages: 12
                Categories
                Research Article
                Biology
                Ecology
                Behavioral Ecology
                Population Ecology
                Medicine
                Global Health
                Infectious Diseases
                Neglected Tropical Diseases
                Dengue Fever
                Vectors and Hosts
                Mosquitoes
                Public Health
                Disease Ecology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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