Oviposition site selection by the dengue vector Aedes aegypti and its implications for dengue control.
ABSTRACT: 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.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.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.
Project description:Current Aedes aegypti larval control methods are often insufficient for preventing dengue epidemics. To improve control efficiency and cost-effectiveness, some advocate eliminating or treating only highly productive containers. The population-level outcome of this strategy, however, will depend on details of Ae. aegypti oviposition behavior.We simultaneously monitored female oviposition and juvenile development in 80 experimental containers located across 20 houses in Iquitos, Peru, to test the hypothesis that Ae. aegypti oviposit preferentially in sites with the greatest potential for maximizing offspring fitness. Females consistently laid more eggs in large vs. small containers (??=?9.18, p<0.001), and in unmanaged vs. manually filled containers (??=?5.33, p<0.001). Using microsatellites to track the development of immature Ae. aegypti, we found a negative correlation between oviposition preference and pupation probability (??=?-3.37, p<0.001). Body size of emerging adults was also negatively associated with the preferred oviposition site characteristics of large size (females: ??=?-0.19, p<0.001; males: ??=?-0.11, p?=?0.002) and non-management (females: ??=?-0.17, p<0.001; males: ??=?-0.11, p<0.001). Inside a semi-field enclosure, we simulated a container elimination campaign targeting the most productive oviposition sites. Compared to the two post-intervention trials, egg batches were more clumped during the first pre-intervention trial (??=?-0.17, P<0.001), but not the second (??=?0.01, p?=?0.900). Overall, when preferred containers were unavailable, the probability that any given container received eggs increased (??=?1.36, p<0.001).Ae. aegypti oviposition site choice can contribute to population regulation by limiting the production and size of adults. Targeted larval control strategies may unintentionally lead to dispersion of eggs among suitable, but previously unoccupied or under-utilized containers. We recommend integrating targeted larval control measures with other strategies that leverage selective oviposition behavior, such as luring ovipositing females to gravid traps or egg sinks.
Project description:Aedes aegypti (L.) is the primary vector of dengue, the most important arboviral infection globally. Until an effective vaccine is licensed and rigorously administered, Ae. aegypti control remains the principal tool in preventing and curtailing dengue transmission. Accurate predictions of vector populations are required to assess control methods and develop effective population reduction strategies. Ae. aegypti develops primarily in artificial water holding containers. Release recapture studies indicate that most adult Ae. aegypti do not disperse over long distances. We expect, therefore, that containers in an area of high development site density are more likely to be oviposition sites and to be more frequently used as oviposition sites than containers that are relatively isolated from other development sites. After accounting for individual container characteristics, containers more frequently used as oviposition sites are likely to produce adult mosquitoes consistently and at a higher rate. To this point, most studies of Ae. aegypti populations ignore the spatial density of larval development sites.Pupal surveys were carried out from 2004 to 2007 in rural Kamphaeng Phet, Thailand. In total, 84,840 samples of water holding containers were used to estimate model parameters. Regression modeling was used to assess the effect of larval development site density, access to piped water, and seasonal variation on container productivity. A varying-coefficients model was employed to account for the large differences in productivity between container types. A two-part modeling structure, called a hurdle model, accounts for the large number of zeroes and overdispersion present in pupal population counts.The number of suitable larval development sites and their density in the environment were the primary determinants of the distribution and abundance of Ae. aegypti pupae. The productivity of most container types increased significantly as habitat density increased. An ecological approach, accounting for development site density, is appropriate for predicting Ae. aegypti population levels and developing efficient vector control programs.
Project description:When devising methods to sample Aedes aegypti (L.) eggs from naturally-occurring containers to investigate selective oviposition, failure to take into account certain aspects of Ae. aegypti behavior can bias study inferences. In Iquitos, Peru, we tested three assumptions related to designing Ae. aegypti oviposition field studies, as follows: 1) lining containers with paper as an oviposition substrate does not affect oviposition; 2) diurnal egg-laying activity peaks in the late afternoon or early evening, and there is little oviposition during midday; and 3) the gonotrophic cycle length of wild females averages from 3 to 4 d. When wild females were presented with containers lined and unlined with paper toweling, the presence of paper increased oviposition in plastic and metal containers, but had no effect in cement containers. Recording the number of eggs laid by Ae. aegypti every 2 h throughout the day delineated a bimodal diurnal oviposition pattern, with a small morning peak, decreased activity during midday, and a predominant peak in the late afternoon and evening from 16:00 to 20:00 h. Daily monitoring of captive individual Fo females revealed that the gonotrophic cycle length was typically 3-4 d for the Iquitos population. These findings will be used to adjust field study design to 1) account for sampling eggs using paper toweling, and 2) determine the time of day and number of days over which to sample Ae. aegypti eggs. We explored how failure to consider these behaviors could potentially bias field assessments of oviposition preferences.
Project description:The yellow fever mosquito, Aedes aegypti, the global vector of dengue and yellow fever, is inexorably linked to water-filled human-made containers for egg laying and production of progeny. Oviposition is stimulated by cues from water containers, but the nature and origin of these cues have not been elucidated. We showed that mosquito females directed most of their eggs to bamboo and white-oak leaf infusions, and only a small fraction of the eggs were laid in plain water containers. In binary choice assays, we demonstrated that microorganisms in leaf infusions produced oviposition-stimulating kairomones, and using a combination of bacterial culturing approaches, bioassay-guided fractionation of bacterial extracts, and chemical analyses, we now demonstrate that specific bacteria-associated carboxylic acids and methyl esters serve as potent oviposition stimulants for gravid Ae. aegypti. Elucidation of these compounds will improve understanding of the chemical basis of egg laying behavior of Ae. aegypti, and the kairomones will likely enhance the efficacy of surveillance and control programs for this disease vector of substantial global public health importance.
Project description:Mass trapping of gravid females represents one promising strategy for the development of sustainable tools against Aedes aegypti. However, this technique requires the development of effective odorant lures that can compete with natural breeding sites. The presence of conspecific larvae has been shown to stimulate oviposition. Hence, we evaluated the role of four major molecules previously identified from Ae. aegypti larvae (isovaleric, myristoleic, myristic [i.e. tetradecanoic], and pentadecanoic acids) on the oviposition of conspecific females, as well as their olfactory perception to evaluate their range of detection. Using flight cage assays, the preference of gravid females to oviposit in water that previously contained larvae (LHW) or containing the four larval compounds was evaluated. Then, compounds and doses inducing the highest stimulation were challenged for their efficacy against LHW. Only isovaleric acid elicited antennal response, suggesting that the other compounds may act as taste cues. Pentadecanoic acid induced significant oviposition stimulation, especially when dosed at 10 ppm. Myristoleic acid and isovaleric acid deterred oviposition at 10 and 100 ppm, while no effect on oviposition was observed with myristic acid irrespectively of the dose tested. When the four compounds were pooled to mimic larvae's chemical signature, they favored oviposition at 1 ppm but negatively affected egg-laying at higher concentrations. When properly dosed, pentadecanoic acid and the blend of compounds may be promising lures for ovitraps as they could compete with LHW. Due to their low volatility, their effect should be further evaluated under field conditions, in addition with long-range attractants for developing effective tools against gravid females.
Project description:The mosquito virus vector Aedes (Ae.) aegypti exploits a wide range of containers as sites for egg laying and development of the immature life stages, yet the approaches for modeling meteorologically sensitive container water dynamics have been limited. This study introduces the Water Height and Temperature in Container Habitats Energy Model (WHATCH'EM), a state-of-the-science, physically based energy balance model of water height and temperature in containers that may serve as development sites for mosquitoes. The authors employ WHATCH'EM to model container water dynamics in three cities along a climatic gradient in México ranging from sea level, where Ae. aegypti is highly abundant, to ~2100 m, where Ae. aegypti is rarely found. When compared with measurements from a 1-month field experiment in two of these cities during summer 2013, WHATCH'EM realistically simulates the daily mean and range of water temperature for a variety of containers. To examine container dynamics for an entire season, WHATCH'EM is also driven with field-derived meteorological data from May to September 2011 and evaluated for three commonly encountered container types. WHATCH'EM simulates the highly nonlinear manner in which air temperature, humidity, rainfall, clouds, and container characteristics (shape, size, and color) determine water temperature and height. Sunlight exposure, modulated by clouds and shading from nearby objects, plays a first-order role. In general, simulated water temperatures are higher for containers that are larger, darker, and receive more sunlight. WHATCH'EM simulations will be helpful in understanding the limiting meteorological and container-related factors for proliferation of Ae. aegypti and may be useful for informing weather-driven early warning systems for viruses transmitted by Ae. aegypti.
Project description:Aedes aegypti (L.; Diptera: Culicidae) has been established in the southwestern United States for several decades, but relationships between humans and mosquitoes in this arid region are not well-characterized. In August 2012, the outdoor premises of 355 houses within 20 neighborhoods in Tucson, Arizona were surveyed for containers that could provide larval habitat for Ae. aegypti mosquitoes. At the same time, a knowledge, attitudes and practices (KAP) questionnaire was administered to a resident of each house surveyed for immature mosquitoes. The KAP questionnaire assessed respondents' knowledge and concerns about vector-borne illnesses as well as practices they used to avoid mosquitoes. Of the houses surveyed, 91% had at least one container present, and 64% had at least one container with standing water. On average, each house had 2.2 containers with water at the time of the survey. The overall House Index (proportion of premises surveyed with at least one container with Ae. aegypti immatures present) was 13%. Based on questionnaire responses, there was a significant positive association between the number of residents in the home and the odds of finding Ae. aegypti positive containers on the premises, while household income showed a significant negative association. The reported frequency of checking for standing water was also significantly associated with the odds of finding immatures, although the nature of this association was ambiguous. Flower pots were the principal type of container with Ae. aegypti larvae. These findings show that larval habitat is widely available even in an arid environment and city with good housing and sanitation infrastructure.
Project description:In the Peruvian Amazon, the dengue vector Aedes aegypti is abundant in large urban centers such as Iquitos. In recent years, it has also been found in a number of neighboring rural communities with similar climatic and socioeconomic conditions. To better understand Ae. aegypti spread, we compared characteristics of communities, houses, and containers in infested and uninfested communities.We conducted pupal-demographic surveys and deployed ovitraps in 34 communities surrounding the city of Iquitos. Communities surveyed were located along two transects: the Amazon River and a 95 km highway. We calculated entomological indices, mapped Ae. aegypti presence, and developed univariable and multivariable logistic regression models to predict Ae. aegypti presence at the community, household, or container level.Large communities closer to Iquitos were more likely to be infested with Ae. aegypti. Within infested communities, houses with Ae. aegypti had more passively-filled containers and were more often infested with other mosquito genera than houses without Ae. aegypti. For containers, large water tanks/drums and containers with solar exposure were more likely to be infested with Ae. aegypti. Maps of Ae. aegypti presence revealed a linear pattern of infestation along the highway, and a scattered pattern along the Amazon River. We also identified the geographical limit of Ae. aegypti expansion along the highway at 19.3 km south of Iquitos.In the Peruvian Amazon, Ae. aegypti geographic spread is driven by human transportation networks along rivers and highways. Our results suggest that urban development and oviposition site availability drive Ae. aegypti colonization along roads. Along rivers, boat traffic is likely to drive long-distance dispersal via unintentional transport of mosquitoes on boats.
Project description:The dynamic of arbovirus vectors such as Aedes aegypti and Ae. albopictus remains poorly understood in large cities in central Africa. Here, we compared the larval ecology, geographical distribution and degree of infestation of Ae. aegypti and Ae. albopictus in Yaoundé, the capital city of Cameroon, and estimated their Stegomyia indices revealing a significant potential risk of arbovirus transmission. An entomological survey was conducted in April-May 2018 in a cluster of houses randomly selected. Each selected house was inspected, the number of inhabitants was recorded, and potential and positive containers for Aedes were characterized. Stegomyia and pupae-based indices were estimated. Overall, 447 houses and 954 containers were inspected comprising 10,801 immature stages of Aedes with 84.95% of Ae. albopictus and 15.05% of Ae. aegypti. Both species bred mainly in discarded tanks and used tyres, associated with turbid water and the presence of plant debris inside containers. Aedes albopictus was the most prevalent species in almost all neighbourhoods. The house index, Breteau index, and container index were higher for Ae. albopictus (38.26%, 71.81%, and 29.61%) compared to those of Ae. aegypti (25.73%, 40.93%, and 16.88%). These indices are high compared to the thresholds established by Pan American Health Organization and World Health Organization, which suggests a high potential risk of arbovirus transmission.
Project description:Oviposition site selection by gravid females is an important determinant of the distribution, abundance, and dynamics of dipteran hematophagous insects. The presence of conspecific immature stages in a potential oviposition site could, on the one hand, indicate the suitability of that site but on the other hand could indicate the potential for intraspecific competition. In this paper, we present a graphic model suggesting that the trade-off between these two opposing forces could result in a hump-shaped density-dependent relationship between oviposition rate and conspecific immature stage density (hereafter, the "Hump-shaped regulation model") with positive effects of aggregation prevailing at low densities and negative effect of intraspecific competition prevailing at higher densities. We field-tested the predictions of this model at both the egg- and the larval levels with Aedes albopictus and evaluated if and how these relationships are affected by resource enrichment. We found support for the hump-shaped regulation model at both the larval and the egg levels. Using oviposition cups containing varying numbers of conspecific larvae, we showed that the oviposition activity of Ae. albopictus first increases and then decreases with larvae number. Medium enrichment resulted in higher hatching rate, and demonstrated linear relations for the no-enrichment treatment where larvae density range was low and hump-shaped relationship for the enriched medium that had a wider larvae density range. Using pairs of oviposition cups, we showed that at low egg densities mosquitoes laid more eggs on substrates containing pre-existing eggs. However, at higher egg densities, mosquitoes laid more eggs on a virgin substrate. Based on our results and on a meta-analysis, we suggest that due to study design or methodological shortcomings the hump-shaped regulation model is often left undetected and that it is likely to be more common than currently thought.