Spatio-Temporal Impacts of Aerial Adulticide Applications on Populations of West Nile Virus Vector Mosquitoes

doi:10.21203/rs.3.rs-92266/v1

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Spatio-Temporal Impacts of Aerial Adulticide Applications on Populations of West Nile Virus Vector Mosquitoes

https://doi.org/10.21203/rs.3.rs-92266/v1

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published 24 Feb, 2021

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Background: Aerial applications of insecticides that target adult mosquitoes are widely used to reduce transmission of West Nile virus to humans during periods of epidemic risk. However, estimates of the reduction in abundance following these treatments typically focus on single events and can vary widely due to stochastic variation in population dynamics and trapping success unrelated to the treatment.

Methods: To overcome these limitations and assess real-world efficacy using observational data from 12 years of vector control operations, we fitted generalized additive models to mosquito surveillance data from CO₂-baited traps in Sacramento and Yolo counties, California from 2006-2017. The models accounted for the expected spatial and temporal trends in the abundance of adult female Culex tarsalis and Culex pipiens in the absence of aerial spraying. Estimates for the magnitude of deviation from baseline abundance following aerial spray events were obtained from the models.

Results: One-week post-treatment with pyrethroid or pyrethrin products, Cx. pipiens abundance was reduced by a mean of 52.4% (95% CI: -65.6, -36.5%) while the use of at least one organophosphate pesticide resulted in a 76.2% (95% CI: -82.8, -67.9%) reduction. For Cx. tarsalis one-week post-treatment resulted in a 30.7% (95% CI: -54.5, 2.5%) reduction; pesticide class was not a significant factor for this species. Repetition of spraying over three to four consecutive weeks resulted in similar estimates for Cx. pipiens and a somewhat smaller magnitude for Cx. tarsalis.

Conclusions: Aerial adulticides are effective for rapid short-term reduction of the abundance of the primary West Nile virus vectors, Cx. tarsalis and Cx. pipiens. A larger magnitude of reduction is estimated for Cx. pipiens, possibly due to the species’ focal distribution. Effects of aerial sprays on Cx. tarsalis populations are likely moderated by the species’ large dispersal ability, population sizes, and vast productive larval habitat present in the study area. Our modeling approach provides a way to estimate effects of public-health pesticides on vector populations using real-world observational data and accounting for contextual factors like spatio-temporal relationships, weather, and habitat and expands upon past studies that have focused on effects of individual aerial treatment events.

Parasitology

vector control

insecticides

Culex tarsalis

Culex pipiens

GAM

generalized additive models

spatial-temporal model

mosquitoes

mosquito-borne disease

West Nile virus

West Nile virus (WNV; genus Flavivirus, family Flaviviridae) causes a potentially fatal, neuroinvasive mosquito-borne disease (1). It is maintained in an enzootic cycle between birds and mosquitoes (2, 3), predominantly in the genus Culex (4), and can spillover to infect horses and humans, both of which are dead-end hosts vulnerable to disease (5). Culex (Cx.) tarsalis and Cx. pipiens complex mosquitoes are the primary enzootic and epizootic vectors in California (6, 7). While 80% of human infections are asymptomatic, clinical manifestations can include acute febrile illness, encephalitis, flaccid paralysis, and death (8). Often the severe form results in long-term physical and mental disabilities (9). WNV invaded California in 2003 and has become endemic (7). An average of 238 neuroinvasive cases occur statewide annually with approximately one-third occurring in the Central Valley, where the landscape is dominated by large-scale agriculture punctuated by cities and small towns (10).

As no human vaccine exists, prevention of human diseases relies primarily on personal protective measures (i.e. wearing long sleeves, using insect repellent, and avoiding the dawn/dust periods when mosquitoes bite) and vector control by local vector control districts or health departments (11, 12). In periods of epidemic risk when large numbers of WNV-infected Culex mosquitoes are detected near human population centers, large-scale aerial applications of insecticides are utilize to rapidly reduce the abundance of adult mosquitoes and disrupt virus transmission cycles, thereby reducing zoonotic transmission risk (13).

Three main classes of pesticide products have been licensed for use in aerial spray applications in California; pyrethrins, pyrethroids, and organophosphates (12, 14, 15). Pyrethrins are naturally derived insecticides from chrysanthemum flowers (Chrysanthemum cineriaefolium) that inactivate sodium channels in the insect nervous system, resulting in paralysis and death (15). Pyrethroids are synthetically derived pyrethrins with a similar mode of action and longer half-life. Organophosphates inhibit acetylcholinesterase, affecting neurotransmission and causing uncontrolled nerve activation and death in insects (14).

A standard method for evaluating the efficacy of an aerial spray event compares pre- to post-treatment mosquito trap counts inside the treatment zone versus changes for the same period in an adjacent unsprayed control area (16). This method, first proposed by Mulla et al. (17), has been adapted to and widely used in evaluating the efficacy of aerial spraying for reducing the abundance of female mosquitoes and has been extended to assess changes in other indicators of risk, namely infection prevalence in mosquitoes, human cases, and reported dead birds with WNV infection (16). However, reported estimates vary widely, with some studies even indicating occasional increases in trap counts following spray events (18–21).

Despite its wide use, the assumptions behind Mulla’s formula are often violated, resulting in confounded estimates. First, treatment and control sites are often not independent due to the spatial connectivity of populations with mosquito dispersal and immigration (22). With the connectivity and potential drift of pesticides via wind, there is the potential that insecticide sprays have wider population impacts than just the targeted spray zone (20). Second, the difference in pre- to post- trap count ratios in and between areas are not solely due to control measures, but rather are impacted by weather, seasonality in mosquito populations, differential presence of larval breeding sources or simply stochastic variation in trapping success (18, 20, 21). Overall, Mulla’s formula neglects the spatio-temporal structure of mosquito populations and external factors impacting the random volatility of mosquito trapping success.

To overcome the limitations of assessing the efficacy of aerial sprays on the individual spray event basis, we paired long-term surveillance and vector control records (12 years) from Sacramento-Yolo Mosquito and Vector Control District (SYMVCD) in California to capture baseline spatio-temporal mosquito population dynamics and estimate the magnitude and duration of the impacts of aerial sprays on the abundance of Cx. pipiens and Cx. tarsalis, the predominant WNV vectors in California. We chose a generalized additive modeling (GAM) framework to capture the nonlinear population dynamics and associations inherent to mosquito collections.

Study Area

The study area encompasses Sacramento and Yolo counties, California (Fig 1) which have a combined area of approximately 5,126 km² and a population of approximately 1.73 million people in 2016 (23). Sacramento County is 34.12% urban and 65.88% rural with the majority of urban areas consisting of the concentrated Sacramento urban center and surrounding suburbs. In comparison, Yolo County is 4.61% urban and 95.39% rural with smaller, more dispersed urban areas (24). These counties, located in the northern part of California’s Central Valley, are characterized by a Mediterranean climate with hot, dry summers (Jul mean temperature: 25.8 °C, May-Sep mean total rainfall: 3.18 cm) and mild, rainy winters (Jan mean temperature: 9.6 °C, Oct-Apr mean total rainfall: 47.30 cm) (25) and extensive irrigated agriculture, especially rice and row crops such as tomatoes. Sacramento-Yolo Mosquito and Vector Control District (SYMVCD), established in 1946 to protect the public from nuisance mosquito biting and mosquito-borne diseases, manages mosquito populations in Sacramento and Yolo counties (26).

Aerial Treatments and Mosquito Collections

SYMVCD provided the spatial polygons (Fig 1b) and associated data detailing the date, area targeted for spraying, number of consecutive nights of spraying in the same location, and pesticide product used for all aerial sprays during the study period (1,021 unique nights of spraying during 930 spray events).

Mosquito collection records for CDC CO₂-baited EVS traps (28) from SYMVCD for the years 2006-2017 (Fig 1c) were obtained with permission through the CalSurv Gateway (29), an online database hosting data from California vector control agencies. Any records that indicated trap malfunctions or which unfeasibly ran longer than one night were excluded. Each record (n = 24,344) contained latitude, longitude, date, number of traps employed, and total female Cx. tarsalis and Cx. pipiens captured. Distribution of traps and spray events by year (Additional file 1) and season (Additional file 2) are presented in the Supplementary Information.

Any records that indicated trap malfunctions or which were operated for more than one night were excluded. For each species separately, we removed the collection reports corresponding to the top 5% of trap counts in each week to remove the influence of outliers (i.e., large singular deviations from broader abundance trends) on smooth functions subsequently estimated by the models.

All geographic data were projected from geographic to planar coordinates (Albers conic equal-area, EPSG 3310, NAD83) using the rgdal package in R statistical software (version 3.3.2; (30,31)) for all data processing and analysis.

Covariate Development

To isolate the effects of aerial insecticide treatments within out final statistical model, we first developed a set of spatio-temporal and environmental covariates to explain the long- and short-term trends in Cx. tarsalis and Cx. pipiens abundance. Inclusion of these covariates established a counterfactual basis in the models for the expectation in the absence of control, leaving the additional terms characterizing aerial insecticide sprays to explain any deviations attributable to the treatments.

For each remaining trap collection (n = 23,707 for Cx. pipiens; n = 23,678 for Cx. tarsalis), we derived a set of temperature variables to capture the effect of weather on trap collections. The mean temperature during the host-seeking period (dusk to dawn) and 30-year monthly average temperature were determined for each collection using 4-km resolution data provided by the PRISM Climate Group (32). We calculated the deviation in temperature from the monthly average during the host-seeking period to capture activity rates on the night of trapping (i.e., warmer/colder than ‘normal’ resulting in higher/lower mosquito activity and resulting trap counts). As mosquito developmental rates are highly impacted by temperature (33,34), we also calculated the average temperature during the two-week period immediately preceding the trap collection to capture short-term effects of weather on mosquito abundance. Rainfall was not considered because amounts were negligible in the study area during the season when aerial insecticide applications occurred.

To characterize the larval habitat present around a trap location and to incorporate the sharp changes in land use across the study area, we used the 30x30m gridded land cover data from the 2011 National Land Cover database (27). We used the classification of all pixels within a 5km radius area surrounding each trap to determine the proportion of three non-overlapping land use categories: urban, cultivated crops, and natural (Fig 1a). Land use categories were chosen to represent larval habitat and bionomics of the Cx. pipiens and Cx. tarsalis (35). The radius was chosen based on known dispersal distances for the species (36,37). The ‘urban’ category encompasses all levels of developed land (i.e. structures, roads, and constructed materials). The ‘crops’ category represents annual irrigated crops which are predominantly rice in the study area. The remaining classifications were combined to create the ‘natural’ category.

We quantified the spatio-temporal intersections between spray zone polygons and trap locations to quantify the degree to which antecedent spray events impacted mosquito collections. Spatial coverage of each trap was quantified as the average proportion of the area from which a trap collects mosquitoes (‘collection area’) that was covered by aerial treatment zones during the four weeks preceding the collection. Using a conservative estimate on Culex flight distance (36–39) and to account for insecticide drift during application, we used a 5km radius collection area for both species. The temporal sequence of overlapping sprays during the four weeks preceding a collection (modeled as a factor for each unique sequence) was used to capture any lagged effects and impacts of repeated spray events. For each week preceding a collection, the total proportion of the collection area overlapping with the treatment zone was assessed. When multiple treatment zones overlapped with a single collection area in a week, we assumed an additive effect, summing the proportions of overlap from each unique spray up to a maximum of 1.0 that represented complete coverage. We used the average spatial coverage of targeted spray zones during all weeks with at least one overlapping spray event to quantify the spatial impact of sprays for each specified temporal sequence of spraying. Traps > 5km from all treatment zones had a spatial coverage of zero and corresponded to the reference level of the temporal sequence factor. These traps were included to capture baseline spatio-temporal mosquito dynamics in the absence of aerial treatments. Therefore, the impact of aerial spray events on collections was quantified with a two-fold approach, namely with the factor corresponding to the sequence of weeks when spraying overlapped during the preceding four weeks and the average proportion of the collection area that overlapped under that sequence.

According to guidelines from the California Department of Public Health, periods of high risk for arbovirus transmission are characterized in part by abnormally high mosquito abundance (12). In order to capture this dramatic deviation from ‘normal’ abundance that our smoothed modeling framework could not capture, but that precipitated aerial spray events, we also applied a prospective assessment to identify spray events closely following each collection. To account for the time required to respond to a high-risk period, we assessed the presence of overlapping treatment zones with a collection in the following four weeks on the weekly scale, similar to the above retrospective assessment of sprays.

To capture potential differences between broad classes of pesticides used (organophosphate vs. pyrethrin and pyrethroids combined), we included a binary indicator variable for whether at least one spray event associated with a particular trap collection used an organophosphate. Sample sizes were too small to further investigate differences between pyrethrins and pyrethroids or between individual insecticide products.

We considered time in a variety of ways to capture trends in mosquito abundance in two parts: typical annual seasonality and coarser spatial-temporal trend over the twelve-year study period. Using the trap collection dates, ‘week’ (number of weeks from the start of the study period; range 1-626) and ‘day’ (range 1-365) variables were created to capture a continuous yearly effect and seasonality, respectively. We interacted the ‘day’ variable with each category of land use (i.e. ‘urban’, ‘crops’, and ‘natural’) to capture the seasonal trend in these different habitats. Each individual seasonality curve was weighted by the proportion of land use in that category within 5 km of the trap collection to produce a single unified seasonal trend that reflected the specific habitat composition for that collection.

Statistical Analysis

We developed generalized additive models (GAMs) to relate nightly trap counts of female mosquitoes, either Cx. tarsalis or Cx. pipiens, to aerial adulticide applications, adjusted for variation in trap counts due to spatio-temporal mosquito dynamics. We chose GAMs because of the flexible parameterization of smooth functions of covariates to explain spatial and temporal trends (40,41). Covariates considered to explain baseline mosquito dynamics were day or week of the year, year, location, land use, two-week average temperature, and nightly deviations from average temperature during trapping, the presence of a spray event in the following one to four weeks (high risk period), and pesticide class used in the aerial spray. Either a smooth function or a factor were used in fitting the covariates with the choice between these forms, along with spline and basis dimension if a smooth function was chosen, based on model fit and biological relevance. Cyclic cubic regression splines were used to prevent discontinuity between the ends of the smooth representing the seasonal patterns (aka between Dec 31 and Jan 1). Thin plate regression splines were chosen for most covariates because they are isotropic and have been shown to be the optimal smoother of any given basis dimension (42). A cubic regression spline was used in the spatio-temporal surface due to its superior performance over thin plate regression splines for the large amount of observations (43).

We fit negative binomial GAMs using the gam function in R (version 3.3.2; package mgcv) (30,44) with restricted estimation maximum likelihood (REML) as the smoothing parameter estimation method. We choses a negative binomial function to account for the over-dispersed nature of trap count data. We used backward selection guided by AIC (45) to reach our final model. In each model, we included an on offset term for the number of traps operated per trapping event. All covariates were included in the initial model and choices of interactions between covariates entered into the initial model were guided by biological relevance. We used concurvity, a measure of collinearity for smooth functions (range 0-1; 43), and visually examined deviance residuals for consistency in space and time to assess the final model fit.

Using the other covariates to establish the expected abundance of each species in the absence of aerial spraying, we estimated the mean change in predicted abundance across the range of spray regimes observed in the data, using the Bayesian posterior covariance matrix for the parameters that accounted for smoothing parameter uncertainty (43). We simulated 10,000 random draws from the posterior distribution of the fitted model, a multivariate normal distribution with mean equal to the estimated model coefficients and covariance matrix of the parameters, to predict the abundance of each species across the spatial and temporal sequences of sprays observed in the data. For each draw, we then calculated the mean change in abundance from the baseline no-spray scenario at each point on the spatio-temporal surface, along with the corresponding 95% confidence interval. Estimates of efficacy from the model were compared with those derived from Mulla’s formula (16,17).

Data overview and model selection

The relative abundance (number of females per trap-night) of Cx. pipiens and Cx. tarsalis varied spatially during the peak WNV season from late Jun to early Oct when aerial sprays occurred (Fig 2). Typically, higher abundance of Cx. pipiens was observed in urban areas whereas higher abundance of Cx. tarsalis was typically in non-urbanized areas near irrigated agriculture.

The final model for each species included an offset for the number of traps run per collection event; and smooth functions of space by time (on the weekly timescale across the twelve years), day of the year by each land use category (‘urban’, ‘crops’, and ‘natural’), two-week average temperature, nightly deviations in average temperature during trapping, and spatio-temporal impacts of aerial spraying. The resulting smooth relationships for each species are illustrated in Fig 3 (see Additional files 3-4 for spatio-temporal surfaces for all years for each species). Construction of smooth function used in the final models are outlined in Supplementary Table 1 (Additional file 5). All smooth functions were highly significant (P < 0.001). A random intercept for site location was included to account for repeated collections at the same location, fitted using coefficients penalized by a ridge penalty (46). We also retained, based on reductions in AIC, parameters for the presence of sprays in the 1 & 4 and 1, 2, & 3 weeks following the trap collection for Cx. tarsalis and Cx. pipiens, respectively (Supplementary Table 2, Additional file 6). Based on reduction in AIC, only the model for Cx. pipiens retained the term indicating the presence of at least one spray event with an organophosphate pesticide during the previous four weeks, as compared to all sprays using combinations of pyrethrin or pyrethroid products (-48.9% change in abundance for ≥ 1 organophosphate, P < 0.001).

The largest magnitude of variability in the baseline abundance for both species was due primarily to the seasonality covariates, followed by the spatio-temporal surface. The temperature covariates contributed the smallest magnitude to establishing abundance, but all smoothed functions were highly significant (P < 0.001). In all smooth functions, positive estimates correspond to increases in the population, negative estimates correspond to decreases in the population, and 0 indicates no modulation in abundance at that covariate value.

The distribution of the final model residuals was right-skewed for both species indicating the model underestimated extreme trap counts. However, no spatial or temporal pattern remained in the deviance residuals (Additional files 7-8). Both models had low estimated concurvity values (43) for the aerial spraying smooth function with the rest of the model parameters (Cx. pipiens: 0.145; Cx. tarsalis: 0.148). This indicates that the smooth estimates for the impact of aerial spraying were not confounded by other parameters. In addition, the relatively high deviance explained value for both models (Cx. pipiens: 44.0%; Cx. tarsalis: 62.3%) indicates good model fit despite for the complex dynamics inherent in mosquito populations.

Effects of aerial insecticide treatments

A smooth surface of the spatio-temporal impacts on Cx. pipiens abundance is presented for treatments with only pyrethrin or pyrethroid products (Fig 4A) or with at least one organophosphate product (Fig 4B). For Cx. tarsalis, the difference in impact by broad pesticide class was not retained in the final model, so a single smooth is presented (Fig 4C). Overall, the models estimated a lower magnitude of change in Cx. tarsalis abundance as compared to Cx. pipiens. For example, following aerial spraying with full spatial coverage, we estimated a mean one-week Cx. pipiens abundance change of -52.4% (95% CI: -65.6, -36.5%) if all spray events had used pyrethroid or pyrethrin products. If at least one organophosphate product had been used, we estimated a -76.2% (95% CI: -82.8, -67.9%) mean change in Cx. pipiens abundance. In contrast, Cx. tarsalis populations with full spatial coverage by aerial sprays showed an estimated -30.7% (95% CI: -54.5, 2.5%) mean change one-week post-spraying regardless of the product class.

For both species, larger reductions in abundances were estimated in areas with higher spatial coverage of aerial sprays (large proportion of spatial overlap) than those on the fringes (low proportion of spatial overlap). Sprays occurring closer in time to collections were generally estimated to result in larger reductions in abundance compared to those longer ago. At longer time lags (i.e., two to four weeks post-spraying), higher than expected abundance for both species was estimated, with the increase only occurring in Cx. pipiens populations following sprays with pyrethrins and pyrethroids.

The majority of temporal spray sequences lacked data across the full range of spatial overlap (0-100%); we did not estimate the change in abundance for these areas. Data were sparser or lacking for higher spatial coverage during multiple weeks of spraying. For regions of the spatio-temporal surface with data support, the reduction one-week post-spraying with full spatial coverage was the largest reduction predicted for Cx. tarsalis. In contrast, Cx. pipiens populations on the fringes of spray events for the preceding four weeks results in a similar reduction as for populations with full spatial coverage by aerial sprays one-week ago (all pyrethrin/pyrethroids: -54.3% (95% CI: -81.0, -6.2%) change; at least one organophosphate: -77.2% (95% CI: -90.4, -53.9%) change).

Comparison to conventional estimates

As a comparison for our model results, we applied the conventional approach of Mulla’s formula (16,17) to the combined trapping and control records from 2006-2017 to estimate the efficacy of sprays. Considering trapping one-week before and after a spray event and using a 5km buffer around the targeted spray zone as the adjacent comparison area, we were able to calculate the effect for 30 spray events (3.23%) for Cx. pipiens and Cx. tarsalis; the majority of spray events lacked traps in all of the required spatial and temporal locations for the calculation. Most of the estimates for the change in abundance indicated a reduction in trap counts, but estimates varied widely, ranging from complete population elimination (100% decrease) up to 11,000% increases following a spray event (Additional file 9). Most estimates for Cx. pipiens indicated varying degrees of reduction while those for Cx. tarsalis spanned reductions to increases.

This study found that aerial insecticide treatments achieve substantial short-term reductions in both Cx. tarsalis and Cx. pipiens populations. Previous studies have assessed the short-term impact of aerial spraying on mosquito abundance and highlighted the volatility of estimates across space and time. In order to overcome the limitations of using single events to estimate the efficacy of aerial spraying on reducing the abundance of WNV vector mosquitoes, we used a large dataset of surveillance and control records together with GAM models. This modeling framework allowed us to establish baseline mosquito adult abundance and identify deviations from expected nightly abundance attributed to aerial spraying as well as the spatial and temporal impacts of aerial applications. Our results indicate that aerial sprays do achieve population reduction for both Cx. pipiens and Cx. tarsalis with heterogeneity in the magnitude and pattern of reduction between species and pesticide product.

The differences in the magnitude and pattern of estimated response between species can be attributed partially to the different bionomics of the individual mosquito species. In the study area, Cx. pipiens are predominantly peridomestic with larval habitats limited primarily to backyard sources and stormwater systems in urbanized areas (35, 47). Thus, areas targeted by aerial insecticide treatments would span a large fraction of any particular population, leaving few adults to repopulate the treated area from proximal unsprayed locations. In contrast, Cx. tarsalis breed in agricultural areas and may disperse into surrounding agricultural and urban areas (35, 48, 49). This species also has a larger typical dispersal distance and achieves higher population densities than Cx. pipiens (35–37). Aerial insecticide treatments typically target only a small fraction of the total available habitat for Cx. tarsalis, often near urbanized areas, and any effect of aerial sprays could be moderated by immigration of adult Cx. tarsalis from surrounding unsprayed locations, potentially from distant locations (38, 50). Therefore, the best suppression for Cx. tarsalis populations would be achieved in isolated areas, as has been reported previously (22). Additionally, repetition of sprays on the weekly scale is less effective at controlling Cx. tarsalis than Cx. pipiens because of the rapid immigration and emergence of new adults from large areas of productive larval habitat.

While our estimated reduction in abundance of Culex mosquitoes show some similarity to previous published estimates of aerial spray events from Sacramento and Yolo counties (Table 3), our methodology also accounted for contextual factors, resulting in more robust estimates of the average effect of spraying. Previous estimates exhibited spatial heterogeneity (19). Utilizing covariates to capture the spatial structure, temperature deviations, and varying distribution of larval habitats removed the confounding impact of these factors on our model results. Similarly, previous estimates have varied, in part because Mulla’s formula cannot fully capture spatio-temporal nuances of mosquito population dynamics. For example, Lothrop et al. (20) observed 73% increases in Cx. tarsalis abundances post-spraying despite observing mortality in caged sentinel mosquitoes and large reductions during previous spray events. The authors attributed the estimated increase to the dynamics of Cx. tarsalis populations at the time of the study, particularly the large emergence of Cx. tarsalis following the annual flooding of the nearby wetlands that was not captured by the Mulla’s formula framework and the fact that the sprays were not impacting mosquitoes in the productive larval habitats. Previous estimates also use differing time interval lengths to estimate mosquito abundance before and after spray events. The heterogeneity in these time intervals combined with the heterogeneity of resulting estimates (Table 1) highlights the need to use consistent time intervals to improve generalizability of estimates between studies.

Our model structure most closely compares to the study design used by Elnaiem et al. (21) where a timescale of one week before and after a spray event with a pyrethroid pesticide was chosen when assessing mosquito abundance (Table 1). Our estimates for reduction for Cx. pipiens (-52.4%) and Cx. tarsalis (-30.7%) are lower than the observed reductions (Cx. pipiens: -75%; Cx. tarsalis: -48.7%). While qualitatively similar, the differences in magnitude may be due to differences in analytical methods, shifts from pyrethrin to pyrethroids over time, or the longer twelve-year time period of our study that could have yielded a more conservative estimate of average spray effects.

The smooth functions associated with land use categories in the final GAMs accurately captured known seasonal and population dynamics. Cultivated crops were the primary source of Cx. tarsalis with smaller contributions from other non-urban land types during the warmest months of the year, accurately representing the presence of highly productive larval habitats in clean, recently created water sources characteristic of cultivated crops (35, 48, 52). Urbanized areas did not produce large numbers of Cx. tarsalis during the WNV season as they contain few suitable larval habitats for this species. The estimated peak in abundance occurred in late July, but remained high through September, capturing the variation in timing of the peak across the years of the study. Populations of Cx. tarsalis in the Sacramento Valley are greatest from July-September (35, 53, 54). The steep slope of the curve up to the peak mimicked the rapid increase in Cx. tarsalis observed at the start of the planting season (35, 54). For Cx. pipiens, urbanized areas largely contributed to abundance throughout the year with additional contributions in natural areas (aka non-cultivated croplands) later in the season, reflecting the presence of larval habitats in artificial structures like storm drains or dairy wastewater lagoons (55, 56). Crops generally had lower Cx. pipiens abundance across the season, reflecting the general lack of high quality suitable larval habits in these areas.

Temperature anomalies during trapping and the two-week average antecedent temperature prior to trapping contributed to the overall abundance of both species, albeit relatively weakly in the presence of the other spatio-temporal terms. Their inclusion in the model was required to fully account for mosquito dynamics and night-to-night fluctuations in trapping success. Concordant with previous experiments, extremes in the average temperatures reduced abundance for both species illustrating the negative impacts on mosquito developmental rates and adult survivorship (33, 34). The estimated region of positive contribution to abundance for both species (Cx. pipiens: 19.2–25.4 °C; Cx. tarsalis: 18.9–27.0 °C) was narrower than the thermal tolerance of the species, but contains the observed regions of rapid developmental and high reproduction rates and the typical temperature ranges during the summer. As expected, small anomalies in average temperature on the night of trapping made relatively small contributions to change in abundance while extreme deviations result in much more marked change, highlighting the non-linear relationship underlying temperature and trap success.

It is interesting to note the additional marked reduction in Cx. pipiens abundance when at least one organophosphate product was used, especially as compared to the lack of a similar difference in Cx. tarsalis populations. As mentioned above, the class of product used may be more important for Cx. pipiens due to their focal distributions and more limited dispersal (35, 57). As an aerial spray will likely impact a large proportion of the localize Cx. pipiens population at once, there will be limited immigration from unsprayed segments of the population in the nearby proximity. Therefore, the full effect of an aerial spray is discernable. In contrast, the dispersed nature of Cx. tarsalis populations facilitates rapid immigration from surrounding unsprayed locations (35, 36, 38), thus diluting any difference in effect between product classes; any difference is not discernable against the background population dynamics accounted for in our modeling framework. Another factor contributing to the difference by species could be insecticide resistance as resistance to pyrethroids and organophosphates have been reported for both species in California (14, 58, 59). If Cx. pipiens populations in the study area were more resistant to pyrethroids than Cx. tarsalis, this could explain the increased efficacy of organophosphates for Cx. pipiens. However, since we found a stronger effect of pyrethroids on Cx. pipiens as compared to Cx. tarsalis, resistance does not fully explain the observed difference. Alternatively, a single organophosphate spray may be insufficient to produce a marked difference in Cx. tarsalis populations; a repetition may be required. The underlying shape of the smooth function of spatio-temporal impacts of aerial spraying for either species likely differs between product classes and the specific timing and number of different products used, but sparse data prevented us from including an interaction to assess these dynamics.

A potential population rebound effect occurred for both species at more distant time lags from spraying where abundance was estimated to be higher than expected two to four (Cx. pipiens under pyrethrin and pyrethroid sprays) and three to four (Cx. tarsalis) weeks post-spray. Appropriately spaced treatments in time may be required to maintain a long-term reduction in population abundance. However, such a rebound does not negate the potential value of aerial treatments for achieving short-term reductions in the abundance of WNV-infected adult mosquitoes during periods of epidemic risk.

The increase in abundance at low spatial coverages of sprays for both species could reflect excito-repellency of pesticides at the fringes of targeted areas. Excito-repellency, a form of behavioral avoidance, combines two forms of sub-lethal exposure that results in mosquito movement away from a chemical source; contact excitation (increased activity upon contact) and non-contact spatial repellency (60–62). These non-toxic behavioral impacts of pesticides were first identified in Anopheles mosquitoes in response to DDT and later with insecticide-treated bed nets and indoor residual spraying (63–65). Populations of Cx. quinquefasciatus, another species in the Cx. pipiens complex, exhibit strong contact excitation and poor spatial repellency to pyrethroid, organophosphate, and carbamate pesticides (66, 67). No study has investigated excito-repellency in Cx. tarsalis populations. The behavioral avoidance of Culex to pesticides could be pushing mosquitoes out of the spray zones, resulting in an increase in abundance around the fringes of sprays.

A limitation of choosing a GAM framework is that we were only able to capture the average effects of covariates on nightly mosquito trap counts and unable to fully account for large stochastic fluctuations inherent to mosquito populations. However, GAMs easily allowed us to incorporate nonlinear relationships between abundance and covariates without having to constrain relationships with a priori knowledge. In particular, we were able to capture the higher-order relationships and correlation across space and time with the three-dimensional spatio-temporal function. The form of the smooth relationships in the final model did appear to approximate what is observed in nature. Other strengths of our modeling approach are that it takes into account regional differences in mosquito populations, population dynamics and seasonality in different land use types, and the impacts of short-term (night) and longer-term (two week) weather, resulting in robust estimation of the baseline expected abundance in the absence of spray effects, allowing us to isolate the deviations in abundance due to aerial spraying.

However, even with the large amount of data available, data were inadequate to estimate the impact of aerial spraying reliably for certain time lags or spatial coverages that were rare or absent in the data. This is primarily due to typical SYMVCD spraying and trapping practices due to logistical and financial constraints. SYMVCD concentrated their mosquito collections efforts near urban areas to maximize the sensitivity for assessing the risk in proximity to human populations while minimizing time and costs associated with large-scale mosquito surveillance. Additionally, in an effort to control mosquitoes in known problem areas (highly productive larval habitats in proximity to the margins of urban areas) and reduce aerial applications over urban areas, the majority of areas receiving repeated sprays across the WNV season are in more rural areas where the mosquito trapping is sparser. This limited the data and statistical power to quantify the full range of spatial overlap with aerial sprays.

We were also unable to explicitly account for drift outside the target zones during sprays, as has been previously described (20). Our use of a continuous variable to measure spray coverage within the 5 km-radius collection areas surrounding each trap partially accounts for this effect. As such, however, we are unable to fully parse out the effect of aerial spraying on populations outside aerial spray zones and limited our analysis to only assess spatial coverage of traps within targeted spray zones.

Additionally, we were unable to estimate the relative effects of different lengths of multi-night spray events (one vs two vs three consecutive nights) due to data limitations and our analytical choice to aggregate all sprays on the weekly scale to achieve the balance between robust estimates and operationally relevant information for vector control districts. These limitations of observational studies such as this one could be addressed in future experimental field trials.

Aerial adulticides were shown to achieve short-term reductions in the abundance of the primary West Nile virus vectors, Cx. tarsalis and Cx. pipiens. A greater reduction was estimated for Cx. pipiens, likely due to its focal distribution in urbanizes areas and limited dispersal. The use of organophosphate products versus a combination of pyrethrins and pyrethroids increased the magnitude of reduction estimated for Cx. pipiens while the difference by broad insecticide class was not significant for Cx. tarsalis. The effects of aerial sprays on Cx. tarsalis populations were likely moderated by the species broad dispersal ability, large population sizes, and vast expanses of productive larval habitat in the study area. Therefore, the best control of Cx. tarsalis would be achieved in areas with isolated or highly spatially segmented populations.

For both species, aerial spraying reduced abundance at high spatial coverage while reductions were also estimated at lower spatial coverage, at albeit greatly reduced magnitudes, indicating that aerial sprays had some impacts beyond the target zone. There was also evidence for population rebounds at periods of two to four weeks post-spraying.

Our modeling approach allowed us to utilize observational data to isolate aerial treatment effects while taking into account contextual factors like spatio-temporal relationships, weather, and habitat that contribute to stochastic variation in nightly trap counts. This is an important advance that complements experimental trials and expands upon conventional observational approaches that summarize population changes following aerial treatments at individual time points.

Further work should expand upon these methods to estimate the change in WNV transmission potential and resulting human infections following aerial spray events.

GAM: generalized additive model

SYMVCD: Sacramento-Yolo Mosquito and Vector Control District

WNV: West Nile virus

Ethics approval and consent to participate: Not applicable

Consent for publication: Not applicable

Availability of data and materials: The data that support the findings of this study were obtained from the Sacramento-Yolo Mosquito and Vector Control District. These data were used with permission for the current study and are not publicly available. Data are however available from the authors upon reasonable request and with permission from the Sacramento-Yolo Mosquito and Vector Control District.

Competing interests: The authors declare that they have no competing interests.

Funding: KH acknowledges funding support from the Floyd & Mary Schwall Fellowship in Medical Research at UC Davis, and KH and CB acknowledge support from the Pacific Southwest Center of Excellence in Vector-Borne Diseases funded by the U.S. Centers for Disease Control and Prevention (Cooperative Agreement 1U01CK000516). KH acknowledges supported by the National Center for Advancing Translational Sciences, National Institutes of Health, through grant number UL1 TR001860 and linked award TL1 TR001861.

Authors’ contributions: KH performed the analysis and wrote the initial draft of the manuscript. CB conceived the project idea, supervised the research, and contributed to revisions of the manuscript. RR provided statistical guidance. All authors read and approved the final manuscript.

Acknowledgements: We would like to thank Ruben Rosas, Marcia Reed, Sarah Wheeler, Samer Elkashef and Gary Goodman from Sacramento-Yolo Mosquito & Vector Control District for providing trapping and aerial treatment data used in this study and for their insight and feedback on mosquito control practices.

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Table 1

Estimated change in Culex mosquito populations following aerial spray events in California using Mulla’s formula.
Location City, county	Year	Nights Sprayed^*	Product Class	Comparison Length^†	Species	% Change^‡	Reference
Davis, Yolo	2006	2	pyrethrin	2 days before, 2 days after	Cx. pipiens	− 58.0	(19)
Davis, Yolo	2006	2	pyrethrin	2 days before, 2 days after	Cx. tarsalis	− 25.6
Woodland, Yolo	2006	2	pyrethrin	2 days before, 2 days after	Cx. pipiens	− 77.7
Woodland, Yolo	2006	2	pyrethrin	2 days before, 2 days after	Cx. tarsalis	− 46.8
Sacramento, Sacramento	2005	3	pyrethrin	7 days before, 7 days after	Cx. pipiens	− 75.0	(21)
Sacramento, Sacramento	2005	3	pyrethrin	7 days before, 7 days after	Cx. tarsalis	− 48.7	(21)
Sacramento, Sacramento	2006	3	pyrethrin	3 days before, 3 days after	Cx. pipiens	− 39.3	(51)
Sacramento, Sacramento	2006	3	pyrethrin	3 days before, 3 days after	Cx. tarsalis	− 57.3	(51)
Coachella valley, Riverside	2005 (Mar)	3 alt^	pyrethroid	5 days before, 1 day after	Cx. tarsalis	− 93.0	(20)
	2005 (Jun)	3 alt^	pyrethroid	5 days before, 1 day after	Cx. tarsalis	− 77.0
	2005 (Sep)	3 alt^	pyrethroid	5 days before, 1 day after	Cx. tarsalis	73.0
^* Number of consecutive nights sprayed in spray event.
^† Length of time before and after an aerial spray event used when comparing of trap counts.
^‡ Percent change in Culex abundance following an aerial spray event as calculated using Mulla’s formula (16, 17).
^ Aerial spraying occurred on 3 alternate nights.

Additionalfile9.pdf
Estimated percent change in Cx. pipiens and Cx. tarsalis populations with Mulla’s formula. Change estimated for the 30 aerial sprays in Sacramento and Yolo counties, CA (2006-2017) with associated trap collections within the targeted zone (treated) and an adjacent 5km buffer (control) within one-week before and one-week following spraying.
Additionalfile8.pdf
Spatial and temporal distribution of model deviance residuals for Cx. tarsalis for 2006-2017. Residuals presented spatially at the associated trapping location (random jitter of ≤ 1 km applied for visualization of repeated events).
Additionalfile7.pdf
Spatial and temporal distribution of model deviance residuals for Cx. pipiens for 2006-2017. Residuals presented spatially at the associated trapping location (random jitter of ≤ 1 km applied for visualization of repeated events).
Additionalfile6.docx
Change (%) in nightly abundance from expected for collections preceding aerial spraying. Table indicating the final model estimates for change in expected trap-counts for collections in the one to four weeks preceding an aerial spray event.
Additionalfile5.docx
Smooth functions included in the final GAMs for both Cx. tarsalis and Cx. pipiens. Table outlining the construction of smooth function used in the final models, including spline type and basis dimensions chosen.
Additionalfile4.pdf
Spatial surface for Cx. tarsalis at midpoint of typical WNV season (week of Aug 1). Surface presented for each year (2006-2017) is a slice from the three-dimensional spatio-temporal smoothed function. Contours applied for visualization of estimates.
Additionalfile3.pdf
Spatial surface for Cx. pipiens at midpoint of typical WNV season (week of Aug 1). Surface presented for each year (2006-2017) is a slice from the three-dimensional spatio-temporal smoothed function. Contours applied for visualization of estimates.
Additionalfile2.pdf
Location of CO2-baited mosquito trapping events and aerial spray events stratified by season. Season defined into three-month intervals. A random jitter of ≤ 1 km applied to trapping locations for visualization of repeated events at the same site. Each spray event polygon represents the area targeted during a single aerial spray application.
Additionalfile1.pdf
Location of CO2-baited mosquito trapping events and aerial spray events stratified by year (2006-2017). A random jitter of ≤ 1 km applied to trapping locations for visualization of repeated events at the same site. Each spray event polygon represents the area targeted during a single aerial spray application.

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Spatio-Temporal Impacts of Aerial Adulticide Applications on Populations of West Nile Virus Vector Mosquitoes

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