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. 2015 Nov 2;53(1):31–38. doi: 10.1093/jme/tjv170

Development and Evaluation of an Attractive Self-Marking Ovitrap to Measure Dispersal and Determine Skip Oviposition in Aedes albopictus (Diptera: Culicidae) Field Populations

Timothy J Davis 1, Phillip E Kaufman 1,2, Andrew J Tatem 3,4, Jerome A Hogsette 5, Daniel L Kline 5
PMCID: PMC4723682  PMID: 26534725

Abstract

Aedes albopictus (Skuse) is a container-breeding species with considerable public health importance. To date, Ae. albopictus oviposition behavior has been assessed in outdoor conditions, but only with laboratory-reared specimens. In outdoor large-cage and field studies, we used an attractive self-marking ovipositional device to assess Ae. albopictus skip oviposition behavior. In field studies, 37 wild Ae. albopictus that visited an attractive self-marking ovisite were subsequently captured at a sticky ovitrap within a 4-d period. Because the average Ae. albopictus gonotrophic period is 4.5–6 d, the wild-caught Ae. albopictus visited at least two oviposition sites within a single gonotrophic period. This provided field-based indirect evidence of skip oviposition. The mean distance traveled (MDT) during the 20-d evaluations ranged from 58 to 78 m. The maximum observed distance traveled was 149 m, which was the outer edge of our trapping ability. As populations of Ae. albopictus increased, the MDT during the 4- and 20-d post-marking period increased significantly. Additional observations of wild-marked and captured Aedes triseriatus (Say) are discussed.

Keywords: installment oviposition, egg distribution, vector surveillance, Aedes triseriatus

Knowledge of mosquito dispersal is important for understanding mosquito-borne disease epidemiology and developing effective control strategies (Guerra et al. 2014). Mosquitoes disperse to locate sugar sources, mates, resting sites, bloodmeals, and oviposition sites. In mosquitoes that display skip oviposition, the female will disperse over an area in search of multiple oviposition sites within a single gonotrophic cycle (Mogi and Mokry 1980). Aedes albopictus (Skuse), the Asian tiger mosquito, appears to exhibit skip oviposition behavior (Rozeboom et al. 1973, Davis et al. 2015; Fonseca et al. 2015).

Aedes albopictus dispersal has been examined in several studies (Bonnet and Worcester 1946, Mori 1979, Niebylski and Craig 1994, Honorio et al. 2003, Liew and Curtis 2004, Maciel-de-Freitas et al. 2006, Lacroix et al. 2009, Marini et al. 2010). In most studies, Ae. albopictus adults have remained in an area less than 120 m from the release site (Bonnet and Worcester 1946, Niebylski and Craig 1994, Lacroix et al. 2009, Marini et al. 2010); however, in some studies, this mosquito dispersed >800 m (Honorio et al. 2003, Maciel-de-Freitas et al. 2006). In mosquitoes that exhibit skip oviposition, little information has been reported in regards to the distance traveled between oviposition sites (Honorio et al. 2003, Liew and Curtis 2004). This knowledge is critical to development of new approaches in Ae. albopictus control where skip ovipositing mosquitoes might be used to distribute an insect growth regulator (IGR) to multiple larval habitats (Caputo et al. 2012, Gaugler et al. 2012). The distance traveled by contaminated mosquitoes during skip oviposition will determine the extent to which such a control measure can be dispersed utilizing auto-dissemination techniques.

An attractive self-marking ovitrap (ASMO) using fluorescent dusts was developed and used to directly examine the distance traveled from one ovisite to another and indirectly determine the occurrence of skip oviposition. Laboratory studies were conducted to examine the ASMO’s marking potential, the influence of marking dusts on survivorship, and the ability of sticky ovitraps to recapture marked mosquitoes. The ASMO was deployed in the field to mark naturally occurring Ae. albopictus populations with dust, while sticky ovitraps were positioned to capture the marked mosquitoes at secondary ovisites. Substantiating that field populations of Ae. albopictus display skip oviposition and determining the distance traveled between oviposition sites would enable mosquito control personnel to exploit skip oviposition behaviors for management purposes.

Materials and Methods

ASMO Caged Trials

Two evaluative studies were conducted to test the effectiveness of the ASMO. An indoor cage study was performed to evaluate the ability of an ASMO to mark Ae. albopictus females and determine the influence of fluorescent dusts (Day-Glo Color Corp., Cleveland, OH and United States Radium Corp., Hackettstown, NJ) on survivorship after marking. An outdoor screened enclosure study was conducted to examine the potential for Ae. albopictus females to be self-marked by an ASMO and collected by sticky ovitraps; and to determine the influence of fluorescent dusts on dispersal distance.

The ASMO consisted of a 1.8-liter plastic container (16 cm in diameter by 11 cm in depth) painted black with a 6-cm hole cut in the center of the lid (Fig. 1a). A 15 by 150-mm-diameter plastic petri dish lid (Corning Inc., Corning, NY) was placed snuggly in the container at a height of 4 cm from the bottom (Fig. 1b). The petri dish had an 8-cm hole cut in the center. The inside of the ASMO was coated with fluorescent dusts applied with a 113-g bulb duster (The Centro Company, North Liberty, IA). An oak leaf infusion (600 mL), added as an attractant, was carefully poured into the container through the hole in the petri dish. The infusion was formulated by adding 150 g of fallen live oak (Quercus virginiana Miller) leaves to 15 liters of well water in a container that was sealed, placed outside, and allowed to ferment for 7 d, as modified from Allan and Kline (1995).

Fig. 1.

Fig. 1.

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An attractive self-marking ovitrap (ASMO) and sticky ovitrap used to monitor Aedes albopictus (Skuse) skip oviposition. (A) ASMO with the lid attached. (B) ASMO with the lid removed to display the fluorescent dust-coated interior. (C) Sticky ovitrap with lid removed to display sticky panels and captured mosquitoes.

Indoor ASMO Study

For the indoor ASMO marking evaluation study, there were five treatments consisting of infusion-baited ASMOs treated individually with one of four fluorescent dusts; two Day-Glo® (Cleveland, OH) fluorescent dusts (Horizon Blue®, Rocket Red®), or two US Radium (Hackettstown, NJ) fluorescent dusts (Yellow 2267 and Green 1953), or an undusted control. The study was conducted in a randomized complete block design with three blocks of five cages for a total of 15 cages per replication. This test was replicated five times, providing an overall n = 15 for each treatment. Each treatment ASMO was placed individually inside a 61 by 61 by 61-cm screened cage. The cages were held at 25 ± 1°C, 75 ± 5% RH, and a photoperiod of 12:12 (L:D) h. Mosquitoes were provided 5% sucrose solution-soaked cotton balls for the duration of the study.

The source and rearing of the mosquito colony used in the indoor ASMO evaluations was described in Davis (2013). These mosquitoes were blood-fed 7 d after emergence using bovine blood-filled sausages, and then held for an additional 5 d. Twenty gravid Ae. albopictus (laboratory colony generations F2–F7) were released into each cage with a treatment ASMO. After a 48-h exposure to the ASMO, mosquitoes were removed by aspiration and examined on a chill table (3.8°C) under long-range ultraviolet (UV) light (Scorpion Master, Chandler, AZ) to detect marked individuals. All marked mosquitoes were returned to their respective cages from which the ASMO was removed and the unmarked mosquitoes were discarded. Thereafter, every 24 h, dead mosquitoes were removed from the cages and the daily mortality rate (DMR) was recorded until all mosquitoes were dead. The DMR was the number of deaths during a 24-h interval divided by the number of individuals alive during the start of that interval multiplied by 100 (Smiley 1985). The mean DMR was calculated and compared for each treatment.

Outdoor ASMO Study

An outdoor screened enclosure ASMO evaluation study was conducted to examine the potential for Ae. albopictus females to self-mark at an ASMO and subsequently be captured at a sticky ovitrap. The influence of fluorescent dusts on dispersal distances was also evaluated. Aedes albopictus (generations F4–F9) were fed and held as previously described. The five treatments used in the indoor cage study were also used in this study. A 61 by 61 by 61-cm screened cage was placed in the center of one of several large [9.2 m in width by 18.3 m in length by 4.9 m in height, gabled to 6.1 m (Kline 1999)] outdoor screened enclosures located at USDA-CMAVE, Gainesville, FL. Each treatment consisted of 20 gravid Ae. albopictus initially released into the cage that was placed on the ground and contained an infusion-baited, treated ASMO. After a 24-h exposure, the top of the cage was opened inside the screened enclosure, releasing the mosquitoes into the screened enclosure in which 16 infusion-baited sticky ovitraps had been placed. The sticky ovitraps were distributed evenly around the ASMO treatment cage by dividing the area within the large screened enclosure into four concentric rings (radius of each = N + 1 m, where N = 0, 1, 2, and 3 m) and placing a trap every 3.14 m2. This resulted in the following number of traps placed at the edge of each concentric ring within each enclosure: one trap at 0-1 m, three traps at 1–2 m, five traps at 2–3 m, and seven traps at 3–4 m. All ASMOs and sticky traps were placed on the ground.

Sticky ovitraps consisted of the aforementioned 1.8-liter black plastic containers with inside walls lined with two sticky panels made from 7 by 21.6-cm-long strips of transparency film (3M, St. Paul, MN), coated with Catchmaster bulk glue (The Catchmaster Co., Brooklyn, NY) and attached with paper clips (Ritchie et al. 2003) (Fig. 1c). Sticky panels were collected 24 h after the ASMO treatment cage was opened. The numbers of marked and unmarked mosquitoes on the sticky panels were recorded. The mean distance traveled (MDT) was calculated and compared for each treatment. This study was conducted as a complete randomized design with five replications per treatment.

Field Studies

Field experiments were conducted in Gainesville, FL, at a cemetery and on the University of Florida campus to determine if Ae. albopictus females visit two or more oviposition sites within a gonotrophic cycle and to assess the distance traveled between oviposition sites.

An infusion-baited ASMO was placed at a known Ae. albopictus developmental site at each location. A circle with a radius of 150 m was marked around the ASMO and 50 sticky ovitraps were distributed over this area (Fig. 2). To facilitate distribution of the sticky ovitraps within the circle, the trapping area was divided into five concentric rings (radius of each = N + 30 m, where N = 0, 30, 60, 90, 120, and 150 m) and the number of sticky ovitraps placed was approximately one for every 1,413-m2 area, although trap placement was clustered owing to habitat variation described below. Thus, the trapping density is represented by the following number of traps placed within each concentric ring: 2 traps at 0–30 m, 6 traps at 30–60 m, 10 traps at 60–90 m, 14 traps at 90–120 m, and 18 traps at 120–150 m. Because actual trap placement was dependent on the location of appropriate available habitat and site restrictions, traps were more clustered in some areas within a ring (Fig. 2). Regardless of trap-to-trap spacing, all traps were placed in habitats that were shaded and contained vegetation (Lambrecht 1971). All sticky ovitraps were georeferenced with a hand-held global positioning system (GPS) device (MiTAC International Corp., San Dimas, CA). All ASMOs and sticky traps were placed on the ground.

Fig. 2.

Fig. 2.

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Aerial images of the two field sites used to evaluate Aedes albopictus (Skuse) skip oviposition located in Gainesville, FL: (A) a graveyard and (B) the University of Florida campus. Each field site had 50 sticky ovitraps (represented by dots) located in 30-m concentric rings originating from a centrally placed attractive self-marking ovitrap. Map data: Google.

ASMOs at each location were treated with the same fluorescent dust color, using the method described above. After 4 d in the field, the ASMOs were replaced with new ASMOs containing a different dust color. Dust colors in both ASMOs were rotated using the following schedule: red on days 0–4, blue on days 4–8, yellow on days 8–12, and green on days 12–16. Following the 12–16-d exposure, ASMOs were removed from the field and no ASMO was present during the next 16 d. Thus, each trial consisted of a 32-d period when self-marked mosquitoes of each dust color were available to be trapped in sticky ovitraps for a minimum of 20 d. Each 32-d trial was replicated six times at both locations between June 5 and September 5, 2011, and June 5 and September 5, 2012. Following passage of Tropical Storm Debbie, municiple mosquito control was conducted through the application of Aqua-reslin® (permethrin and piperonyl butoxide) from a ground-based truck once every 2 wk around the cemetery site beginning in late June 2012. No mosquito abatement was conducted in 2011 or at the University site in 2012.

All sticky ovitraps were serviced every 4 d by replacing sticky panels, the oak infusion, and any missing or damaged traps. Retrieved sticky panels were examined under long-wave UV light and the number of marked and unmarked Ae. albopictus and Aedes triseriatus (Say) was recorded. Aedes albopictus and Ae. triseriatus were identified using the keys of Darsie and Morris (2003). The collected mosquitoes were subsequently dissected to determine if developed eggs were present using the method of Lounibos et al. (1990). During each replicate, captured self-marked mosquitoes were recorded by color for each trapping period. The marked mosquitoes captured within 4 d of the same color being placed in the ASMO were considered as having visited two ovisites within a gonotrophic cycle, based on the average time per gonotrophic cycle of 4.5–6 d for Ae. albopictus (Gubler and Bhattacharya 1971, Mori and Wada 1977).

Statistical Analysis

All data analyses were conducted in JMP® Version 8 (SAS Institute 2009). Data from the indoor ASMO evaluation were analyzed to determine the effectiveness of the ASMO to mark mosquitoes and the influence of marking dusts on the DMR. The hypothesis that the mean number of mosquitoes marked for each treatment was equal was tested using a two-way analysis of variance (ANOVA). In addition, the DMR for each treatment was examined using the two-way ANOVA. The Tukey–Kramer Honestly Significant Difference (HSD) multiple means comparison was completed to examine differences among the treatment means, where alpha = 0.05 for each pairwise comparison.

The outdoor screened enclosure ASMO evaluation data were analyzed to determine the influence of marking dusts on dispersal distances. Treatment MDTs were compared using a one-way ANOVA and the Tukey–Kramer HSD multiple means comparison.

The field study examined naturally occurring female Ae. albopictus and Ae. triseriatus following visitation to an ASMO through their distance traveled both within the five trapping periods as well as the MDT across the experiment. The distance traveled within a trapping period was analyzed using a mixed-model ANOVA in JMP® Pro Version 11 (SAS Institute 2009). Each species was evaluated separately, with trapping period as a fixed effect and the variables year and site as random effects. A Tukey–Kramer HSD test was applied to the trapping period data.

The MDT was calculated for those mosquitoes captured in the first 4-d period at each study site following an initial color placement during each of the six replicates (n = 12). In addition, the MDT during a 20-d period was calculated for each of the six replicates (n = 12). To account for unequal sticky trap distribution and sticky trap loss, the MDT was calculated according to Lillie et al. (1981):

MDT=∑(EC × median distance of annulus)for all anuli total EC

where the estimated captures (EC) are the number of captures that would be expected if the trap density was equal in each annulus:

EC = Number of observed marked captures per annulus Number of sticky ovitraps per annulus × CF

where the correction factor (CF) was used to account for differences in trap densities among annuli:

CF=area of annulustotal trapping area × total number of sticky ovitraps in trapping area

A two-way ANOVA was completed to account for site and year variance on the MDT. This comparison was conducted for the MDT within the first 4 d of each color placement and the overall 20-d MDT and was calculated for Ae. albopictus and Ae. triseriatus independently. A Student t-test was used to identify differences in the MDTs. The maximum observed distance travelled (ODTmax) was defined as the linear distance from the ASMO to the most distant positive sticky ovitrap and was determined for each year.

Linear regression analysis was conducted on the MDT data to determine the impact of distance dispersed during oviposition, while accounting for mosquito population changes. To accomplish this, the distance traveled by self-marked mosquitoes from an ASMO within the trapping period in which the mosquito was subsequently captured was assembled within both the 4-d and the overall 20-d capture periods. Thereafter, the MDT of marked mosquitoes was regressed upon the total number of marked and unmarked conspecific female mosquitoes captured at each site during each replication. To assess the relationship of MDT to mosquito population changes, a one-way ANOVA was completed to determine if the slope of the regression line was greater than zero. The slope was considered significantly different from zero if the P-value was below 0.05. Linear regression analyses were performed for both field sites on the MDTs that were converted using the CF of Lillie et al. (1981) over the six replications.

Results

ASMO Evaluation Studies

In indoor testing of the ASMO with fluorescent dust, the average proportion of marked gravid mosquitoes ranged from 75 to 81%. The DMR ranged from 24.1 to 24.9. No significant difference was found when comparing the average proportion of mosquitoes marked by each color or the DMR.

In outdoor screened enclosure studies, 66–70% of the Ae. albopictus gravid females released were found to have self-marked and were subsequently captured on sticky ovitraps. This demonstrated that the mosquitoes visited multiple ovisites within one gonotrophic cycle. No significant difference between the MDT for mosquitoes exposed to fluorescent dusts (range = 2.49–2.66 m) and those mosquitoes exposed to an ASMO without dust (2.49 m) was observed.

Field Studies

During the trial, 2,067 gravid Ae. albopictus and 501 gravid Ae. triseriatus were collected from sticky ovitraps (Table 1). Among the gravid mosquitoes collected, 37 Ae. albopictus and 17 Ae. triseriatus had visited an ASMO and were captured within 4 d of being self-marked (Table 1). The MDT in the first 4 d of being self-marked was not significantly different between sampling years for either species. An MDT of 22.50 m and 31.33 m was recorded for gravid Ae. albopictus collected in 2011 and 2012, respectively. Aedes triseriatus had an MDT in the first 4 d of being self-marked of 56.11 and 67.54 m in 2011 and 2012, respectively.

Table 1.

Number of gravid female Aedes albopictus (Skuse) and Ae. triseriatus (Say) that were captured in sticky ovitraps at a cemetery and on the University of Florida campus in Gainesville, FL

Measure Ae. albopictus Ae. triseriatus
Total captured 2,067 501
Self-marked/Captured in first 4 d 37 17
Self-marked/Captured in 20 d 155 52
MDT in first 4 d 2011a 22.50 56.11
MDT in first 4 d 2012a 31.33 67.54
MDT in 20 d 2011b 58.07 83.85
MDT in 20 d 2012b 77.90 93.18
ODTmax 2011c 149.00 148.00
ODTmax 2012c 149.00 148.00
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Mosquitoes were self-marked by visiting an attractive self-marking ovitrap before being captured in sticky ovitraps between June 5 through September 5, in both 2011 and 2012. All distances are measured in meters.

aMean distance traveled (MDT) in the first 4 d during each year per species was not significantly different.

bMean distance traveled (MDT) in a 20-d period is measured in meters and the distances traveled during each year for Ae. albopictus were significantly different (F1,8 = 6.95, P = 0.03), but were not different for Ae. triseriatus.

cMaximum observed distance traveled (ODTmax) is measured in meters.

Within 20 d of being self-marked, 155 gravid Ae. albopictus and 52 gravid Ae. triseriatus visited and were captured on a sticky ovitrap (Table 1). The MDT for Ae. albopictus females within 20 d of being self-marked was significantly (F1,8 = 6.95, P = 0.03) different between 2011 (58.07 m) and 2012 (77.90 m). Aedes triseriatus had an MDT within 20 d of being self-marked of 83.85 and 93.18 m in 2011 and 2012, respectively. The ODTmax for self-marked individuals of both species was recorded in the farthest sampling annuli of 120–150 m. This was similar among species and sites.

A significant relationship between the five trapping periods and distance traveled was observed in self-marked and sticky ovitrap captured Ae. albopictus (F4,172.4 = 29.01, P < 0.001) and Ae. triseriatus (F4,29.9 = 6.44, P < 0.001) (Fig. 3). For Ae. albopictus, mosquitoes dispersed from the ASMO significantly further from the first (28 m) to the third (92 m) trapping period; however, no differences were observed among the final three trapping periods, where mean distance captured was 92–95 m. During the first trapping period, Ae. triseriatus were captured a mean distance of 67 m from the ASMO. Only during the fourth and fifth trapping periods, when mosquitoes dispersed to 120 and 133 m, respectively, were mosquitoes captured at significantly greater distances.

Fig. 3.

Fig. 3.

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Mean (±SEM) distance of marked Aedes albopictus (Skuse) and Ae. triseriatus (Say) captured on five successive 4-d trapping periods during 2011 and 2012, in Gainesville, FL. Columns with differing uppercase or lowercase letters indicate significant differences between mean capture distances within a species (α = 0.05, Tukey’s HSD).

A positive relationship was observed between conspecific mosquito population size and the distance traveled by captured self-marked mosquitoes (Figs. 4 and 5). As presented in these figures, an increasing slope documented an increase in marked mosquito captures as the overall conspecific mosquito population increased. As populations of Ae. albopictus increased, the MDT during the 4-d post-marking period significantly increased (F1,10 = 50.57, P < 0.01) (Fig. 4). The association of these two variables also was significant (F1,6 = 27.56, P < 0.01) for Ae. triseriatus during the 4-d post-marking period (Fig. 4). During the 20-d post-marking period, the relationship between the conspecific population increase and the MDT of marked mosquitoes was observed as significant for Ae. albopictus (F1,10 = 31.75, P < 0.01) but not for Ae. triseriatus (Fig. 5).

Fig. 4.

Fig. 4.

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Linear regression of the mean distance traveled (MDT) of marked (A) Aedes albopictus (Skuse) and B) Ae. triseriatus (Say) captured over 4 d following marking in relation to the mean number of marked and unmarked conspecifics captured per sticky ovitrap (ST) in 2011 and 2012 in Gainesville, FL.

Fig. 5.

Fig. 5.

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Linear regression of the mean distance traveled (MDT) of marked (A) Aedes albopictus (Skuse) and (B) Ae. triseriatus (Say) captured over 20 d following a marking period in relation to the mean number of marked and unmarked conspecifics captured per sticky ovitrap (ST) in 2011 and 2012 in Gainesville, FL.

Discussion

The ASMO evaluated herein proved an effective tool to document Ae. albopictus skip oviposition in a field environment. Both Ae. albopictus and Ae. triseriatus were self-marked and captured within a 4-d period, therefore, providing field-based evidence that these two species visit more than one oviposition site within a single gonotrophic cycle.

The higher recapture rates of marked mosquitoes in the enclosure study are not surprising, given the essentially forced marking system used to dust mosquitoes, the inherent limited movement within the enclosure, and lack of alternative oviposition sites. However, Ae. albopictus has demonstrated a preference for high-quality larval habitat when performing skip oviposition in laboratory experiments (Davis et al. 2015).

In this study, marked Ae. albopictus dispersed greater distances from the ASMO as time progressed, but the population seemed to stabilize around 90 m from the initial marking site. Marked Ae. triseriatus were captured at distances twice as far during the early trapping periods and were captured about 25 m further than Ae. albopictus at the later trapping periods. Movement by these mosquitoes may be associated with ovisite, nectar meal, resting site, or bloodmeal-searching behaviors. The work of Honorio et al. (2003) documented that laboratory-reared and released gravid Ae. albopictus females distributed their eggs heterogeneously throughout an environment and traveled over 800 m in 6 d during oviposition. Marini et al. (2010), also using marked and released laboratory-reared, but blood-fed, Ae. albopictus, reported that in two of three trials, the MDT from the release location increased as days after release increased. Our studies provide the first evidence that wild populations of Ae. albopictus move through the environment during the deposition of an egg batch and establish an association that the distance traveled from a point source increases over time.

In addition to time-associated impacts on dispersal distance, population size also affected dispersal of gravid females. The number of gravid females collected per sticky trap is an indication of adult population size and a potential predictor of population dynamics. The positive association between population growth and increased dispersal may occur for several reasons. As populations increase, competition for limited resources also may increase, specifically in the larval habitat, and result in density-dependent larval mortality (Service 1985, Washburn 1995). Indirect and direct competition for access to larval nutritional resources has been shown to increase Ae. albopictus larval mortality, reduce adult size and female fecundity, and trigger adult behavioral responses (Chan 1971, Mori 1979, Blackmore and Lord 2000, Yoshioka et al. 2012). Mori (1979) reported that Ae. albopictus larvae reared under crowded conditions dispersed further than those reared in uncrowded conditions. Aedes albopictus were found to perform more skip oviposition when presented low-quality habitats that contained larvae in crowded conditions than when provided high-quality larval habitats (Davis et al. 2015). Therefore, during times when populations are high and competition for resources increases, ovipositing females may move greater distances seeking higher-quality immature habitats, as compared with the dispersal pattern when populations are low and habitats are more suitable. The limitations on the current study, where mosqutioes were marked at one site and captured on a sticky tape at the second site, do not allow for the direct assessment of skip oviposition. However, our evidence of multiple ovisite visitations within a single gonadatrophic cycle taken with results of Davis et al. (2015) and Fonseca et al. (2015) strongly suggest that Ae. albopictus are conducting skip oviposition.

The density- and habitat-dependent oviposition selection behavior identified in this study should be considered when planning vector surveillance, considering mosquito population management, and assessment of pathogen transmission risk. Similarly, in assessing St. Louis encephalitis (SLE) virus transmission by Culex nigripalpus Theobald in Florida, Day et al. (1990) reported that this mosquito changed its behavioral response to environmental factors that resulted in the subsequent facilitation of pathogen transmission. Day et al. (1990) found that parous Cx. nigripalpus were positively associated with time and that gravid females were negatively associated with daily rainfall, especially during years in which SLE was detected with increased frequency. A periodic cycling of larval habitat quality (high-quality habitat – low-quality habitat – high-quality habitat) was observed to lead to enhanced SLE viral amplification and transmission, and the modeling of these habitat qualities assisted in predicting SLE risk (Day and Curtis 1994).

The use of ovisites as container-inhabiting mosquito control devices has gained interest in the research community and our results support this concept. Devices have been developed to contaminate a skip ovipositing mosquito with an IGR such that the mosquito will transfer the chemical to other ovisites (Caputo et al. 2012, Gaugler et al. 2012). To maximize effectiveness, the placement of IGR-treated ovisites in the environment should take into account Ae. albopictus population densities. During times of high population densities, ovipositing Ae. albopictus will disperse over greater distances and treated ovisites could be placed further apart than when Ae. albopictus populations are at low densities. However, the exact placement distance of IGR-treated ovisites may depend on factors such as suitable resting sites, nectar source availability, and competing ovisites. Further studies that examine the effectiveness of IGR-treated ovisites, when used at different spatial placements in association with Ae. albopictus population densities, would improve the successful application of autodissemination control techniques.

Acknowledgments

We thank James Becnel, Joyce Urban, Neil Sanscrainte, John Sivinksi, Charlie Stuhl, Chris Holderman, Emma Weeks, and Lois Wood for their contributions to this research. We thank the staff of the Evergreen Cemetery who granted access to their property to conduct research. AJT acknowledges funding support from the RAPIDD program of the Science and Technology Directorate, Department of Homeland Security, and the Fogarty International Center, National Institutes of Health. The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Air Force, Department of Defense, or the U.S. Government.

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