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. 2015 Jan 15;9(1):e0003406.
doi: 10.1371/journal.pntd.0003406. eCollection 2015 Jan.

Male mosquitoes as vehicles for insecticide

Affiliations

Male mosquitoes as vehicles for insecticide

James W Mains et al. PLoS Negl Trop Dis. .

Abstract

Background: The auto-dissemination approach has been shown effective at treating cryptic refugia that remain unaffected by existing mosquito control methods. This approach relies on adult mosquito behavior to spread larvicide to breeding sites at levels that are lethal to immature mosquitoes. Prior studies demonstrate that 'dissemination stations,' deployed in mosquito-infested areas, can contaminate adult mosquitoes, which subsequently deliver the larvicide to breeding sites. In some situations, however, preventative measures are needed, e.g., to mitigate seasonal population increases. Here we examine a novel approach that combines elements of autocidal and auto-dissemination strategies by releasing artificially reared, male mosquitoes that are contaminated with an insecticide.

Methodology: Laboratory and field experiments examine for model-predicted impacts of pyriproxyfen (PPF) directly applied to adult male Aedes albopictus, including (1) the ability of PPF-treated males to cross-contaminate females and to (2) deliver PPF to breeding sites.

Principal findings: Similar survivorship was observed in comparisons of PPF-treated and untreated males. Males contaminated both female adults and oviposition containers in field cage tests, at levels that eliminated immature survivorship. Field trials demonstrate an ability of PPF-treated males to transmit lethal doses to introduced oviposition containers, both in the presence and absence of indigenous females. A decline in the Ae. albopictus population was observed following the introduction of PPF-treated males, which was not observed in two untreated field sites.

Conclusions/significance: The results demonstrate that, in cage and open field trials, adult male Ae. albopictus can tolerate PPF and contaminate, either directly or indirectly, adult females and immature breeding sites. The results support additional development of the proposed approach, in which male mosquitoes act as vehicles for insecticide delivery, including exploration of the approach with additional medically important mosquito species. The novelty and importance of this approach is an ability to safely achieve auto-dissemination at levels of intensity that may not be possible with an auto-dissemination approach that is based on indigenous females. Specifically, artificially-reared males can be released and sustained at any density required, so that the potential for impact is limited only by the practical logistics of mosquito rearing and release, rather than natural population densities and the self-limiting impact of an intervention upon them.

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Conflict of interest statement

I have read the journal’s policy and the authors of this manuscript have the following competing interests: JWM, CLB and SLD are paid employees of MosquitoMate, a for-profit company. This does not alter our adherence to all PLOS policies on sharing data and materials.

Figures

Figure 1
Figure 1. Diagram comparing the auto-dissemination station-based approach with the ADAM approach.
In (A), an auto-dissemination station is attractive to indigenous female mosquitoes (grey), which enter and become contaminated with a persistent juvenile hormone analogue (PPF) that does not harm the adult. The PPF-contaminated females (black) exit the trap and transfer the PPF to immature mosquito breeding sites. In (B and C), the ADAM approach is based on manufacturing adult male mosquitoes that are dusted with PPF (black), which are released into a treatment area. The PPF-treated males can then (B) directly transfer PPF to immature mosquito breeding sites and (C) indirectly transfer PPF by cross-contaminating indigenous females, which subsequently transfer the PPF to breeding sites.
Figure 2
Figure 2. Survivorship of male Ae. albopictus treated with Pyriproxyfen/Dayglo dust compared to untreated males.
Figure 3
Figure 3. An example of an ovisite removed from a field cage trial.
Arrows point to pyriproxyfen dust on the sides of the cup and to two dead adult Ae. albopictus floating in the water.
Figure 4
Figure 4. Adults removed from field cages were examined for insecticidal activity using immature bioassays.
Letters above the bars indicate significant differences (p < 0.01, Wilcoxon). The number of replicates is shown above each column. Bars show standard errors.
Figure 5
Figure 5. Oviposition cups removed from field cages were separate into three different components (i.e. cup, paper lining, and water), and each was examined for insecticidal activity using immature bioassays.
For each component, screened (S) and unscreened (U) cups are compared, along with the negative (N) and positive (P) controls. Letters above the bars indicate significant differences (p < 0.01). The number of replicates is shown above each column. Bars show standard errors.
Figure 6
Figure 6. Field sites for male introduction experiments in Lexington, Kentucky.
(A) Field Experiment 1 Site consisted of a single point introduction site (red circle), six BG trap sites (blue circle) and nine ovisites (yellow circles). (B) Field Experiment 2 Site consisted of a single point introduction site and six ovisites. Images are from http://datagateway.nrcs.usda.gov/GDGHome.aspx. Bars = 60ft.
Figure 7
Figure 7. Results of Field Trial 1.
(A) Ae. albopictus adults are monitored using BG traps at three sites. Grey bars indicate introductions of PPF-dusted males at Site 3 only. Beginning after Week 13, a consistent population decline is observed at Site 3, which is not observed at the untreated sites. Lines show a three-week moving average for the adult collections. (B) Bioassays of artificial oviposition sites show increased larval mortality up to 150m from the Site 3 release point. In contrast, low mortality is observed in bioassays of ovisites within untreated areas.
Figure 8
Figure 8. In the absence of an indigenous Ae. albopictus population, i.e., Field Trial 2, increased immature mortality is observed following the introduction of PPF-treated males.
During the pre-release period, good larval survival is observed in bioassays of water sampled from ovisites at both the Untreated and Treated sites. Following male introductions, reduced survival is observed at the Treated site only. Significant differences are indicated above the columns (Wilcoxon). Bars show standard deviation.
Figure 9
Figure 9. Immature survivorship in bioassays is correlated with distance from the introduction point in Field Trial 2, but only during the PPF-male introduction period.
A bivariate fit of Survival versus distance is significant, but only during the two weeks of male introductions.

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