Indirect transfer of pyriproxyfen to European honeybees via an autodissemination approach

The frequency of arboviral disease epidemics is increasing and vector control remains the primary mechanism to limit arboviral transmission. Container inhabiting mosquitoes such as Aedes albopictus and Aedes aegypti are the primary vectors of dengue, chikungunya, and Zika viruses. Current vector control methods for these species are often ineffective, suggesting the need for novel control approaches. A proposed novel approach is autodissemination of insect growth regulators (IGRs). The advantage of autodissemination approaches is small amounts of active ingredients compared to traditional insecticide applications are used to impact mosquito populations. While the direct targeting of cryptic locations via autodissemination seems like a significant advantage over large scale applications of insecticides, this approach could actually affect nontarget organisms by delivering these highly potent long lasting growth inhibitors such as pyriproxyfen (PPF) to the exact locations that other beneficial insects visit, such as a nectar source. Here we tested the hypothesis that PPF treated male Ae. albopictus will contaminate nectar sources, which results in the indirect transfer of PPF to European honey bees (Apis mellifera). We performed bioassays, fluorescent imaging, and mass spectrometry on insect and artificial nectar source materials to examine for intra- and interspecific transfer of PPF. Data suggests there is direct transfer of PPF from Ae. albopictus PPF treated males and indirect transfer of PPF to A. mellifera from artificial nectar sources. In addition, we show a reduction in fecundity in Ae. albopictus and Drosophila melanogaster when exposed to sublethal doses of PPF. The observed transfer of PPF to A. mellifera suggests the need for further investigation of autodissemination approaches in a more field like setting to examine for risks to insect pollinators.
Author summary Autodissemination approaches have attracted a significant amount of attention for mosquito control because of the advantages of self-delivery of small amounts of highly potent insect growth regulators (IGRs) such as pyriproxyfen (PPF) to oviposition locations. However, while PPF may be delivered to oviposition locations by the mosquito vehicles, these treated mosquitoes may also be delivering PPF to nectar sources that other insects may visit, in particular important insect pollinators. Here we have examined for the direct transfer of PPF to nectar sources and the indirect transfer to the European honey bee. We show PPF is being deposited on artificial nectar sources and is being indirectly transferred to European honey bees. The results are discussed in reference to the potential risks to important insect pollinators of using autodissemination approaches for mosquito control.