Indirect transfer of pyriproxyfen to European honeybees via an autodissemination approach

Abstract

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.

Nectar Source and Pollinator Cross Contamination and Persistence of Pyriproxyfen Associated with the Use of Autodissemination Techniques for Mosquito Control

“…gambiae Giles, and An. arabiensis Patton when treated with nonlethal doses of PPF (Harris et al 2013, Koama et al 2015, Ahmed et al 2020, Rhyne and Richards 2020, Kancharlapalli et al 2021. PPF has also been demonstrated to impact hatching rates, pupation rates, capping rates, and adult emergence rates in A. mellifera (Chen et al 2016).…”

“…Here we built upon previous studies, which demonstrated indirect transfer of PPF to artificial nectar sources and A. mellifera L. in laboratory cages housing PPF treated Ae. albopictus males (Kancharlapalli et al 2021). Semifield cage studies were conducted to examine for the indirect transfer of PPF to nectar sources and V. cardui with the use of PPF dusted male Ae.…”

“…albopictus males and 30 painted lady butterflies were released into the semifield cages at the same time. Semifield cages also housed 2 oviposition containers (350 ml) (CSBD LLC, Charlotte, NC) filled with 200 ml of fermented water and lined with seed germination paper, 2 artificial nectar sources constructed as previously described (Kancharlapalli et al 2021), and 4 L. angustifolia flowering plants. Vanessa cardui adults, L. angustifolia flowers, the cotton wick and filter paper from the artificial nectar source, and water from oviposition cups were collected after 5 days and frozen at À208C.…”

“…Previously, we reported that releasing PPF dusted Ae. albopictus males into laboratory cages resulted in the indirect transfer of PPF to the European honeybee Apis mellifera (L.) and direct transfer to nectar sources (Kancharlapalli et al 2021). However, while these experiments were an essential first step in determining the routes of PPF transfer to an insect pollinator and nectar sources using autodissemination of IGRs, they were performed on a small scale in laboratory cages, making it difficult to control for space effects.…”

Evaluation of In2Care® mosquito stations for suppression of the Australian backyard mosquito,Aedes notoscriptus

“…The potential for mosquitoes to distribute pyriproxyfen to other parts of the ecosystem where it would influence other insect systems should be considered before widespread application of the technology is implemented, as some lab studies have shown pyriproxyfen transfer by male mosquitoes (artificially dosed with high quantities of pyriproxyfen) to bees during nectar feeding (Kancharlapalli et al 2021). In2Care ® Stations, however, specifically target gravid female Aedes mosquitoes that only disseminate pyriproxyfen to water bodies during egg-laying, and these will be less likely to visit flowers for sugar feeding at that stage.…”