Do pollinators prefer pesticide-free plants? An experimental test with monarchs and milkweeds.

Published online
08 Dec 2020
Content type
Journal article
Journal title
Journal of Applied Ecology

Olaya-Arenas, P. & Scharf, M. E. & Kaplan, I.
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Hundreds of recent studies have voiced concern over the negative impacts of non-target pesticides on pollinator health. However, pesticide loads are highly variable across agricultural landscapes and it is unclear whether pollinators exhibit behavioural responses (e.g. aversion) that mediate their exposure risk under realistic foraging environments. We tested whether monarch butterfly Danaus plexippus adults and larvae base their oviposition and foraging decisions, respectively, on the presence and concentration of pesticide residues on their milkweed host-plant, Asclepias syriaca. To do so, we experimentally simulated field-realistic exposure for six of the most commonly detected pesticides--one insecticide, two herbicides and three fungicides--either alone or in combination. These laboratory and greenhouse manipulations experimentally paired an untreated control with the pesticides at their mean or maximum concentrations. Last, we used a two-year field survey to correlate pesticide concentration on milkweed leaves with monarch oviposition. Butterflies placed fewer eggs on milkweeds treated with a cocktail containing all six pesticides at their maximum concentrations, resulting in c. 30% less oviposition compared to the solvent control. Neonate (1st instar) larvae also showed a preference for pesticide-free leaves in paired disc assays for four out of six compounds tested, with feeding aversion observed at both mean and maximum concentrations. Later instars did not show a comparable behavioural reaction to pesticide presence or concentration, but this could be partially due to the feeding-deterrent properties of the acetone solvent used. In the field, per plant egg load was negatively correlated with increasing leaf concentration for one of the herbicides, metolachlor; although all pesticides tested showed similar oviposition trends. Synthesis and applications. Our data provide evidence that monarchs are capable of adaptively adjusting their oviposition and foraging behaviours based on which pesticides are present on their host-plants. Importantly, this preference was observed at field-relevant concentrations, suggesting that monarchs behaviourally regulate pesticide exposure risk for their offspring by avoiding contaminated plants. Variability in pesticide identity and/or load among milkweeds within/between habitat patches should be considered in future restoration efforts aimed at attracting butterflies for larval development, as well as the relative importance of pesticides compared with other plant factors (e.g. genotype or species, developmental stage) known to affect oviposition. More broadly, this work illustrates some of the limitations of no-choice trials and suggests that experimental designs embracing field-scale heterogeneity in pesticide presence and concentration will lead to more realistic non-target impact assessments and improved management.

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