Upper-limit agricultural dietary exposure to streptomycin in the laboratory reduces learning and foraging in bumblebees

Abstract

In the past decade, the broadcast-spray application of antibiotics in US crops has increased exponentially in response to bacterial crop pathogens, but little is known about the sublethal impacts on beneficial organisms in agroecosystems. This is concerning given the key roles that microbes play in modulating insect fitness. A growing body of evidence suggests that insect gut microbiomes may play a role in learning and behaviour, which are key for the survival of pollinators and for their pollination efficacy, and which in turn could be disrupted by dietary antibiotic exposure. In the laboratory, we tested the effects of an upper-limit dietary exposure to streptomycin (200 ppm)—an antibiotic widely used to treat bacterial pathogens in crops—on bumblebee ( Bombus impatiens ) associative learning, foraging and stimulus avoidance behaviour. We used two operant conditioning assays: a free movement proboscis extension reflex protocol focused on short-term memory formation, and an automated radio-frequency identification tracking system focused on foraging. We show that upper-limit dietary streptomycin exposure slowed training, decreased foraging choice accuracy, increased avoidance behaviour and was associated with reduced foraging on sucrose-rewarding artificial flowers flowers. This work underscores the need to further study the impacts of antibiotic use on beneficial insects in agricultural systems.

Effects of a field-sprayed antibiotic on bee foraging behavior and pollination in pear orchards

“…Given the need for conspecific pollen transfer for the pollination of pear trees (Webster, 2002), we hypothesized that a decline in floral visitation would lead to reduced pollination and lower fruit production. In terms of bumble bee foraging outcomes in the lab, we hypothesized that antibiotic exposure would negatively impact foraging, in parallel with our hypothesis for honey bees (Avila et al, 2022;Ortiz-Alvarado et al, 2020). We thus predicted that antibiotic-fed bumble bees would move and forage less compared to the biological and control treatment.…”

“…Bacterial disease management is key to pome fruit production, yet it carries unknown consequences for beneficial insects and pollination services. While there are few laboratory studies on the impact of bactericide treatments on pollinators, all indicate that antibiotics could impact bee foraging (Avila et al, 2022; Ortiz-Alvarado et al, 2020). Our field-based results are consistent with these laboratory studies.…”

“…Studies examining these antibiotics on bees can be grouped into two categories: (1) exposure levels equal or below the maximum allowed concentrations (≤ 200 ppm), and (2) above (>200 ppm). Exposure levels in the first group (≤ 200 ppm) are not lethal to bumble bees (Marceau et al, 2021; Meeus et al, 2013), but can deplete bumble bee symbionts (Meeus et al, 2013), decrease flower visits per forager, and reduce sucrose consumption in an artificial foraging arena (Avila et al, 2022). Exposures at higher doses can decrease bumble bee (Marceau et al, 2021) and honey bee survival (Raymann et al, 2017), irreversibly deplete the honey bee symbionts (Raymann et al, 2018, 2017), impact honey bees’ ability to fight pathogens (Li et al, 2017), negatively affect honey bee olfactory learning (Zhang et al, 2020) and delay the onset of honey bee foraging (Ortiz-Alvarado et al, 2020).…”