Agri-environment scheme nectar chemistry can suppress the social epidemiology of parasites in an important pollinator.

Arran J Folly,Hauke Koch,Mark J F Brown,Philip C Stevenson,Iain W Farrell

doi:10.1098/rspb.2021.0363

Abstract

Emergent infectious diseases are one of the main drivers of species loss. Emergent infection with the microsporidian Nosema bombi has been implicated in the population and range declines of a suite of North American bumblebees, a group of important pollinators. Previous work has shown that phytochemicals found in pollen and nectar can negatively impact parasites in individuals, but how this relates to social epidemiology and by extension whether plants can be effectively used as pollinator disease management strategies remains unexplored. Here, we undertook a comprehensive screen of UK agri-environment scheme (AES) plants, a programme designed to benefit pollinators and wider biodiversity in agricultural settings, for phytochemicals in pollen and nectar using liquid chromatography and mass spectrometry. Caffeine, which occurs across a range of plant families, was identified in the nectar of sainfoin (Onobrychis viciifolia), a component of UK AES and a major global crop. We showed that caffeine significantly reduces N. bombi infection intensity, both prophylactically and therapeutically, in individual bumblebees (Bombus terrestris), and, for the first time, that such effects impact social epidemiology, with colonies reared from wild-caught queens having both lower prevalence and intensity of infection. Furthermore, infection prevalence was lower in foraging bumblebees from caffeine-treated colonies, suggesting a likely reduction in population-level transmission. Combined, these results show that N. bombi is less likely to be transmitted intracolonially when bumblebees consume naturally available caffeine, and that this may in turn reduce environmental prevalence. Consequently, our results demonstrate that floral phytochemicals at ecologically relevant concentrations can impact pollinator disease epidemiology and that planting strategies that increase floral abundance to support biodiversity could be co-opted as disease management tools.

Highlights

Two prominent drivers of biodiversity loss are emerging infectious diseases (EID) [1,2,3,4,5,6,7] and the reduction of natural habitat [8,9,10,11,12,13], often as a direct consequence of intensive agriculture [14,15,16]
We identified the alkaloid caffeine in the nectar of sainfoin (Onobrychis viciifolia) using a retention time (Rt) of 6.11 min and a mass-to-charge ratio (m/z) of 195.09, which has known biological activity [56,57]
We show that caffeine, which may be encountered by bumblebees in agri-environment schemes (AES) landscapes, can negatively impact both the individual and social epidemiology of a key bumblebee pathogen, N. bombi

Summary

Introduction

Two prominent drivers of biodiversity loss are emerging infectious diseases (EID) [1,2,3,4,5,6,7] and the reduction of natural habitat [8,9,10,11,12,13], often as a direct consequence of intensive agriculture [14,15,16]. Given that animals consume naturally occurring, bioactive compounds in their diets [48,49,50], inspiration for novel medications to combat endemic and emergent parasitic infections may be drawn from an animal’s pre-existing diet [51,52,53], as has been shown to be the case for individual bumblebees [34,35,36] Such studies have yet to address the social epidemiology of pollinator parasites, which is key to their success in highly social insects [54]. Our results show that caffeine did reduce infection intensity and prevalence in individual bumblebees and that this impact was reflected in our colony-level experiments

Results

Discussion

Findings

Methodology