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

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.

A neonicotinoid pesticide alters how nectar chemistry affects bees

“…Furthermore, across taxa, bees can vary in their ability to cope with NSMs, perhaps as a result of evolutionary history with specific plant taxa (Tiedeken et al., 2016). As interest grows in understanding the benefits of nectar and pollen secondary chemistry in agroecosystems (Adler et al., 2021; Folly et al., 2021; Fowler et al., 2020) or use in promoting pollination service (Arnold et al., 2021), our results suggest an important caveat, which is that systemic pesticides may alter these dynamics.…”

“…Caffeine, for example, in the nectar of plants such as Citrus, Coffea and Onobrychis (sainfoin) increases bee activity (e.g. Figure 2c), reduces parasite load (Folly et al., 2021) and promotes pollen transfer (Thomson et al., 2015). The addition of IMD, which B. impatiens workers do not show any preference for on its own (Muth et al., 2020), and which limits activity (Figure 2c,d), would likely result in lowered visitation rate with potential negative impacts on plant fitness.…”

Understanding effects of floral products on bee parasites: Mechanisms, synergism, and ecological complexity

“…Given the high degree of variability in antiparasitic effects found even among congeneric host species ( Fowler et al, 2022 ), there is a clear need to expand the scope of research to include a wider diversity of bee species. This need is particularly urgent in light of evidence that disease burden is associated with population declines, at least in bumble bees ( Averill et al, 2021 ; Cameron et al, 2011 ), and interest in using flowering species with demonstrated antiparasitic effects to reduce disease burden in wild bees ( Folly et al, 2021 ). To evaluate the utility of such approaches, we need to know how floral products influence disease in a wide range of bee species, and particularly those of conservation concern.…”

“…Inhibitory effects of the same or related compounds also differ between target microorganisms. While caffeine is not biologically active against C. bombi ( Richardson et al, 2015 ), it inhibits a microsporidian parasite of bumble bees, Nosema bombi ( Folly et al, 2021 ), and the closely related N. ceranae, which infects honey bees ( Bernklau et al, 2019 ). Furthermore, variation in response to a compound across genotypes within a species provides an additional nuance to understanding bioactivity.…”

“…Moreover, the question of whether bees self-medicate has important implications for pollinator conservation efforts. Several recent studies documenting antiparasitic effects of pollen or nectar of specific plant species advocate for increased planting of these species as a strategy for managing disease and promoting bee populations ( Folly et al, 2021 ; Giacomini et al, 2018 ). Setting aside broader questions regarding the utility of this approach ( Fowler et al, 2022 ; Palmer-Young et al, 2017a ), its impact will depend heavily on whether bees self-medicate.…”