Pollen extracts and constituent sugars increase growth of a trypanosomatid parasite of bumble bees

Abstract

Phytochemicals produced by plants, including at flowers, function in protection against plant diseases, and have a long history of use against trypanosomatid infection. Floral nectar and pollen, the sole food sources for many species of insect pollinators, contain phytochemicals that have been shown to reduce trypanosomatid infection in bumble and honey bees when fed as isolated compounds. Nectar and pollen, however, consist of phytochemical mixtures, which can have greater antimicrobial activity than do single compounds. This study tested the hypothesis that pollen extracts would inhibit parasite growth. Extracts of six different pollens were tested for direct inhibitory activity against cell cultures of the bumble bee trypanosomatid gut parasite Crithidia bombi. Surprisingly, pollen extracts increased parasite growth rather than inhibiting it. Pollen extracts contained high concentrations of sugars, mainly the monosaccharides glucose and fructose. Experimental manipulations of growth media showed that supplemental monosaccharides (glucose and fructose) increased maximum cell density, while a common floral phytochemical (caffeic acid) with inhibitory activity against other trypanosomatids had only weak inhibitory effects on Crithidia bombi. These results indicate that, although pollen is essential for bees and other pollinators, pollen may promote growth of intestinal parasites that are uninhibited by pollen phytochemicals and, as a result, can benefit from the nutrients that pollen provides.

Sunflower pollen reduces a gut pathogen in worker and queen but not male bumble bees

“…The mechanism underlying the medicinal effect of sunflower pollen is currently unknown. Chemical extracts from sunflower pollen reduced the growth of bacteria and fungi (Fatrcová‐Šramková et al ., 2016) but increased Crithidia growth in vitro (Palmer‐Young & Thursfield, 2017) and did not reduce Crithidia to the level of pure sunflower pollen in bee assays (Adler et al ., 2020). A compound in heather nectar ( Calluna vulgaris ) reduced Crithidia infection by removing the flagellum and preventing attachment to the gut wall (Koch et al ., 2019); the spiky pollen coat of sunflower could mechanically inhibit attachment via similar mechanisms.…”

From plant fungi to bee parasites: mycorrhizae and soil nutrients shape floral chemistry and bee pathogens

“…Fine scale shifts in the diverse sugars, secondary compounds, and other nutrients in nectar (Bentley and Elias 1983) may alter bee-pathogen interactions, and it is thus important to study bee-disease dynamics in the context of real nectar. Sugar concentration and composition can influence Crithidia growth (Conroy et al 2016, Palmer-Young andThursfield 2017) directly or possibly synergistically with secondary metabolites in nectar . Few studies have examined the effects of secondary compounds in real nectar on bee pathogens (Tiedeken et al 2016).…”

Crithidia bombican infect two solitary bee species while host survivorship depends on diet

“…Specifically, increased access to food could increase infections by (1) directly providing nutrients to the pathogen; or (2) improving host quality for the pathogen. Conversely, food availability could suppress pathogens by (3) enabling physiologically costly immune responses; and/or (4) providing antimicrobial compounds (Conroy et al ., 2016; Palmer-Young and Thursfield, 2017). While we did not find that pollen access directly influenced the likelihood or severity of C. bombi infections (Figs 1 and 3), others have found that pollen-deprivation in bumble bees can reduce C. bombi infections (Logan et al ., 2005; Conroy et al ., 2016).…”

“…Bumble bees infected with C. bombi (Richardson et al ., 2015) and honey bees infected with N. ceranae (Mayack and Naug, 2009) often consume more pollen, likely to compensate for the energetic cost of mounting an immune response (Moret and Schmid-Hempel, 2000). Interestingly, the role of pollen on C. bombi growth varies depending on whether the assessments are conducted in vitro or in vivo ; for example, sunflower pollen in vitro increases pathogen growth (Palmer-Young and Thursfield, 2017), while in vivo this pollen type has a strong inhibitory effect on the pathogen when consumed by bumble bees (Giacomini et al ., 2018; LoCascio et al ., 2019). When inhibitory, secondary compounds appear to facilitate these anti- C. bombi interactions in bumble bees (Richardson et al ., 2015; Koch et al ., 2017).…”

“…The relationship between nutrition and bee disease dynamics is complex, as diet quality and diversity can support immunocompetence and reduce infections in some instances, while increasing disease burdens in other cases (Koch et al ., 2017; Dolezal and Toth, 2018). A bee's diet is made up of nectar and pollen, both of which have primary metabolites such as sugars, amino acids and lipids, as well as secondary compounds, such as flavonoids, terpenoids and alkaloids, with the potential to decrease (Richardson et al ., 2015) or increase (Palmer-Young and Thursfield, 2017) infections. In a world dominated by agricultural landscapes, with low floral diversity and frequent movement of commercial bee colonies that can potentially introduce pathogens into wild solitary bee populations (Kremen et al ., 2002; Otterstatter and Thomson, 2008; Furst et al ., 2014; Alger et al ., 2019), understanding the interplay between nutrition and pathogen burdens is important for protecting pollinator health.…”