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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.

SUBMITTER: Palmer-Young EC

PROVIDER: S-EPMC5426351 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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

Palmer-Young Evan C EC Thursfield Lucy L

PeerJ 20170509

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 activit ...[more]

PMID: 28503378

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Project description:Recent declines in bumble bee populations are of great concern and have prompted critical evaluations of the role of pathogen introductions and host resistance in bee health. One factor that may influence host resilience when facing infection is the gut microbiota. Previous experiments with Bombus terrestris, a European bumble bee, showed that the gut microbiota can protect against Crithidia bombi, a widespread trypanosomatid parasite of bumble bees. However, the particular characteristics of the microbiome responsible for this protective effect have thus far eluded identification. Using wild and commercially sourced Bombus impatiens, an important North American pollinator, we conducted cross-wise microbiota transplants to naive hosts of both backgrounds and challenged them with a Crithidia parasite. As with B. terrestris, we find that microbiota-dependent protection against Crithidia operates in B. impatiens Lower Crithidia infection loads were experimentally associated with high microbiome diversity, large gut bacterial populations, and the presence of Apibacter, Lactobacillus Firm-5, and Gilliamella spp. in the gut community. These results indicate that even subtle differences between gut community structures can have a significant impact on a microbiome's ability to defend against parasite infections.IMPORTANCE Many wild bumble bee populations are under threat due to human activity, including through the introduction of pathogens via commercially raised bees. Recently, it was found that the bumble bee gut microbiota can help defend against a common parasite, Crithidia bombi, but the particular factors contributing to this protection are unknown. Using both wild and commercially raised bees, we conducted microbiota transplants to show that microbiome diversity, total gut bacterial load, and the presence of certain core members of the microbiota may all impact bee susceptibility to Crithidia infection. Bee origin (genetic background) was also a factor. Finally, by examining this phenomenon in a previously uninvestigated bee species, our study demonstrates that microbiome-mediated resistance to Crithidia is conserved across multiple bumble bee species. These findings highlight how intricate interactions between hosts, microbiomes, and parasites can have wide-ranging consequences for the health of ecologically important species.

Project description:Habitat fragmentation can have severe effects on plant pollinator interactions, for example changing the foraging behaviour of pollinators. To date, the impact of plant population size on pollen collection by pollinators has not yet been investigated. From 2008 to 2010, we monitored nine bumble bee species (Bombus campestris, Bombus hortorum s.l., Bombus hypnorum, Bombus lapidarius, Bombus pascuorum, Bombus pratorum, Bombus soroensis, Bombus terrestris s.l., Bombus vestalis s.l.) on Vaccinium uliginosum (Ericaceae) in up to nine populations in Belgium ranging in size from 80 m(2) to over 3.1 ha. Bumble bee abundance declined with decreasing plant population size, and especially the proportion of individuals of large bumble bee species diminished in smaller populations. The most remarkable and novel observation was that bumble bees seemed to switch foraging behaviour according to population size: while they collected both pollen and nectar in large populations, they largely neglected pollen collection in small populations. This pattern was due to large bumble bee species, which seem thus to be more likely to suffer from pollen shortages in smaller habitat fragments. Comparing pollen loads of bumble bees we found that fidelity to V. uliginosum pollen did not depend on plant population size but rather on the extent shrub cover and/or openness of the site. Bumble bees collected pollen only from three plant species (V.uliginosum, Sorbus aucuparia and Cytisus scoparius). We also did not discover any pollination limitation of V. uliginosum in small populations. We conclude that habitat fragmentation might not immediately threaten the pollination of V. uliginosum, nevertheless, it provides important nectar and pollen resources for bumble bees and declining populations of this plant could have negative effects for its pollinators. The finding that large bumble bee species abandon pollen collection when plant populations become small is of interest when considering plant and bumble bee conservation.

Dataset Information

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

Publications

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

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