The Butterflies of Costa Rica and Their Natural History

Bumblebees (Bombus) are charismatic and important pollinators. They are one of the best-studied insect groups, especially in terms of ecology, behavior, and social structure. As many species are declining, there is a clear need to understand more about them. Microbial symbionts, which can influence many dimensions of animal life, likely have an outsized role in bumblebee biology. Recent research has shown that a conserved set of beneficial gut bacterial symbionts is ubiquitous across bumblebees. These bacteria are related to gut symbionts of honeybees, but have not been studied as intensively. Here, we synthesize studies of bumblebee gut microbiota, highlight major knowledge gaps, and suggest future directions. Several patterns emerge, such as symbiont-host specificity maintained by sociality, frequent symbiont loss from individual bees, symbiont-conferred protection from trypanosomatid parasites, and divergence between bumblebee and honeybee microbiota in several key traits. For many facets of bumblebee–microbe interactions, however, underlying mechanisms and ecological functions remain unclear. Such information is important if we are to understand how bumblebees shape, and are shaped by, their gut microbiota. Bumblebees may prove a useful system for microbiome scientists, providing insights into general principles of host–microbe interactions. We also note how microbiota could influence bumblebee traits and responses to stressors. Finally, we propose that tinkering with the microbiota could be one way to aid bumblebee resilience in the face of global change.

The gut microbiota of bumblebees

Pollen stored by bees undergoes a fermentation marked by the presence of lactic acid bacteria and yeasts. It results in bee bread. Past studies have singled out Starmerella (Candida) magnoliae as the most common yeast species in honey bee-stored bee bread. Starmerella species are ecological specialists with potential biotechnological value. The rarity of recent studies on yeasts in honey bees prompted us to generate new information on yeast diversity during the conversion of bee-collected pollen to bee bread. Bees and stored pollen from two apiaries in Belgium were sampled, a yeast isolation protocol was developed, yeast isolates were grouped according to their macro- and micromorphology, and representative isolates were identified using DNA sequences. Most of the 252 identified isolates belonged to the genera Starmerella, Metschnikowia, and Zygosaccharomyces. The high abundance of yeasts in fresh bee bread decreased rapidly with the storage duration. Starmerella species dominated fresh bee bread, while mostly Zygosaccharomyces members were isolated from aged bee bread. Starmerella (Candida) apis, a rarely isolated species, was the most frequent and abundant species in fresh bee bread. Yeasts from the bee’s honey stomach and from pollen pellets obtained from bees hind legs were dominated by Metschnikowia species. The distinctive communities from pollen pellets over fresh bee bread to aged bee bread indicate a non-random distribution of these yeasts.

https://www.mdpi.com/2076-2607/8/11/1789/pdf

Specialisation of Yeast Genera in Different Phases of Bee Bread Maturation.

Microbial metabolism can shape cues important for animal attraction in service-resource mutualisms. Resources are frequently colonized by microbial communities, but experimental assessment of animal-microbial interactions often focus on microbial monocultures. Such an approach likely fails to predict effects of microbial assemblages, as microbe-microbe interactions may affect in a non-additive manner microbial metabolism and resulting chemosensory cues. Here, we compared effects of microbial mono- and cocultures on growth of constituent microbes, volatile metabolite production, sugar catabolism, and effects on pollinator foraging across two nectar environments that differed in sugar concentration. Growth in co-culture decreased the abundance of the yeast Metschnikowia reukaufii, but not the bacterium Asaia astilbes. Volatile emissions differed significantly between microbial treatments and with nectar concentration, while sugar concentration was relatively similar among mono- and cocultures. Coculture volatile emission closely resembled an additive combination of monoculture volatiles. Despite differences in microbial growth and chemosensory cues, honey bee feeding did not differ between microbial monocultures and assemblages. Taken together, our results suggest that in some cases, chemical and ecological effects of microbial assemblages are largely predictable from those of component species, but caution that more work is necessary to predict under what circumstances non-additive effects are important.

https://par.nsf.gov/servlets/purl/10162412

Microbial Co-Occurrence in Floral Nectar Affects Metabolites and Attractiveness to a Generalist Pollinator

About 90% of all flowering plant species are pollinated by animals. Animals are attracted to flowers because they often provide food in the form of nectar and pollen. While floral nectar is assumed to be initially sterile, it commonly becomes colonized by yeasts after animals have visited the flowers. Although yeast communities in floral nectar appear simple, community assembly depends on a complex interaction between multiple factors. Yeast colonization has a significant effect on the scent of floral nectar, foraging behavior of insects and nectar consumption. Consumption of nectar colonized by yeasts has been shown to improve bee fitness, but effects largely depended on yeast species. Altogether, these results indicate that dispersal, colonization history and nectar chemistry strongly interact and have pronounced effects on yeast metacommunities and, as a result, on bee foraging behavior and fitness. Future research directions to better understand the dynamics of plant–microbe–pollinator interactions are discussed.

Yeast-nectar interactions: metacommunities and effects on pollinators.

The presence of yeasts in pollen and floral nectar is rather the norm than the exception. Due to the metabolic activities of yeasts, sugar and amino acid composition of nectar often drastically change and may negatively impact the nutritional value of nectar for pollinators and hence insect fitness. On the other hand, the presence of yeasts in floral nectar may also increase its nutritional value due to yeast's probiotic effect and the release of yeast's metabolites. In this study, we investigated whether the presence of defined flower‐ and insect‐associated yeasts affected individual and colony fitness of the bumble bee pollinator Bombus terrestris. Specifically, we tested whether the presence of yeasts in nectar affected bumble bee foraging behavior and nectar consumption, individual growth and colony development, larval and queen mortality, and mating success. Quantitative analyses of sugar and amino acid profiles showed that nectar yeasts significantly affected the chemical composition of nectar. However, dual‐choice experiments indicated that yeast inoculation did not significantly affect foraging behavior or consumption rates. Nest development, on the other hand, was significantly affected by the presence of yeasts, but effects largely depended on species identity, with Candida bombiphila, Metschnikowia gruessii, and Rhodotorula mucilaginosa having the largest positive impact on colony growth. Interestingly, the effects at the colony level were more pronounced than at the individual level. In vitro growth tests further showed that yeasts have the potential to suppress the growth of the bumble bee gut pathogen Crithidia bombi. Overall, these results demonstrate that nectar‐inhabiting yeasts can have diverse effects on bumble bee fitness and therefore may mediate plant–pollinator mutualisms.

Tomás Aledón-Catalá

Papers

The impact of yeast presence in nectar on bumble bee behavior and fitness