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Hungry for quality—individual bumblebees forage flexibly to collect high-quality pollen

Abstract

Nutritional deficits may be one factor contributing to the ongoing decline of wild and managed bees. As a consequence, interest in understanding the effect of floral resource availability on nutritional intake - and subsequently bee health and performance - has increased. However, the proximate mechanisms underlying bee foraging choices are still poorly understood. We do, for instance, not yet know whether and how bees assess the nutritional quality of pollen or whether they use information on pollen quality to adjust foraging patterns. In a previous study, we showed that Bombus terrestris workers use their sense of taste to discriminate pollen differing in concentration and, thus, nutrient content. We now investigated whether they translate this ability into foraging behavior by observing microcolonies offered the choice between two feeders containing different pollen types and concentrations and, thus, qualities. We examined whether bumblebees used direct (chemotactile) or indirect (olfactory) cues to assess pollen quality and whether they individually assessed pollen quality or relied on larval feedback. By changing pollen quality after 21 days, we further tested whether information on pollen quality was subsequently associated with other (faster assessable) cues (e.g., odor) or continuously re-assessed. We found that bees always preferred pollen of higher quality and individually assessed quality based on chemotactile cues. Moreover, changing pollen quality resulted in rapid equivalent changes in foraging behavior, even without feedback from larvae. Consequently, individual bumblebee foragers continuously re-assess pollen quality to provide their colonies with high-quality food.

Significance statement

The ongoing decline of wild and managed bees is likely driven by several factors with nutritional deficits being one of them. Because bees are amongst the most important pollinators, interest in understanding the effect of floral resource availability on nutritional intake and, subsequently, bee health and performance has increased. However, the proximate mechanisms underlying bee foraging choices are still poorly understood. In this study, we investigated how bumblebees differentiate between different pollen qualities by observing microcolonies offered the choice between different diets. We found that bees always preferred pollen of higher quality and individually assessed quality based on chemotactile cues. This finding increases our understanding of how social bees assess nutritional quality and make appropriate foraging choices.

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Acknowledgments

We thank Alexander Keller for the DNA meta-barcoding analysis of the honeybee-collected pollen and two anonymous reviewers for their insightful comments which greatly helped to improve our manuscript. Funding for SDL and FAR was provided by the Deutsche Forschungsgemeinschaft (DFG projects: LE 2750/1-1 and LE 2750/5-1), and SDL was further supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Würzburg (Postdoc Plus).

Authors’ contributions

The study was conceived by SDL and JS and performed by FAR. FAR, SDL, and JS wrote the manuscript.

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Correspondence to Sara D. Leonhardt.

Additional information

Communicated by W. Hughes

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Figure S1

Palynological composition of honeybee-collected pollen. Given is the relative abundance of pollen of different plant genera/families in the mixture. Pollen was analyzed using DNA meta-barcoding following the protocol established and described by Keller et al. (2015) and Sickel et al. (2015). (DOC 268 kb)

Figure S2

Daily food collection [μg/individual] of two different pollen types by 6 Bombus terrestris microcolonies, being offered a choice between (A) pure apple or almond pollen (black) and apple or almond pollen diluted with cellulose at a ratio of 1:10 (grey) and (B) pure apple pollen (black) or pure almond pollen (grey). Each dot represents one data point (i.e. the amount of food collected [μg] per individual per day for each colony). Generalized additive mixed effect models were used to fit smoothers to the data showing mean trends [±95% confidence intervals, dashed lines] over time. (DOC 138 kb)

Figure S3

Daily food collection [μg/individual] of two different pollen types by 6 Bombus terrestris microcolonies, being offered a choice between (A) high quality (i.e. pure bee-collected) pollen (black) and low quality (i.e. bee-collected pollen diluted with cellulose at a ratio of 1:10) pollen (grey) and (B) the same treatment but with egg clumps taken out each day. Each dot represents one data point (i.e. the amount of food collected [μg] per individual per day for each colony). Generalized additive mixed effect models were used to fit smoothers to the data showing mean trends [±95% confidence intervals, dashed lines] over time. (DOC 130 kb)

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Ruedenauer, F.A., Spaethe, J. & Leonhardt, S.D. Hungry for quality—individual bumblebees forage flexibly to collect high-quality pollen. Behav Ecol Sociobiol 70, 1209–1217 (2016). https://doi.org/10.1007/s00265-016-2129-8

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Keywords

  • Bee decline
  • Nutrients
  • Nutrition
  • Optimal foraging
  • Pollen
  • Protein