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Research Article

Nectar vs. pollen loading affects the tradeoff between flight stability and maneuverability in bumblebees

Andrew M. Mountcastle, Sridhar Ravi, and Stacey A. Combes
  1. aDepartment of Organismic and Evolutionary Biology, Harvard University, Concord Field Station, Bedford, MA 01730;
  2. bSchool of Aerospace Mechanical and Manufacturing Engineering, Royal Melbourne Institute of Technology, Bundoora 3083, VIC, Australia

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PNAS first published August 3, 2015; https://doi.org/10.1073/pnas.1506126112
Andrew M. Mountcastle
aDepartment of Organismic and Evolutionary Biology, Harvard University, Concord Field Station, Bedford, MA 01730;
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  • For correspondence: mountcastle@fas.harvard.edu
Sridhar Ravi
bSchool of Aerospace Mechanical and Manufacturing Engineering, Royal Melbourne Institute of Technology, Bundoora 3083, VIC, Australia
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Stacey A. Combes
aDepartment of Organismic and Evolutionary Biology, Harvard University, Concord Field Station, Bedford, MA 01730;
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  1. Edited by May R. Berenbaum, University of Illinois at Urbana-Champaign, Urbana, IL, and approved July 1, 2015 (received for review March 27, 2015)

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Significance

Many insects carry substantial loads during flight. Although this behavior is often critical for survival and reproduction, few studies have examined its consequences for flight performance. Bumblebees regularly carry two types of loads in different locations: pollen on their legs or nectar in their abdomen. We found that when bees carry a pollen load rather than a nectar load, they are more stable but less maneuverable in flight, supporting the concept of a tradeoff between stability and maneuverability—a notion that is frequently suggested but has rarely been tested, particularly in flying insects. Our findings also suggest that wind conditions may influence what resources pollinators choose to collect, which would have important consequences for pollination dynamics and colony fitness.

Abstract

Bumblebee foragers spend a significant portion of their lives transporting nectar and pollen, often carrying loads equivalent to more than half their body mass. Whereas nectar is stored in the abdomen near the bee’s center of mass, pollen is carried on the hind legs, farther from the center of mass. We examine how load position changes the rotational moment of inertia in bumblebees and whether this affects their flight maneuverability and/or stability. We applied simulated pollen or nectar loads of equal mass to Bombus impatiens bumblebees and examined flight performance in a wind tunnel under three conditions: flight in unsteady flow, tracking an oscillating flower in smooth flow, and flower tracking in unsteady flow. Using an inertial model, we estimated that carrying a load on the legs rather than in the abdomen increases a bee’s moment of inertia about the roll and yaw axes but not the pitch axis. Consistent with these predictions, we found that bees carrying a load on their legs displayed slower rotations about their roll and yaw axes, regardless of whether these rotations were driven by external perturbations or self-initiated steering maneuvers. This allowed pollen-loaded bees to maintain a more stable body orientation and higher median flight speed in unsteady flow but reduced their performance when tracking a moving flower, supporting the concept of a tradeoff between stability and maneuverability. These results demonstrate that the types of resources collected by bees affect their flight performance and energetics and suggest that wind conditions may influence resource selection.

  • insect
  • foraging
  • turbulence
  • energetics
  • biomechanics

Footnotes

  • ↵1A.M.M. and S.R. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: mountcastle{at}fas.harvard.edu.
  • Author contributions: A.M.M., S.R., and S.A.C. designed research; A.M.M. and S.R. performed research; A.M.M., S.R., and S.A.C. contributed new reagents/analytic tools; A.M.M. and S.R. analyzed data; and A.M.M., S.R., and S.A.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1506126112/-/DCSupplemental.

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Bumblebee flight with nectar vs. pollen load
Andrew M. Mountcastle, Sridhar Ravi, Stacey A. Combes
Proceedings of the National Academy of Sciences Aug 2015, 201506126; DOI: 10.1073/pnas.1506126112

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Bumblebee flight with nectar vs. pollen load
Andrew M. Mountcastle, Sridhar Ravi, Stacey A. Combes
Proceedings of the National Academy of Sciences Aug 2015, 201506126; DOI: 10.1073/pnas.1506126112
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