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Research Article

Bumblebees perceive the spatial layout of their environment in relation to their body size and form to minimize inflight collisions

View ORCID ProfileSridhar Ravi, Tim Siesenop, View ORCID ProfileOlivier Bertrand, View ORCID ProfileLiang Li, Charlotte Doussot, View ORCID ProfileWilliam H. Warren, View ORCID ProfileStacey A. Combes, and View ORCID ProfileMartin Egelhaaf
  1. aDepartment of Neurobiology and Cognitive Interaction Technology Center of Excellence, Bielefeld University, 33615 Bielefeld, Germany;
  2. bSchool of Engineering and Information Technology, University of New South Wales, Canberra 2914, ACT, Australia;
  3. cDepartment of Collective Behavior, Max Planck Institute of Animal Behavior, 78464 Konstanz, Germany;
  4. dCentre for the Advanced Study of Collective Behaviour, University of Konstanz, 78464 Konstanz, Germany;
  5. eDepartment of Biology, University of Konstanz, 78464 Konstanz, Germany;
  6. fDepartment of Cognitive, Linguistic & Psychological Sciences, Brown University, Providence, RI 02912;
  7. gDepartment of Neurobiology, Physiology and Behavior, University of California, Davis, CA 95616

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PNAS December 8, 2020 117 (49) 31494-31499; first published November 23, 2020; https://doi.org/10.1073/pnas.2016872117
Sridhar Ravi
aDepartment of Neurobiology and Cognitive Interaction Technology Center of Excellence, Bielefeld University, 33615 Bielefeld, Germany;
bSchool of Engineering and Information Technology, University of New South Wales, Canberra 2914, ACT, Australia;
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  • ORCID record for Sridhar Ravi
  • For correspondence: sridhar.ravi@adfa.edu.au
Tim Siesenop
aDepartment of Neurobiology and Cognitive Interaction Technology Center of Excellence, Bielefeld University, 33615 Bielefeld, Germany;
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Olivier Bertrand
aDepartment of Neurobiology and Cognitive Interaction Technology Center of Excellence, Bielefeld University, 33615 Bielefeld, Germany;
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  • ORCID record for Olivier Bertrand
Liang Li
cDepartment of Collective Behavior, Max Planck Institute of Animal Behavior, 78464 Konstanz, Germany;
dCentre for the Advanced Study of Collective Behaviour, University of Konstanz, 78464 Konstanz, Germany;
eDepartment of Biology, University of Konstanz, 78464 Konstanz, Germany;
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Charlotte Doussot
aDepartment of Neurobiology and Cognitive Interaction Technology Center of Excellence, Bielefeld University, 33615 Bielefeld, Germany;
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William H. Warren
fDepartment of Cognitive, Linguistic & Psychological Sciences, Brown University, Providence, RI 02912;
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  • ORCID record for William H. Warren
Stacey A. Combes
gDepartment of Neurobiology, Physiology and Behavior, University of California, Davis, CA 95616
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  • ORCID record for Stacey A. Combes
Martin Egelhaaf
aDepartment of Neurobiology and Cognitive Interaction Technology Center of Excellence, Bielefeld University, 33615 Bielefeld, Germany;
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  • ORCID record for Martin Egelhaaf
  1. Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved October 16, 2020 (received for review August 12, 2020)

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Significance

Like many other animals, including humans, insects frequently move through densely cluttered environments to perform activities critical for their survival, such as foraging. Vertebrates avoid collisions by perceiving their surroundings in relation to their body size and form, but it is unknown whether insects, with much smaller brains, possess such skills. We discovered that flying bumblebees judge the gap between obstacles relative to their wingspan and reorient themselves to fly sideways through tight spaces. Our findings suggest that bees too evaluate the affordance of their surroundings and account for their own size and form to safely navigate through complex environments. This facet of insect flight poses questions about the neural requisites for perception of self-size in animals.

Abstract

Animals that move through complex habitats must frequently contend with obstacles in their path. Humans and other highly cognitive vertebrates avoid collisions by perceiving the relationship between the layout of their surroundings and the properties of their own body profile and action capacity. It is unknown whether insects, which have much smaller brains, possess such abilities. We used bumblebees, which vary widely in body size and regularly forage in dense vegetation, to investigate whether flying insects consider their own size when interacting with their surroundings. Bumblebees trained to fly in a tunnel were sporadically presented with an obstructing wall containing a gap that varied in width. Bees successfully flew through narrow gaps, even those that were much smaller than their wingspans, by first performing lateral scanning (side-to-side flights) to visually assess the aperture. Bees then reoriented their in-flight posture (i.e., yaw or heading angle) while passing through, minimizing their projected frontal width and mitigating collisions; in extreme cases, bees flew entirely sideways through the gap. Both the time that bees spent scanning during their approach and the extent to which they reoriented themselves to pass through the gap were determined not by the absolute size of the gap, but by the size of the gap relative to each bee’s own wingspan. Our findings suggest that, similar to humans and other vertebrates, flying bumblebees perceive the affordance of their surroundings relative their body size and form to navigate safely through complex environments.

  • affordances
  • insect flight
  • self-size perception
  • navigation
  • cluttered environments

Footnotes

  • ↵1To whom correspondence may be addressed. Email: sridhar.ravi{at}adfa.edu.au.
  • Author contributions: S.R., T.S., and M.E. designed research; S.R., T.S., O.B., and C.D. performed research; S.R., L.L., W.H.W., S.A.C., and M.E. analyzed data; and S.R., O.B., L.L., C.D., W.H.W., S.A.C., and M.E. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2016872117/-/DCSupplemental.

Data Availability.

All data are included in the manuscript and supporting information.

Published under the PNAS license.

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Bumblebees perceive the spatial layout of their environment in relation to their body size and form to minimize inflight collisions
Sridhar Ravi, Tim Siesenop, Olivier Bertrand, Liang Li, Charlotte Doussot, William H. Warren, Stacey A. Combes, Martin Egelhaaf
Proceedings of the National Academy of Sciences Dec 2020, 117 (49) 31494-31499; DOI: 10.1073/pnas.2016872117

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Bumblebees perceive the spatial layout of their environment in relation to their body size and form to minimize inflight collisions
Sridhar Ravi, Tim Siesenop, Olivier Bertrand, Liang Li, Charlotte Doussot, William H. Warren, Stacey A. Combes, Martin Egelhaaf
Proceedings of the National Academy of Sciences Dec 2020, 117 (49) 31494-31499; DOI: 10.1073/pnas.2016872117
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