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Research Article

Way-finding in displaced clock-shifted bees proves bees use a cognitive map

James F. Cheeseman, Craig D. Millar, Uwe Greggers, Konstantin Lehmann, Matthew D. M. Pawley, Charles R. Gallistel, Guy R. Warman, and Randolf Menzel
  1. aDepartment of Anaesthesiology, School of Medicine, and
  2. bSchool of Biological Sciences, University of Auckland, Auckland, 1142, New Zealand;
  3. cAllan Wilson Centre for Molecular Ecology and Evolution, Palmerston North, PN4442, New Zealand;
  4. dInstitute of Biology–Neurobiology, Free University of Berlin, 14195 Berlin, Germany;
  5. eInstitute of Natural and Mathematical Sciences, Massey University, Auckland, 0745, New Zealand; and
  6. fDepartment of Psychology and Center for Cognitive Science, Rutgers University, Piscataway, NJ 08854-8020

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PNAS June 17, 2014 111 (24) 8949-8954; first published June 2, 2014; https://doi.org/10.1073/pnas.1408039111
James F. Cheeseman
aDepartment of Anaesthesiology, School of Medicine, and
bSchool of Biological Sciences, University of Auckland, Auckland, 1142, New Zealand;
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  • For correspondence: j.cheeseman@auckland.ac.nz galliste@ruccs.rutgers.edu
Craig D. Millar
bSchool of Biological Sciences, University of Auckland, Auckland, 1142, New Zealand;
cAllan Wilson Centre for Molecular Ecology and Evolution, Palmerston North, PN4442, New Zealand;
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Uwe Greggers
dInstitute of Biology–Neurobiology, Free University of Berlin, 14195 Berlin, Germany;
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Konstantin Lehmann
dInstitute of Biology–Neurobiology, Free University of Berlin, 14195 Berlin, Germany;
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Matthew D. M. Pawley
aDepartment of Anaesthesiology, School of Medicine, and
eInstitute of Natural and Mathematical Sciences, Massey University, Auckland, 0745, New Zealand; and
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Charles R. Gallistel
fDepartment of Psychology and Center for Cognitive Science, Rutgers University, Piscataway, NJ 08854-8020
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  • For correspondence: j.cheeseman@auckland.ac.nz galliste@ruccs.rutgers.edu
Guy R. Warman
aDepartment of Anaesthesiology, School of Medicine, and
bSchool of Biological Sciences, University of Auckland, Auckland, 1142, New Zealand;
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Randolf Menzel
dInstitute of Biology–Neurobiology, Free University of Berlin, 14195 Berlin, Germany;
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  1. Contributed by Charles R. Gallistel, May 1, 2014 (sent for review January 22, 2014)

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    Fig. 1.

    The average-vector hypothesis. Bee is captured at the feeder F bound for the hive H on vector FH and released at a release site R. It flies the vector FH from R, discovers its error at D, recognizes the landmarks L1 and L2, and flies the average of the associated home vectors, which is the vector (L1H + L2H)/2.

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    Fig. 2.

    Layout of the experimental site. A large flat open field bordered by a row of bushes, a road and a river. Perpendicular to the bushes ran two irrigation channels. Representative bee flights shown. (A) In Exp. 1 bees were trained from hive H1 to the feeder F1 along the yellow dotted line. (B) In Exp. 2 bees were trained from hive H2 to feeder F2 along the white dotted line. The release site in Exp. 1 was R1. In Exp. 2 two release sites were used, R2 and R3. The radar (black triangle at the origin) was positioned ∼60 m from the row of bushes stretching along a small road and a river. H1 is located at the upper part of the western irrigation channel. H2 is located on the edge of the bushes to the south. The blue lines in the figures show representative flight paths from control bees, the red lines from clock-shifted bees.

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    Fig. 3.

    Initial vector flight components (vector flights) of bees in Exps. 1 and 2. Clock-shifted bees shown in red and control bees shown in blue. (A) Exp. 1: clock-shifted mean vector angle 24°, (95% CI 7°,41°); control mean vector angle 322°, (95% CI 319°, 325°). (B) Exp. 2: clock-shifted mean angle 276°, (95% CI 244°, 308°); control mean vector angle 271°, (95% CI 240°, 301°). Scale in meters.

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    Fig. 4.

    Kernel density (kde) plots overlaid on a Google map showing the homing behavior of animals from the point of release in Exps. 1 and 2. (A) Exp. 1 control bees (n = 13); (B) Exp. 1 clock-shifted bees (n = 24); (C) Exp. 2 control bees (n = 8); (D) Exp. 2 clock-shifted bees (n = 12). The color maps indicate the probability of a bee being at a particular coordinate with blue indicating low and red indicating higher probability of occurrence. The white dashed lines indicate the expected sun-compass orientation angle under each experimental condition. Scale in meters from the radar.

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    Table 1.

    Postvector flight data of the bees in Exps. 1 and 2

    ExperimentGroupNo. of animals returning home/totalMean time ± SEM (s)Mean distance ± SEM (m)*
    Experiment 1Clock shifted19/24154 ± 301,687 ± 287
    Control11/13140 ± 241,452 ± 108
    Experiment 2Clock shifted10/12173 ± 64948 ± 172
    Control7/895 ± 31772 ± 119
    • ↵* A significant difference between the total distance traveled in Exps. 1 and 2, P = 0.0007.

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The bee reads its map
James F. Cheeseman, Craig D. Millar, Uwe Greggers, Konstantin Lehmann, Matthew D. M. Pawley, Charles R. Gallistel, Guy R. Warman, Randolf Menzel
Proceedings of the National Academy of Sciences Jun 2014, 111 (24) 8949-8954; DOI: 10.1073/pnas.1408039111

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The bee reads its map
James F. Cheeseman, Craig D. Millar, Uwe Greggers, Konstantin Lehmann, Matthew D. M. Pawley, Charles R. Gallistel, Guy R. Warman, Randolf Menzel
Proceedings of the National Academy of Sciences Jun 2014, 111 (24) 8949-8954; DOI: 10.1073/pnas.1408039111
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    - Oct 02, 2014
Proceedings of the National Academy of Sciences: 111 (24)
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