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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 August 18, 2015 112 (33) 10527-10532; 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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  • Fig. 1.
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    Fig. 1.

    Load treatments and their predicted effects on body moment of inertia, maneuverability, and stability. (A) Load treatments consisted of either attaching a pair of small steel ball bearings to the dorsal surface of the anterior-most plate of the abdomen, simulating a nectar load (blue) or attaching a single ball bearing to the corbicula (“pollen basket”) on the outer face of each hind tibia, simulating a pollen load (red). Yellow stars indicate the approximate location of the COM, around which the body rotates, based on results of the inertial model illustrated in Fig. S1. (B) Estimated change in moment of inertia (I) around the three rotational axes when a load is carried on the legs vs. on the abdomen. Values are derived from an inertial model of a bumblebee body subject to each load treatment (see Table S1 for MOI values). (C) Predicted consequences of the changes in MOI with leg loading (compared with abdominal loading) on flight stability (Upper) and maneuverability (Lower).

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    Fig. S1.

    Still frames from high-speed videos of a bumblebee subjected to the abdominal load treatment (A) and the leg load treatment (B).

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    Fig. S2.

    Model of a bumblebee body used to estimate moments of inertia, consisting of separate ellipsoids representing the head, thorax, abdomen, and two hind legs. Dimensions and masses for each body segment were taken from measurements of dissected bumblebees. (A) Unloaded body, with no additional weights attached. (B) Abdominal (simulated nectar) load treatment, with two blue spheres representing ball bearings as they were positioned on bees in our experiments (i.e., attached to the anterior plate of the abdomen). In the model, the ball bearings are not in direct contact with the abdominal segment because of limitations on the model’s abdominal angle imposed by the parallel axis theorem, as described in Materials and Methods. (C) Leg (simulated pollen) load treatment, with two red spheres representing ball bearings attached to the corbiculae on the hind legs. Estimated MOI values for each treatment are reported in Table S1.

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    Fig. 2.

    Representative paired flight trials under each load treatment (abdominal load in blue, leg load in red), for the three flight conditions. (A) Unsteady vortex street flow with a stationary flower (VORT). (B) Laminar airflow with a laterally oscillating flower (FLR). (C) Unsteady vortex street flow with a laterally oscillating flower (VORT/FLR). For each flight condition, we show the 3D trajectories (top row), lateral position of the bee relative to the flower (indicated by a black dashed line) through time (middle row), and a subsection of body roll rate through time (bottom row).

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    Fig. 3.

    Body rotation rates for each load treatment (abdominal load in blue, leg load in red) in the VORT condition (A), FLR condition (B), and VORT/FLR condition (C). Box and whisker plots show the median, quartiles, and range of data points, with outliers plotted as plus signs. Asterisks indicate a significant difference at P < 0.05. In all flight conditions, bees with leg loads displayed lower average (absolute) roll and yaw rates than they did with abdominal loads. (A) For the VORT condition, rotation rates were filtered to exclude frequencies below 5 Hz, to isolate the high-frequency body dynamics associated with unsteady flow perturbations. (B) For the FLR condition, rotation rates were filtered to exclude motions above 5 Hz, to isolate the low-frequency, voluntary casting motions associated with flower tracking. (C) For the VORT/FLR condition, the entire 0- to 50-Hz frequency range was analyzed.

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    Fig. 4.

    Flower tracking performance for each load treatment (abdominal load in blue, leg load in red) in the FLR condition (top row, A–C) and the VORT/FLR condition (bottom row, D–F). (A and D) Polar plots depicting the correlation between lateral position of the bee and the flower (displayed along the radial axis) and the bee’s phase lag in tracking flower oscillations (displayed along the angular axis). (B, C, E, and F) Box and whisker plots showing the median, quartiles, and range of data points, with outliers plotted as plus signs. Asterisks indicate a significant difference at P < 0.05. Bees with loaded legs in the FLR condition had a significantly lower correlation and a significantly higher phase lag than bees with loaded abdomens (A), exhibited significantly higher flight path sinuosity (B), and flew with a significantly lower median velocity (C). In the VORT/FLR condition, there was no significant difference in correlation, phase lag (D), path sinuosity (E), or median flight velocity (F) between bees with loaded legs vs. loaded abdomens.

Tables

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    Table S1.

    Estimated moments of inertia about the three axes of rotation for a model bumblebee body

    Load treatmentBody moment of inertia, I (kg m2)
    RollYawPitch
    No load8.49 × e−103.57 × e−94.54 × e−9
    Abdominal/nectar9.44 × e−103.64 × e−94.79 × e−9
    Leg/pollen1.15 × e−94.29 × e−94.72 × e−9
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    Table S2.

    P values from paired t tests to assess differences in body rotation rates between load treatments under the three flight conditions

    Embedded Image
    • We applied three different frequency filters to the rotation rates: 0–5 Hz to isolate low-frequency, voluntary casting motions associated with flower tracking; 5–50 Hz to isolate higher-frequency body dynamics associated with flow perturbations; and 0–50 Hz to assess combined effects on both low- and high-frequency body dynamics. In our analysis, we focused on the results highlighted in gray, because these were the most relevant frequency ranges for each flight treatment. Values in bold indicate significance at the 0.05 level; where a significant difference was found, bees always displayed higher rotation rates with the abdominal load.

Data supplements

  • Supporting Information

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    • Download Movie_S01 (AVI) - Representative bumblebee flight trial for the VORT condition (abdominal load treatment).
    • Download Movie_S02 (AVI) - Representative bumblebee flight trial for the FLR condition (abdominal load treatment).
    • Download Movie_S03 (AVI) - Representative bumblebee flight trial for the VORT/FLR condition (abdominal load treatment).
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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, 112 (33) 10527-10532; 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, 112 (33) 10527-10532; DOI: 10.1073/pnas.1506126112
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