Research ArticleBIRDS

How birds direct impulse to minimize the energetic cost of foraging flight

See allHide authors and affiliations

Science Advances  17 May 2017:
Vol. 3, no. 5, e1603041
DOI: 10.1126/sciadv.1603041
  • Fig. 1 A new aerodynamic force platform accurately measures the complete transfer of vertical impulse generated during foraging flights.

    (A) Two plates, each connected to three force sensors (black discs), integrate the pressure field along the top and bottom surfaces of the “control volume” in which the bird flies. Instrumented perches measure leg forces during takeoff (red) and landing (blue). Five kinematic high-speed cameras are synchronized with force measurements at 1000 Hz. Mirrors on the bottom plate provide a ventral view of the projected area swept out by the wings (see Materials and Methods). (B) To test how distance and inclination (γ) between perches modify bimodal locomotion, five variations were used: 20-cm (dark green), 40-cm (green), and 75-cm (light green) level (γ = 0°) versus 75-cm ascending (γ = +20°; light blue) and descending (γ = −20°; purple) flights. (C) A typical 75-cm, level flight force recording shows parrotlets support bodyweight primarily with their legs (red and blue) and wing downstrokes (black line and gray shaded regions). (D) Legs are the dominant weight support contributors. Bars show mean ± SD for N = 4 birds and n = 5 flights each, except that 20- and 40-cm wing contributions are n = 10 (see Materials and Methods). The platform and perches recover ~100% of vertical impulse needed to support bodyweight.

  • Fig. 2 Parrotlets primarily support bodyweight during downstrokes, but as they pitch up before landing, upstroke contributions increase.

    Parrotlets frequently fold their wings to bound mid–75-cm flights, which contributes little to weight support. Solid lines indicate the vertical forces on the takeoff perch (red), force plates (black), and landing perch (blue) (see legends in Fig. 1C). (A) Parrotlets primarily long jump up to 20 cm, beyond which they flap their wings to support their bodyweight. (B and C) Level long jump and flight over 40 and 75 cm. (D and E) During the 75-cm ascending and descending flights, parrotlets adjust the force they exert on the takeoff versus landing perch. Frames (from movies S1 to S5) showing the bird at the start of each downstroke are overlaid in corresponding photos. An additional frame showing the bird bounding is included in (C) to (E). All frames shown were recorded by the camera indicated in Fig. 1A, so the perspective may give the impression of nonlevel flight in (A) to (C). Colored circles encode flight variations for Figs. 3 and 4.

  • Fig. 3 As inclination increases from −20° to 20°, parrotlets increase takeoff impulse and decrease landing impulse.

    Across all inclinations, upstroke contributions increase with body angle. During takeoff (A) and landing (B), the legs exert vertical (solid line) and horizontal forces (dashed line) on the perch to accelerate and decelerate. Takeoff angle increases with inclination, whereas landing angle decreases. In contrast, takeoff speed remains relatively constant across 40- and 75-cm flights (inset; table S1). (C) Net impulse is the integrated vertical leg force [(A) and (B)] minus bodyweight. Impulse transfer shifts from landing to takeoff for ascending flight, and vice versa for descending. (D) During the first wingbeats after toe-off (see Materials and Methods for wingbeat selection criteria), bodyweight is primarily supported by downstroke impulse (dashed boundaries, end of downstroke). (E) Just before touchdown, the upstroke contribution to bodyweight support increases. Bird avatars show how body angle and actuator disc area increase from takeoff to landing wingbeats. (F) The upstroke to downstroke vertical impulse ratio increases with body angle, regardless of flight inclination. (A to C) Panels show mean results for each flight variation with N = 4, n = 5. (D to F) Panels show mean results for 75-cm variations with N = 4, n = 3. SDs are shown by shaded regions in (A), (B), (D), and (E) and by error bars in (C) and (F).

  • Fig. 4 Foraging parrotlets select takeoff angles that minimize the mechanical energy needed to extend long jumps with flapping wings.

    The long jumps of parrotlets and their antecedents are greatly extended by (proto)wingbeats. (A) The mechanical energy required to long jump and fly between perches depends on takeoff angle, distance, and inclination. Circles mark actual average takeoff angles used, and bolded regions denote SDs, showing that parrotlets preferred close to optimal long jumps. (B) Even one proto-wingbeat, with modest aerodynamic weight support during the downstroke and an inactive upstroke, extends the long jump range of all birds and their antecedents substantially [bird antecedent masses; (35)]. The increase in energetic cost required is offset by foraging gain. More powerful wingbeats require a smaller body mass, consistent with evolutionary trends in bird antecedents (37). Simulated proto-wingbeats were limited to those that would require a muscle mass–specific power within what parrotlets require for a downstroke with full weight support (see Materials and Methods for details). The vertical dashed line indicates 30% bodyweight support, which smaller bird antecedents were likely capable of generating with their protowings (35). The open circle (mean) and bolded region (±SD) on the parrotlet curve show the predicted increase in the long jump range based on the measured exerted impulse during 20-cm flights (N = 4, n = 5; except for two flights, where the bird did not flap its wings).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/5/e1603041/DC1

    fig. S1. Key components of the AFP.

    fig. S2. Inconsistent weight support during 20-cm jumping flights.

    fig. S3. Horizontal takeoff and landing impulses.

    fig. S4. Body angle correlations and changes during flight.

    fig. S5. Effect of proto-wingbeat timing on distance and power required for a long jump.

    fig. S6. Linear approximation for the long-jump range versus wingbeat impulse.

    fig. S7. Representative force traces of individuals during 75-cm flights.

    fig. S8. Velocity components during flight.

    fig. S9. Key parameters used in modeling bird foraging flights.

    fig. S10. Mechanical energy model results assuming zero elastic storage.

    table S1. Takeoff and landing velocity data from Fig. 3 (A and B).

    table S2. Mechanical energy model input parameter values and predictions for foraging flight.

    table S3. Time rate of change of the tau function (Formula.

    table S4. Bird antecedent parameters from Dececchi et al. (35) used in the protowing model.

    movie S1. In vivo weight support recording of a Pacific parrotlet during level, 20-cm flight.

    movie S2. In vivo weight support recording of a Pacific parrotlet during level, 40-cm flight.

    movie S3. In vivo weight support recording of a Pacific parrotlet during level, 75-cm flight.

    movie S4. In vivo weight support recording of a Pacific parrotlet during ascending (+20°), 75-cm flight.

    movie S5. In vivo weight support recording of a Pacific parrotlet during descending (−20°), 75-cm flight.

  • Supplementary Materials

    This PDF file includes:

    • fig. S1. Key components of the AFP.
    • fig. S2. Inconsistent weight support during 20-cm jumping flights.
    • fig. S3. Horizontal takeoff and landing impulses.
    • fig. S4. Body angle correlations and changes during flight.
    • fig. S5. Effect of proto-wingbeat timing on distance and power required for a long jump.
    • fig. S6. Linear approximation for the long-jump range versus wingbeat impulse.
    • fig. S7. Representative force traces of individuals during 75-cm flights.
    • fig. S8. Velocity components during flight.
    • fig. S9. Key parameters used in modeling bird foraging flights.
    • fig. S10. Mechanical energy model results assuming zero elastic storage.
    • table S1. Takeoff and landing velocity data from Fig. 3 (A and B).
      table S2. Mechanical energy model input parameter values and predictions for foraging flight.
    • table S3. Time rate of change of the tau function ( τ ).
    • table S4. Bird antecedent parameters from Dececchi et al. (35) used in the protowing model.

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • movie S1 (.mp4 format). In vivo weight support recording of a Pacific parrotlet during level, 20-cm flight.
    • movie S2 (.avi format). In vivo weight support recording of a Pacific parrotlet during level, 40-cm flight.
    • movie S3 (.mp4 format). In vivo weight support recording of a Pacific parrotlet during level, 75-cm flight.
    • movie S4 (.mp4 format). In vivo weight support recording of a Pacific parrotlet during ascending (+20°), 75-cm flight.
    • movie S5 (.mp4 format). In vivo weight support recording of a Pacific parrotlet during descending (−20°), 75-cm flight.

    Files in this Data Supplement: