Research ArticleAPPLIED ECOLOGY

Biomechanics of hover performance in Neotropical hummingbirds versus bats

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Science Advances  26 Sep 2018:
Vol. 4, no. 9, eaat2980
DOI: 10.1126/sciadv.aat2980
  • Fig. 1 Neotropical hummingbird and nectarivorous bat species converged on hovering while foraging from flowers.

    (A) A long-billed hermit (Phaethornis longirostris) hovers in front of a lobster claw (Heliconia), and a Geoffroy’s tailless bat (Anoura geoffroyi) sticks its head in a ring-gentian (Symbolanthus) to drink nectar and eat pollen (illustrations based on photos from C. Jiménez and N. Muchhala). (B) We studied hummingbird species (N = 17), nectarivorous bat species (N = 2), and frugivorous bat species (N = 1) living in the same habitat in Coto Brus, Costa Rica (species acronyms explained in table S1).

  • Fig. 2 Time-resolved vertical aerodynamic force measurements in freely flying hummingbirds and bats in vivo.

    (A) A rufous-tailed hummingbird (Amazilia tzacatl) hovers at an artificial feeder, while high-speed cameras record wing kinematics. A mirror below the feeder allows a third perspective of the hovering bird for more accurate 3D reconstruction. A perch (red) instrumented with custom capacitive force sensors measures takeoff and landing forces for accurate weight measurements between each flight. Carbon fiber force plates (blue) mechanically integrate the pressure field generated by the bird and allow us to resolve the instantaneous vertical aerodynamic force. (B) A nectar bat (Glossophaga soricina) hovers in the same aerodynamic force platform but does not drink from the artificial feeder. Full flight recordings from the hummingbird (C) and bat (D) show how body weight is supported by the perch before takeoff and by the aerodynamic force generated with the wings in flight. Hummingbirds landed back on the perch or feeder after each flight, while bats often landed inverted perching on small screw heads on the side walls, which results in zero measured force after the flight. By zooming in to a 0.35-s window, we can see the large downstroke humps and smaller upstroke humps in each wingbeat for hummingbirds (E) and nectar bats (F). Unfiltered forces are shown in light blue and green.

  • Fig. 3 Hummingbirds primarily rely on lift to support body weight, and bats increase wing angle of attack and stroke plane angle to include drag.

    (A) The hummingbird (blue; n = 88 individuals from 17 species) stroke is sinusoidal, while bats (red; n = 16 individuals from three species) have a longer downstroke period, followed by a faster upstroke (shaded areas are SD across individuals). (B) With a larger vertical elevation amplitude, bats produce an oval “O”-shaped wing tip trace, while hummingbirds generate a classic “U” trace with a double harmonic. (C) Hummingbirds twist their wings during both the downstroke and upstroke, while bat wings have less twist during the downstroke and much more twist during the upstroke. (D) Bats retract their wings during the upstroke, reducing their wingspan up to 35%. (E) Hummingbirds operate their wings at lower angles of attack than bats, at the wing radius of gyration r2 (25) where the center of pressure acts. (F) Radial angle-of-attack distribution from the base (0%) to the wing tip (100%) averaged over the high dynamic pressure phase of the stroke [thickened lines in (E); see Materials and Methods and fig. S6]. Bat wings operate at much higher angles of attack along their wingspan than hummingbirds (ill-defined near the root where chord velocity approaches zero; inverted wings have negative angles). (G) Wing stroke path (at r2) and chord angles of attack show that bats tilt the stroke plane and increase angle of attack to orient relatively more drag (orange) upward to support body weight (purple) in addition to lift (green), explaining the wingbeat-averaged vector magnitudes in the avatars (1) (lift and drag are shown as unit vectors on airfoil, and velocity vectors are shown as proportionally scaled black vectors; small gray cross, shoulder; cross width and height represents 10° wing sweep and elevation).

  • Fig. 4 Bats compensate aerodynamic inefficiency due to weight support asymmetry with low disk and wing loadings, which help minimize aerodynamic power.

    (A) Hummingbirds (blue) support more of their body weight during the upstroke compared to the inactive upstroke of bats (red). (B) Body weight is supported by accelerating air downward through the stroke plane, which requires induced power (1). The hummingbird’s ability to support body weight more uniformly over the upstroke and downstroke reduces induced power asymmetry, which makes them more efficient than bats (see the “Induced power calculation” section). (C) Regardless, hummingbirds and bats need similar induced power per unit body mass to hover. (D) Bats accomplish equivalent induced power by compensating for their higher temporal induced power cost factor with a lower (E) actuator disk loading (body weight per swept wing area). (F) Similarly, bats have a much lower wing loading due to their disproportionally larger wing lengths (fig. S5C; shaded areas and error bars are SD across individuals).

  • Fig. 5 Hummingbirds accommodate flower angle with their body angle and supple neck, keeping wingbeat frequency and vertical force distribution nearly consistent.

    (A) A green hermit (Phaethornis guy; top) and rufous-tailed hummingbird (A. tzacatl; bottom) hover at a feeder in three orientations: 45°, 0°, and 90°. Comparison of the average wingbeat frequency and normalized vertical force for two green hermits (B and C) and three rufous-tailed hummingbirds (D to F) reveals that these parameters are not substantially modulated by hummingbirds to accommodate a flower angle. Across all individuals, and relative to the angled (45°) feeder, the stroke plane angle only decreased by 1° ± 2° for the horizontal (0°) feeder and only increased by 2° ± 4° for the vertical (90°) feeder. Shaded areas and error bars represent SD across the hundreds of wingbeats recorded during three flights per individual for each feeder orientation.

  • Fig. 6 Nectarivorous bats generate more upstroke weight support than fruit bats during slow hovering flight by inverting their wing further.

    (A) All 17 hummingbird species converged on generating similarly elevated weight support during the upstroke. (B) The amplitude of upstroke weight support averaged over a 10% wingbeat interval (74 to 84% of the wingbeat cycle) confirms this (see table S1 for species names sorted by mass). (C) In contrast, nectar bats produce noticeably more vertical force during the upstroke than the fruit bat. (D) The vertical force amplitude is significantly different (78 to 88% of the wingbeat cycle). (E) This difference is explained by the radial angle-of-attack distribution for the upstroke (based on Fig. 3F), which shows pronounced differences in the angle of attack (<0%, inverted wing) of the wing tip (75 to 100% span). (F) At the wing tip, hummingbirds use angles around −15° to generate lift efficiently. Nectar bats (G. soricina, green; A. geoffroyi, orange) flick their wing tips back at around −35°, generating significant lift and drag, whereas fruit bats (Artibeus watsoni, purple) operate at −52°, generating more drag. Shaded areas and error bars represent SD across individuals. *P < 0.05, **P < 0.01 (light gray comparison bar; nonsignificant; see the “Statistical analysis” section).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/9/eaat2980/DC1

    Fig. S1. Bats hover at two times higher Reynolds numbers than hummingbirds.

    Fig. S2. Phylogenetic tree of the hummingbirds and bats in the study.

    Fig. S3. Beyond the radial angle-of-attack distribution, kinematic parameters do not vary much across bat species.

    Fig. S4. Hummingbirds generate substantially more vertical force during the upstroke than bats, and the nectar bats outperform the fruit bat.

    Fig. S5. Morphological and kinematic parameters of the sampled species.

    Fig. S6. Definition of the wing tip speed range associated with high lift production during the downstroke and upstroke.

    Fig. S7. Aerodynamic force platform verification.

    Table S1. Overview of wingbeats analyzed for force processing.

    Movie S1. Force measurements and wingbeat segmentation.

    Movie S2. Wing tracking and kinematic parameters.

  • Supplementary Materials

    The PDF file includes:

    • Fig. S1. Bats hover at two times higher Reynolds numbers than hummingbirds.
    • Fig. S2. Phylogenetic tree of the hummingbirds and bats in the study.
    • Fig. S3. Beyond the radial angle-of-attack distribution, kinematic parameters do not vary much across bat species.
    • Fig. S4. Hummingbirds generate substantially more vertical force during the upstroke than bats, and the nectar bats outperform the fruit bat.
    • Fig. S5. Morphological and kinematic parameters of the sampled species.
    • Fig. S6. Definition of the wing tip speed range associated with high lift production during the downstroke and upstroke.
    • Fig. S7. Aerodynamic force platform verification.
    • Table S1. Overview of wingbeats analyzed for force processing.
    • Legends for movies S1 and S2

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mp4 format). Force measurements and wingbeat segmentation.
    • Movie S2 (.mp4 format). Wing tracking and kinematic parameters.

    Files in this Data Supplement:

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