Flapping Tail Membrane in Bats Produces Potentially Important Thrust during Horizontal Takeoffs and Very Slow Flight

Historically, studies concerning bat flight have focused primarily on the wings. By analyzing high-speed video taken on 48 individuals of five species of vespertilionid bats, we show that the capacity to flap the tail-membrane (uropatagium) in order to generate thrust and lift during takeoffs and minimal-speed flight (<1 m s−1) was largely underestimated. Indeed, bats flapped the tail-membrane by extensive dorso-ventral fanning motions covering as much as 135 degrees of arc consistent with thrust generation by air displacement. The degree of dorsal extension of the tail-membrane, and thus the potential amount of thrust generated during platform launches, was significantly correlated with body mass (P = 0.02). Adduction of the hind limbs during upstrokes collapsed the tail-membrane thereby reducing its surface area and minimizing negative lift forces. Abduction of the hind limbs during the downstroke fully expanded the tail-membrane as it was swept ventrally. The flapping kinematics of the tail-membrane is thus consistent with expectations for an airfoil. Timing offsets between the wings and tail-membrane during downstrokes was as much as 50%, suggesting that the tail-membrane was providing thrust and perhaps lift when the wings were retracting through the upstoke phase of the wing-beat cycle. The extent to which the tail-membrane was used during takeoffs differed significantly among four vespertilionid species (P = 0.01) and aligned with predictions derived from bat ecomorphology. The extensive fanning motion of the tail membrane by vespertilionid bats has not been reported for other flying vertebrates

Post hoc Tukey-Kramer Multiple-Comparison Test showed significant differences (DF = 35, Critical Value = 3.814, Alpha = 0.05) among vespertilionid species in degree of tail-membrane sweep during takeoff from a horizontal platform.

<p>Post hoc Tukey-Kramer Multiple-Comparison Test showed significant differences (DF = 35, Critical Value = 3.814, Alpha = 0.05) among vespertilionid species in degree of tail-membrane sweep during takeoff from a horizontal platform.</p

Orchestrating a tail-membrane flap.

<p><b>A</b>) 1–2. Fringed myotis (<i>Myotis thysanodes</i>) illustrating adduction of its rear limbs to collapse the tail-membrane during the upstroke. 3–4. Abduction of the hind-limbs at the top of the upstroke occurs in preparation for the tail-membrane downstroke, thereby maximizing surface area and air displacement leading to rearward thrust. 5. Collapsing of the tail-membrane at the bottom of the downstroke in preparation for the next upstroke. B) Sequence drawings illustrating motion and timing between wings and tail-membrane motions during initial phase of a platform takeoff by Townsend's big-eared bat (<i>Corynorhinus townsendii</i>).</p

Change in oscillation offsets relative to body mass A.

<p>Histogram showing extent of oscillation offsets between the left wing and tail tip during the upstroke (blue bars) and downstroke (red bars) for the little brown myotis (<i>M. lucifugus</i>), plotted against individuals that varied in body mass. <b>B.</b> Regression plot of the offset data shows the switch-over point of regression lines where downstroke offsets (red line) become more pronounced than upstroke offsets (blue line) in relation to body mass. Although neither regression line is statistically significant due to high variation in the sample, the consistent trend towards greater offsets occuring during downstrokes as body mass increases suggests meaningful shifting of kinematics with mass.</p

Stroke initiation offsets.

<p>Stroke offsets between the left wing and tail-membrane are illustrated by plotting the digitized motions of the left wrist (blue line) and tip of the tail (red line) for the little brown myotis (<i>Myotis lucifugus</i>) through three wingbeat cycles. In this example, the individual used intitiation offsets of the upstroke and downstroke timings in order to produce asynchronous flapping between the wings and the tail-membrane. Black lines indicate degree of divergence in timing of downstroke motions (oscillation offsets).</p

Illustration of hypothetical model of how thrust and lift may be generated.

<p>Using the tail-membrane fanning motions (black arrow indicates direction of travel) of a long-eared myotis (<i>Myotis evotis</i>), we illustrate a hypothetical duel-use of the tail-wing wherein dorsal extension and downstoke above the body plane delivers thrust, whereas ventral flexion generates thrust and also lift when held in a curved position below the body axis. This positioning would be analogous to an airplane extending its flaps to increase air-speed above a flight surface.</p

Comparative takeoff dynamics.

<p>Using comparable still images between species (upper, long-eared myotis, <i>Myotis evotis</i>; lower, short-tailed fruit bat, <i>Carollia perspicillata</i>) we show how the long-eared myotis used extensive dorsal extension of tail-membrane to initiate rearward thrust production, whereas the short-tailed fruit bat did not.</p

Tail-membrane extension relative to body mass.

<p>Model two regression analysis showed a significantly positive relationship between (LogN) dorsal extension of the tail-membrane above the body plane and (LogN) mass (g) of individual little brown myotis (<i>M. lucifugus</i>), indicating that degree of dorsal extension of the tail-membrane is mechanically adjusted relative to mass to be lifted.</p

Stroke tempo offsets.

<p>Stroke tempo offsets between left wing and tail-membrane as illustrated by plots of the digitized motions of the wrist (blue line) and tail tip (red line) for the fringed myotis (<i>Myotis thysanodes</i>) across wingbeat cycles one through five. In this example, the individual showed little to no stroke intiation offsets, but instead used differential flap rates between the wings and tail-membrane to afford asynchrony of motion. The angles of the red and the blue arrows indicate oscillation offsets via stroke tempo.</p

Angle of attack of the tail-membrane during fanning motion.

<p>Graphic illustrating how the tail-membrane produces foreward thrust during a platform takeoff. The tip of the tail moves along a sinusoidal path through each stroke cycle represented by the curved black-line. Blue lines indicate the position of the tail-membrane relative to the sinusoidal path. The upstroke of the folded tail-membrane would likely be aerodynamically passive, whereas the downstroke provides a thrust force realtive to pitch angle and angle of attack. Numbers indicate tail-membrane position from top to bottom for a single downstroke. T = Thrust, L = Lift, D = Drag. Inset diagram illustrates how angle of attack and pitch angle were calculated for each tail-membrane position during the downstroke. A path tangent was drawn for each point position of the tail tip. α is the angle of attack of the tail-membrane relative to path (here illustrated for position 4 of the downstroke).</p