How small deviations in kinematics and body form dictate muscle performances in the finely tuned avian downstroke
- 1. Stanford University
- 2. California State University Los Angeles
- 3. University of Montana
- 4. University of Groningen
Description
Avian takeoff requires peak pectoralis muscle power to generate sufficient aerodynamic force during the downstroke. Subsequently the much smaller supracoracoideus recovers the wing during the upstroke. How the pectoralis work loop is tuned to power flight is unclear. We integrate wingbeat-resolved muscle, kinematic and aerodynamic recordings in vivo with a new mathematical model to disentangle how the pectoralis muscle overcomes wing inertia and generates aerodynamic force during takeoff in doves. Doves reduce the incidence of their wing mid-downstroke to efficiently generate aerodynamic force, resulting in an aerodynamic power dip, that allows transferring excess pectoralis power into tensioning the supracoracoideus tendon to assist the upstroke—improving the pectoralis work loop efficiency simultaneously. Integrating extant bird data, our model shows how the pectoralis of birds with faster wingtip speed need to generate proportionally more power. Finally, birds with disproportionally larger wing inertia need to activate the pectoralis earlier to tune their downstroke.
Notes
Methods
The experimental setup consisted of three time-synchronized systems which imaged the 3D surface of the dove, measured the aerodynamic forces produced by the dove, and measured the activation and lengthening of the pectoralis muscles of four doves. To image the 3D wing surface of each dove at 1000 Hz, we used a structured-light system. We measured the vertical and horizontal aerodynamic forces produced by the dove at 2000 Hz using an aerodynamic force platform (AFP). Finally, sampling at 10,000 Hz, we used electromyography (EMG) to measure the electrical activation of the pectoralis and sonomicrometry to measure the strain of the pectoralis. We analyzed the second wingbeat after takeoff for four 2-year-old near-white Ringneck doves (Streptopelia risoria; 3 males, 1 female), which were trained to fly between perches (1.6 cm diameter) 0.65 m apart inside of the AFP. We recorded 5 flights from each dove while measuring the muscle activity for a total of 20 flights. To assess the effect of surgery and the recording cable on flight behavior, we also recorded doves 3 and 4 during five pre-surgery flights, and dove 3 during five post-surgery flights, but without the cable needed to measure muscle activity attached. The perches were mounted 0.36 m above the bottom plate of the AFP, and the residual descent angle between the takeoff and landing perch was 2 degrees. Training involved light tapping on the tail to initiate a flight to the other perch. Some flights were rejected as outliers due to inaccurately eliciting a flight or equipment failure (noisy or missing sonomicrometry signal; insufficient suspended cable length allotment). All experiments were approved by and in accordance with Stanford University's Institutional Animal Care and Use Committee. Further details are provided in the paper.
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DoveMuscles_DataCode.zip
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Additional details
Related works
- Is cited by
- 10.1242/jeb.149708 (DOI)
- 10.7554/eLife.89968.1 (DOI)