Abstract
Previous studies showed that birds primarily use their hindlimbs to propel themselves into the air in order to take-off. Yet, it remains unclear how the different parts of their musculoskeletal system move to produce the necessary acceleration. To quantify the relative motions of the bones during the terrestrial phase of take-off, we used biplanar fluoroscopy in two species of birds, diamond dove (Geopelia cuneata) and zebra finch (Taeniopygia guttata). We obtained a detailed 3D kinematics analysis of the head, the trunk and the three long bones of the left leg. We found that the entire body assisted the production of the needed forces to take-off, during two distinct but complementary phases. The first one, a relatively slow preparatory phase, started with a movement of the head and an alignment of the different groups of bones with the future take-off direction. It was associated with a pitch down of the trunk and a flexion of the ankle, of the hip and, to a lesser extent, of the knee. This crouching movement could contribute to the loading of the leg muscles and store elastic energy that could be released in the propulsive phase of take-off, during the extension of the leg joints. Combined with the fact that the head, together with the trunk, produced a forward momentum, the entire body assisted the production of the needed forces to take-off. The second phase was faster with mostly horizontal forward and vertical upward translation motions, synchronous to an extension of the entire lower articulated musculoskeletal system. It led to the propulsion of the bird in the air with a fundamental role of the hip and ankle joints to move the trunk upward and forward. Take-off kinematics were similar in both studied species, with a more pronounced crouching movement in diamond dove, which can be related to a large body mass compared to zebra finch.
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Acknowledgements
The authors acknowledge the organisers of the XROMM course, EL Brainerd, SM Gatesy, DB Baier, and others at Brown University, RI, USA, in June 2010, for their informative course and their work for continually improving the method. We thank BW Tobalske and B Jackson for the surgery they performed on the animals, as well as KE Crandell for her support during the data acquisition. The authors would like to acknowledge the Concord field station, especially A Biewener for the accommodation and equipment access as well as his remarks on the draft of the manuscript. Thanks to I Ross for his help with the CT scan acquisition at the Harvard facilities. The authors want to acknowledge the anonymous reviewers whose comments significantly improved the paper.
Funding
This research was supported by grants from the UMR 7179, lʼAction Transversale du Muséum National dʼHistoire Naturelle formes possibles, formes réalisées and from Ecole Doctorale Frontières du Vivant and Bettencourt-Schueller Foundation fellowships. Travels were paid by the UMR 7179.
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Communicated by: Sven Thatje
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Supplementary Material 1
Resultant forces profiles in Diamond Dove (a) and Zebra Finch (b) during take-off, modified from Provini et al. (2012b). (PDF 39 kb)
Supplementary Material 2
Location of the implanted markers (in black) and virtual markers (in red) on the head (a), the pelvis (b), the left femur (c), left tibiotarsus (d) and left tarsometatarsus (e).The size of the markers has been magnified to facilitate their identification on the figure. (PDF 765 kb)
Supplementary Material 3
Video of the terrestrial phase of take-off of a Diamond Dove and a Zebra Finch (WMV 7349 kb)
Supplementary Material 4
ACS (a-f), JCS conventions (h) for each bones and reference pose (g). Craniolateral and lateral view of the head ACS (a), craniolateral and lateral view of the trunk ACS (b), craniolateral and lateral view of the left acetabular ACS (c), craniolateral and dorsal view of the femur ACSs (d), craniolateral and dorsal view of the tibiotarsus ACSs (e), craniolateral and dorsal view of the tarsometatarsus ACSs (f). Craniolateral and dorsal views of the reference pose (g), showing the JCSs axes when all translations and rotations are 0. To differentiate the bones that are overlapping we used several colours (orange for the head, light yellow for the trunk, yellow for the femur, white for the tibiotarsus, light yellow for the tarsometatarsus). Anterolateral view of the head, trunk and hindlimbs showing the joint coordinate systems (JCSs) (h) by which flexion-extension (blue), abduction-adduction (green) and long-axis rotations (red) were measured at the hip, knee and ankle and by which antero-posterior (red), left-right (green) and ventro-dorsal (blue) translations, as well as yaw (blue), pitch (green) and roll (red) were measured at the head and pelvis. (PDF 1077 kb)
Supplementary Material 5
Segmented regressions calculated on Trtx (red) and Trtz (blue) through take-off sequence in each trial of Diamond Dove take-off (a) and Zebra Finch (b). Breakpoint value is indicated as well as the r 2 of the segmented regression for each trial. (PDF 151 kb)
Supplementary Material 6
Mean velocities calculated on the Trunk vertical and horizontal translations. Means are represented with a solid line, the envelop represents standard deviation, for Diamond Dove (a) on the left and Zebra Finch (b). (PDF 59 kb)
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Provini, P., Abourachid, A. Whole-body 3D kinematics of bird take-off: key role of the legs to propel the trunk. Sci Nat 105, 12 (2018). https://doi.org/10.1007/s00114-017-1535-8
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DOI: https://doi.org/10.1007/s00114-017-1535-8