Abstract The origin of avian flight is one of the most controversial debates in Paleontology. This paper investigates the wing performance of Caudipteryx, the most basal non-volant dinosaur with pennaceous feathered forelimbs by using modal effective mass theory. From a mechanical standpoint, the forced vibrations excited by hindlimb locomotion stimulate the movement of wings, creating a flapping-like motion in response. This shows that the origin of the avian flight stroke should lie in a completely natural process of active locomotion on the ground. In this regard, flapping in the history of evolution of avian flight should have already occurred when the dinosaurs were equipped with pennaceous remiges and rectrices. The forced vibrations provided the initial training for flapping the feathered wings of theropods similar to Caudipteryx.

Author summary The origin of avian flight in the perspective of mechanics has been investigated for the first time. We reported the first evidence for flapping hypothesis based on principle of physical modeling. This is significant because using modal effective mass method and reconstructed Caudipteryx, the most basal non-volant winged dinosaur, we captured significant and negligible modes and realized that resonance oscillation of Caudipteryx wings could occur as the running speed approached to the primary frequencies. Such forced vibrations induced by legs' motions during running trained the Caudipteryx and the other feathered dinosaurs to flap their wings.

Citation: Talori YS, Zhao J-S, Liu Y-F, Lu W-X, Li Z-H, O'Connor JK (2019) Identification of avian flapping motion from non-volant winged dinosaurs based on modal effective mass analysis. PLoS Comput Biol 15(5): e1006846. https://doi.org/10.1371/journal.pcbi.1006846 Editor: Daniel Martins, Universidade Federal de Santa Catarina, BRAZIL Received: August 29, 2018; Accepted: February 5, 2019; Published: May 2, 2019 Copyright: © 2019 Talori et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the manuscript and its Supporting Information files. Funding: This work was supported by the National Natural Science Foundation of China under grant 51575291 (URL: http://www.nsfc.gov.cn/, received by J-SZ), the National Major Science and Technology Project of China under grant 2015ZX04002101 (URL: http://www.most.gov.cn/, received by J-SZ), State Key Laboratory of Tribology, Tsinghua University (URL: http://sklt.tsinghua.edu.cn/, received by J-SZ), and the 221 program of Tsinghua University (URL: http://www.tsinghua.edu.cn/, received by J-SZ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction The origin of avian flight has been debated for over 150 years, ever since the discovery of the first fossil of Archaeopteryx in 1861 [1–35]. Being widely considered as the oldest and most basal-known avian taxon, Archaeopteryx is characterized by a long boney tail, three clawed digits forming the manus, teeth throughout the upper and lower jaws, a furcula, a non-ossified sternum, and perhaps most importantly, forelimbs with elongate asymmetrical feathers forming large wings. It is widely accepted that birds are nestled within the derived lineage of theropod dinosaurs, the Maniraptora. However, it is still subject to heavy debate how flight evolved within the Dinosauria, and multiple origins of flight appear increasingly probable [1–12, 24, 31]. Many researchers consider that avian flight evolved through a number of stages from a ground-dwelling quadrupedal reptile [14–18], cursorial bipedal ground-dweller [13–17, 19], and arboreal life [14, 20] including parachuting [14, 21, 22], gliding [14, 16, 20, 22, 23], and eventually achieving active powered flapping flight [14, 16, 20–23]. However, there is increasing support from studies of juvenile birds for a ground up hypothesis in which flight evolved in a terrestrial animal and the flight stroke evolved directly without an intervening gliding phase [36–43]. Among non-avian dinosaurs [20], Caudipteryx represents the most basal taxon with almost completely preserved feathered forelimbs that could be considered ‘proto-wings’ making this taxon important to the study [21] of flight origins [15, 22, 26]. Some other non-volant theropods from the Cretaceous period have been reported with feathered forelimbs [27, 28]. Caudipteryx is a basal member of the Pennaraptora [1], a derived group of maniraptoran dinosaurs, sometimes closely allied with birds and the most primitive group with pennaceous feathers. Caudipteryx has short forelimbs with distally located symmetrical pennaceous feathers and long hindlimbs. The feathering of both fore-and hindlimbs indicates that Caudipteryx was not a volant theropod [26]. Caudipteryx further differs from modern birds which have abbreviated tails and forward centered mass locating near the wings [29]. However, the most primitive winged dinosaur, Caudipteryx, is clearly terrestrial, investigating the aerodynamic properties of the proto-wings of Caudipteryx has the potential to shed light on the origin of avian flight [30]. We estimated the maximum running speed of Caudipteryx to be about 8 m/s. This value was based on the skeletal hindlimb proportions of BPM 00001 and on adopting the assumptions [44, 45] with respect to the limb posture of small theropods and the range of Froude numbers (up to 17) they might have utilized in running (see S1 Speed for detailed calculation about speed) [44, 45]. We also focused our analysis on a literally generic Caudipteryx with a body mass of 5 kg, a realistic value given that an empirical equation for estimating theropod body masses on the basis of femoral length [46] produces results ranging from 4.74 kg to 5.18 kg (mean value = 4.96 kg) for a total of five described specimens (see S1 Mass for detailed calculation about mass) [24, 47, 48]. Any part, mechanism or system has its particular natural frequencies and corresponding mode shapes [46–51]. Mathematically we can compute which natural frequency and related mode shape is significant and effective to take them into account [49, 52]. The theory of modal effective mass is based on natural frequency, modal analysis and effective masses associated with different directions [49]. The modal effective mass is a measure to classify the importance of a mode shape when a structure is excited by the enforced acceleration from base. A high effective mass in a certain direction will lead to a high reaction force at the base and will be easily excited. Resonance phenomenon occurs on the Caudipteryx when the frequency of the forced vibrations excited by running legs is matched with any natural frequency of Caudipteryx. Hence, by detecting effective natural frequencies of the whole body and analysis of corresponding mode shapes, the velocities of the Caudipteryx that stimulate the wings to flap can be obtained (50 cm is measured for the step length of Caudipteryx). To this end, a simplified mathematical model, a Finite Element Model, a reconstructed physical model of Caudipteryx, and experiment on young ostrich have been utilized. The simplified mathematics model helps us to understand how to face with the kinematics of Caudipteryx. Finite Element (FE) model gives a precise and acceptable result to compare with the reconstructed model on the test rig and experiment on running juvenile ostrich proves the mathematical analyses and simulations.

Results Mathematical model shows the first mode of the forced vibrations to flap the wings when Caudipteryx ran on the ground at the speed of about 2 m/s, the mode shape of which is expressed with a vector of n 1 = (0.393 0.62 0.62 0.158 0.158 0.432 0.45)T. The FE model analysis results of the modal effective mass of the Caudipteryx (Table E in S1 Table) indicate that the effective natural modes occur only in vertical direction (Y-axis) and they are almost zero in lateral motions (X and Z axes). It expresses that the first natural frequency of about 1.99 Hz is not effective, but the second one of about 2.58 Hz and the third mode of about 5.79 Hz considering the maximum speed of Caudipteryx (the forecasted velocity is about 8 m/s for Caudipteryx) are effective and important. In other words, the oscillation about the torso axis is the first mode (S1 Fig). Therefore, the Caudipteryx should roll its whole body about the torso direction when they ran at a low speed (around 2 m/s) near the first primary frequency. The second primary mode (the most effective mode) occurred as the running speed approached to 2.5 m/s. It means flapping modes were easily excited at low frequency while Caudipteryx ran on the ground at the velocity from around 2.5 m/s to a little faster than 5.8 m/s (S1 Fig). We fabricated four simplest plate wings with different sizes and did experiments on the ostrich to compare the lift forces obtained from the flapping wings passively applied by forced vibrations during running. At the same running speed, the wings with filament feathers (1st wing) provided the smallest lift, the largest value of which is less than 0.13 N, while the ones with longer feathers could provide larger lift (2nd and 3rd wings), and the longest feather (4th wing) could provide the largest lift which exceeds 0.42 N (S3 Fig).

Discussion In the simplified rigid body system of seven degrees of freedom of Caudipteryx, the whole system can be excited by the displacements of feet, x 4 and x 5 during running. After this excitation, the whole body masses move along their individual vertical directions in this model (Fig 1). It illustrates the kinematics of Caudipteryx mathematically. In order to obtain the precise results using computer simulation, Finite Element Method reveals the phenomenon that the maximum effective mass occurs in the second mode which is a flapping mode. Only in the most effective mode, could the wings of Caudipteryx be excited to flap evidently and then sense lift. Therefore, the results of the FEM model (second model) through Finite Element Method have been considered because of having the highest accuracy. On the other hand, in the FE model simulated by FEM, computer calculations represent that the first natural frequency which had been roughly calculated in the first mathematical model (first model) is almost equal to that of the FEM model; and the other natural frequencies (from the second to the seventh) in comparison with the FEM model (second model) have some deviations but still acceptable. Also in the first model the modal effective masses of each natural mode might not be equal to the accurate FEM model, but the summation of which in simplified seven-degree-of-freedom model must be 5 kilograms. The reason is the limitation on the number of elements/masses (solely seven masses) and having only one DOF in the vertical direction. The effective mass analysis discovers that the first mode has never been effective (Table E in S1 Table). As the speed approached to the second primary frequency, the Caudipteryx output the second oscillation mode. It is the flapping of the wings up and down with the same amplitudes and same directions. The simulation has been extended by either increasing or decreasing the mass of each part of the Caudipteryx (Table D in S1 Table) and assumed eight excessive masses except the actual one (S5 Fig) (by measuring) from 2 kg to 10 kg in a similar geometrical model. Hence, the frequencies and corresponding effective masses in Y-axis have been studied (Table F in S1 Table). The analyses reveal that the performance of effective modes of any model (models A, B, …, I) are identical but at different frequencies. It means that in all mass distribution models, effective mode mainly depends on the creature’s velocity. When the forced vibration frequency is near the second natural frequency, the flapping mode will be occurred. The natural frequency decreases from 4.0 Hz in mass model A to 1.8 Hz in mass model I (S5 Fig) in the second mode. Therefore, as the weight of the creature increases, the velocity necessary to reach flapping mode might be decreased. With the observation of the experiments, we realized that when the speed of the reconstructed Caudipteryx robot on the test rig (S2 Fig) reached 2.31 m/s (near the value of what has been simulated by FEM model), the robot’s wings started to output most obvious flapping motions which is the resonance of forced vibrations in physics (Fig 4). Using theory of modal effective mass and reconstruction of Caudipteryx zoui (BPM0001) (S6 Fig and Table A in S1 Table), we infer that flapping flight could be developed earlier than gliding in the evolution of avian flight. When the running speed was near the second primary speed of about 2.5 m/s, both wings of the Caudipteryx generated oscillations similar to flapping wings. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 4. Forced vibrations of wings of Caudipteryx robot deduced by test rig ( Forced vibrations of wings of Caudipteryx robot deduced by test rig ( S1 Video ) which approaches the flapping flight of modern birds [ 56 ]. Through curve iteration, we obtained the flapping function ϴ right = 932.7sin(19.01t−3.35)+28.18sin(15.25t−5.103)+898.2 sin(19.16t+6.034) and ϴ left = 135.6 sin(6.453t+1.808)+1558 sin(0.4013t+6.198)+6.517 sin(18.87t + 0.4756). We here defined the anticlockwise motion of both wings as the positive direction. Therefore, the down stroke for the left wing is a positive motion while the down stroke for the right wing is a negative one. https://doi.org/10.1371/journal.pcbi.1006846.g004 Step length in running animals varies with speed and gait and animals do not just have one step length. Any given velocity in this research such as 2, 2.5 and 5.79 m/s dedicated to first, second and third modes was obtained by measuring and assuming some parameters from the fossil such as step length, stiffness and mass (see S1 Text for detailed explanations about Caudipteryx velocity and step length). To eliminate these uncertain values, we used interval analysis which is a powerful mathematical tool in engineering (see S1 Text for detailed explanations about Interval Analysis method). Modal effective mass and Interval Analysis represent that flapping motion occurred at lower velocity. It means, if step length was between 30 cm to 70 cm and if mass was between 3 to 7 kg, Caudipteryx had flapping motion and it occurred at lower velocities (there must be a value that will render the second mode although we do not know the exact number which is in a certain Interval). Hence, the velocities of 2.5 m/s and 5.86 m/s are only two cases among all possibilities. Therefore, the conclusion that the second and the third modes must occur at a certain value is an objective conclusion. Further, the physical phenomenon of flapping motion (induced by forced harmonious vibrations) always be generated in running, but we cannot obtain the precise value of running speed since it might be expressed with an interval of velocity. Hence, the role of body oscillation during a run should be taken into account in order to understand the origin and evolution of avian flapping wings. Experiment results on ostrich indicated that the vibrations of the feathered wings were easily induced when ostrich ran on the ground. Under the assumption of the same length of forearms for the feathered dinosaurs, the wing with the shortest feathers generated the flapping motions with the largest amplitude while the ones with longer feathers produced the flapping motions with smaller amplitudes (S4 Fig). This is interpreted by the air resistance. The larger the wing area, the larger the resistance, and the smaller the amplitude for the passive vibrations. This experiment suggests that the flapping motion might be developed by the forced vibrations during terrestrial locomotion when the winged dinosaur appeared on the earth. However, the lift obtained from the running-foot forced vibrations shows that the longer and larger the wing was, the larger the lift would be (S3 Fig). Therefore, forced vibrations may represent the earliest stages in the evolution of forelimb flapping in winged theropods. This suggests that flapping behavior evolved in non-volant theropods long time ago before they could actively fly. Experiments on the Caudipteryx robot based on the fossil (Caudipteryx sp. IVPP V12430) and the experiments on artificial wings placed on the back of a juvenile ostrich indicated that the forced vibrations of plumage forearms during walking and running taught the winged theropods to flap their wings. These analyses suggest that the impetus of the evolution of powered flight in the theropod lineage that lead to Aves may have been an entirely natural phenomenon produced by bipedal motion in the presence of feathered forelimbs.

Acknowledgments The authors acknowledge the kind suggestions from Prof. Dr. Pascal Godefroit from Royal Belgian Institute of Natural Sciences, Prof. Dr. Corwin Sullivan from the Department of Biological Sciences, University of Alberta, Canada, Prof. Dr. Zhong-He Zhou and Prof. Dr. Min Wang from the Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, 100044, P. R. China.