Reconstruction of the Hindlimb Locomotion of Confuciusornis (Aves) and Its Implication for the Origin of Avian Flight
Keywords:
Early birds; habit behavior; take-off; musculoskeletal system; simulation techniques
Ariticle ID:
55
Abstract
As one of the most basal avian clades, the Confuciusornithids are ideal in revealing the early evolution of avian flight. Birds’ hindlimbs are functionally diverse and contain a wealth of information about their behavior. The hindlimb of Confuciusornis, however, has only been studied in detail in terms of functional morphology, and quantitative studies that directly assess locomotor ability are relatively lacking. This has led to certain controversies on the behavior of Confuciusornis. This paper reviews the debates over the life habits and take-off ability of Confuciusornis, which are closely related to their hindlimb function. Several methodologies adopted engineering techniques, including the geometrical analysis of long bones, physiological reconstruction of muscles, kinematic and kinetic characteristics estimating, and appendage locomotor mechanism analysis, are recommended for estimating the hindlimb functions of Confuciusornis. Considering that the fossil bones are fragile, irregular in shape, and usually deformed, it is appropriate to apply computer numerical simulation techniques to such studies. A sufficient functional quantitative study will help clarify early bird locomotor behavior, which will provide clues and evidence for further exploration of the origin of bird flight and early bird movement.
References
1. Zhou, Z. (2004). The origin and early evolution of birds: Discoveries, disputes, and perspectives from fossil evidence. Naturwissenschaften, 91, 455–471.
2. Heers, A. M., Dial, K. P. (2012). From extant to extinct: Locomotor ontogeny and the evolution of avian flight. Trends in Ecology & Evolution, 27, 296–305.
3. Xu, X., Zhou, Z., Dudley, R., Mackem, S., Chuong, C. M. et al. (2014). An integrative approach to understanding bird origins. Science, 346, 1253293.
4. Gatesy, S. M., Dial, K. P. (1996). Locomotor modules and the evolution of avian flight. Evolution, 50, 331–340.
5. Butler, P. J. (1991). Exercise in birds. Journal of Experimental Biology, 160, 233–262.
6. Heers, A. M., Dial, K. P. (2015). Wings versus legs in the avian bauplan: Development and evolution of alternative locomotor strategies. Evolution, 69, 305–320.
7. Dial, K. P. (2003). Wing-assisted incline running and the evolution of flight. Science, 299, 402–404.
8. Provini, P., Tobalske, B. W., Crandell, K. E., Abourachid, A. (2012). Transition from leg to wing forces during take-off in birds. Journal of Experimental Biology, 215, 4115–4124.
9. Abourachid, A., Höfling, E. (2012). The legs: A key to bird evolutionary success. Journal of Ornithology, 153, 193–198.
10. Benson, R. B. J., Choiniere, J. N. (2013). Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proceedings of Biological Sciences, 280, 20131780.
11. Wang, M., O’Connor, J., Zhou, Z. (2019). A taxonomical revision of the confuciusornithiformes (Aves: Pygostylia). Vertebrata Palasiatica, 57, 1–37.
12. Hou, L., Zhou, Z., Martin, L. D., Feduccia, A. (1995). A beaked bird from the Jurassic of China. Nature, 377, 616–618.
13. Chiappe, L. M., Ji, S. A., Ji, Q., Norell, M. A. (1999). Anatomy and systematics of the confuciusornithidae (Theropoda, Aves) from the late Mesozoic of Northeastern China. Bulletin of the American Museum of Natural History, 242, 1–89.
14. Sun, M. (2018). Aerodynamics of animal flight. Acta Aerodynamica Sinica, 36, 122–128.
15. Chatterjee, S., Templin, R. J. (2012). Palaeoecology, aerodynamics, and the origin of avian flight. In: Talent, J. A. (Ed.), Earth and life: global biodiversity, extinction intervals and biogeographic perturbations through time, pp. 585–612. Dordrecht: Springer Netherlands.
16. Hou, L., Martin, L. D., Zhou, Z., Feduccia, A., Zhang, F. (1999). A diapsid skull in a new species of the primitive bird Confuciusornis. Nature, 399, 679–682.
17. Zhang, F., Zhou, Z., Benton, M. J. (2008). A primitive confuciusornithid bird from China and its implications for early avian flight. Science China Earth Sciences, 51, 625–639.
18. Zhang, F., Zhou, Z., Li, D., Li, Z. (2009). The present situation of confuciusornithids research. Chinese Journal of Nature, 31, 8–11.
19. Ji, Q., Chiappe, L. M., Ji, S. (1999). A new late Mesozoic confuciusornithid bird from China. Journal of Vertebrate Paleontology, 19, 1–7.
20. Wang, M. (2014). Taxonomical revision, ontogenetic, habitat and phylogenetic analyses of enantiornithes (Aves: Ornithothoraces) of China (Ph.D. Thesis). Chinese Academy of Sciences, Beijing.
21. McIntosh, A. P. (2017). Geometric morphometric analysis of the pedal claw of the early cretaceous bird confuciusornis sanctus (Confuciusornithidae) and its functional and behavioral implications (Master of Science). DePaul University.
22. Falk, A. R., Lamsdell, J. C., Gong, E. (2021). Principal component analysis of avian hind limb and foot morphometrics and the relationship between ecology and phylogeny. Paleobiology, 47, 314–336.
23. Zhou, Z., Farlow, J. (2001). Flight capability and habits of Confuciusornis. In: Gauthier, J. A., Gall, L. F. (Eds.), New perspectives on the origin and early evolution of birds, pp. 237–254. New Haven: Yale University Press.
24. Longrich, N. R., Vinther, J., Meng, Q., Li, Q., Russell, A. P. (2012). Primitive wing feather arrangement in Archaeopteryx Lithographica and Anchiornis Huxleyi. Current Biology, 22, 2262–2267.
25. Falk, A. R., Kaye, T. G., Zhou, Z., Burnham, D. A. (2016). Laser fluorescence illuminates the soft tissue and life habits of the early cretaceous bird Confuciusornis. PLoS One, 11, e0167284.
26. Zheng, X., O’Connor, J. K., Wang, X., Pan, Y., Wang, Y. et al. (2017). Exceptional preservation of soft tissue in a new specimen of Eoconfuciusornis and its biological implications. National Science Review, 4, 441–452.
27. Nudds, R. L., Dyke, G. J. (2010). Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science, 328, 887–889.
28. Paul, G. S. (2010). Comment on “Narrow Primary Feather Rachises in Confuciusornis and Archaeopteryx suggest poor flight ability”. Science, 330, 320.
29. Lees, J., Garner, T., Cooper, G., Nudds, R. (2017). Rachis morphology cannot accurately predict the mechanical performance of primary feathers in extant (and therefore fossil) feathered flyers. Royal Society Open Science, 4, 160927.
30. Guo, Y., Zhao, Y., Zhou, Y., Yang, J., Wang, Y. et al. (2021). Computational fluid dynamics will shed a new light on functional-morphological studies of confuciusornithids (Aves) in Eastern Asia during early cretaceous. Fresenius Environmental Bulletin, 36, 7470–7475.
31. Wang, I., Guo, Y., An, X., Zhao, Y., Wang, J. (2019). Three-dimensional reconstruction and numerical simulation of flight performance of Confuciusornis. Open Journal of Natural Sciences, 7, 590–595.
32. Pittman, M., Kaye, T. G., Wang, X., Zheng, X., Dececchi, T. A. et al. (2022). Preserved soft anatomy confirms shoulder-powered upstroke of early theropod flyers, reveals enhanced early pygostylian upstroke, and explains early sternum loss. Proceedings of the National Academy of Sciences of the United States of America, 119, e2205476119.
33. Bonser, R., Rayner, J. (1996). Measuring leg thrust forces in the common starling. Journal of Experimental Biology, 199, 435–439.
34. Earls, K. D. (2000). Kinematics and mechanics of ground take-off in the starling Sturnis Vulgaris and the quail Coturnix coturnix. Journal of Experimental Biology, 203, 725–739.
35. Heppner, F. H., Anderson, J. G. T. (1985). Leg thrust important in flight take-off in the pigeon. Journal of Experimental Biology, 114, 285–288.
36. Provini, P., Abourachid, A. (2018). Whole-body 3D kinematics of bird take-off: Key role of the legs to propel the trunk. Science of Nature, 105, 12.
37. Crandell, K. E., Smith, A. F., Crino, O. L., Tobalske, B. W. (2018). Coping with compliance during take-off and landing in the diamond dove (Geopelia Cuneata). PLoS One, 13, e0199662.
38. Wang, M., Zhou, Z. (2017). The evolution of birds with implications from new fossil evidences. In: Maina, J. N. (Ed.), The biology of the avian respiratory system: evolution, development, structure and function, pp. 1–26. Cham: Springer International Publishing.
39. Bell, A., Marugán-Lobón, J., Navalón, G., Nebreda, S. M., DiGuildo, J. et al. (2021). Quantitative analysis of morphometric data of pre-modern birds: Phylogenetic versus ecological signal. Frontiers in Earth Science, 9, 663342.
40. Provini, P., Goupil, P., Hugel, V., Abourachid, A. (2012). Walking, paddling, waddling: 3D kinematics anatidae locomotion (Callonetta leucophrys). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 317, 275–282.
41. Gatesy, S. M., Middleton, K. M. (1997). Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology, 17, 308–329.
42. Bell, A., Chiappe, L. M. (2011). Statistical approach for inferring ecology of Mesozoic birds. Journal of Systematic Palaeontology, 9, 119–133.
43. Navalón, G., Bjarnason, A., Griffiths, E., Benson, R. B. J. (2022). Environmental signal in the evolutionary diversification of bird skeletons. Nature, 611, 306–311.
44. Zeffer, A., Johansson, L. C., Marmebro, A. (2003). Functional correlation between habitat use and leg morphology in birds (Aves). Biological Journal of the Linnean Society, 79, 461–484.
45. Habib, M. B., Ruff, C. (2008). The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society, 153, 601–624.
46. Raikow, R. J. (1985). Systematic and functional aspects of the locomotor system of the Scrub-birds, Atrichornis, and lyrebirds, Menura (Passeriformes: Atrichornithidae and Menuridae). Records of the Australian Museum, 37(4), 211–228.
47. Wang, L., Wei, X., Liang, X., Zhang, Z. (2021). Ontogenetic changes of hindlimb muscle mass in Cabot’s tragopan (Galliformes, Phasianidae) and their functional implications. Anatomical Record, 304, 2841–2855.
48. Mosto, M. C. (2017). Comparative hindlimb myology within the family falconidae. Zoomorphology, 136, 241–250.
49. Gatesy, S. M. (2002). Locomotor evolution on the line to modern birds. In: Chiappe, L. M., Witmer, L. M. (Eds.), Mesozoic birds: Above the heads of dinosaurs, pp. 432–447. Berkeley, CA: University of California Press.
50. Hutchinson, J. R., Allen, V. (2009). The evolutionary continuum of limb function from early theropods to birds. Naturwissenschaften, 96, 423–448.
51. Zhou, Z., Hou, L. (1998). Confuciusornis and the early evolution of birds. Vertebrata Palasiatica, 36, 136–146.
52. Zinoviev, A. V. (2009). An attempt to reconstruct the lifestyle of confuciusornithids (Aves, Confuciusornithiformes). Paleontological Journal, 43, 444–452.
53. Tobalske, B. W., Altshuler, D. L., Powers, D. R. (2004). Take-off mechanics in hummingbirds (Trochilidae). Journal of Experimental Biology, 207, 1345–1352.
54. Tobalske, B. W., Hedrick, T. L., Dial, K. P., Biewener, A. A. (2003). Comparative power curves in bird flight. Nature, 421, 363–366.
55. Kullberg, C., Lafrenz, M. (2007). Escape take-off strategies in birds: The significance of protective cover. Behavioral Ecology and Sociobiology, 61, 1555–1560.
56. Currey, J. D. (2002). Bones: Structure and mechanics. Princeton: Princeton University Press.
57. Currey, J. D. (2012). The structure and mechanics of bone. Journal of Materials Science, 47, 41–54.
58. Biewener, A. A. (1982). Bone strength in small mammals and bipedal birds: Do safety factors change with body size? Journal of Experimental Biology, 98, 289–301.
59. Erickson, G. M., Catanese III, J., Keaveny, T. M. (2002). Evolution of the biomechanical material properties of the femur. Anatomical Record, 268, 115–124.
60. Cowgill, L. W., Warrener, A., Pontzer, H., Ocobock, C. (2010). Waddling and toddling: The biomechanical effects of an immature gait. American Journal of Physical Anthropology, 143, 52–61.
61. Nadell, J. A. (2017). Ontogeny and adaptation: A cross-sectional study of primate limb elements (Ph.D. Thesis). Durham University, Durham.
62. Wei, X., Zhang, Z. (2019). Ontogenetic changes of geometrical and mechanical characteristics of the avian femur: A comparison between precocial and altricial birds. Journal of Anatomy, 235, 903–911.
63. Carlson, K. J., Judex, S. (2007). Increased non-linear locomotion alters diaphyseal bone shape. Journal of Experimental Biology, 210, 3117–3125.
64. Agostini, G. M., Ross, A. H. (2011). The effect of weight on the femur: A cross-sectional analysis. Journal of Forensic Sciences, 56, 339–343.
65. Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R., Kram, R. et al. (2000). How animals move: An integrative view. Science, 288, 100–106.
66. Lieber, R. L., Fridén, J. (2000). Functional and clinical significance of skeletal muscle architecture. Muscle & Nerve, 23, 1647–1666.
67. Alexander, R. M. (2003). Principles of animal locomotion. Princeton: Princeton University Press.
68. Bryant, H. N., Russell, A. P. (1992). The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Philosophical Transactions of the Royal Society B: Biological Sciences, 337, 405–418.
69. Witmer, L. M. (1995). The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason, J. J. (Ed.), Functional morphology in vertebrate paleontology, pp. 19–33. Cambridge, UK: Cambridge University Press.
70. Benton, M. J. (2010). Studying function and behavior in the fossil record. PLoS Biology, 8, e1000321.
71. Rayfield, E. J. (2019). What does musculoskeletal mechanics tell us about evolution of form and function in vertebrates? In: Bels, V., Whishaw, I. (Eds.), Feeding in vertebrates, pp. 45–70. Cham: Springer.
72. Carrano, M. T., Hutchinson, J. R. (2002). Pelvic and hindlimb musculature of Tyrannosaurus Rex (Dinosauria: Theropoda). Journal of Morphology, 253, 207–228.
73. Hutchinson, J. R. (2002). The evolution of hindlimb tendons and muscles on the line to crown-group birds. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 133, 1051–1086.
74. Hutchinson, J. R., Frank, C. A., Silvia, S. B., Scott, L. D. (2005). Analysis of hindlimb muscle moment arms in Tyrannosaurus rex using a three-dimensional musculoskeletal computer model: Implications for stance, gait, and speed. Paleobiology, 31, 676–701.
75. Sellers, W. I., Pond, S. B., Brassey, C. A., Manning, P. L., Bates, K. T. (2017). Investigating the running abilities of Tyrannosaurus rex using stress-constrained multibody dynamic analysis. PeerJ, 5, e3420.
76. Allen, V. R., Kilbourne, B. M., Hutchinson, J. R. (2021). The evolution of pelvic limb muscle moment arms in bird-line archosaurs. Science Advances, 7, eabe2778.
77. Hutchinson, J. R. (2001). The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society, 131, 169–197.
78. Rubenson, J., Lloyd, D. G., Besier, T. F., Heliams, D. B., Fournier, P. A. (2007). Running in ostriches (Struthio camelus): Three-dimensional joint axes alignment and joint kinematics. Journal of Experimental Biology, 210, 2548–2562.
79. Brainerd, E. L., Baier, D. B., Gatesy, S. M., Hedrick, T. L., Metzger, K. A. et al. (2010). X-ray reconstruction of moving morphology (XROMM): Precision, accuracy and applications in comparative biomechanics research. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 313A(5), 262–279.
80. Seth, A., Hicks, J. L., Uchida, T. K., Habib, A., Dembia, C. L. et al. (2018). Opensim: Simulating musculoskeletal dynamics and neuromuscular control to study human and animal movement. PLoS Computational Biology, 14, e1006223.
81. Delp, S. L., Anderson, F. C., Arnold, A. S., Loan, P., Habib, A. et al. (2007). Opensim: Open-source software to create and analyze dynamic simulations of movement. IEEE Transactions on Biomedical Engineering, 54, 1940–1950.
82. Bishop, P. J., Cuff, A. R., Hutchinson, J. R. (2021). How to build a dinosaur: Musculoskeletal modeling and simulation of locomotor biomechanics in extinct animals. Paleobiology, 47, 1–38.
83. Lockley, M. G., Harris, J. D. (2010). On the trail of early birds: A review of the fossil footprint record of avian morphological and behavioral evolution. In: Ulrich, P. K. (Ed.), Trends in ornithology research, pp. 1–63. Hauppauge: Nova Science Publishers.
84. Alexander, R. M. (1976). Estimates of speeds of dinosaurs. Nature, 261, 129–130.
85. Thulborn, R. A. (1982). Speeds and gaits of dinosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology, 38, 227–256.
86. Bishop, P. J., Clemente, C. J., Weems, R. E., Graham, D. F., Lamas, L. P. et al. (2017). Using step width to compare locomotor biomechanics between extinct, non-avian theropod dinosaurs and modern obligate bipeds. Journal of the Royal Society Interface, 14, 20170276.
87. Kubo, T., Benton, M. J. (2009). Tetrapod postural shift estimated from permian and triassic trackways. Palaeontology, 52, 1029–1037.
88. Lallensack, J. N., Falkingham, P. L. (2022). A new method to calculate limb phase from trackways reveals gaits of sauropod dinosaurs. Current Biology, 32, 1635–1640.
89. Falk, A. R. (2011). Tracking Mesozoic birds across the world. Journal of Systematic Palaeontology, 9, 85–90.
90. Xing, L., Lockley, M. G., Jia, C., Klein, H., Niu, K. et al. (2021). Lower cretaceous avian-dominated, theropod, thyreophoran, pterosaur and turtle track assemblages from the Tugulu Group, Xinjiang, China: Ichnotaxonomy and palaeoecology. PeerJ, 9, e11476.
91. Falk, A. R., Lim, J. D., Hasiotis, S. T. (2014). A behavioral analysis of fossil bird tracks from the haman formation (Republic of Korea) shows a nearly modern avian ecosystem. Vertebrata Palasiatica, 52, 129–152.
92. Gatesy, S. M. (1990). Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology, 16, 170–186.
93. Middleton, K. M., Gatesy, S. M. (2000). Theropod forelimb design and evolution. Zoological Journal of the Linnean Society, 128, 149–187.
94. Erdemir, A., McLean, S., Herzog, W., van den Bogert, A. J. (2007). Model-based estimation of muscle forces exerted during movements. Clinical Biomechanics, 22, 131–154.
95. Lin, Y. C., Dorn, T. W., Schache, A. G., Pandy, M. G. (2012). Comparison of different methods for estimating muscle forces in human movement. Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, 226, 103–112.
96. Anderson, F. C., Pandy, M. G. (2001). Static and dynamic optimization solutions for gait are practically equivalent. Journal of Biomechanics, 34, 153–161.
97. Rankin, J. W., Rubenson, J., Hutchinson, J. R. (2016). Inferring muscle functional roles of the ostrich pelvic limb during walking and running using computer optimization. Journal of the Royal Society Interface, 13, 20160035.
98. Bates, K. T., Manning, P. L., Margetts, L., Sellers, W. I. (2010). Sensitivity analysis in evolutionary robotic simulations of bipedal dinosaur running. Journal of Vertebrate Paleontology, 30, 458–466.
99. Sellers, K. C., Middleton, K. M., Davis, J. L., Holliday, C. M. (2017). Ontogeny of bite force in a validated biomechanical model of the American alligator. Journal of Experimental Biology, 220, 2036–2046.
100. Morgan, E. F., Bouxsein, M. L. (2005). Use of finite element analysis to assess bone strength. BoneKEy Osteovision, 2, 8–19.
101. Richmond, B. G., Wright, B. W., Grosse, I., Dechow, P. C., Ross, C. F. et al. (2005). Finite element analysis in functional morphology. Anatomical Record, 283, 259–274.
102. Rayfield, E. J. (2007). Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annual Review of Earth and Planetary Sciences, 35, 541–576.
103. Marcé-Nogué, J., Püschel, T. A., Kaiser, T. M. (2017). A biomechanical approach to understand the ecomorphological relationship between primate mandibles and diet. Scientific Reports, 7, 8364.
104. Wei, X., Zhang, Z. (2021). Femoral mechanical performance of precocial and altricial birds: A simulation study. Avian Research, 12, 18.
2. Heers, A. M., Dial, K. P. (2012). From extant to extinct: Locomotor ontogeny and the evolution of avian flight. Trends in Ecology & Evolution, 27, 296–305.
3. Xu, X., Zhou, Z., Dudley, R., Mackem, S., Chuong, C. M. et al. (2014). An integrative approach to understanding bird origins. Science, 346, 1253293.
4. Gatesy, S. M., Dial, K. P. (1996). Locomotor modules and the evolution of avian flight. Evolution, 50, 331–340.
5. Butler, P. J. (1991). Exercise in birds. Journal of Experimental Biology, 160, 233–262.
6. Heers, A. M., Dial, K. P. (2015). Wings versus legs in the avian bauplan: Development and evolution of alternative locomotor strategies. Evolution, 69, 305–320.
7. Dial, K. P. (2003). Wing-assisted incline running and the evolution of flight. Science, 299, 402–404.
8. Provini, P., Tobalske, B. W., Crandell, K. E., Abourachid, A. (2012). Transition from leg to wing forces during take-off in birds. Journal of Experimental Biology, 215, 4115–4124.
9. Abourachid, A., Höfling, E. (2012). The legs: A key to bird evolutionary success. Journal of Ornithology, 153, 193–198.
10. Benson, R. B. J., Choiniere, J. N. (2013). Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proceedings of Biological Sciences, 280, 20131780.
11. Wang, M., O’Connor, J., Zhou, Z. (2019). A taxonomical revision of the confuciusornithiformes (Aves: Pygostylia). Vertebrata Palasiatica, 57, 1–37.
12. Hou, L., Zhou, Z., Martin, L. D., Feduccia, A. (1995). A beaked bird from the Jurassic of China. Nature, 377, 616–618.
13. Chiappe, L. M., Ji, S. A., Ji, Q., Norell, M. A. (1999). Anatomy and systematics of the confuciusornithidae (Theropoda, Aves) from the late Mesozoic of Northeastern China. Bulletin of the American Museum of Natural History, 242, 1–89.
14. Sun, M. (2018). Aerodynamics of animal flight. Acta Aerodynamica Sinica, 36, 122–128.
15. Chatterjee, S., Templin, R. J. (2012). Palaeoecology, aerodynamics, and the origin of avian flight. In: Talent, J. A. (Ed.), Earth and life: global biodiversity, extinction intervals and biogeographic perturbations through time, pp. 585–612. Dordrecht: Springer Netherlands.
16. Hou, L., Martin, L. D., Zhou, Z., Feduccia, A., Zhang, F. (1999). A diapsid skull in a new species of the primitive bird Confuciusornis. Nature, 399, 679–682.
17. Zhang, F., Zhou, Z., Benton, M. J. (2008). A primitive confuciusornithid bird from China and its implications for early avian flight. Science China Earth Sciences, 51, 625–639.
18. Zhang, F., Zhou, Z., Li, D., Li, Z. (2009). The present situation of confuciusornithids research. Chinese Journal of Nature, 31, 8–11.
19. Ji, Q., Chiappe, L. M., Ji, S. (1999). A new late Mesozoic confuciusornithid bird from China. Journal of Vertebrate Paleontology, 19, 1–7.
20. Wang, M. (2014). Taxonomical revision, ontogenetic, habitat and phylogenetic analyses of enantiornithes (Aves: Ornithothoraces) of China (Ph.D. Thesis). Chinese Academy of Sciences, Beijing.
21. McIntosh, A. P. (2017). Geometric morphometric analysis of the pedal claw of the early cretaceous bird confuciusornis sanctus (Confuciusornithidae) and its functional and behavioral implications (Master of Science). DePaul University.
22. Falk, A. R., Lamsdell, J. C., Gong, E. (2021). Principal component analysis of avian hind limb and foot morphometrics and the relationship between ecology and phylogeny. Paleobiology, 47, 314–336.
23. Zhou, Z., Farlow, J. (2001). Flight capability and habits of Confuciusornis. In: Gauthier, J. A., Gall, L. F. (Eds.), New perspectives on the origin and early evolution of birds, pp. 237–254. New Haven: Yale University Press.
24. Longrich, N. R., Vinther, J., Meng, Q., Li, Q., Russell, A. P. (2012). Primitive wing feather arrangement in Archaeopteryx Lithographica and Anchiornis Huxleyi. Current Biology, 22, 2262–2267.
25. Falk, A. R., Kaye, T. G., Zhou, Z., Burnham, D. A. (2016). Laser fluorescence illuminates the soft tissue and life habits of the early cretaceous bird Confuciusornis. PLoS One, 11, e0167284.
26. Zheng, X., O’Connor, J. K., Wang, X., Pan, Y., Wang, Y. et al. (2017). Exceptional preservation of soft tissue in a new specimen of Eoconfuciusornis and its biological implications. National Science Review, 4, 441–452.
27. Nudds, R. L., Dyke, G. J. (2010). Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science, 328, 887–889.
28. Paul, G. S. (2010). Comment on “Narrow Primary Feather Rachises in Confuciusornis and Archaeopteryx suggest poor flight ability”. Science, 330, 320.
29. Lees, J., Garner, T., Cooper, G., Nudds, R. (2017). Rachis morphology cannot accurately predict the mechanical performance of primary feathers in extant (and therefore fossil) feathered flyers. Royal Society Open Science, 4, 160927.
30. Guo, Y., Zhao, Y., Zhou, Y., Yang, J., Wang, Y. et al. (2021). Computational fluid dynamics will shed a new light on functional-morphological studies of confuciusornithids (Aves) in Eastern Asia during early cretaceous. Fresenius Environmental Bulletin, 36, 7470–7475.
31. Wang, I., Guo, Y., An, X., Zhao, Y., Wang, J. (2019). Three-dimensional reconstruction and numerical simulation of flight performance of Confuciusornis. Open Journal of Natural Sciences, 7, 590–595.
32. Pittman, M., Kaye, T. G., Wang, X., Zheng, X., Dececchi, T. A. et al. (2022). Preserved soft anatomy confirms shoulder-powered upstroke of early theropod flyers, reveals enhanced early pygostylian upstroke, and explains early sternum loss. Proceedings of the National Academy of Sciences of the United States of America, 119, e2205476119.
33. Bonser, R., Rayner, J. (1996). Measuring leg thrust forces in the common starling. Journal of Experimental Biology, 199, 435–439.
34. Earls, K. D. (2000). Kinematics and mechanics of ground take-off in the starling Sturnis Vulgaris and the quail Coturnix coturnix. Journal of Experimental Biology, 203, 725–739.
35. Heppner, F. H., Anderson, J. G. T. (1985). Leg thrust important in flight take-off in the pigeon. Journal of Experimental Biology, 114, 285–288.
36. Provini, P., Abourachid, A. (2018). Whole-body 3D kinematics of bird take-off: Key role of the legs to propel the trunk. Science of Nature, 105, 12.
37. Crandell, K. E., Smith, A. F., Crino, O. L., Tobalske, B. W. (2018). Coping with compliance during take-off and landing in the diamond dove (Geopelia Cuneata). PLoS One, 13, e0199662.
38. Wang, M., Zhou, Z. (2017). The evolution of birds with implications from new fossil evidences. In: Maina, J. N. (Ed.), The biology of the avian respiratory system: evolution, development, structure and function, pp. 1–26. Cham: Springer International Publishing.
39. Bell, A., Marugán-Lobón, J., Navalón, G., Nebreda, S. M., DiGuildo, J. et al. (2021). Quantitative analysis of morphometric data of pre-modern birds: Phylogenetic versus ecological signal. Frontiers in Earth Science, 9, 663342.
40. Provini, P., Goupil, P., Hugel, V., Abourachid, A. (2012). Walking, paddling, waddling: 3D kinematics anatidae locomotion (Callonetta leucophrys). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 317, 275–282.
41. Gatesy, S. M., Middleton, K. M. (1997). Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology, 17, 308–329.
42. Bell, A., Chiappe, L. M. (2011). Statistical approach for inferring ecology of Mesozoic birds. Journal of Systematic Palaeontology, 9, 119–133.
43. Navalón, G., Bjarnason, A., Griffiths, E., Benson, R. B. J. (2022). Environmental signal in the evolutionary diversification of bird skeletons. Nature, 611, 306–311.
44. Zeffer, A., Johansson, L. C., Marmebro, A. (2003). Functional correlation between habitat use and leg morphology in birds (Aves). Biological Journal of the Linnean Society, 79, 461–484.
45. Habib, M. B., Ruff, C. (2008). The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society, 153, 601–624.
46. Raikow, R. J. (1985). Systematic and functional aspects of the locomotor system of the Scrub-birds, Atrichornis, and lyrebirds, Menura (Passeriformes: Atrichornithidae and Menuridae). Records of the Australian Museum, 37(4), 211–228.
47. Wang, L., Wei, X., Liang, X., Zhang, Z. (2021). Ontogenetic changes of hindlimb muscle mass in Cabot’s tragopan (Galliformes, Phasianidae) and their functional implications. Anatomical Record, 304, 2841–2855.
48. Mosto, M. C. (2017). Comparative hindlimb myology within the family falconidae. Zoomorphology, 136, 241–250.
49. Gatesy, S. M. (2002). Locomotor evolution on the line to modern birds. In: Chiappe, L. M., Witmer, L. M. (Eds.), Mesozoic birds: Above the heads of dinosaurs, pp. 432–447. Berkeley, CA: University of California Press.
50. Hutchinson, J. R., Allen, V. (2009). The evolutionary continuum of limb function from early theropods to birds. Naturwissenschaften, 96, 423–448.
51. Zhou, Z., Hou, L. (1998). Confuciusornis and the early evolution of birds. Vertebrata Palasiatica, 36, 136–146.
52. Zinoviev, A. V. (2009). An attempt to reconstruct the lifestyle of confuciusornithids (Aves, Confuciusornithiformes). Paleontological Journal, 43, 444–452.
53. Tobalske, B. W., Altshuler, D. L., Powers, D. R. (2004). Take-off mechanics in hummingbirds (Trochilidae). Journal of Experimental Biology, 207, 1345–1352.
54. Tobalske, B. W., Hedrick, T. L., Dial, K. P., Biewener, A. A. (2003). Comparative power curves in bird flight. Nature, 421, 363–366.
55. Kullberg, C., Lafrenz, M. (2007). Escape take-off strategies in birds: The significance of protective cover. Behavioral Ecology and Sociobiology, 61, 1555–1560.
56. Currey, J. D. (2002). Bones: Structure and mechanics. Princeton: Princeton University Press.
57. Currey, J. D. (2012). The structure and mechanics of bone. Journal of Materials Science, 47, 41–54.
58. Biewener, A. A. (1982). Bone strength in small mammals and bipedal birds: Do safety factors change with body size? Journal of Experimental Biology, 98, 289–301.
59. Erickson, G. M., Catanese III, J., Keaveny, T. M. (2002). Evolution of the biomechanical material properties of the femur. Anatomical Record, 268, 115–124.
60. Cowgill, L. W., Warrener, A., Pontzer, H., Ocobock, C. (2010). Waddling and toddling: The biomechanical effects of an immature gait. American Journal of Physical Anthropology, 143, 52–61.
61. Nadell, J. A. (2017). Ontogeny and adaptation: A cross-sectional study of primate limb elements (Ph.D. Thesis). Durham University, Durham.
62. Wei, X., Zhang, Z. (2019). Ontogenetic changes of geometrical and mechanical characteristics of the avian femur: A comparison between precocial and altricial birds. Journal of Anatomy, 235, 903–911.
63. Carlson, K. J., Judex, S. (2007). Increased non-linear locomotion alters diaphyseal bone shape. Journal of Experimental Biology, 210, 3117–3125.
64. Agostini, G. M., Ross, A. H. (2011). The effect of weight on the femur: A cross-sectional analysis. Journal of Forensic Sciences, 56, 339–343.
65. Dickinson, M. H., Farley, C. T., Full, R. J., Koehl, M. A. R., Kram, R. et al. (2000). How animals move: An integrative view. Science, 288, 100–106.
66. Lieber, R. L., Fridén, J. (2000). Functional and clinical significance of skeletal muscle architecture. Muscle & Nerve, 23, 1647–1666.
67. Alexander, R. M. (2003). Principles of animal locomotion. Princeton: Princeton University Press.
68. Bryant, H. N., Russell, A. P. (1992). The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Philosophical Transactions of the Royal Society B: Biological Sciences, 337, 405–418.
69. Witmer, L. M. (1995). The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason, J. J. (Ed.), Functional morphology in vertebrate paleontology, pp. 19–33. Cambridge, UK: Cambridge University Press.
70. Benton, M. J. (2010). Studying function and behavior in the fossil record. PLoS Biology, 8, e1000321.
71. Rayfield, E. J. (2019). What does musculoskeletal mechanics tell us about evolution of form and function in vertebrates? In: Bels, V., Whishaw, I. (Eds.), Feeding in vertebrates, pp. 45–70. Cham: Springer.
72. Carrano, M. T., Hutchinson, J. R. (2002). Pelvic and hindlimb musculature of Tyrannosaurus Rex (Dinosauria: Theropoda). Journal of Morphology, 253, 207–228.
73. Hutchinson, J. R. (2002). The evolution of hindlimb tendons and muscles on the line to crown-group birds. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 133, 1051–1086.
74. Hutchinson, J. R., Frank, C. A., Silvia, S. B., Scott, L. D. (2005). Analysis of hindlimb muscle moment arms in Tyrannosaurus rex using a three-dimensional musculoskeletal computer model: Implications for stance, gait, and speed. Paleobiology, 31, 676–701.
75. Sellers, W. I., Pond, S. B., Brassey, C. A., Manning, P. L., Bates, K. T. (2017). Investigating the running abilities of Tyrannosaurus rex using stress-constrained multibody dynamic analysis. PeerJ, 5, e3420.
76. Allen, V. R., Kilbourne, B. M., Hutchinson, J. R. (2021). The evolution of pelvic limb muscle moment arms in bird-line archosaurs. Science Advances, 7, eabe2778.
77. Hutchinson, J. R. (2001). The evolution of femoral osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society, 131, 169–197.
78. Rubenson, J., Lloyd, D. G., Besier, T. F., Heliams, D. B., Fournier, P. A. (2007). Running in ostriches (Struthio camelus): Three-dimensional joint axes alignment and joint kinematics. Journal of Experimental Biology, 210, 2548–2562.
79. Brainerd, E. L., Baier, D. B., Gatesy, S. M., Hedrick, T. L., Metzger, K. A. et al. (2010). X-ray reconstruction of moving morphology (XROMM): Precision, accuracy and applications in comparative biomechanics research. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 313A(5), 262–279.
80. Seth, A., Hicks, J. L., Uchida, T. K., Habib, A., Dembia, C. L. et al. (2018). Opensim: Simulating musculoskeletal dynamics and neuromuscular control to study human and animal movement. PLoS Computational Biology, 14, e1006223.
81. Delp, S. L., Anderson, F. C., Arnold, A. S., Loan, P., Habib, A. et al. (2007). Opensim: Open-source software to create and analyze dynamic simulations of movement. IEEE Transactions on Biomedical Engineering, 54, 1940–1950.
82. Bishop, P. J., Cuff, A. R., Hutchinson, J. R. (2021). How to build a dinosaur: Musculoskeletal modeling and simulation of locomotor biomechanics in extinct animals. Paleobiology, 47, 1–38.
83. Lockley, M. G., Harris, J. D. (2010). On the trail of early birds: A review of the fossil footprint record of avian morphological and behavioral evolution. In: Ulrich, P. K. (Ed.), Trends in ornithology research, pp. 1–63. Hauppauge: Nova Science Publishers.
84. Alexander, R. M. (1976). Estimates of speeds of dinosaurs. Nature, 261, 129–130.
85. Thulborn, R. A. (1982). Speeds and gaits of dinosaurs. Palaeogeography, Palaeoclimatology, Palaeoecology, 38, 227–256.
86. Bishop, P. J., Clemente, C. J., Weems, R. E., Graham, D. F., Lamas, L. P. et al. (2017). Using step width to compare locomotor biomechanics between extinct, non-avian theropod dinosaurs and modern obligate bipeds. Journal of the Royal Society Interface, 14, 20170276.
87. Kubo, T., Benton, M. J. (2009). Tetrapod postural shift estimated from permian and triassic trackways. Palaeontology, 52, 1029–1037.
88. Lallensack, J. N., Falkingham, P. L. (2022). A new method to calculate limb phase from trackways reveals gaits of sauropod dinosaurs. Current Biology, 32, 1635–1640.
89. Falk, A. R. (2011). Tracking Mesozoic birds across the world. Journal of Systematic Palaeontology, 9, 85–90.
90. Xing, L., Lockley, M. G., Jia, C., Klein, H., Niu, K. et al. (2021). Lower cretaceous avian-dominated, theropod, thyreophoran, pterosaur and turtle track assemblages from the Tugulu Group, Xinjiang, China: Ichnotaxonomy and palaeoecology. PeerJ, 9, e11476.
91. Falk, A. R., Lim, J. D., Hasiotis, S. T. (2014). A behavioral analysis of fossil bird tracks from the haman formation (Republic of Korea) shows a nearly modern avian ecosystem. Vertebrata Palasiatica, 52, 129–152.
92. Gatesy, S. M. (1990). Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology, 16, 170–186.
93. Middleton, K. M., Gatesy, S. M. (2000). Theropod forelimb design and evolution. Zoological Journal of the Linnean Society, 128, 149–187.
94. Erdemir, A., McLean, S., Herzog, W., van den Bogert, A. J. (2007). Model-based estimation of muscle forces exerted during movements. Clinical Biomechanics, 22, 131–154.
95. Lin, Y. C., Dorn, T. W., Schache, A. G., Pandy, M. G. (2012). Comparison of different methods for estimating muscle forces in human movement. Proceedings of the Institution of Mechanical Engineers, Part H: Journal of Engineering in Medicine, 226, 103–112.
96. Anderson, F. C., Pandy, M. G. (2001). Static and dynamic optimization solutions for gait are practically equivalent. Journal of Biomechanics, 34, 153–161.
97. Rankin, J. W., Rubenson, J., Hutchinson, J. R. (2016). Inferring muscle functional roles of the ostrich pelvic limb during walking and running using computer optimization. Journal of the Royal Society Interface, 13, 20160035.
98. Bates, K. T., Manning, P. L., Margetts, L., Sellers, W. I. (2010). Sensitivity analysis in evolutionary robotic simulations of bipedal dinosaur running. Journal of Vertebrate Paleontology, 30, 458–466.
99. Sellers, K. C., Middleton, K. M., Davis, J. L., Holliday, C. M. (2017). Ontogeny of bite force in a validated biomechanical model of the American alligator. Journal of Experimental Biology, 220, 2036–2046.
100. Morgan, E. F., Bouxsein, M. L. (2005). Use of finite element analysis to assess bone strength. BoneKEy Osteovision, 2, 8–19.
101. Richmond, B. G., Wright, B. W., Grosse, I., Dechow, P. C., Ross, C. F. et al. (2005). Finite element analysis in functional morphology. Anatomical Record, 283, 259–274.
102. Rayfield, E. J. (2007). Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annual Review of Earth and Planetary Sciences, 35, 541–576.
103. Marcé-Nogué, J., Püschel, T. A., Kaiser, T. M. (2017). A biomechanical approach to understand the ecomorphological relationship between primate mandibles and diet. Scientific Reports, 7, 8364.
104. Wei, X., Zhang, Z. (2021). Femoral mechanical performance of precocial and altricial birds: A simulation study. Avian Research, 12, 18.
Published
2023-09-15
How to Cite
Wei, X., Guo, Y., & Zhao, Y. (2023). Reconstruction of the Hindlimb Locomotion of Confuciusornis (Aves) and Its Implication for the Origin of Avian Flight. Molecular & Cellular Biomechanics, 20(2), 49-61. Retrieved from https://sin-chn.com/index.php/mcb/article/view/55
Issue
Section
Review
Copyright (c) 2023 authors
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright on all articles published in this journal is retained by the author(s), while the author(s) grant the publisher as the original publisher to publish the article.
Articles published in this journal are licensed under a Creative Commons Attribution 4.0 International, which means they can be shared, adapted and distributed provided that the original published version is cited.
Submit a Paper
