The aero body righting of frog Rana rugulosus via hindleg swings.
Rana rugulosus
biomechanics
hindleg air-righting
jumping kinematics
Journal
Journal of experimental zoology. Part A, Ecological and integrative physiology
ISSN: 2471-5646
Titre abrégé: J Exp Zool A Ecol Integr Physiol
Pays: United States
ID NLM: 101710204
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
25
06
2022
received:
10
01
2022
accepted:
27
06
2022
pubmed:
12
7
2022
medline:
21
9
2022
entrez:
11
7
2022
Statut:
ppublish
Résumé
Frogs can keep an excellent aerial balance for landing and achieve consecutive jumps reliably. A safe landing requires an accurate body righting in the air. However, there is no systematic study on how the frogs adjust the aerial postures and body attitudes after jumping. The stretched long hindlegs swung quickly in the aerial phase, which revealed a clear relationship with the body attitudes. This study aimed to verify the function of frogs' hindlegs on aero body righting in the air. We captured the motions of both hindlegs and found the hindlegs adopted two movement modes, the bilateral parallel, and separated swings. The hindleg-induced torques by the two movements were negatively correlated with the body's angular accelerations on pitch and roll, respectively. Moreover, an analytical model was derived based on the conservation of angular momentum and verified by the dynamic simulations. Thus, we confirmed that the hindlegs are the dominant mechanism in aerial pitch and roll controls. We anticipate our achievements to inspire the design of air-righting tools.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
823-834Subventions
Organisme : National Natural Science Foundation of China
ID : 51905120
Organisme : Shenzhen Science and Technology Innovation Program
ID : RCBS20210609103901011
Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Azizi, E., & Abbott, E. M. (2013). Anticipatory motor patterns limit muscle stretch during landing in toads. Biology Letters, 9(1), 20121045. https://doi.org/10.1098/rsbl.2012.1045
Azizi, E., Larson, N. P., Abbott, E. M., & Danos, N. (2014). Reduce torques and stick the landing: Limb posture during landing in toads. Journal of Experimental Biology, 217(Pt 20), 3742-3747. https://doi.org/10.1242/jeb.108506
Ekstrom, L. J., & Gillis, G. B. (2015). Pre-landing wrist muscle activity in hopping toads. Journal of Experimental Biology, 218(15), 2410-2415. https://doi.org/10.1242/jeb.113985
Emerson, S. B., & De Jongh, H. J. (1980). Muscle activity at the ilio-sacral articulation of frogs. Journal of Morphology, 166(2), 129-144. https://doi.org/10.1002/jmor.1051660202
Emerson, S. B., & Koehl, M. A. R. (1990). The interaction of behavioral and morphological change in the evolution of a novel locomotor type-Flying frogs. Evolution, 44(8), 1931-1946. https://doi.org/10.2307/2409604
Essner, J. R. L., Suffian, D. J., Bishop, P. J., & Reilly, S. M. (2010). Landing in basal frogs: Evidence of saltational patterns in the evolution of anuran locomotion. Die Naturwissenschaften, 97(10), 935-939. https://doi.org/10.1007/s00114-010-0697-4
Gans, C., & Parsons, T. S. (1966). On the origin of the jumping mechanism in frogs. Evolution, 20(1), 92. https://doi.org/10.2307/2406151
Garant, X., & Gosselin, C. (2021). Design and experimental validation of reorientation manoeuvres for a free falling robot inspired from the cat righting reflex. IEEE Transactions on Robotics, 37(2), 482-493. https://doi.org/10.1109/TRO.2020.3031241
Gillis, G., Ekstrom, L., & Azizi, E. (2014). Biomechanics and control of landing in toads. Integrative and Comparative Biology, 54(6), 1136-1147. https://doi.org/10.1093/icb/icu053
Gillis, G. B., Akella, T., & Gunaratne, R. (2010). Do toads have a jump on how far they hop? Pre-landing activity timing and intensity in forelimb muscles of hopping Bufo marinus. Biology Letters, 6(4), 486-489. https://doi.org/10.1098/rsbl.2009.1005
Gillis, G. B., & Biewener, A. A. (2000). Hindlimb extensor muscle function during jumping and swimming in the toad (Bufo marinus). Journal of Experimental Biology, 203(Pt 23), 3547-3563.
Griep, S., Schilling, N., Marshall, P., Amling, M., Hahne, L. M., & Haas, A. (2013). Pectoral girdle movements and the role of the glenohumeral joint during landing in the toad, Rhinella marina (Linnaeus, 1758). Zoomorphology, 132(3), 325-338. https://doi.org/10.1007/s00435-013-0189-0
James, R. S., & Wilson, R. S. (2008). Explosive jumping: Extreme morphological and physiological specializations of Australian rocket frogs (litorianasuta). Physiological and Biochemical Zoology, 81(2), 176-185. https://doi.org/10.1086/525290
Jusufi, A., Zeng, Y., Full, R. J., & Dudley, R. (2011). Aerial righting reflexes in flightless animals. Integrative and Comparative Biology, 51(6), 937-943. https://doi.org/10.1093/icb/icr114
Kargo, W. J., Nelson, F., & Rome, L. C. (2002). Jumping in frogs: Assessing the design of the skeletal system by anatomically realistic modeling and forward dynamic simulation. Journal of Experimental Biology, 205(12), 1683-1702.
Libby, T., Moore, T. Y., Chang-Siu, E., Li, D., Cohen, D. J., Jusufi, A., & Full, R. J. (2012). Tail-assisted pitch control in lizards, robots and dinosaurs. Nature (London), 481(7380), 181-184. https://doi.org/10.1038/nature10710
Lu, L., Jiaxuan, Z., & Yinfeng, X. (2018). Landing posture adjustment and buffer performance analysis of a cat robot [Conference Paper]. 2018 2nd IEEE Advanced Information Management, Communicates, Electronic and Automation Control Conference (IMCEC) Proceedings. 357-363.
Mai, M. T., & Lieber, R. L. (1990). A model of semitendinosus muscle sarcomere-length, knee and hip-joint interaction in the frog hindlimb. Journal of Biomechanics, 23(3), 271-279. https://doi.org/10.1016/0021-9290(90)90017-W
McKnight, D. T., Nordine, J., Jerrett, B., Murray, M., Murray, P., Moss, R., & Schwarzkopf, L. (2020). Do morphological adaptations for gliding in frogs influence clinging and jumping? Journal of Zoology, 310(1), 55-63. https://doi.org/10.1111/jzo.12725
Nauwelaerts, S., & Aerts, P. (2006). Take-off and landing forces in jumping frogs. Journal of Experimental Biology, 209(1), 66-77. https://doi.org/10.1242/jeb.01969
O'Reilly, J. C., Summers, A. P., & Ritter, D. A. (2000). The evolution of the functional role of trunk muscles during locomotion in adult amphibians. American Zoologist, 40(1), 123-135. https://doi.org/10.1668/0003-1569(2000)040[0123:TEOTFR]2.0.CO;2
Olson, J. M., & Marsh, R. L. (1998). Activation patterns and length changes in hindlimb muscles of the bullfrog Rana catesbeiana during jumping. Journal of Experimental Biology, 201(Pt 19), 2763-2777.
Paskins, K. E., Bowyer, A., Megill, W. M., & Scheibe, J. S. (2007). Take-off and landing forces and the evolution of controlled gliding in Northern flying squirrels Glaucomys sabrinus. Journal of Experimental Biology, 210(8), 1413-1423. https://doi.org/10.1242/jeb.02747
Peplowski, M. M., & Marsh, R. L. (1997). Work and power output in the hindlimb muscles of Cuban tree frogs Osteopilus septentrionalis during jumping. Journal of Experimental Biology, 200(Pt 22), 2861-2870.
Peters, S. E., Kamel, L. T., & Bashor, D. P. (1996). Hopping and swimming in the leopard frog, Rana pipiens. 1. Step cycles and kinematics. Journal of Morphology, 230(1), 1-16. https://doi.org/10.1002/(SICI)1097-4687(199610)230:1%3C1::AID-JMOR1%3E3.0.CO;2-N
Porro, L. B., Collings, A. J., Eberhard, E. A., Chadwick, K. P., & Richards, C. T. (2017). Inverse dynamic modelling of jumping in the red-legged running frog Kassina maculata. Journal of Experimental Biology, 220(10), 1882-1893. https://doi.org/10.1242/jeb.155416
Wang, H., Wang, L., Shao, J., Liu, T., & Dai, Z. (2013). Long hindlimbs contribute to air-righting performance in falling tree frogs. Journal of Mechanics in Medicine and Biology, 13(6SI), 1340023. https://doi.org/10.1142/S021951941340023X
Wang, Z., Ji, A., Endlein, T., Samuel, D., Yao, N., Wang, Z., & Dai, Z. (2014). The role of fore- and hindlimbs during jumping in the Dybowski's frog (Rana dybowskii). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 321(6), 324-333. https://doi.org/10.1002/jez.1865
Xiao, J., Lin, F., Li, Y., Li, B., & Yang, X. (2021). On the kinematics of forelimb landing of frog Rana rugulosus. Journal of Biomechanics, 121, 110417. https://doi.org/10.1016/j.jbiomech.2021.110417
Zhang, Z., Yang, J., & Yu, H. (2014). Effect of flexible back on energy absorption during landing in cats: A biomechanical investigation. Journal of Bionic Engineering, 11(4), 506-516. https://doi.org/10.1016/S1672-6529(14)60063-9
Zhang, Z., Zhao, J., Chen, H., & Chen, D. (2017). A survey of bioinspired jumping robot: Takeoff, air posture adjustment, and landing buffer. Applied Bionics and Biomechanics, 2017, 1-22. https://doi.org/10.1155/2017/4780160
Zhao, J., Zhao, T., Xi, N., Mutka, M. W., & Xiao, L. (2015). MSU tailbot: Controlling aerial maneuver of a miniature-tailed jumping robot. IEEE-ASME Transactions on Mechatronics, 20(6), 2903-2914. https://doi.org/10.1109/TMECH.2015.2411513
Zhen, S., Huang, K., Zhao, H., & Chen, Y. (2015). Why can a free-falling cat always manage to land safely on its feet? Nonlinear Dynamics, 79(4), 2237-2250. https://doi.org/10.1007/s11071-014-1741-2