Xinsen Wei, Zihui Zhang. 2021: Femoral mechanical performance of precocial and altricial birds: a simulation study. Avian Research, 12(1): 18. DOI: 10.1186/s40657-021-00253-w
Citation: Xinsen Wei, Zihui Zhang. 2021: Femoral mechanical performance of precocial and altricial birds: a simulation study. Avian Research, 12(1): 18. DOI: 10.1186/s40657-021-00253-w

Femoral mechanical performance of precocial and altricial birds: a simulation study

Funds: 

National Natural Science Foundation of China 31471951

More Information
  • Corresponding author:

    Zihui Zhang, zihuizhang@cnu.edu.cn

  • Received Date: 04 Jan 2021
  • Accepted Date: 17 Apr 2021
  • Available Online: 24 Apr 2022
  • Publish Date: 23 Apr 2021
  • Background 

    As the major load-bearing structures, bones exhibit various properties related to mechanical performance to adapt to different locomotor intensities. The habits and ontogenetic changes of locomotion in animals can, thus, be explored by assessing skeletal mechanical performance.

    Methods 

    In this study, we investigated the growing femoral mechanical performance in an ontogenetic series of Cabot's Tragopans (Tragopan caboti) and Pigeons (Columba livia domestica). Micro-computed tomography-based finite element analysis was conducted to evaluate the stress, strain, and strain energy density (SED) of femora under axial and radial loading.

    Results 

    Femora deflected medio-laterally and dorso-ventrally under axial and radial loading, respectively. Femora deformed and tensed more severely under radial loading than axial loading. In adult individuals, Cabot's Tragopans had lower strain and SED than pigeons. During ontogeny, the strain and SED of pigeons decreased sharply, while Cabot's Tragopans showed moderately change. The structural properties of hatchling pigeons are more robust than those of hatchling Cabot's Tragopans.

    Conclusions 

    Limb postures have dominant effect on skeletal deformation. The erect posture is preferred by large mammals and birds to achieve a high safety factor of bones during locomotion. Adult Cabot's Tragopans have stronger femora than pigeons, reflecting a better bone adaption to the terrestrial locomotion of the studied pheasant species. Changes in strain and SED during growth reflect the marked difference in locomotor ability between precocial and altricial hatchlings. The femora of hatchling Cabot's Tragopans were built with better energy efficiency than deformation resistance, enabling optimized mechanical performance. In contrast, although weak in mechanical function at the time of hatching, pigeon femora were suggested to be established with a more mature structural design as a prerequisite for rapid growth. These results will be helpful for studies regarding developmental patterns of fossil avian species.

  • Correction to: Avian Res (2021) 12:19

    https://doi.org/10.1186/s40657-021-00254-9

    Following publication of the original article (Hou et al. 2021), the authors identified an error in Fig. 1. The correct figure is given below.

    Figure  1.  The experiment design in this study

    The original article (Hou et al. 2021) has been updated.

  • Abourachid A, Hackert R, Herbin M, Libourel PA, Lambert F, Gioanni H, et al. Bird terrestrial locomotion as revealed by 3D kinematics. Zoology. 2011;114: 360–8.
    Alexander RM. Principles of animal locomotion. Princeton: Princeton University Press; 2003.
    Alexander RM, Jayes AS, Maloiy GMO, Wathuta EM. Allometry of the limb bones of mammals from shrews (Sorex) to elephant (Loxodonta). J Zool. 1979a;189: 305–14.
    Alexander RM, Maloiy GMO, Njau R, Jayes AS. Mechanics of running of the ostrich (Struthio camelus). J Zool. 1979b;187: 169–78.
    Alexander RM, Ker RF, Bennett MB. Optimum stiffness for leg bones. J Zool. 1990;222: 471–8.
    Arias-Moreno AJ, Ito K, van Rietbergen B. Accuracy of beam theory for estimating bone tissue modulus and yield stress from 3-point bending tests on rat femora. J Biomech. 2020;101: 109654.
    Biewener AA. Bone strength in small mammals and bipedal birds: do safety factors change with body size? J Exp Biol. 1982;98: 289–301.
    Biewener AA. Scaling body support in mammals: limb posture and muscle mechanics. Science. 1989;245: 45–8.
    Biewener AA. Biomechanical consequences of scaling. J Exp Biol. 2005;208: 1665–76.
    Biewener AA, Taylor CR. Bone strain: a determinant of gait and speed? J Exp Biol. 1986;123: 383–400.
    Biewener AA, Swartz SM, Bertram JE. Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus. Calcif Tissue Int. 1986;39: 390–5.
    Bishop PJ, Hocknull SA, Clemente CJ, Hutchinson JR, Barrett RS, Lloyd DG. Cancellous bone and theropod dinosaur locomotion Part II—a new approach to inferring posture and locomotor biomechanics in extinct tetrapod vertebrates. PeerJ. 2018;6: e5779.
    Carrier DR. Ontogenetic limits on locomotor performance. Physiol Zool. 1996;69: 467–88.
    Carrier DR, Auriemma J. A developmental constraint on the fledging time of birds. Biol J Linn Soc. 1992;47: 61–77.
    Carrier DR, Leon LR. Skeletal growth and function in the California gull (Larus californicus). J Zool. 1990;222: 375–89.
    Carter DR. Mechanical loading histories and cortical bone remodeling. Calcif Tissue Int. 1984;36(Suppl 1): S19-24.
    Carter DR, Fyhrie DP, Whalen RT. Trabecular bone density and loading history: regulation of connective tissue biology by mechanical energy. J Biomech. 1987;20: 785–94.
    Clark J, Alexander RM. Mechanics of running by quail (Coturnix). J Zool. 1975;176: 87–113.
    Cosman MN, Britz HM, Rolian C. Selection for longer limbs in mice increases bone stiffness and brittleness, but does not alter bending strength. J Exp Biol. 2019.
    Cracraft JL. The functional morphology of the hind limb of the domestic pigeon, Columba livia. Bull Am Mus Nat Hist. 1971;144: 171–268.
    Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33: 744–50.
    Currey JD. What determines the bending strength of compact bone? J Exp Biol. 1999;202: 2495–503.
    Currey JD. Bones: structure and mechanics. Princeton: Princeton University Press; 2002.
    Currey JD. How well are bones designed to resist fracture. J Bone Miner Res. 2003;18: 591–8.
    Dial KP, Greene E, Irschick DJ. Allometry of behavior. Trends Ecol Evol. 2008;23: 394–401.
    Doblaré M, Garcı́a JM, Gómez MJ. Modelling bone tissue fracture and healing: a review. Eng Fract Mech. 2004;71: 1809–40.
    Doube M, Kłosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone. 2010;47: 1076–9.
    Dumont ER, Grosse IR, Slater GJ. Requirements for comparing the performance of finite element models of biological structures. J Theor Biol. 2009;256: 96–103.
    Eberle S, Göttlinger M, Augat P. Individual density-elasticity relationships improve accuracy of subject-specific finite element models of human femurs. J Biomech. 2013;46: 2152–7.
    Erickson GM, Catanese J III, Keaveny TM. Evolution of the biomechanical material properties of the femur. Anat Rec. 2002;268: 115–24.
    Gatesy SM. Guineafowl hind limb function. I: cineradiographic analysis and speed effects. J Morphol. 1999;240: 115–25.
    Gere JM. Mechanics of materials. Pacific Grove: Brooks/Cole Thomson Learning; 2001.
    Goetz JE, Derrick TR, Pedersen DR, Robinson DA, Conzemius MG, Baer TE, et al. Hip joint contact force in the emu (Dromaius novaehollandiae) during normal level walking. J Biomech. 2008;41: 770–8.
    Hedenström A, Rosén M. Predator versus prey: on aerial hunting and escape strategies in birds. Behav Ecol. 2001;12: 150–6.
    Helgason B, Perilli E, Schileo E, Taddei F, Brynjólfsson S, Viceconti M. Mathematical relationships between bone density and mechanical properties: a literature review. Clin Biomech. 2008;23: 135–46.
    Herrel A, Gibb AC. Ontogeny of performance in vertebrates. Physiol Biochem Zool. 2006;79: 1–6.
    Jepsen KJ, Silva MJ, Vashishth D, Guo XE, van der Meulen MC. Establishing biomechanical mechanisms in mouse models: practical guidelines for systematically evaluating phenotypic changes in the diaphyses of long bones. J Bone Miner Res. 2015;30: 951–66.
    Main RP, Biewener AA. Skeletal strain patterns and growth in the emu hindlimb during ontogeny. J Exp Biol. 2007;210: 2676–90.
    Morgan EF, Bouxsein ML. Use of finite element analysis to assess bone strength. BoneKEy-Osteovision. 2005;2: 8–19.
    Olea G, Hernando A, Lombardo D. Heterochronic events in the ontogeny of Columba livia, Coturnix coturnix and Gallus gallus domesticus. Rev Colomb Cienc Pecu. 2016;29: 274–82.
    Pelker RR, Friedlaender GE, Markham TC, Panjabi MM, Moen CJ. Effects of freezing and freeze-drying on the biomechanical properties of rat bone. J Orthop Res. 1984;1: 405–11.
    Rayfield EJ. Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annu Rev Earth Planet Sci. 2007;35: 541–76.
    Rayfield EJ. What does musculoskeletal mechanics tell us about evolution of form and function in vertebrates? In: Bels V, Whishaw I, editors. Feeding in vertebrates. Berlin: Springer; 2019. p. 45–70.
    Ricklefs RE. Adaptation, constraint, and compromise in avian postnatal development. Biol Rev Camb Philos Soc. 1979a;54: 269–90.
    Ricklefs RE. Patterns of growth in birds. V. A comparative study of development in the starling, common tern, and Japanese quail. Auk. 1979b;96: 10–30.
    Ruff CB, Holt B, Trinkaus E. Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation. Am J Phys Anthropol. 2006;129: 484–98.
    Stoessel A, Fischer MS. Comparative intralimb coordination in avian bipedal locomotion. J Exp Biol. 2012;215: 4055–69.
    Wang L, Wei XS, Liang XX, Zhang ZH. Ontogenetic changes of hindlimb muscle mass in Cabot's tragopan (Galliformes, Phasianidae) and their functional implications. Anat Rec. 2021.
    Wei X, Zhang Z. Ontogenetic changes of geometrical and mechanical characteristics of the avian femur: a comparison between precocial and altricial birds. J Anat. 2019;235: 903–11.
    Wen Z, Zheng G. Artificial raising and breeding of Cabot's Tragopan (Tragopan caboti). Chin J Zool. 1998;33: 22–7 (in Chinese).
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