Volume 13 Issue 1
Mar.  2022
Turn off MathJax
Article Contents
Xinxin Liang, Mingjie Liu, Chenxi Ying, Zihui Zhang. 2022: Myological variation in the hindlimb of three raptorial birds in relation to foraging behavior. Avian Research, 13(1): 100053. doi: 10.1016/j.avrs.2022.100053
Citation: Xinxin Liang, Mingjie Liu, Chenxi Ying, Zihui Zhang. 2022: Myological variation in the hindlimb of three raptorial birds in relation to foraging behavior. Avian Research, 13(1): 100053. doi: 10.1016/j.avrs.2022.100053

Myological variation in the hindlimb of three raptorial birds in relation to foraging behavior

doi: 10.1016/j.avrs.2022.100053
More Information
  • Corresponding author: E-mail address: zihuizhang@cnu.edu.cn (Z. Zhang)
  • Received Date: 23 Jan 2022
  • Accepted Date: 23 Jul 2022
  • Rev Recd Date: 26 Jun 2022
  • Available Online: 11 Oct 2022
  • Publish Date: 02 Aug 2022
  • Raptors share a common predatory lifestyle, but are different in food preferences and hunting behavior. The grip force and talons' grasping capabilities are fundamentally crucial for subduing and killing their prey to feed, but the abilities and differences to generate force are less known. In this study, the entire pelvic muscles were dissected with the muscle mass and fibre length measured and physiological cross-sectional area counted in the Common Kestrel (Falco tinnunculus), Eurasian Sparrowhawk (Accipiter nisus), and Long-eared Owl (Asio otus). Statistical tests were performed to explore the possible differences in architectural parameters among species. These species were same in distributing the greatest proportion of muscle mass to the shank region and the digital flexor functional group, allocating more than 60% muscle mass in relation to total single leg muscle mass to the same seven individual muscles including flexor digitorum longus (FDL), flexor hallucis longus (FHL), and tibialis cranialis (TC) which are three major muscles responsible for talon closure. Interspecies differentiations were most present in the shank and tarsus instead of other regions of the leg, which might reflect their difference in hunting mode and foot use. Greater force-generation capacity of FHL and some anatomical features suggest that digits 1 and 2 work together as an efficiently vise-like set, playing more critical role than digits 3–4 in foraging of diurnal raptors but to a different degree. In accordance with zygodactyl foot morphology, each digit of the Long-eared Owl plays a subequal role when hunting, evidenced by anatomical and architectural features. Because of its unique insertion to the base of the pygostyle, the striking numerical difference in the development of M. caudofemoralis was possibly related to raptors' flight behavior and feeding ecology. Concluded from anatomical and architectural aspects, the similarities and differences of the hindlimb musculature were correlated to common predatory lifestyle and different foraging behaviors in three raptor species. These results illustrated the underlying myological basis for the functional capacities of the leg muscles and may provide additional information useful in further biomechanical investigation and computer simulation.

     

  • loading
  • Backus, S.B., Sustaita, D., Odhner, L.U., Dollar, A.M., 2015. Mechanical analysis of avian feet: multiarticular muscles in grasping and perching. R Soc Open Sci. 2, 140350. doi: 10.1098/rsos.140350
    Barton, N., Houston, D., 1994. Morphological adaptation of the digestive tract in relation to feeding ecology of raptors. J. Zool. 232, 133–150. doi: 10.1111/j.1469-7998.1994.tb01564.x
    Bates, K.T., Falkingham, P.L., 2018. The importance of muscle architecture in biomechanical reconstructions of extinct animals: a case study using Tyrannosaurus rex. J. Anat. 233, 625-635. doi: 10.1111/joa.12874
    Baumel, J.J., Wilson, J.A., Bergren, D.R., 1990. The ventilatory movements of the avian pelvis and tail: function of the muscles of the tail region of the pigeon (Columba livia). J. Exp. Biol. 151, 263-277. doi: 10.1242/jeb.151.1.263
    Bribiesca-Contreras, F., Parslew, B., Sellers, W.I., 2019. A quantitative and comparative analysis of the muscle architecture of the forelimb myology of diurnal birds of prey (Order Accipitriformes and Falconiformes). Anat. Rec. 302, 1808-1823. doi: 10.1002/ar.24195
    Carril, J., Mosto, M., Picasso, M.B.J., Tambussi, C.P., 2014. Hindlimb myology of the monk parakeet (Aves, Psittaciformes). J. Morphol. 275, 732-744. doi: 10.1002/jmor.20253
    Conroy, R., Weigl, P., Clark, J., Ward, A., 1997. Functional morphology of owl hindlimbs: Implications for prey selection and resource partitioning. Am. Zool. 37, 37A.
    Cracraft, J., 1971. The functional morphology of the hind limb of the domestic pigeon, Columba livia. Bull. Amer. Mus. Nat. Hist. 144, 171-268.
    Csermely, D., Bertè, L., Camoni, R., 1998. Prey killing by Eurasian Kestrels: the role of the foot and the significance of bill and talons. J Avian Biol. 29, 10-16. doi: 10.2307/3677335
    Csermely, D., Gaibani, G., 1998. Is foot squeezing pressure by two raptor species sufficient to subdue their prey? Condor 100, 757-763. doi: 10.2307/1369762
    Csermely, D., Bagni, L., 2003. The predatory behaviour of common kestrels facing various types of prey. J. Ethol. 21, 107-110. doi: 10.1007/s10164-002-0083-6
    Csermely, D., Rossi, O., 2006. Bird claws and bird of prey talons: Where is the difference? Ital. J. Zool. 73, 43-53. doi: 10.1080/11250000500502368
    Einoder, L., Richardson, A., 2006. An ecomorphological study of the raptorial digital tendon locking mechanism. Ibis 148, 515-525. doi: 10.1111/j.1474-919X.2006.00541.x
    Einoder, L., Richardson, A., 2007a. The digital tendon locking mechanism of owls: variation in the structure and arrangement of the mechanism and functional implications. Emu 107, 223-230. doi: 10.1071/MU06019
    Einoder, L., Richardson, A., 2007b. Aspects of the hindlimb morphology of some Australasian birds of prey: a comparative and quantitative study. Auk 124, 773-788. doi: 10.1093/auk/124.3.773
    Falster, D.S., Warton, D.I., Wrigth, I.J., 2006. SMATR: standardised major axis test and rutines, v. 2.0. http://www.bio.mq.edu.au/ecology/SMATR/.
    Fisher, H.I., 1946. Adaptations and comparative anatomy of the locomotor apparatus of New World vultures. Amer. Midl. Nat. 35, 545-727. doi: 10.2307/2421553
    Fisher, H.I., 1957. The function of M. depressor caudae and M. caudofemoralis in pigeons. Auk 74, 479-486. doi: 10.2307/4081747
    Fowler, D.W., Freedman, E.A., Scannella, J.B., 2009. Predatory functional morphology in raptors: interdigital variation in talon size is related to prey restraint and immobilisation technique. PLoS One. 4, e7999. doi: 10.1371/journal.pone.0007999
    Gans, C., 1982. Fiber architecture and muscle function. Exerc. Sport Sci. Rev. 10, 160-207.
    Gatesy, S.M., Dial, K.P., 1993. Tail muscle activity patterns in walking and flying pigeons (Columba livia). J. Exp. Biol. 176, 55-76. doi: 10.1242/jeb.176.1.55
    Goslow, G.E., 1971. The attack and strike of some North American raptors. Auk 88, 815-827. doi: 10.2307/4083840
    Goslow, G.E., 1972. Adaptive mechanisms of the raptor pelvic limb. Auk 89, 47-64. doi: 10.2307/4084059
    Hayward, G.D., Garton, E.O., 1988. Resource partitioning among forest owls in the river of No Return Wilderness, Idaho. Oecologia 75, 253-265. doi: 10.1007/BF00378606
    Hertel, F., 1994. Diversity in body size and feeding morphology within past and present vulture assemblages. Ecology 75, 1074-1084. doi: 10.2307/1939431
    Hertel, F., 1995. Ecomorphological indicators of feeding behavior in recent and fossil raptors. Auk 112, 890-903. doi: 10.2307/4089021
    Hertel, F., Maldonado, J.E., Sustaita, D., 2015. Wing and hindlimb myology of vultures and raptors (Accipitriformes) in relation to locomotion and foraging. Acta Zool. 96, 283-295. doi: 10.1111/azo.12074
    Hudson, G.E., 1948. Studies on the muscles of the pelvic appendage in birds II: The heterogeneous order Falconiformes. Amer. Midl. Nat. 39, 102-127. doi: 10.2307/2421432
    Jollie, M., 1977. A contribution to the morphology and phylogeny of the Falconiformes, Parts II and III. Evol. Theor. 2, 115-300.
    Lieber, R.L., Fridén, J., 2000. Functional and clinical significance of skeletal muscle architecture. Muscle Nerve 23, 1647-1666. doi: 10.1002/1097-4598(200011)23:11<1647::AID-MUS1>3.0.CO;2-M
    Lo Coco, G.E., Motta, M.J., Mosto, M.C., Picasso, M.B.J., 2020. Wing and tail myology of Tyto furcata (Aves, Tytonidae). J. Morphol. 281, 450-464. doi: 10.1002/jmor.21111
    Madan, M.A., Rayfield, E.J., Bright, J.A., 2017. Scaling and functional morphology in strigiform hind limbs. Sci Rep. 7, 44920. doi: 10.1038/srep44920
    Marti, C., 1974. Feeding ecology of four sympatric owls. Condor 76, 45-61. doi: 10.2307/1365983
    McClure, C., Westrip, J., Johnson, J., Schulwitz, S., Virani, M.Z., Davies, R., et al., 2018. State of the world's raptors: Distributions, threats, and conservation recommendations. Biol Conserv. 227, 390-402. doi: 10.1016/j.biocon.2018.08.012
    Mendez, J., Keys, A., 1960. Density and composition of mammalian muscle. Metabolism 9, 184-188.
    Mosto, M.C., Picasso, M.B.J., Montes, M.M., Krone, O., 2020. Tail myology and flight behaviour: Differences between caracaras, falcons and forest falcons (Aves, Falconiformes). Acta Zool. 101, 292-301. doi: 10.1111/azo.12294
    Mosto, M.C., Carril, J., Picasso, M.B.J., 2013. The hindlimb myology of Milvage Chimango (Polyborinae, Falconidae). J. Morphol. 274, 1191-1201. doi: 10.1002/jmor.20172
    Mosto, M.C., 2017a. Comparative hindlimb myology within the family Falconidae. Zoomorphology 136, 241-250. doi: 10.1007/s00435-017-0343-1
    Mosto, M.C., 2017b. The hindlimb myology of Tyto alba (Tytonidae, Strigiformes, Aves). Anat. Histol. Embryol. 46, 25-32. doi: 10.1111/ahe.12227
    Riegert, J., Lövy, M., Fainová, D., 2009. Diet composition of Common Kestrels (Falco tinnunculus) and Long-eared Owls (Asio otus) coexisting in an urban environment. Ornis Fenn. 86, 123-130.
    Rosen, M., Hedenstrom, A., 2002. Soaring flight in the Eleonora's Falcon (Falco eleonorae). Auk 119, 835-840. doi: 10.1093/auk/119.3.835
    Sharir, A., Milgram, J., Shahar, R., 2006. Structural and functional anatomy of the neck musculature of the dog (Canis familiaris). J. Anat. 208, 331-351. doi: 10.1111/j.1469-7580.2006.00533.x
    Smith, N.C., Wilson, A.M., Jespers, K.J., Payne, R.C. 2006. Muscle architecture and functional anatomy of the pelvic limb of the ostrich (Struthio camelus). J. Anat. 209, 765-779. doi: 10.1111/j.1469-7580.2006.00658.x
    Sun, Y., Si, G., Wang, X., Wang, K., Zhang, Z., 2018. Geometric morphometric analysis of skull shape in the Accipitridae. Zoomorphology 137, 445-456. doi: 10.1007/s00435-018-0406-y
    Sustaita, D., 2008. Musculoskeletal underpinnings to differences in killing behavior between North American accipiters (Falconiformes: Accipitridae) and falcons (Falconidae). J. Morphol. 269, 283-301. doi: 10.1002/jmor.10577
    Sustaita, D., Hertel, F., 2010. In vivo bite and grip forces, morphology and prey-killing behavior of North American accipiters (Accipitridae) and falcons (Falconidae). J. Exp. Biol. 213, 2617-2628. doi: 10.1242/jeb.041731
    Swaddle, J.P., Lockwood, R., 1998. Morphological adaptations to predation in passerines. J. Avian Biol. 29, 172-176. doi: 10.2307/3677195
    Tsang, L.R., McDonald, P.G., 2019. A comparative study of avian pes morphotypes, and the functional implications of Australian raptor pedal flexibility. Emu 119, 14-23. doi: 10.1080/01584197.2018.1483203
    Tsang, L.R., Wilson, L., Ledogar, J., Wroe, S., Attard, M., Sansalone, G., 2019. Raptor talon shape and biomechanical performance are controlled by relative prey size but not by allometry. Sci. Rep. 9, 7076. doi: 10.1038/s41598-019-43654-0
    Vanden Berge, J.C., Zweers, G.A., 1993. Myologia. In: Baumel, J.J., King, A.S., Breazile, J.E., Evans, H.E., Vanden Berge, J.C. (Eds. ), Handbook of Avian Anatomy: Nomina Anatomica Avium. Nuttall Ornithological Club, Cambridge, pp. 189-247.
    Videler, J.J., Weihs, D., Daan, S., 1983. Intermittent gliding in the hunting flight of the kestrel, Falco tinnunculus. J. Exp. Biol. 102, 1-12. doi: 10.1242/jeb.102.1.1
    Volkov, S.V., 2004. The hindlimb musculature of the true owls (Strigidae: Strigiformes): morphological peculiarities and general adaptations. Ornithologia 31, 154-174.
    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. Anat. Rec. 304, 2841-2855. doi: 10.1002/ar.24609
    Wang, X.B., Zhang, Z.H., 2020. Skeletal morphology study on distal hind limb about some birds of prey. J. Capital Normal Univ. Nat. Sci. Ed. 41, 28-34. (in Chinese with English abstract).
    Ward, A.B., Weigl, P.D., Conroy, R.M., 2002. Functional morphology of raptor hindlimbs: implications for resource partitioning. Auk 119, 1052-1063. doi: 10.1093/auk/119.4.1052
    Yang, Y., Wang, H., Zhang, Z., 2015. Muscle architecture of the forelimb of the Golden Pheasant (Chrysolophus pictus) (Aves: Phasianidae) and its implications for functional capacity in flight. Avian Res. 6, 3. doi: 10.1186/s40657-015-0013-2
    Zawadzka, D., Zawadzki, J., 2001. Breeding populations and diets of the Sparrowhawk Accipiter nisus and the Hobby Falco subbuteo in the Wigry National Park (NE Poland). Acta Ornithol. 36, 25-31. doi: 10.3161/068.036.0111
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(6)

    Article Metrics

    Article views (140) PDF downloads(4) Cited by()
    Proportional views

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return