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Proceedings. Biological sciences2016; 283(1843); 20161908; doi: 10.1098/rspb.2016.1908

Timing of head movements is consistent with energy minimization in walking ungulates.

Abstract: Many ungulates show a conspicuous nodding motion of the head when walking. Until now, the functional significance of this behaviour remained unclear. Combining in vivo kinematics of quadrupedal mammals with a computer model, we show that the timing of vertical displacements of the head and neck is consistent with minimizing energy expenditure for carrying these body parts in an inverted pendulum walking gait. Varying the timing of head movements in the model resulted in increased metabolic cost estimate for carrying the head and neck of up to 63%. Oscillations of the head-neck unit result in weight force oscillations transmitted to the forelimbs. Advantageous timing increases the load in single support phases, in which redirecting the trajectory of the centre of mass (COM) is thought to be energetically inexpensive. During double support, in which-according to collision mechanics-directional changes of the impulse of the COM are expensive, the observed timing decreases the load. Because the head and neck comprise approximately 10% of body mass, the effect shown here should also affect the animals' overall energy expenditure. This mechanism, working analogously in high-tech backpacks for energy-saving load carriage, is widespread in ungulates, and provides insight into how animals economize locomotion.
© 2016 The Author(s).
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Publication Date: 2016-12-03 PubMed ID: 27903873PubMed Central: PMC5136594DOI: 10.1098/rspb.2016.1908Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article focuses on the rhythmic head movement in ungulates (hoofed mammals) during walking. The study reveals that this head bobbing serves to minimize their energy expenditure, much like the mechanics seen in high-tech energy-saving backpacks.

Objective and Methods

  • The overarching objective of this research was to understand the functional significance of nodding motions, a common phenomenon observed in ungulates when they walk. To address this, the researchers combined in vivo kinematics data from quadrupedal mammals with a computer-generated model.
  • The focus was mainly on the timing of vertical displacements of the head and neck in accordance with the energy minimization theory in an inverted pendulum walking gait.

Findings

  • The researchers discovered that altering the timing of head movements resulted in increased estimated metabolic cost for carrying the head and neck, which could go up to 63%. This indicates that the head-necks’ systematic oscillations work to optimize energy use.
  • These oscillations also result in weight force fluctuations that are transmitted to the forelimbs. When the load on single support phases increases due to the favorable timing, it redirects the trajectory of the centre of mass (COM), which according to the study is energetically efficient.
  • Conversely, during double support phases, which are considered more energetically expensive due to directional changes of the COM impulse according to collision mechanics, the observed timing decreases the load.

Conclusions and Implications

  • The team concluded that since the head and neck constitute nearly 10% of the body mass, the mechanism they pinpointed has a significant impact on the animals’ overall energy expenditure.
  • This study sheds light on how animals economize locomotion, which can be instrumental in the fields of animal physiology and biomechanics.
  • Moreover, the insight into this natural mechanism, which works similar to high-tech backpacks designed for energy-saving load carriage, could potentially be leveraged in designing more efficient load-bearing equipment in the future.

Cite This Article

APA
Loscher DM, Meyer F, Kracht K, Nyakatura JA. (2016). Timing of head movements is consistent with energy minimization in walking ungulates. Proc Biol Sci, 283(1843), 20161908. https://doi.org/10.1098/rspb.2016.1908

Publication

Proceedings. Biological sciences
ISSN: 1471-2954
NlmUniqueID: 101245157
Country: England
Language: English
Volume: 283
Issue: 1843
PII: 20161908

Researcher Affiliations

Loscher, David M
  • AG Humanbiologie, Department of Biology, Freie Universität Berlin, Albrecht-Thaer-Weg 6, 14195 Berlin, Germany.
Meyer, Fiete
  • FG Mechatronische Maschinendynamik, Department of Mechanics, Einsteinufer 5, Technische Universität Berlin, 10587 Berlin, Germany.
Kracht, Kerstin
  • PAConsult GmbH, Environmental and Structural Dynamics Test Lab, Birkenau 3, 22087 Hamburg, Germany.
Nyakatura, John A
  • AG Morphologie und Formengeschichte, Image Knowledge Gestaltung: an interdisciplinary laboratory, Institute of Biology, Humboldt University, Philippstraße 13, 10115 Berlin, Germany john.nyakatura@hu-berlin.de.

MeSH Terms

  • Animals
  • Biomechanical Phenomena
  • Energy Metabolism
  • Gait
  • Head Movements
  • Horses / physiology
  • Walking

References

This article includes 47 references
  1. Berry HH, Siegfried WR, Crowe TM. Activity patterns in a population of free-ranging wildebeest Connochaetes taurinus at Etosha National Park. Z. Tierpsychol. 59, 229–246, 1982.
    doi: 10.1111/j.1439-0310.1982.tb00340.xgoogle scholar: lookup
  2. Boyd L, Carbonaro D, Houpt K. The 24-hour time budget of Przewalski horses. Appl. Anim. Behav. Sci. 21, 5–17, 1988.
    doi: 10.1016/0168-1591(88)90098-6google scholar: lookup
  3. Neuhaus P, Ruckstuhl KE. Foraging behaviour in Alpine ibex (Capra ibex): consequences of reproductive status, body size, age and sex. Ethol. Ecol. Evol. 14, 373–381, 2002.
    doi: 10.1080/08927014.2002.9522738google scholar: lookup
  4. Lachica M, Aguilera JF. Energy expenditure of walk in grassland for small ruminants. Small Rumin. Res. 59, 105–121, 2005.
    doi: 10.1016/j.smallrumres.2005.05.002google scholar: lookup
  5. Lin L, Dickhoefer U, Müller K, Susenbeth A. Grazing behavior of sheep at different stocking rates in the Inner Mongolian steppe, China. Appl. Anim. Behav. Sci. 129, 36–42, 2011.
    doi: 10.1016/j.applanim.2010.11.002google scholar: lookup
  6. Arnold W, Ruf T, Kuntz R. Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) II. Energy expenditure.. J Exp Biol 2006 Nov;209(Pt 22):4566-73.
    doi: 10.1242/jeb.02536pubmed: 17079726google scholar: lookup
  7. Scantlebury DM, Mills MG, Wilson RP, Wilson JW, Mills ME, Durant SM, Bennett NC, Bradford P, Marks NJ, Speakman JR. Mammalian energetics. Flexible energetics of cheetah hunting strategies provide resistance against kleptoparasitism.. Science 2014 Oct 3;346(6205):79-81.
    doi: 10.1126/science.1256424pubmed: 25278609google scholar: lookup
  8. Gorman ML, Mills MGL, Raath JP, Speakman JR. High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 391, 479–481, 1998.
    doi: 10.1038/35131google scholar: lookup
  9. Nyakatura JA, Andrada E. On vision in birds: coordination of head-bobbing and gait stabilises vertical head position in quail.. Front Zool 2014 Mar 25;11(1):27.
    doi: 10.1186/1742-9994-10-27pmc: PMC3987125pubmed: 24666790google scholar: lookup
  10. Gellman KS, Bertram JEA. The equine nuchal ligament 1, structural and material properties. Vet. Comp. Orthop. Traumatol. 15, 1–6, 2002.
  11. Gellman KS, Bertram JEA. The equine nuchal ligament 2, passive dynamic energy exchange in locomotion. Vet. Comp. Orthop. Traumatol. 15, 7–14, 2002.
  12. Hirasaki E, Kumakura H. Head movements during locomotion in a gibbon and Japanese macaques.. Neuroreport 2004 Mar 22;15(4):643-7.
    doi: 10.1097/00001756-200403220-00014pubmed: 15094468google scholar: lookup
  13. Dunbar DC. Stabilization and mobility of the head and trunk in vervet monkeys (Cercopithecus aethiops) during treadmill walks and gallops.. J Exp Biol 2004 Dec;207(Pt 25):4427-38.
    doi: 10.1242/jeb.01282pubmed: 15557028google scholar: lookup
  14. Dunbar DC, Macpherson JM, Simmons RW, Zarcades A. Stabilization and mobility of the head, neck and trunk in horses during overground locomotion: comparisons with humans and other primates.. J Exp Biol 2008 Dec;211(Pt 24):3889-907.
    doi: 10.1242/jeb.020578pmc: PMC2768006pubmed: 19043061google scholar: lookup
  15. Nauwelaerts S, Clayton HM. Changes in trunk shape and center of mass location in horses during walking. Vet. Med. Aus. 97, 81–86, 2010.
  16. Buchner HH, Savelberg HH, Schamhardt HC, Barneveld A. Head and trunk movement adaptations in horses with experimentally induced fore- or hindlimb lameness.. Equine Vet J 1996 Jan;28(1):71-6.
    doi: 10.1111/j.2042-3306.1996.tb01592.xpubmed: 8565958google scholar: lookup
  17. Fedak MA, Heglund NC, Taylor CR. Energetics and mechanics of terrestrial locomotion. II. Kinetic energy changes of the limbs and body as a function of speed and body size in birds and mammals.. J Exp Biol 1982 Apr;97:23-40.
    pubmed: 7086342doi: 10.1242/jeb.97.1.23google scholar: lookup
  18. Buchner HH, Savelberg HH, Schamhardt HC, Barneveld A. Inertial properties of Dutch Warmblood horses.. J Biomech 1997 Jun;30(6):653-8.
    doi: 10.1016/S0021-9290(97)00005-5pubmed: 9165402google scholar: lookup
  19. Donelan JM, Kram R, Kuo AD. Mechanical work for step-to-step transitions is a major determinant of the metabolic cost of human walking.. J Exp Biol 2002 Dec;205(Pt 23):3717-27.
    pubmed: 12409498doi: 10.1242/jeb.205.23.3717google scholar: lookup
  20. Donelan JM, Kram R, Kuo AD. Simultaneous positive and negative external mechanical work in human walking.. J Biomech 2002 Jan;35(1):117-24.
    doi: 10.1016/S0021-9290(01)00169-5pubmed: 11747890google scholar: lookup
  21. Kuo AD, Donelan JM, Ruina A. Energetic consequences of walking like an inverted pendulum: step-to-step transitions.. Exerc Sport Sci Rev 2005 Apr;33(2):88-97.
    doi: 10.1097/00003677-200504000-00006pubmed: 15821430google scholar: lookup
  22. Ruina A, Bertram JE, Srinivasan M. A collisional model of the energetic cost of support work qualitatively explains leg sequencing in walking and galloping, pseudo-elastic leg behavior in running and the walk-to-run transition.. J Theor Biol 2005 Nov 21;237(2):170-92.
    doi: 10.1016/j.jtbi.2005.04.004pubmed: 15961114google scholar: lookup
  23. Srinivasan M, Ruina A. Computer optimization of a minimal biped model discovers walking and running.. Nature 2006 Jan 5;439(7072):72-5.
    doi: 10.1038/nature04113pubmed: 16155564google scholar: lookup
  24. Kuo AD. The six determinants of gait and the inverted pendulum analogy: A dynamic walking perspective.. Hum Mov Sci 2007 Aug;26(4):617-56.
    doi: 10.1016/j.humov.2007.04.003pubmed: 17617481google scholar: lookup
  25. Bertram JE, Hasaneini SJ. Neglected losses and key costs: tracking the energetics of walking and running.. J Exp Biol 2013 Mar 15;216(Pt 6):933-8.
    doi: 10.1242/jeb.078543pubmed: 23447662google scholar: lookup
  26. Usherwood JR, Williams SB, Wilson AM. Mechanics of dog walking compared with a passive, stiff-limbed, 4-bar linkage model, and their collisional implications.. J Exp Biol 2007 Feb;210(Pt 3):533-40.
    doi: 10.1242/jeb.02647pubmed: 17234623google scholar: lookup
  27. Lee DV, Bertram JE, Anttonen JT, Ros IG, Harris SL, Biewener AA. A collisional perspective on quadrupedal gait dynamics.. J R Soc Interface 2011 Oct 7;8(63):1480-6.
    doi: 10.1098/rsif.2011.0019pmc: PMC3163420pubmed: 21471189google scholar: lookup
  28. Lee DV, Biewener AA. BigDog-inspired studies in the locomotion of goats and dogs.. Integr Comp Biol 2011 Jul;51(1):190-202.
    doi: 10.1093/icb/icr061pubmed: 21659392google scholar: lookup
  29. Kuo AD. Biophysics. Harvesting energy by improving the economy of human walking.. Science 2005 Sep 9;309(5741):1686-7.
    doi: 10.1126/science.1118058pubmed: 16151001google scholar: lookup
  30. Rome LC, Flynn L, Yoo TD. Biomechanics: rubber bands reduce the cost of carrying loads.. Nature 2006 Dec 21;444(7122):1023-4.
    doi: 10.1038/4441023apubmed: 17183310google scholar: lookup
  31. Gellman KS, Bertram JE, Hermanson JW. Morphology, histochemistry, and function of epaxial cervical musculature in the horse (Equus caballus).. J Morphol 2002 Feb;251(2):182-94.
    doi: 10.1002/jmor.1082pubmed: 11748702google scholar: lookup
  32. Dimery NJ, Alexander RM, Deyst KA. Mechanics of the ligamentum nuchae of some artiodactyls. J. Zool. 206, 341–351, 1985.
    doi: 10.1111/j.1469-7998.1985.tb05663.xgoogle scholar: lookup
  33. Bramble DM, Lieberman DE. Endurance running and the evolution of Homo.. Nature 2004 Nov 18;432(7015):345-52.
    doi: 10.1038/nature03052pubmed: 15549097google scholar: lookup
  34. Wang X, Tedford RH. Dogs: their fossil relatives and evolutionary history. p. 219 New York, NY: Columbia University Press, 2008.
  35. Spoor CF, Badoux DM. Descriptive and functional morphology of the neck and forelimb of the striped hyena (Hyaena hyaena, L. 1758).. Anat Anz 1986;161(5):375-87.
    pubmed: 3729006
  36. Spoor CF, Badoux DM. Descriptive and functional morphology of the locomotory apparatus of the spotted hyaena (Crocuta crocuta, Erxleben, 1777).. Anat Anz 1989;168(3):261-6.
    pubmed: 2764282
  37. Tokuriki M, Aoki O. Neck muscle activity in horses during locomotion with and without a rider. In Equine exercise physiology (eds Persson S, Lindholm A, Jeffcott L), pp. 146–150. Davis, CA: ICEEP Publications, 1991.
  38. Robert C, Valette JP, Denoix JM. Surface electromyographic analysis of the normal horse locomotion: a preliminary report. In Conf. on Equine Sports Medicine and Science (eds Lindnor A), 1998.
  39. Zsoldos RR, Kotschwar AB, Kotschwar A, Groesel M, Licka T, Peham C. Electromyography activity of the equine splenius muscle and neck kinematics during walk and trot on the treadmill.. Equine Vet J Suppl 2010 Nov;(38):455-61.
    doi: 10.1111/j.2042-3306.2010.00263.xpubmed: 21059045google scholar: lookup
  40. Farley CT, Blickhan R, Saito J, Taylor CR. Hopping frequency in humans: a test of how springs set stride frequency in bouncing gaits.. J Appl Physiol (1985) 1991 Dec;71(6):2127-32.
    pubmed: 1778902doi: 10.1152/jappl.1991.71.6.2127google scholar: lookup
  41. Farley CT, González O. Leg stiffness and stride frequency in human running.. J Biomech 1996 Feb;29(2):181-6.
    doi: 10.1016/0021-9290(95)00029-1pubmed: 8849811google scholar: lookup
  42. Granata KP, Padua DA, Wilson SE. Gender differences in active musculoskeletal stiffness. Part II. Quantification of leg stiffness during functional hopping tasks.. J Electromyogr Kinesiol 2002 Apr;12(2):127-35.
    doi: 10.1016/S1050-6411(02)00003-2pubmed: 11955985google scholar: lookup
  43. Kim S, Park S. Leg stiffness increases with speed to modulate gait frequency and propulsion energy.. J Biomech 2011 Apr 29;44(7):1253-8.
    doi: 10.1016/j.jbiomech.2011.02.072pubmed: 21396646google scholar: lookup
  44. Rasband WS. ImageJ: image processing and analysis in Java. Astrophysics source code library Record ASCL 1206:013, 2012.
  45. Margaria R. Biomechanics and energetics of muscular exercise. Oxford, UK: Clarendon Press, 1976.
  46. Davis DD. The shoulder architecture of bears and other carnivores. Fieldiana Zool. 81, 285–305, 1949.
  47. Loscher DM, Meyer F, Kracht K, Nyakatura JA. Timing of head movements is consistent with energy minimization in walking ungulates.. Proc Biol Sci 2016 Nov 30;283(1843).
    doi: 10.5061/dryad.rf5bjpmc: PMC5136594pubmed: 27903873google scholar: lookup

Citations

This article has been cited 13 times.
  1. Zhang Q, Chen W, Liang J, Cheng L, Huang B, Xiong C. Influences of dynamic load phase shifts on the energetics and biomechanics of humans. R Soc Open Sci 2023 Aug;10(8):230636.
    doi: 10.1098/rsos.230636pubmed: 37650053google scholar: lookup
  2. Egenvall A, Engström H, Byström A. Back motion in unridden horses in walk, trot and canter on a circle. Vet Res Commun 2023 May 2;.
    doi: 10.1007/s11259-023-10132-ypubmed: 37127806google scholar: lookup
  3. Adachi M, Aoi S, Kamimura T, Tsuchiya K, Matsuno F. Fore-Aft Asymmetry Improves the Stability of Trotting in the Transverse Plane: A Modeling Study. Front Bioeng Biotechnol 2022;10:807777.
    doi: 10.3389/fbioe.2022.807777pubmed: 35721869google scholar: lookup
  4. Clayton H, MacKechnie-Guire R, Byström A, Le Jeune S, Egenvall A. Guidelines for the Measurement of Rein Tension in Equestrian Sport. Animals (Basel) 2021 Sep 30;11(10).
    doi: 10.3390/ani11102875pubmed: 34679895google scholar: lookup
  5. Schikowski L, Eley N, Kelleners N, Schmidt MJ, Fischer MS. Three-Dimensional Kinematic Motion of the Craniocervical Junction of Chihuahuas and Labrador Retrievers. Front Vet Sci 2021;8:709967.
    doi: 10.3389/fvets.2021.709967pubmed: 34490400google scholar: lookup
  6. Suzuki S, Kano T, Ijspeert AJ, Ishiguro A. Spontaneous Gait Transitions of Sprawling Quadruped Locomotion by Sensory-Driven Body-Limb Coordination Mechanisms. Front Neurorobot 2021;15:645731.
    doi: 10.3389/fnbot.2021.645731pubmed: 34393748google scholar: lookup
  7. Tijssen M, Serra Braganςa FM, Ask K, Rhodin M, Andersen PH, Telezhenko E, Bergsten C, Nielen M, Hernlund E. Kinematic gait characteristics of straight line walk in clinically sound dairy cows. PLoS One 2021;16(7):e0253479.
    doi: 10.1371/journal.pone.0253479pubmed: 34288912google scholar: lookup
  8. van Bijlert PA, van Soest AJ', Schulp AS. Natural Frequency Method: estimating the preferred walking speed of Tyrannosaurus rex based on tail natural frequency. R Soc Open Sci 2021 Apr 21;8(4):201441.
    doi: 10.1098/rsos.201441pubmed: 33996115google scholar: lookup
  9. Serra Bragança FM, Hernlund E, Thomsen MH, Waldern NM, Rhodin M, Byström A, van Weeren PR, Weishaupt MA. Adaptation strategies of horses with induced forelimb lameness walking on a treadmill. Equine Vet J 2021 May;53(3):600-611.
    doi: 10.1111/evj.13344pubmed: 32888199google scholar: lookup
  10. Arnold P, Esteve-Altava B, Fischer MS. Musculoskeletal networks reveal topological disparity in mammalian neck evolution. BMC Evol Biol 2017 Dec 13;17(1):251.
    doi: 10.1186/s12862-017-1101-1pubmed: 29237396google scholar: lookup
  11. Egenvall A, Clayton HM, Byström A. Pilot study of locomotor asymmetry in horses walking in circles with and without a rider. PeerJ 2023;11:e16373.
    doi: 10.7717/peerj.16373pubmed: 37933258google scholar: lookup
  12. Lusi CM, Davies HMS. Passive Dynamics of the Head, Neck and Forelimb in Equine Foetuses-An Observational Study. Animals (Basel) 2023 Jun 6;13(12).
    doi: 10.3390/ani13121894pubmed: 37370407google scholar: lookup
  13. Belyaev RI, Kuznetsov AN, Prilepskaya NE. How the even-toed ungulate vertebral column works: Comparison of intervertebral mobility in 33 genera. J Anat 2021 Dec;239(6):1370-1399.
    doi: 10.1111/joa.13521pubmed: 34365661google scholar: lookup
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