The anatomy of a crushing bite: The specialised cranial mechanics of a giant extinct kangaroo

English version

Autoři: D. Rex Mitchell ^aff001
Působiště autorů: Zoology Division, School of Environmental and Rural Sciences, University of New England, Armidale, New South Wales, Australia ^aff001; Department of Anthropology, University of Arkansas, Fayetteville, Arkansas, United States of America ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0221287

Souhrn

The Sthenurinae were a diverse subfamily of short-faced kangaroos that arose in the Miocene and diversified during the Pliocene and Pleistocene. Many species possessed skull morphologies that were relatively structurally reinforced with bone, suggesting that they were adapted to incorporate particularly resistant foods into their diets. However, the functional roles of many unique, robust features of the sthenurine cranium are not yet clearly defined. Here, the finite element method is applied to conduct a comprehensive analysis of unilateral biting along the cheek tooth battery of a well-represented sthenurine, Simosthenurus occidentalis. The results are compared with those of an extant species considered to be of most similar ecology and cranial proportions to this species, the koala (Phascolarctos cinereus). The simulations reveal that the cranium of S. occidentalis could produce and withstand comparatively high forces during unilateral biting. Its greatly expanded zygomatic arches potentially housed enlarged zygomaticomandibularis muscles, shown here to reduce the risk of dislocation of the temporomandibular joint during biting with the rear of a broad, extensive cheek tooth row. This may also be a function of the zygomaticomandibularis in the giant panda (Ailuropoda melanoleuca), another species known to exhibit an enlarged zygomatic arch and hypertrophy of this muscle. Furthermore, the expanded frontal plates of the S. occidentalis cranium form broad arches of bone with the braincase and deepened maxillae that each extend from the anterior tooth rows to their opposing jaw joints. These arches are demonstrated here to be a key feature in resisting high torsional forces during unilateral premolar biting on large, resistant food items. This supports the notion that S. occidentalis fed thick, lignified vegetation directly to the cheek teeth in a similar manner to that described for the giant panda when crushing mature bamboo culms.

Klíčová slova:

Biology and life sciences – Anatomy – Medicine and health sciences – Digestive system – Physiology – Physiological processes – Teeth – Head – Jaw – Musculoskeletal system – Skeleton – Biomechanics – Musculoskeletal mechanics – Muscle physiology – Digestive physiology – Dentition – Eating – Molars – Cranium – Skeletal joints

Zdroje

1. Figueirido B, Tseng ZJ, Martín-Serra A. Skull shape evolution in durophagous carnivorans. Evolution. 2013; 67(7):1975–1993. doi: 10.1111/evo.12059 23815654

2. Wroe S, Clausen P, McHenry C, Moreno K, Cunningham E. Computer simulation of feeding behaviour in the thylacine and dingo as a novel test for convergence and niche overlap. Proc R Soc Lond B Biol Sci. 2007; 274(1627):2819–2828.

3. Constantino PJ, Lee JJW, Morris D, Lucas PW, Hartstone-Rose A, Lee W, et al. Adaptation to hard-object feeding in sea otters and hominins. J Hum Evol. 2011; 61(1):89–96. doi: 10.1016/j.jhevol.2011.02.009 21474163

4. Figueirido B, MacLeod N, Krieger J, De Renzi M, Pérez-Claros JA, Palmqvist P. Constraint and adaptation in the evolution of carnivoran skull shape. Paleobiology. 2011; 37(3):490–518.

5. Figueirido B, Tseng ZJ, Serrano-Alarcón FJ, Martín-Serra A, Pastor JF. Three-dimensional computer simulations of feeding behaviour in red and giant pandas relate skull biomechanics with dietary niche partitioning. Biol Lett. 2014; 10(4):20140196. doi: 10.1098/rsbl.2014.0196 24718096

6. Du Brul EL. Early hominid feeding mechanisms. Am J Phys Anthropol. 1977; 47(2):305–320. doi: 10.1002/ajpa.1330470211 410308

7. Freeman PW. Specialized insectivory: beetle-eating and moth-eating molossid bats. J Mammal. 1979; 60(3):467–479.

8. Greaves WS. The generalized carnivore jaw. Zool J Linnean Soc. 1985; 85(3): 267–274.

9. Demes B, Creel N. Bite force, diet, and cranial morphology of fossil hominids. J Hum Evol. 1988; 17(7):657–670.

10. Van Valkenburgh B. Carnivore dental adaptations and diet: a study of trophic diversity within guilds. In: Gittleman JL, editor. Carnivore behavior, ecology, and evolution. Boston: Springer; 1989. pp. 410–436.

11. Antón SC. Cranial adaptation to a high attrition diet in Japanese macaques. Int J Primatol. 1996; 17(3):401–427.

12. Sacco T, Van Valkenburgh B. Ecomorphological indicators of feeding behaviour in the bears (Carnivora: Ursidae). J Zool. 2004; 263(1):41–54.

13. Ungar PS, Grine FE, Teaford MF. Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS One. 2008; 3(4):e2044. doi: 10.1371/journal.pone.0002044 18446200

14. Figueirido B, Serrano-Alarcón FJ, Slater GJ, Palmqvist P. Shape at the cross-roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory. J Evol Biol. 2010; 23(12):2579–2594. doi: 10.1111/j.1420-9101.2010.02117.x 20942824

15. Tseng ZJ, Wang X. Cranial functional morphology of fossil dogs and adaptation for durophagy in Borophagus and Epicyon (Carnivora, Mammalia). J Morphol. 2010; 271(11):1386–1398. doi: 10.1002/jmor.10881 20799339

16. Terhune CE. Modeling the biomechanics of articular eminence function in anthropoid primates. J Anat. 2011; 219(5):551–564. doi: 10.1111/j.1469-7580.2011.01424.x 21923720

17. Smith AL, Benazzi S, Ledogar JA, Tamvada K, Pryor Smith LC, Weber GW, et al. The feeding biomechanics and dietary ecology of Paranthropus boisei. Anat Rec. 2015; 298(1):145–167.

18. Ledogar JA, Benazzi S, Smith AL, Weber GW, Carlson KB, Dechow PC, et al. The biomechanics of bony facial “buttresses” in South African australopiths: an experimental study using finite element analysis. Anat Rec. 2017; 300(1):171–195.

19. Covey DS, Greaves WS. Jaw dimensions and torsion resistance during canine biting in the Carnivora. Can J Zool. 1994; 72(6):1055–1060.

20. Alexander RM. Factors of safety in the structure of animals. Science Progress. 1981; 67(265):109–130. 7013065

21. Prideaux GJ. Systematics and evolution of the sthenurine kangaroos. University of California Publishing Geological Sciences. 2004; 146:1–623.

22. Rayfield EJ. Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annu Rev Earth Planet Sci. 2007; 35:541–576.

23. Black KH, Archer M, Hand SJ, Godthelp H. The rise of Australian marsupials: a synopsis of biostratigraphic, phylogenetic, palaeoecologic and palaeobiogeographic understanding. In: Talent JA, editor. Earth and Life. Netherlands: Springer; 2012. pp 983–1078.

24. Couzens AM, Prideaux GJ. Rapid Pliocene adaptive radiation of modern kangaroos. Science. 2018; 362(6410):72–75. doi: 10.1126/science.aas8788 30287658

25. Richardson K. Australia’s amazing kangaroos: their conservation, unique biology and coexistence with humans. Collingwood, Victoria: CSIRO Publishing; 2012.

26. Helgen KM, Wells RT, Kear BP, Gerdtz WR, Flannery TF. Ecological and evolutionary significance of sizes of giant extinct kangaroos. Aust J Zool. 2006; 54(4):293–303.

27. Wells RT, Tedford RH. Sthenurus (Macropodidae, Marsupialia) from the Pleistocene of Lake Callabonna, South Australia. Bulletin of the AMNH. 1995; 225:1–111.

28. Janis CM, Buttrill K, Figueirido B. Locomotion in extinct giant kangaroos: were sthenurines hop-less monsters? PLoS One. 2014; 9(10):e109888. doi: 10.1371/journal.pone.0109888 25333823

29. Raven HC, Gregory WK. Adaptive branching of the kangaroo family in relation to habitat. Am Mus Novit. 1946; 1309:1–33.

30. Ride WDL. Mastication and taxonomy in the macropodine skull. In: Cain AJ, editor. Function and Taxonomic Importance. London, UK: Systematics Association Publication; 1959. pp. 33–59.

31. Prideaux GJ, Ayliffe LK, DeSantis LRG, Schubert BW, Murray PF. Gagan MK, et al. Extinction implications of a chenopod browse diet for a giant Pleistocene kangaroo. Proc Natl Acad Sci USA. 2009; 106(28):11646–11650. doi: 10.1073/pnas.0900956106 19556539

32. Prideaux GJ, Gully GA, Couzens AM, Ayliffe LK, Jankowski NR, Jacobs Z, et al. Timing and dynamics of Late Pleistocene mammal extinctions in southwestern Australia. Proc Natl Acad Sci USA. 2010; 107(51):22157–22162. doi: 10.1073/pnas.1011073107 21127262

33. Jankowski NR, Gully GA, Jacobs Z, Roberts RG, Prideaux GJ. A late Quaternary vertebrate deposit in Kudjal Yolgah Cave, south-western Australia: refining regional late Pleistocene extinctions. J Quat Sci. 2016; 31(5):538–550.

34. Johnson CN, Prideaux GJ. Extinctions of herbivorous mammals in the late Pleistocene of Australia in relation to their feeding ecology: no evidence for environmental change as cause of extinction. Austral Ecol. 2004; 29(5):553–557.

35. Mitchell DR, Wroe S. Biting mechanics determines craniofacial morphology among extant diprotodont herbivores: dietary predictions for the giant extinct short-faced kangaroo, Simosthenurus occidentalis. Paleobiology. 2019; 45(1):167–181.

36. Greaves WS. The jaw lever system in ungulates: a new model. J Zool. 1978; 184(2):271–285.

37. Greaves WS. The maximum average bite force for a given jaw length. J Zool. 1988; 214:295–306.

38. Greaves WS. The mammalian jaw: a mechanical analysis. Cambridge UK: Cambridge University Press; 2012.

39. Bramble DM. Origin of the mammalian feeding complex: models and mechanisms. Paleobiology. 1978; 4(3):271–301.

40. Mitchell DR, Sherratt E, Ledogar JA, Wroe S. The biomechanics of foraging determines face length among kangaroos and their relatives. Proc R Soc Lond B Biol Sci. 2018; 285(1881):20180845.

41. Turnbull WD. Mammalian masticatory apparatus. Fieldiana Geol. 1970; 18:149–356.

42. Warburton NM. Comparative jaw muscle anatomy in kangaroos, wallabies, and rat-kangaroos (Marsupialia: Macropodoidea). Anat Rec. 2009; 292(6):875–884.

43. Thomason JJ. Cranial strength in relation to estimated biting forces in some mammals. Can J Zool. 1991; 69(9):2326–2333.

44. Mills JRE. A comparison of lateral jaw movements in some mammals from wear facets on the teeth. Arch Oral Biol. 1967; 12(5):645–661. doi: 10.1016/0003-9969(67)90083-0 5228612

45. Crompton AW, Barnet J, Lieberman DE, Owerkowicz T, Skinner J, Baudinette RV. Control of jaw movements in two species of macropodines (Macropus eugenii and Macropus rufus). Comp Biochem Physiol A Mol Integr Physiol. 2008; 150(2):109–123. doi: 10.1016/j.cbpa.2007.10.015 18065250

46. Sharp AC. Comparative finite element analysis of the cranial performance of four herbivorous marsupials. J Morphol. 2015; 276:1230–1243. doi: 10.1002/jmor.20414 26193997

47. Strait DS, Grosse IR, Dechow PC, Smith AL, Wang Q, Weber GW, et al. The structural rigidity of the cranium of Australopithecus africanus: implications for diet, dietary adaptations, and the allometry of feeding biomechanics. Anat Rec. 2010; 293(4):583–593.

48. Walmsley CW, McCurry MR, Clausen PD, McHenry CR. Beware the black box: investigating the sensitivity of FEA simulations to modelling factors in comparative biomechanics. PeerJ. 2013; 1:e204. doi: 10.7717/peerj.204 24255817

49. Fitton LC, Prôa M, Rowland C, Toro-Ibacache V, O’higgins P. The impact of simplifications on the performance of a finite element model of a Macaca fascicularis cranium. Anat Rec. 2015; 298(1):107–121.

50. Wroe S, Parr WCH, Ledogar JA, Bourke J, Evans SP, Fiorenza L, et al. Computer simulations show that Neanderthal facial morphology represents adaptation to cold and high energy demands, but not heavy biting. Proc R Soc Lond B Biol Sci. 2018; 285(1876):20180085.

51. Davison CV, Young WG. The Muscles of Mastication of Phascolarctos cinereus (Phascolarctidae, Marsupialia). Aust J Zool. 1990; 38:227–240.

52. Crompton AW, Owerkowicz T, Skinner J. Masticatory motor pattern in the koala (Phascolarctos cinereus): a comparison of jaw movements in marsupial and placental herbivores. J Exp Zool A Comp Exp Biol. 2010; 313(9):564–578.

53. Grosse IR, Dumont ER, Coletta C, Tolleson A. Techniques for modeling muscle-induced forces in finite element models of skeletal structures. Anat Rec. 2007; 290(9):1069–1088.

54. Ledogar JA, Dechow PC, Wang Q, Gharpure PH, Gordon AD, Baab KL, et al. (2016) Human feeding biomechanics: performance, variation, and functional constraints. PeerJ. 2016; 4:e2242. doi: 10.7717/peerj.2242 27547550

55. Strait DS, Weber GW, Neubauer S, Chalk J, Richmond BG, Lucas PW, et al. The feeding biomechanics and dietary ecology of Australopithecus africanus. Proc Natl Acad Sci USA. 2009; 106:2124–2129. doi: 10.1073/pnas.0808730106 19188607

56. Clausen P, Wroe S, McHenry C, Moreno K, Bourke J. The vector of jaw muscle force as determined by computer-generated three-dimensional simulation: a test of Greaves’ model. J Biomech. 2008; 41(15):3184–3188. doi: 10.1016/j.jbiomech.2008.08.019 18838138

57. Greaves WS. A functional analysis of carnassial biting. Biol J Linnean Soc. 1983; 20(4):353–363.

58. Spencer MA. Force production in the primate masticatory system: electromyographic tests of biomechanical hypotheses. J Hum Evol. 1998; 34(1):25–54. doi: 10.1006/jhev.1997.0180 9467780

59. Greaves WS. Location of the vector of jaw muscle force in mammals. J Morphol. 2000; 243(3):293–299. doi: 10.1002/(SICI)1097-4687(200003)243:3<293::AID-JMOR6>3.0.CO;2-5 10681474

60. Greaves WS. A relationship between premolar loss and jaw elongation in selenodont artiodactyls. Zool J Linnean Soc. 1991; 101(2):121–129.

61. Perry JM, Hartstone-Rose A, Logan RL. The jaw adductor resultant and estimated bite force in primates. Anatomical Research International. 2011; doi: 10.1155/2011/929848 22611496

62. Greaves WS. A mechanical limitation on the position of the jaw muscles of mammals: the one-third rule. J Mammal. 1982; 63(2):261–266.

63. Greaves WS. Modeling the distance between the molar tooth rows in mammals. Can J Zool. 2002; 80(2):388–393.

64. Therrien F. Feeding behaviour and bite force of sabre-toothed predators. Zool J Linnean Soc. 2005; 145(3):393–426.

65. Goswami A, Milne N, Wroe S. Biting through constraints: cranial morphology, disparity and convergence across living and fossil carnivorous mammals. Proc R Soc Lond B Biol Sci. 2011; 278(1713):1831–1839.

66. Spencer MA. Constraints on masticatory system evolution in anthropoid primates. Am J Phys Anthropol. 1999; 108(4):483–506. doi: 10.1002/(SICI)1096-8644(199904)108:4<483::AID-AJPA7>3.0.CO;2-L 10229390

67. Llamas B, Brotherton P, Mitchell KJ, Templeton JEL, Thomson VA, Metcalf JL, et al. Late Pleistocene Australian marsupial DNA clarifies the affinities of extinct megafaunal kangaroos and wallabies. Mol Biol Evol. 2014; 32(3):574–584. doi: 10.1093/molbev/msu338 25526902

68. Cascini M, Mitchell KJ, Cooper A, Phillips MJ. Reconstructing the evolution of giant extinct kangaroos: comparing the utility of DNA, morphology, and total evidence. Syst Biol. 2018; doi: 10.1093/sysbio/syy080 30481358

69. Davis DD. Masticatory apparatus in the spectacled bear, Tremarctos ornatus. Field Zool. 1955; 37:25–46.

70. Murray P. The sthenurine affinity of the late Miocene kangaroo, Hadronomas puckridgi Woodburne (Marsupialia, Macropodidae). Alcheringa. 1991; 15(4):255–283.

71. Greaves WS. The mammalian postorbital bar as a torsion-resisting helical strut. J Zool. 1985; 207(1):125–136.

72. Hansen RL, Carr MM, Apanavicius CJ, Jiang P, Bissell HA, Gocinski, et al. Seasonal shifts in giant panda feeding behavior: relationships to bamboo plant part consumption. Zoo Biol. 2010; 29(4):470–483. doi: 10.1002/zoo.20280 19862794

73. Davis DD. The giant panda: a morphological study of evolutionary mechanisms. Field Zool. 1964; 3:1–339.

74. Dierenfeld ES, Hintz HF, Robertson JB, Van Soest PJ, Oftedal OT. Utilization of bamboo by the giant panda. J Nutr. 1982; 112(4):636–641. doi: 10.1093/jn/112.4.636 6279804

75. Zhang S, Pan R, Li M, Oxnard C, Wei F. Mandible of the giant panda (Ailuropoda melanoleuca) compared with other Chinese carnivores: functional adaptation. Biol J Linnean Soc. 2007; 92(3):449–456.

The anatomy of a crushing bite: The specialised cranial mechanics of a giant extinct kangaroo

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