Evaluating bony predictors of bite force across the order Carnivora.
PCSA
bony correlates
entheses
masseter
temporalis
Journal
Journal of morphology
ISSN: 1097-4687
Titre abrégé: J Morphol
Pays: United States
ID NLM: 0406125
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
30
06
2021
received:
19
05
2021
accepted:
18
07
2021
pubmed:
28
7
2021
medline:
26
11
2021
entrez:
27
7
2021
Statut:
ppublish
Résumé
In carnivorans, bite force is a critical and ecologically informative variable that has been correlated with multiple morphological, behavioral, and environmental attributes. Whereas in vivo measures of biting performance are difficult to obtain in many taxa-and impossible in extinct species-numerous osteological proxies exist for estimating masticatory muscle size and force. These proxies include both volumetric approximations of muscle dimensions and direct measurements of muscular attachment sites. In this study, we compare three cranial osteological techniques for estimating muscle size (including 2D-photographic and 3D-surface data approaches) against dissection-derived muscle weights and physiological cross-sectional area (PCSA) within the jaw adductor musculature of 40 carnivoran taxa spanning eight families, four orders of magnitude in body size, and the full dietary spectrum of the order. Our results indicate that 3D-approaches provide more accurate estimates of muscle size than do surfaces measured from 2D-lateral photographs. However, estimates of a muscle's maximum cross-sectional area are more closely correlated with muscle mass and PCSA than any estimates derived from muscle attachment areas. These findings highlight the importance of accounting for muscle thickness in osteological estimations of the masticatory musculature; as muscles become volumetrically larger, their larger cross-sectional area does not appear to be associated with a proportional increase in the attachment site area. Though volumetric approaches approximate muscle dimensions well across the order as a whole, caution should be exercised when applying any single method as a predictor across diverse phylogenies.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1499-1513Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Aguirre, L. F., Herrel, A., van Damme, R., & Matthysen, E. (2002). Ecomorphological analysis of trophic niche partitioning in a tropical savannah bat community. Proceedings Biological sciences/The Royal Society, 269, 1271-1278.
Antón SC. 1994. Masticatory muscle architecture and bone morphology in primates. (PhD Dissertation). University of California Berkeley.
Antón, S. C. (1999). Macaque masseter muscle: Internal architecture, fiber length and cross-sectional area. International Journal of Primatology, 20, 441-462.
Arnold, C., Matthews, L. J., & Nunn, C. L. (2010). The 10kTrees website: A new online resource for primate phylogeny. Version 1: Carnivora. Evolutionary Anthropology, 19, 114-118.
Becerra, F., Echeverría, A., Vassallo, A. I., & Casinos, A. (2011). Bite force and jaw biomechanics in the subterranean rodent Talas tuco-tuco (Ctenomys talarum)(Caviomorpha: Octodontoidea). Canadian Journal of Zoology, 89, 334-342.
Becerra, F., Echeverría, A. I., Casinos, A., & Vassallo, A. I. (2014). Another one bites the dust: Bite force and ecology in three caviomorph rodents (Rodentia, Hystricognathi). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 321, 220-232.
Binder, W. J., & Van Valkenburgh, B. (2000). Development of bite strength and feeding behaviour in juvenile spotted hyenas (Crocuta crocuta). Journal of Zoology, 252(3), 273-283.
Blanco, R. E., Rinderknecht, A., & Lecuona, G. (2012). The bite force of the largest fossil rodent (Hystricognathi, Caviomorpha, Dinomyidae). Lethaia, 45, 157-163.
Brassard, C., Merlin, M., Guintard, C., Monchâtre-Leroy, E., Barrat, J., Bausmayer, N., Bausmayer, S., Bausmayer, A., Beyer, M., Varlet, A., & Houssin, C. (2020). Bite force and its relationship to jaw shape in domestic dogs. Journal of Experimental Biology, 223(16), 1-12.
Brassard, C., Merlin, M., Monchâtre-Leroy, E., Guintard, C., Barrat, J., Garès, H., Larralle, A., Triquet, R., Houssin, C., Callou, C., & Cornette, R. (2021). Masticatory system integration in a commensal canid: Interrelationships between bones, muscles and bite force in the red fox. Journal of Experimental Biology, 224(5), jeb224394.
Christiansen, P., & Adolfssen, J. S. (2005). Bite forces, canine strength and skull allometry in carnivores (Mammalia, Carnivora). Journal of Zoology, 266, 133-151.
Christiansen, P., & Wroe, S. (2007). Bite forces and evolutionary adaptations to feeding ecology in carnivores. Ecology Letters, 88, 347-358.
Davis, J. L., Santana, S. E., Dumont, E. R., & Grosse, I. R. (2010). Predicting bite force in mammals: Two-dimensional versus three-dimensional lever models. The Journal of Experimental Biology, 213, 1844-1851.
Dechow, P. C., & Carlson, D. S. (1990). Occlusal force and craniofacial biomechanics during growth in rhesus monkeys. American Journal of Physical Anthropology, 83, 219-237.
Demes, B., & Creel, N. (1988). Bite force, diet, and cranial morphology of fossil hominids. Journal of Human Evolution, 17, 657-670.
Deutsch, A. R., Dickinson, E., Leonard, K. C., Pastor, F., Muchlinski, M. N., & Hartstone-Rose, A. (2020). Scaling of anatomically derived maximal bite force in primates. The Anatomical Record, 303, 2026-2035.
Dumont, E., Herrel, A., Medellin, R., Vargas-Contreras, J., & Santana, S. (2009). Built to bite: Cranial design and function in the wrinkle-faced bat. Journal of Zoology, 279, 329-337.
Emerson, S. B., & Radinsky, L. (1980). Functional analysis of Sabertooth cranial morphology. Paleobiology, 6, 295-312.
Ewer, R. F. (1973). The carnivores. Cornell University Press.
Fabre, A. C., Perry, J. M., Hartstone-Rose, A., Lowie, A., Boens, A., & Dumont, M. (2018). Do muscles constrain skull shape evolution in Strepsirrhines? The Anatomical Record, 301(2), 291-310.
Forbes-Harper, J., Crawford, H., Dundas, S., Warburton, N., Adams, P., Bateman, P., Calver, M., & Fleming, P. (2017). Diet and bite force in red foxes: Ontogenetic and sex differences in an invasive carnivore. Journal of Zoology, 303, 54-63.
Gans, C. (1982). Fiber architecture and muscle function. Exercise and Sport Sciences Reviews, 10, 160-207.
Gans, C., & Bock, W. J. (1965). The functional significance of muscle architecture - a theoretical analysis. Ergebnisse der Anatomie und Entwicklungsgeschichte, 38, 115-142.
Grandal-d'Anglade, A. (2010). Bite force of the extinct Pleistocene cave bear Ursus spelaeus Rosenmüller from Europe. Comptes Rendus Palevol, 9, 31-37.
Gröning, F., Jones, M. E., Curtis, N., Herrel, A., O'Higgins, P., Evans, S. E., & Fagan, M. J. (2013). The importance of accurate muscle modelling for biomechanical analyses: A case study with a lizard skull. Journal of the Royal Society Interface, 10(84), 20130216.
Harbers, H., Neaux, D., Ortiz, K., Blanc, B., Laurens, F., Baly, I., Callou, C., Schafberg, R., Haruda, A., Lecompte, F., Casabianca, F., Studeur, J., Renaud, S., Cornette, R., Locatelli, U., Vigne, J.-D., Herrel, A., & Cucchi, T. (2020). The mark of captivity: Plastic responses in the ankle bone of a wild ungulate (Sus scrofa). Royal Society Open Science, 7(3), 192039.
Harbers, H., Zanolli, C., Cazenave, M., Theil, J. C., Ortiz, K., Blanc, B., Locatelli, Y., Schafberg, R., Lecompte, F., Baly, I., Laurens, F., Callou, C., Vigne, J.-D., Herrel, A., Puymerail, L., & Cucchi, T. (2020). Investigating the impact of captivity and domestication on limb bone cortical morphology: An experimental approach using a wild boar model. Scientific Reports, 10(1), 1-13.
Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: Investigating evolutionary radiations. Bioinformatics, 24(1), 129-131.
Hartstone-Rose, A., Dickinson, E., Worden, N., Deutsch, A., & Hirschkorn, G. (in press). Masticatory muscle architectural correlates of dietary diversity in Canidae, Ursidae, and across the order Carnivora. The Anatomical Record.
Hartstone-Rose, A., Hertzig, I., & Dickinson, E. (2019). Bite force and masticatory muscle architecture adaptations in the dietarily diverse Musteloidea (Carnivora). The Anatomical Record, 302, 2287-2299.
Hartstone-Rose, A., Perry, J. M., & Morrow, C. J. (2012). Bite force estimation and the fiber architecture of felid masticatory muscles. The Anatomical Record, 295, 1336-1351.
Hawkey, D. E., & Merbs, C. F. (1995). Activity-induced musculoskeletal stress markers (MSM) and subsistence strategy changes among ancient Hudson Bay Eskimos. International Journal of Osteoarchaeology, 5, 324-338.
Henderson, C. (2013). Do diseases cause entheseal changes at fibrous entheses? International journal of Paleopathology, 3, 64-69.
Henderson, C. Y., Mariotti, V., Pany-Kucera, D., Villotte, S., & Wilczak, C. (2013). Recording specific entheseal changes of fibrocartilaginous entheses: Initial tests using the Coimbra method. International Journal of Osteoarchaeology, 23, 152-162.
Herrel, A., Damme, R. V., Vanhooydonck, B., & Vree, F. D. (2001). The implications of bite performance for diet in two species of lacertid lizards. Canadian Journal of Zoology, 79(4), 662-670.
Herrel, A., De Grauw, E. D., & Lemos-Espinal, J. A. (2001). Head shape and bite performance in xenosaurid lizards. Journal of Experimental Zoology, 290(2), 101-107.
Herrel, A., & O'Reilly, J. C. (2006). Ontogenetic scaling of bite force in lizards and turtles. Physiological and Biochemical Zoology, 79(1), 31-42.
Karakostis, F. A., Hotz, G., Scherf, H., Wahl, J., & Harvati, K. (2017). Occupational manual activity is reflected on the patterns among hand entheses. American Journal of Physical Anthropology, 164, 30-40.
Karakostis, F. A., & Lorenzo, C. (2016). Morphometric patterns among the 3D surface areas of human hand entheses. American Journal of Physical Anthropology, 160, 694-707.
Law, C. J., Duran, E., Hung, N., Richards, E., Santillan, I., & Mehta, R. S. (2018). Effects of diet on cranial morphology and biting ability in musteloid mammals. Journal of Evolutionary Biology, 31, 1918-1931.
Leonard KC, Worden N, Boettcher ML, Dickinson E, Hartstone-Rose A. (2021). Effects of long-term ethanol storage on muscle architecture. The Anatomical Record, 2021, 1-12.
Leonard, K. C., Worden, N., Boettcher, M. L., Dickinson, E., Omstead, K. M., Burrows, A. M., & Hartstone-Rose, A. (2021). Anatomical and ontogenetic influences on muscle density. Scientific Reports, 11, 1-11.
Lieber, R. L. (1986). Skeletal muscle adaptability. I: Review of basic properties. Developmental Medicine and Child Neurology, 28, 390-397.
Lieber, R. L., & Fridén, J. (2000). Functional and clinical significance of skeletal muscle architecture. Muscle & Nerve, 23, 1647-1666.
Meers, M. B. (2002). Maximum bite force and prey size of tyrannosaurus rex and their relationships to the inference of feeding behavior. Historical Biology, 16, 1-12.
Meyers, J. J., Herrel, A., & Birch, J. (2002). Scaling of morphology, bite force and feeding kinematics in an Iguanian and a Scleroglossian lizard. In P. Aerts, K. D'Août, A. Herrel, & R. Van Damme (Eds.), Topics in functional and ecological vertebrate morphology (pp. 47-62). Shaker Publishing.
Milella, M. (2014). The influence of life history and sexual dimorphism on entheseal changes in modern humans and African great apes. PLoS One, 9, e107963.
Nowak, R. M. (1991). Walker's mammals of the world (5th ed.). Johns Hopkins UP.
Paradis, E., & Schliep, K. (2019). Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3), 526-528.
Penrose, F., Cox, P., Kemp, G., & Jeffery, N. (2020). Functional morphology of the jaw adductor muscles in the Canidae. The Anatomical Record, 303, 2878-2903.
Perry, J. M. G., St Clair, E. M., & Hartstone-Rose, A. (2015). Craniomandibular signals of diet in adapids. American Journal of Physical Anthropology, 158, 646-662.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & Team, R. C. (2006). Nlme: Linear and nonlinear mixed effects models, 3(4), 109.
Powell, P. L., Roy, R. R., Kanim, P., Bello, M. A., & Edgerton, V. R. (1984). Predictability of skeletal muscle tension from architectural determinations in Guinea pig hindlimbs. Journal of Applied Physiology, 57, 1715-1721.
Rabey, K. N., Green, D. J., Taylor, A. B., Begun, D. R., Richmond, B. G., & McFarlin, S. C. (2015). Locomotor activity influences muscle architecture and bone growth but not muscle attachment site morphology. Journal of Human Evolution, 78, 91-102.
Radinsky, L. B. (1981a). Evolution of skull shape in carnivores, 1: Representative modern carnivores. Biological Journal of the Linnean Society, 15, 369-388.
Radinsky, L. B. (1981b). Evolution of skull shape in carnivores, 2: Additional modern carnivores. Biological Journal of the Linnaean Society, 16, 337-355.
Rayne, J., & Crawford, G. N. C. (1972). The relationship between fibre length, muscle excursion and jaw movement in the rat. Archives of Oral Biology, 17, 859-872.
Revell, L. J. (2012). Phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217-223.
Ross, C. F., Porro, L. B., Herrel, A., Evans, S. E., & Fagan, J. F. (2018). Bite force and cranial bone strain in four species of lizards. Journal of Experimental Biology, 221(23), jeb180240.
Santana, S., & Dumont, E. (2009). Connecting behaviour and performance: The evolution of biting behaviour and bite performance in bats. Journal of Evolutionary Biology, 22, 2131-2145.
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
Thomason, J. J. (1991). Cranial strength in relation to estimated biting forces in some mammals. Canadian Journal of Zoology-Revue Canadienne De Zoologie, 69, 2326-2333.
Turcotte, C., Rabey, K., Green, D., & McFarlin, S. (in press). Muscle attachment sites and behavioral reconstruction: An experimental test of muscle-bone structural response to habitual activity. American Journal of Physical Anthropology.
Turcotte, C. M., Green, D. J., Kupczik, K., McFarlin, S., & Schulz-Kornas, E. (2020). Elevated activity levels do not influence extrinsic fiber attachment morphology on the surface of muscle-attachment sites. Journal of Anatomy, 236, 827-839.
Wallace, I. J., Winchester, J. M., Su, A., Boyer, D. M., & Konow, N. (2017). Physical activity alters limb bone structure but not entheseal morphology. Journal of Human Evolution, 107, 14-18.
Williams, S. H., Peiffer, E., & Ford, S. (2009). Gape and bite force in the rodents Onychomys leucogaster and Peromyscus maniculatus: Does jaw-muscle anatomy predict performance? Journal of Morphology, 270, 1338-1347.
Williams-Hatala, E., Hatala, K., Hiles, S., & Rabey, K. (2016). Morphology of muscle attachment sites in the modern human hand does not reflect muscle architecture. Scientific Reports, 6, 28353.
Wilson, D. E., & Mittermeier, R. A. (2009). Handbook of the mammals of the world Vol 1: Carnivores. Lynx Edicions.
Wroe, S., McHenry, C., & Thomason, J. (2005). Bite club: Comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proceedings of the Royal Society B: Biological Sciences, 272, 619-625.
Zumwalt, A. (2006). The effect of endurance exercise on the morphology of muscle attachment sites. Journal of Experimental Biology, 209, 444-454.