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We provide the first predictions of bite force B S in a wide sample of living and fossil mammalian predators. To compare between taxa, we calculated an estimated bite force quotient BFQ as the residual of B S regressed on body mass. Estimated B S adjusted for body mass was higher for marsupials than placentals and the Tasmanian devil Sarcophilus harrisii had the highest relative B S among extant taxa.
The highest overall B S was in two extinct marsupial lions.
BFQ in hyaenas were similar to those of related, non-osteophagous taxa challenging the common assumption that osteophagy necessitates extreme jaw muscle forces. High BFQ in living carnivores was associated with greater maximal prey size and hypercarnivory. For fossil taxa anatomically similar to living relatives, BFQ can be directly compared, and high values in the dire wolf Canis dirus and thylacine Thylacinus cynocephalus suggest that they took relatively large prey.
Direct inference may not be appropriate where morphologies depart widely from biomechanical models evident in living predators and must be considered together with evidence from other morphological indicators.
Extremely high BFQ in the marsupial lion, Thylacoleo carnifex , indicates that it filled a large-prey hunting niche.
Important unanswered questions are: Answers will define the limits of using B S estimate as a predictor of behaviour and prey size in fossil species. Our sample comprised 49 specimens representing 39 taxa 31 extant and eight extinct.
The dry skull method, derived from relationships between skull dimensions and jaw muscle cross-sectional areas, models the jaw as a simple lever. It is most applicable to the anterior-most portion of the jaw, where the caniniform teeth are located Electronic Appendix, section A. Consequently, and because morphology of the canines has long been considered a significant predictor of predatory behaviour in mammalian carnivores Wroe et al.
To compare bite forces in taxa of greatly differing body masses an estimated bite force quotient BFQ was calculated using the residuals of regression table 1 ; Electronic Appendix, section A.
Variance in allometry adjusted bite force is small relative to that for absolute B S Thomason ; Electronic Appendix, section D and a second advantage of using BFQ is that it allows more meaningful comparisons based on small datasets.
This quality is particularly valuable in analyses incorporating fossil taxa where sample sizes are limited. Individual data points are: Species abbreviations as in table 1. Measurements and calculations were taken from prepared skulls. Methods for body mass estimations given in Electronic Appendix, section A.
The highest B S estimate adjusted for body mass were in two extinct marsupial lions, Thylacoleo carnifex and Priscileo roskellyae The lowest was also in a fossil marsupial, Thylacosmilus atrox Among extant carnivorous mammals the highest BFQ was in the Tasmanian devil, Sarcophilus harrisii Mean BFQ was higher in marsupials than placentals versus 98 , although marsupials do not have larger heads—relationships between head lengths and body masses in dasyuromorphians were similar to those of canids, and thylacoleonids were similar to felids figure 2.
Power regressions are shown for felids black dashed line , canids grey solid line , dasyuromorphians grey dashed line , thylacoleonids black solid line. Symbols as in figure 1. The average BFQ for Felidae was slightly less than in Canidae and dogs had greater head to body size figure 2 , but the difference in this instance was not significant.
CB S was considerable for specialist bone-crackers included in our study, the spotted and brown hyaenas Crocuta crocuta and Hyaena hyaena and the Tasmanian devil S. However, in the two hyaenids, BFQ at the canine was exceeded by several non-osteophagous carnivorans figure 1 ; table 1 and BFQ for the Tasmanian devil was not much above average for dasyuromorphians and less than in two marsupial lions.
BFQ at the carnassial teeth followed a similar pattern Electronic Appendix, section C , an expected result because the position of the carnassial varies little among mammalian predators Greaves As an upper restriction on niche, a predator's maximal prey size is an important component of its ecology and is likely to be strongly influenced by its biomechanical limits.
Predator body mass has been shown to correlate with maximal prey size in mammals Meers Among extant canids, the four hypercarnivores that often prey on animals larger than themselves, the grey wolf Canis lupus lupus , dingo C.
BFQ was consistently lower in the five more solitary, omnivorous foxes, jackals and coyote characterized by relatively low maximal prey sizes 80— Thus, although the ability to bring down large prey in canids is related to cooperative hunting, it is still reflected in a higher BFQ.
Within living Felidae, BFQ values were 57 and 75 for the two species that specialize in relatively small prey, while BFQ was 94 or greater for the seven known to take relatively large prey table 2. B S adjusted for body mass was also low in bears 44—78 , which are restricted to relatively small prey Meers BFQ was higher in extant dasyuromorphian marsupials, but the same trends were evident. The lowest BFQ was in the eastern quoll Dasyurus viverrinus , which takes comparatively smaller prey and is less carnivorous than the other marsupials considered see below.
Overall, BFQ was or higher in 15 of the 16 extant placental and marsupial carnivores sampled that take prey larger than their own maximal body masses. In 12 of the 14 extant species where maximal prey size was less than the species' mean body mass, BFQ was less than table 2.
Bite force adjusted for body mass allometry BFQ , maximal prey size and feeding category in 31 extant mammalian carnivores. Maximal body mass data largely from Meers For additional data see Electronic Appendix, section A. Results suggest that, relative to body mass, calculated canine B S is considerably higher in marsupials than in placentals and this cannot simply be explained by differences in head size. The presence of the superfast myosin isoform in both carnivorans and dasyuromorphians suggests that their muscle microphysiology is similar Hoh et al.
Differences between these two groups may relate to brain volumes, which, in carnivorans, are around two and a half times that of marsupial carnivores Wroe et al. Within the temporal region of the skull, cross-sectional area places limits on the maximal force that can be generated by muscle Thomason , and expansion of brain volume impinges on available muscle area within the zygoma.
Consequently, within a skull of given length and width, greater brain size impinges on maximal B S. Extant carnivorans may have more precisely targeted killing behaviours than marsupial counterparts Ewer and through greater efficiency may be able to accomplish similar results with less B S.
Because mean BFQ in marsupials is much higher than in placentals, our finding that the relatively omnivorous D. If in vivo testing shows that placentals produce bite forces that are similar, after adjustment for body mass, to marsupials, it will probably be a result of differences in jaw muscle anatomy, such as muscle pennation or microphysiology, although none have been clearly identified to date.
Mean BFQ was lower in cats than canids, reflecting the smaller head size of cats relative to body mass, but relative to skull length, CB S in felids was greater, possibly because of their greater skull width relative to length Electronic Appendices, sections E and F.
Although extant canids and dasyuromorphians have higher mean BFQ than felids, the shorter skull of cats may confer greater resistance to forces produced by struggling prey. Cats also have more powerful, flexible forelimbs, of critical utility in violent, close quarter interactions and may recruit ventral cervical musculature to assist in jaw closure Van Valkenburgh et al. Our finding that BFQ at both the canine and carnassial in osteophages were often comparable to, and sometimes less than, many non-osteophagous relatives was unexpected.
This may have important implications regarding the biomechanics of osteophagy.
In most carnivores, maximal bite forces are used in the killing bite at the canines where maximal loads will be distributed between adjacent teeth in the anterior region of the jaw. In contrast, osteophagy requires the concentration of high loads on a limited part of the food item in order to produce material failure. The highest bite forces are typically achievable in carnassial biting, which is restricted to one side of the mandible rather than distributed between left and right jaws Greaves In hyaenids, maximum forces may be generated immediately anterior to the carnassial Werdelin Moreover, from observation, osteophages may use kinetic, rather than static bites to crack bones, further increasing loads.
Consequently, theoretical forces that can be achieved are far greater than those experienced during a canine bite. The application of maximal bite forces at post-canine teeth on hard materials requires very robust dentitions, as evidenced in specialized bone-crackers such C.
Our results suggest that although the capacity of teeth and probably crania to resist high stresses on hard substances in the cheek—tooth row is an essential adaptation to specialized osteophagy in mammals, particularly high bite strength relative to body size is not. The flipside of this argument is that many felids and canids could theoretically apply relatively greater bite forces at a single point in the cheek—tooth row than could a same-sized hyaenid.
However, we posit that in practice, non-osteophageous taxa will not voluntarily develop maximal bite forces in a post-canine bite because neither their dentitia nor their crania are optimized to resist such high stresses in this region. Unused capacity at the carnassial in non-osteophages may be an incidental product of the requirement for high B S at the canines as part of their killing strategy.
Our results demonstrate that among living mammalian carnivores, BFQ is a broad indicator of relative prey size and feeding ecology. However, considered in isolation, B S adjusted for body mass is not an infallible predictor.
In the aardwolf Proteles cristatus , BFQ is low 77 , but higher than in some bears, a viverrid and two small cat species table 2. Although this finding is consistent in that all take relatively small prey, it does not reflect the fact that P.
Interestingly, the unusual, hypotrophied post-canine morphology of the aardwolf unambiguously suggests that vertebrates are rarely taken, but the canines are quite well developed. Together with moderate BFQ, this indicates that it is physically capable of killing much larger prey than it does.
The retention of functional canines and moderate BFQ in P. Either way, the aardwolf clearly lies outside generalized biomechanical subcategories, such as the cat and dog types, which themselves differ in details including head shape, canine cross-sectional morphologies and killing behaviour.
This example demonstrates well that BFQ may not directly reflect feeding ecology for morphologically atypical taxa that do not fit within generalized biomechanical models. Consequently, in the reconstruction of ecology for fossil carnivores, BFQ must be qualified against the type and extent of morphological departure from biomechanical sub-categories observable in living species.
For example, predictions incorporating BFQ for fossil cats, or taxa with cat-like morphologies, are best made on the basis of comparisons with extant felids. Neither cranial, nor post-cranial morphology of the thylacine, Thylacinus cynocephalus , differ greatly from those of living dasyuromorphians Wroe Our finding that BFQ was comparable to extant dasyuromorphians known to take relatively large prey is contra these interpretations table 1.
Similarly, high BFQ in the Miocene thylacinid, Nimbacinus dicksoni , suggests that relatively large prey were accessible to this anatomically conservative species. Likewise, among fossil placentals, morphology of the dire wolf C. Some fossil taxa included in our analyses clearly fell well outside extant morphotypes.
Having secured large prey with its muscular forelimbs, S. The reduced cross-sectional area of the canines in sabrecats may require relatively less bite force than that used by living Panthera M. Meers, personal communication. In the marsupial sabretooth, T. Current functional models of sabretooth killing behaviour include: Because absolute CB S in S.
Our results do not rule out this possibility, but are contra the conclusion that bite force in S. However, in the marsupial sabretooth, CB S and BFQ are both so low that we consider our result supportive of a primarily neck-driven use of the canines and strongly contra the possibility that T.
For the marsupial lion, T. If the killing mechanism of T. However, although cat-like in many respects, its dentition is unusual and interpretation of feeding ecology in the marsupial lion has long attracted controversy Wells et al. Our findings confirm that short outlever arms and anteriorly placed muscle resultants conferred high mechanical efficiency Wells et al.
Brought together with a very high B S , these carnassials may have enabled T. When CB S and BFQ are considered together with forelimb, cervical and lumbar morphology that converges on that of marsupial and placental sabretooths, as well as taphonomic data Janis ; Wroe ; Argot , the marsupial lion may have been capable of taking sub-adults of the heaviest available prey Wroe et al.
The dry skull method, because it takes into account subtle changes in the shape of the skull and jaws, provides estimates of B S that can be applied across unrelated taxa and thus allows quantitative comparisons of this important component of a predator's biomechanical performance. Adjusted for body mass, our estimates of B S i show variations that are broadly consistent with patterns of predatory behaviour and diet observed in extant carnivores, ii provide a basis for predicting maximal prey size in extinct mammalian predators that are morphologically similar to extant predators, iii allow quantifiable comparisons of biomechanics within ecomorphs, where there are no living analogues, such as sabretooths and iv challenge the widely held assumption that osteophagy requires relatively higher B S than that seen in non-osteophagous relatives.
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Forgot your username? Enter your email address below and we will send you your username. Restricted access. Biological Sciences http: Section Supplemental Material. References Akersten W. Los Angeles County. J, Pastor J. F, Sanchez I.
Argot C. Bicknevicus A. L vol. Cornell University Press. Binder W. Daniel W. Crocodilian biology and evolution , Grigg G. Chipping Norton: Surrey Beatty. Ewer R.
Farlow J. Greaves W. Hoh J. Y, Lim J. Y, Kang L. A Expression of superfast myosin in the jaw-closing muscles of Crocodylus porosus.
Chipping Norton, NSW: Janis C. Jones M.