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Bite club: Comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa

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We provide the first predictions of bite force (BS) 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 BS regressed on body mass. Estimated BS adjusted for body mass was higher for marsupials than placentals and the Tasmanian devil (Sarcophilus harrisii) had the highest relative BS among extant taxa. The highest overall BS 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. Relatively low BFQ values in two extinct carnivores with morphologies not represented among extant species, the sabrecat, Smilodon fatalis, and marsupial sabretooth, Thylacosmilus atrox, support arguments that their killing techniques also differed from extant species and are consistent with 'canine-shear bite' and 'stabbing' models, respectively. Extremely high BFQ in the marsupial lion, Thylacoleo carnifex, indicates that it filled a large-prey hunting niche.
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Bite club: comparative bite force in big biting
mammals and the prediction of predatory
behaviour in fossil taxa
Stephen Wroe
1,
*
, Colin McHenry
2
and Jeffrey Thomason
3
1
School of Biological Sciences (A08), University of Sydney, NSW, Australia 2006
2
School of Environmental and Life Sciences (Earth Sciences), University of Newcastle, NSW, Australia 2308
3
Department of Biomedical Sciences, University of Guelph, Ontario, Canada N1G 2W1
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. Relatively low BFQ values in two extinct carnivores with morphologies not represented among
extant species, the sabrecat, Smilodon fatalis, and marsupial sabretooth, Thylacosmilus atrox, support
arguments that their killing techniques also differed from extant species and are consistent with ‘canine-
shear bite’ and ‘stabbing’ models, respectively. Extremely high BFQ in the marsupial lion, Thylacoleo
carnifex, indicates that it filled a large-prey hunting niche.
Keywords: bite force; prey size; osteophagy; Carnivora; Dasyuromorphia; Thylacoleonidae
1. INTRODUCTION
Bite force (B
S
) is an important aspect of carnivore ecology,
with the potential to shed light on the evolution of
community structure and prey size in fossil taxa (Meers
2002; Vizcaı
´
no & de Iuliis 2003; Rayfield 2004). However,
empirical data are not easily obtained; B
S
has been
measured in only three mammalian carnivore species
(Thomason 1991; Dessem & Druzinsky 1992; Binder &
Van Valkenburgh 2000) and the comparative biology of B
S
in mammals has remained largely unexplored. Important
unanswered questions are: is bite force (i) allometrically
related to body mass, (ii) phylogenetically constrained,
(iii) more strongly influenced by skull length or skull
width, (iv) relatively higher in bone-cracking specialists
and (v) related to prey size in extant taxa? Answers will
define the limits of using B
S
estimate as a predictor of
behaviour and prey size in fossil species.
2. MATERIAL AND METHODS
We calculated theoretical maximum bite forces using the ‘dry
skull’ method (Thomason 1 991; Electronic Appendices,
sections A and B). 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. 1998; Farlow & Pianka 2002), we
have largely restricted our discussion to estimates of force for
static bites at the canines (CB
S
). However, analyses of B
S
at
the carnassial showed the same qualitative trends as for CB
S
(Electronic Appendix, section C). A further advantage of the
‘dry skull’ method is that because results are derived solely
from skull morphology, comparisons can be made between
fossil and extant taxa.
The relationship between CB
S
and body mass between
species is allometri c (figure 1; Meers 2002; r
2
Z0.85). 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). ‘Average’ BFQ was set at 100. Variance in allometry
adjusted bite force is small relative to that for absolute B
S
(Thomason 1991; 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.
3. RESULTS
The highest B
S
estimate adjusted for body mass were
Proc. R. Soc. B
doi:10.1098/rspb.2004.2986
Published online
* Author for correspondence (swroe@bio.usyd.edu.au).
Received 28 July 2004
Accepted 16 October 2004
1 q 2005 The Royal Society
in two extinct marsupial lions, Thylacoleo carnifex (194)
and Priscileo roskellyae (196). The lowest was also in a fossil
marsupial, Thylacosmilus atrox (41). Among extant carni-
vorous mammals the highest BFQ was in the Tasmanian
devil, Sarcophilus harrisii (181). For placentals, BFQ was
greatest in the Pleistocene dire wolf, Canis dirus (163).
Another canid, the African hunting dog, Lycaon pictus, had
the highest BFQ for living Carnivora (142).
Mean BFQ was higher in marsupials than placentals
(158 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).
However, relative to body mass, CB
S
was significantly
higher in dasyuromorphians than in canids (F
1,13
Z33.51,
p!0.01) and significantly higher in thylacoleonids than in
cats (F
1,11
Z11.84, p!0.01).
The average BFQ for Felidae (104) was slightly less
than in Canidae (110) and dogs had greater head to body
size (figure 2), but the difference in this instance was not
significant. Across all taxa, skull width was a better
predictor of CB
S
than skull length (r
2
Z0.92 and 0.78,
respectively; Thomason 1991).
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. harrisii). 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 1983).
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 2002).
Amo ng extant canids, the four hypercarnivores that
often prey on animals larger than themselves, the grey
wolf (Canis lupus lupus), dingo (C. l. dingo), African
hunting dog (L. pictus) and the dhole (Canis alpinus), have
the highest BFQ (108–142). BFQ was consistently lower
in the five more solitary, omnivorous foxes, jackals and
coyote characterized by relatively low maximal prey sizes
(80–97). 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 la rge prey (table 2).
B
S
adjusted for body mass was also low in bears
(44–78), which are restricted to relatively small prey
(Meers 2002). BFQ was higher in extant dasyuromor-
phian marsupials, but the same trends were evident. The
lowest BFQ was in the eastern quoll (Dasyurus viverrinus),
which takes comparatively smaller p rey and is less
carnivorous than the other marsupials considered (see
below). Overall, BFQ was 100 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
100 (table 2). The difference between large and small prey
specialists was significant (t(28)ZK4.92, p!0.01) and
hypercarnivores had significantly higher values for
BFQ than more o mnivorous species (t(28)ZK3.33,
p!0.02; table 2).
4. DISCUSSION
(a) Comparisons between extant taxa
Results suggest that, relative to body mass, calculated
canine B
S
is considerably higher in marsupials than in
Th.c
Sm.f
Cr.c
C.l.l
S.h
D.m
C.l.d
C.la
T.c
V.v
P.l
L.p
F.c
P.o
Thy.a
1.5
2.0
2.5
3.0
3.5
0 0.5 1.0 1.5 2.0 2.5 3.0
log10 BoM (kg)
log10 CBs (N)
F.s
+
Figure 1. Log predicted canine bite force (CB
S
) plotted against log body mass (BoM). Reg ression for all extant taxa Z solid
black line. Individual data points are: for felids (open triangles), canids (grey filled triangles), dasyuromorphians, grey filled
squares, thylacoleonids (black filled squares), hyaenids (grey filled diamonds), ursids, a mustelid and a viverrid (g rey crosses),
and a thylacosmilid (open squares). Species abbreviations as in table 1.
2 S. Wroe and others Bite force and predatory behaviour
Proc. R. Soc. B
placentals and this cannot simply be explained by
differences in head size. The presence of the superfast
myosin isoform in both carnivorans and dasyuromor-
phians suggests that their muscle microphysiology is
similar (Hoh et al. 2001). Differences between these two
groups may relate to brain volumes, which, in carnivor-
ans, are around two and a half times that of marsupial
carnivores (Wroe et al. 2003). Within the temporal
region of the skull, cross-sectional area places limits on
the maximal force that can be generated by muscle
(Thomason 1991), 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 1969)
and through greater efficiency may be able to accom-
plish similar results with less B
S
. Because mean BFQ in
marsupials is much high er than in placentals, our
finding that the relatively omnivorous D. viverrinus has
a BFQ well within the range of hypercarnivorous
placentals is consistent with this interpretation. 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
Table 1. Measurements of basal skull length (BSL) and maximum skull width at the zygoma (SWZ); and estimates of body mass
(BoM), canine bite force (CB
S
), and bite force quotient (BFQ), for 39 taxa of recent and fossil mammals.
(Measurements and calculations were taken from prepared skulls. Methods for body mass estimations given in Electronic
Appendix, section A. Fossil taxa indicated with †.)
species family BSL (cm) SWZ (cm) BoM (kg) CB
S
(N) BFQ
Alopex lagopus Canidae 13.86 8.05 8.2 178 97
Canis alpinus Canidae 17.69 10.78 16.5 314 112
Canis aureus Canidae 13.53 8.12 7.7 165 94
Canis lupus dingo (C l.d) Canidae 18.04 9.97 17.5 313 108
Canis lupus hallstromi Canidae 15.95 9.41 12.3 235 100
Lycaon pictus (L.p) Canidae 18.52 13.18 18.9 428 142
Vulpes vulpes (V.v) Canidae 13.79 7.35 8.1 164 92
Urocyon cineroargentus Canidae 11.91 6.14 5.3 114 80
Canis latrans (C.la) Canidae 18.85 9.86 19.8 275 88
Canis lupus lupus (C.l.l) Canidae 22.92 13.22 34.7 593 136
Canis dirus Canidae 26.19 17.58 50.8 893 163
Ursus americanus Ursidae 24.39 17.2 105.2 541 64
Ursus arctos Ursidae 26.96 16.28 128.8 751 78
Ursus thibetanus Ursidae 20.92 11.07 77.2 312 44
Meles meles Mustelidae 12.31 8.05 11.4 244 109
Gennetta tigrinus Viverridae 10.93 5.19 6.2 73 48
Crocuta crocuta (Cr.c) Hyaenidae 23.64 16.73 69.1 773 117
Hyaena hyaena Hyaenidae 19.98 15.18 40.8 545 113
Proteles cristatus Hyaenidae 12.46 7.22 9.3 151 77
Panthera onca (P. o ) Felidae 22.25 18.63 83.2 1014 137
Panthera tig ris Felidae 28.86 22.73 186.9 1525 127
Acinonyx jubatus Felidae 15.93 12.30 29.5 472 119
Felis yagouaroundi Felidae 10.09 6.94 7.1 127 75
Lynx rufus Felidae 7.58 5.93 2.9 98 100
Felis concolor (F. c ) Felidae 16.77 12.92 34.5 472 108
Felis sylvestris (F. s ) Felidae 7.51 5.39 2.8 56 58
Neofelis nebulosa Felidae 16.74 11.88 34.4 595 137
Panthera leo (P. l ) Felidae 33.41 24.81 294.6 1768 112
Panthera pardus Felidae 18.01 13.02 43.1 467 94
Smilodon fatalis †(Sm.f) Felidae 29.48 19.53 199.6 976 78
Dasyurus maculatus (D.m) Dasyuridae 10.09 6.01 3.0 153 179
Dasyurus viverrinus Dasyuridae 7.27 4.15 0.87 65 137
Sarcophilus harrisii (S.h) Dasyuridae 13.96 11.17 12.0 418 181
Nimbacinus dicksoni Thylacinidae 13.24 8.08 5.3 267 189
Thylacinus cynocephalus (T. c) Thylacinidae 25.04 14.83 41.7 808 166
Priscileo roskellyae Thylacoleonidae 8.34 6.34 2.7 184 196
Wakaleo vanderleurei Thylacoleonidae 18.53 12.58 41.4 673 139
Thylacoleo carnifex †(Th.c) Thylacoleonidae 24.04 20.15 109.4 1692 194
Thylacosmilus atrox †(Thy.a ) Thylacosmilidae 257.71 139.65 106 353 41
Bite force and predatory behaviour S. Wroe and others 3
Proc. R. Soc. B
musculature to assist in jaw closure (Van Valkenburgh
et al. 2003; Anto
´
n et al. 2004).
(b) Bite force and osteophagy
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 re garding 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
0
5
10
15
20
25
30
35
40
1 10 100 1000
BoM (kg)
BSL (cm)
Figure 2. Basal skull length (BSL) plotted against body mass (BoM). 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.
Table 2. Bite force adjusted for body mass allometry (BFQ), maximal prey size and feeding category in 31 extant mammalian
carnivores.
(RMPS, maximal prey size (1, greater than maximal body mass of predator; 2, less than maximal body mass of predator); FC,
feeding category (1, hypercarnivore; 2, other); ‘—’, insufficient data. Maximal body mass data largely from Meers (2002).For
additional data see Electronic Appendix, section A.)
species common name family BFQ RMPS FC
Alopex lagopus Arctic fox Canidae 97 2 2
Canis alpinus Dhole Canidae 112 1 1
Canis aureus golden jackal Canidae 94 2 2
Urocyon cineroargentus grey fox Canidae 80 2 2
Canis lupus dingo Dingo Canidae 108 1 2
Canis lupus hallstromi singing dog Canidae 100
Lycaon pictus African hunting dog Canidae 142 1 1
Vulpes vulpes red fox Canidae 92 2 2
Canis latrans Coyote Canidae 88 2 2
Canis lupus lupus grey wolf Canidae 136 1 1
Ursus americanus black bear Ursidae 64 2 2
Ursus arctos brown bear Ursidae 78 2 2
Ursus thibetanus Asiatic bear Ursidae 44 2 2
Gennetta tigrinus striped genet Viverridae 48 2 2
Meles meles European badger Mustelidae 109 2 2
Crocuta crocuta spotted hyaena Hyaenidae 117 1 1
Hyaena hyaena brown hyaena Hyaenidae 113 1 1
Proteles cristatus Aardwolf Hyaenidae 77 2 2
Panthera onca jaguar Felidae 137 1 1
Panthera tigris tiger Felidae 127 1 1
Felis concolor cougar Felidae 108 1 1
Acinonyx jubatus cheetah Felidae 119 1 1
Felis yagouaroundi jaguarundi Felidae 75 2 1
Lynx rufus bobcat Felidae 100 1 1
Felis sylvestris catus cat Felidae 58 2 1
Neofelis nebulosa clouded leopard Felidae 137 1 1
Panthera leo lion Felidae 112 1 1
Panthera pardus leopard Felidae 94 1 1
Dasyurus maculatus spotted-tailed quoll Dasyuridae 179 1 1
Dasyurus viverrinus eastern quoll Dasyuridae 137 2 2
Sarcophilus harrisii Tasmanian devil Dasyuridae 181 1 1
4 S. Wroe and others Bite force and predatory behaviour
Proc. R. Soc. B
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 1983). In hyaenids, maximum
forces may be generated immediat ely anterior to the
carnassial (Werdelin 1989). Moreover, from observation,
osteophages may use kinetic, rather than static bites to
crack bones, fur ther 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. crocuta, H. hyaena and S. harrisii.
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.
(c) Bite force and the prediction of feeding ecology
(i) Extant carnivores
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 viverr id 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. cristatus subsists largely on termites. Interest-
ingly, 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. cristatus may be related to intra and/or interspecific
defence. 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 mor-
phologies and killing behaviour. This example demon-
strates 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.
(ii) Extinct taxa with morphologically similar
extant relatives
Neither cranial, nor post-cranial morphology of the
thylac ine, Thylacinus cynocephalus, differ greatly from
those of living dasyuromorphians (Wroe 2003). Based
on low rates of canine tooth breakage and snout
morphology, it has been argued that thylacines may have
been restricted to small or medium sized prey (Jones 2003;
Johnson & Wroe 2003). Our finding that BFQ was
comparable to extant dasyuromor phians known t o
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. dirus) is similar to that of living relatives. If
C. dirus was a social hunter, then its high BFQ (163)
relative to extant canids su ggests that it preyed on
relatively large animals.
(iii) Extinct taxa without morphologically similar
living relatives
Some fossil taxa included in our analyses clearly fell well
outside extant morphotypes. Major differences between
the sabrecat Smilodon fatalis and all extant felids,
including extreme hypertr ophy of the canine s, very
powerful forelimbs, lengthening of the neck and short-
ening of the lumbar region, leave little doubt that it used
killing techniques not represented among living carni-
vores and regularly took large prey (Janis 1994; Anto
´
n&
Galobar t 1999; Anto
´
n et al. 2004; Argot 2004).
Notwithstanding its high absolute CB
S
compared with
large living felids, BFQ in S. fatalis was low (78). Having
secured large prey with its muscular forelimbs, S. fatalis
used its hypertrophied canines to effect fatal trauma
(Anto
´
n et al. 2004; Argot 2004). 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. atrox, both BFQ (41) and absolute B
S
were
extremely low, but as with S. fatalis,post-cranial
adaptations and canine morphology indicate a killing
technique without present day analogy and systematic
predation on relatively large taxa (Argot 2004).
Current functional models of sabretooth killing be-
haviour include: (i) the ‘stabbing’ model in which the
force applied to the canines is primarily neck-driven
(Anto
´
n & Galobart 1999; Argot 2004) and (ii) a ‘canine-
shear bite’, in which significant absolute force is required
of the jaw adductors in conjunction with input from neck
muscles (Akersten 1985). Because absolute CB
S
in
S. fatalis is high, and BFQ is considerably higher than
in T. atrox, our results are consistent with the ‘canine
shear-bite’ model for the sabrecat, with significant force
required of the jaw adductors in conjunction with cervical
musculature. From estimates of bending strength in the
mandibular cor pus, Bickne vicus & Van Valkenburgh
(1996) posit that S. fatalis may have applied a sustained
throat clamping bite. Our results do not rule out
this possibility, but are contra the conclusion that bite
Bite force and predatory behaviour S. Wroe and others 5
Proc. R. Soc. B
force in S. fatalis was comparable to that of similar sized
pantherines. 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. atrox applied a
sustained throat bite to dispatch large prey.
For the marsupial lion, T. carnifex, BFQ was the highest
of any large predator and its CB
S
approached that of a lion
(Panthera leo ) more than twice its size (table 1). If the
killing mechanism of T. carnifex was functionally equival-
ent to that of extant felids, our results suggest that it could
take prey much larger than itself. 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. 1982; Wroe et
al. 2004a). Our findings confirm that short outlever arms
and anteriorly placed muscle resultants conferred high
mechanical efficiency (Wells et al. 1982). The marsupial
lion’s vertical shearing ‘carnassial’ cheek–teeth are rela-
tively larger than in any other mammalian carnivore (Wells
et al. 1982; Werdelin 1988). Brought together with a very
high B
S
, these carnassials may have enabled T. carnifex to
rapidly slice through tracheas or vital blood vessels and
quickly dispatch large, potentially dangerous prey,
although mechanical simulation will be required to
confirm this. 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 1994; Wroe 2003; Argot
2004), the marsupial lion may have been capable of taking
sub-adults of the heaviest available prey (Wroe et al.
2004b).
5. CONCLUSIONS
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 import-
ant component of a predator’s biomechanical perform-
ance. Adjusted for body mass, our estimates of B
S
(i) show
variations that are broadly consistent with patterns of
predatory behaviour and diet obser ved in extant carni-
vores, (ii) provide a basis for predicting maximal prey size
in extinct mammalian predators that are morpholog ically
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. Mechanical simulations a nd
further investigations of jaw muscle anatomies and the
mechanics of the skull, using FEA modelling (Daniel &
McHenr y 2001; Snively & Russell 2002; Rayfield 2004)
and in vivo force measurement, will fur ther clarify these
patterns and permit examination of the following predic-
tions inferred from our analyses: (i) the biomechanics of
osteophagy are more tightly constrained by the structural
properties of the carnivore’s skull and dentition than by
muscle force, (ii) non-osteophagous large prey specialists
should be reluctant to apply all available muscle force in a
post-canine bite, because of the threat of material failure
(moreover, their crania will be optimized to resist stress
at the canines, while in specialist bone-crackers skulls will
be optimized to resist stress near the carnassial) and (iii) if
in vivo testing shows that placentals produce bite forces
that are similar after allometric adjustment to marsupials,
it will be because of differences in muscle anatomy and
organization.
We are much indebted to M. Meers, J. Farlow, A. Herrel,
G. Erickson, B. Van Valkenburgh, L. Werdelin, E. Rayfield,
E. Snively, D. Hu ber, C. Vineyard, M. Crowther,
P. Christiansen and M. Jones for advice on previous versions
and the provision of unpublished data. We also thank
D. Wroe, P. Adam, P. Clausen, I. Johnston, S. Johnston,
D. Hochuli and K. Wyatt. Work was funded by a University of
Sydney Research Fellowship (to S.W.).
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Bite force and predatory behaviour S. Wroe and others 7
Proc. R. Soc. B
... pairs of teeth in contact during the bite, and only one of them is modelled here. Hence, the sphere is assigned a mass of m = 3 kg, being one fourth of the mass of a lion's head [121]. ...
... Additionally, a downwards force of F = 442 N is applied to the sphere as one fourth of a lion's bite strength [121]. The sphere is also assigned an initial velocity of v i = 2 m/s. ...
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It has been suggested that the large theropod dinosaur Tyrannosaurus rex was capable of producing extremely powerful bite forces and resisting multi-directional loading generated during feeding. Contrary to this suggestion is the observation that the cranium is composed of often loosely articulated facial bones, although these bones may have performed a shock-absorption role. The structural analysis technique finite element analysis (FEA) is employed here to investigate the functional morphology and cranial mechanics of the T. rex skull. In particular, I test whether the skull is optimized for the resistance of large bi-directional feeding loads, whether mobile joints are adapted for the localized resistance of feeding-induced stress and strain, and whether mobile joints act to weaken or strengthen the skull overall. The results demonstrate that the cranium is equally adapted to resist biting or tearing forces and therefore the 'puncture-pull' feeding hypothesis is well supported. Finite-element-generated stress-strain patterns are consistent with T. rex cranial morphology: the maxilla-jugal suture provides a tensile shock-absorbing function that reduces localized tension yet 'weakens' the skull overall. Furthermore, peak compressive and shear stresses localize in the nasals rather than the fronto-parietal region as seen in Allosaurus, offering a reason why robusticity is commonplace in tyrannosaurid nasals.
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Borophaginae is the largest of the three subfamilies of the dog family Canidae, with some 66 species, spanning approximately 34 m.y. (Orellan to Blancan). Not surprisingly, this extensive radiation of canids includes a diverse array of dietary types, ranging from hypocarnivorous to hypercarnivorous and durophagous. The last 16 m.y. of borophagine history is dominated by hypercarnivorous forms that were the dominant doglike predators within their faunas. Because of their relatively robust skeletons and their resemblance to extant hyenas in craniodental morphology, many or most of these hypercarnivorous species, particularly those of the late Miocene and Pliocene, have been assumed as primarily scavengers rather than hunters. The classification of most hypercarnivorous borophagines as scavengers relegates them to much less important roles in the ecology and evolution of their respective communities than does a classification as hunters. Unlike hunters, scavengers are unlikely to influence the evolution of the animals they eat, and are expected to exist at relatively low densities as do the only extant scavenging carnivorans, brown (Parahyaena brunnea) and striped hyenas (Hyaena hyaena). Given the substantial fossil record of the Borophaginae, it seems unlikely that all or most of the hypercarnivorous forms were primarily scavengers. Moreover, if some hunted, the larger species might be expected to have done so in groups, as large canids hunt in packs today. Here we examine possible foraging modes within the Borophaginae using morphometrics and two new approaches to estimating the typical prey size of extinct carnivores. The craniodental morphology of the Borophaginae is compared with that of the living Caninae and Hyaeninae (hyaenids exclusive of Proteles cristata, the aardwolf) based on measurements that reflect relative tooth size, jaw muscle leverage, rigidity of the dentary, and grinding versus slicing function of the teeth. The Borophaginae are found to be intermediate in morphology between the Caninae and Hyaeninae. Unlike hyaenids and like canines, they retain substantial postcarnassial molars. However, like hyaenids, the borophagines had significantly stronger jaws and enhanced jaw muscle leverage compared to other canids. Prey size is estimated for borophagines based on correlation between dentary height and typical prey size in living canids. These results are compared with those produced using a recently published energetic model that predicts that all carnivores larger than about 21 kg feed on prey as large or larger than themselves. The methods provide similar predictions, resulting in a list of 11 borophagines (all subtribes Aelurodontina and Borophagina) that probably consumed large prey. Comparisons with extant hyaenids reveal that the sole hunter of large prey, the spotted hyena (Crocuta), differs from the two mainly scavenging species, the brown and striped hyenas, in being significantly larger, more abundant, and widespread. Moreover, morphometric comparisons indicate that spotted hyenas have a more hypercarnivorous dentition. Given this, it is expected that the largest, most common borophagines with the most reduced dental grinding areas hunted most of their food. Based on their craniodental morphology and abundance in the record, Epicyon saevus, E. haydeni, Borophagus secundus, Aelurodon ferox, and A. taxoides were hunters. Although it is clear that Aelurodon and Borophagus were more capable of grasping prey than are extant canids, no borophagine evolved sharp, curved claws as in felids. Consequently, their ability to grapple with prey seems to have been limited, and packs were probably more successful at making a kill than individuals. Previous workers have argued against hunting in borophagines based on heavy dental wear, robust skeletal morphology, and external brain features. None of these precludes either hunting or hunting in packs in our view, and sharp teeth are not required for making a kill. While limb morphology and skeletal proportions of most or all borophagines do not appear adapted for the kind of hunts observed today in the African wild dog Lycaon pictus, long-distance, high-speed pursuits over shorter distances would have been possible for borophagines. The association between external brain morphology and social behavior in living carnivorans has not been fully explored, and seems a weak criterion for sociality in extinct species.
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Predators with Pouches provides a unique synthesis of current knowledge of the world’s carnivorous marsupials—from Patagonia to New Guinea and North America to Tasmania. Written by 63 experts in each field, the book covers a comprehensive range of disciplines including evolution and systematics, reproductive biology, physiology, ecology, behaviour and conservation. Predators with Pouches reveals the relationships between the American didelphids and the Australian dasyurids, and explores the role of the marsupial fauna in the mammal community. It introduces the geologically oldest marsupials, from the Americas, and examines the fall from former diversity of the larger marsupial carnivores and their convergent evolution with placental forms. The book covers all aspects of carnivorous marsupials, including interesting features of life history, their unique reproduction, the physiological basis for early senescence in semelparous dasyurids, sex ratio variation and juvenile dispersal. It looks at gradients in nutrition—from omnivory to insectivory to carnivory—as well as distributional ecology, social structure and conservation dilemmas.
Article
The borophagine canids were bone-cracking scavengers in the Miocene-Pleistocene of North America. In this they parallel the Recent hyenas. This paper analyzes the borophagine adaptation in relation to that of hyaenids, using Osteoborus cyonoides as an example. The emphasis during canid evolution on the posterior molars, which is a derived condition, created a constraint on the adaptation of borophagines. This constraint meant that the borophagines used P4/4 as bone-cracking teeth, whereas hyaenids use P3/3. Other than the evolution of a specialized bone-cracking tooth, the borophagines adapted to bone cracking by evolving a vaulted and strengthened skull for the dissipation of the strong forces generated during bone cracking. -from Author
Article
The feeding behavior of the theropod dinosaur Tyrannosaurus rex is investigated through analysis of two variables that are critical to successful predation, bite force and prey body mass, as they scale with the size of the predator. These size-related variables have important deterministic effects on the predator's feeding strategy, through their effects on lethal capacity and choice of prey. Bite force data compiled for extant predators (crocodylians, carnivorans, chelonians and squamates) are used to establish a relationship between bite force and body mass among extant predators. These data are used to estimate the maximum potential bite force of T. rex, which is between about 183,000 and 235,000 N for a bilateral bite. The relationship between maximum prey body mass and predator body mass among the same living vertebrates is used to infer the likely maximum size of prey taken by T. rex in the Late Cretaceous. This makes it possible to arrive at a more rigorous assessment of the role of T. rex as an active predator and/or scavenger than has hitherto been possible. The results of this analysis show that adult Triceratops horridus fall well within the size range of potential prey that are predicted to be available to a solitary, predaceous T. rex. This analysis establishes boundary conditions for possible predator/prey relationships among other dinosaurs, as well as between these two taxa.
Article
The morphology of the cervical vertebrae and skull structures associated with the neck musculature was studied in the felid sabertooth Homotherium latidens from the Spanish early Pleistocene site of Incarcal. Cervical anatomy of Homotherium was compared to that of modern pantherine cats, Smilodon, and other sabertoothed carnivores, and the relationship between neck function and killing behavior was investigated. Homotherium latidens possesses the structures associated with the canine shear-bite, as described in Smilodon. Our study of muscle insertion areas in the cervical vertebrae of Homotherium does not support previous statements about unusually strong scalenes and their role in stabbing. Instead, we see evidence of increased muscular control of various movements of the neck, including lateral flexion, depression and extension. These features, and the greater relative length of the neck in Homotherium and other machairodonts, are interpreted as adaptations for delivering a canine shear-bite in precise areas of the body of relatively large prey.