Content uploaded by Stephen W Wroe
Author content
All content in this area was uploaded by Stephen W Wroe
Content may be subject to copyright.
Content uploaded by Stephen W Wroe
Author content
All content in this area was uploaded by Stephen W Wroe
Content may be subject to copyright.
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.).
REFERENCES
Akersten, W. A. 1985 Canine function in Smilodon
(Mammalia: Felidae: Machairodontinae). Contrib. Sci.
Nat. Hist. Mus. Los Angeles County 356, 1–22.
Anto
´
n, M. & Galobart, A
´
. 1999 Neck function and predatory
behaviour in the scimitar toothed cat Homotherium latidens
(Owen). J. Vertebr. Paleontol. 19, 771–784.
Anto
´
n, M., Salesa, M. J., Pastor, J. F., Sanchez, I. M., Fraile,
S. & Morales, J. 2004 Implications of the mastoid anatomy
for larger extant felids for the evolution and predator y
behaviour of sabretoothed cats (Mammalia, Carnivora,
Felidae). Zool. J. Linn. Soc. 140, 207–221.
Argot, C. 2004 Functional adaptive features of the postcranial
skeleton of a sabertooth borhyaenoid, Thylacosmilus atrox
(Metatheria), and palaeobiologic implications. Alcheringa
28, 229–266.
Bicknevicus, A. R. & Van Valkenburgh, B. 1996 Design for
killing: craniodental adaptations of predators. In Carnivore
behavior, ecology and evolution, vol. 2 (ed. J. L. Gittleman)
pp. 393–428. Ithaca: Cornell University Press.
Binder, W. J. & Van Valkenburgh, B. 2000 Development of
bite strength and feeding behaviour in juvenile spotted
hyena (Crocuta crocuta). J. Zool. Lond. 252, 273–283.
Daniel, W. J. T. & McHenry, C. 2001 Bite force to skull stress
correlation—modelling the skull of Alligator mississippiensis.
In Crocodilian biology and evolution (ed. G. C. Grigg,
F. Seebacher & C. E. Franklin), pp. 135–143. Chipping
Norton: Surrey Beatty.
Dessem, D. & Druzinsky, R. E. 1992 Jaw-muscle activity in
ferrets (Mustela putorius furo). J. Morphol. 213, 275–286.
Ewer, R. F. 1969 Some observations on the killing and eating of
prey by two dasyurid mar supials: the Mulgara, Dasycercus
cristicauda, and the Tasmanian devil, Sarcophilus harrisii. Z.
Tierpsychol. 26, 23–38.
Farlow, J. O. & Pianka, J. R. 2002 Body size overlap, habitat
partitioning and living space requirements of terrestrial
vertebrate predators: implications for the palaeoecology of
large theropod dinosaurs. Hist. Biol. 16, 21–40.
Greaves, W. S. 1983 A functional analysis of carnassial biting.
Zool. J. Linn. Soc. 20, 353–363.
Hoh, J. F. Y., Lim, J. H. Y., Kang, L. D. H. & Lucas, C. A.
2001 Expression of superfast myosin in the jaw-closing
muscles of Crocodylus porosus.InCrocodilian biology and
evolution (ed. G. C. Grigg, F. Seebacher & C. E. Franklin),
pp. 156–164. Chipping Norton, NSW: Surrey Beatty.
Janis, C. M. 1994 The sabertooth’s repeat performances.
Nat. Hist. 103, 78–83.
Johnson, C. & Wroe, S. 2003 Causes of extinctions of
vertebrates during the Holocene of mainland Australia:
arrival of the dingo or human impact? Holocene
13, 109–116.
6 S. Wroe and others Bite force and predatory behaviour
Proc. R. Soc. B
Jones, M. E. 2003 Convergence in ecomorphology and
guild structure among marsupial and placental carnivores.
In Predators with pouches: the biology of carnivorous
marsupials (ed. M. Jones, C. Dickman & M. Archer),
pp. 285–296. Collingwood: CSIRO Publishing.
Meers, M. B. 2002 Maximum bite force and prey size of
Tyrannosaurus rex and their relationships to the inference
of feeding behaviour. Hist. Biol. 16, 1–12.
Rayfield, E. J. 2004 Cranial mechanics and feeding
in Tyrannosaurus rex. Proc. R. Soc. B 271, 1451–1459.
(doi:10.1098/rspb.2004.2755.)
Snively, E. & Russell, A. 2002 The tyrannosaurid metatarsus:
bone strain and inferred ligament function. Senck. Lethaea
82, 35–42.
Thomason, J. J. 1991 Cranial strength in relation to
estimated biting forces in some mammals. Can. J. Zool.
69, 2326–2333.
Van Valkenburgh, B., Sacco, T. & Wang, X. 2003 Pack
hunting in Miocene borophagine dogs: evidence from
craniodental morphology and body size. Bull. Am. Mus.
Nat. Hist. 279, 147–162.
Vizcaı
´
no, S. F. & de Iuliis, G. 2003 Evidence for advanced
carnivory in fossil armadillos (Mammalia Xenarthra,
Dasypodidae). Paleobiology 29, 123–1388.
Wells, R. T., Horton, D. R. & Rogers, P. 1982 Thylacoleo
carnifex Owen (Thylacoleonidae): marsupial carnivore? In
Carnivorous marsupials (ed. M. Archer), pp. 573–586.
Sydney: Royal Zoological Society of NSW.
Werdelin, L. 1988 Circumventing a constraint: the case of
Thylacoleo carnifex (Marsupialia: Thylacoleonidae). Aust.
J. Zool. 36, 565–571.
Werdelin, L. 1989 Constraint and adaptation in the bone-
cracking canid Osteoborus (Mammalia: Canidae). Paleo-
biology 15, 387–401.
Wroe, S. 2003 Australian marsupial carnivores: an over view
of recent advances in palaeontology. In Predators with
pouches: the biolog y of carnivorous marsupials (ed. M. E.
Jones, C. Dickman & M. Archer), pp. 102–123. Colling-
wood: CSIRO.
Wroe, S., Brammall, J. & Cooke, B. N. 1998 The skull of
Ekaltadeta ima (Marsupialia: Hypsiprymnodontidae):
an analysis of some cranial features among marsupials
with notes on the inference of carnivory in mammals.
J. Paleontol. 72, 738–751.
Wroe, S., Myers, T., Seebacher, F., Kear, B., Gillespie, A.,
Crowther, M. & Salisbury, S. 2003 An alternative method
for predicting body-mass: the case of the marsupial lion,
Thylacoleo carnifex. Paleobiology 29, 404–412.
Wroe, S., Argot, C., Crowther, M. & Dickman, C. 2004a On
the rarity of big fierce carnivores and primacy of isolation
and area: tracking large mammalian carnivore diversity
on two isolated continents. Proc. R. Soc. B 271, 1203–1211.
(doi:10.1098/rspb.2004.2694.)
Wroe, S., Crowther, M., Dortch, J. & Chong, J. 2004b
The size of the largest marsupial and why it matters.
Proc. R. Soc. B 271 (Suppl.), S34–S36. (doi:10.1098/
rsbl.2003.0095.)
The supplementary Electronic Appendix is available at http://dx.doi.
org/10.1098/rspb.2004.2986 or via http://www.pubs.royalsoc.ac.uk.
As this paper exceeds the maximum length normally permitted, the
authors have agreed to contribute to production costs.
Bite force and predatory behaviour S. Wroe and others 7
Proc. R. Soc. B
