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Proc. R. Soc. Lond. B (2004) 271, 1451–1459 1451 2004 The Royal Society
DOI 10.1098/rspb.2004.2755
Downloaded from rspb.royalsocietypublishing.org on May 23, 2011
(a) (b)
n l
or po ltf sq
p aof
en mf
m qi
m
j
pt q
tearing bite vertical bite
Figure 1. Tyrannosaurus rex skull and FEM. (a) Skull of BHM 3033, left lateral view; and (b) 2D FE-mesh of BHM 3033
depicting skull as ‘fused’ without mobile sutures. Grey areas indicate surfaces constrained from moving in all translatory
directions, arrows indicate direction of bite force applied to all teeth, either vertical or horizontal ‘tearing’. Abbreviations:
aof, antorbital fenestra; en, external naris; j, jugal; l, lacrimal; ltf, lower temporal fenestra; m, maxilla, n, nasals; or, orbit;
p, premaxilla; po, postorbital; pt, pterygoid; q, quadrate; qj, quadratojugal; sq, squamosal. Scale bar 10 cm.
2002; Jenkins et al. 2002; Snively & Russell 2002), includ- mobility are based on observations of numerous specimens
ing large theropod crania (Rayfield et al. 2001, 2002). (see above).
All previous FEMs have treated the skull as a single unit
(e.g. Rayfield et al. 2001). In this paper, the stress environ- (b) Jugal–postorbital contact
ment of a fused FE-skull model is assessed, after which The postorbital laps a smooth groove running down half the
results obtained from the fused skull model are used to length of the anterior surface of the ascending process of the
predict the mechanical effect of introducing regions of jugal (figure 2a). Postorbital–jugal contact surfaces are variably
mobility. Introducing simple sutural contacts into the rugose, with BHM 3033 bearing smooth articulation surfaces
FEM then permits an evaluation of these predictions. while ANMH 5027 and MOR 555 possess more rugose surfaces
Such investigation highlights the potential of FEA in test- along the length of the contact. Furthermore, in AMNH 5027
ing hypotheses of cranial design and evolution. The results and MOR 555, the anterior surface of the lower half of the
of the FEM system have implications for the suitability ascending process bears a pronounced roughened region that
of puncture–pull as a feeding strategy for T. rex and the marks the ventral extent of postorbital overlap. A depressed
functional significance, if any, of maintaining patent groove running along the posterior surface of the descending
sutures between cranial bones in an animal with an appar- process of the postorbital marks the contact with the jugal. In
ently bone-crushing bite. all specimens observed and those documented in the literature
(e.g. Brochu 2003) this contact is patent and potentially mobile,
with the exception of MOR 008, in which the left jugal–
2. MATERIAL AND METHODS
postorbital contact is fused internally, probably as a result of
Specimens studied: AMNH 5027: American Museum of the advanced age of this specimen (Molnar 1991). Additionally,
Natural History, New York; BHM 3033: Black Hills Museum, minor interdigitations at the anterior edge of the postorbital–
Hill City, South Dakota; MOR 555: Museum of the Rockies, jugal suture in AMNH 5027 may have limited movement along
Bozeman, Montana; SDSM 12047: South Dakota School of the suture in this particular skull. Overlapping flanges at the
Mines, Rapid City, South Dakota; RTMP 81.6.1: Royal Tyrell postorbital–jugal contact surface generally prevent rotation in
Museum of Palaeontology, Drumheller, Canada. the transverse and parasagittal axis, but sliding of the jugal
anteroventrally–posterodorsally against the postorbital is permit-
(a) Anatomical observations of sutural mobility ted (figure 2a).
Four facial sutures commonly appear patent and slightly
mobile in T. rex skulls observed. These are the maxilla–jugal, (c) The maxilla–jugal contact
postorbital–jugal, quadratojugal–jugal and postorbital–squam- The anterior portion of the jugal forks medially and laterally,
osal contacts. Two of these sutures are not universally mobile: ventral to its contact with the lacrimal. The medial fork laps on
the quadratojugal–jugal suture is fused in some specimens (e.g. to the medial surface of the maxilla while the lateral fork further
AMNH 5027) and movement at the postorbital–squamosal divides into a dorsal and ventral component, between which
would be restricted by attachment of the superficial and possibly slots a narrow process of the maxilla (as noted by Molnar
medial slips of the M. adductor mandibulae externus, which (1991)). Additionally the dorsal edge of an extended maxillary
originate in part along the lateral supra-temporal fenestra mar- process laps the ventrolateral edge of the jugal along a pos-
gin. The remaining two sutures, namely the maxilla–jugal and teriorly extended groove (figure 2b). In none of the observed
postorbital–jugal contacts, remain patent in nearly all observed specimens was the maxilla–jugal contact fused. Dorsoventral
specimens, and are the main focus of this analysis. Patent, yet and mediolateral movement plus rotation about the transverse
apparently immobile, sutures exist between many other cranial and parasagittal axes is prevented by the interlocking mediolat-
bones, and future analysis will attempt to elucidate the signifi- eral and dorsoventral articulations. The distinct anteroposterior
cance of these sutures. It should be noted that although the orientation of all contacts suggest that slight anteroposterior
FEMs use a particularly loosely articulated skull (BHM 3033; sliding movement plus some limited rotation about the longi-
figure 1) as a template, the following descriptions of cranial tudinal axis of the jugal is permitted at this suture (figure 2b).
(a) (b)
m aof l
po
po pal ltf
l or ltf
j
sq
m
qi
j
(c) (d)
Figure 2. Sutural morphology and mobility. (a) Postorbital–jugal suture in Tyrannosaurus rex; (b) maxilla–jugal suture in T.
rex; (c) 2D FEM of T. rex skull with mobile postorbital–jugal contact; and (d ) 2D FEM of T. rex skull with mobile maxilla–
jugal contact. Double-headed arrows indicate direction of slight adjustive movement at suture. Single-headed arrows indicate
location of ‘suture’ in FE-mesh. Illustrations after BHM 3033. Grey areas and abbreviations as defined in figure 1; pal,
palatine.
(d ) Finite element modelling postorbital–jugal suture (not shown). The mobile FEMs (figure
A two-dimensional (2D) FEM of a T. rex skull was created. A 2c,d) were created by introducing breaks in the FE-mesh at the
lateral-aspect photograph of BHM 3033 (Hell Creek Formation, location of the appropriate suture in the actual skull.
South Dakota; figure 1a) was digitized in Scion Image
(www.scioncorp.com). Outline x,y coordinates were imported (e) Bite force magnitude and distribution
into the Geostar geometry creator component of the Cosmosm Tyrannosaurus rex may have been capable of generating
FEA package (v. 2.0 for Unix; SRAC Corp. CA, USA and Cenit 13 400 N bite force at a single posterior tooth (Erickson et al.
Ltd, UK). A series of 5 cm thick surfaces was created then 1996). Using moment arm calculations to extrapolate this value
‘meshed’ to produce an interconnected grid of three-noded tri- rostrally along the tooth row, a total of 78 060 N was divided
angular FEs representing the lateral aspect of the cranium between biting teeth (therefore assuming 156 120 N bilaterally,
(figure 1b). Each element was attributed the mechanical proper- less than, but approaching, values estimated by Meers (2002)).
ties of bovine Haversian bone after Rayfield et al. (2001). However, it may be argued that being first to contact a prey
The model represents a 2D section of the left aspect of the item, the large caniniform teeth received the majority of bite
skull: the palate and braincase were not included. 2D models force (sensu Rayfield et al. 2001). In accordance with this sugges-
are used as a first approximation in orthopaedic biomechanical tion, the two large caniniform teeth (figure 1b) were allocated
modelling, and using simple FEMs offers the potential to gener- 13 000 N each, while the smaller incisiform and posterior maxil-
ate mechano-functional hypotheses (Carter et al. 1998), which lary teeth were allocated lesser values scaled to the size of the
may be further tested by digitally modifying future models. The teeth. In this model a total of 31 000 N was applied.
2D models presented here were constrained from moving about FEAs were performed to assess the stress response to this load
the lower temporal fenestra (figure 1b) to focus upon the stress in a fused or mobile skull. First, vertical dorsally directed bite
response of the rostrum, which as a more planar structure than forces representing the ‘puncture’ aspect of feeding were applied
the posterior skull is more appropriate for 2D modelling. Stress to the tooth tips in all four models and the corresponding stress
patterns posterior to the constraining surfaces, including the and strain patterns were calculated. The analyses were then
effect of condylar and muscular forces in the posterior skull, rerun applying instead a horizontally orientated, anteriorly
were not analysed and this region of the skull should therefore directed bite force to represent the ‘pull’ tearing force, generated
be ignored in relevant figures. by the resistance of flesh and bone against the teeth during tug-
Four structurally different FEMs were constructed by manip- ging and flesh-procuring behaviour (figure 1b). Multiple tearing
ulating the base model: an initial ‘fused’ solid model with no analyses applying moment-calculated forces, variable tooth-size-
mobile regions (figure 1b) and three modified ‘mobile’ models related forces and equal forces to all teeth were investigated.
showing differing degrees of intracranial mobility; a mobile post- Because bite force was hypothetical but identical in related mod-
orbital–jugal suture (figure 2c), a mobile maxilla–jugal suture els, relative rather than absolute patterns of stress and strain
(figure 2d), and a model with both a mobile maxilla–jugal and could be assessed.
biting tearing
(a) 1.60270 × 106 (d) 2.89480 × 106
–1.1411 × 105 1.06920 × 105
–1.8309 × 106 –2.6810 × 106
–3.5478 × 106 –5.4689 × 106
–5.2646 × 106 –8.2568 × 106
–6.9815 × 106 –1.1045 × 107
–8.6983 × 106 –1.3833 × 107
–1.0415 × 107 –1.6620 × 107
–1.2132 × 107 –1.9408 × 107
Figure 3. Stress in the fused FE Tyrannosaurus rex skull model generated by vertical biting (left column) or tearing (right
column). (a) Principal stress 3 [P3], compressive stress; (b) P1 tensile stress; (c) shear stress; (d ) P3 compressive stress; (e) P1
tensile stress; and ( f ) shear stress. Divergent arrows indicate orientation of tensile stress trajectories; convergent arrows
indicate orientation of compressive stress trajectories. Units are Pa or Nm⫺2. See electronic Appendix C for strain plots.
biting tearing
(a) 1.77650 × 106 (e) 2.88710 × 106
–2.1138 × 105 9.4602 × 104
–2.1993 × 105 –2.6979 × 106
–4.1871 × 106 –5.4903 × 106
–6.1750 × 106 –8.2828 × 106
–8.1629 × 106 –1.1075 × 107
–1.0151 × 107 –1.3868 × 107
–1.2139 × 107 –1.6660 × 107
–1.4126 × 107 –1.9453 × 107
Figure 4. Stress in the mobile FE Tyrannosaurus rex skull models generated by vertical biting (left column) or tearing (right
column). (a,b,e, f ) have a mobile postorbital–jugal suture; (c,d,g,h) have a mobile maxilla–jugal suture. (a) Principal stress 3
[P3], compressive stress; (b) P1 tensile stress; (c) P3 compressive stress; (d ) P1 tensile stress; (e) P3 compressive stress; ( f ) P1
tensile stress; ( g) P3 compressive stress; and (h) P1 tensile stress. Divergent arrows indicate orientation of tensile stress
trajectories; convergent arrows indicate orientation of compressive stress trajectories. Units are Pa or Nm–2. See electronic
Appendices B and C for shear stress and strain plots.
edge is tensed while the anterior edge compresses along sheared also (figure 3f ). Considering that the angle of bite
its curvature (figure 3d,e). Compressive vectors are less force shifts by 90° from biting to tearing, stress distri-
obvious in the maxilla but longitudinally orientated com- bution and orientation are surprisingly similar in both sets
pression is maintained in the dorsal maxilla, nasal and lac- of models. There are, however, noticeable differences in
rimal (figure 3d ). Large shear stresses are still observed in stress–strain magnitude between the two loading con-
the nasals as during vertical biting, and the teeth are ditions (table 1).
Table 1. Comparison of peak stress and strain values: owing to the simplistic nature of model, regard values as relative rather
than absolute.
(Stress values are megapascals (MPa); strain values are microstrain (); X or Y refers to direction of peak strain.)
peak peak
peak tensile compressive peak shear peak tensile compressive peak XY
stress (P1) stress (P3) stress strain strain shear strain
vertical biting fused model 11.4 ⫺12.1 4.6 1100 (X ) ⫺1100 (X ) 1300
post.-jugal kinesis 10.2 ⫺14.1 5.1 1160 (X ) ⫺1300 (X ) 1620
max.-jugal kinesis 85.2 ⫺117.0 43.2 12400 (X ) ⫺11500 (X ) 12400
double kinesis 85.2 ⫺117.0 43.2 12400 (X ) ⫺11500 (X ) 12400
tearing biting fused model 16.8 ⫺19.4 7.2 2080 (Y ) ⫺1830 (Y ) 2170
post.-jugal kinesis 13.9 ⫺19.5 7.3 2080 (Y ) ⫺1820 (Y ) 2170
max.-jugal kinesis 120.8 ⫺156.4 54.3 16190 (X ) ⫺14320 (X ) 15810
double kinesis 120.8 ⫺156.4 54.3 16200 (X ) ⫺14330 (X ) 15810
(b) Predicting the effect of introducing cranial 3d,e with figure 4g,h; see electronic Appendices A and B
mobility from solid finite element models for shear plots). Stress distribution is comparable during
(i) Maxilla–jugal suture biting and tearing (compare biting figure 4c,d to tearing
This suture is located at the point of peak tensile stress figure 4g,h). Dorsal to the antorbital fenestra, the skull
in the biting skull model, and at a region of high magni- experiences bending stresses as the lacrimal and possibly
tude (but not peak) tension in the tearing skull model the posterior maxilla experience tension as the nasals are
(figure 3b,e). Tensile vectors are oriented along the pre- compressed (figure 4c,d,g,h). Although opening the max-
dicted axis of suture movement (slightly more so in biting illa–jugal suture has removed large tensile stresses from
than tearing: compare figures 2b and 3b,e) and it is pre- the ventral skull, peak stresses have been concentrated
dicted that the introduction of suture mobility will act to dorsal to the antorbital fenestra at magnitudes of 7 to 11
reduce regional tensile stress, although whether the skull times greater than fused model peak stress–strain values
will be weaker or stronger is unclear. Small compressive (table 1). The dominant effect of the maxilla–jugal suture
vectors act perpendicularly to the axis of movement in the is such that the introduction of a second mobile joint at
biting skull (not shown) and may operate to maintain con- the postorbital–jugal contact has no modifying effect on
tact of opposing joint surfaces. mechanical performance and cranial stress patterns (see
electronic Appendix A).
(ii) Postorbital–jugal suture
Low-magnitude compressive vectors act along the long
4. DISCUSSION
axis of the postorbital–jugal strut during biting and tear-
ing, and tensile stresses are absent (figure 3a–d ). This pat- Stress–strain distribution and orientation are remark-
tern is not congruent with the predicted axis of ably similar during simulations of both biting and tearing.
postorbital–jugal suture movement (figure 2a). It would Morphological features that resist biting loads are used
therefore be predicted that mobilizing the postorbital– equally in the resistance of tearing forces, meaning that
jugal suture should have a negligible effect upon stress dis- the skull appears to be equally well adapted for the ‘punc-
tribution and overall strength of the skull under both ture’ and ‘pull’ components of the proposed feeding strat-
biting regimes. egy. Fused-skull models and those with a mobile
postorbital–jugal suture are characterized by ventral ten-
(c) The effect of introducing sutures into a finite sion and posterodorsally arcing compression from the
element model tooth row to the skull roof, whereas models with a mobile
As predicted, introducing a mobile postorbital–jugal maxilla–jugal suture experience bending stress in the roof
suture into a FE-skull model has no notable effect on of the snout, dorsal to the antorbital fenestra. Tensile and
stress distribution and magnitude during biting and tear- compressive patterns appear similar, but not identical, to
ing (table 1 and compare figure 4a,b with figure 3a,b and those observed in a three-dimensional (3D) Allosaurus fra-
figure 4e, f with figure 3d,e). Apart from a loss of com- gilis FEM during bilateral bite loading (Rayfield et al.
pression in the postorbital bar (compare figure 3a,d with 2001; figure 3).
figure 4a,e) and marginal alterations to shear stress (see
electronic Appendices A and B) in the mobile postorbital– (a) Rostral stress transmission
jugal model, the stress environment and peak stresses and It has been suggested that T. rex cranial suture mor-
strain are practically identical to that of the fused skull. phology dictates that biting-induced compressive stresses
Introducing a mobile contact at the maxilla–jugal suture pass directly from the maxilla to the nasals and bypass the
removes tensile and shear stresses along the ventral region maxilla–lacrimal contact (Hurum & Sabath 2003). FEMs
of the skull model. Peak tensile, compressive and shear confirm that compressive stresses do bypass the lacrimal
stresses are instead concentrated in the posterior portion when the maxilla–jugal suture is mobile (figure 4c,g). The
of the nasals and in the lacrimal dorsal to the antorbital maxilla–lacrimal contact is subject to large tensile bending
fenestra (compare figure 3a,b with figure 4c,d and figure stresses instead (figure 4d,h). The complex interlacing
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of stresses found during simulated biting and tear- of Tyrannosaurus rex to Varanus. J. Vert. Paleontol. 23A, 37A.
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Erickson, G. M. & Olson, K. H. 1996 Bite marks attributable
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Using stress vectors generated in fused cranial models
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introducing sutural mobility and the possible functional Fastnacht, M., Hess, N., Frey, E. & Weiser, H.-P. 2002 Finite
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This research was supported by the Natural Environment Hurum, J. H. & Sabath, K. 2003 Giant theropod dinosaurs
Research Council, UK, via postgraduate studentship from Asia and North America: skulls of Tarbosaurus bataar
(GT04/97/47/ES), an Emmanuel College Research Fellowship and Tyrannosaurus rex compared. Acta Palaentologica. Polon-
and a Royal Society equipment grant. For providing access to ica 48, 161–190.
specimens in their care, I thank M. Norell (American Museum Hutt, S., Naish, D. W., Martill, D. M., Barker, M. J. &
of Natural History), P. Larson (Black Hills Museum), J. R. Newbery, P. 2001 A preliminary account of a new tyranno-
Horner (Museum of the Rockies), P. R. Bjork (South Dakota saurid theropod from the Wessex Formation (Early
School of Mines) and P. J. Currie (Royal Tyrell Museum of Cretaceous) of southern England. Cret. Res. 22, 227–242.
Palaeontology). D. B. Norman (Department of Earth Sciences, Jaslow, C. R. 1990 Mechanical properties of cranial sutures. J.
University of Cambridge) and P. Upchurch (Department of Biomech. 23, 313–321.
Earth Sciences, University College London) assisted in reading Jaslow, C. R. & Biewener, A. A. 1995 Strain patterns in the
and commenting on earlier drafts of this manuscript. horncores, cranial bones and sutures of goats (Capra hircus)
during impact loading. J. Zool. Lond. 235, 193–210.
Jenkins, I. 1997 Finite element analysis of skull dynamics in
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