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PHYLOGENETIC, BEHAVIORAL, AND DIETARY CONSTRAINTS
ON FELID MASTICATORY MORPHOLOGY
by
Pamela A. Wittenberg
Approved:
A thesis submitted in partial fulfillment of the requirements for
the degree of Master of Arts in the Department of
Biological Anthropology and Anatomy in the
Graduate School of Duke University
1995
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TABLE OF CONTENTS
Introduction and scope of paper 1
Carnivorans as eutherians 4
Felids as carnivorans 6
Convergence and the felid "ecomorph" 7
Anatomy and Function of the felid masticatory apparatus
Dentition
8
Muscular anatomy
14
Temporomandibular joint
21
Mandibular morphology
26
Jaw mechanics
31
Mastication
38
Cranial morphology
44
Conclusions and areas for future research
55
Literature cited
58
INTRODUCTION AND SCOPE OF PAPER
A key innovation in the evolution of the mammalian masticatory apparatus was
the ability to achieve medial-lateral excursion of the jaw and unilateral occlusion,
leading to more precise occlusal patterns and therefore more effective comminution of
food items. The masticatory apparatus and Jaw movements of certain "primitive" extant
mammals (e.g., Didelphis (Crompton & Hiiemae, 1970; Hiiemae & Crompton, 1971;
Crompton et al., 1977) Echinosorex (Turnbull, 1970), Tenrec (Oron & Crompton,
1985) and Suncus (Dotsch & Dantuma, 1989)) have been used as models to recreate the
masticatory movements of early mammals. Using these animals as a basis for the
primitive mammalian condition, one can assess the relative derivation of the
masticatory patterns of other mammals. As a consequence of the remodeling of the
primitive mammalian condition over the course of mammalian evolution, "specialized"
groups of animals such as carnivores, ungulates, and rodents can be identified based on
various masticatory adaptations (Turnbull, 1970; Weijs, 1994). The adaptations in the
masticatory apparatus of these specialized mammals is often linked to constraints
imposed by the material properties of their diet. For example, herbivorous animals
have a very coarse diet that requires extensive processing by the dentition; this has led
to the association between a coarse diet and certain features of the masticatory system
such as a "high" temporomandibular joint, a dominant masseter and medial pterygoid,
a large mandibular angle, a high degree of lateral excursion of the mandible, and
simultaneous occlusion along the length of the grinding tooth row. In contrast,
carnivores, which in general process their food very little, have a "low"
temporomandibular joint, a dominant temporalis, a small mandibular angle, a low
degree of lateral excursion of the mandible, and back to front occlusion of the
specialized carnassial teeth.
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While generalizations such as these hold true for many animals, exceptions
immediately come to mind, and make it apparent that divisions on the basis of diet
alone are not adequate. In fact, apart from studies of the dentition, very few clear links
between diet (i.e., "herbivorous" versus "carnivorous") and masticatory morphology
have been demonstrated (Weijs, 1994); in many instances, numerous other aspects of
animals' lives come into play, some of which may be equally, if not more important, in
determining the morphology and function of the masticatory apparatus. Such factors
include:
* Evolutionary history; Barring extreme convergence and reorganization of the
masticatory apparatus, the masticatory morphology of closely related animals,
regardless of their dietary habits, will tend to be more similar than the masticatory
morphology of more distantly related animals.
* Relative size and development of sense organs: Due to the close proximity of the
sensory and masticatory systems, the relative development of structures associated with
vision, olfaction, and hearing may affect the structure of the masticatory apparatus.
* Relative brain size; The size of the brain imposes certain limits on muscle
attachment area; these limitations can be overcome, to some degree, by modifications
in the osieological structure of the braincase, such as pneumatization and the
development of bony crests.
* Behavior associated with food acquisition: The mode of prey capture and the forces
exerted during predatory behavior will affect the morphology of the masticatory
apparatus.
* Non-masticatory functions; Grooming, social display, intraspecific combat, and
other aspects of animals' ecology may affect the morphology of the masticatory
apparatus.
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An instructive example of the effect of these numerous factors on the
morphology of the masticatory apparatus is found among the members of the order
Carnivora. The masticatory apparatus of carnivorans differs little from the primitive
mammalian condition, in which the temporalis is the dominant jaw adductor. Their
specialized dental morphology stands in stark contrast to many features of their
masticatory apparatus that show only weak correlations with diet (Weijs, 1994). For
example, while herbivory is common among ursids and procyonids and is reflected in
their derived dental morphology, their muscle orientation is very similar to the typical
carnivoran pattern, indicating that phylogenetic influence, in this case, has a more
profound effect on masticatory morphology than does diet. The influence of phylogeny
is also apparent in the myrmecophagous "aardwolf" (Proteles), which shows clear
dietary adaptation in the reduction of the cheek teeth, but which retains the muscular
and cranial morphology more typical of its strong-jawed, bone-cracking relatives, such
as Crocuta and Hyaena. In felids, which are clearly dentally adapted to a diet of meat,
cranial and masticatory morphology are also strongly influenced by the relative size of
the sense organs (most notably the enlargement of the eyes and reduction of the snout),
and by the demands of their predatory lifestyle.
Among carnivorans, felids are unique in possessing a relatively low degree of
dietary, behavioral, and morphological diversity. While there are some exceptions,
felids are in general solitary, nocturnal hunters, strict meat-eaters, and, while they are
among the most variable extant carnivorans in terms of body size (Gittleman, 1985),
they are extremely conservative in their overall morphology. They are easily
distinguished from other carnivorans by their globular cranium, shortened rostrum, and
their large, forward-facing orbits. With minor variations in detail, this gestalt appears
in other carnivorans and non-carnivorans and is therefore insufficient for use in family
3
diagnosis, which instead relies primarily on the morphology of dental and basicranial
characters.
In this paper I intend to examine the phylogenetic, behavioral, and dietary
factors that influence the masticatory morphology of felids. A review of this topic is
quite extensive because both the morphology and behavior of modern felids is so well
studied. This great attention paid to felids has yielded a great deal of information that
bears on the correlation between various aspects of their masticatory function and their
ecology. Before examining this work in detail, it is necessary to place felids within a
frame of reference by briefly outlining their taxonomic affinities and acknowledging the
phenomenon of convergence between felids and other mammals.
CARNIVORANS AS EUTHERIANS
The late Cretaceous paleoryctid Cimolestes is often regarded as a "basal
carnivore", although the likelihood that it is a paraphyletic assemblage of many
different taxa makes precise determinations of relationships difficult (Flynn et al.,
1988). The carnassial dentition of Cimolestes indicates that it was specialized for
carnivory, but that it was clearly different from the later Carnivora and Creodonta in
having its carnassial dentition spread along the length of the post-canine tooth row. In
the Carnivora and Creodonta, this carnassial function is restricted to specific loci of the
post-canine tooth row (M1/M2 or M2/M3 in creodonts, P^M, in carnivorans). Along
with features of the tarsus and internal cranium, this restriction of carnassial function
has been used to unite the Creodonta and Carnivora as sister taxa (McKenna, 1975;
Flynn et al., 1988), although some workers claim that strong evidence in support of
such a union is lacking (Wyss & Flynn, 1993). Other workers have proposed grouping
the Carnivora with various fossil ungulates within the Ferungulata (Simpson, 1945),
4
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with various "insectivores" (Lillegraven, 1969; Van Valen, 1969; McKenna, 1975)
with the Archonta (or some subset thereof) (Goodman et al., 1985; Shoshani, 1986), or
simply as somehow closely related to all eutherians other than edentates and pangolins
(Novacek & Wyss, 1986). This latter claim is perhaps most revealing, as the
relationship of the Carnivora to other eutherians is anything but clear-cut, and for many
workers remains as one of the more persistent problems in mammalian systematics
(Flynn et al, 1988; Wozencraft, 1989; Wyss & Flynn, 1993 and references therein).
Thankfully, the divisions within the confines of the Carnivora are much better
understood and more widely agreed upon. Carnivorans are divided into two major
clades, the Caniformia and the Feliformia (Wozencraft, 1989; Wyss & Flynn, 1993).
The Caniformia consists of two subdivisions, the Ursoidea (Otariidae, Ursidae) with
their more primitive bullar morphology and pattern of basicranial arterial circulation,
and the more derived Canoidea (Canidae, Mustelidae, Phocidae, Procyonidae). The
monophyletic Feliformia or Feloidea includes the Felidae, Herpestidae, Hyaenidae, and
Viverridae and is united on the basis of various basicranial, bullar, postcranial, and
dental features. Within this group, felids and hyaenids are most closely related and are
distinct from the viverrids; these three families in turn are further distinguished from
the more primitive herpestids (Wozencraft, 1989).
Since its inception, the Carnivora has undergone numerous changes in
membership and affinities, and has acquired its own extensive vocabulary. Because this
paper does not intend to serve as a review of the systematics of the Carnivora, use of
these terms is limited, and a detailed explanation of them is unwarranted. However, in
addition to ordinal and familial terms, the general terms "carnivoran" and "carnivore"
will both be used, and may be subject to misinterpretation if not defined at the outset.
"Carnivoran" will be used when referring to taxa within the order Carnivora (regardless
5
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of dietary habits) and "carnivore" will be used to denote any meat-eater, without
reference to its taxonomic position. Generic and specific names within the Felidae
follow the classification by Wozencraft (1989).
FELIDS AS CARNIVORANS
The boundaries of the Felidae are unquestioned, although divisions at the
generic level may be complicated by the morphological uniformity within the family
(Flynn et al., 1988). Dental characters related to the reduction and simplification of the
cheek teeth, and cranial characters related to high bite force and well-developed visual
abilities (Radinsky, 1981a) are diagnostic for the family, and contrast markedly with
the generalized nature of the postcranial skeleton. Within the Felidae, there is a clear
division between the large and small cats based on a suite of cranial and dental
characters (Werdelin, 1983) as well as differences in the hyoidean apparatus associated
with roaring abilities (Pocock, 1916a).
When both living and extinct cats are considered, a division can be made
between paleofelids, an entirely extinct group with sabertooth adaptations, and the
neofelids or "true cats", which includes the extant felids and their ancestors, as well as
another distinct carnivoran group with sabertooth adaptations.
The paleofelids appeared during the Oligocene, and are often regarded as the
earliest true felids, although some workers claim they should be relegated to a distinct
family within the Carnivora, the Nimravidae, (Martin, 1980; Baskin, 1981; Hunt,
1989). Within this group is found a striking array of sabertooth adaptations, including
one of the most specialized forms, Barbourofelis (cf. Turnbull, 1978), which survived
until about 7 mya.
The neofelids trace their roots to ancestors with short canines, such as the civet-
like Proailurus from the Miocene of France (de Beaumont, 1964; Thenius, 1967). The
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civet-like features of this genus are the basis of the claim that felids arose from small,
arboreal viverrid-like carnivores (Martin, 1989). The neofelids underwent a major
diversification in the late Miocene, which produced the modern felids as well as several
genera of sabertooths.
CONVERGENCE AND THE FELID "ECOMORPH '
Within the Carnivora, Martin (1989) recognized a series of "ecomorphs", or
morphologically similar forms which have appeared over the course of carnivoran
evolution and which are the result of similar selective pressures. He identifies cat-like,
civet-like, mustelid-like, and dog-like forms. While some of the convergences observed
within the Carnivora may be attributable to close relationship, the similarity in adaptive
schemes observed between mammals of widely disparate orders suggests that the range
of morphological adaptations to a carnivorous lifestyle is in fact quite narrow, resulting
in a much higher probability of convergence (Martin, 1989). The cat-like ecomorph has
appeared not only among felid carnivorans, but in other carnivoran families and other
mammalian orders.
Perhaps the most bizarre and most widely studied incidence of convergence of
cat-like forms is that of the "sabertooths" which evolved independently at least four
times in three mammalian orders: in hyaenodontid creodonts {Apataelurus ,
Machaeroides), borhyaenid marsupials (Thylacosmilus), paleofelid carnivorans
{Dinictis, Hoplophoneus, Eusmilus, Barbourofelis), and neofelid {Pseudaeluriis,
Homotherium, Smilodon) carnivorans. These forms converge markedly in terms of their
cranial and masticatory morphology, an area studied in depth by Emerson and Radinsky
(1980).
7
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Perhaps less dramatic is the convergence seen between neofelids and the
Malagasy fossa, Cryptoproctaferox. The fossa is the most highly adapted of all the
viverrids to a purely predaceous lifestyle (Ewer, 1973), and converges strongly on
several aspects of felid morphology in its reduced dental formula (P/3.C*/,.P3/3.Mi/i),
well-developed carnassials, and loss of postcarnassial elements. Placement of the fossa
within the Felidae has been suggested on the basis of these dental characters, as well as
cranial features such as a globular skull and foreshortened rostrum which result in an
overall cat-like appearance (Milne-Edwards & Grandidier, 1867; Gregory & Heilman,
1939; de Beaumont, 1964; Hemmer, 1976a). However, numerous cranial, postcranial
and soft tissue structures place it firmly within the Viverridae (Petter, 1974;
Wozencraft, 1989), the family to which it was allocated when first described (Bennett,
1833).
In identifying a mustelid-like ecomorph, Martin (1989) grouped together
animals possessing a suite of features associated with a semi-fossorial way of life.
While felids and mustelids do not converge in this aspect of their lifestyles, members of
one mustelid subfamily, the Mustelinae, do converge strongly on felid dental and
masticatory morphology in possessing elongate, blade-like carnassials and short,
powerful jaws (Ewer, 1973).
MASTICATORY ANATOMY AND FUNCTION IN THE FELIDAE
DENTAL MORPHOLOGY
While the P‘^/M, carnassial pair is the defining dental character for the
Carnivora, felids are further distinguished from other carnivorans on the basis of
simplification of the dentition, particularly the carnassials, which assume the shape of
two simple blades. This extreme modification of the carnassials in felids has led to the
8
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notion that felids have the highest shearing capacity among carnivorans. This statement
however, is misleading and should instead state that felids have simplified their
carnassials to the point where simple two-bladed shearing is the only method of
fragmenting food items. Other carnivorans, such as procyonids, for example, possess
carnassials that are secondarily derived for omnivory. These teeth are-not as blade-like
as those of felids, but they are likely more adapted to shearing function, for the
combined length of their numerous small shearing crests is likely quite high compared
to felids, which have a single shearing crest extending along the length of the tooth.
Uniformity across the Felidae in development of shearing capacity to the exclusion of
crushing capacity is a reflection of the low dietary diversity within the family, and is in
marked contrast to many other carnivoran families, in which differences in diet result
in markedly different dental morphology and specialization between taxa (Ewer, 1973).
In addition to possessing a simplified dentition which emphasizes shearing over
crushing capacity, felids as a group are characterized by robust canines, reduced
postcarnassial elements, and a reduced dental formula through the loss of both pre- and
post-carnassial elements. These dental adaptations are closely tied to the strict diet of
vertebrate flesh, the high bite force, and the quick dispatch of struggling prey that
characterize the feeding and predatory habits of felids.
The chisel-shaped incisors of felids usually bear three small cusps (Savage,
1977), and are unique in that they are arranged in a straight transverse row, rather than
the convex arcade typical of most mammals (Flynn et al., 1988). The incisors help the
canines maintain a firm hold on struggling prey during capture, and are used in feeding
to remove fur or feathers from a kill and to remove bits of flesh from bones (Kitchener,
1991).
9
!iwTr farw’fb !A^t! nolwn
ibrtJ by^^frmi? ’ivt.(' W</ntN tst*
iv ^K•r)l Jl^f <lflC yi't /( boUtli} ’;jNvi nfqrtT}.’, rftwwj yfii ia .
S'
*1 ?n »wt5’i!Uv«t’h;'> r.iHiO inifi^ lw<!
5iB
.V’ .,1 5i». iJWJirr ijto-/hyb i»/tj
'1 . ' *^S '*^‘ n
^lii n;> , froJtariiji * Qt -ivjm \ftoiltf *i^fi 'i«»4tti.vji
rt^rf oiiMb ?i.
llK»r» -IM- V>1|»JSi^SlL«|T «>
a: ■' !T1
Uhffi iclifoct boTj5^<iWtfe|r
2i . ■ ,;:. . ''■ :>« Zjh^ ■§
Uur/jy j^il» Jli tl3)»lw ytiim </»
y'T" ^
4rT<!'i rT3V/a? t.m ylfea^tum m
T»'/t7 fit
•a ’ " ’ i ' ' ^ ^ a
>01^) ^3ilt tiap»b'bin(3b'5:i i^ WM
I?i 1o jeib /35W. aji> oi aisrfi .Snr3n43^»ifl|iuw^
^ - - .Vif,',
i"- ’, , $ - ' -^- %■ . • '--.S'
,, ai^» iftrtiin . wf). 4rs>'i*-iij 4wr ^tfj lorn
*tj ^Ari r0ii2iil ihm .lo ,‘^gsfq'^^1^t^fi^*s^^30!5 artJ
‘ f ■'*'•■■ ® IP K j*,.
jt!()fti|»rt hi l»*»m sor, s<^8 Wti.l m^ii i£>aitiO
^ ?S ■ »L ^' ' . . , ' S'-'
iSi
Typically, a large diastema separates the diminutive incisors from the larger,
mediolaterally compressed canines, which dominate the anterior dentition, and which,
along with the carnassials, are the main functional components of the felid dentition.
This diastema varies greatly in size among the Felidae; it is nearly absent in the cheetah
{Acinonyx), and largest in the clouded leopard (Neofelis) (Pocock, 1916b). The
mediolateral compression (anteroposterior thickening) of the canines in carnivorans and
many other mammals indicates that the canines are stronger in resisting bending in the
parasagittal plane. This is a reflection of the fact that normal jaw adduction occurs
more in the parasagittal than the transverse plane, and bending moments produced
during feeding activities such as biting and ripping flesh from a kill bend the canines in
the parasagittal plane (Van Valkenburgh & Ruff, 1987). However, felid canines differ
from those of other carnivorans in being markedly stronger in resisting bending in the
parasagittal plane (Figure la) (Van Valkenburgh & Ruff, 1987).
Figure 1. Schematic drawing of felid canine teeth, showing:
a) AP diameter (arrow), which reflects strengtii in bending in die parasagittal plane
(experienced during jaw adduction and ripping flesh from a kill)
b) mediolateral diameter (arrow), which reflects strengdi in bending in die transverse plane
(independent of ordial jaw movement; inflicted by struggling prey).
(after Van Valkenburgh & Ruff, 1987).
10
This increased canine robusticity is a biomechanical necessity for felids, because
their killing bites are deeper and more powerful than those of other carnivorans such as
canids (Radinsky, 1981a), and therefore their canines experience greater bending
moments in the parasagittal plane during jaw adduction than do those of other
carnivorans. Additionally, the canines of felids are more robust mediolaterally than
those of other carnivorans, and are therefore relatively stronger in resisting bending in
the transverse plane (Figure lb). This finding is not, however, attributable to Jaw
mechanics alone, since orthal movements of the jaws produce bending primarily in a
parasagittal plane, and produce little if any bending in the transverse plane. Instead, the
prey capture and killing techniques of felids have been found to account for their
mediolaterally robust canines (Van Valkenburgh & Ruff, 1987).
In capturing prey, felids use one of two types of killing bites, depending on the
relative size of the prey item (Leyhausen, 1979). Relatively small prey is killed
instantly by a bite to the nape of the neck, which dislocates the cervical vertebrae,
severs the spinal cord, and may crush the back of the skull (Kruuk & Turner, 1967;
Schaller & Vasconcelos, 1978). The thick neck musculature and in certain cases the
presence of horns or antlers in large prey precludes the use of the nape bite, because
the canines are (usually) unable to penetrate deeply enough to reach the vertebral
column, and because horns and antlers are a source of potential injury to the predator.
Instead, relatively large prey are killed by a throat or snout bite, which occludes the
trachea and results in eventual death by suffocation (Haglund, 1966; Kruuk &. Turner,
1967; Grobler, 1981; Sunquist, 1981). In some instances (i.e. capture of medium size
prey by Acinonyx) the throat bite may cause instantaneous death as a result of spinal
cord damage, rather than by suffocation (Ewer, 1973). All these methods of prey
dispatch result in large, unpredictable oblique and mediolateral stresses on the canines
11
ful jfin r* jnii!£> ailrTt’
U 1<f MWl} instil i)A& iSf9iSk$(tit!l^sdi
yftilsA 4A^ >->ic*q-y v/ft^iscw -H-irt* yr>?»KMi ^aiim
\o»lj»i ■ff‘i muii ntiiriftr pKiitisHhhH oife '4'l|p-i3WoM^, t
E-'
•M
.■: nf ifntMin*^ >.«»*« .y«uf>iy;j*»f«fea«i
>A9T^>I fe 'il> ;p^if QwMe^n^SS^Ilyl ■
'“^ -’■■■'J^a' ' ■^' W tSq''k '‘"'^
ST
;VdOl ^ 3lu»i^) |ta}la sili n»v^
'’,sii#" sqf^!:', 5|il( }o u^o ^’i
., - ■ 2.tr«>/4 w^t^q
iitit^anw arti' /bsyi, ’ '■'
.Kito^ 01 ptfipi «i£^*Tfi':.i&o«.|tfiic4i
JP?' iPi! ‘l(*-i''tf‘'‘''‘ ~'' . "■■ ,-Ef"*i '^ ■'' -iS^ .ii3l*' " "^'',1. ,'
.^miT ;od^i f^vla
-fH •'^ ■
LUT -mvi'-aiMnuk, - .. ..;.'™.J|k- r* '' ‘''’ ' O
due to a) the likelihood of tooth-bone contact and/or b) the struggles of prey, and
require that the canines of felids be buttressed against large forces exerted both in the
parasagittal and transverse planes (Van Valkenburgh & Ruff, 1987).
With the obvious exception of felid premolars are quite simple and
unspecialized, and vary in number between species. The loss of the anterior premolars
in some species of felids is the source of variation in the familial dental formula
(typically P/3.CV1.PV2.MV1.), which varies from a minimum of 26 to a maximum of
30; P2 is regularly absent in some short-faced species of certain genera (Lynx, Caracal,
Profelis, Prionailurus, Acinonyx, Otocolobus), and P2 may also be absent as an
anomaly in other species (Ewer, 1973). The upper fourth premolar is remarkably
altered from the primitive carnivoran condition in its elongate shape, the reduction and
anterior displacement of the protocone, and the reorientation of the cutting blade into
an anteroposterior plane (Figure 2). The elongate, antero-posteriorly oriented P'^
Figure 2. Occlusal view of camassial dentition in: a) a felid (Felis), and b) a primitive
carnivoran (Miacis), showing tlie difference in die size and placement of die protocone ( *).
and orientation of die shearing blades (heavy lines). (From Savage, 1977)
12
fanft .^1 tci ^ ^sama:) ^U ^ihDOt 11*1151^ <)d uub
*M f!i rttod mK>{ pgial iMic?3fa i^t^^?^j>Illu^j'^tJ^lbt^5^ «> ^a/i^OBa ^rtf *fifli
.(W' : .Oufl A naV;.
Mfnt ^l<i'»ii-, 'Jjjifp dliT bib> ,*q "ft) fir^H^j^irsi ajoivtiy? «wf* (<»iW
rti^<«tt* *n K/il-^Jiia aiU>*) aiol ‘jilT .?.*jTt>3q2 TOtImian Hi nsv bf?«i .h93(*l«j3qcnu
fiionriu^ IwttSfb l/.iUjTfEfi ^ noiiiwu/'^owucwr ijfb ^t 2bU^V'te <Nftc»ii.jii
r.
lo 4Tn*»tiixwn fTfiirRii!(ni « ftioil mhAy rMlv^
Vi^^cO (roa^s fUfijfi^ ai irtiarfei 2i •q ;0t
uti iji ogift yftiTi S b«e ^c<v\ojibK
ii laiomfsiq isqqM .%w3y »^5q^ r Nm a) yiAffioiw
I tsj ' ■ .^
bna adi?l/l2S7 wi3 .sq$a^ s«j^4}0|3hU( m aoillbqo5amoyiftiaj^ limU
* H ^-
3fTniw3 3(li Ja n<fe<wi09i bac mmM
',■* - ■' ■" *g
biifnsii-*»5 v<i<«m^vo't%^ni^ ,#|fi5nQt&r& aitig'r^ysa^lq TOf^^mjoiasnt rw
i-t; / 1" »i ^ _
EJ
*sW.
— / ^r-*^/ 'rtt' " ISN
— — ‘‘Z^kc-^ . /\ ®^^CL^i£_>,sl
Si^
©
1
itr
IV' iMfV} ii fdua* V Cfl»i-;4iO Jswtrt
i*'isr nf.. .f <»
<'. ft*f ^tt^lt yvitwll ftitUnlif '#»ij (W‘iii«w bm
occludes with a similarly oriented and designed M‘. The blade of P'^ extends from the
paracone anteriorly to the metacone posteriorly, is convex lingually in occlusal view,
and bears a "carnassial notch" (Matthew, 1910) at its center. The blade of M* extends
from the paraconid anteriorly to the protoconid posteriorly, is convex labially in
occlusal view, and also bears a carnassial notch. This opposing convexity of the lingual
and labial surfaces of the P"* and the M*, respectively, and the opposing concavity of
the carnassial notches permits only limited points of contact between the blades; as the
teeth occlude, the point contacts move along the blade and converge to create a lozenge
shaped space, which locks food in preparation for shearing, and prevents the food item
from slipping anteriorly.
The loss of crushing functions, the simplification of tooth pattern, the loss of
postcarnassial elements, and the increasing efficiency of the carnassials are the main
trends in the evolution of carnivore molars (Savage, 1977). Among carnivorans, felids
are extreme examples of these trends. Over the course of felid evolution, all post-
carnassial molars have either been lost or are reduced to mere pegs in the maxilla,
leaving only one molar as a functional component of the dentition.
While the evolution of the felid dentition is characterized by the trend toward
simplification of the dentition through emphasis on shearing over crushing abilities and
the reduction in size, number, and complexity of teeth, this does not imply that the jaw
movements effecting the function of these teeth are simple in any way. Rather, the
proper functioning of the dentition requires a muscular setup sufficient in size and
orientation to exert a high bite force at the canines, while also effecting fine occlusal
adjustment necessary to engage the carnassials, thus ensuring their proper function and
protecting their easily fractured blades from damage caused by malocclusion.
13
MUSCULAR ANATOMY
Turnbull's (1970) classic comparative study of mammalian masticatory
musculature sets up a dichotomy between "generalized" and "specialized" masticatory
arrangements. He identified "generalized" mammals (such as Didelphis and
Echinosorex) , which are presumed to be similar to primitive mammals, in that the
temporalis is the dominant jaw adductor, and the "pterygoids" (which he grouped
together) function as accessories to the temporalis. This condition is contrasted with the
"specialized" masticatory morphology of mammals such as carnivores, ungulates and
rodents. While carnivores rank as a specialized group relative to the generalized
mammalian masticatory condition, they do so largely by virtue of their specialized
dentition, as the relative size, orientation, and attachment pattern of their masticatory
muscles is quite similar to that of more generalized mammals.
The masticatory musculature of the domestic cat {Felis catus, Felis domesticus)
is well described in the literature and is often used as a model for all felids, or as a
generalized carnivore model. While there are slight differences in the masticatory
musculature among felids, these differences are for the most part a result of allometric
differences seen in the large range in felid body size, and do not have marked effects
on the relative size and orientation of the masticatory muscles. Some of these
differences are obvious upon inspection of a large and small felid skull (Figure 3).
Figure 3. Comparison of skull proportions in felids of different body sizes,
a) Panthera leo b) Lynx rufus (From Vaughan, 1972)
14
.Lih.\ -A EiV.i««
'35 ,, ,' *, Si;'
■m njJ'symii
\noir. WJTrm io J>v|jinic<^frs) aw'as^o j^EurJinwT -j
bfiB "bf«:it6ion^s’' n3^w*Jj^ fmojorfo^b < qn uat
n
bail za ffiDs^ mi
9rt *«i
Mdt fibi IwSRustJnoo n^(iH)fjQa_.3ffrtT .talRKjqfma.t sib 6i zifhQui^rjM m
. ’i-^' ,'■
«f«<Ujj|fjij .wiovittTfio
>!S&.
boKi^Kiorr^ ^tui^ u) 'a^/bitlaimfOtg ^ JlmJ) oBtfW .onJibcn
' ' ^ ..V,' 'S® ' ■> ' m ..j>
g
liiwb lio ^ p^: ob^yiib s,
'(iPJC3tU«iftrn ifsrtllr^ 'tmnso ..S8li»^bBf»»4lif|J 'tif .;^}isa^
'Ul
.fiiummm ^?rieft>rj:»5pion{ m laJb^ a ii||
.?3kim it^a wlo if'yra tsdT
'?!
aiB lo jlr.' ipi t*j4»f|j ffi li2>W «1
'OIBab^j^m Pit) ■ pi; SiA- v^
Mtt^ai Jt .'kIJ' ipt -.‘‘juinlaaeura
ak)DT)-9 ba;^!am aypri )on 5<S3 m fff»r.<5:fnf!n»fll&
■‘■ii-.
li
•it
3«>t(itesmoZ .esls«u<n YWBStam s* 1o noBlniStifo tiiwijjsj^^ „ ^
>s
m^!-
■'tf^
'^■' ''■'■■ .' p'
■» ;.:j^
&. '■ ■-;■ ^.■
%J../- 'j
t'Arii - - h.^^'''''i;
Because brain size does not increase at the same rate as does body size, the
braincase of large felids provides relatively less surface area for muscular attachment.
Therefore, large and small felids differ in the degree to which crests and tuberosities
provide attachment area for masticatory muscles (Ewer, 1973). With this in mind, the
descriptions below are used as a rough model for all felids, although they draw largely
from descriptions of the musculature of the domestic cat, particularly works by Toldt
(1905) and Turnbull (1970).
Temporalis
The temporalis is the largest of the masticatory muscles in felids, accounting for
roughly 50% of the total weight of the jaw musculature (Turnbull, 1970). It originates
from the sides of the braincase and along the frontal and parietal bones dorsally, along
the lambdoidal crest posteriorly, and along the zygomatic arch, zygomatic portion of
the frontal, and ligamentous postorbital bar anteriorly (Figure 4a, c). The temporalis is
divided into superficial, deep, and zygomatic portions, all of which attach either
directly or indirectly to the coronoid process, and fan out to cover much of the lateral
surface of the braincase. These distinct parts of the temporalis clearly have very
different functions by virtue of their very different orientations. The posterior part of
the temporalis has been singled out as a particularly important muscular division in
carnivorans (Smith and Savage, 1959; Scapino, 1981) that functions during predation
to prevent dislocation of the TMJ as a result of ventrally and anteriorly oriented forces.
Masseter
The second largest of the jaw adductors in felids is the masseter, which consists
of a deep and superficial portion, and which originates from the ventral border of the
zygomatic arch to insert onto the mandible (Figure 4a, d). The masseter is variously
described as being divided into four lobes at both insertion and origin (Toldt, 1905) or
15
PS
amfiffUtiJ fw •'jiftnarcu'H itfio
a
li)1 UfflR SJfchiiP. .^lOi ni LrittittiSid
jfDiHwrs^iC f>f»h •Tl?)iii-/.' OJ f 3 j «:jU tMft^^J (Iwrt^
iffij ,lmim nf vnii rtuW l iswil'f .3
yl^s^Sii v^flib y-yjj itjfuorttit 'Ijb 'i?i l.^i»fn rtgaai !t««
mcril
JtiioT Xtf^iiKiW <hlrtl|i>jtmf{ ,|ljs 1)l<fe;»f{?y(i>
;a
'T Isil
>01 '^/ifiuii^jue <i{ lislt^irtii s4T
fesjejo^iw U fOt^l .(hf^niioTI W!»
,x)hjijiot> vtwod H)4»bi{ ^/1f mofi
)o fioH+oq oiiftfrj^^vA mr^rUbiQktmfilf 6tiJ
« V(\T twa a<ti
-h '- ■ ' . '^' y' ^ ...
IcrwAf aib^o ^
.,- afe * p.'’^
0., ^wv yvail ?i{irf6qto acuilwe iH
■ ' 15 , ■ • "\ •■ ■ V
% ftcq ^trfr .znw/t^naiiD il^).% :>
s
n.i"0<?l«Vy#t> vi;tu(t)W(iq e i?n «s»J^ wSj _-
nflUfibsik 5nsi*fb ifloMoa Cl^^r ^iwulono^
HI
s
iLl
4i
."
. .iJ
au
tn latmid Ifnirt^v 4? «1o
'.,'‘r'". ■ , - i%j ’■ ' a ‘ "^’:
'gfjuoiwv «f'%s*a8m '3ilT ^
10 ( Wl .>biWl j a?^tiu. tyji;. fl^J^'^’H M iwiiiliflob
at its origin only (Turnbull, 1970). The deep layer of these four masseteric lobes insert
into the masseteric fossa on the lateral surface of the mandibular ramus, but the
superficial layers of the four lobes have no direct connection with the mandible.
Instead, they insert onto a tendinous raphe which joins the masseter and medial
pterygoid, and which continues posteriorly to attach to the auditory tube. Toldt (1905)
described this raphe as a unique adaptation among carnivorans that allows the masseter
to be well-developed without a concomitant increase in the size of the mandibular
angle.
In animals with a large masseter, including most herbivores, the mandibular
angle is expanded to provide a large attachment area for the masseter (Radinsky, 1985).
While increasing the potential size and therefore the power of the masseter, this
increase in the size of the mandibular angle may also limit gape, as extremely wide jaw
opening may risk occlusion of important cervical structures (Herring, 1972). For
animals in which wide gape is not an important consideration, such as herbivores, one
would expect constraints on the maximum size of the mandibular angle to be minor. A
notable exception to this prediction is found in certain artiodactyls in which wide gape
is important in social display; in this case, wide gape is achieved despite the large size
of the mandibular angles by flaring them laterally (Herring, 1975). A similar lateral
shift of the angular process has also been proposed as a means of achieving the
particularly large gape typical of many sabertooths (Matthew, 1916). Carnivorous
mammals have the most stringent gape requirement among mammals, due to their need
to engage the posteriorly situated carnassials during prey consumption (Herring &
Herring, 1974). If in fact gape is constrained by the risk of occluding important
cervical structures, one would expect the mandibular angle, and therefore the size of
the masseter in carnivorous mammals to be highly constrained in maximum
16
"ig
fwii jad *i»f»i' I iRitifill/ncn! Irni^S^^VtJ fiiaSlR^^
. , IS
itSmai lijfft ( j/l’ ?(jf(>^'rf»dy/ ti)(iji«n'|}!<^^ jxawjf .tintatwl ®
' Sl^.
(>' jOj ■» i?|f ttT ' ■ fUYirtUft artf
•'Kf
ww*4#WT» 3«tj fwoffcd fjutj irraiK)yif
ifew
TfllwtttbsKtm -fwt? i^sfsit ^>ri|ni af.^armi s ivotUtw^^^fc^^
a 2B
9
’isi:
,yab)»ii«Jl) ^5^r»«;*ji/^i Sft? lO^ aSiiJ » « algd*
& li^ .lamffrm %{\if >0 T^;(i/c»q srii r^totorfi iin« 9<<a gni^Acw* MaiW
500 w? dGfig ibjfi^o^rr^ jyo
/\ TcifRfn 5ff «rt Tk^ludjivfigtfl blfli \o aijt^ bluoM?
^r*
~ ■ fit "ft ' I
liitemi Tiilrrm« A .(Wl
aiil lo
r :|!0t voifb^ i; ^ u9^>t} aiS^' •’te Mdi
^UtilOvfRI^n .v(rtI41:
F;3 ^., ^ ■ ■’■ I^v ^:./r
93
■^!*
.4^’,
. lit^ i.. "-
jfifU'loqmi sf^tjuimiJo ij?fi '(fi fefliri rtROo^^ a 1 1 1 t
' ... . (-■
Figure 4. Masticatory musculature of Felis. (From Turnbull, 1970)
a) Lateral view showing superficial aspect of temporalis, masseter and digastric.
b) Lateral view with masseter and digastric removed, showing zygomaticomandibularis and
medial pterygoid.
c) Lateral view with zygomatic arch and zygomaticomandibularis removed, exposing die
insertion of temporalis.
d) Ventral view of superficial musculature, showing die raphe between die medial pterygoid
and masseter.
e) Ventral view of deep musculature, showing the medial and lateral pterygoids.
17
mi.
ttmi' .
*^,, --■' , ''4
■*ini0fnmi0 ‘':;i^ '
niV**
rr.|i<.
'•i;^
Snrt»-K' •,
*^'**i'
%
'LJLliL
w ,><^
, ■W'-'
-iai?^i
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... , ■ ^ ,. J. ’’
.B$ ■■ . ...V . ,
_ n’''"»isSPi
..^~ ■■ . ^■' \ ■
y ii,’#..
^v;i
,!■' ' jii:.
tf-* ;#r::'
.:. :J-'
o
>: _,: .'%_is,; iS ■ - , , . L. !.*i ' ,
^aS.'Jv
■T,. I ■ ■'*>■' ^W" '
$
'•m-, . .1^. ■ .<»■- ■■•’-■-if '-, -n .--'
" "■■■'' ^- ■
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'il-y;:t'4
’ ■■'^'^%w:''j!nr'^^
size. For felids, which have the largest relative masseter size among carnivorans
(Buckland-Wright, 1978) this limitation might be overcome by the tendinous raphe
described above, which provides a large attachment area for the masseter without a
concomitant increase in the size of the mandibular angle.
An alternative view of the function of this raphe is that of Becht (1953), in
which the "loop" formed by the connection of the masseter and medial pterygoid via
the raphe can slide posteriorly when a particularly large food item is placed at the
posterior dentition, thus increasing maximum gape. Although the superficial masseter
and medial pterygoid do indeed form a loop-like structure, the fixed placement of the
deep masseter within the masseteric fossa results in the anterior border of the masseter
being fixed, rather than mobile, relative to the last molar.
Zygomaticomandibularis
The zygomaticomandibularis arises from the medial surface of the zygomatic
arch and the temporal aponeurosis, and at points of close contact, may fuse with the
masseter and the temporalis. Fibers of the zygomaticomandibularis insert on the
mandible in the masseteric fossa, and converge with fibers of the temporalis to insert
on the coronoid process of the mandible (Figure 4b),
Medial Pterygoid
The medial pterygoid has a deep and a superficial portion, both of which arise
from the ventral border of the infratemporal fossa and portions of the pterygoid fossa.
From these points of origin, its fibers extend posteriorly and laterally to insert on the
medial face of the angular process, ascending ramus of the mandible, and the
aforementioned tendinous raphe connected to the superficial masseter (Figure 4b,d,e).
18
a«nov?mis34nom8 «k avtieisfj .mn ^
yfUiM^ turmihuM^ttj \(<j wioo'wv^) &<t wf^irw ?iiigiiW*ti4TBliiS*a)
M
a ruaftrtw 73i«w:?k«i ^dJ u>l mbrndowiB ,f»fotk bodiTJftab
ylgnis Tfiludi’bni^ wl
>1*1 tfxastiofitwocji
fu; >(£:^ !■) >r;sd(|xr^
cfv tiiftg^fKsi^ fiibbfn huyj 3rtT l<^ ii6!i^bi«<j3 rtairlw
'-:..|ip-
uf
ir. bsaijlq w njair bJ^'S^T^sJ b ^siIw »bik n*a ariq#! aiti
b<b i%uo<bJA ,ii^insb
9rtJ In bn»
'lawwwyi: Id' wirr^dh^B |^. <qi»j^
. ... .,
.tBiord dtl) pj
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m
Diiwuogi^ alt? 'to a^^rliy?. jdt«>m :)ili qjui)
bit! bm How^
art,) .a^in4bR4rte#di;d^
fj 'V'. '. .... ' . >m^' BT" " ' V)
lip^'- cW'.^lmPqd?Sl:j3'a-1<) ^2ib(|ri>,rtrt:<w
.5'“
S', ,, ■ '^■."'..',.,.-.f .iifS'
<MiTJs ffpFrtw '10 iljod "ifipiJTO^ i^>bn«
:...-.yit.-. ‘-‘ fff
911^51^) 3fdtb;is?f]i »rij no^ iJI
■'iL
m
i(t^
"' -. -. .4
Drti bjifi ,i>fi5feaBmS(irti.-to
■■'.M iffl -, ' . ^
'> - • ^Uia i'wmmifT^: ''■ vs^may ' wmmf^ ..f^ vr. »
Lateral Pterygoid
The lateral pterygoid is the smallest of the masticatory muscles in the cat,
consisting only of a small bundle of fibers that arises beneath the foramen rotundum
and extends posteriorly to insert just inferior and medial to the mandibular condyle
(Figure 4d). The muscle consists of two similarly constructed divisions which are
tendinous at one end and form a fleshy muscular belly at the opposite end. These two
divisions have opposite orientations such that the fleshy end of one division lies against
the tendinous end of the other division, a configuration which is functionally important,
as the muscle fibers rotate through 180 degrees from origin to insertion. By having a
muscle belly adjacent to a tendon, rather than another muscle belly, the muscle can
contract without "wringing out its fluids" (Turnbull, 1970).
The lateral pterygoid is a feeble and, as it turns out, underutilized muscle in
felids and, presumably other carnivorans (Turnbull, 1970). The lateral pterygoids on
both the working and the balancing sides are silent during opening and are active only
during the end of the closing phase, when they become active simultaneously with the
digastrics (Gorniak & Cans, 1980). Their primary function is to aid the digastrics in
jaw abduction; this is in contrast to their role in other animals in producing bilateral
protrusive movements (absent in felids due to the structure of the temporomandibular
joint) or lateral shifts of the mandible (accomplished in felids primarily by the medial
pterygoid, deep temporalis, and zygomaticomandibularis) (Gorniak & Gans, 1980).
However, the asymmetric activity of the working- and balancing-side lateral pterygoids
indicates that this muscle likely plays a role in effecting close approximation of the
carnassials. In felids, the lateral pterygoid has no attachment to the temporomandibular
joint capsule and articular disc (Noble & Creanor, 1992), whereas most mammals show
19
mubwiM ^ tifil UlMOfTiKt jrlodli In iHvtl^d liiMIM ‘‘
.r-'
,, : .-
o*^-i o«»*ff Jwt r^tt4tlq|l»:^l^f^
'$• l^mM/l x.G' AftoJWni oi
vy'-
■'M,.
Jlw#iv<T) ‘iifwbm fj^nob
iti l^siJuAiwbau n .JinwiU ^
't ' '• Ife? ' MWfwi- ■.’ ■ '' '■ ■ " '*Tlfe
jifWiagp
[>;3 .iS' I • ' x':"'- *'■ B
^>fb rtr^w vl J ^ k> bfia <Kfe ^
■nl^jisiij#^.ij,»flr&{«:.|?, li .nlcD^ ipwO) iPN«4|^!^
^^y|i^4i/#w/»<^^lm5^,4>l1l Vj lear^ifi^.) ;“?f»t><fi:5>vofn aviRMtWi
liife?ifT. jiiU iu^i iO
'>v :4A/rTtiS;>)V^^‘i^iibrfc^ ;bif« >si,.'®
llWstef
arU 1o f1f^fc^n^«ryJ^|,qI|^h #ey*ict: :4#li^fe«uwm «I4| bill ■^■'
m ■ ■ ■*- 1?^" ■ E -.,
!?>
^«i(i«ti«*.i>c'si><5m»i #)’<' il> Hiv’,m3s»H"i<r isbSi &i6avwis lH»)(W<‘itf> .nWeVnl .ziciz^stsa
i\'. , - ' - rk.
such an attachment pattern as a reflection of the developmental history of these three
structures (Harpman & Woollard, 1938).
Digastric
The digastric morphology of carnivorans is well-known as a result of a study
(Scapino, 1976) which attempted to dispel the notion that relative to other mammals,
the attachments and proportions of the digastric are highly conservative within the
Carnivora. While it is true that the digastric of carnivorans is genrally large and
columnar and spans the distance between the cranium and mandible, some carnivorans
differ markedly from the typical carnivoran pattern. In some aquatic or semi-aquatic
species of several carnivoran families (otariidae, phocidae, mustelidae) the digastric is
large and powerful as an adaptation for rapid abduction of the jaw immediately prior to
prey capture. Felids differ from other carnivorans not in the relative size of the
Figure 5, Lateral view of skull of Canis familiaris (above) and Felis concolor (below).
(From Scapino, 1976) a) attachment areas of digastric to lateral face of mandible
(sltaded area), b) total lengtli of digastric attachment (solid bar), c) position of
mandibular symphysis (S), and d) position of mandibular symphysis in Canis if facial
skeleton lengdi is hypothetically shortened to equal tliat of Felis (S').
20
•xn/U Stull ^ no^iacfl;^ 6 f£ nmftft ifd rbui*
‘A fuwi^ul-f) niymw
HHHH
iiMli 0 # 46 n ^usiovirrtiij *10 ^ij^^lort^pwn 3ns«!3|»b1«fT -v
. ®
■••Hil‘ '->) {iib srli t rd t<kyj(j«fr:5rf48 J^fiw (dtCi .ortIsqpKjSl)
D^' ^
D.i< nifHiw fjviiiivr^rioii \:i(iglfl m >iHOinfjq<yiq Ui* mnaiwbajiifi sirfJ
en«TtJVi{tiBi) 'to o'flltfiaib ^1 Jferb am’ jrf if a^lirtVj(n«|Qvitt^
' '-^ ■ ,
'Tfjnjji kMirm/jinjnl af3#8^4<b iwtf to
M TP
slhtupssrinm io ^moe rtl .fi.mijjtq Td^ib s:!il
■ a '
•': .linwgru 3;ii (rislutaiffim. l0m3l!e w wtoje 9
ta ■' '.-1^ ^'‘ -'^ ’ i.®'‘ **
i!ti itshq ^««jtfbarwfu wi?(art) 'io Wqif l® fts <0 lu^awoq to ag^
1^.
^jiii Ki asiE ^v(i|[^Qr 5^ rir }Wi |flr*c^^^Hib,1^^ usTltb ibiJo^ ^»Tq^'
lU.'
li‘Mi»M) toll ia'AliiA
,f’^> in M '0i0h4g j
■; fi', .M-
n..' ",!.',
digastric, but in its positioning, which is altered as a result of their reduced jaw length
and stringent gape requirements.
In felids, the digastric arises posterior to the tympanic bulla, and extends
anteriorly medial to the masseter to insert on the mandible (Figure 4a,d,e). At roughly
its midpoint, it is divided into two muscle bellies by an often indistinct tendinous
intersection. As shown in Figure 5, the insertion of the digastric (solid bar below
mandible) in felids differs from the typical carnivoran pattern, represented by Canis, in
that it extends anteriorly to reach the symphyseal area; the same is not true for
canids, even when the length of the facial skeleton is altered to equal that of the felids.
It has been suggested that this anterior insertion of the digastric arose in felids in
conjunction with the development of a shortened facial skeleton as a means of
achieving a wide gape (Scapino, 1976). Because the shorter facial skeleton of felids
relative to canids requires a wider gape in order to achieve a similar degree of
separation of the canines and carnassials, the insertion of the digastric is shifted
anteriorly; this has the effect of lengthening the muscle and increases the distance
through which the muscle can maintain tension to effect abduction.
TEMPOROMANDIBULAR JOINT (TMJ)
In determining the potential movements of the jaw it is necessary to examine not
only the placement and direction of pull of the masticatory muscles, but also the gross
structure of the TMJ, for its construction plays a large, perhaps even primary, role in
determining the degree of mandibular movement. The temporomandibular joint of
felids, as in all carnivorans, consists of an elongate, cylindrical mandibular condyle
which fits into a correspondingly shaped glenoid fossa on the zygomatic process of the
temporal bone. The bony structure of the glenoid fossa creates a trough for the
transversely expanded mandibular condyle and therefore grossly limits motion at the
21
m
32
f ; -1
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t %
h%f
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' ^'w.Wjs
t « .'
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ii>srji
F''s»»i 'n
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r
ipP'^^^W^P^ipE
* j w f fr^. ' j;
.^<11 ,{ i '
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ulli"»'il
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(*' J s
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joint to the orthal movements of abduction and adduction. A well-developed
postglenoid process and a small anteglenoid process form the posterior and anterior
boundaries of the glenoid fossa. Interposed between the glenoid fossa and mandibular
condyle is a thin articular disc that divides the joint capsule into superior and inferior
compartments and is attached to the joint capsule (Fox, 1965; Gorniak & Cans, 1980).
The emphasis on the hinge-like motion of the felid mandible in descriptions of
carnivoran jaw mechanics (e.g., Smith & Savage, 1959; Becht, 1954) obscures the
fact that movement at the TMJ is quite complex, with rotation and translation occurring
about three axes (Gorniak & Gans, 1980). While the primary jaw movement is rotation
about a transverse axis passing through both mandibular condyles (as in jaw adduction),
other movements, although very minor in terms of displacement, are necessary for
engaging the carnassials. Most notably, this is accomplished by mediolateral translation
of the condyles within the glenoid fossae. Despite the stout ante- and postglenoid
processes, anterior displacement of one condyle can occur when the mandible rotates
about a second axis passing vertically through the opposite condyle. A third axis of
rotation is defined when the working side mandible encounters resistance in jaw
closing. In this situation, the working side of the mandible is (for the most part)
immobilized and rotates about its long axis as the balancing side continues to close.
In a felid skull, movement about these three axes is easy to demonstrate, and the
TMJ can be disarticulated with little effort. In living felids, however, the degree to
which these motions occur is restricted by the joint capsule and its ligamentous
thickenings, which provide the major source of stability for the joint when gape is
wide. In this situation, the capsular ligaments limit the degree of jaw rotation and
translation about all three axes; they are particularly well developed in areas lacking
bony support, and aid in preventing dislocation of the joint. Stout medial and lateral
22
A brw ntirtow4>ci» \& lansimavarn i£dl}i9 W<l OJ iniot
K
lon-jirtfi b/iB ToiTwnoq ')(t) nnol ^l»Dtr^q ItHonslgoinii Ite^r/e o bionalaiioq ^
SJ ^
fflL-
iBh«»lbiiWTt l**in biottalij arlr hunnaiij -mi lo 2$fiRbf[Mxi
5' '2?'. ■
TCiii - inr bmi ignaqu/. « '>«! slUAqirj 3ni1>( aril PR»trtvib 'srij ^elb nirt* Ji «( ®
■]»> .;r^% 9fUf?.<4B3 oji
iw er
to ?.wfjaqii&2ab iti 9l(5fbri*rn ‘jrit io «t3S)om sjiibtagrtiW afb no «iaijfJqma »%T V' t lig
" ^ ,
'>rit mtHut'ki I . Jria^fl I ,, 1 ttiirnlt ..
Si4i ■_ BT *
irtniocoo iwttslafict) Inti* not:^uo!^ri^'v ,ySf<:jm«wi'5i}laj> #' l'MT 3!b )ri l«am&vora isriJIos!
••rr
ffofiftjcn if tmmmim wbc yir^’ci ari^ aitri’#;i(,QSk^ ^ ;)^«?riT(oO*>) ftlxA 93irtJj,iw^
^dVofv^ilbbA ^4^ t)l laV I9iff)dv«nint n luods
•i . . ^ '3 !
toT YwijiftiWJTsn atfl 1b ^ riaw* 'ri|iii Torilo
•oiiiiteftrw biiattriortrJtJi l«oM ^riJ
^ ,, ' ' ,.
■ ’vw , ..a,
e«aif afditem nsri'^ idm-m^ wi ,2a«wo<yt<i
•i; ■' : , , , , iji ■
)o ftiim ini/tt A af^A>qqG #jt8 bficmsi « miodfi
wfit m aoiiaiRl^T >t5irtiro6fi^ aMlbmb risriw ‘jamlab ndii«lcn
nuq itkim aril \cPt) ^i sfiJitwjgm. sriJ ^ w* .jrtfaoio *^ •
® ■ JBi *18,': S ' ' ^jtv.
m.
3...
m
Hf
,040^01 «awr^lrt03 tbix 3rf3 8slsij?&jcri #atw^t i3rtt
0^
life;*
t)rtj link ,miiinrm^ m ei. »aif)j baariJ 1bod4'^fi^rt9v<3^^ « nl
'■■'ffw
01 ttib rt)%J.iol3b'$bijliife jjd'fiBa tMT
^Ht riairiw
m , , ,"■ ;: ' imm ,, - $■
„ ai aqfi| nariw ip^ oiil vit ^0 ob|7**^ HMri^v* y«snin»>fatil} ^
Si S3 p %^''" ' ' '" ''^ '^'■■■''
■ bufi noii4ir/i wf{(1o aril timtl R’rii nl ,obiw *
•■ Pf. . ' '.V' : ' y ‘-t' **"
pjxiilri BfiiiiB fli ba<|biwfo tbw iiGiiKlen^’Utn
'» '^Y.
fct(»ii Ifilbam liwlii SSrri) >> \flQd sr.
capsular ligaments form the side walls of the joint capsule, and along with the posterior
capsular ligament, limit transverse translation of the condyles and unilateral rotation of
the mandibular rami about their long axes. The mandible is buttressed against posterior
displacement by the stout postglenoid process, while anterior displacement is prevented
by the posterior capsular ligament and the small anteglenoid process. The anterior wall
of the Joint capsule is much thinner and weaker than are the other walls which bear
well-developed capsular ligaments, and it probably contributes little to limiting motion.
In addition to the capsular ligaments, stability of the TMJ is achieved by the
surrounding masticatory musculature, most notably the posterior parts of the temporalis
and masseter (Scapino, 1981).
When considering the importance of capsular ligaments and muscles in
maintaining the integrity of the joint, it is important to note that these elements limit
various motions only when the jaw is opened wide (i.e., the tips of the canines are
separated). As the jaw closes and the teeth near occlusion, the role of restricting motion
at the TMJ is shifted from capsular to dental elements. As the tips of the canines pass
one another, placement of the lower canines into the diastema between the upper
canines and incisors limits translation of the condyles within the fossae, and prevents
rotation of the mandibular rami about their long axes. As closing proceeds, the
overlapping carnassial blades further restrict these motions while also preventing
anterior displacement of the condyles.
Studies of the TMJ have attributed its position relative to the mandibular tooth
row (i.e. "high", as in herbivores, or "low", as in carnivores) to improving the
mechanical advantage of masticatory muscles (Smith & Savage, 1959) or effecting
simultaneous occlusion of the dentition (Davis, 1964). In one of the first major studies
of mammalian jaw mechanics. Smith & Savage (1959), state that the location of the
23
TMJ above the horizontal level of the mandibular tooth row in herbivores increases the
moment arm and therefore the mechanical advantage of the masseter muscle. In
contrast, the TMJ of carnivorous mammals lies in the same plane as the mandibular
tooth row, resulting in a reduced moment arm and decreased mechanical advantage of
the masseter, and an increased moment arm and mechanical advantage of the
temporalis.
In his study of mammalian jaw joint position, Greaves (1974) presents an
alternative to previous studies which focus on the relationship between the TMJ and the
mandibular tooth row. He examines the rationale that movement of the TMJ results in
increased mechanical advantage of certain masticatory muscles, and finds this to be an
unsatisfactory explanation for TMJ position. In discussing the problems of this
explanation, he focuses on ways (other than movement of the TMJ) in which increased
mechanical advantage of masticatory muscles can be effected, the conservatism of the
basicranial region, the importance of the relative distances between mandibular and
maxillary tooth rows and the TMJ, and the TMJ position relative to discrete functional
loci of the dentition, rather than relative to the tooth row as a whole.
The mechanical advantage of individual masticatory muscles can be altered in a
number of ways, including changing the relative positions of the TMJ and tooth row,
changing the jaw geometry and/or changing the patterns of muscle attachment. While
Smith & Savage (1959) focus on the fact that elevation of the TMJ above the
mandibular tooth row increases the mechanical advantage of the masseter (as in
herbivores) and depression of the TMJ results in increased mechanical advantage of the
temporalis (as in carnivorous mammals), Greaves points out that simply elevating the
TMJ may not be the "best" method of imparting increased mechanical advantage.
Remodeling of the mandible by altering its overall length, the morphology of the
24
HfU tSafirHOIt' ill WM $0 ^
K
^i'«cb tMT* ss
^ -... (| 'fit
ni .9titvm TOuw-am ^aiawwfc^’l^iipii^^ fcstt*
vUiHikiiui:ft :*rti sAilq 9Htr^ ol (foil k> ll43r jiu ^Wfimscn.
"to ug^unvbA b^wRM^ Ijjji miA ji?»/jrt«>m b^K?l3fo^»^ Jt fH rfitxi^
9rtf' >0 jo»f5TO»rt-:-jj^.ypftfm)B
.aiismiSai
,i!i iJfiaaiq eavi^tO >/ici>))j£K| wH^ fmiimmm 'iQ vbvu mif nf
m
nfb Uns If^T tos^irf ){|i:dewuH«tfj 3(1+ ap c3(h«if avbemaslB^
.0 '»- , iM ' -■'O- ^ '■ a~m
/iaadoi «|/tJ zlwtH {)ftfi yiqJKVrt>|(n
a
3irti wfoidoiq J)rt} r»t .fidwlwq 04 T ioT itottftirjrtqxii
a ^ ^ "s
iiiiiWRnwt). iMv-f ititewao) !iMl,..»'#ioi}Bndf«9.^
■ffi ig ,C^, - . -.T, . —
3(ti -grillKVT^aaoci-aiLf isf::
Iti;
^ . -
^tF 'Maaifcmi
ijl
iSr-'!
bflj littidwisffi jrr^^n tmamitsd
'!V"
5cvi3iz»i> cfl yvij&wi JJb: to to (1)<x>KNrtallF)<(fini
'--B wdtR'i wixrjdfiab to^''iSl:
^ - .r “ '"
k- (« bitajiiis 'id' niSSi'
tbnoi 'ulii tMT' i>rb »’+‘n
f j, ' ^ ■ '-''.2^^
j!
>jj4W F.7^n(ifc>W!a;4>laa^frT 1* v/«[ to'gn^sFtoa
3ji> -avto I.MT' ^rfj
m-.
3^ 10 agBm^vb^ji toiffifbam b'>;ww)3W bos <»iovfthad«
0 ' '1!F .'«■ ' ■' "*' ■ ' '
,■'■■■•..- .|l^ "Mt '■•'S
3
^^mifivvb ift.-siV dltioqoiaj ^
coronoid and/or angular processes, and/or the orientation of the tooth row can change
the moment arms and mechanical advantage of various muscles just as effectively as
moving the TMJ. Furthermore, the complexity of the TMJ, its close proximity to other
important basicranial structures, and the consistent relationship between the position of
the TMJ relative to the maxillary tooth row in both fossil and recent mammals are cited
as evidence for the conservatism of the TMJ and the low probability that sufficient
selection pressure exists to warrant its movement (Greaves, 1974).
In the case of carnivorans, Greaves asserts that consideration of the position of
the TMJ above, below, or on the same plane as the mandibular tooth row is a moot
point. Rather, the important consideration is the difference in the position of
mandibular versus maxillary tooth rows relative to the TMJ. If these distances are
equal, as shown in Figure 6a, occlusion will occur simultaneously along the entire
b
a
Figure 6. The effect of TMJ-tootli row distances on occlusion. (m=distance from
surface of mandibular tooth row to TMJ; n=distance from surface of maxillary toodi
row to TMJ.) (From Greaves, 1974)
a) Simultaneous occlusion of die toodi rows occurs when the distance between die TMJ
and both tooth rows is equal, b) Scissor-like occlusion occurs when the distance
between die TMJ and bodi toodi rows is unequal.
25
IM
~m ■'■'^' ■ ^
/ ,,^ . ■ - ^ ■ r3RSSI
-1iib«i-y#fij}^QM^ owi?t> Id ^L‘- «— -J|4ito^.''i*- -- .
ncnfiw!*^ js»it,/A*«Mr->! mitmqioi
?ir^
m
“ia , ""■'“'■Tv -
■3
tiH *mrji:i5>bc
P.€A^J|4'
'$],... >.■ '. ■‘‘'^
li • '4 .vmbx^^rn
^ - ’■ "^ 'T ’'il ' ,
5ur iBoniaHt^ -^eaiiT T^ .'»rU tw Kt^ Vttlil • '^- »>Kj^wd^b^airo
|flt^ ' ^ Mm.
.fhrtli »iyo8e»t>-» /H'> <■*».■
fljdftw , , ,
y^SW>i«4j-
length of the tooth row. If these distances are different, as shown in Figure 6b, initial
occlusion occurs posteriorly and proceeds anteriorly in a scissor-like fashion. Thus,
Greaves argues that whether the TMJ lies above, below or in the same horizontal plane
as the mandibular tooth row is of little consequence; as long as the distances between
the tooth rows and the TMJ are different, the carnassials can be correctly positioned
and effect the scissor-like occlusion necessary for proper carnassial function.
Furthermore, Greaves states that in carnivorans, the positioning of the TMJ
relative to the entire tooth row is not as critical as is the positioning of the TMJ relative
to the carnassial blades, since this is the area where the shearing action occurs. In
carnivores, he argues, the distance between the TMJ and the shearing blades of the
upper and lower carnassials should be unequal (Figure 6) in order to effect scissor-like
occlusion from back to front. However, this statement seems to be an unnecessary
addition to Greaves' argument, because as far as the proper functioning of the
carnassials is concerned, the presence of carnassial notches allows the carnassials to
accomplish the task at hand regardless of the manner of occlusion. Because each
carnassial possesses a carnassial notch, approximation of these teeth, whether in
scissor-like or simultaneous occlusion, creates a lozenge shaped space that traps the
food item between the carnassials and prevents it from slipping anteriorly.
MANDIBULAR MORPHOLOGY
The tight link between felid predatory behavior and the strength of dental
elements was noted earlier in the discussion of the morphology of felid canines, which
are able to resist the heavy mediolateral and anteroposterior loading encountered in
predation and feeding. A similar adaptation is also present in felid mandibles, which
possess greater strength in resisting bending in oblique, parasagittal, and transverse
26
itfjim .dti fti nwwl* iB .Jftsiaritijb m H .won ii»iU >o rii^ajt »>
.evjff nmM t m »l»®80iq tma mrri>» nd^lctoo
da«»q ktaOsi-Mid wwa aHl Hi m wr>tet» t/VJKiift «»yiR3^
na5W9d wafiaj«?b »rtJ tc ^*01 ioi allfDlo I'l wot wlutiftem ^ m
bff^tfHtieoq vimivtQ M<>o s*lj ,mot»l)rfe im IMT oAi b<w »wot fijooi odj
.ftoiiifjuT noreu!a:io svUi^io*^^ lo^ls bi^
Ml- .
.■M-
° 8!>-^ »9^ ' '*^' 'a'''' '*" ' T' '"^
S'/Oqlirt U^T i}43: ip (:Mi''ii>iM^pn ii 'WrW'
t»] .2111930 tfOiiOB ^fllTf^fU 5<<j -qifbHW ti
aife 1(7 aataW iB IMt !Mi sawovioigq
m
'-sS'"
.:t^
a4f**Toa2i'9< loanpol'isffino q<v0''''5^^S)..kup^ HWMs
• 5P' ‘ , ; -i.r
. ..:'■■■' ■^", •■.*... - ??: iJ-
3«ti Icj wiffioituntil lief 'isdyfioiO oj aoiifttbs
■'•! iiE ' ■■_, ® gj
oi 2lfi:»«is6rtKra o(fi awoHs lo^pup^sPiq
'" n."" .. 1W-. ’®* ' . '.I# ■"' ■ ' ,^ _
W
..^ ■■ ,■ ®-
■■ Vt . . «'■ -■'• ■ B.-" @tmia
cto .rtowImTlo Adi} djikjmo^
•pfli «qcTHiirt3 bt)(Otfd* Tfnss;^^ B latsspo IS
^ ,>*? ;® • ' "V , "’■ ■'.,... ■ .'■
" ^ ' ■— . Mr. '•’-' •rtLA-'— &f" '■ ■•'ll
L I '
______ ' B* ® -X^v
toolr Ifx sfU^bna wvMd^ yioj^qiq Mk>t nppw^pd pfft
' ■ ; iSi’ ^ ’ - ' ' T
t<v/ ■# qo&osfb ^ ZH
‘?^'i
w„.
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pfwvaBru twiB .Iwi^fWiBq .3BipHdo m gnijbffi^^ r|i
planes than those of other carnivorans, a reflection of the greater loads applied to their
jaws in prey capture and consumption (Radinsky, 1981a; Biknevicius & Ruff, 1992).
Greater strength of the mandibular corpus in resisting bending in the parasagittal plane
is a structural necessity to counter the deep, powerful, and (often) sustained killing
bites of felids. The strong canine bite of felids is a consequence of the greater
mechanical advantage of the felid temporalis compared to the temporalis of canids, for
example (Radinsky, 1981a; Van Valkenburgh & Ruff, 1987). Because a strong canine
bite results in a high degree of corpus bending (Hylander, 1986), buttressing of the
felid mandible allows it to resist greater bending forces than is the case for other
carnivorans.
The powerful canine killing bite of felids relative to that of other carnivorans is
usually attributed to their relatively shorter Jaw length (Kruuk & Turner, 1967; Eaton,
1970; Kruuk, 1972; Schaller, 1972; Ewer, 1973; Leyhausen, 1979; Van Valkenburgh
& Ruff, 1987). The abbreviation of the felid skull results in a reduced moment arm of
resistance, increasing the mechanical advantage of the masticatory muscles, and
increasing bite force. Therefore, given a canid and a felid with similarly sized muscles,
the felid will be able to produce more force at its canines (Van Valkenburgh & Ruff,
1987).
Greaves (1985) also addresses the notion of higher bite force in felids, but does
so in a rather different fashion and reaches conclusions which contradict those of Van
Valkenburgh & Ruff (1987). He states that the mechanical advantage of the jaw lever
system in carnivores is unaffected by changes in jaw length because all carnivorans
possess similar jaw geometry regardless of the length to width relationship of the jaws.
Instead, the primary factor influencing bite force is the relative jaw width among
carnivorans. Greaves states that in a felid and a canid of the same jaw length (Figure
27
7a,b & 7c, d), the geometry of the jaw lever system is the same, while overall body size
is tremendously different. The larger body size of the felid translates into a difference
Figure 7. Dorsal views of camivoran skulls; shaded area represents jaw length, vertical
lines indicate equal jaw length, horizontal lines indicate equal jaw width. (From
Greaves, 1985) a) gray fox (Urocyon cinereoargenteus) b) bobcat {Lynx rufus)
c) domestic dog {Canis familiaris) d) mountain lion {Felis concolor)
in absolute muscle mass and a much greater bite force than that of the canid. In a felid
and a canid of similar jaw width (7b, c) overall body size is similar, as is the absolute
masticatory muscle mass. Thus, the similarity in jaw geometry and muscle mass
translates into a similar bite force for these two animals.
The way in which the hemimandibles are joined at the midline has been
investigated in depth for carnivorans (Scapino, 1981) and has been found to vary
considerably depending on factors such as body size, diet, dental morphology and the
demands of prey capture. The anatomy of the mandibular symphyses of carnivorans can
be grouped into four classes, based on details of the hard and soft anatomy of this
region, and in many carnivorans, these divisions have clear functional correlates. The
28
■a;., V a'/'??
' 'T' ^ {
Aii
' Ia
,/
symphyseal anatomy of felids is apparently a consequence of the masticatory demands
imposed upon them by virtue of their body size.
Stated in the simplest of terms, the mandibular symphysis is the site where the
symphyseal plates of the hemimandibles meet in the midline and are bound together by
a three-walled capsule. Ligamentous thickenings of this capsule and ligaments spanning
the distance between the symphyseal plates help lend stability to the joint; the size and
degree of development of these ligaments is a reflection of the various stresses imposed
on the symphysis. A strong superior ligament resists the potential for separation of the
joint dorsally, while the weaker inferior and posterior capsular ligaments limit the
potential for separation ventrally and posteriorly. Also aiding in resisting separation
forces and providing joint stability are transverse and cruciate ligaments, which span
the distance between the symphyseal plates. A fibrocartilage pad is variably present
anterosuperiorly between the opposing plates, and is surrounded posteriorly and
inferiorly by a series of interdigitating rugosities and concavities of the symphyseal
plates, which, depending on their height, provide added stability to the joint. The
anatomy of these features and the degree to which they lend stability to the joint are the
grounds for dividing the symphyses of carnivorans into four groups (Scapino, 1981).
Class 1 symphyses are characterized by symphyseal plates that are flat or which
bear slight interdigitating rugosities and concavities; a conspicuous fibrocartilage pad
intervenes between the symphyseal plates and fills a significant portion of the joint
surface. Class II symphyses are similar to class I symphyses, but higher rugosities and
deeper opposing concavities result in more interdigitation of the symphyseal plates. All
symphyses of small cats are classified as class I symphyses, while class II symphyses
are absent among felids. Class III symphyses have a very small or absent fibrocartilage
pad and increased interdigitation of the symphyseal plates compared to class I or class
29
I
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II symphyses, and are present in large cats. Class IV symphyses are totally fused, and,
with the possible exception of a partially fused symphysis in Felis marmorata, are not
present in felids.
The grouping of nearly all felids into two symphyseal classes is apparently a
consequence of body size. All small cats have a class I symphysis, which allows slight
flexion and mobility at the joint, while large cats (with the possible exception of
Acinonyx) have a class III symphysis, which is much stiffer, and has little mobility
compared to a class I symphysis.
Scapino (1981) attributed this difference in symphyseal anatomy to the external
and internal effects of scaling encountered by large versus small cats. External effects
include the fact that as animals undergo a linear size increase, the increase in the mass
and load-bearing capacity of their supporting structures is positively allometric
(Yamada & Evans, 1970; Anderson et al., 1979). Thus, large felids consuming large
prey must exert relatively greater masticatory forces than small felids consuming small
prey, because the supporting tissues of the larger prey are more resistant to
fragmentation.
Intrinsic factors influencing symphyseal anatomy concern the maintenance of
geometric similarity across a wide range of body sizes. If a felid were to double in size
and maintain functional equivalence (i.e. the ability to exert isometric tension at
optimum muscle lengths), muscle cross-sectional area would necessarily have to
increase by a factor of eight, or muscle pinnation patterns would have to be drastically
rearranged (Scapino, 1981). Because a marked increase in cross-sectional area does not
occur, and the internal architecture of the muscle is much the same in large and small
felids, the masticatory strength of large felids is expected to be relatively less than that
of small felids (Davis, 1962). This, in conjunction with the aforementioned finding that
30
the prey of large felids is more resistant to fragmentation, leads to the conclusion that
large felids are at a dual disadvantage; while the structural elements of their prey
require them to generate a relatively larger masticatory force, they are less able to do
so because of the limitations associated with their larger body size.
As a way of countering this dual disadvantage, Scapino (1981) states that large
felids have acquired a stiff (class III) symphysis as a replacement for the primitive
carnivoran condition of a flexible (class I) symphysis. Because a stiff symphysis is
better able to transmit force between the balancing and working sides of the mandible
(Hylander, 1977, 1979; Beecher, 1977, 1979), large felids are able to recruit more
balancing side muscle force than are smaller felids which have a relatively less stiff
symphysis.
JAW MECHANICS
While most recent studies of mammalian jaw mechanics assume that occlusion is
unilateral, and that both jaw joint reaction forces and muscular activity are bilateral
(although not equal), many early studies failed to acknowledge all of these facts, and
therefore were unable to explain the forces generated during mastication (e.g. Gysi,
1921; Davis, 1955; Smith & Savage, 1959; Turnbull, 1970).
In a study of the spectacled bear {Tremarctos ornatus), Davis (1955), states that
the typical class III lever model typically used to describe the mechanics of the
vertebrate jaw is an oversimplification, particularly in the case of carnivorans, and
presents a new model of the carnivoran jaw as a modified class 1 lever. Under a class
III lever system (Figure 8a), the forces exerted by the masticatory muscles produce a
dorsally oriented force at the jaw joint (the fulcrum) that exceed the physical limits of
the joint and lead to failure. As an alternative, modeling the carnivoran jaw as a couple
(Figure 8b) has the effect of reducing forces acting at the joint to zero.
31
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Rgure 8. Tliree lever models of mammalian jaw mechanics. R = resistance (force
exerted at dentition); E=effort exened by masticatory muscles; F = force at
temporomandibular Joint. (From Davis, 1955)
assuming that the temporalis and masseter exert equal forces which act to rotate the
joint around a transverse axis. However, this alternative is also not completely
satisfactory given the fact that the temporalis and masseter do not in fact exert equal
forces. Because the temporalis is larger and much more powerful in carnivorans than is
the masseter, Davis presents a bent lever (or modified class I lever. Figure 8c), which
has a better mechanical advantage than the class III lever and which is a better
approximation of the true function at the joint. Because the bent lever model (Figure
8c) does not reduce the force at the fulcrum to zero, as does the couple, the large
postglenoid process of CcU’nivorans is needed to resist the large posteriorly directed
force at the joint.
Turnbull (1970) slightly modified Davis' findings, by pointing out that the
couple is indeed an appropriate model, especially for the Carnivora, because of the
synergistic action of the masseter and medial pterygoid. He also presents the "useful
32
"O' Y. -^' 'i}.*
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m
mam-
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''■' ^^^ ■ "'' ''^i* "W "” •i'E H* * J^.
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power" formula as a way of addressing jaw mechanics in a comparative light.
Combining aspects of muscle characteristics such as relative proportion (mass, weight,
or volume), position, cross-sectional thickness, attachment points, shape, leverage, and
direction of pull results in a single value for a given muscle, which can be used to make
elementary comparisons of the mechanical efficiency of masticatory muscles between
taxa. Using this formula, Turnbull finds Felis to be easily distinguished from other taxa
on the basis of the small size and underutilization of the pterygoid musculature, a
characterisic he finds is typical for carnivorans.
These and other early analyses of mammalian jaw mechanics focus on the
function of the dentition, masticatory muscles, and jaw joint on only one side of the
head. Such models are clearly not adequate in predicting jaw mechanics, as studies of
mastication in many mammals have demonstrated that masticatory muscles are active
bilaterally (Dessem, 1989; Hiiemae, 1976; Kallen and Cans, 1972; Hylander, 1979;
Gorniak & Cans, 1980; Weijs & Dantuma, 1981) and that there is bilateral resistance
of reaction forces at the temporomandibular joints (Hylander & Bays, 1978, 1979;
Hylander, 1979). Evidence such as this led to the belief that considering the jaw in
lateral perspective is not always the ideal way to address jaw function, and prompted
several workers to advocate looking at jaw function in "less traditional" ways, such as
from a frontal (Hylander, 1975), or occlusal perspective (Greaves, 1978), thus
incorporating the bilateral function of the muscles, dentition, and TMJ.
In particular, Greaves (1983, 1985) proposed a bilateral model for studying
aspects of the function of the carnivore masticatory apparatus. First developed for
ungulates (Greaves, 1978), and then expanded and applied to carnivores (Greaves,
1983, 1985), this model considers the relative magnitude and position of resultant jaw
muscle forces, the relative positions of masticatory muscles and teeth along the length
33
of the mandible, and the tradeoff between gape and bite force. Greaves' model assumes
only three points of contact between the mandible and skull during mastication: one
between each mandibular condyle and the corresponding glenoid fossa, and one at the
vertex of the carnassial notch on the working side; these three points demarcate the
"triangle of support" (Greaves, 1978). The model also assumes that the forces exerted
by the jaw adductors are resolved into a resultant force acting in a plane perpendicular
to that of the three contact points. Figure 9 shows a felid mandible with various points
mentioned in the text indicated by the appropriate letters. Under the conditions of this
Figure 9. Dorsal view of die lower Jaw of Felis catus. Jr, Jl=right and left jaw joints;
c=camassial toodi. (From Greaves. 1983)
model, bilaterally symmetrical action of the jaw adductors acting at points A and B
produces a maximum resultant force at point O, midway between the mandibular rami
near the point of muscle insertion. The jaw lever is represented by the line JrOC, which
34
connects the left carnassial and right mandibular condyle. The differential activity of
the muscles on opposite sides of the head will determine where along the line AB (i.e.
O, P, Q, B) the muscle resultant will lie and what line radiating from the carnassial
notch will represent the jaw lever (i.e. JrOC, MPC, NQC), as larger forces exerted by
muscles of one side will shift the resultant force toward that side. Differences in the
positioning of muscles along the lines JrT and JIC will have the effect of placing the
resultant force more anteriorly (along line OG) or posteriorly (along line MO).
Two models bear on the positioning of the resultant muscle force along the
length of the jaw. The first (Greaves, 1982) states that placement of the muscle
resultant anterior to a point one-third of the way along the length of the jaw results in
large torsional forces about the long axis of the jaw, and therefore the possibility of
failure of the mandibular corpus during feeding. To prevent this torsion, the resultant
force of the jaw adductors is predicted to lie somewhere along the first one-third of the
jaw. Greaves' model was initially developed for ungulates, the jaws of which
presumably undergo torsion, which in their case would be a result of internal forces
(their own masticatory muscles); this is in contrast to the jaws of carnivores, which are
not only subject to internal torsional forces as a result of the action of masticatory
muscles, but which are also subject to external torsional forces as a result of struggling
prey. The increased robusticity of the mandibular corpus of some carnivoran jaws
(Biknevicius & Ruff, 1992) may lend some resistance to torsional as well as bending
forces, in which case, the anterior position of the masticatory muscles may not be as
highly constrained in carnivores as Greaves states.
The second model (Greaves 1983) predicts the position of the resultant force
along the length of the jaw in carnivorous mammals, in which gape and bite force are
equally important. Anterior placement of the muscles (at points F and K in Figure 9)
35
■^1 “ ' '!i3
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,*1.1) a/, ^ m(i
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^1 (tf ejntt*'i*T»iCl .a&jj* iui^< bt«wuJ<;iO'jp> yftit)t{;g5i iijiH iHw •^a aftah) MJasarm^
jd
■ -- '!"V
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:>bw^rfnc« sflT .wM^1o rtignai^
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111
I ■•
utsiliiasit i«i) ,o<>igi0)'«tft|i 0|v^v* ^
••'^' / ’ 1^ ^ •IT-
9fli la biri&“ttfir> mi^ aril griolft orb^)c#»tQ « ^ arfi K) acyhd
■i4'r‘..i. ...i'^ iifl^ t
.. a...,E . 3s‘si ,e5?ioVioiBo:1iO;twiiiad)^ o'j ' t?j5*i)^f(^, iTiV'^iift :\i^tiim^.mmmW |h^iiiWb)*S
'4 ..^ ^
iC*-
L^’'|r^''
SH ■ ^ ' **
' y’loit'iijssfl/tr'ta nolitsu airtiW b «ii b;r!oi3f.wi tnsrv'fajitl j^aldtie vino ion
^ilgjurt)? ^ ilossi ■ fi Bfi •zaohyi'^a.^hiay^^ , oi'
B ^ ^ ■ ' ^ " '^■'
gnlbnwi )?fi Haw u liuxoie’ioror itr^ijJvanalllf)^,^
m \ '•m ^ ■■''^ ■w,
t0 «tJ*wi yjjni ^'j^cw^jp4jntartrfo:^0a^^^ n< I
^ IS
91M v>ioi a#'w4 Isntt' '^Qij;,::fl'>»;|v/ r(?s*;l^t3SMS^4iW0T^'«^ dib, snol*., .“
{Q nr;i ,h0« 7
''%'' ' . ^nilH< •T’V
applies a larger proportion of the muscle force at the bite point, but, in the case of
carnivorans ingesting relatively large prey, has the undesired effect of limiting gape by
interfering with the use of the carnassials. Maximizing gape by moving the masticatory
muscles posteriorly, however, has the equally undesirable effect of severely reducing
bite force. Because carnivorans need a wide gape to engage their posteriorly placed
carnassials and/or to grasp relatively large prey, and because they need a high bite
force to penetrate and maintain a hold on the prey, one would expect carnivorans to
have a jaw geometry which maximizes both gape and bite force. By comparing bite
force with the position of the jaw adductors at various points along the mandible,
Greaves (1983) concluded that the widest gape is coupled with maximum bite force
when the muscle resultant force is at a position 60% of the distance from jaw joint to
carnassial. Movement anteriorly or posteriorly from this 60% position results in a
drastic drop in either gape or bite force.
While Greaves attempts to remedy some of the inherent limitations of earlier
models of mammalian jaw mechanics, his model, at least as it applies to carnivores has
several limitations. When Greaves originally (1978) outlined his bilateral model of the
jaw mechanics of ungulates, he assumed that maximization of bite force occurs along
the length of the grinding tooth row. In extending his model to carnivores, he held this
part of the model constant in assuming that bite force in carnivores is similarly
maximized, but at a specific locus along the tooth row, the vertex of the carnassial
notch. While for a given muscle morphology, the bite force exerted at the carnassial
locus will always be higher than that exerted at the canines (due to the closer proximity
of the carnassial to the TMJ), it unclear why the carnassial, rather than another tooth,
such as the canine, should be site of bite force maximization.
36
There is indeed limited evidence that could be inferred as evidence that bite
force is maximized at the carnassials; forces of 2.0-23.25 kg were recorded at the
canines in Felis domesticus while forces up to 28 kg were recorded at the carnassials
(Lucas, 1982). However, given the inherent difficulties in accurately recording bite
force in often uncooperative subjects, the degree to which these numbers reflect reality
is not without question. It could be argued that bite force must be higher at the
carnassials than at the canines because the carnassials, by virtue of their elongate shape
and therefore greater area of contact with the food item, are less able to penetrate prey
than are the canines. However, the material that felid carnassials most often contact is
vertebrate flesh (a soft, brittle material), whereas the canines regularly encounter bone
(a hard, brittle material). As mentioned above in the discussion of felid killing behavior
and dental morphology, felid canines fracture the vertebral column and occasionally the
occiput of their struggling (and often relatively large) prey; this unpredictable loading
regime has been used to explain the relatively robust canines of felids relative to other
carnivorans (Van Valkenburgh & Ruff, 1987). In conjunction with this robusticity, it
could be argued that the bite force at the canines must be higher than at the carnassials
if the canines are to effectively fracture a hard, brittle material such as bone. Because
prey capture and killing is a necessary precursor to the relatively less demanding task of
severing flesh, it seems more logical to model the carnivore jaw under the assumption
that bite force is maximized at the canine, not at the carnassial. Viewed in this manner,
the bite force at the carnassials is a secondary, albeit functionally important, result of
canine function, rather than the primary determinant of jaw function.
Greaves also assumes that the muscle resultant is oriented perpendicular to the
long axis of the jaw. While this may be true during certain segments of feeding and
predatory sequences, it is clearly an oversimplification for the activities of the felid
37
masticatory system as a whole, for quantification of several aspects of felid morphology
(e.g., canine robusticity, mandibular robusticity, orientation and activity of masticatory
and nuchal musculature), and observations of felid behavior indicate that the forces
during feeding and predation are anything but predictable in terms of their magnitude
and direction.
MASTICATION
Although the way in which mastication proceeds from time of food ingestion to
time of swallowing is implicit in most descriptions of masticatory morphology and jaw
mechanics, recent use of cineradiographic and electromyographic techniques have
greatly improved the level of knowledge about the process of mastication. Along with
the introduction of a great number of descriptive terms for various phases in the process
of reducing food, these studies have elucidated how the patterns and degree of activity
of the masticatory muscles vary within and among mammals and how these patterns are
influenced by both the structural and material properties of the food items ingested.
Masticatory Sequences
A masticatory sequence can be defined as the series of events which begins with
ingestion of a food item, reduction of the food item, and swallowing of the resultant
bolus (Hiiemae, 1978). Within this sequence, one can identify handling, transport, and
masticatory cycles. Handling cycles involve the ingestion of the food item, while
transport cycles can be divided into stage 1 and stage 2 transport cycles (Hiiemae &
Crompton, 1985), which involve moving the food item from the anterior to the
posterior dentition, and moving the food posteriorly from the cheek teeth in preparation
for swallowing.
38
M
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()a?2:>Sfti 2/n9jr booT lehi>?i;n^ bus Imilim 34ril*iisd yd torr«u&n}
'.. ■: ■
Itt!— m- jft>'
•■' S»!i'SS3iaj“, ,^ , ..
... I
^ttj' noojfSj^ ’’
Ufi6 ,§rt»Tf>nwi^*n*jS UB’»’43!;}d fUfiliW rS^MnafiHV tuiocf'
^ ■ / ■ : ' ' " ra
,,, , .., si^w .,ni:5)Si’: boo5
5k(i m lOfWrtE mb TXfbil .mmrtw^
® ' ft- ■'^
t?"'
vfj rnoi^ N(<T0JV^^|ivo^^ bnji ,nrMindk itoi isiibq ^
si
Masticatory cycles intervene between handling and phase 2 transport cycles, and
are concerned with the reduction of food items. Masticatory cycles are of two types:
puncture-crushing cycles, in which there is tooth-food-tooth contact, and the teeth do
not intercuspate, and chewing cycles, in which the teeth achieve direct contact with
each other. Within the masticatory cycle, three different strokes can be distinguished.
The closing stroke (or fast close) occurs as the lower jaw moves upwards and the teeth
converge. This is followed by the power stroke (or slow close) in which the teeth meet
and muscular effort is used in breaking up the food item. The opening stroke moves the
teeth apart, and is divisible into a slow open and fast open, which may be interrupted
by a slight closing movement (Gorniak & Cans, 1980). More recently, opening
movements of mammalian jaws have been described as consisting of three phases: 01,
02, and 03 (Hiiemae & Crompton, 1985; Schwartz et al., 1989; Thexton &
Crompton, 1989; Lund & Enomoto, 1988). 01 and 02 are comparable to the slow
open phase identified above, while 03 corresponds to the fast open phase. While these
movements may afford more precise descriptions of jaw movements, as noted by
Thexton & McGarrick (1994), the fact that many of the earliest studies of cat
mastication employed older terms makes comparisons between various studies
cumbersome.
Jaw Movements
A widely used method of examining jaw movements in mammals has been to
map the movement of the canines in vertical and horizontal planes using
cineradiography (Figure 10). This method shows that felids have the lowest degree of
transverse motion among the masticatory cycles among mammals. Because of this, the
movements of the jaws in felids and indeed in most carnivorous mammals is usually
characterized as purely hinge-like, as discussed earlier. However, concentration on this
39
hinge-like motion obscures the fact that lateral motion, although a small component of
the masticatory cycle in felids, is crucial to the close approximation and proper function
of the carnassials.
Opossum Tretshrew
broum bat
Figure 10. Ltiwer jaw movements in various mammals, shown in frontal view with die
working side on die right side of the jaws. Note small degree of lateral movement in the
cat cycle, as compared to other mammals. (From Hiiemae, 1976)
Muscle Activity
The use of electromyography in studies of felids (as well as other carnivores)
has led to a more detailed understanding of the activity of the masticatory muscles and
has helped to dispel the widely held notion that purely vertical motion is the only
direction of jaw movement in felids. As far as is known, all carnivores chew
unilaterally (Scapino, 1981), and the disparity in width of upper and lower jaws
necessitates that there be some asymmetrical activity of the jaw muscles to bring the
carnassials into occlusion. The description that follows is based largely on the work of
Gorniak & Cans (1980), unless otherwise cited.
The reduction sequence begins with bilateral activity of the digastrics effecting a
slight opening of the jaws in a vertical plane. Additionally, the opening cycle may be
40
!
interrupted by "closing reversal" movements effected by low-level bilateral activity in
the zygomaticomandibulares and deep masseters. This closing movement occurs as the
food item is repositioned on the working side. Following this brief closing motion, the
digastrics resume their bilateral activity, and continue to be active throughout the
opening phase until maximum gape is achieved. As the jaw nears maximum gape, the
zygomaticomandibulares become active bilaterally in order to slow jaw opening. For
the most part, the jaw adductors on both sides of the head are active simultaneously
during closing, with only slight differences in the relative timing of onset and end of
activity. At the start of closing, the deep temporalis of the working side, the medial
pterygoid of the balancing side, and the balancing- and working-side
zygomaticomandibulares contract to adduct the jaw and shift it laterally toward the
working side. As closing proceeds, the jaw muscles are active bilaterally. However,
slight asymmetry in the activity of the working-side zygomaticomandibularis and
masseter and the balancing-side medial pterygoid maintains the deviation of the jaw
toward the working side throughout the reduction sequence. When the teeth contact a
food item, the bilateral activity of the jaw adductors becomes increasingly asymmetric,
and the speed of closure is reduced. As closure proceeds, the lower jaw rotates about
its long axis due to unilateral resistance on the working side, and the adducting forces
of the balancing side are transferred through the mandibular symphysis to the working
side.
While there is indeed asymmetry in the muscle activity of felids, as described
above, this asymmetry is very slight in comparison to other mammals (including some
carnivorans), in which there may be significant differences in the timing and activity of
muscles on either side of the head. Weijs (1994) divides the masticatory muscles of
mammals into three groups based on the timing of their activity: vertically-oriented
41
l'W|wnw»i'
.fwi)
‘ ' ' ' ; ' . i,. ''.yi
symmetric closers (zygomaticomandibularis, temporalis), which are active
symmetrically during fast close; triplet I muscles (working-side temporalis; balancing-
side superficial masseter and medial pterygoid), which move the jaw toward the
working side during fast close; and triplet II muscles (balancing-side temporalis;
working side superficial masseter and medial pterygoid), which move the jaw to the
balancing side during the power stroke. The degree of synchrony in the timing of the
these muscle groups is associated with the amount of transverse movement that occurs
during the power stroke; variations in this synchronization led Weijs to distinguish a
number of "specializations" in the masticatory patterns of mammals. One type of
specialization is found among felids, mustelids, and bats, wherein synchronization of
triplets I and II follows the initial activity of the symmetrical closers, and occurs as a
result of the intercuspation of the canines (bats) or of both the canines and the
carnassials (felids and mustelids). Synchrony of muscle activity also occurs in rodents,
but is accompanied by bilateral occlusion and protrusive/retrusive movements of the
jaw. The synchrony in the jaw muscle activity of felids results in a very reduced
horizontal component of the masticatory cycle.
Influences of other structures on mastication
Aside from the activity of the masticatory muscles discussed above, other
structures, while not always directly exerting force to reduce food, are equally
important in mastication. These accessory structures are of two types: structures which
aid in positioning food for proper carnassial function (tongue, hyoid) and structures
which effectively increase the force exerted by the masticatory muscles (nuchal
musculature).
The tongue is vital in transferring food within the mouth. The tongue moves the
food posteriorly and laterally to be chewed following ingestion, switches the food item
42
-jfpifsnslcd -irtETottmu 3**e-gft< iity^/) I tsltfitt nift ift|«ahJ3>mfrttt
9^ ^mi^i wet nffr i>vi&n il^jfrfw ,
•wUnfjqnrs* 3biV^4onBfKcJ) aala^wtrr tl Dlqfl! bets ,',»0*gL >4^ a4«r ||ph{t^^
srtf t)j worn dofdw ,(biO^’{iaiq lub;^ bits Wirtaii/n Urateqi#* obk ^ni^how
arfj lo snfmk wb ni A^kjiia lawoc) oHi ^!it'Wl> obit ^Iboi}^
® ' ■■»■ n ^ j «aL-^
^ ■'''* "v ' '' ' w
• •rffrii^iiilb a}.»^9WrHi
'*,.•■ „ . , ■ fii ®
;2, ^»^^0 ■i'ffc ifitcl r/t<54ff|i':EBai SiT t ni lo lodmfiifl
.:»5! **
to noilBsTrtoufjib'^^ >«c4 hm^. «l^.(toMisit&kx>q2
M ■ " ■ .-.-^^a m ® K- '
''a
8 2& fl03W> b^B ^rntfOl'i
'mn e^kii' II
.m
'»/!/ bnB aa<Tmia &rl) srt^ to rKjb^ ^
" ‘j ■
,e]/i3bdi rti ^iuoaoxjalfi Vy^rp'i^^'iZ Imw abito^ alfibwamto
!&
b(»6 '{^ b^‘w3<jmoaiai ai tod
b^omboi YtoY
. V “ ; . ^IbVJg '{ibis:iikmi ^ H i Ic m^oqfnoplittjoadtod
to miMudoI
aj»tb3UOT' »rii tmif 3mtA
' If.
i»
■v.-t]"
Ylficups. *sn
m
fbWw «^iiU3tn32 ov?Jto 5i# wtotob^e nmi&’Atmn ni infnoqmi
.abgnoJ) toi 3mfW»ii4iS;i ni biBi
-■>;!>,-
e ^ ' MHHi . '.■x^A\mmm:4
oMj R!J*^m ow^fKil bilT ,4jbpfS)aii:| ^bhv xi jiygnta
<V '• V. ■■®' liJ'''
,noij?KMt(4j 3^niV(dttoV sri '(ilsa»ltt) bfta^vitoiiajjsoq
% ;J
from side to side, and moves the resulting bolus posteriorly to be swallowed. In
addition, movements of the tongue may assist the neck and masticatory musculature in
disengaging food from the canines. While the bilateral activity of the digastrics
produces the majority of the opening movement of the Jaw, EMG observations of the
activity of the semispinalis capitis musculature in cats (Gorniak & Gans, 1980) suggest
that the nuchal musculature produces an upward movement of the head during opening.
This effectively increases the speed of opening, which helps to disengage food from the
canines so it may be transferred posteriorly to the carnassials. Similarly, closing is
accompanied by a downward movement of the head that increases the speed of closing,
and because of the inertia of the food item, results in it being punctured by the
maxillary dentition. While these findings are the results of laboratory observations of
cats feeding on prepared food items, observations of feeding and killing behavior in
wild felids report downward movements of the head, suggesting that these movements
may add force to the canine bite in prey capture. Studies of the attachment patterns of
the head depressors in sabertooths have also suggested that head depression played an
important role in their predatory behavior (Matthew, 1910; Riggs, 1934).
Influence of food size/consistency on masticatory sequences
Studies by Thexton & McGarrick (1994) and Gorniak & Gans (1980) focused
on the ways in which food of varying types and sizes influence the process of
mastication and the activity of masticatory musculature. With increasing hardness and
size of food items, masticatory sequence length increases (due to increasing number and
duration of masticatory cycles), the number of times the food changes position
increases, movements of the head and tongue are more pronounced, and gape is wider.
In addition, the jaw musculature is overall more active when harder foods are chewed,
and the magnitude of activity in the temporalis, medial pterygoid, and masseter reflects
43
:v. 'vj ffxj'll
■ 'i ' y
relative food consistency, while that in the digastric and lateral pterygoid reflects the
degree of displacement of the mandible in vertical and horizontal planes.
CRANIAL MORPHOLOGY
While much of the research described thus far focuses on specific aspects of the
felid masticatory apparatus such as dental elements, mandibular morphology, or
anatomy of the masticatory muscles, several studies have focused on the overall
structure of the skull. While some of these studies are interested in how the shape of
the skull influences masticatory morphology of various taxa and vice versa (Buckland-
Wright, 1978; Greaves, 1985, 1994), others focus on what functional differences exist
among carnivores (Radinsky, 1981a, 1981b, 1982; Werdelin, 1986), or what
differences in overall skull shape might reveal about phylogeny (Werdelin, 1983;
Salles, 1992), while some consider both of these aspects (Radinsky, 1981a). The
following discussion will briefly outline several of these approaches and their bearing
on determining the multiplicity of factors which influence masticatory and cranial
morphology.
In his work on patterns of force transmission in domestic cats, Buckland-Wright
(1978) attempted to demonstrate a correspondence between the microstructure of the
skull bones and the distribution of force generated by the masticatory musculature.
Microradiography isolated areas within the skull that had a high concentration of force-
transmitting structures and which presumably were sites of stress during mastication. In
vivo bone strain was measured on anesthetized cats, in which electrodes stimulated
activity of the masseter and temporalis musculature; this approach gave information
about the magnitude and nature (compressive or tensile) of the strain occurring at
various points on the skull, but did not reveal information about the direction of this
strain. To make up for this limitation, the skulls were coated with colophonium resin.
44
m
ipp iWrt?'] fuinmnofi L1116 ifiotTw 'al^fco^ni dfWIo mniis|pigp^b
\A
I®"' ' MIK
nil teld'rKiqvji ♦*«.» R>.u'iT>')t
io fa
‘arn «!) :''io%ii'm^^'-^ia)tj6cfe »ifi
m-
^o rti m ^4^up. mssitftrk^
>TlPF*S|{)k §4^0 9twi3ttim T
t)rifll'3»3tii^> R?iftv4&iy 8bi<?hj^ >0 'nnf^i^m ^^i^nuftni HtrAidfis
iKf .r
. fii ' •; "' -iri '^ ■
^fiHw *|^{ mbB^V/
:fMl .niJ^mV/} yo^ioii/i^ Itfcpvt* Si
" i- > . ' ' 0 K
^nati ilnrtr i^ne wii^soi^ k iftt.^V;)j ylTiiiwtf fll-w msfwu«M> ^fWoll<y|
a«
=«• V
.Irish'^
o ® f*
11^ »J«10VmTj|3 ,^aOW:
ygayiqj^
,»ip Qi|e!fmob hj noi>.«j4«?Jn5if ao ilww iirt n1
"'■
at*j 34 A mtt h09^m^» (ZVQl)
o‘ ' ""■'" '
. ■■ ' :>rfF ,rjrf>od ;|bi#
'©■ - '/ ® : ;
-^>10^ I0 rfOU5iifit»a)ip!» Hjid -6 t)frfi »jijiti ad^ytrStr^y ®diij bmti^
«\ .iwibKwW&fii ^huU i<j
b^pmu? At 2«^» b^j3i{fW37if ftji ur,^: nianw ^od wW
«j4 k Monyjifb nil! Ji/rt^n‘nf>;^rfi(^im 4fft frp ?|n;^ ciiohav
fttrt 3rtJ itjcgfs'
m
ntdsfi tK)7£oa
y..!T*'‘ • *■!** '•*^? ■ -j v-i
£ ■ “i.- >#i
U. ’
1
threads representing the temporalis and masseter muscles were affixed to the skulls, and
various loading regimes were applied. Cracks produced in the resin yielded information
about the direction of the force exerted by the masticatory musculature. The skulls were
then cleaned and strain gauges applied to various points, and the skull was reloaded,
again bilaterally at the canines, then at the carnassials. The result of these different
approaches was the identification of various helices or loops through which the forces
generated during mastication pass from the facial bones to the rest of the skull. The
magnitude of the force transmitted varies according to the locus of biting, but is
predicted by Buckland-Wright to fall along regular, helical paths in the skull, a point
later addressed by Greaves (1985, 1994).
By combining the use of stereo microradiography, strain gauges, and resin-
coated skulls, Buckland-Wright attempted to remedy the inherent limitations of earlier
studies, which relied on inferring force distribution from bone microstructure but said
little about important matters such as the magnitude of the forces present. However,
despite its use of varied and complementary approaches, the validity of Buckland-
Wright's study is limited by the fact that it does not accurately reflect the ways in
which the masticatory apparatus of felids functions during the unpredictable acts of
feeding and predation. The most obvious of these limitations is one that is common to
many experimental approaches to studies of mastication, and concerns the degree to
which the experimental setup reflects the "natural" feeding behavior of the animal
under investigation. More important, perhaps, is the fact that the loading regimes are
not consistent with what is known about the symmetry (or, more appropriately, the
asymmetry) of muscle activity and occlusal patterns in felids. Although this study did
incorporate observations on living animals, the bilaterally symmetrical activity of their
masticatory muscles was induced by electrodes, observed under anesthesia, and effected
45
teti dliijk texmi, 5Tt»y/ BalWijm tjW^^ ^)rl?
, *Sp
uOU5r»r»5Jm boWwv (ft ^h5i)q<|fi sufw |i<;(iiiti^ 2uoiiiiv
nrff Htu>s ^(fV o^umitrA'inrt. (ipjsutmtn i)fi^ »rti
■ ,„ ■ "W a,
.b?>ba)j3i ,iijw tw»r ,2imo<| fioomyo) nicvz bna bwiwia notj
jurn'itltb lUiiWi offT .^fawasoua adi la fmdj fisniffwi f>KJ ifi ylUiatatid nisss
jMT/iol ^J rteliW/ rtjguOTflf ww «mlas<yK|i}i
?i Ufd ,^aid 'lo .uioot t)ti} &:>'jat :t4j lo ibujingawi®
E’ - ' , '
)«ioq E litfjii' 3fii n{ ?iticq IWibfl .iJsJjig!^ ol jrHsihW-^fifWaoa yd baoibaiTj
(27
) gs^/iD yd tiamTtibs iml
ati^ bff5 n'ffiij? lo at»»i sfffj goiaidmcp yS
■:W:
Sf*
f jiitw ^ 4B3i»rt«i s>fli ybarnii bv idgiW^bn^jiyoB bmmj
iB '
biae jud'aitoturiiWTafm.anod m6T> rfofjud^jgf^ gntvia^M rio bsf tar rbW^r
,iav&waH aoae^l!^ panoV-Sfl/lo as iliJMfj mi'ioqtni lyods aidif"
ffi eyjtw adf Joafisi yb)ii'ii/bnTf ion i^b yd Mndl « ybw* «■ JiiJhW
■ lo «iid« jitiirtbibs^Mir all) gbItMb atfirnsQ!!^ ittjie^zjun adj ft&dw
-^1-. . , rs ' :-'' '■
oiaaouHuo 2i ifiUj fuxo/i ^moaunn^fi mii^Q i^;tm .:fim
M
# fdli^Jnv)« bni^ ,tf
, oj !!afe»i<w tpit9^ri»qxsi(a*ii^^^
4! . ' »■ ® ■¥
2 Isminfi 5rf! ^ " ><11 ?ja^rbf ^riw
3H8 ^ntbsol afU fCwiiV bib smjM noimiijjavni labno .
' - , ■ (3“.' ■ jw.' 'M,., ■ '
V ■" '. 7'®"%"”/ '7 r . ■ " '■
lia/b i0iv?jW5 toTf'Wfmyj /l|tfi»fiti^5fii, dO 2«^4fc^itS^,o»iCKpoo«f
IwiisTts o/!it ,«ifi5dif»wc labdii b3viaj«j[^> afiv? a^icMa/m yioiijotlcBm
a bilateral bite force. While a bilaterally symmetrical canine bite may sometimes occur
during felid predation, asymmetrical, unpredictable loading of the canines occurs as a
result of tooth-bone contact during the killing bite and is a more likely scenario for the
loading patterns of the anterior dentition. Similarly, loading of the carnassials is not
bilaterally symmetrical, as they are engaged unilaterally through asymmetry in the
activity of the masticatory muscles. Unilateral rather than bilateral loading of the teeth
would be likely to alter the nature and direction of force transmission in the face and
cranium predicted by Buckland-Wright's model.
While the masseter and temporalis muscles comprise the bulk of the masticatory
muscles, their activity is coincident with that of the less powerful, but nonetheless very
important zygomaticomandibulares and medial and lateral pterygoids, all of which were
ignored in Buckland-Wright's study. These muscles are oriented differently from the
temporalis and masseter, and therefore would likely alter the observed patterns of force
distribution were they to be included, and may act in certain cases to counteract the
forces exerted by the temporalis and masseter, and thus affect the measured bone
strain. A better approximation of the true patterns of force distribution might be
accomplished by measuring strain in freely feeding, rather than anesthetized subjects,
which would allow a closer approximation of their "true" feeding behavior by
incorporating unilateral occlusion and bilaterally asymmetric and synergistic activity of
the entire muscle assemblage. The data gleaned from the experiments on resin-coated
skulls are similarly limited in the degree to which they accurately reflect masticatory
function in felids, as they represent bilaterally applied forces from only two (temporalis
and masseter) of the jaw adductors.
Studies modeling the skull as a cylinder (Greaves, 1985) or a half-cylinder
(Covey & Greaves, 1994) focus on the relationship of skull form to the torsional forces
46
,v •• . w
w *3o sjirt imf/uo lAK;ffT}3f»i;m<? «#frW i
■ >*■*
ft4» >ri biIeT®§»ih«Jb
■•)ji(j'''i^f' , B ■ ■ , ' sS*'',
94s W* OMkT r. '
^ , • ' ■ ' ''* '."^' ■■ Wi
mvslf^ afiirvs ->(i» .YNlJrmi
±*-f
a;
!*I ■ ..
m
^Iwf nfii ai^it^ifmo ^Ibm^^^i^uqrnpy .i«t» jJiffW
.‘i. ■■•'.» ' V®"'
sfpkMiiocn iu4
m _
;yii itmi imiA^ m tmoiifif
■?s
fff
Sim xikrotfOM
s
■iW' .
noi^udiir^'tti s&Y
4it#
’''T:bm;o';
jiSj
JH 7d ■1i<>jyit'd:id^4ri
m
ni <(ff
'hiW " '& •'^f ii fetiSb, <y^
> V ," i'
■ ■*' ' ' ' '"'i^: '■•f ■■ ■ '
•. ra,^ 'm-andl
'■ ' -.Jfii^ ■ f!
■tl?
'^«lli‘y.>j1|ij1 It
assumed to be generated by the masticatory musculature during unilateral occlusion. In
the first study, Greaves developed a theoretical model to account for the presence or
absence of a postorbital bar in various mammals. He hypothesized that in animals with
a large masseter/pterygoid complex, such as selenodont artiodactyls, a postorbital bar
acts as a strut to resist the high torsional forces generated along the outer surface of the
skull; this structure is presumed to be absent in carnivores because of the different
orientation of the temporalis, which exerts lower torsional forces in these animals.
Figure 11. Drawing of a cylinder superimposed on the skull of a selenodont artiodactyl
to show die direction of rotation (arrows) of die anterior and posterior ends of the skull
as a result of unilateral mastication, and die torsional strains produced on the cylinder
surface as a result of twisting about the long axis of the skull. (From Greaves. 1985)
Greaves hypothesizes that during unilateral chewing in selenodont artiodactyls, the
masticatory musculature pulls ventrally on both sides of the skull, while the mandible
of the working side pushes the skull dorsally at the bite point. The reaction force at the
balancing side condyle also pushes dorsally on the skull but does so at a more posterior
position. This loading regime results in the anterior and posterior parts of the skull
being rotated in opposite direction at the weak orbital region (Figure 1 1). This in turn
47
nl iiuiWtlTO
K' !Hu(»D'^ tn l8l>?>m B b«<^l»y5»b' .-4v*»>p ,t(J^
ifcrtw H)ii!rni/!« ftj jwji <ii 'awi a ^o sooj
&m r m
'H^leraDiAiu? K)JW) rrtlr.gfioit baiinsnrfg.^^^ r{|{t4 trti mm ro «: as sOd^
i&'
;^iJ,
ip o? td n^atiomst
J»a ■ “ ■ ' ffe." Jg , -^
sr^f' JI^ W^;- . '''
■fil. r, T . ". . — ,' . ; -. ^•‘.-
■ fA-' ■'. S:® - y';
■■'r>
' ^-fr- ,
j:}>jirt»i^v nlfMiWwwnQ .|l yjaj^ ; i
)(U»I_« 'if»« nr?>|»|g tl>4^M|S»^W m.$HtHT> Ift ^ ■ ,
'■ ■• ■ ■’ ■• • TJO; . •* .'X,
M
'4:
'^^)>^l <> <)ja 'u4 Sib :Mis^«*'tefi>.iti vkj«jin:i u ^ "
^ at- ._. __ ,(Ti : ...
9^1 ill'crDftboiJu* ni U«r &9vs6^
4li<j(iJi||pfti flfrij !»tf)rjv/ SlUJia drfi )o fitoci 0» ' ^
' R?* ! •‘.‘iw
^/b4s>da^:ii<»te .!;ii
■■•ip?'' ^
wjoiioq swcH' a iSiOz'^h
■- - - ^ '■ ^ - ■ ■“ ' :r.n ... ■*■ ,„,,■ * <1
SE , *1 >5
..iir.. kf
•t Mitfl
ii' EF
nittt M i yiu^ei^^ l/TftdiO m&flfffsot aui^
*■' F: “ ' ' ■‘'j %’. ' ,«» ,m
results in torsion of the skull, with maximal tensile and compressive forces occurring
along helices positioned at an angle of 45° to the long axis of the skull, and at an angle
of 90° to each other along the surface of the skull. Greaves assumes that the tensile
forces along these helices represent the weakest areas of the skull when it is loaded in
torsion, and that buttressing of the skull against torsion should occur along the length of
these helices. Greaves (1985) points out that the postorbital bar of selenodont
artiodactyls occurs at this position, and attributes this to its role in resisting skull
torsion occurring during unilateral chewing.
Greaves' model is problematic for the assumptions it makes regarding both the
magnitude of the forces that produce twisting of the skull and the behavior of the skull
during this twisting. In addition to these problematic assumptions, recent strain gauge
data (Hylander, 1991) refutes some of the predictions of Greaves' model.
Greaves' model assumes for the sake of simplicity that the asymmetric skull
loading during mastication in selenodont artiodactyls consists of three main types:
ventral forces applied to either side of the skull by the masseter/pterygoid muscles, a
dorsal force produced by the mandible at the bite point, and a ventral force at the
balancing side condyle. Although Greaves acknowledges that balancing and working
side muscle force is not always equal, he asserts that regardless of their asymmetry,
they both apply "significant ventral forces to the skull". While he discounts this
asymmetry in the activity of the masticatory muscles, he then emphasizes the degree of
asymmetry of the condylar reaction forces to the point of disregarding the smaller
reaction force at the working side condyle in favor of the greater balancing side
condyle reaction forces.
Greaves' modeling of a complex biological structure such as the skull as a
cylinder is problematic for a number of reasons. While he uses an example of a stick of
48
^^iaTr0^:^ ^3^x ali?iid| tismfiUsna iJi^v v.ik4? siH 1t>'jff»?fic(j ajoaas
® ffl
aiaffn rie ik Ikjb i\iUi lo UM w ‘ «i|,'jsfi
fw .'I II jjfttiw r)'HV> m'am
W (b^atJ 5«i{ 'iiioui -»u3BO Mwtifte (*' »ir.oj tesat jfjofinw
tfit riK>ri ji ^,CKiq|^«a <4fi? loi 'lavusiO
'• g lloie^ffjlo tfimHnd aiiih^ arft^o abjmnjwi
-isfcWfrt ■‘faVisS^^^ /ilitb
" '■ -' ‘ . 1^' . ' " ' ' ^
U«3li JBifi itfij nvJ l^y^»«B .te4i«5nj i^svtmO ®
!P
..
!w{| ilisfltt^ lBi2iiiSv JJikiq Ijfcnoti
' , ,f.. - fW^
:»l>is 8^i0aBt£d
' ■ • V.-^ '■■■ ' . '" , - ■ ■ ''^'^r' 'W
■■ ..■" .-'Wltfe " ' , • ■ ••^ ■'
2>rft* m ^S3^# nofS^m aiJj >f»
chalk breaking along a helix oriented at 45° to its long axis as an approximation of the
behavior of the skull when loaded in torsion, it is immediately apparent that neither the
material nor the structural properties of the skull are analogous to those of a stick of
chalk. Bone can rarely, if ever, be modeled as a homogenous material, as it varies in
its structure and therefore in its strength, depending on the location within the skull and
on the nature and direction of the load applied. Secondly, even if bone could be
assumed to be homogenous, the structure of the skull itself precludes one from
assuming that it will act as a cylinder of homogenous material. Reasons for this include
the tapering of the skull from posterior to anterior as well as the presence of vacant
spaces such as the orbits, sinuses, and cranial cavity, all of which alter the patterns of
force transmission in the idealized cylindrical model.
In addition to the theoretical difficulties imposed by the complexity of the skull,
and therefore the limited applicability of a cylindrical model for the behavior of the
skull during mastication, recent experimental evidence refutes Greaves’ predictions
about the types of forces generated in the skull during mastication. In addition to the
role of the postorbital bar in resisting torsional forces during mastication, Greaves
asserts that the supraorbital ridges found in primates also play a significant role in
resisting torsion of the skull. The postorbital bar of the working side is predicted to
resist compressive forces, while the supraorbital ridge of the same side, lying at an
angle of approximately 90° to the postorbital bar, is predicted to resist tensile forces.
Recent measurements of in vivo bone strain of the working-side primate supraorbital
region indicate that tensile forces do not in fact occur in this region. Instead, this region
experiences bending in the frontal plane, and the strain produced in this area is in fact
low compared to other regions of the face due to increased buttressing of this area
(Hylander, 1991).
49
nsi afmJ ?ni o) m i>*fr^ lttari & ><^d
nfti tsilitsfi /jaJwt^mrtii H n of 4a?fw%wJU artt lo -lojvwtod
^’" -■ 0 ™
^ “* ' ^
ni ik>jwv j| tu Jaiiwujn c dc ?<
r .'i
brtR 5iti niit'iw nojJji .>f)f ^rij. *jo gftibjiSQab .ffigitsii? ail m fojti aiuiatni* 01
®s'"'
ad haM s^iam adi bo
riM
abilofii 4id> Tt^VefKMBd^l J0imm Mw H mthrptimoiiM
' ' , ' l» »pr‘
m/iiAfiv 10 a/il 2E Ifftw as TOhaj^a 03 i«iijoto<5 ttroil Hiii* 4jdi ^0 gfiiiaqitJ adi
to tiTiaiiijq^t tajls ifoi^iw jwif ai doot asoftqa
,iknl4j adi )oxJi*(|»|q0iftt
ffl ' ;'
a«L‘lo i<jivari3(i adJ tol |^fli toiballv5^t1o '(rtlidao!iio^^ adi BTOlatadJ bat
aflou’^oi/iq '»3vM0 iswu^o^t grth^^iii Ikii
."i'
,^2:v
<iiyii330 .fiptefkfirn y«hub‘ earned' ldnoU><»
ni c: 'ieiq eai^iftfl'iqni w*i«# g!»^t9n Ij5i3f<<icanqi/g adi iwij gnatSi
'V' . ■ '<aJ ‘ iM
. -,- .,.jj H ' 1^ ■-'. V ■ '^S3i^
nt P, 'i(\fS!t ,§«n ra'
ty j»3)“i&wq 3^ o) I0 oi^
*i3 ’ *
■%■ .. i:f . .. . , ' #
•!!P
i«*^T T#t* nuBoibrtriWMiai
«»IB iil'b Wl>mq, ^la -iat^^j iSfa
. •■,■ ,> ' ■ jfe' . - B
S3I6 ifdi Hj ^dtaaiitifd baf<af^i'a/irurjif'5)>i> 331^ 01 baifiqrnoo woJfi
Despite these problems, the cylindrical model is used by Covey & Greaves
(1994) to explore the behavior of the carnivore skull under torsion. Unlike artiodactyls,
which presumably experience great torsional forces as a result of unilateral biting along
the cheek teeth (Greaves, 1985), the authors assert that carnivores experience high
torsional forces generated during unilateral canine, rather than carnassial, biting.
With this in mind, the authors hypothesize that, as in ungulates, asymmetrical
loading of the jaw during canine biting should result in tensile and compressive forces
that are along helices oriented at 45° angles to the long axis of the skull, and that
emanate from the two structures encountering the most resistance during unilateral
canine biting: the working side canine and the balancing side condyle (Figure 12).
Additionally, the length to width ratio of the skull determines its strength in resisting
these forces, since variation in skull length and width presumably result in different
positioning of these helices relative to one another and to the ends of the skull. In short,
the authors state that for skulls of the same width, longer skulls will experience greater
torsion than will shorter skulls.
Because of the relations between skull length and width and the relative
positions of the canine and TMJ, the helices in the dog-like skull (Figure 12a) are
equivalent and lie along a line connecting the anterior and posterior aspects of the skull,
any additional skull strength would be accomplished by buttressing in the area along
this helical path. In contrast, the helices in a more elongate skull (Figure 12b) are
separated and do not extend to both anterior and posterior aspects of the skull. In this
situation, torsional strains will occur along each helix and the space between them must
be bridged with bone, a "metabolically expensive" building material (Covey &
Greaves, 1994), in order to form a single helix which connects the anterior and
posterior ends of the skull, and which
50
.M - ,'|I r l ibtjit* )j .(TtwirlvjJ 'Hh
1'ii , \ii}^ ihy^mt -'li
it-,. .-. f,
w. mBm
•■ /■-■ .K- 4-vr,>f,u,4. isMf jw©.?Srf(Ss^ rtmi
f'.;
.r’tU (III S[B .‘i'lf i^btilf ft Hi
’V ■ ^^Bfias!
ic.li hni^. ?jiw( '
'i, ■,/•■' 'V, '' ' '
W4iijfcl#iifj <4 ^ «U jmT^vVtuasflJa
v-vtsSaiJ^oi m^atmt *!j
«* <•'»«»< ftitemiueiy) jti^w-^l^^si tJtiHt 4 a^ ’
&
io
IT
^ V ..».W ■■ . , «•
"'T' ov43mS^4'(U i»'Ki ■ . ' ii''" r' '
E
* ;w 's'- 1 9^in;4M4* 55*(Kh<* «li,>tWT ieti^mxa 'Sii*?© uieSJliaq^
-hh'i e m bm:. ' , ':
■i.' .
s»«nil||^
A^iaum .(u'Htii' w
B ^ ^
■wl^^lfKi: ,i^. '(' <id4':.,t>n%lMBifiWjfste
'?ja £^.' w-
1
■.^.r, ilL' „ «'t ■' 1 , i. ,/is. '“ Li ' ,! ■■ ^
i
.'# ■ .kisWrfad
■3r
' “M ■'*•
m . *?■<■
IW/v
ix 'flW
H,1J
Rgiire 12. Tliree skulls with different length to width ratios, which influence the
placement of die helices emanating from die jaw joint (solid line) and from die working
canine (dotted line), (from Greaves, 1994)
resists failure under tension along this helix. In the cat-like skull (Figure 12c), two
helices extending from the anterior to the posterior end of the skull are presumed to
impart these skulls with added strength in resisting torsion, without needing extra bone
to do so.
The authors describe skulls of this type (found in felids and some mustelids) as
"overbuilt", for they are shorter than they need to be to effectively resist torsion.
Additionally, they assert that such an overbuilt skull is important for animals in which
large forces are exerted during unilateral canine biting, and/or in which the canine teeth
51
jm
Ijglll^"'™ •wtauH^ri «!»:*( a(nCP,Il^w*rf
%aUvi\i>t HU nff'wt ^ls'■■f^Hi^ii,;,■4.■l|l{^6i^^ ariilo linimaatq,
tf>kTrt) ..ftmiJ
owl ,(!3i£ ! arafgif!) lltioig f^o DifSft
"S^ ....-i5..i .fc-;. _■: '■• •• ...r,.-: .^L. mr'^ mm
* ''/--> ■' 'i '<■.
^2i.4slT >*irVl4^n4?if5? hAUiife 41^*4/
02 oi^Oi 9
n
. -^ ' ' %* ' ' '-1^ '■
rtolft'*^ n< ak..'kfTsr idJ »f:ivnoqmh*i ti?)iilJliu(*l9Vo rifi ihm ysuii .YtlflnoJjtlibA
ufJt 4i>iifw ni w\bn4:ism)ld o^x tt^diol 9|^
M l\ ■
are subjected to large unilateral loading, as is the case in felids. By extension, the
"underbuilt" skulls, with a high length to width ratio (Figure 12b), are less equipped to
resist torsion; in order to do so, they require buttressing along helical paths on the
skull. In apparent justification of this model, the authors state that carnivorans with a
high length to width ratio "are not expected and are not found".
Unfortunately, the extension of Greaves' original model to carnivores is not
without its own set of problems. It suffers from the same limitations regarding the
legitimacy of the analogy between a complex structure such as the skull and a cylinder
of homogeneous material. More importantly, perhaps is the fact that torsion in a
cylinder is independent of that cylinder's length. Therefore, each of the skulls in Figure
12 should experience the same degree of torsion despite differences in length.
Additionally, the helices superimposed on the skulls in Figure 12 are not oriented at 45
degrees to the long axis of the skull, but are actually closer to 25 or 30 degrees; this
invalidates the assumption that helices oriented at 45 degrees to the long axis of the
skull will connect the canine and the balancing side condyle, which are presumably
experiencing the most resistance. In light of the various problems mentioned above for
both of these models, Greaves' acknowledgment that torsional forces are not the only
important influence on carnivoran skull shape seems particularly fitting, and leads one
to look at other factors, many of them discussed above, and others discussed below,
which may be more important in determining cranial and masticatory morphology.
In a series of papers, Radinsky (1980, 1981a, 1981b, 1982, 1984) measured
variables pertaining to aspects of jaw geometry, overall skull shape (length, width,
height), relative brain size, relative development of sensory organs, and size and
strength of the masticatory muscles and linked his findings to aspects of the killing
behavior of some carnivorans. He inferred that among carnivorans, felids have a high
52
I ^ B”
yfi .rwIm Ri <u« *« b5J:;dii<iir«
o) 6«Kjqi.u|iU luial i'
“ '□ " ■■
^rit no. ^dh-;q |,®'j(bd,^noU4«i;i*2^tirw'd' Jiijiurm :fWitMiQ3
E mMTti'/inm iJirtt inotiJur^ im lUiif ®
^ ' ' " tii„„ '
' bzuid! rCv‘. »no s\£r^ 't^ii#. ' rf jiiH
ft»^ ^i g»T0vi»Tjf'O‘.-o* l5iyiiTf j,wlf.|jPWx '
•J vs 'If ''*® '-'■ .
; sjijj ««Rte. il' to m liwo tti juoi^tw
■ ' . ''.r: V ' . ■ E'-
' m ite : ^ fineewa^brtj Tobwii^
' “ tt. fi
■di''»E'b5frv»i«*> stti ^ .liCtlsrtbirtbbA
"f^- 'J;' ~
Biffi ‘T%ii^b;Wt'iO '2l£:.of t'llola; iim isooi «Jj oi ^
, M' ' ^ " f"
%fii "lo lU^ gnol^jriJ -aaotuiib Jit iis ba)iT6lib«)aits«i iciir ^la(ti^l6Vrti
'± ' ' ' ' ' 1^1 ' ' _ fli
^■^V'Of^r. .to i>I ' 'a.^oiairf'kW' w,n wli,
’ VJ<0',9^4 io^t-l3A'Vl#Knwt' l/in6k«i(«:}i3Sj*>(iiiTiab't>f'//3tto' ,<d<i<;^''»8»ffilO'tl^
';jA. ... '. Sx'f ■ ■ "
■'„ "V
laS^sP'-
Ji IT' - ■■'■_^ ,
fr - *s
-toLi ,'’.ii,v^ -3
boi: ^fenfi^w yno«||3f-- W ,,{itjsit$4;
■0
Q
■■B<
SI 'fl
liii ft' W4<^-'4fiiaJ bail ji^^ . ail,
■ ' ' '■ 4 ' a, " ^ '" ..an^, .. '■■'m.;':.^''
bite force (indicated by a large temporalis moment arm), and powerful neck
musculature (indicated by high occipital width), presumably as a reflection of their
killing behavior.
Werdelin (1986) used a subset of Radinsky's original variables to assess the
primary functional differences between placental carnivorans and the dasyurid
marsupials. In possessing canid-like, viverrid-like, and hyaenid-like forms, the
ecological diversity of the marsupial family Dasyuridae is, in many respects
comparable to that of the Carnivora. However, Werdelin found dasyurid cranial
morphology to be no more variable than that of a single family within the Carnivora,
an observation that he attributed to the posterior placement of the marsupial carnassials
within the tooth row. Werdelin argues that in contrast to carnivorans, this posterior
placement reduces the evolutionary plasticity of the dasyurid dentition. This is in
contrast to carnivorans, in which postcarnassial teeth are present and modified in many
families to yield markedly different adaptations (Butler, 1946). Therefore, based on
Werdelin's findings, the phylogenetic history of dasyurids and the constraints it
imposes on their masticatory morphology seems to have a much stronger influence on
the morphology of the skull and the masticatory apparatus than do aspects of their diet
and ecology. This argument is weakened, however, when it is noted that the species
included in Werdelin's study represent only those dasyurids that have a diet composed
primarily of vertebrates. By excluding those species that include a large portion of non-
vertebrate food items in their diet, Werdelin has in fact excluded the majority of the
species within this family of marsupials. Perhaps if the rest of these species were to be
included in his analysis, the diversity in dasyurid cranial and dental morphology would
approach that of the Carnivora.
53
MinwoCi bHH M fc«,T»a»!jbi3i) aonj^'^'S
Iff* flofofer H .*.B Wtl$mt#rt5iq .(ihbiw
-
biKjyisb 3rl> 1>«je i!rt^ilCivjinio
aif] o) >»aiHatHv kmMfVi
Si!
mis '. bftst
ffiinfi'fij^bfTuyedb baiiDi .;R3<y‘//infir> !i#b tft fmixof
,£iovifiifi:>;.pfb <»iitJfw Yfil!i<ii 9(3^ 01^ ad ot X30briqicwi!i.«
^ ^ m
odi>o v*3ri(n>*d> wo^im^iKb ne
'*' . ' "' ^ , Ik ^ '"' iSl-
esfi) ft
p , ,
iSI- ■ ... 'Ki
fif'zi ftirlt inoiuin^fb b<^uy^cb.>.^T,|o $dj «Kubat4n
^ ^ R! .; ; l>»!
yfi*rn nrMibom bne ?noeaic( sifi Im^c^ijiiiRaow^ rf'Jii*^f fii ,m£iovim^ ^ m
.aie^aldfiT
no
IKl.-
no^fti>ii^{ni •jv^al r*) n^«:dSoc|m»
toih >0 i*j’ab<|g|&'V‘j|> ftfiiii
'^7: " ^‘' ‘
<ttj« >0 u 5i)iirfj<ir lekif
5ft^^ryiiir?i|M^5fU'S:)i)iiIn55a'4i^ nia# .%,fi<Mfai^ i?c^’ 53i^&»v
b yihiwnli^
- I'’’ ,T.*' TI*^ .*8 '
-.isjvQfW y90:oWcn©('fi'
^ . nriovii^D <5fd .'lo ^ jJtft: rtojsoji
While many studies are focused primarily on determining functionally important
aspects of cranial morphology in carnivorans, they may also have some implications for
systematics. Based on his initial results from canids, felids, mustelids, and viverrids,
Radinsky (1981a) suggested that certain features of skull morphology might afford a
means (in addition to using middle ear and basicranial anatomy) by which family-level
diagnoses among carnivorans could be made. Subsequent analyses revealed a great deal
of overlap in the skull morphology of these carnivorans with additional taxa (hyaenids,
procyonids, and ursids), which precludes their use in family-level diagnoses, but which
may not preclude their use in making distinctions within carnivoran families (Radinsky,
1982).
Another approach that concentrated on the potential systematic implications of
cranial morphology is a study by Werdelin (1983), in which dental characters were
used along with a small set of cranial characters to make systematic distinctions among
felids. He found that species of the genus Lynx, while only weakly linked as a group on
the basis of dental characters, are strongly linked on the basis of cranial characters such
as postorbital constriction and postorbital width. His results show a fairly clear division
between large and small cats, although two species intermediate to these two groups
reveal interesting aspects of the constraints of size on cranial morphology.
The first species, the clouded leopard (Neofelis nebuLosa), is intermediate in size
between large and small cats, and is most notable for its large canines, which, relative
to skull size, mirror the proportions of some sabertooths. Neofelis seems to have cranial
proportions similar to those of the large cats (pantherines), without having reached
pantherine cranial size. Fells concolor, on the other hand, has cranial proportions more
typical of small cats (such as Lynx), but in overall size is more similar to the large cats.
These results show that there are in fact quite distinct differences in skull morphology
54
"oxm^
aaj Mf 11
i»/i r <.ai-i)»Ut»»f^’*}if}'»'i( -jvtH 0114 '^«M/ 'ad' ,ff>fe^ovumj
Mil; fbihH j^jfTjw f<4i.j|l ,iSp4>i|o«,oiif'<4
, . viS) ® 4g
, r"J^1iir^^J<'\ >R j^tiaseSi*
4kX4> lAu/ J
fiM&j/ ji ri liffi ,tbi:rta!cocwc
$iQirM)‘Vi(it} i^i}a
& ih
Ilu
yd' tbm> I *rt '
^ ■ ^^ ^ M / ■ “ ^ -‘i
nf»qiitij,b#»|fiiii;i::|p a rf|j^!gn<34«;b*i^
'te . , , '<^' , . ^
ffcwi ^ Umrta'W'
^ tq/mu 'ksiiii .')ai«t ^
:a y 'Si V . *■ '' iP:' '^L _ '■ 7^1 , ^
- .-fc' 'jQ. , m' M ijji^ . .. ® . 34 iSite'.
t . .. ,
rji
iff
at.,, ■'
IS'
f^'. .a.. ,%. . ' ,. ■#fe-:>
h(^ jKv^ ; i« Sift*
-'M r
IJj^ ' ' ' ' *J' •■■' ^
:in<iMhhu iflit
in at least a few felid species, and that these differences may be largely the result of
size change within lineages.
Another area examined in Radinsky's (1981a) research on the differences in
carnivoran skulls is that of relative orbit size, which is highest in felids, suggesting a
larger eyeball size and greater visual abilities. In addition to the implications that sheer
size has for visual abilities, orbital convergence (the degree to which the orbits are
directed forward) and frontation (the degree to which the orbits are directed toward the
end of the snout) are also important considerations for a visually-directed predator.
Other than primates, felids have the highest degree of convergence coupled with
relatively high frontation and rostral regression (Cartmill, 1970). These features are
presumed to be the result of shifting the duties of prey detection and capture away from
the snout to the eyes and forelimbs, respectively. The result is a rostrum which in felids
is "reduced to a visually-guided killing instrument" (Cartmill, 1970 p. 374).
CONCLUSIONS AND AREAS FOR FUTURE RESEARCH
As the preceding overview indicates, felid masticatory morphology has been the
subject of many studies, some of which have managed to outline clear links between
the demands of a predatory lifestyle and the form and function of the masticatory
apparatus. Despite the depth of inquiry and the extent of the data that has been gleaned
from such studies, however, much work remains to be done. Potential areas for future
research fall into two general categories: refining what is already known about felid
mastication and expanding this field of inquiry to other carnivorous mammals.
As stated above, a common criticism of studies of mastication concerns the
degree to which data gathered reflect the true masticatory activities of freely feeding
animals. This criticism is particularly valid for felids, given the very different demands
55
>») vftffi i«flt t^is ,my9(i» wai! i i A i#ni
■i4>
iji ia^n'jialllb inti ng rbifi9?3i b;»*lil«*yr> ifessw n»tlooA ..^
B nf ii liairfw ,3^8 fit4la ninovfimj>
30
IIL^ ^ m#IS9^
if'iij widio 3rf4 o> 3ijtira5«^(tym>a]iOHho Ifii^v tdl aed jwil |
rbH)‘^g*'^i|9tb’Srfo fttij|aim>7> bn* (Irtiwyiol
• • .
51C a3lwl6afrg^;>(|7 XhvbSly^
_ .■■■' 'i^'- Q *' -,
rnoT^-rYBWB b#f&;n(^o0b'b '?4J od.i»; b^^
iib^'
abital f» rb«1#’mttTllt>j''«' <s«
a : .«:'? . ■ :?>5f " *' '.iji
jsi'')tj<^c,M
:q (J\0I a oi twSitejT'* il
~ . ri
^nm^k^WtA
:M _ s:. . "" 'fli
\iii»m^ ff3*«il “j^lo MJfilWi mtm '.rnkm
.p .j. 'f^'"V’', fe
i ri?qSb i:2W«Sqq«' '
'"‘"■-•<l:'.','^'‘
j^:;i
>5wiu> Kil -sBq.b 9d m ?JfvBj^3T jlKf^ *bMt| .\x;>^^r4 riaue mo^
?is^
m
u3/b;80i3a/<![52> e ^'<yod&>5WB«^ #A
b. jfbt'jWb'vV’i^v of4/'f73Y/^,;4bl:W^pfiyv;^ ;ie;t.
placed on their masticatory apparatus depending on whether they are engaged in
feeding or predatory behavior. Most of the work done thus far has emphasized the first
of these two behaviors by focusing on the muscular activity necessary to bring the
carnassials into occlusion and break up food items of varying size, shape, and
consistency. While carnassial function is certainly important in breaking food up into
pieces small enough to be swallowed, I believe that for felids the importance of
carnassial function is secondary to that of the canines, in that the use of the canines
precedes that of the carnassials, and proper canine function is therefore a necessary
precursor to carnassial use. In this respect, I believe it is important that future studies
of felid mastication also concentrate on the canines and the activity patterns of the
masticatory muscles when these teeth are engaged during predation. Doing so would
allow a comparison of the patterns of muscular activity during these two types of jaw
adduction that presumably place very different demands on the masticatory system.
In addition to gathering further data on the masticatory apparatus of felids,
investigation of other mammals that have been said to converge on felids in cranial and
masticatory morphology, diet, and behavior will shed light on the degree to which this
perceived convergence is valid. The most notable candidates for such a study include
the Malagasy "fossa", Cryptoprocta ferox (Carnivora, Viverridae), and mustelids of the
subfamily Mustelinae. Both the fossa and the mustelines converge on felids in their
reduced dental formula, well-developed carnassials, loss of postcarnassial elements,
shortened rostrum, convergent orbits, and predatory behavior. Using the data that is
presently known for felids, a comprehensive study of the predatory behavior,
masticatory morphology and masticatory function of these convergent carnivorans
would identify those aspects of their morphology which are dictated by the demands of
a predatory lifestyle.
56
?2-)i1 srfi ‘iHH vrioN -him diOtq iscHM vV)3«fsytq 10
mU /H‘4rjii i^'MoayffT arffntiswjw^ vci «ioivArtftrf«!(WJ
B , I
M' jS" ,11. -jj,
(vn&wti a ^4•«^^,*n<^^ »i nti»jwiai' to ^<siiiwirt ut> ^jfxtHS'K}:
nitwi* 0h mmi0fu^i /i n T
m ■-® ,: 'a ' Si"' ,
fifnow at finiDiJ <04^ mfi) rjii^u/ii yitoJtQMiflM
w^t )o 4ii> % $im^mm # ■
bn4 ifiiitinD jij r4iH ifilj trxfe^ to ndjl^ka^
'^ ';- V'ii *■: te
tnH jkithr
■vvu,
iAii> .x;gs>f<yttq;Kfftf xWia^M
*F ■ ■'■ "' ' ^^- . ■^paro -^" 7^. ^ :
,v,‘ ' _ ' ■ ■ ®, -ia a ^
jid) VftiifjwwwTt bifjti {-^iihh^o^iV Ya8;gsl«M ^
5rti to .jUf^frt |ii»j^ jrnmix/i b9nal'lort^
.■ '■
. -wi </ Krittfi y ^k^lt y^'-n'kottit. vljnijitnq
i# iilioliTz*9ti e»tO yd jp^iiaswy jyi y^iaio/jtjjojry '^iM) *fe v't^nobt Wwiw
I «^virwil<r yioifibsT^ »
Through further study of felid behavior as well as masticatory morphology and
function, much can be learned about the demands of a lifestyle which is characterized
by a strict diet of vertebrate flesh, solitary hunting, and predation on (often) relatively
large prey. Additionally, by studying other animals that converge on this way of life,
we can not only better understand how and in what instances this lifestyle dictates
cranial and masticatory morphology, but we can also begin to address how other
important, non-masticatory features of animals also dictate their cranial and masticatory
morphology.
57
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Glv
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srfr«^ dfi brrc pui<fEJCKfx|f^m ni 9j^j^ inl
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AJ< k«i« wbo>^ a .zbd) .nr gMWiSiir> nr saiiWiq iuil bfta
aifmibs^iA :j}ot^tiaLl vrff?y>i to ’itout»0/j3r,bh£ noi^wfiA > ;v.!»'£ol
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vv
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^li ni gnib^sj \o fens X sSni^Si
Umad :g»wftifUO aX fisdtmA ^ ^
.0 ,^1^ /Soloifitjom p
a ji ' « a ' ■■ , iK'
inJ ,SHM3lla^^ b<^T acinallH®*
UsftCiii&fti^ M$^ M<!f i juMsf ^
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^Wftmavrjm 9dt <iS^>()/#A l M fiw*94T>X^as^
m.
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'ti rf-..: 'a1? ,„•
.:f^A
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' ,<?oiri>ftA ,l .mA fbi^Sn^rn ^l^Sl
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rti ■aJiti vio4^ziEJm
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s
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a
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• ioya inTfO •
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ra
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:jSji
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^ M lasjujT to' H 'iitaiiitej
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■%. , "S' ii ' M'' ^ ^ 3» ' *
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mifmnm ) t toztrio^l' to *11
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i:gLf1)i-^4!t rtf «ra©«^vTO‘'Oimi*Jtd#.
4*' ffl[;;, _ j®J. ■ 'i'*!
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