Implications of the mastoid anatomy of larger extant felids for the evolution and predatory...

Zoological Journal of the Linnean Society, 2004, 140, 207–221. With 7 figures

© 2004 The Linnean Society of London, Zoological Journal of the Linnean Society, 2004, 140, 207–221 207

Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin-nean Society of London, 2004? 2004140?207221Original Article

M. ANTÓN ET AL. MASTOID ANATOMY IN FELIDS

*Corresponding author. E-mail: [email protected]

Implications of the mastoid anatomy of larger extant felids for the evolution and predatory behaviour of sabretoothed cats (Mammalia, Carnivora, Felidae)

MAURICIO ANTÓN1*, MANUEL J. SALESA1, JUAN FRANCISCO PASTOR2,ISRAEL M. SÁNCHEZ1, SUSANA FRAILE1 and JORGE MORALES1

1Departamento de Palaeobiología, Museo Nacional de Ciencias Naturales. C. José Gutiérrez Abascal, 2. 28006 Madrid, Spain2Museo Anatómico, departamento de Anatomía Humana, Universidad de Valladolid, C. Ramón y Cajal 7, 47005 Valladolid, Spain

Received November 2002; accepted for publication July 2003

Muscle attachments in the mastoid region of the skull of extant felids are studied through dissection of two adulttigers Panthera tigris (Linnaeus, 1758) Pocock, 1930, a lion Panthera leo (Linnaeus, 1758) Pocock, 1930 and a pumaPuma concolor (Linnaeus, 1771) Jardine, 1834, providing for the first time an adequate reference for the study of theevolution of that region in sabretoothed felids. Our study supports the inference by W. Akersten that the main mus-cles inserting in the mastoid process in sabretooths were those originating in the atlas, rather than those from theposterior neck, sternum and forelimb. Those inferences were based on the anatomy of the giant panda, Ailuropodamelanoleuca (David, 1869) Milne-Edwards, 1870, raising uncertainties about homology, which were founded, asrevealed by our results. The mastoid muscle insertions in extant felids differ in important details from thosedescribed for Ailuropoda, but agree with those described for domestic cats, hyenas and dogs. The large, antero-ventrally projected mastoid process of pantherines allows a moderate implication of the m. obliquus capitis anteriorin head-flexion. This contradicts the widespread notion that the function of this muscle in carnivores is to extend theatlanto-cranial joint and to flex it laterally, but supports previous inferences about the head-flexing function ofatlanto-mastoid muscles in machairodontines. Sabretooth mastoid morphology implies larger and longer-fibredatlanto-mastoid muscles than in pantherines, and that most of their fibres ran inferior to the axis of rotation of theatlanto-occipital joint, emphasizing head-flexing action. © 2004 The Linnean Society of London, Zoological Journalof the Linnean Society, 2004, 140, 207–221.

ADDITIONAL KEYWORDS: basicranial morphology – Felinae – hunting behaviour – Machairodontinae – neckmuscles – skull.

INTRODUCTION

The predatory behaviour of sabretoothed carnivorousmammals has been a matter of debate for nearly a cen-tury, and it remains one of the most intriguing issuesin modern palaeontology. With no extant carnivoredisplaying such adaptations, we are left with the fossilremains, and our knowledge of functional anatomy, topropose credible hypotheses about the way those pred-ators used their elongated upper canines for preyprocurement.

The most recent group to evolve sabretooth adapta-tions were the machairodontines, members of the sub-family Machairodontinae within the true-cat family,Felidae. Like all derived sabretoothed mammals, thefelid sabretooths differed from their non-sabretoothedrelatives in showing modified mastoid regions, andthese modifications were recognized by early workersas a key feature for understanding the animal’s modeof attack.

The precise interpretation of the meaning of thesabretooths’ mastoid morphology has varied consider-ably. In the early 20th century, Matthew (1910) pro-posed his ‘stabbing’ theory, according to which the

208 M. ANTÓN ET AL.

© 2004 The Linnean Society of London, Zoological Journal of the Linnean Society, 2004, 140, 207–221

sabretooths used the neck-flexing and head-flexingmuscles to power a downward stroke or stab, thusallowing the upper canines to penetrate into the fleshof prey. The mandible would have virtually no role inthis kind of attack, and the clear adaptations for gapeseen in sabretooths would be meant to keep the lowerjaw out of the way of the stabbing motion. In Mat-thew’s scheme, the supposed hypertrophy of severalmuscles that depress the head and neck was the key tothe success of the stabbing motion. As evidence forthat adaptation, he mentioned the enlarged trans-verse processes of cervical vertebrae, which house theinsertions for a group of neck-flexing muscles calledthe scalenes, and the enlarged mastoid process, whichin turn houses the insertions for the sterno-cleido-mastoid group, a set of muscles that depress the head,pulling from their origins at the sternum and upperarm (Fig. 1). Matthew’s theory was refined by Simpson(1941), who proposed that the inertia of the predator’srush toward prey would be incorporated into the stab-bing motion, and it was accepted by many specialistsfor several decades. However, other workers (Bohlin,1947) argued that, among other problems, the long,flattened upper canines of sabretoothed cats were toofragile to withstand such violent use (Biknevicius &van Valkenburgh, 1996).

Most problems of the stabbing theory were satisfac-torily overcome with the ‘canine shear-bite’ hypothesis(Akersten, 1985), according to which the sabretoothskilled prey by means of a modified type of bite. InAkersten’s scenario, the jaw-closing muscles have asupporting role during the bite, but the main force forpenetration of the upper canines is provided by thehead-flexing action of the atlanto-mastoid muscula-ture. In the canine shear-bite, the mandible has aclear part to play as support for the opposing action ofthe upper canines, and the modifications for wide gapeare seen as adaptations to allow the lower jaw to playsuch a role while allowing clearance between theupper and lower canines. In addition, a recent study(Antón & Galobart, 1999) has shown that the cervicalmorphology of sabretooths reflects adaptations forstrong muscular control of motions of the neck includ-ing extension and lateral rotation, as would be neces-sary to provide support for a canine shear-bite, ratherthan the exclusive emphasis on efficient neck flexionrequired by the ‘stabbing’ theory.

A central difference between Matthew’s hypothesisand Akersten’s is that the former considers that themodifications in the mastoid region of sabretooths canbe explained as related to changes in the insertionarea, and function, of the brachiocephalic and sterno-mastoid muscles, whereas in Akersten’s view, theatlanto-mastoids were the most important musclesinvolved. In other words, Akersten gave more impor-tance to rotation of the head around the atlanto-

occipital joint, whereas advocates of the stabbing the-ory emphasized the importance of flexion of the wholeneck and head turning around the thoraco-cervicaljoint and posterior cervical intervertebral joints(Fig. 1). But when Akersten needed to support hisideas on anatomical grounds, he found a paucity of

Figure 1. Schematic drawing of the skull and cervical ver-tebrae of the scimitar-toothed cat Homotherium latidensshowing the hypothetical motions of the stabbing bite (top)and the canine shear bite (bottom). In the first case themain rotation is around a point behind the thoraco-cervicaljoint (white circle) and the posterior cervicals, whereas inthe second case, the main rotation occurs at the atlanto-occipital joint (white circle). In the stabbing model (top),the pull of the brachiocephalic muscles (single headedarrow) and of the scalenes (two headed arrow) provides themain force for the strike. In the canine shear-bite model(bottom), the pull of the atlanto-mastoid muscles (shorttwo-headed arrow) is the most important force for the pen-etration of the upper canines.

MASTOID ANATOMY IN FELIDS 209


detailed studies about the muscle insertions in themastoid region of large cats. In his own words,‘Descriptions of modern felid and canid anatomy oftenignore, or are not consistent in the terminology andinterpretation of those muscles’ (Akersten, 1985: 5).As a result, he based his hypothesis on a publishedstudy on the anatomy of the giant panda (Davis,1964). Akersten’s choice was supported by the com-mon-sense assumption of similarity in the dispositionof muscle insertions across different families and evensuborders within the Carnivora, but it gave rise touncertainties about homology, creating an unsatisfac-tory situation, which has lasted to this day.

Over 15 years later, we still lack detailed compara-tive data from the anatomy of the animals that wouldprovide the most adequate comparison, i.e. the living,large members of the family Felidae, to which theextinct machairodontines belong. The most usefulstudy of the muscles of a large felid is Barone’s (1967)paper on the myology of the lion, in which the neckmusculature is described in detail, but insertion areasin the mastoid region are only mentioned and notdescribed or figured. Similarly, for the domestic cat,anatomical studies abound, but again the insertionareas of muscles have been described (Reinhard &Jennings, 1935; Barone, 1989) but not figured in suf-ficient detail; regardless, the differences in morphol-ogy between small cats and pantherines go beyondmere size and, as commented below, may imply differ-ences in muscle function.

A further complication lies in the fact that all anat-omy treatises state that the action of the muscles mostrelevant to Akersten’s analysis, the obliquus capitiscranialis, is to extend and to rotate laterally theatlanto-cranial joint, rather than flexing the head aswas assumed by Akersten (Evans & Christensen,1979; Barone, 1989). A more recent, specific study ofthe suboccipital muscles in the neck of the domesticcat shows that the atlanto-mastoids generate littletorque in the saggital plane (Selbie, Thomson & Rich-mond, 1993). With these data in mind, Akersten’shypothesis would imply a case of function shift in amuscle group for the machairodontines (Bryant,1996). But it is also feasible that these muscles have ahead-flexing action in some modern carnivores,reflected in mastoid morphology.

This study intends to provide detailed informationabout the muscle insertions in the mastoid area ofmodern pantherines, and then to discuss the likelyimplications of our findings in terms of the evolutionand functional anatomy of sabretoothed cats.

MATERIAL AND METHODS

An adult lioness Panthera leo, two adult tigersPanthera tigris, one male and one female, an adult

female puma Puma concolor and an adult femalegenet Genetta genetta (Linnaeus, 1758) Cuvier,1816 were dissected by the authors at the Anat-omy Department of the University of Valladolid. Allspecimens were captive animals coming from theZoological Park of Matapozuelos, Valladolid prov-ince. We also incorporated information from a pre-vious dissection of an adult female striped hyaenaHyaena hyaena (Linnaeus, 1758) Brünnich, 1771and an adult male binturong Arctictis bingturong(Raffles, 1821) Temminck, 1824 from the MadridZoological Park. We also studied osteological mate-rial of extant and extinct carnivores to compare themorphology of the mastoid region. The skulls ofextant carnivores studied (besides those of the dis-sected species) include specimens of domestic catFelis catus Linnaeus, 1758, spotted hyena Crocutacrocuta (Erxleben, 1777) Kaup, 1828 and wolfCanis lupus Linnaeus, 1758. Reference is alsomade of published material of extinct machairodon-tine felids of the genera Homotherium Fabrini,1890 and Smilodon Lund, 1842, as well as descrip-tions of giant panda Ailuropoda melanoleuca(David, 1869) Milne-Edwards, 1870 and otherursids.

The dissected specimens were fresh and were notprepared with any preservation products, so theobservation of muscle fibres was excellent but dis-section had to proceed quickly before the tissuesdeteriorated. Each specimen was dissected in a sin-gle session, except in the case of the tigress andthe puma, which were frozen and subjected to asecond session. In all specimens, dissection pro-ceeded from the most external muscle layer, exceptin the lioness, which had been partly defleshedbefore our dissection, so that muscles externalto the splenius were damaged or missing, butthe deeper layers relevant for this study wereintact.

In each specimen, we dissected the neck musclesthat insert on the mastoid region and on adjacentareas of the skull and we identified origin and inser-tion areas of each muscle. We made both digital andconventional photographs of each subsequent mus-cle layer in each specimen, and relevant details ofmuscle structure and insertion were sketched inpencil directly from the dissected specimens. Skullsof large pantherines were available for comparisonand identification of skull features that emergedduring dissection, and the skulls and skeletons ofeach dissected specimen were subsequently pre-pared for detailed observation of the relevant osteo-logical details.

We followed the muscular nomenclature used by(Barone, 1989) in his treatise on the anatomy ofdomestic mammals.



RESULTS

MUSCLE ATTACHMENTS IN THE MASTOID AREA OF EXTANT LARGER FELIDS

The most external muscle inserting in the mastoidarea is the brachiocephalicus, which originates on thehumerus and has an aponeurotic insertion extendingfrom near the tip of the mastoid up the mastoid crestand nuchal crest to the midline (Fig. 2). Immediatelyinternal to this muscle appear the fibres of the rhom-boideus and splenius, which originate at the anteriorthoracic spinous processes and terminate in a commonaponeurosis extending just internal to that of the bra-chiocephalic, and with broadly the same extension(Fig. 3). At this same level, the fibres of the sterno-mastoid muscle are seen, extending from their originat the sternum and terminating in a tendinous inser-tion on the tip of the mastoid process. Some fibres ofthe sternomastoid extend upwards, sharing with thebrachiocephalic a common aponeurotic insertion alongthe mastoid crest (Fig. 3)

Internal to the m. splenius is the muscle mass of theextensors of the neck, including the biventer cervicis,semispinossus capitis, complexus and longissimuscapitis, which have fleshy insertions on the occipitalarea, above the mastoid region. Inferior to these canbe observed the obliquus muscles: the obliquus capitiscaudalis extending from the spine of the axis to thedorsal surface of the atlas wings, and the obliquuscapitis cranialis, extending from the ventral side of theatlas wings to the mastoid process. The mastoid inser-tion of the latter muscle is fleshy and extensive, cov-ering much of the area of the process (Fig. 4A, B). Inthe atlas, the origin area of the obliquus capitis crani-alis occupies most of the ventral surface of the wing.The superior fibres of this muscle are short, owing tothe small distance between their origin and insertion,but the inferior fibres span a considerable distancebetween the atlas wing and the lower part of the mas-toid process. The insertion area in the skull is broadestat its inferior tip. Superiorly, the insertion area is notrestricted to the mastoid process, and continues in anarrowing band up the nuchal crest. In the felid spec-imens dissected by us, we did not find evidence of anaccessory portion of this muscle extending dorsallyfrom the lip of the atlas wing, as described for the dog(Evans & Christensen, 1979; Done et al., 1995). In thepuma specimen there were some additional fibresextending dorsal to the atlas wing, in a position sim-ilar to the mentioned ‘accessory portion’. Unlike themain portion of the muscle, these fibres form a thinlayer, superficial to the m. obliquus capitis caudalisand covered by the m. splenius. Cranially, these fibresmingle with the latter muscle before it inserts on thenuchal crest (Fig. 4B).

The origin of the m. digastricus on the paroccipitalprocess is found to be variable in extent. In all casesthe main fibres of the muscle attach to the paroccipitalprocess tip, but whereas in the male tiger the insertionwas apparently restricted to that process, on thetigress some fibres of the muscle went to the tip of themastoid, and in the lioness the insertion extended tothe area around the base of the process, even into theadjacent part of the tympanic bulla (Fig. 5A) In themandibular ramus, the digastric muscle insertionextends from the level of the first molar anteriorly,reaching the level of the symphisis.

The muscle rectus capitis lateralis originates on asmall area of the ventral side of the atlas wing, medialto the attachment of the m. obliquus capitis cranialis,and inserts on the medial side of the paroccipital pro-cess, medial to the insertion of the m. obliquus capitiscranialis. In the puma, the insertion reaches the tip ofthe paroccipital process, adjacent to the insertion ofthe m. digastricus (Fig. 5B). In the genet, some fibresattach to the tympanic bulla.

MUSCLE ATTACHMENTS IN MACHAIRODONTINES AND IN OTHER CARNIVORES

The mastoid area in machairodont felids differs fromthat of extant larger felids in several ways (Fig. 6).The mastoid process itself is more developed, and itprojects in an antero-ventral direction to varyingextent, almost touching the postglenoid process in themore derived machairodont genera such as Smilodonand Homotherium. The paroccipital process is vari-ably reduced, especially in some of the more derivedmachairodont genera, and as a result the tip of themastoid process has a greater ventral projection thanthe tip of the paroccipital, whereas the reverse is truefor the extant felids. The texture of the mastoid pro-cess is often more rugose than in extant felids, andmore so in the more derived taxa. The orientation ofthe tip of the process is variable, facing anteriorly insome taxa, just as in extant felids, whereas in othertaxa it faces inferiorly. In most cases the process tip isproportionally broader and more distinctly sculptedthan in extant felids. The mastoid crest is usuallymore developed with a greater lateral expansion, andas a result the surface of the mastoid process itselftends to face more inferiorly and posteriorly, and lesslaterally, than in extant felids (Fig. 7).

Compared with machairodontine and extant felids,the mastoid area of canids shows a relatively smallmastoid process and a relatively large paroccipitalprocess. The mastoid process tip in canids is not placedinferior but actually level with, or dorsal to, the axis ofrotation of the atlanto-occipital joint, whereas theparoccipital process tip projects considerably moreventrally. In bears and in the giant panda, the mastoid



Figure 2. Photograph and schematic representation of superficial layer of head and neck muscles of male puma. 1, m.brachiocephalicus.



Figure 3. Photograph and schematic representation of intermediate plane of neck muscles of male puma. 2, m. trapezius;3, m. splenius; 4, m. sternomastoideus.

process is much larger and projects far more ventrallythan in the wolf, and indeed more than in extantfelids. In hyaenids, the paroccipital is ventrally pro-jected and anteriorly placed and thus very close to the

mastoid process, and the insertion area for the m.obliquus capitis cranialis is contained in the verticallyorientated band between the paroccipital and the mas-toid crest.



In his description of the giant panda, Davis (1964)figures a bundle of muscle fibres similar in position tothe accessory portion of the m. obliquus capitis crani-alis described in the dog (Evans & Christensen, 1979;Done et al., 1995). As noted above, we did not find evi-dence of such a portion in the studied pantherines,although a thin band of muscle fibres was observed inthe puma. In a binturong and a striped hyaena previ-ously dissected by us there was no accessory portion,but in the genet, as in the puma, we observed a thinband of muscle stemming from a small aponeurosisthat envelopes the lateral border of the atlas wing.These fibres appear to be continuous with the m. obliq-uus capitis cranialis but they join cranially with them. splenius and they lack a separate insertion area inthe skull.

DISCUSSION

Our observations of the muscle insertions in the mas-toid region of modern felids support most of Akersten’sinterpretations about the myology of extinct sabre-tooths, but also allow us to update and revise hisdiscussion of the head-flexing musculature. As he cor-rectly extrapolated from Davis’s (1964) study of thegiant panda, the muscle fibres having a most exten-sive attachment area in the mastoid process are thoseoriginating on the ventral side of the atlas wings.Given the distant relationship between felids and thegiant panda, Akersten cautioned that the musclesextending between the ventral surfaces of the atlaswings to the postero-lateral margins of the mastoidprocess in Smilodon ‘may or may not be homologouswith those of Ailuropoda’ (Akersten, 1985: 5). Ourresults show that those concerns about homology werefounded, because there are important differences indetail between the positions of the muscle insertionsin extant felids and those described by Davis (1964) forAiluropoda. In figure 19 of Davis (1964) the insertionof the m. obliquus capitis cranialis is seen to occupymuch of the surface of the mastoid and paroccipitalprocesses, extending to an area medial to the latter,whereas the m. rectus capitis lateralis is seen to inserton a portion of the mastoid process lateral to the inser-tion of the previous muscle. Thus there appear to betwo atlanto-mastoid muscles in the giant panda. Bycontrast, in extant felids dissected by us, the m. obliq-uus capitis cranialis insertion occupies most of themastoid process, whereas the m. rectus capitis later-alis inserts outside the mastoid process, in and nearthe medial surface of the paroccipital process andmedial to the insertion of the previous muscle. The lat-ter condition agrees with that described for the domes-tic cat (Reinhard & Jenning, 1935; Barone, 1989), lion(Barone, 1967), and with that described and figuredfor the domestic dog (Barone, 1989), striped hyena

(Spoor & Badoux, 1986) and genet (this paper). Con-sequently, it can be said that in all these animals theonly atlanto-mastoid muscle is the m. obliquus capitiscranialis. These differences suggest an apomorphiccondition for the panda or for the whole Ursidae, oralternatively Davis (1964) may have been wrong aboutthe identity of the muscles in the specimen availableto him. In any event, dissection of additional speci-mens of Ailuropoda would be desirable in order toclarify this subject.

Some of the observed differences among thereviewed carnivores in the disposition of some rele-vant muscles may have a functional significance: thepresence of an accessory dorsal portion of the m. obliq-uus capitis cranialis in the giant panda (as figured butnot mentioned by Davis, 1964: fig. 92) and in the dog(where it is described as having a separate insertion inthe skull; Evans & Christensen, 1979) would point tothe existence of an extensor function of the musclebesides that of head-flexion. By contrast, its reductionor absence among the reviewed members of the Feli-formia points to an almost exclusive flexor action.

The lack of comparative data led Akersten to saythat ‘modern felids and canids possess tiny mastoidprocesses with only very minute muscles extendingbetween them and the atlas wings’ (Akersten, 1985:5). Our results show that generalization to be wrong.Although it is true that modern canids have relativelysmall mastoid processes (Fig. 7), those of tigers andlions are relatively much larger, providing attachmentareas for powerful atlanto-mastoid muscles. A furtherdifference between large canids and larger felids isthat the mastoid process of the latter projects furtherdownwards than in the former, not only enlarging themuscle attachment area but also changing the actionof the atlanto-mastoid muscles. Effectively, the fibresof the m. obliquus capitis cranialis in larger felids arelocated more clearly below the level of the occipitalcondyles, and as a result of this change, the contrac-tion of that muscle is more effective at flexing thehead, whereas in canids the head-flexing action wouldbe less efficient and the muscle would contribute tostabilize the atlanto-cranial articulation when con-tracting bilaterally, while unilateral contractionrotates the head laterally (Barone, 1989). In thedomestic cat, there is little ventral projection of themastoid process, and the atlanto-mastoid muscles aresaid to generate little torque on the sagittal plane (Sel-bie et al., 1993). So we can say that modern largerfelids show an incipient stage of the implication of theatlanto-mastoid musculature in head flexion duringthe bite, which would become far more emphasized inmachairodontines. Contribution of the neck muscula-ture to vertical motions of the head associated withmastication is already known in domestic cats(Gorniak & Gans, 1980), so that the adaptation of



Figure 4. (A) Photograph and schematic representation of deep muscles of the neck in male tiger. 5, m. obliquus capitiscaudalis; 6, m. obliquus capitis cranialis; 8, m. digastricus; At, lateral border of the atlas wings; Ax, dorsal border of axis. (B)Photograph and schematic representation of deep muscles in a male puma. f, additional superficial fibres of m. obliquuscapitis cranialis, dorsal to the atlas wing.

A



B

Figure 4. Continued



Figure 5. (A) Photograph and schematic representation of deep muscles of the neck in a lioness. The posterior portion ofthe temporalis muscle has been removed to make visible the nuchal region of skull and neck muscles attaching to it. 7, deepextensors of the neck, including rectus capitis dorsalis major and minor; Am, auditory meatus; Mp, mastoid process; Nc,nuchal crest. (B) Photograph and schematic representation of deep muscles of the neck of a male puma in ventral view. 9,m. rectus capitis lateralis.

A



B

Figure 5. Continued



Figure 6. Photographs of the mastoid region of skull in female lion, Panthera leo (top) and scimitar-toothed cat, Homoth-erium latidens (bottom) from Incarcal, Spain (IN-I 929). Note that the back of the skull is broken in the fossil. Muscle inser-tion areas are marked; muscle numbering as in Figs 1–5. M, mastoid process; P, paroccipital process.

MP

MP



sabretooths would simply elaborate on an existing bio-mechanical system (Bryant, 1996).

All this is in contrast with the interpretations ofMatthew, who considered that the most relevant mus-cles for head flexion in machairodonts where the m.brachiocephalicus (his cleidomastoids) and m. sterno-mastoideus, and showed these muscles as occupyingwith their attachments the full extent of the mastoidprocess (Matthew, 1910: figure 9).

Our results clearly show that the insertion of the m.brachiocephalicus and the more superior portions ofthe sterno-mastoids, although broadly coinciding withthe position indicated in Matthew’s figure, are actu-ally aponeurotic and restricted to a thin band in theouter margin of the mastoid process, i.e. in the mas-

toid crest, whereas the attachment of the m. sterno-mastoideus is restricted to the process tip. Theinsertion of the m. obliquus capitis cranialis, by con-trast, is fleshy and extensive, and the action of thismuscle is likely to have had a stronger effect on theflexion of the head.

These findings support the interpretation that theaction of the atlanto-mastoid musculature (i.e. the m.obliquus capitis cranialis) was the most relevant forhead-flexing motions aiding the penetration of theupper canines into the flesh of prey. The immediateimplication of this is that the relevant action involvedwas rotation of the head around the atlanto-occipitaljoint (an action associated with the canine shear-bite),rather than rotation of the whole neck and head

Figure 7. Drawing of the skull and anterior cervicals of Panthera tigris (top) and Homotherium latidens (bottom) withfibres of selected muscles. Muscle numbering as in Figs 1–5. A black circle in the condylar area represents the position ofthe rotation centre of the atlanto-occipital articulation. Notice how, in Homotherium, most fibres of the obliquus capitis cra-nialis extend well below that centre of rotation, and would therefore have a stronger head-flexing action. Notice also howthe greater distance between the posterior tip of the atlas wings and the tip of the mastoid process in Homotherium makesfor longer inferior fibres of the obliquus capitis cranialis muscle.



around the thoraco-cervical joint (an action associatedwith the ‘stabbing’ bite). In the canine shear-bite, mus-cular action from a static start provides the main forcefor penetration, whereas in the ‘stabbing’ interpreta-tion, the momentum gathered during rotation of thehead along a wide arc, or even during the leap towardprey, is invoked to explain canine penetration. It istrue nonetheless that the downward projection of thetip of the mastoid process would improve the efficiencyof the sternomastoid muscles as head flexors, anaction which would be incorporated to the canineshear-bite mechanics as discussed by Akersten (1985)and Antón & Galobart (1999).

The reduction in size and in ventral projection of theparoccipital process in sabretooths implies changes inthe action of the m. digastricus, which is to depress themandible. In spite of the variation observed in theextent of the area of origin of this muscle in the extantfelids studied, the main attachment is always on thetip of the paroccipital, and the lesser the ventral pro-jection of the process tip, the greater the distancebetween the origin and insertion of the fibres of the m.digastricus. Such an increase in the vertical span ofthe fibres would be advantageous in terms of theincreased gape required by the canine shear-bite(Antón & Galobart, 1999).

CLOSING COMMENT: ANATOMICAL DESCRIPTIONS, SOFT TISSUE

RECONSTRUCTION AND PALAEOBIOLOGICAL INFERENCE

The importance of soft tissue reconstruction in fossilvertebrates is being more and more widely recognizedamong evolutionists. As summarized by Witmer (1995:20) ‘(1) Soft tissues largely are responsible for theexistence, maintenance and form of bones, (2) judge-ments about the form and actions of soft tissues are(implicitly if not explicitly) the basis for a host ofpalaeobiological inferences; and (3), with regard tosystematics, soft tissue relationships may providetestable hypotheses on independence or nonindepen-dence of phylogenetic characters’.

However, accurate soft tissue reconstruction isimpossible without a sound database about the rela-tionships between bone and soft tissue in extant taxa.Unfortunately, it appears that descriptive mono-graphs about the gross anatomy of animals have lostthe favour of current zoological science, due at least inpart to a prejudice among modern scientists againstthe descriptive aspect of natural history (Gould, 1989–1991: 96–100). However, the field of palaeobiologicalinference provides many occasions to regret the pau-city of accurate descriptions of modern organisms, andof the musculo-skeletal systems of modern vertebrates

in particular, the case of the mastoid region in carni-vores being just one example of the problem. When-ever palaeobiologists attempt to reconstruct softtissues in fossil mammals, the descriptive anatomicalreferences cited are often remarkably ancient (Spoor& Badoux, 1986; Witmer, Sampson & Solounias, 1999;Naples & Martin, 2000).

While preparing his monograph about the giantpanda, Davis commented about the lack of comparativeinformation in plaintive terms: ‘The muscles of the Car-nivora are comparatively well known, but even for thisorder our knowledge is at a primitive level. Descrip-tions are incomplete and inaccurate, often doing littlemore than establish the fact that a given muscle ispresent in species dissected. Even for domestic carni-vores – the dog and the cat – the standard referenceworks are full of inaccuracies and are inadequatelyillustrated. Most of the genera of Carnivora have neverbeen dissected at all.’ (Davis, 1964: 146). He goes on tocomment on the importance of muscular differences forthe overall problem of evolutionary mechanisms, butthen asks: ‘How can such differences be detected andevaluated?. Certainly not on the basis of existingdescriptions and illustrations.’ (Davis, 1964: 146).

Most of the descriptions that we used as reference todiscern the pattern of muscle insertions in the mastoidregion in carnivores simply did not exist when Daviswrote his monograph, but even those references arenot enough, either in detail or range of species treated,to solve the problem, and in general the situationtoday remains much as it was in 1964. With ourresults in hand, and given the insufficient referencesavailable to Davis, there is now reason to question theinterpretations that he made of atlanto-mastoid mus-culature in Ailuropoda, but in order to add to the dis-cussion, it would be necessary to describe additionalspecimens of the giant panda, and of other ursids.Such investigations would be especially pertinent tothe subject of atlanto-mastoid muscle function insabretooths, because the giant panda and other ursidsshare a mastoid morphology different from most mod-ern carnivores and intriguingly similar to that ofmachairodontines (Akersten, 1985).

As Witmer commented, ‘the accuracy of soft tissuereconstructions is vital because mistakes in soft-tissueinference cascade upwards through the “inverted pyr-amid” of paleobiological inference, amplifying theerror.’ (Witmer, 1995: 22). If the soft tissue inferencesare based on an insufficient or inaccurate databaseabout the anatomy of modern taxa, then all the sub-sequent steps will be questionable.

CONCLUSIONS

The results of our study show that the most extensivemuscular insertions in the mastoid process of modern



big cats are those of the obliquus capitis cranialis. Thesternomastoid muscle inserts on the tip of the mastoidprocess, and the m. brachiocephalicus inserts througha thin aponeurotic band along the mastoid crest. Them. digastricus inserts on the tip of the paroccipitalprocess but can extend to adjacent areas depending onindividual variation.

These results allow interpretation, in terms of mus-cle function, of the differences in mastoid morphologybetween modern pantherines and machairodontines.The enlarged, ventrally projecting mastoid process ofthe latter implies that the insertion area of the atlan-tomastoid muscles was larger and that the more infe-rior fibres of these muscles had an enhanced action ashead flexors, being able to rotate the head along alarge arc around the atlanto-occipital articulation. Thehead-flexing action of the portions of the sternomas-toid inserting on the mastoid process tip would also beimproved by the ventral projection of the latter,whereas the function of the m. brachiocephalicuswould be little altered. The fibres of the m. digastricuswere probably longer in machairodontines as a resultof the reduction of the paroccipital process, whichimplied that the process tip was higher and thus fur-ther from the insertion of the m. digastricus in themandibular ramus.

ACKNOWLEDGEMENTS

This paper was supported by project MCT-BTE2002-00410. We are grateful to Angel Galobart (Instituto dePalaeontología Miquel Crusafont) and Josep Tarrús(Museu Arqueológic Comarcal de Banyoles) for theopportunity to study the fossils of Homotherium lati-dens from Incarcal.

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Implications of the mastoid anatomy of larger extant felids for the evolution and predatory...

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