Aspects of the Functional Morphology in the Cranial and Cervical Skeleton of the Sabre-Toothed Cat Paramachairodus Ogygia (Kaup, 1832) (Felidae

Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Linnean Society of London, 2005? 2005 1443 363377 Original Article FUNCTIONAL MORPHOLOGY OF P. OGYGIAM. J. SALESA ET AL. Zoological Journal of the Linnean Society, 2005, 144, 363–377. With 11 figures Aspects of the functional morphology in the cranial and cervical skeleton of the sabre-toothed cat Paramachairodus ogygia (Kaup, 1832) (Felidae, Machairodontinae) from the Late Miocene of Spain: implications for the origins of the machairodont killing bite MANUEL J. SALESA1*, MAURICIO ANTÓN2, ALAN TURNER1 and JORGE MORALES2 1School of Biological & Earth Sciences, Byrom Street, Liverpool John Moores University, Liverpool, L3 3A F , U K 2Departamento de Palaeobiología, Museo Nacional de Ciencias Naturales-CSIC, José Gutiérrez Abascal, 2. 28006 Madrid, Spain Received January 2004; accepted for publication March 2005 The skull and cervical anatomy of the sabre-toothed felid Paramachairodus ogygia (Kaup, 1832) is described in this paper, with special attention paid to its functional morphology. Because of the scarcity of fossil remains, the anatomy of this felid has been very poorly known. However, the recently discovered Miocene carnivore trap of Batallones-1, near Madrid, Spain, has yielded almost complete skeletons of this animal, which is now one of the best known machairodontines. Consequently, the machairodont adaptations of this primitive sabre-toothed felid can be assessed for the first time. Some characters, such as the morphology of the mastoid area, reveal an intermediate state between that of felines and machairodontines, while others, such as the flattened upper canines and verticalized mandibular symphysis, show clear machairodont affinities. © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363-377. ADDITIONAL KEYWORDS: Batallones – Carnivora – Felinae – functional anatomy – Mammalia – Miocene – pantherine – Turolian – Vallesian. straint in each group, still remain essentially a mystery. INTRODUCTION Sabre-toothed predators have evolved several times among different orders of mammals and in somewhat different forms even among nonmammalian synapsids (Turner & Antón, 1997). The similarities in detail between often completely unrelated taxa are so remarkable that the sabre-tooth adaptation has become a text-book example of convergent evolution. However, exactly how it evolved in each case, what the main evolutionary pressures were and where the balance lay between adaptation and phylogenetic con- One of the reasons for this lack of resolution is the fact that within each convergent group of sabre-tooth predators it is usually the most derived, crown taxa that are the best known anatomically while the basal taxa have much poorer fossil records. Thus, among the Machairodontinae (the sabre-toothed subfamily within the extant family Felidae), the crown taxa such as Homotherium and Smilodon from the Pliocene and Pleistocene have been known for many decades thanks to complete skulls and skeletons, while the fossil record of basal genera such as Paramachairodus from the Late Miocene have traditionally consisted of scarce and fragmentary material. The situation is not *Corresponding author. E-mail: [email protected] © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 363 364 M. J. SALESA ET AL. very different across the various families of mammalian sabre-tooths, including the Nimravidae and Barbourofelidae among the Carnivora (Peigné, 2002; Morlo, Peigné & Nagel, 2004) and the marsupial Thylacosmilidae (Argot, 2003, 2004). Consequently, no studies of the functional morphology of Paramachairodus have yet been published. The discovery of Batallones-1, a new Late Miocene fossil locality near Madrid, Spain, has yielded a large number of specimens of P . o gygia, with at least 24 individuals represented and including several skull and mandibles (Salesa, 2002). This locality has been interpreted as a carnivore trap based on its special characteristics, such as the presence of an extremely high percentage of carnivores (98%) and the morphology of the site, essentially a hole with semivertical walls (Antón & Morales, 2000; Morales et al., 2000). The carnivore guild of Batallones-1 also includes the lion-sized sabre-toothed felid Machairodus aphanis- tus, the bear-dog Amphicyon sp. aff. A. castellanus, the primitive hyaenid Protictitherium crassum and other carnivores such as mustelids and Simocyon batalleri, a medium-sized carnivore related to the extant red panda (Antón & Morales, 2000; Morales et al., 2000; Salesa & Fraile, 2000; Salesa, 2002; Antón et al., 2004a; Peigné et al., 2005). The result of this unbalanced fossil record is that emphasis on a series of highly convergent crown taxa has led to an exaggerated perception of homogeneity in adaptation and to suggestions that the so-called ‘sabre-tooth complex’ would be under ‘strong pleiotropic control’ (Dawson et al., 1986). A better fossil record and a detailed study of basal taxa would greatly help to clarify the origins of this predatory adaptation, in particular of the ‘canine shear-bite’, the derived killing bite modality that has been proposed as a functional explanation of the morphology of crown sabre-toothed taxa such as Smilodon and Homotherium (Akersten, 1985; Antón & Galobart, 1999) The genus Paramachairodus Pilgrim, 1913 includes primitive, leopard-sized sabre-toothed cats known from the Late Miocene faunas of Eurasia (Beaumont, 1975; Morales & Soria, 1977; Montoya, 1994; Morlo, 1997; Salesa et al., 2003). Two species have been traditionally referred to this genus: P . o gygia (Kaup, 1832), of Vallesian-Early Turolian age (MN 9–11 of Mein, 1975) and P . o rientalis (Kittl, 1887) of Turolian age (MN 11–13), distinguished by several dental traits. The more primitive species, P . o gygia, had noncrenulated upper canines, a P4 without ectostyle and with a strong protocone, and a P3 with a posterointernal expansion. P . o rientalis had crenulated upper canines, a P4 with a well marked ectostyle as well as a reduced, backwardly displaced protocone and a P3 reduced in size and without posterointernal expansion (Salesa et al., 2003). In 1924, Zdansky created the species P . m aximiliani for a damaged skull from the Late Miocene of China. The differences between this third species and P. o rientalis are largely confined to the more curved upper canines of P . m aximiliani, where there are crenulations on both keels (Zdansky, 1924). These characters are now considered to be of little systematic value, because crenulations are not equally evident in both keels. Thus for most authors, P . m aximiliani is a synonym of P . o rientalis (Pilgrim, 1931; Beaumont, 1978; Salesa, 2002; Salesa et al., 2003). The anatomy of Paramachairodus has been largely unknown, because it is present in only a few fossil localities such as Pikermi (Greece, MN 12), Maragha (Iran, MN 11) or Eppelsheim (Germany, MN 9) and represented by relatively scarce material. Most finds have been of dentitions. While it has long been clear that Paramachairodus was a sabre-toothed cat, the absence of more extensive anatomical information has meant that its machairodont adaptations and wider aspects of its palaeobiology have remained unknown. In this paper we present a functional analysis of the cranial, mandibular and cervical anatomy of P . o gygia, concentrating on aspects directly related to the canine shear-bite adaptation. This analysis has revealed an intermediate morphology between the extant felines and the more derived sabre-toothed cats such as Smilodon or Homotherium. MATERIAL AND METHODS Functional study of the cranial and cervical anatomy of Paramachairodus ogygia has been possible because of the great number of newly available fossils of this species: a total of 16 skulls, 12 mandibles and several vertebrae belonging to the Batallones-1 assemblage. All the material is housed at the Museo Nacional de Ciencias Naturales-CSIC in Madrid, Spain. Comparisons with other Felidae have been made using the extant felines Panthera leo, Panthera tigris, Panthera pardus, Panthera onca, Uncia uncia, Neofelis nebu- losa, Caracal caracal, Lynx pardina and Puma con- color, belonging to the collections of the Museo Anatómico de la Universidad de Valladolid and Museo Nacional de Ciencias Naturales (Madrid). We also used published information on modern felid anatomy (Barone, 2000; Reinhard & Jennings, 1935; Sisson & Grossman, 1962) and on the morphology of other, more derived sabre-toothed cats such as Smilo- don fatalis and Homotherium latidens. The latter taxa were chosen as the ideal reference for comparison with P. o gygia because they exemplify the most derived state for the sabre-toothed adaptations within the Machairodontinae, whilst P . o gygia occupies a near basal position in the same subfamily. The degree of machairodont adaptations appears to be essentially © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 FUNCTIONAL MORPHOLOGY OF P . O GYGIA 365 independent of such body size differences as those observed between P . o gygia and the referred taxa. Differences in the height of the crown of the upper canines between P . o gygia and reference taxa were assessed using an ANOVA on the index between crown height and basal skull length. All the measured upper canines were unworn specimens. Differences in relative elongation of the neck were assessed by calculating an index between the corpus length of the atlas and the third cervical vertebra. The lack of associated C3 and atlas of P . o gygia in Batallones-1 was overcome by taking an average measurement between several isolated C3 and atlas vertebrae and comparing the resultant index with similar indices of reference taxa using a Student’s t-test. These results provided the most reliable indication of elongation of the neck in the absence of complete, associated cervical series of P. o gygia. In the more derived members of this group, the paraoccipital process becomes very reduced, almost vestigial, and the mastoid process is hyper-developed (Emerson & Radinsky, 1980), overlapping the auditory bulla in its growth in some genera such as Smilodon (Fig. 1). Thus, the mastoid region of P . o gygia can be considered primitive for the Machairodontinae, but it is clearly within the machairodont lineage because its morphology is derived in relation to the earliest felids of the genera Proailurus and Pseudaelurus. There are few known basicranial remains of these genera, but in the Proailurus-like skull from Ginn Quarry (Hunt, 1998: fig. 19A), and in the holotype of Pseudaelurus validus (Rothwell, 2001: fig. 3), the paroccipital process can be seen to be well developed ventrally, surpassing the level of the mastoid process; this condition is also found in fossil and extant species of the Felinae. The mastoid process is the attachment area for some important muscles directly involved in headdepression movements, such as the brachiocephalicus (which has its origin on the humerus), part of the fibres of the sternocephalicus (extending from the manubrium of the sternum) and the obliquus capitis anterior (with its origin on the ventrolateral surface of the atlas wings) (Reinhard & Jennings, 1935; Barone, 2000). The inferred position of these attachments on the cranium of P . o gygia is shown in Figure 2. The anteroventral displacement of these attachment areas in the Machairodontinae in relation to the Felinae caused by the modification of the mastoid process has an important consequence. The distance between the muscular attachment areas and the atlanto-cranial articulation enlarges, resulting in an increase in the length of the lever arm of the flexor muscles of the head (Antón & Galobart, 1999) and thus producing a more powerful contraction. Moreover, there is another interesting implication of this displacement of muscle attachment areas. In the primitive model, exemplified by the felines, the main function of the obliquus capitis anterior is the extension of the head on the atlas (Sisson & Grossman, 1962; Barone, 2000). This is because a great number of the fibres of this muscle are disposed above the point of rotation of the head over the atlas (Fig. 3A) and thus their contraction produces the extension of the head. In the sabre-toothed cats, most of the fibres of the obliquus capitis anterior are below the point of rotation of the head (Fig. 3B) because of the anteroventral displacement of the mastoid process. The function of this muscle is thus ventral flexion of the head, a motion directly involved in the canine shear-bite (Antón et al., 2004b), as discussed further in the final section. FUNCTIONAL MORPHOLOGY OF THE SKULL AND MANDIBLE GENERAL CRANIAL MORPHOLOGY The skull of P . o gygia shows an overall morphology similar to that of a pantherine cat (Figs 1, 6, 11), although there are some differences. The shape of the nasals is neither completely rectangular, as in Smilo- don or Homotherium, nor triangular, as in most of the pantherines, but shows an intermediate morphology. All nuchal, lambdoid and sagittal crests are well developed, and the join between sagittal and frontal crests is situated at the level of the postorbital processes of the frontal bone, as in pantherines and felines in general. The zygomatic arch of P . o gygia is broadly similar to that of a pantherine, but with a postorbital process that is almost vestigial, unlike the pantherines in which this process is large and pointed. The tympanic bullae of P . o gygia are similar to those of the pantherines. They are rounded, but less inflated than in the latter, and extend from the anterior margin of the mastoid process to the posterior margin of the postglenoid process. MASTOID AREA The morphology of the mastoid region in P . o gygia shows an intermediate condition between that of the more derived Pleistocene sabre-toothed cats, such as Smilodon or Homotherium, and that of the fossil and extant Felinae. The paraoccipital process of P . o gygia is relatively smaller than in the latter, whereas the mastoid process has a similar size to that in the felines, although it is displaced in an anteroventral direction (Fig. 1). This morphology is plesiomorphic for the sabre-toothed cats. The reduction of the paroccipital process in the sabre-toothed cats, including P . o gygia, can be related to the need to increase the gape of the mandible © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 366 M. J. SALESA ET AL. p.p. p.p. p.p. m.p. m.p. m.p. <ul style="display: flex;"><li style="flex:1">A</li><li style="flex:1">B</li><li style="flex:1">C</li></ul>5 cm DFigure 1. Left mastoid morphology of some species of Felidae showing the different development of the mastoid process (m.p.) and paraoccipital process (p.p.). A, Panthera leo. B, Paramachairodus ogygia from Batallones-1, B-1377. C, Smilodon fatalis from Rancho La Brea. D, B-1377, skull of P . o gygia from Batallones-1 in left lateral view with mastoid area circled. because of the enlargement of the upper canines. The function of the digastricus muscle, whose insertion areas are the paroccipital process and the ventral flange of the dentary, is to open the mandible (Sisson & Grossman, 1962; Barone, 2000). If the ventral projection and size of the paramastoid process is reduced, which is the condition shown by sabre-toothed felids, the attachment of this muscle is displaced dorsally, increasing fibre lengths and thus allowing efficient contraction at larger gapes (Emerson & Radinsky, 1980; Antón & Galobart, 1999). The morphology of the mastoid region in P . o gygia shows an early stage of the skull modifications that will reach their maximum development in the later Machairodontinae, such as Smilodon or Homothe- rium. The remodelling of this area in P . o gygia produces an increase in the force generated by the flexor muscles of the head and an increase in the maximum gape of the mandible. These changes suggest that the development of the canine shear-bite, the machairodont type of killing bite, had already started in this Late Miocene species (Salesa, 2002). This kind of © 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 FUNCTIONAL MORPHOLOGY OF P . O GYGIA 367 AOb. Cap. Post. brachiocephalicus Br. Ob. Cap. Ant. rectus capitis lateralis digastricus sterno- Ob. Cap. Post. cephalicus obliquus capitis anterior BFigure 2. Inferred areas of muscular attachment on the skull of Paramachairodus ogygia. Ob. Cap. Ant. Br. attack consisted of a well-aimed bite to the throat of the prey, which damaged its blood vessels and trachea and resulted in almost instantaneous death. This is in contrast with the feline killing method where the prey has to be suffocated with a bite in the throat lasting several minutes (Turner & Antón, 1997). These two different hunting methods explain the significant differences in the cranial and cervical morphology of the Felinae and Machairodontinae, and they are already present in one of the most primitive machairodonts, P . o gygia (Martin, 1980; Biknevicius & van Valkenburgh, 1996; Turner & Antón, 1997; Antón & Galobart, 1999). This kind of attack was probably developed in parallel by other ‘sabre-toothed’ carnivores, such as the Barbourofelines and Thylacosmilinae, and their mastoid anatomy shows some analogies with that of the true sabre-toothed felids (Turner & Antón, 1997; Morales et al., 2001). Figure 3. Anatomical disposition of the muscles brachiocephalicus (Br.), obliquus capitis anterior (Ob. Cap. Ant.) and obliquus capitis posterior (Ob. Cap. Post.) in Felinae and Machairodontinae. A, Panthera leo. B, Homotherium latidens (artwork by M. Antón). correlated with the existence of a high vertical stress in that zone during the canine shear-bite, due in part to the use of the mandible as an anchor. The curved mandibular symphysis of felines does not suffer such stress during the attack, because this is achieved with the maxilla and mandible biting at the same time (Biknevicius, van Valkenburgh & Walker, 1996). Another possible interpretation, compatible with the one outlined above, is that an increase in the vertical height of the symphysis is an efficient way to counter symphyseal bending due to axial twisting of the mandibular corpora, an argument that has been put forward to explain the vertically high symphyses of sabre-toothed therapsids (Jenkins, Thomasson & Norman, 2002). It is also possible that the verticalized mandibular symphysis of P . o gygia and other sabre-toothed cats can be explained as a consequence of reorganization in the alveolar zone of the lower canines. Because of the smaller palate width of the sabre-toothed cats relative to the felines, the lower canines had to become verticalized to allow occlusion. Nevertheless, it is probable that both mechanisms acted together, creating the specialized symphysis model of the Machairodontinae. Some sabre-toothed cat taxa, such as Homotherium and Megantereon, developed a mandibular flange, a kind of ventral projection in the symphysis that could MANDIBULAR SYMPHYSIS The mandibular symphysis of P . o gygia is strongly verticalized, forming an almost square angle with the ventral flange of the mandibular corpus (Fig. 4B). Owing to this verticalization, its anterior surface is flat and describes a distinctive plane. This morphology, typical of the sabre-toothed cats (Fig. 4C), is clearly different from the feline model, in which the anteroventral surface of the mandible is gently curved upwards (Fig. 4A). The morphology of the mandibular symphysis of P . o gygia can be related to the canine shear-bite, in which the mandible acts as an anchor while the head is flexed downwards, sinking the upper canines into the flesh of prey. This morphological change in the mandibular symphysis of P . o gygia relative to the feline model can be

Aspects of the Functional Morphology in the Cranial and Cervical Skeleton of the Sabre-Toothed Cat Paramachairodus Ogygia (Kaup, 1832) (Felidae

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