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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Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean 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: Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 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 3AF, UK 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.

INTRODUCTION straint in each group, still remain essentially a mystery. Sabre-toothed predators have evolved several times One of the reasons for this lack of resolution is the among different orders of mammals and in somewhat fact that within each convergent group of sabre-tooth different forms even among nonmammalian synapsids predators it is usually the most derived, crown taxa (Turner & Antón, 1997). The similarities in detail that are the best known anatomically while the basal between often completely unrelated taxa are so taxa have much poorer fossil records. Thus, among remarkable that the sabre-tooth adaptation has the Machairodontinae (the sabre-toothed subfamily become a text-book example of convergent evolution. within the extant family Felidae), the crown taxa such However, exactly how it evolved in each case, what the as Homotherium and Smilodon from the Pliocene and main evolutionary pressures were and where the Pleistocene have been known for many decades balance lay between adaptation and phylogenetic con- thanks to complete skulls and skeletons, while the fossil record of basal genera such as Paramachairodus from the Late Miocene have traditionally consisted of *Corresponding author. E-mail: [email protected] scarce and fragmentary material. The situation is not

364 M. J. SALESA ET AL. very different across the various families of mam- Consequently, no studies of the functional morphology malian sabre-tooths, including the Nimravidae and of Paramachairodus have yet been published. Barbourofelidae among the Carnivora (Peigné, 2002; The discovery of Batallones-1, a new Late Miocene Morlo, Peigné & Nagel, 2004) and the marsupial fossil locality near Madrid, Spain, has yielded a large Thylacosmilidae (Argot, 2003, 2004). number of specimens of P. ogygia, with at least 24 The result of this unbalanced fossil record is that individuals represented and including several skull emphasis on a series of highly convergent crown taxa and mandibles (Salesa, 2002). This locality has been has led to an exaggerated perception of homogeneity interpreted as a carnivore trap based on its special in adaptation and to suggestions that the so-called characteristics, such as the presence of an extremely

‘sabre-tooth complex’ would be under ‘strong pleiotro- high percentage of carnivores (98%) and the morphol- Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 pic control’ (Dawson et al., 1986). A better fossil record ogy of the site, essentially a hole with semivertical and a detailed study of basal taxa would greatly help walls (Antón & Morales, 2000; Morales et al., 2000). to clarify the origins of this predatory adaptation, in The carnivore guild of Batallones-1 also includes the particular of the ‘canine shear-bite’, the derived killing lion-sized sabre-toothed felid Machairodus aphanis- bite modality that has been proposed as a functional tus, the bear-dog Amphicyon sp. aff. A. castellanus, the explanation of the morphology of crown sabre-toothed primitive hyaenid Protictitherium crassum and other taxa such as Smilodon and Homotherium (Akersten, carnivores such as mustelids and Simocyon batalleri, 1985; Antón & Galobart, 1999) a medium-sized carnivore related to the extant red The genus Paramachairodus Pilgrim, 1913 includes panda (Antón & Morales, 2000; Morales et al., 2000; primitive, leopard-sized sabre-toothed cats known Salesa & Fraile, 2000; Salesa, 2002; Antón et al., from the Late Miocene faunas of Eurasia (Beaumont, 2004a; Peigné et al., 2005). 1975; Morales & Soria, 1977; Montoya, 1994; Morlo, In this paper we present a functional analysis of the 1997; Salesa et al., 2003). Two species have been tra- cranial, mandibular and cervical anatomy of P. ogygia, ditionally referred to this genus: P. ogygia (Kaup, concentrating on aspects directly related to the canine 1832), of Vallesian-Early Turolian age (MN 9–11 of shear-bite adaptation. This analysis has revealed an Mein, 1975) and P. orientalis (Kittl, 1887) of Turolian intermediate morphology between the extant felines age (MN 11–13), distinguished by several dental and the more derived sabre-toothed cats such as traits. The more primitive species, P. ogygia, had non- Smilodon or Homotherium. crenulated upper canines, a P4 without ectostyle and with a strong protocone, and a P3 with a posterointer- MATERIAL AND METHODS nal expansion. P. orientalis had crenulated upper canines, a P4 with a well marked ectostyle as well as a Functional study of the cranial and cervical anatomy reduced, backwardly displaced protocone and a P3 of Paramachairodus ogygia has been possible because reduced in size and without posterointernal expansion of the great number of newly available fossils of this (Salesa et al., 2003). species: a total of 16 skulls, 12 mandibles and several In 1924, Zdansky created the species P. maximiliani vertebrae belonging to the Batallones-1 assemblage. for a damaged skull from the Late Miocene of China. All the material is housed at the Museo Nacional de The differences between this third species and Ciencias Naturales-CSIC in Madrid, Spain. Compari- P. orientalis are largely conﬁned to the more curved sons with other Felidae have been made using the upper canines of P. maximiliani, where there are extant felines Panthera leo, Panthera tigris, Panthera crenulations on both keels (Zdansky, 1924). These pardus, Panthera onca, Uncia uncia, Neofelis nebu- characters are now considered to be of little systematic losa, Caracal caracal, Lynx pardina and Puma con- value, because crenulations are not equally evident in color, belonging to the collections of the Museo both keels. Thus for most authors, P. maximiliani is a Anatómico de la Universidad de Valladolid and Museo synonym of P. orientalis (Pilgrim, 1931; Beaumont, Nacional de Ciencias Naturales (Madrid). 1978; Salesa, 2002; Salesa et al., 2003). We also used published information on modern felid The anatomy of Paramachairodus has been largely anatomy (Barone, 2000; Reinhard & Jennings, 1935; unknown, because it is present in only a few fossil Sisson & Grossman, 1962) and on the morphology of localities such as Pikermi (Greece, MN 12), Maragha other, more derived sabre-toothed cats such as Smilo- (Iran, MN 11) or Eppelsheim (Germany, MN 9) and don fatalis and Homotherium latidens. The latter taxa represented by relatively scarce material. Most ﬁnds were chosen as the ideal reference for comparison with have been of dentitions. While it has long been clear P. ogygia because they exemplify the most derived that Paramachairodus was a sabre-toothed cat, the state for the sabre-toothed adaptations within the absence of more extensive anatomical information has Machairodontinae, whilst P. ogygia occupies a near meant that its machairodont adaptations and wider basal position in the same subfamily. The degree of aspects of its palaeobiology have remained unknown. machairodont adaptations appears to be essentially

FUNCTIONAL MORPHOLOGY OF P. OGYGIA 365 independent of such body size differences as those In the more derived members of this group, the observed between P. ogygia and the referred taxa. paraoccipital process becomes very reduced, almost Differences in the height of the crown of the upper vestigial, and the mastoid process is hyper-developed canines between P. ogygia and reference taxa were (Emerson & Radinsky, 1980), overlapping the auditory assessed using an ANOVA on the index between crown bulla in its growth in some genera such as Smilodon height and basal skull length. All the measured upper (Fig. 1). Thus, the mastoid region of P. ogygia can be canines were unworn specimens. Differences in rela- considered primitive for the Machairodontinae, but it tive elongation of the neck were assessed by calculat- is clearly within the machairodont lineage because its ing an index between the corpus length of the atlas morphology is derived in relation to the earliest felids

and the third cervical vertebra. The lack of associated of the genera Proailurus and Pseudaelurus. There are Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 C3 and atlas of P. ogygia in Batallones-1 was overcome few known basicranial remains of these genera, but in by taking an average measurement between several the Proailurus-like skull from Ginn Quarry (Hunt, isolated C3 and atlas vertebrae and comparing the 1998: fig. 19A), and in the holotype of Pseudaelurus resultant index with similar indices of reference taxa validus (Rothwell, 2001: fig. 3), the paroccipital pro- using a Student’s t-test. These results provided the cess can be seen to be well developed ventrally, sur- most reliable indication of elongation of the neck in passing the level of the mastoid process; this condition the absence of complete, associated cervical series of is also found in fossil and extant species of the Felinae. P. ogygia. The mastoid process is the attachment area for some important muscles directly involved in head- depression movements, such as the brachiocephalicus FUNCTIONAL MORPHOLOGY OF THE SKULL (which has its origin on the humerus), part of the AND MANDIBLE fibres of the sternocephalicus (extending from the GENERAL CRANIAL MORPHOLOGY manubrium of the sternum) and the obliquus capitis anterior (with its origin on the ventrolateral surface of The skull of P. ogygia shows an overall morphology the atlas wings) (Reinhard & Jennings, 1935; Barone, similar to that of a pantherine cat (Figs 1, 6, 11), 2000). The inferred position of these attachments on although there are some differences. The shape of the the cranium of P. ogygia is shown in Figure 2. nasals is neither completely rectangular, as in Smilo- The anteroventral displacement of these attach- don or Homotherium, nor triangular, as in most of the ment areas in the Machairodontinae in relation to the pantherines, but shows an intermediate morphology. Felinae caused by the modification of the mastoid pro- All nuchal, lambdoid and sagittal crests are well cess has an important consequence. The distance developed, and the join between sagittal and frontal between the muscular attachment areas and the crests is situated at the level of the postorbital pro- atlanto-cranial articulation enlarges, resulting in an cesses of the frontal bone, as in pantherines and increase in the length of the lever arm of the flexor felines in general. The zygomatic arch of P. ogygia is muscles of the head (Antón & Galobart, 1999) and broadly similar to that of a pantherine, but with a thus producing a more powerful contraction. postorbital process that is almost vestigial, unlike the Moreover, there is another interesting implication of pantherines in which this process is large and pointed. this displacement of muscle attachment areas. In the The tympanic bullae of P. ogygia are similar to those of primitive model, exemplified by the felines, the main the pantherines. They are rounded, but less inflated function of the obliquus capitis anterior is the exten- than in the latter, and extend from the anterior mar- sion of the head on the atlas (Sisson & Grossman, gin of the mastoid process to the posterior margin of 1962; Barone, 2000). This is because a great number of the postglenoid process. 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. MASTOID AREA In the sabre-toothed cats, most of the fibres of the The morphology of the mastoid region in P. ogygia obliquus capitis anterior are below the point of rota- shows an intermediate condition between that of the tion of the head (Fig. 3B) because of the anteroventral more derived Pleistocene sabre-toothed cats, such as displacement of the mastoid process. The function of Smilodon or Homotherium, and that of the fossil and this muscle is thus ventral flexion of the head, a extant Felinae. The paraoccipital process of P. ogygia motion directly involved in the canine shear-bite is relatively smaller than in the latter, whereas the (Antón et al., 2004b), as discussed further in the final mastoid process has a similar size to that in the section. felines, although it is displaced in an anteroventral The reduction of the paroccipital process in the direction (Fig. 1). This morphology is plesiomorphic for sabre-toothed cats, including P. ogygia, can be related the sabre-toothed cats. to the need to increase the gape of the mandible

366 M. J. SALESA ET AL.

p.p.

p.p. m.p. Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 m.p. ABCm.p.

5 cm D

Figure 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. ogygia from Batallones-1 in left lateral view with mastoid area circled. because of the enlargement of the upper canines. The The morphology of the mastoid region in P. ogygia function of the digastricus muscle, whose insertion shows an early stage of the skull modifications that areas are the paroccipital process and the ventral will reach their maximum development in the later flange of the dentary, is to open the mandible (Sisson Machairodontinae, such as Smilodon or Homothe- & Grossman, 1962; Barone, 2000). If the ventral pro- rium. The remodelling of this area in P. ogygia projection and size of the paramastoid process is reduced, duces an increase in the force generated by the flexor which is the condition shown by sabre-toothed felids, muscles of the head and an increase in the maximum the attachment of this muscle is displaced dorsally, gape of the mandible. These changes suggest that the increasing fibre lengths and thus allowing efficient development of the canine shear-bite, the machairo- contraction at larger gapes (Emerson & Radinsky, dont type of killing bite, had already started in this 1980; Antón & Galobart, 1999). Late Miocene species (Salesa, 2002). This kind of

Ob. Cap. Post. brachiocephalicus Br. Ob. Cap. Ant. rectus capitis Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 lateralis

sterno- digastricus Ob. Cap. Post. cephalicus obliquus capitis anterior B

Figure 2. Inferred areas of muscular attachment on the skull of Paramachairodus ogygia. Br. Ob. Cap. Ant. 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 Figure 3. Anatomical disposition of the muscles brachio- contrast with the feline killing method where the prey cephalicus (Br.), obliquus capitis anterior (Ob. Cap. Ant.) has to be suffocated with a bite in the throat lasting and obliquus capitis posterior (Ob. Cap. Post.) in Felinae several minutes (Turner & Antón, 1997). and Machairodontinae. A, Panthera leo. B, Homotherium These two different hunting methods explain the latidens (artwork by M. Antón). significant differences in the cranial and cervical morphology of the Felinae and Machairodontinae, and they are already present in one of the most primitive correlated with the existence of a high vertical stress machairodonts, P. ogygia (Martin, 1980; Biknevicius in that zone during the canine shear-bite, due in part & van Valkenburgh, 1996; Turner & Antón, 1997; to the use of the mandible as an anchor. The curved Antón & Galobart, 1999). This kind of attack was mandibular symphysis of felines does not suffer such probably developed in parallel by other ‘sabre-toothed’ stress during the attack, because this is achieved with carnivores, such as the Barbourofelines and Thylacos- the maxilla and mandible biting at the same time milinae, and their mastoid anatomy shows some (Biknevicius, van Valkenburgh & Walker, 1996). analogies with that of the true sabre-toothed felids Another possible interpretation, compatible with the (Turner & Antón, 1997; Morales et al., 2001). 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 SYMPHYSIS mandibular corpora, an argument that has been put The mandibular symphysis of P. ogygia is strongly forward to explain the vertically high symphyses of verticalized, forming an almost square angle with the sabre-toothed therapsids (Jenkins, Thomasson & Nor- ventral flange of the mandibular corpus (Fig. 4B). man, 2002). Owing to this verticalization, its anterior surface is It is also possible that the verticalized mandibular flat and describes a distinctive plane. This morphol- symphysis of P. ogygia and other sabre-toothed cats ogy, typical of the sabre-toothed cats (Fig. 4C), is can be explained as a consequence of reorganization in clearly different from the feline model, in which the the alveolar zone of the lower canines. Because of the anteroventral surface of the mandible is gently curved smaller palate width of the sabre-toothed cats relative upwards (Fig. 4A). The morphology of the mandibular to the felines, the lower canines had to become verti- symphysis of P. ogygia can be related to the canine calized to allow occlusion. Nevertheless, it is probable shear-bite, in which the mandible acts as an anchor that both mechanisms acted together, creating the while the head is flexed downwards, sinking the upper specialized symphysis model of the Machairodontinae. canines into the flesh of prey. Some sabre-toothed cat taxa, such as Homotherium This morphological change in the mandibular sym- and Megantereon, developed a mandibular flange, a physis of P. ogygia relative to the feline model can be kind of ventral projection in the symphysis that could

A Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 A

C 5 cm

Figure 4. Left hemimandibles of Felidae showing differences in the development of the mandibular coronoid process. A, Panthera leo. B, Paramachairodus ogygia from Batallones-1. C, Smilodon fatalis from Rancho La Brea.

have been a reinforcement of this area. However, the significance of this structure is not clear, because its absence or presence does not have clear phylogenetic Figure 5. Comparative views of the skull and mandible of or biomechanical implications. For example, within two Smilodontini species. A, Paramachairodus ogygia. B, the tribe Smilodontini, Smilodon, the most strongly Megantereon cultridens (artwork by M. Antón). built among the sabre-toothed cats, does not show this trait and neither does P. ogygia, whereas it is present in Megantereon (Fig. 5). As we pointed out earlier, during the machairodont In summary, the significance of this structure is bite the mandibular symphysis supported a strong unclear, and its absence in P. ogygia clearly did not vertical tension, which seems to be the main evolu- affect the development of a verticalized, derived man- tionary pressure that produced the verticalized sym- dibular symphysis. physis. If the morphology of the mandibular flange is observed in detail, we can see that it is not the thick structure that might be expected in such a biomechani- CORONOID PROCESS cally stressed area. Rather, it is a more or less fragile The coronoid process of the more derived sabre- bony sheet, projected downwards only in the most lat- toothed felids is highly reduced in relation to the feline eral parts of the symphysis. This structure also pattern (Fig. 4A, C) as a consequence of reorganiza- appears in other groups of sabre-toothed carnivorans, tion in the fibres of the temporalis muscle, which such as the marsupial Thylacosmilus atrox and most became longer and more vertical, a change related to of the nimravids, such as Hoplophoneus or Eusmilus. the need to increase the maximum gape (Emerson &

Table 1. Skull and upper canine measurements for Paramachairodus ogygia and nine species of Felinae. Abbreviations: CH, canine height; ML, canine mesiodistal length; BB, canine buccolingual breadth; BL, skull basal length; BL/CH index, index between BL and CH

Number Species CH ML BB BL BL/CH index

- P. tigris 35.98 18.93 14.57 247.35 6.875 - P. tigris 37.12 18.69 14.48 247.35 6.664 2415 P. onca 32.69 16.25 13.30 197.25 6.034 125 P. onca 36.04 17.68 14.43 204.80 5.683 409 P. concolor 24.40 12.02 9.87 176.60 7.238 Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 1599 P. pardus 29.29 14.06 10.80 167.75 5.727 MNCN-4259 P. pardus 28.61 12.36 9.24 157.74 5.513 - U. uncia 30.11 11.93 10.08 156.85 5.209 - N. nebulosa 36.67 12.25 10.30 157.10 4.284 - N. nebulosa 36.30 12.85 10.08 157.10 4.328 MNCN-4060 P. leo 40.89 20.63 14.21 262.30 6.415 MNCN-4060 P. leo 40.90 20.31 14.18 262.30 6.413 275 P. concolor 22.99 11.28 9.11 153.84 6.692 2 P. concolor 27.04 13.42 10.83 171.15 6.330 MNCN-60 L. wiedii 11.99 5.57 3.81 82.41 6.873 MNCN-60 L. wiedii 11.97 5.72 3.87 82.41 6.885 MNCN-16784 L. pardina 16.09 6.49 5.20 91.95 5.715 MNCN-4260 P. leo 46.38 25.04 17.30 310.90 6.700 MNCN-4260 P. leo 45.86 24.84 17.09 310.90 6.780 MNCN-16825 P. leo 48.35 25.43 17.13 320.85 6.640 B-1377 P. ogygia 39.94 --165.55 4.145 B-847 P. ogygia 36.06 --168.15 4.663 B-847 P. ogygia 36.03 15.15 - 168.15 4.667 B-5197 P. ogygia 37.91 15.39 9.41 159.80 4.215 B-5197 P. ogygia 39.84 15.72 - 159.80 4.011 B-4869 P. ogygia 33.25 13.81 - 157.15 4.726

Radinsky, 1980; Martin, 1980; Antón et al., 2004a). odonts may have been more related to changes in the P. ogygia has a coronoid process that is only slightly orientation of the fibres of the temporalis muscle than reduced in comparison with a pantherine cat (Fig. 4B). to changes in the mandibular gape. This morphology is also seen in the contemporaneous sabre-toothed felid Machairodus aphanistus (Antón et al., 2004a) and reflects the primitive pattern of the UPPER CANINES temporalis muscle in these first machairodontines. An index of the basal length of the skull vs. the upper canine crown height was calculated for P. ogygia and nine species of Felinae (Table 1). These data were CONDYLAR PROCESS analysed by ANOVA; the results are given in Table 2. The condylar process of P. ogygia shows a similar It can be seen that there are significant differences orientation to that of the pantherines (Fig. 4A, B) and between both groups, in that P. ogygia has relatively clearly differs from that of Smilodon fatalis (Fig. 4C). longer upper canines than the Felinae. The upper In the more derived sabre-toothed cats, the condylar canines of P. ogygia are also laterally flattened process is orientated posteroventrally, in order to (Fig. 6), whereas in Felinae their section is rounded. allow great gapes, whereas in the pantherines this They also lack crenulations, which is the primitive orientation is posterodorsal. Thus, P. ogygia shows the condition, although these are not present in all sabre- plesiomorphic state of this character, which indicates toothed species. While crenulations in the upper that the gapes produced by its mandible would not be canines would help to penetrate the flesh, their pres- very different from those produced by pantherine cats. ence is obviously a minor requirement in the develop- This morphology of P. ogygia also suggests that the ment of the canine shear-bite, as showed by the changes in the coronoid process of the early machair- absence of this trait in the large upper canines of other

Table 2. Results of ANOVA for BL/CH index in Table 1

Sum of squares d.f. Mean square FP

Between groups 14.056 1 14.056 24,755 0.000 Within groups 13.628 24 0.568 Total 27.684 25 Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 A B

5 cm

C D

Figure 6. Skulls and mandibles of four individuals of Paramachairodus ogygia from Batallones-1. A, B-847. B, B-4322. C, B-4778. D, B-7022.

sabre-toothed cat such as Megantereon, a more FUNCTIONAL MORPHOLOGY OF CERVICAL VERTEBRAE derived species than P. ogygia. The possession of ﬂattened and elongated upper The atlas wings of P. ogygia project backward a little canines is a clear machairodont trait, and its presence more than in the pantherines, but not as far as in in P. ogygia is enough for us to infer that this species other, more derived sabre-toothed cats such as had already developed the specialized hunting method Homotherium or Smilodon, in which this posterior of this group. If P. ogygia tried to kill prey as felines projection is extreme (Fig. 7). This morphology do, with either a nape bite or a suffocating bite, then increases the breadth and ﬁbre length of the obliquus either violent contact with bone or the lateral motions capitis anterior (Fig. 8), which runs from the ventral of the struggling prey could have caused breakage of surface of the atlas wings to the mastoid process, and the upper canines, which were inherently more fragile the obliquus capitis posterior, which extends from the than the rounded-section upper canines of a feline dorsal surface of the atlas wings to the lateral surface (Emerson & Radinsky, 1980; Turner & Antón, 1997; of the spinous process of the axis (Fig. 8) (Barone, Antón & Galobart, 1999). 2000; Salesa, 2002; Antón et al., 2004b). In more

Table 3. Atlas and third vertebra (C3) measurements for A B Paramachairodus ogygia, six species of Felinae and the viverrid Genetta genetta. Abbreviations: VCL. vertebral corpus length; C3/AT index, index between vertebral corpus length of C3 and Atlas. The specimens of P. ogygia do not correspond to single individuals, so the index was calculated with the average of each VCL, 38.60 for Atlas, and 3 cm 26.62 for C3

C3/AT Number Element Species VCL index Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020

B-3874 (1) Atlas P. ogygia 39.51 B-4914 Atlas P. ogygia 41.69 B-1274 Atlas P. ogygia 36.28 B-4318 Atlas P. ogygia 38.78 B-ss Atlas P. ogygia 36.76 B-4318c C3 P. ogygia 24.71 C B-744 (5) C3 P. ogygia 28.53 0.690 2440 Atlas P. pardus 44.95 2440 C3 P. pardus 24.19 0.538 1599 Atlas P. pardus 42.76 Figure 7. Development of the atlas wings in dorsal view. 1599 C3 P. pardus 21.37 0.500 A, Panthera pardus. B, Paramachairodus ogygia, a 2415 Atlas P. onca 45.39 specimen with an associated axis, before preparation. 2415 C3 P. onca 22.77 0.502 C, Smilodon fatalis from Rancho La Brea (modiﬁed from 125 Atlas P. onca 49.80 Merriam & Stock, 1932). 125 C3 P. onca 25.80 0.518 409 Atlas P. concolor 41.29 409 C3 P. concolor 21.01 0.509 obliquus capitis 275 Atlas P. concolor 39.25 anterior 275 C3 P. concolor 22.91 0.584 obliquus capitis - Atlas P. tigris 60.35 posterior - C3 P. tigris 29.40 0.487 MNCN-16810 Atlas L. pardina 21.70 MNCN-16810 C3 L. pardina 9.66 0.445 1518 Atlas C. caracal 23.25 1518 C3 C. caracal 13.82 0.594 MNCN-14233 Atlas G. genetta 15.62 brachiocephalicus MNCN-14233 C3 G. genetta 12.72 0.814

Figure 8. Composite reconstruction of the skull, mandible and cervical vertebrae of Paramachairodus ogygia, based produces an increase in their contraction strength. In on material of several individuals from Batallones-1, show- addition, the increased distance between the origin and ing the inferred position of the main cranio-cervical mus- insertion of these muscles produces a lengthening of the cles relevant to the canine shear-bite (artwork by M. lever arm, which also serves to increase the strength of Antón). action (Akersten, 1985; Antón & Galobart, 1999). In P. ogygia, the third to seventh cervical vertebrae seem to be long in relation to those of the pantherine derived machairodonts, such as Smilodon and cats (Figs 9, 10). To assess this, an index between the Homotherium, this process of the axis is lengthened corpus length of C3 and atlas was calculated for posteriorly, which also increases the breadth of the P. ogygia, Genetta genetta and six species of Felinae obliquus capitis posterior. Nevertheless, the spinous (Table 3), and these data analysed with a Student’s t- process in P. ogygia has a pantherine-like morphology, test. P. ogygia shows a low sexual dimorphism index with little backward projection, thus showing a (Salesa, 2002) and the selected vertebrae used in the primitive state for this character. analysis were all very similar in size. The result is The enlargement in the breadth of the muscles shown in Table 4, demonstrating that there are signiﬁ- involved in the ﬂexion and lateral rotation of the head cant differences between P. ogygia and Felinae, such

© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 372 M. J. SALESA ET AL. Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020

5 cm A

Figure 9. Photographs of ﬁrst to seventh cervical vertebrae (C1-C7) (anterior to left) in dorsal view. A, Paramachairodus ogygia from Batallones-1, respectively, B-4561, B-5407, B-744 (5), B-5458, B-5459, B-707 (12) and B-707 (12) (the latter have the same number); B, Panthera pardus, 1599.

Table 4. Results of Student’s t-test for C3/AT index of can be related to the necessity for greater accuracy in Table 3 the neck movements during the canine shear-bite (Schaub, 1925; Ballesio, 1963; Turner & Antón, 1997; Sig. Mean Antón & Galobart, 1999). However, since primitive t-test d.f. (2-tailed) difference viverrids such as G. genetta also have long necks, this trait could be a primitive character retained by sabre- C3/AT index -10.939 8 0.000 -0.170 toothed cats. Greater knowledge of cervical morphology in early felids, such as Proailurus and Pseudaelurus, is necessary in order to settle this issue. that P. ogygia has a longer C3 in relation to the atlas In Homotherium and Smilodon, a clear reinforcement than the Felinae. G. genetta also shows signiﬁcant dif- in the transverse processes of the cervical vertebrae ferences in this index. can also be observed in addition to this cervical length- As several authors have discussed, a long neck is a ening. These processes are the insertion areas of the trait typical of the more derived machairodonts, and scalenus and longus capitis (Antón & Galobart, 1999),

© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 FUNCTIONAL MORPHOLOGY OF P. OGYGIA 373 Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020

5 cm A

Figure 10. Photographs of the first to seventh cervical vertebrae (C1-C7) (anterior to left) in Fig. 9, in lateral view. A, Paramachairodus ogygia from Batallones-1. B, Panthera pardus. the main flexors of the neck (Barone, 2000). P. ogygia which reach their highest development in the more does not show this change, its transverse processes derived sabre-toothed felids of the Plio-Pleistocene being very similar in size and morphology to those of such as Homotherium and Smilodon, can be summa- the pantherine cats. rized as follows: In summary, the neck morphology of P. ogygia shows 1. Presence of elongated and flattened upper canines. a combination of some machairodont traits, such as 2. Verticalization of the mandibular symphysis. the lengthening of the whole vertebrae, and primitive 3. Reduction of the coronoid process of the mandible. ones, such as the small backwards projection of the 4. Enlargement and anteroventral displacement of atlas wings and the overall morphology of the cervical the mastoid process. vertebrae. 5. Reduction of the paroccipital process. 6. Strong backwards projection of the atlas wings and PALAEOETHOLOGICAL IMPLICATIONS lengthening of the spinous process of the axis. 7. Lengthening of the corpus of the cervical vertebrae. The morphology of the skull and cervical region in 8. Enlargement of the transverse processes of the cer- P. ogygia shows the beginning of the typical adapta- vical vertebrae. tions of the Machairodontinae, which are closely related to the highly specialized killing method of this As described above, P. ogygia shows a clear develop- group by means of the so-called canine shear-bite ment of characters 1 and 2 only; characters 3, 4, 5 and (Akersten, 1985). These cranio-cervical modifications, 7 are only moderately derived relative to the feline

© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 374 M. J. SALESA ET AL. model, while character 6 is very moderately expressed atlas wings, remained in a relatively primitive state. and character 8 is not present. Nevertheless, this morphological mosaic reveals that Although P. ogygia did not develop a complete the most important aspects of the canine shear-bite machairodont cranio-cervical plan, the presence of were the flattened upper canines and the verticalized elongated and flattened upper canines undoubtedly symphyseal morphology, which are directly related to points towards the canine shear-bite as the prey- the cutting-action and to stabilization of the bite. killing method. The extant felines kill with either a Other aspects, such as the strength of the head flexor prolonged bite to the throat or muzzle of prey, result- muscles, seem to have been less critical and were fur- ing in its strangulation or suffocation (Schaller, 1972; ther emphasized only later in evolution.

Turner & Antón, 1997; Antón et al., 2004b), or with a What does this morphology mean in the context of Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 strong bite to the nape, which causes death by break- machairodont palaeoethology? P. ogygia had devel- ing the skull or spinal cord (Leyhausen, 1979; Turner oped the main morphological traits for the canine & Antón, 1997). shear-bite, but it was also far from the highly derived The first method is used with large prey, whereas pattern shown by the latest sabre-toothed cats. There the second is only applied to small animals, which are several behavioural implications of the differences have cranial bones fragile enough to avoid damaging between P. ogygia and both the pantherines and the the canines of the predator (Seidensticker & McDou- crown machairodontines. For example, if we compare gal, 1993). If sabre-toothed cats tried to kill their prey the morphology of the skull and neck in P. ogygia with with these feline techniques, the long and flattened the superficially similar extant clouded leopard, upper canines would probably have been broken, Neofelis nebulosa (Fig. 11), we find that the pan- either by hitting bone or because of the lateral ten- therine cat has an overall skull morphology compara- sions caused by the struggling of prey during the bite ble to that of the machairodont, with upper canines (Emerson & Radinsky, 1980; Turner & Antón, 1997; also of comparable crown height. However, in the Antón & Galobart, 1999). extant species the upper canines are not flattened, the Consequently, the upper canines of the sabre- mandibular symphysis is not as verticalized, the toothed cats were likely to have been used in a differ- mastoid process remains primitively small and with- ent way, and were probably developed to bite the out ventral projection, while the length of the neck is throat of the prey with a head flexion movement that typical for a pantherine (Gonyea, 1976b). This set of cut blood vessels and trachea, thus producing rapid differences is enough to indicate the presence of cor- death through combined suffocation and rapid blood responding differences in killing behaviour, with the loss. During this motion, the mandible acted as an clouded leopard using a typical pantherine bite and anchor. That would be the reason why the morphology the early machairodont already relying more heavily of the mandibular symphysis developed into a verti- on the immobilization and quick killing of prey calized and stabilizing border. The use of the machair- through blood loss. odonts’ powerful forepaws for the immobilization of However, if we compare P. ogygia with Megantereon prey during the bite further contributed to protecting (a derived Plio-Pleistocene machairodontine, between the fragile upper canines from violent lateral tensions a leopard and a jaguar in size and possibly descended (Rawn-Schatzinger, 1992; Lewis, 1997; Turner & from Paramachairodus), the main behavioural differ- Antón, 1997). ences would be that the younger taxon would kill prey In general, all cranial modifications of sabre-toothed even faster and more efficiently than P. ogygia, and cats can be seen as related to their specialized hunting would also have had access to relatively larger prey. If and killing method. Thus the hyper-development of they had been sympatric, then both sabre-toothed the mastoid process and the backwards projection of taxa would have been in direct competition for the atlas wings increased the leverage arm and resources due to their overlapping body sizes. Both strength of the head flexor muscles, while the dorsal species would also have shared similar solitary habits displacement of the paroccipital process and the and a preference for wooded environments, as reduction of the coronoid process increased the inferred from aspects of their body proportions that maximum gape. Other modifications contributed to have been shown to be related to ambush hunting reinforce the neck, mandible and skull in order to (Kurtén, 1968; Van Valkenburgh, 1987; Marean, 1989; withstand the development of powerful forces during Turner & Antón, 1997; Agustí & Antón, 2002; Salesa, the kill. 2002) and to closed-habitat preferences in felids (Gon- The cranio-mandibular morphology of P. ogygia yea, 1976a, b). shows that this species had developed some important In the event of hypothetical direct competition, machairodont traits, such as the elongated and flat- Megantereon would have been at a distinct advantage tened upper canines and verticalized mandibular sym- because of its more efficient machairodont adapta- physis. Other regions, such as the mastoid area and tions. However, in the Vallesian of Eurasia, P. ogygia

suffered the highest pressure, although improvement of the other structures involved in the bite was A achieved by later species. Another useful comparison can be made with the Metailurini, a separate tribe within the Machairodon- tinae, which also demonstrates a mosaic evolution of the sabre-toothed adaptations but with a lesser development of derived characters. This group was initially characterized by the presence of moderately ﬂattened

upper canines, whilst the cranio-mandibular morphol- Downloaded from https://academic.oup.com/zoolinnean/article-abstract/144/3/363/2627519 by guest on 18 May 2020 ogy remained primitive, similar to that of the feline cats. Only in the latest Plio-Pleistocene species of the group do we see the appearance of more derived machairodont features (Werdelin & Lewis, 2001). It has been proposed that the machairodont method of attack was developed to hunt prey relatively larger than those of the felines (Gonyea, 1976a; Emerson & B Radinsky, 1980; Akersten, 1985; Rawn-Schatzinger, 1992; Turner & Antón, 1997). With their strong forepaws, the sabre-toothed cats would have been able to overpower large animals such as horses, giraffes or bovids, in order to apply a rapid and mortal cutting bite to the throat, instead of the prolonged bite of the felines. This is a quicker and safer way to kill such animals, because the time of contact with the living prey is shortened. However, the body weight of P. ogygia has been esti- mated at between 28 and 65 kg (Salesa, 2002), which Figure 11. Comparative views of the skull and mandible is within the range of an extant puma, Puma concolor. of (A) Neofelis nebulosa, and (B) Paramachairodus ogygia At this size, it is difficult to imagine this felid as a (artwork by M. Antón). hunter of very large animals, and the use of the canine shear-bite to kill prey quickly, thus reducing the energy expended in hunting activities and the contact was without competition in its leopard-like niche, and time needed to ensure a kill, is a more reasonable its hunting techniques, basically similar to if less interpretation. Nevertheless, the evolution of refined than those of later machairodonts, would have machairodonts produced such large and often strongly been enough for efficient deployment of the canine built animals that the latest species of this group shear-bite. This in turn would have allowed it to dis- (Smilodon and Homotherium) were probably able to patch prey sufficiently quickly to gain precious time hunt relatively larger prey than the pantherines before it attracted the undesired attention of compet- (Lewis, 1997; Turner & Antón, 1997). itors and potential kleptoparasites such as amphicy- In summary, reducing the risk during hunting activ- onids, large hyaenids and the lion-sized sabre-toothed ities is very important for all predators, because any cats of the genus Machairodus. It is in this general tooth or bone breakage or wound will drastically palaeoecological context that the success of the early reduce the capacity to hunt and may lead to starvation machairodont adaptations of P. ogygia should be and death. We suggest that this ecological constraint understood. was the main pressure that led to the appearance of Paramachairodus ogygia is a good example of the the sabre-toothed cat model. mosaic evolution of the first sabre-toothed cats, and demonstrates how this new model of felids may have ACKNOWLEDGEMENTS originated. It is interesting that another early machairodont, the lion-sized Machairodus aphanistus, The authors thank Dr Francisco Pastor (Facultad de shows a comparable pattern of mosaic morphology in Medicina, Universidad de Valladolid, Spain), for skull and mandible (Antón et al., 2004a). Thus the kindly loaning the extant specimens for comparison. early acquisition of flattened and elongated upper This study is part of the research project BTE2002- canines in these primitive sabre-toothed cats was 00410 (Dirección General de Investigación-MCYT) accompanied by the reinforcement of the areas that and EX2003-0243 (Secretaría de Estado de Educación

© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377 376 M. J. SALESA ET AL. y Universidades del MECD). We thank the Comu- Félidés (Carnivores). Archives des Sciences Physiques et nidad Autónoma de Madrid (Dirección General de Pat- Naturelles, Genève 31 (3): 219–227. rimonio Histórico) for continuous funding support and Biknevicius AR, van Valkenburgh B. 1996. Design for kill- research permissions. A.T. thanks the British Council ing: craniodental adaptations of mammalian predators. In: for travel funding. Additional support was provided by Gittleman JL, ed. Carnivore behavior, ecology and evolution, the National Geographic Society (Grant 6964–01). We Vol. 2. London: Cornell University Press, 393–428. also thank an anonymous referee, whose comments Biknevicius AR, van Valkenburgh B, Walker J. 1996. Inci- improved the quality of the manuscript. sor size and shape: implications for feeding behaviors in saber-toothed cats. 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