Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The
nean Society of London, 2005? 2005
1443
363377
Original Article
Lin-
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
1
School of Biological & Earth Sciences, Byrom Street, Liverpool John Moores University, Liverpool,
L3 3AF, UK
2
Departamento 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
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-
*Corresponding author. E-mail: [email protected]
straint in each group, still remain essentially a
mystery.
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
© 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).
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. ogygia (Kaup,
1832), of Vallesian-Early Turolian age (MN 9–11 of
Mein, 1975) and P. orientalis (Kittl, 1887) of Turolian
age (MN 11–13), distinguished by several dental
traits. The more primitive species, P. ogygia, had noncrenulated upper canines, a P4 without ectostyle and
with a strong protocone, and a P3 with a posterointernal expansion. P. orientalis had crenulated upper
canines, a P4 with a well marked ectostyle as well as a
reduced, backwardly displaced protocone and a P 3
reduced in size and without posterointernal expansion
(Salesa et al., 2003).
In 1924, Zdansky created the species P. maximiliani
for a damaged skull from the Late Miocene of China.
The differences between this third species and
P. orientalis are largely confined to the more curved
upper canines of P. maximiliani, 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. maximiliani is a
synonym of P. orientalis (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.
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. ogygia, 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 aphanistus, 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).
In this paper we present a functional analysis of the
cranial, mandibular and cervical anatomy of P. ogygia,
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 nebulosa, Caracal caracal, Lynx pardina and Puma concolor, 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 Smilodon fatalis and Homotherium latidens. The latter taxa
were chosen as the ideal reference for comparison with
P. ogygia because they exemplify the most derived
state for the sabre-toothed adaptations within the
Machairodontinae, whilst P. ogygia 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. OGYGIA
independent of such body size differences as those
observed between P. ogygia and the referred taxa.
Differences in the height of the crown of the upper
canines between P. ogygia 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. ogygia 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. ogygia.
FUNCTIONAL MORPHOLOGY OF THE SKULL
AND MANDIBLE
GENERAL
CRANIAL MORPHOLOGY
The skull of P. ogygia 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 Smilodon 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. ogygia 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. ogygia 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. ogygia
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. ogygia
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.
365
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. ogygia 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. ogygia 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.
The reduction of the paroccipital process in the
sabre-toothed cats, including P. ogygia, 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.
A
B
m.p.
5 cm
m.p.
C
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
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. ogygia
shows an early stage of the skull modifications that
will reach their maximum development in the later
Machairodontinae, such as Smilodon or Homotherium. The remodelling of this area in P. ogygia 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. OGYGIA
367
A
Ob. Cap. Post.
brachiocephalicus
Br.
Ob. Cap. Ant.
rectus capitis
lateralis
sternocephalicus
digastricus
obliquus capitis
anterior
Ob. Cap. Post.
B
Figure 2. Inferred areas of muscular attachment on the
skull of Paramachairodus ogygia.
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. ogygia (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).
MANDIBULAR
SYMPHYSIS
The mandibular symphysis of P. ogygia 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. ogygia 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. ogygia relative to the feline model can be
Ob. Cap. Ant.
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. ogygia 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
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377
368
M. J. SALESA ET AL.
A
A
B
B
5 cm
C
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
or biomechanical implications. For example, within
the tribe Smilodontini, Smilodon, the most strongly
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
bite the mandibular symphysis supported a strong
vertical tension, which seems to be the main evolutionary pressure that produced the verticalized symphysis. 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 biomechanically stressed area. Rather, it is a more or less fragile
bony sheet, projected downwards only in the most lateral parts of the symphysis. This structure also
appears in other groups of sabre-toothed carnivorans,
such as the marsupial Thylacosmilus atrox and most
of the nimravids, such as Hoplophoneus or Eusmilus.
Figure 5. Comparative views of the skull and mandible of
two Smilodontini species. A, Paramachairodus ogygia. B,
Megantereon cultridens (artwork by M. Antón).
In summary, the significance of this structure is
unclear, and its absence in P. ogygia clearly did not
affect the development of a verticalized, derived mandibular symphysis.
CORONOID
PROCESS
The coronoid process of the more derived sabretoothed felids is highly reduced in relation to the feline
pattern (Fig. 4A, C) as a consequence of reorganization in the fibres of the temporalis muscle, which
became longer and more vertical, a change related to
the need to increase the maximum gape (Emerson &
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377
FUNCTIONAL MORPHOLOGY OF P. OGYGIA
369
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
2415
125
409
1599
MNCN-4259
MNCN-4060
MNCN-4060
275
2
MNCN-60
MNCN-60
MNCN-16784
MNCN-4260
MNCN-4260
MNCN-16825
B-1377
B-847
B-847
B-5197
B-5197
B-4869
P. tigris
P. tigris
P. onca
P. onca
P. concolor
P. pardus
P. pardus
U. uncia
N. nebulosa
N. nebulosa
P. leo
P. leo
P. concolor
P. concolor
L. wiedii
L. wiedii
L. pardina
P. leo
P. leo
P. leo
P. ogygia
P. ogygia
P. ogygia
P. ogygia
P. ogygia
P. ogygia
35.98
37.12
32.69
36.04
24.40
29.29
28.61
30.11
36.67
36.30
40.89
40.90
22.99
27.04
11.99
11.97
16.09
46.38
45.86
48.35
39.94
36.06
36.03
37.91
39.84
33.25
18.93
18.69
16.25
17.68
12.02
14.06
12.36
11.93
12.25
12.85
20.63
20.31
11.28
13.42
5.57
5.72
6.49
25.04
24.84
25.43
15.15
15.39
15.72
13.81
14.57
14.48
13.30
14.43
9.87
10.80
9.24
10.08
10.30
10.08
14.21
14.18
9.11
10.83
3.81
3.87
5.20
17.30
17.09
17.13
9.41
-
247.35
247.35
197.25
204.80
176.60
167.75
157.74
156.85
157.10
157.10
262.30
262.30
153.84
171.15
82.41
82.41
91.95
310.90
310.90
320.85
165.55
168.15
168.15
159.80
159.80
157.15
6.875
6.664
6.034
5.683
7.238
5.727
5.513
5.209
4.284
4.328
6.415
6.413
6.692
6.330
6.873
6.885
5.715
6.700
6.780
6.640
4.145
4.663
4.667
4.215
4.011
4.726
Radinsky, 1980; Martin, 1980; Antón et al., 2004a).
P. ogygia has a coronoid process that is only slightly
reduced in comparison with a pantherine cat (Fig. 4B).
This morphology is also seen in the contemporaneous
sabre-toothed felid Machairodus aphanistus (Antón
et al., 2004a) and reflects the primitive pattern of the
temporalis muscle in these first machairodontines.
CONDYLAR
PROCESS
The condylar process of P. ogygia shows a similar
orientation to that of the pantherines (Fig. 4A, B) and
clearly differs from that of Smilodon fatalis (Fig. 4C).
In the more derived sabre-toothed cats, the condylar
process is orientated posteroventrally, in order to
allow great gapes, whereas in the pantherines this
orientation is posterodorsal. Thus, P. ogygia shows the
plesiomorphic state of this character, which indicates
that the gapes produced by its mandible would not be
very different from those produced by pantherine cats.
This morphology of P. ogygia also suggests that the
changes in the coronoid process of the early machair-
odonts may have been more related to changes in the
orientation of the fibres of the temporalis muscle than
to changes in the mandibular gape.
UPPER
CANINES
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
analysed by ANOVA; the results are given in Table 2.
It can be seen that there are significant differences
between both groups, in that P. ogygia has relatively
longer upper canines than the Felinae. The upper
canines of P. ogygia are also laterally flattened
(Fig. 6), whereas in Felinae their section is rounded.
They also lack crenulations, which is the primitive
condition, although these are not present in all sabretoothed species. While crenulations in the upper
canines would help to penetrate the flesh, their presence is obviously a minor requirement in the development of the canine shear-bite, as showed by the
absence of this trait in the large upper canines of other
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377
370
M. J. SALESA ET AL.
Table 2. Results of ANOVA for BL/CH index in Table 1
Between groups
Within groups
Total
Sum of squares
d.f.
Mean square
F
P
14.056
13.628
27.684
1
24
25
14.056
0.568
24,755
0.000
B
A
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
derived species than P. ogygia.
The possession of flattened and elongated upper
canines is a clear machairodont trait, and its presence
in P. ogygia is enough for us to infer that this species
had already developed the specialized hunting method
of this group. If P. ogygia tried to kill prey as felines
do, with either a nape bite or a suffocating bite, then
either violent contact with bone or the lateral motions
of the struggling prey could have caused breakage of
the upper canines, which were inherently more fragile
than the rounded-section upper canines of a feline
(Emerson & Radinsky, 1980; Turner & Antón, 1997;
Antón & Galobart, 1999).
FUNCTIONAL
MORPHOLOGY OF CERVICAL VERTEBRAE
The atlas wings of P. ogygia project backward a little
more than in the pantherines, but not as far as in
other, more derived sabre-toothed cats such as
Homotherium or Smilodon, in which this posterior
projection is extreme (Fig. 7). This morphology
increases the breadth and fibre length of the obliquus
capitis anterior (Fig. 8), which runs from the ventral
surface of the atlas wings to the mastoid process, and
the obliquus capitis posterior, which extends from the
dorsal surface of the atlas wings to the lateral surface
of the spinous process of the axis (Fig. 8) (Barone,
2000; Salesa, 2002; Antón et al., 2004b). In more
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FUNCTIONAL MORPHOLOGY OF P. OGYGIA
B
A
3 cm
C
Figure 7. Development of the atlas wings in dorsal view.
A, Panthera pardus. B, Paramachairodus ogygia, a
specimen with an associated axis, before preparation.
C, Smilodon fatalis from Rancho La Brea (modified from
Merriam & Stock, 1932).
obliquus capitis
anterior
obliquus capitis
posterior
brachiocephalicus
Figure 8. Composite reconstruction of the skull, mandible
and cervical vertebrae of Paramachairodus ogygia, based
on material of several individuals from Batallones-1, showing the inferred position of the main cranio-cervical muscles relevant to the canine shear-bite (artwork by M.
Antón).
derived machairodonts, such as Smilodon and
Homotherium, this process of the axis is lengthened
posteriorly, which also increases the breadth of the
obliquus capitis posterior. Nevertheless, the spinous
process in P. ogygia has a pantherine-like morphology,
with little backward projection, thus showing a
primitive state for this character.
The enlargement in the breadth of the muscles
involved in the flexion and lateral rotation of the head
371
Table 3. Atlas and third vertebra (C3) measurements for
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
26.62 for C3
Number
Element
Species
VCL
B-3874 (1)
B-4914
B-1274
B-4318
B-ss
B-4318c
B-744 (5)
2440
2440
1599
1599
2415
2415
125
125
409
409
275
275
MNCN-16810
MNCN-16810
1518
1518
MNCN-14233
MNCN-14233
Atlas
Atlas
Atlas
Atlas
Atlas
C3
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
Atlas
C3
P. ogygia
P. ogygia
P. ogygia
P. ogygia
P. ogygia
P. ogygia
P. ogygia
P. pardus
P. pardus
P. pardus
P. pardus
P. onca
P. onca
P. onca
P. onca
P. concolor
P. concolor
P. concolor
P. concolor
P. tigris
P. tigris
L. pardina
L. pardina
C. caracal
C. caracal
G. genetta
G. genetta
39.51
41.69
36.28
38.78
36.76
24.71
28.53
44.95
24.19
42.76
21.37
45.39
22.77
49.80
25.80
41.29
21.01
39.25
22.91
60.35
29.40
21.70
9.66
23.25
13.82
15.62
12.72
C3/AT
index
0.690
0.538
0.500
0.502
0.518
0.509
0.584
0.487
0.445
0.594
0.814
produces an increase in their contraction strength. In
addition, the increased distance between the origin and
insertion of these muscles produces a lengthening of the
lever arm, which also serves to increase the strength of
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
cats (Figs 9, 10). To assess this, an index between the
corpus length of C3 and atlas was calculated for
P. ogygia, Genetta genetta and six species of Felinae
(Table 3), and these data analysed with a Student’s ttest. P. ogygia shows a low sexual dimorphism index
(Salesa, 2002) and the selected vertebrae used in the
analysis were all very similar in size. The result is
shown in Table 4, demonstrating that there are significant 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.
5 cm
A
B
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
Table 3
C3/AT index
t-test
d.f.
Sig.
(2-tailed)
Mean
difference
-10.939
8
0.000
-0.170
that P. ogygia has a longer C3 in relation to the atlas
than the Felinae. G. genetta also shows significant differences in this index.
As several authors have discussed, a long neck is a
trait typical of the more derived machairodonts, and
can be related to the necessity for greater accuracy in
the neck movements during the canine shear-bite
(Schaub, 1925; Ballesio, 1963; Turner & Antón, 1997;
Antón & Galobart, 1999). However, since primitive
viverrids such as G. genetta also have long necks, this
trait could be a primitive character retained by sabretoothed cats. Greater knowledge of cervical morphology in early felids, such as Proailurus and
Pseudaelurus, is necessary in order to settle this issue.
In Homotherium and Smilodon, a clear reinforcement
in the transverse processes of the cervical vertebrae
can also be observed in addition to this cervical lengthening. These processes are the insertion areas of the
scalenus and longus capitis (Antón & Galobart, 1999),
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FUNCTIONAL MORPHOLOGY OF P. OGYGIA
5 cm
373
A
B
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
does not show this change, its transverse processes
being very similar in size and morphology to those of
the pantherine cats.
In summary, the neck morphology of P. ogygia shows
a combination of some machairodont traits, such as
the lengthening of the whole vertebrae, and primitive
ones, such as the small backwards projection of the
atlas wings and the overall morphology of the cervical
vertebrae.
which reach their highest development in the more
derived sabre-toothed felids of the Plio-Pleistocene
such as Homotherium and Smilodon, can be summarized as follows:
1.
2.
3.
4.
5.
6.
PALAEOETHOLOGICAL IMPLICATIONS
The morphology of the skull and cervical region in
P. ogygia shows the beginning of the typical adaptations of the Machairodontinae, which are closely
related to the highly specialized killing method of this
group by means of the so-called canine shear-bite
(Akersten, 1985). These cranio-cervical modifications,
7.
8.
Presence of elongated and flattened upper canines.
Verticalization of the mandibular symphysis.
Reduction of the coronoid process of the mandible.
Enlargement and anteroventral displacement of
the mastoid process.
Reduction of the paroccipital process.
Strong backwards projection of the atlas wings and
lengthening of the spinous process of the axis.
Lengthening of the corpus of the cervical vertebrae.
Enlargement of the transverse processes of the cervical vertebrae.
As described above, P. ogygia shows a clear development of characters 1 and 2 only; characters 3, 4, 5 and
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
and character 8 is not present.
Although P. ogygia did not develop a complete
machairodont cranio-cervical plan, the presence of
elongated and flattened upper canines undoubtedly
points towards the canine shear-bite as the preykilling method. The extant felines kill with either a
prolonged bite to the throat or muzzle of prey, resulting in its strangulation or suffocation (Schaller, 1972;
Turner & Antón, 1997; Antón et al., 2004b), or with a
strong bite to the nape, which causes death by breaking the skull or spinal cord (Leyhausen, 1979; Turner
& Antón, 1997).
The first method is used with large prey, whereas
the second is only applied to small animals, which
have cranial bones fragile enough to avoid damaging
the canines of the predator (Seidensticker & McDougal, 1993). If sabre-toothed cats tried to kill their prey
with these feline techniques, the long and flattened
upper canines would probably have been broken,
either by hitting bone or because of the lateral tensions caused by the struggling of prey during the bite
(Emerson & Radinsky, 1980; Turner & Antón, 1997;
Antón & Galobart, 1999).
Consequently, the upper canines of the sabretoothed cats were likely to have been used in a different way, and were probably developed to bite the
throat of the prey with a head flexion movement that
cut blood vessels and trachea, thus producing rapid
death through combined suffocation and rapid blood
loss. During this motion, the mandible acted as an
anchor. That would be the reason why the morphology
of the mandibular symphysis developed into a verticalized and stabilizing border. The use of the machairodonts’ powerful forepaws for the immobilization of
prey during the bite further contributed to protecting
the fragile upper canines from violent lateral tensions
(Rawn-Schatzinger, 1992; Lewis, 1997; Turner &
Antón, 1997).
In general, all cranial modifications of sabre-toothed
cats can be seen as related to their specialized hunting
and killing method. Thus the hyper-development of
the mastoid process and the backwards projection of
the atlas wings increased the leverage arm and
strength of the head flexor muscles, while the dorsal
displacement of the paroccipital process and the
reduction of the coronoid process increased the
maximum gape. Other modifications contributed to
reinforce the neck, mandible and skull in order to
withstand the development of powerful forces during
the kill.
The cranio-mandibular morphology of P. ogygia
shows that this species had developed some important
machairodont traits, such as the elongated and flattened upper canines and verticalized mandibular symphysis. Other regions, such as the mastoid area and
atlas wings, remained in a relatively primitive state.
Nevertheless, this morphological mosaic reveals that
the most important aspects of the canine shear-bite
were the flattened upper canines and the verticalized
symphyseal morphology, which are directly related to
the cutting-action and to stabilization of the bite.
Other aspects, such as the strength of the head flexor
muscles, seem to have been less critical and were further emphasized only later in evolution.
What does this morphology mean in the context of
machairodont palaeoethology? P. ogygia had developed the main morphological traits for the canine
shear-bite, but it was also far from the highly derived
pattern shown by the latest sabre-toothed cats. There
are several behavioural implications of the differences
between P. ogygia and both the pantherines and the
crown machairodontines. For example, if we compare
the morphology of the skull and neck in P. ogygia with
the superficially similar extant clouded leopard,
Neofelis nebulosa (Fig. 11), we find that the pantherine cat has an overall skull morphology comparable to that of the machairodont, with upper canines
also of comparable crown height. However, in the
extant species the upper canines are not flattened, the
mandibular symphysis is not as verticalized, the
mastoid process remains primitively small and without ventral projection, while the length of the neck is
typical for a pantherine (Gonyea, 1976b). This set of
differences is enough to indicate the presence of corresponding differences in killing behaviour, with the
clouded leopard using a typical pantherine bite and
the early machairodont already relying more heavily
on the immobilization and quick killing of prey
through blood loss.
However, if we compare P. ogygia with Megantereon
(a derived Plio-Pleistocene machairodontine, between
a leopard and a jaguar in size and possibly descended
from Paramachairodus), the main behavioural differences would be that the younger taxon would kill prey
even faster and more efficiently than P. ogygia, and
would also have had access to relatively larger prey. If
they had been sympatric, then both sabre-toothed
taxa would have been in direct competition for
resources due to their overlapping body sizes. Both
species would also have shared similar solitary habits
and a preference for wooded environments, as
inferred from aspects of their body proportions that
have been shown to be related to ambush hunting
(Kurtén, 1968; Van Valkenburgh, 1987; Marean, 1989;
Turner & Antón, 1997; Agustí & Antón, 2002; Salesa,
2002) and to closed-habitat preferences in felids (Gonyea, 1976a, b).
In the event of hypothetical direct competition,
Megantereon would have been at a distinct advantage
because of its more efficient machairodont adaptations. However, in the Vallesian of Eurasia, P. ogygia
© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 144, 363–377
FUNCTIONAL MORPHOLOGY OF P. OGYGIA
A
B
Figure 11. Comparative views of the skull and mandible
of (A) Neofelis nebulosa, and (B) Paramachairodus ogygia
(artwork by M. Antón).
was without competition in its leopard-like niche, and
its hunting techniques, basically similar to if less
refined than those of later machairodonts, would have
been enough for efficient deployment of the canine
shear-bite. This in turn would have allowed it to dispatch prey sufficiently quickly to gain precious time
before it attracted the undesired attention of competitors and potential kleptoparasites such as amphicyonids, large hyaenids and the lion-sized sabre-toothed
cats of the genus Machairodus. It is in this general
palaeoecological context that the success of the early
machairodont adaptations of P. ogygia should be
understood.
Paramachairodus ogygia is a good example of the
mosaic evolution of the first sabre-toothed cats, and
demonstrates how this new model of felids may have
originated. It is interesting that another early
machairodont, the lion-sized Machairodus aphanistus,
shows a comparable pattern of mosaic morphology in
skull and mandible (Antón et al., 2004a). Thus the
early acquisition of flattened and elongated upper
canines in these primitive sabre-toothed cats was
accompanied by the reinforcement of the areas that
375
suffered the highest pressure, although improvement
of the other structures involved in the bite was
achieved by later species.
Another useful comparison can be made with the
Metailurini, a separate tribe within the Machairodontinae, 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 morphology 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 &
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 estimated at between 28 and 65 kg (Salesa, 2002), which
is within the range of an extant puma, Puma concolor.
At this size, it is difficult to imagine this felid as a
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
time needed to ensure a kill, is a more reasonable
interpretation. Nevertheless, the evolution of
machairodonts produced such large and often strongly
built animals that the latest species of this group
(Smilodon and Homotherium) were probably able to
hunt relatively larger prey than the pantherines
(Lewis, 1997; Turner & Antón, 1997).
In summary, reducing the risk during hunting activities is very important for all predators, because any
tooth or bone breakage or wound will drastically
reduce the capacity to hunt and may lead to starvation
and death. We suggest that this ecological constraint
was the main pressure that led to the appearance of
the sabre-toothed cat model.
ACKNOWLEDGEMENTS
The authors thank Dr Francisco Pastor (Facultad de
Medicina, Universidad de Valladolid, Spain), for
kindly loaning the extant specimens for comparison.
This study is part of the research project BTE200200410 (Dirección General de Investigación-MCYT)
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 Comunidad Autónoma de Madrid (Dirección General de Patrimonio Histórico) for continuous funding support and
research permissions. A.T. thanks the British Council
for travel funding. Additional support was provided by
the National Geographic Society (Grant 6964–01). We
also thank an anonymous referee, whose comments
improved the quality of the manuscript.
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