Content uploaded by Manuel J. Salesa
Author content
All content in this area was uploaded by Manuel J. Salesa
Content may be subject to copyright.
Introduction
Few mammalian fossils have attracted as much
interest among both palaeontologists and the wider
public as the sabre-toothed, or machairodontine,
cats. With that interest has come a huge variety of
interpretations of both form and function, most
notably of course in relation to the extreme and
seemingly bizarre development of the upper canine
teeth. It would seem as though every conceivable
(and in some cases inconceivable) way in which
these teeth might have been used has been put for-
ward at one time or another. Such difficulties in
interpretation stem largely from the lack of any
extant analogue, an absence that made it especially
hard for 19th Century specialists to classify the first,
fragmentary fossil finds of sabre-tooths correctly,
since there was simply no concept of a cat-like ani-
mal with enlarged, flattened canine teeth. Indeed, in
the early days of formal palaeontological study the
leading French authority Cuvier (1824) even placed
some machairodontine material from Italy and Ger-
many within the bear genus Ursus, although this
error was soon recognised and corrected by Bravard
Changing ideas about the evolution and functional
morphology of Machairodontine felids
El cambio de ideas acerca de la evolución y morfología functional
de los félidos Machairodontinos
A. Turner1, M. Antón2, M.J. Salesa2, J. Morales2
ABSTRACT
Sabre-toothed felids, the machairodontines, have attracted much attention among palaeontologists
for many decades, not only because of their spectacular morphology but also because they are a striking
example of convergent evolution that is most probably linked to strong selective pressures. In this paper
we provide a summary of the changing interpretations of their functional anatomy and evolution, from
early hypotheses proposing a stabbing mode of attack and a pleiotropic control of the complex of
machairodont morphologies, to the current views favouring the canine shear-bite model and a mosaic
evolution of anatomical features.
Keywords: Felidae, Machairodontinae, Functional Anatomy, Evolutionary History
RESUMEN
Los félidos de dientes de sable, los macairodontinos, han ejercido una especial atracción entre los
paleontólogos durante muchas décadas, no sólo por su espectacular morfología, sino también debido a
que son un llamativo ejemplo de evolución convergente, probablemente ligada a una fuerte presión
selectiva. En este trabajo suministramos una recopilación de los cambios de interpretación acerca de su
anatomía functional y evolución, desde las primeras hipótesis en las que se proponía un ataque por
apuñalamiento y un control pleitrópico del complejo morfológico macairodontino, hasta los actuales pun-
tos de vista que favorecen un modelo de mordedura muy especializado y una evolución en mosaico de
los carácteres anatómicos.
Palabras clave: Felidae, Machairodontinae, Anatomía functional, Historia Evolutiva
1School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool, L3 3AF, United Kingdom.
Email: A.Turner@ljmu.ac.uk
2Departamento de Paleobiología, Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal, 2. 28006 Madrid, Spain.
Estudios Geológicos, 67(2)
julio-diciembre 2011, 255-276
ISSN: 0367-0449
doi:10.3989/egeol.40590.188
e390-11 Turner.qxd 30/1/12 14:19 Página 255
(1828) who assigned the specimens, together with
others from Perrier (France), to the Felidae.
However, in this paper we have no wish to
become enmeshed in the subsequent tangled argu-
ments about precise taxonomic attributions to gen-
era and species that have taken place over 200 years
of research into the machairodontine felids, and tax-
onomic matters are therefore relegated to a way of
identifying the material mentioned. Instead we
choose to stay with the interpretations of form and
function that have been applied to various members
of the felid subfamily Machairodontinae as a whole,
and in doing so we concentrate on two major areas
of interest. The first deals with the question of the
function of the dentition, especially in the more
derived, crown species of the various lineages that
are known from the Pliocene and Pleistocene, the
members of the tribes Homotheriini and Smilodon-
tini. The second deals with the origin of the spe-
cialised features of those dentitions and their inte-
gration with the entire morpho-functional complex
of these top predators. Of course, as we hope to
show, understanding of either of these two areas
involves an appreciation of both. This seems to us
an appropriate subject in a volume intended as a
tribute to Leonard Ginsburg, whose own work has
included so many aspects of that area of palaeonto-
logical interest.
Evolutionary History of the
Machairodontinae
The cat family, the Felidae, appears to have origi-
nated in Eurasia, where the earliest known form is
Proailurus lemanensis, an animal about the size of a
modern ocelot, found in Late Oligocene deposits
(about 30 Ma) in France. Proailurus lemanensis
was about 40 cm high at the shoulder, and although
it probably looked perfectly cat-like it had a more
primitive, elongated skull than living felines and a
more complete dentition, including P1, p1, double-
rooted P2 and p2, a well-developed talonid on m1
and an m2. During the Miocene, primitive cats
close to Proailurus gave rise to two different lin-
eages, the conical-toothed cats of the subfamily
Felinae and the sabre-toothed forms of the subfami-
ly Machairodontinae. The earliest known member
of this subfamily is Pseudaelurus quadridentatus
(Beaumont, 1975; Salesa et al., 2010a),best known
from middle Miocene deposits in France, which
was a leopard-sized cat with slightly flattened upper
canines and a gently angled mandibular symphysis
(fig. 1). While members of the Felinae are the only
felids present in extant faunas, most of the felid fos-
sil record from the Miocene onwards is dominated
by the sabre-toothed machairodontines. Thus the
African felid guild prior to the mid-Pliocene con-
sisted almost entirely of machairodontines (Turner
& Antón, 2004) with the exception of two conical-
toothed species, Diamantofelis ferox and D. minor,
from 17 Ma old deposits at the Namibian locality of
Arrisdrift. Only from around 3.5 Ma do members of
the Felinae begin to appear in Africa and it is only
after the disappearance of the African machairodon-
tines by around 1.5 Ma that they became the sole
representatives of the family in the continent. In
other continents this pattern of appearance and
replacement has its own and often quite different
pattern and timescale (Turner & Antón, 1999;
Antón et al., 2005). In fact, members of the Felinae
are known since the early Miocene in Eurasia but in
general the fossil record of this subfamily is restrict-
ed to species of relatively small body size until the
pantherins became widespread in the late Pliocene,
and until then, the large cat niche was exclusively
occupied by sabre-toothed forms. Thus, by any
standards, the machairodontines were a major and
long-lived group of diverse species, and remained
the dominant large mammalian hypercarnivores in
the terrestrial ecosystems of four continents for
most of the Neogene. They were by no means the
bizarre, inefficient and rather short-term evolution-
256 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 1.—Life reconstruction of the primitive machairodont felid
Pseudaelurus quadridentatus
, based on fossils from the French
middle Miocene site of Sansan (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 256
ary experiment that the popular literature would
sometimes have us believe.
As is well known, other groups of mammals
besides the Felidae have converged with the
machairodontines in the development of sabre-
toothed adaptations. Within the order Carnivora, the
family Nimravidae is a striking example of conver-
gence, with Palaeogene genera such as Eusmilus
and Hoplophoneus resembling to an astonishing
extent the cranial morphology of advanced felid
sabre-tooths (fig. 2) such as Megantereon. Bar-
bourofelis, Sansanosmilus and several related gen-
era were also classified as members of the Nimravi-
dae, but their anatomy is rather different from that
of typical nimravids leading some specialists to
include them within the Felidae (Morales et al.,
2001). However, their ear region differs significant-
ly from that of felids, as observed by Bryant (1991)
and Hunt (1987), and it may be justified to keep
those genera in a new, separate family, the Bar-
bourofelidae, as proposed by Morlo et al. (2004)
(fig. 3). While the nimravids were essentially a
Palaeogene group, and most of them were already
extinct when the felids made their first appearance,
the barbourofelids evolved in the Miocene and there
was overlap and possibly competition between
them and the true machairodontines.
It may be worth commenting here that the word
“machairodont”, meaning “knife-tooth”, which is
often used as an adjective to denote the presence
of sabre-tooth morphology in any mammalian car-
nivore (“machairodont cats”, or “machairodont
carnivores”), is sometimes used to refer to the
machairodontine felids (“the machairodonts”). In
fact, the genus name “Machairodus”, which has the
same Greek root, has been used more informally,
(often without italics), especially by French palaeon-
tologists, to refer to any sabre-toothed carnivore. To
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 257
Fig. 2.—Skull, mandible and cervical vertebrae (A) and recon-
structed appearance of the head and neck (B) of the American
nimravid
Hoplophoneus mentalis
, based on fossils from the
Chadron formation (USA). The similarities in detail with the
anatomy of felid sabre-tooths like
Megantereon
are striking (Art-
work by M. Antón).
Fig. 3.—Skull (A), reconstructed masticatory muscles (B) and
restored life appearance (C) of the American barbourofelid
Bar-
bourofelis fricki
, from the late Miocene (Hemphilian) of North
America. Within the order Carnivora, this is probably the species
that shows the most derived machairodont specialisations in its
skull (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 257
avoid confusion, we prefer to use here the word
machairodontine when referring to felid sabre-tooths.
Dental function in machairodontines
The elongated upper canines are one of the most
striking features of the skeleton of a machairodon-
tine felid, and in order to stress their spectacular
appearance many reconstructions of the life appear-
ance of the animals tend to feature them in an open-
mouthed pose. The dagger-like nature of the
canines thus exposed seems to suggest use in a stab-
bing manner to kill, and many of the earlier 19th and
20th Century ideas put forward in support of this
notion were usefully summarised by Simpson
(1941), who was himself a strong advocate of that
interpretation of their function across a range of
species of felids and nimravids (figure 4). Interest-
ingly, Merriam & Stock (1932: 25), in one of the
most extensive studies of any machairodontine cat
ever undertaken based on the material from Rancho
La Brea in Los Angeles, had concluded that the
American genus Smilodon used both stabbing and
slicing in what they termed “consumating an
attack”. The stabbing argument was forcibly reject-
ed at the time by Bohlin (1940, 1947), who also
summarised some of the earlier ideas and interpre-
tations while arguing that a slicing function alone
was more probable on both ecological and biome-
chanical grounds. Bohlin’s ecological argument was
also based on evidence from Rancho La Brea,
which in his view indicated that Smilodon probably
operated there as a scavenger, while his biomechan-
ical argument was based on a lengthy discussion of
the implications of attempting to stab into the body
of a large ungulate and kill it, and stressed the high
probability of damage to the teeth that would result.
However, Kurtén (1968) in his consideration of
European Pleistocene mammals suggested that
while Homotherium may have used its canines to
slice, those of Megantereon together with the pow-
erful neck and massive forequarters of the latter
species suggested to him a stabbing function. In his
later discussion of North American Pleistocene
mammals Kurtén (Kurtén & Anderson, 1980) reiter-
ated this functional distinction between Homotheri-
um and Megantereon, and suggested that the latter
genus was ancestral, and functionally similar, to
Smilodon (fig. 5).
In a detailed study of the functional morphology
of the skull and anterior cervical vertebrae of
Smilodon, Akersten (1985) concluded that the teeth
were too blunt to permit stabbing, particularly as
part of an initial attack. Like Bohlin, he also argued
that excessive force would be needed to achieve a
kill and that the risk of damage to the teeth was too
great, and pointed out that the mandible was always
likely to be an impediment to an effective stab. He
then proposed a model for the machairodontine
killing bite that solved many of the problems of the
previous competing hypotheses. This model, known
as the “Canine Shear Bite”, implied that the preda-
tor would bite at a convex surface in the prey’s
body with jaws at full gape, and then use the
mandible as an anchor to provide support while the
whole skull was pulled down by the neck muscles
acting on the mastoid process (fig. 6). Once this
motion had caused initial penetration of the upper
canines into the flesh of prey, and as the jaws
closed, the gape became small enough to allow the
adductor muscles of the mandible to pull efficiently
during the rest of the killing bite. Akersten went on
to suggest that a backwards pull of the head was
used to cause further damage and to tear off a whole
chunk of flesh, and thought that the belly of large
ungulates was the most likely target for such a
killing bite. Akersten’s proposal has some parallels
with that of Merriam & Stock (1932), who consid-
ered the side of the victim as the most likely target.
Akersten’s view was supported by Martin (1989),
although he suggested that a killing bite to the neck
of prey was a more credible scenario than a belly
bite since the abdomen was more easily defended
258 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 4.—Reconstruction of the head of the American
machairodontine
Smilodon
shown in a hypothetical stabbing
motion (A), compared with a human hand wielding a knife (B), to
illustrate the analogy proposed by the stabbing hypothesis (Art-
work by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 258
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 259
Fig. 5.—Skulls in side view of the homotheriin
Homotherium
(A),
and of the smilodontins
Megantereon
(B) and
Smilodon
(C), illus-
trating the differences between the two machairodontine tribes
that led Kurtén (1968) to suggest a more slicing function for the
canines of homotheriins, and a more stabbing function for the
smilodontins (Artwork by M. Antón).
Fig. 6.—Reconstruction of the head of
Homotherium
illustrating
the process of the Canine Shear-Bite as hypothesised by Aker-
sten (1985) for the genus
Smilodon
. First (A), the predator opens
its jaws at full gape to encompass a chunk of skin and flesh on a
convex area of the prey’s body. At such a wide gape, the adduc-
tor muscles of the mandible such as the
temporalis
and
masseter
,
are too stretched to exert enough force for initiating a strong clo-
sure of the jaws. In the next stage (B), the whole head is ventrally
flexed around the atlanto-cranial articulation using the force of the
anterior neck musculature, while the front of the mandible, in con-
tact with the prey’s body, acts as an anchor. This motion allows
the initial penetration of the canine tips into the flesh of the prey.
In the next stage (C), the upper canines sink deep enough to
decrease the gape of the jaws to an angle where the adductor
muscles can exert their full force and produce a deeper bite. At
this point it is feasible that the machairodont pulled back its whole
head, tearing a large chunk of flesh from the prey. However, this
pull is not a necessary condition for the effectiveness of the killing
bite (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 259
by a struggling prey, the curvature of the belly was
too low for an effective bite and even if a successful
bite was made it would not lead to an especially
quick death. Biknevicius & Van Valkenburgh
(1996) and Turner & Antón (1997) also supported
Akersten’s hypothesis, but the latter authors gave
further consideration to the whole problem, using
Akersten’s hypothesis as a starting point. Like Mar-
tin, they considered that a canine shear-bite to the
throat of an immobilised prey would be more plau-
sible than a bite to the belly, based, for instance, on
consideration of the relative sizes of a skull of
Megantereon and the neck of a horse (Turner &
Antón, 1997, fig. 4.24), as shown here in fig. 7. The
resultant occlusion and/or severance of the wind-
pipe and several major blood vessels would ensure
a relatively quick and efficient death and reduce
risk of damage to the teeth, which would be kept
well away from any larger bone masses and have
any torsion produced by a struggling prey min-
imised, a conclusion matching that arrived at more
recently by McHenry et al. (2007).
One further way for sabre-tooths to protect their
upper canines against torsion during the killing bite
is to enlarge the contact surface between the canine
crown and the gum or gingiva, a feature that has
been inferred for Smilodon from the extension of
the cementum beyond the root-crown contact on the
cervix of the upper canines (Riviere & Wheeler,
2005). This configuration would provide several
functional advantages: on the one hand, the gingival
component of the periodontal ligament would pro-
260 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 7.—Skull and mandible of the smilodontin
Megantereon
shown in three stages of a Canine Shear-Bite applied to the neck of an
equid (A, B and C), the latter shown in a transversal section at the level of the second cervical vertebra. As the illustration shows, vital
structures such as larger blood vessels and the trachea of prey are in a vulnerable position in the anterior neck, making it an ideal tar-
get for the killing bite (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 260
vide additional stability to the tooth; on the other
hand, since the gingiva also acts as a tactile organ, it
would help the animal know when the tooth had
reached maximum functional penetration.
Biknevicius & Van Valkenburgh (1996) suggest-
ed that the strength of the upper canines, at least in
Smilodon, would have meant that it could have
resisted breakage during struggles with a wounded
prey, provided that the jaws were fully closed dur-
ing a canine shear-bite. However, they proposed
that this fully closed bite was most likely to have
been an effective method of control for “a weak-
ened prey that had already received several quick
but debilitating canine sheer-bites” (Biknevicius &
Van Valkenburgh, 1996, p. 422), which seems a
self-contradictory argument. In fact they went on to
suggest that death may have been induced by means
of a throat hold, which seems to us more likely but
which in our view could only have been achieved
with the prey held firmly using claws and the body
weight of the predator and without preliminary
attempts to bite elsewhere. Such a quick death, min-
imising danger to the predator, strikes us as the
most plausible interpretation of canine shear-bite
function, since it is hard to see how even a well-
placed bite in the abdomen of a prey animal is like-
ly to be achieved either with any degree of control
or in a manner that would produce a rapid fatality.
The interpretation of a single throat bite to an
immobilised prey would apply broadly across the
range of derived machairodontine cats, as exempli-
fied in the case of Homotherium (Antón & Galo-
bart, 1999), and would imply that the original func-
tional advantage of large canines lay in the speed
and efficiency of the kill of medium-sized prey
using the canine shear-bite (fig. 8). We shall see in
the subsequent section how this interpretation in turn
sheds light on the evolution of the machairodontine
cat functional complex.
Feeding, gape and implications for the
reconstruction of soft tissues
The killing bite is only one of the aspects of the
cranio-dental function of sabre-toothed felids that
has led to conflicting interpretations. An equally
important problem is how machairodontines dealt
with the carcass and got food from it. Large canine
teeth may appear something of an impediment to
eating in a cat-like manner, and this led Miller
(1969) to propose that sabre-toothed cats would
need an especially elongated lip line, reaching fur-
ther back than is the case in extant cats, in order to
get food into the side of the mouth. But the relative-
ly and absolutely large incisor battery of many
species, often set well forward of the upper canines
and in the derived crown species in particular incor-
porating the lower ones, must have helped to over-
come that problem, as summarised by Bohlin
(1940) and discussed in detail by Turner & Antón
(1997, fig. 4.25). That the incisors would be used
by some machairodontines to pull flesh from the
bones of a carcass is further suggested by the evi-
dence of tooth marks attributed to Homotherium on
the bones of prey from a possible den in Friesen-
hahn Cave (Texas, USA) (Marean, 1989). Just as
important is the fact that modern cats use their car-
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 261
Fig. 8.—Dorsal view of the homotheriin
Homotherium
killing a
horse. The detail of the skull, cervical vertebrae and anterior tho-
racic vertebrae (A) to which the trajectories of selected muscles
have been added, shows how the great vertebral length and
enlarged transverse processes provide for improved action of the
muscles that rotate the neck. The drawing of the reconstructed
animals (B) illustrates how the predator could position its body
ideally for using its own weight to subdue and immobilise the
prey, while rotating its neck in order to orientate the head with
almost surgical precision for the bite (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 261
nassials to cut the skin and flesh of prey, and a com-
parison of the skull morphology and inferred posi-
tion of soft tissues in pantherins and machairodon-
tines shows that they were perfectly able to use
their carnassials in a similar fashion without any
interference from their elongated upper canines
(Turner & Anton, 1997) (fig. 9).
These considerations lead us to the next major
source of debate about function and reconstructed
appearance: the gape needed for the mandible to
clear the upper canine tips and the length of the lip
line. Life appearance of machairodontines has been
as much a matter of debate as function, especially
because of their highly specialised dentition and
jaw apparatus (Bryant, 1996). In earlier reconstruc-
tions, such as those of Smilodon undertaken by C.
R. Knight (Merriam & Stock, 1932, figs. 4-5), the
head was usually distinctly cat-like, but Miller
(1969) raised objections to that view, based not only
on the argument mentioned above that a cat-like lip
line would not allow food to enter the side of the
mouth but also that it would not permit the gape
needed to accommodate the canines (fig. 10).
Besides suggesting that the lip line should be set
much farther back, he also proposed that the exter-
nal nose should be considerably shorter and the
nostrils retracted, the dorsal profile of the skull
straightened and the ears set relatively lower on the
skull, thereby giving the animal a distinctly non-
catlike appearance.
Turner & Antón (1997, p. 138-142) rejected
Miller’s argument at some length, but returned to
the point in more detail in a subsequent publication
(Antón et al., 1998) with a fuller consideration of
the reconstructed facial appearance of Smilodon in
view of the wider support that Miller’s interpreta-
tions appeared to have enjoyed. After a thorough
262 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 9.—Reconstructed head (A) and skull (B) of
Smilodon
apply-
ing a carnassial bite to a carcass. As this illustration shows, the
large upper canines of machairodontines were not an obstacle
for this kind of bite, in which the food is taken directly through the
side of the mouth, and where a normal cat-like mouth opening
allows the carnassial teeth to separate and puts them in direct
contact with the body of the prey (Artwork by M. Antón).
Fig. 10.—An illustration of the proposed life appearance of
Smilodon
based on the arguments of Miller (1969). This drawing
is consistent with the proportions of the actual skull, but shows
such hypothetical features as the caudally elongated lip line and
the shortened nasal cartilage (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 262
review, employing first-hand study of skulls, dissec-
tions of a number of living felids and an extensive
examination of the skulls of fossil felines,
machairodontines and other larger Carnivora
together with detailed reconstructions of the facial
musculature of fossil felids, they were able to con-
clude that a broadly cat-like appearance was entire-
ly appropriate (fig. 11). Although based on a
detailed consideration of Smilodon, their conclu-
sions have clear applicability across the range of
machairodontine taxa, and imply not only a cat-like
appearance but also a cat-like pattern of eating, with
the incisors pulling off soft tissues and the cheek
teeth employed in slicing. A later facial reconstruc-
tion of Homotherium (Antón et al., 2009) showed a
combination of broadly cat-like appearance with a
unique head shape resulting from unmistakable
homotheriin cranial proportions such as a straight
dorsal profile, a projecting incisor battery and a
deep mandibular symphysis implying an elongated,
tall and square muzzle (fig. 12). This detailed
reconstruction not only revealed the likely life
appearance of the Pleistocene scimitar-tooth cats,
but also led to questions about early interpretations
of an Upper Palaeolithic statuette from the French
Pyrenees site of Isturitz as a stone-age depiction of
Homotherium. In fact, comparison of our recon-
struction with images of the statuette indicated that
the latter was most likely a representation of a cave
lion.
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 263
Fig. 11.—Step by step reconstruction of the head of
Smilodon
. A, skull and mandible; B, with reconstructed masticatory muscles and
neck musculature; C, with superficial musculature; D, life appearance (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 263
The origin of the specialised machairodont
features
Since machairodontines, despite an undoubtedly
cat-like appearance, are so obviously different from
living species, an assumption underlying many
attempts to interpret the functional morphology of
the machairodonts has been that they preyed on
unusually large and usually thick-skinned ungu-
lates, or “pachyderms” to use an obsolete term, as
exemplified in the paper by Simpson (1941) and
more recent authors (Anyonge, 1996; Bakker,
1998). A second, but less explicitly expressed
assumption has been that the extreme suite of
machairodontine morphologies exemplified in the
crown taxa Smilodon, Megantereon and Homotheri-
um are typical of all machairodontines, and have
evolved in parallel “under strong pleiotropic con-
trol” (Dawson et al., 1986) as an adaptation to tack-
ling such large prey. But of course these three taxa
are known from Pliocene and Pleistocene deposits;
they are the latest and probably most derived of the
machairodontines, and we have until recently
known very much less about the morphology of
earlier taxa. The extent and nature of mosaic evolu-
tion in morphology has therefore been unknown,
with only the recognition that a functioning com-
plex of characters must have been the pattern at any
one time as a guide to interpretation.
This situation changed with the recovery of
machairodontine remains from ~ 9 Ma deposits at
the Spanish fossil locality of Batallones-1, near
Madrid. The material provides numerous complete
or semi-complete individuals of two species, the
large, lion-sized Machairodus aphanistus (Antón et
al., 2004) and the smaller, leopard-sized Promegan-
tereon ogygia, previously referred to the genus
Paramachairodus (Salesa et al., 2005, 2006) but
now referred to a genus first erected by Kretzoi
(Salesa et al., 2010a). In both cases we are able to
discern something of the origins of the large upper
canine of the machairodont functional complex
within a more primitive cranio-mandibular mor-
phology and a biomechanical structure much more
like that of a modern feline cat (fig. 13).
In the case of M. aphanistus, the highly
derived, elongated and flattened upper canines are
similar to those seen in later taxa such as Homoth-
erium, where they were evidently used within a
complex of equally derived cranio-mandibular
adaptations (fig. 14). But in M. aphanistus they
are present in a cranium where the incisor arc is
not well-developed, the lower canines are large,
the post-canine teeth are not particularly derived
in the machairodontine direction and the gape size
was only moderately greater than that in modern
felid species (Antón et al., 2004). The force of
head depression to assist bite, as indicated by size
and direction of neck muscle insertions, is greater
than that of modern pantherin cats but clearly
much less than that seen in derived machairodon-
tines (fig. 15). These morphological features sug-
gest predatory behaviour that differed both from
264 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 12.— Skull (A), reconstructed musculature (B) and restored
life appearance of the head (C) of
Homotherium
. Notice the
prominent, square outline of the muzzle due to the straight
nasals, high mandibular symphysis and protruding incisors (Art-
work by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 264
that of extant pantherins and from that hypothe-
sized for derived machairodontines. While it may
have killed by penetrating the flesh of the throat
with its canines to induce blood loss, just as has
been inferred for the derived taxa, the upper
canines of M. aphanistus would have been inade-
quate for either a crushing nape bite or a suffocat-
ing throat bite. On the other hand, features such as
the insertions and orientations of the masseter and
temporalis muscles and the size of the lower
canines indicate that the force applied to both
upper and lower canines through contraction of the
jaw-closing musculature at moderate gapes pro-
vided the main power for the bite, just as in pan-
therins and other modern cats.
Rather than suggesting concentration on animals
much larger than themselves, the limited adaptation
for gape and the primitive biting mechanism in M.
aphanistus suggest that its upper canines originally
evolved as an adaptation for killing prey within the
size range of those killed by modern felids of com-
parable size, and that a horse or antelope was the
largest prey that M. aphanistus could kill efficiently
and regularly. The key advantage of the initial
development of sabre-like teeth would then lie in
the efficiency of a killing bite that caused massive
blood loss instead of suffocation. Such a mosaic of
features also contradicts the idea of “strong
pleiotropic control” for the derived machairodon-
tine features as some kind of “all or nothing pack-
age”, and suggests instead that they have evolved
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 265
Fig. 13.—Reconstructed skeletons of the machairodontines
Machairodus aphanistus
(left, background) and
Promegantereon ogygia
(foreground), based on material from the Vallesian (late Miocene) site of Batallones-1 (Artwork by M. Antón).
Fig. 14.—Skull (A), reconstructed musculature (B) and restored
life appearance of the head (C) of
Machairodus aphanistus
.
Notice the gently convex dorsal outline of the skull and scarcely
protruding incisor battery compared with
Homotherium
in figure
12 (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 265
independently in each lineage of sabre-toothed
mammalian predators.
This interpretation is strengthened when we con-
sider the pattern seen in the second machairodon-
tine from Batallones-1, Promegantereon ogygia. In
overall appearance the skull and many features of
the dentition of this smaller species are broadly
similar to those of a pantherin felid, but the upper
canines are moderately elongated and flattened and
the mandibular symphysis is strongly verticalised
(Salesa et al., 2005) (fig. 16). These features are
allied to a neck morphology that shows only mod-
estly-developed machairodontine traits, but the total
package points to the importance of a canine shear-
bite where head flexion operated in conjunction
with the mandible acting as an anchor (Salesa et al.,
2005). Thus while the overall morphology is still
very far from the functional complex seen in the
Plio-Pleistocene sabre-toothed crown taxa, it is
again most plausibly interpreted as an adaptation to
quick and efficient killing of prey close in size to
the predator. Moreover, the risk of canine damage
from bone contact probably meant that the animal
would have avoided smaller prey species (Salesa et
al., 2006). Further support for these interpretations
comes from consideration of the forelimb anatomy
in P. ogygia (Salesa et al., 2010b), where the mor-
phology is clearly adapted for powerful extension
and supination of the forearm while providing rein-
forced stability to the elbow and shoulder. The first
phalanx, or dewclaw, is particularly robust, and the
overall impression is of great strength able to pro-
vide rapid capture and immobilisation of prey so
that a throat bite could be made with minimal risk
to the predator and its teeth. With such increased
efficiency in killing, there would also be a signifi-
cant reduction in energy expenditure (Salesa et al.,
2006). At the time of writing, investigations of the
functional anatomy of the forelimb of Machairodus
aphanistus have yet to be completed, but it will be
interesting to see the extent to which these parallel
features are seen in P. ogygia.
Hunting, ecology and social behaviour
Hunting is the most obvious aspect of machairodon-
tine behaviour about which the fossils are likely to
provide useful clues, but any attempt to reconstruct
such activities must take into account other aspects,
such as sociality and ecology, which are also close-
ly linked with their predatory strategies. Of course
266 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 15.—Skull and cervical vertebrae of
Machairodus aphanistus
, based on fossil material from Batallones-1 (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 266
with extant felids, direct observation is all we need
to determine if they are social or solitary or if they
live in open or closed environments, but with fossil
cats we are left to make inferences from their anato-
my and from the context of the fossil sites. Strong
sexual dimorphism in extant Carnivora has been
suggested to correlate with breeding behaviour, par-
ticularly amongst the Felidae where it is evident in
the highly social lion, a species in which males
compete aggressively for females (Gittleman & Van
Valkenburgh, 1997). On this basis, sexual dimor-
phism in extinct Felidae may therefore be of some
palaeoecological significance (Turner, 1984), and is
an obvious avenue to explore.
Van Valkenburgh & Sacco (2002) applied the
idea of a relationship between sexual dimorphism
and breeding system to the study of social behav-
iour in Smilodon fatalis from the Rancho La Brea.
They found a low level of sexual dimorphism,
which they took to be consistent with a typical
felid social structure in which both sexes are usual-
ly solitary, and males defend a territory that
includes those of the females. But the precise sig-
nificance to be attached to any given level of
dimorphism across a range of species is open to
debate. As Van Valkenburgh & Sacco (2002) point-
ed out, both lions and leopards appear quite dimor-
phic, despite the fact that one is solitary and the
other social. They also argued that both tigers,
Panthera tigris, and jaguars, Panthera onca, are
significantly less dimorphic, and concluded from
this that while high dimorphism does not necessari-
ly imply a lion-like social structure, reduced dimor-
phism does imply its absence. Turner & Antón
(1997) had argued that the high numbers of
Smilodon remains found at Rancho La Brea in rela-
tion to remains of prey species could themselves be
an indication of higher levels of social interaction,
and a more recent study by Carbone et al. (2009)
has suggested that parallels between events at mod-
ern simulated kill sites and the relative abundance
of predators at Rancho La Brea may now support
ideas of sociality in that species at that site. In fact,
and as suggested by Van Valkenburgh & Sacco
(2002), it is possible that Smilodon, or any
machairodontine for that matter, could have been
social while not sharing the particular social sys-
tem of lions with its consequent intense competi-
tion between males for access to females. An alter-
native system could be one with a monogamous
alpha pair acting as the centre of the social group,
as happens among extant carnivores in the moder-
ately dimorphic modern wolves.
One feature of the Smilodon sample from Ran-
cho La Brea that has been seen as evidence of
group behaviour is the presence of healed injuries
in fossil bones of the sabre-tooth, since it has been
suggested that injured individuals would have died
before their fractures healed unless allowed to eat
at the kills of other group members (Heald, 1989).
This idea has been rebutted extensively by MacCall
et al. (2003) who provide veterinary data about the
timing of bone healing in injured felines and about
their resistance to starvation, suggesting that the
examples of healed injuries found at La Brea are
compatible with solitary behaviour. According to
these authors, injuries like the ones seen at the site
can heal naturally fast enough to allow the animal
to survive until it is capable of hunting or at least
of opportunistic scavenging. Furthermore, since
felids can only get a fraction of their water require-
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 267
Fig. 16.—Skull (A), reconstructed musculature (B) and restored
life appearance of the head (C) of
Promegantereon ogygia
(Art-
work by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 267
ments from their kills, dehydration comes about
earlier than starvation, and consequently any
injured cat must be mobile enough to walk to water
during the healing period, a mobility that would
also allow it to scavenge opportunistically. Addi-
tionally, they argue that the frequency of injuries is
comparatively low at the site, suggesting that ani-
mals with really severe fractures usually died
before healing and would not have been able to get
to the asphalt seeps for scavenging. Thus the ques-
tion of sociability of Smilodon from Rancho La
Brea remains an open one and more data are obvi-
ously required.
The data from Batallones-1 have been argued to
suggest that Promegantereon ogygia, a smaller ani-
mal with a low degree of sexual dimorphism, may
have exhibited a low degree of competition among
males for the access to females (Salesa et al., 2006)
while the larger Machairodus aphanistus shows
evidence of greater dimorphism (Antón et al.,
2004), implying that the males of the latter species
would had been much more intolerant of the pres-
ence of other adult males in their territories. The
vast majority of the Batallones-1 machairodontine
sample is made up of young adults, suggesting that
it was precisely the dispersing individuals that came
across the natural trap when they entered a territory
left vacant by an adult previously entrapped, a
process that repeated over time could lead to the
accumulation of felid fossils found at the site
(Antón & Morales, 2000).
Whatever interpretation we place on the evidence
for dimorphism, Promegantereon ogygia and
Machairodus aphanistus differed considerably in
their body size (fig. 13), which in turn implies a set
of ecological differences. When different species of
extant felids live in sympatry a marked segregation
exists between them, with the small-sized species
constantly avoiding the often violent encounters
with the large ones. It is known that lions and leop-
ards kill adults and cubs of other felids, and leop-
ards are killed by lions and tigers (Turnbull-Kemp,
1967; Schaller, 1972; Bailey, 1993; Daniel, 1996;
Alderton, 1998; Bothma & Walker, 1999). Thus in
modern ecosystems, the coexistence of two species
of large felids usually occurs in habitats with some
tree cover, which allows the smaller species to take
refuge from the attack of the larger one and so
avoid being killed or having its prey stolen (Morse,
1974). This is the case for lions and leopards in
Africa (Bailey, 1993) and tigers and leopards in
Asia (Seidensticker, 1976). In the case of cheetahs
and lions, both of which can be found in more open
environments, sympatry is possible because chee-
tahs constantly avoid encounters with lions, hunting
during the hours of maximum heat when lions and
hyaenas tend to be inactive and resting in the shade
(Hanby & Bygott, 1979; Durant, 2000). There is
also sympatry among felids of similar size, such as
pumas and jaguars in most of the American conti-
nent (Nuñez et al., 2000), but this is only possible
when resources are rich enough to allow both
species to exist while developing a marked ecologi-
cal segregation based on the avoidance of adult
encounters (Rabinowitz & Nottingham, 1986;
Nuñez et al., 2000). In summary, the sympatry of
two large felid species seems to be determined not
only by the presence of enough tree cover, but also
by high prey biomass (Seidensticker, 1976). In the
case of lions and leopards, this sympatry is facilitat-
ed by the fact that leopards preferably occupy
wooded sections of the habitat, which are less
favourable for lions (Bailey, 1993). The body pro-
portions of P. ogygia and M. aphanistus are very
similar to those of the extant pantherin felids (Sale-
sa et al., 2005; Antón et al., 2004), probably reflect-
ing similar habitat preferences for wooded environ-
ments (fig. 17). The predominance of P. ogygia in
Batallones-1 could imply that the trap was in a
wooded area with at least enough cover to allow
this species to coexist with the larger M. aphanistus
(Antón & Morales, 2000).
It is clear that what is taken as the primary char-
acteristic of these animals, the enlarged upper
canine, evolved in a very different biomechanical
context from that generally considered to be the
norm for machairodontines based solely on consid-
eration of the derived crown taxa. Both M. aphanis-
tus and P. ogygia show cranio-dental morphologies
that differ from those of both the extant, conical-
toothed felines and the crown machairodontine
taxa, but which can plausibly be seen to lie at or
close to the root of development of those features
along the subsequent lineages leading to the
Homotheriini and Smilodontini. Indeed, as Wroe
et al. (2008) have emphasised, the crown
machairodontines show an interesting pattern of
postcranial morphological divergence, with the
dirk-toothed Smilodontini displaying an emphasis
on more power and less speed while the scimitar-
toothed Homotheriini, although distinct, depart
less from the generalised felid morphology seen in
Panthera pardus in terms of the robustness of the
limb bones (fig. 18).
268 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
e390-11 Turner.qxd 30/1/12 14:19 Página 268
The study of the specific function of the dentition
and of the evolution of the craniodental complex in
the Batallones-1 felids shows that an emphasis on
rapid and efficient killing by means of blood loss
was quickly developed. Flattened and elongated
canine teeth, together with an angular mandibular
symphysis, were therefore incorporated into a mor-
phological suite that initially showed few develop-
ments in the direction of the derived machairodon-
tine condition, and a greater emphasis on strong
head depression only appears later in the sequence.
At least in P. ogygia these craniodental features
were matched by great strength in the forelimbs,
massive dewclaws and an evident ability to hold
prey securely. This combination allowed the animal
to minimise the energy expenditure and the risk of
canine breakage (and other injuries) and these
would have been the main advantages associated
with the origin of the machairodontine adaptations
(Salesa et al., 2006). The classic explanation that
has linked machairodontine dentitions with such
strong forelimbs in the derived crown taxa as evi-
dence of concentration on very large prey from the
earliest stages of evolution within each lineage is
now seen to be based on a questionable set of inter-
pretations, as emphasised by Salesa et al. (2010b).
Promegantereon ogygia is recorded in Spain in
both MN 10 (Batallones-1) and MN 11 (Crevil-
lente-2), and the type material is from MN 9
deposits at Epplesheim in Germany (Salesa et al.,
2010a). The two more derived species Para-
machaerodus maximilliani and P. orientalis became
extinct in the Turolian (Late Miocene), and were
replaced by the more derived and jaguar-sized
crown genus Megantereon, although the exact
nature of the relationship between the older and
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 269
Fig. 17.—Reconstruction of the Vallesian environments and fauna around the fossil site complex of Cerro de los Batallones. From left
to right:
Micromeryx
sp.
; Promegantereon ogygia
(on the tree);
Magericyon anceps
(on the ground);
Aceratherium incisivum;
Microstonyx major
(far background);
Tetralophodon longirostris; Hipparion
sp
.; Machairodus aphanistus
; undetermined sivatherine
giraffid; undetermined boselaphine bovid (background);
Protictitherium crassum
(foreground). As in many other Tertiary fossil sites,
the presence of two sabre-tooth species of different sizes, combined with the presence of several species of browsing herbivores,
points to the presence of some tree cover around the site (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 269
younger genera remains to be established. The dis-
appearance of both Promegantereon and Para-
machaerodus may be associated with the progres-
sive aridification that occurred during the Vallesian
and Turolian (Fortelius et al. 2002), which led to
the predominance of savannas over wooded habi-
tats. However, the body proportions of the Plio-
Pleistocene genus Megantereon were broadly com-
parable with those of P. ogygia, with a similarly low
brachial index, suggesting similar preference for
wooded environments, and it thus seems obvious
that it also required some degree of tree cover to
survive. But whilst the cranial and skeletal features
related to the machairodontine type of killing were
still moderate in P. ogygia (Salesa et al., 2005,
2006) they were much more developed in Megan-
tereon, suggesting a more specialised killing behav-
iour in the latter genus, possibly associated with
larger prey size.
Machairodus aphanistus, as the first member of
the machairodontine lineage to attain lion size, was
previously considered ancestral to the more dentally
derived Turolian species Amphimachairodus gigan-
teus. However, this relationship was questioned by
Ginsburg et al. (1981), who argued that several fea-
tures of M. aphanistus, such as the large lower
canines, are too specialized to permit direct ancestry
and went on to propose the smaller, more primitive
species M. alberdiae as the likely ancestor of A.
giganteus. Our own detailed study of the Batal-
lones-1 material (Antón et al., 2004) revealed dif-
ferences in cranial and mandibular anatomy
between M. aphanistus and A. giganteus that were
not evident from the less complete material previ-
ously available (fig. 19). This led to the formal pro-
posal that A. giganteus, which most authors still
included in Machairodus, should indeed be referred
to a separate genus, Amphimachairodus Kretzoi,
1929, although the question of the relationship
between A. giganteus and any particular species of
Machairodus was not addressed. Other early
species of Machairodus are known from Asia
(Schmidt-Kittler, 1976; Sotnikova, 1992) but in all
these primitive taxa the skull morphology remains
virtually unknown. In contrast, complete skulls of
A. giganteus are known from sites in China (Chang,
1957) and Moldavia (Riabinin, 1929), clearly show-
ing that, unlike the overall primitive cranial mor-
270 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Fig. 18.—Skeleton and reconstructed life appearance of
Smilodon
(left) compared with
Homotherium
. Note the more robust propor-
tions of the smilodontin felid (Artwork by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 270
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 271
Fig. 19.—Skull (A), reconstructed musculature (B) and restored life appearance of the head (C) of
Amphimachairodus giganteus
(Art-
work by M. Antón).
e390-11 Turner.qxd 30/1/12 14:19 Página 271
phology seen in the Batallones-1 M. aphanistus
material, it had all the cranial features typical of
advanced machairodonts. Thus, whatever the pre-
cise nature of their relationship, M. aphanistus
clearly exemplifies a less derived stage in
machairodintine evolution than the Turolian taxon,
and it remains likely that A. giganteus had its ori-
gins among animals of Machairodus grade. The
features seen in A. giganteus are further developed
in the Plio-Pleistocene Homotherium, known from
complete skulls from many sites in four continents
(Turner & Antón, 1997).
The spreading of grasslands at the expense of for-
est at the end of the Vallesian (Agustí et al., 1999;
Fortelius et al., 2002) may have restricted the
species diversity of the forest-dwelling sabre-
toothed felids. The postcranial elements of the
largest species of Paramachaerodus, P. maximil-
liani, are virtually unknown, making it impossible
to assess the body proportions of this species; its
size was intermediate between that of the earlier
species of the genus and that of Megantereon, and if
we assume that it was proportioned like a forest-
dwelling felid then this could have meant that the
niche occupied by P. maximilliani became progres-
sively narrower, leading to the disappearance of the
species. Subsequent phases of moist climate during
the Pliocene and Pleistocene would have favoured
the wide expansion of Megantereon, which would
also have preferred wooded habitats. In fact, the
earlier part of the Pliocene with its more warm,
humid climate and extensive forests, saw the expan-
sion of another type of forest-adapted big felid, the
so called “false sabre-tooths” of the genus
Dinofelis.
Did the larger Machairodus aphanistus and sub-
sequent members of the lineage operate as social
predators? Apart from the considerations about sex-
ual dimorphism and breeding system discussed
above, the most important factors affecting social
behaviour in modern carnivores are predator body
size, prey size and vegetation cover. Thus it has
been shown that all the extant larger carnivore
species that are social tend to take prey larger than
themselves and live in mixed or open habitats
(Packer, 1986; Packer et al., 1990; Sunquist & Sun-
quist, 1989), and competition for prey and territory
in such high-visibility environments is exacerbated
as kills and dens are easily detected by competitors.
It thus becomes even more beneficial for large car-
nivores to join forces with conspecifics in order to
defend territory, kills and offspring. Observations
about the conditions of life in extant social preda-
tors cannot establish if such conditions necessarily
led to the evolution of group behaviour in the past,
but they do suggest that, if large carnivores adapted
to take large prey lived in an open environment,
then the likelihood of group behaviour is greater
than if they lived in more closed habitats.
Machairodus, Amphimachairodus and Homoth-
erium were obviously adapted to take prey larger
than themselves and what is known about their
postcranial skeleton indicates they were well adapt-
ed to efficient terrestrial locomotion, with later
forms further departing from the scansorial model
typical of primitive felids and becoming more adept
at sustained locomotion at medium speeds over
long distances (Antón et al., 2004). Such features
are compatible with group behaviour as discussed
above, and it is conceivable that an opening of the
vegetation could have been to the advantage of
these animals, particularly if they were able to kill
quickly and efficiently by employing their upper
canines to inflict a fatal bite to the throat.
Hypotheses about sabre-tooth ecomorphs
The morphological differences between crown
members of the Homotheriini and Smilodontini,
which led Kurtén (1968) to coin the terms “scimi-
tar-toothed cats” for the former and “dirk-toothed
cats” for the latter, were further interpreted by Mar-
tin (1989) as features indicating the existence of
two discrete, well differentiated ecomorphs among
sabre-toothed carnivorans. According to this view,
the possession of moderately high-crowned, strong-
ly flattened and coarsely serrated upper canines like
those of Homotherium or Machairodus would be
predictably associated with relatively slender, long-
limbed skeletons implying fast pursuit of prey and
even possible group behaviour, while the high-
crowned, less flattened canines of Smilodon or
Megantereon, with fine or absent crenulations on
their edges, would correspond with robust, short-
limbed skeletons implying ambush predation and
obligate solitary behaviour. Such ecomorphs are
seen as essentially taxon free, so that although they
coincide with the taxonomical differentiation
between Smilodontini and Homotheriini within the
Felidae, other, non-felid sabre-tooths would also fit
predictably within one or other ecomorph. Thus, the
barbourofelid Barbourofelis or the thylacosmilid
marsupial Thylacosmilus would be typical dirk-
272 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
e390-11 Turner.qxd 30/1/12 14:19 Página 272
tooths, while the nimravid Dinictis was seen as an
example of a non-felid scimitar-tooth.
However, it is now clear that such a rigid demar-
cation does not exist. The discovery of the short-
limbed homotheriin genus Xenosmilus in Pleis-
tocene deposits in Florida (Martin et al., 2000) has
provided a clear example of a machairodontine
combining scimitar-like canines with an extremely
robust skeleton, showing that these felids had con-
siderable evolutionary plasticity and were not con-
strained by a rigid ecomorph model. The Oligocene
nimravid Dinictis is also poorly characterised as a
scimitar-tooth (Scott & Jepsen, 1936) because its
upper canines, while not as high-crowned as those
of other nimravids such as Hoplophoneus or
Eusmilus, were neither exceptionally flattened nor
coarsely crenulated and its limbs, while relatively
gracile, had remarkably short, probably semi-planti-
grade feet very different from the long, digitigrade
feet of Neogene felids such as Homotherium. Fur-
thermore, a recent geometric morphometric analysis
of a wide range of sabre-tooth taxa, felid and non-
felid, has found no support for a differentiation
between “dirk-tooh cats” and “scimitar-tooth cats”
in terms of the morphology of the skull and
mandible, so that it increasingly appears that this
distinction has little relevance beyond the descrip-
tion of canine morphology and the coincidence with
a tribal separation within the Machairodontinae
(Prevosti et al., 2010).
Conclusions
After decades of research on the evolution of
sabre-tooth felids, several trends can be recognised in
this field of investigation. In terms of dental function,
the stabbing hypothesis has gradually lost ground in
favour of the canine shear-bite model, refined by
subsequent studies of the functional anatomy of fos-
sil and extant felids. Suggestions about the need for
radically non-felid facial musculature and external
appearance in order to explain machairodontine feed-
ing behaviour and gape are largely falsified by
detailed anatomical studies of felines and other
extant carnivores. Thus the main differences in life
appearance between felid sabre-tooths and their
extant relatives are a direct consequence of different
skull proportions and muscle insertion areas, imply-
ing generally cat-like appearance but unmistakable
proportions for the heads of crown-taxa within the
Smilodontini and Homotheriini.
The origin of the sabre-tooth complex of adapta-
tions has been difficult to interpret because the
crown taxa of each sabre-tooth lineage have been
traditionally more conspicuous and apparently bet-
ter represented in the fossil record, a bias that has
made the detailed similarities between unrelated
species all the more striking. Such a degree of con-
vergence led to the idea of a strong pleiotropic con-
trol over the entire “machairodont complex” of
anatomical features. The finding of complete and
abundant fossils of the basal machairodontine felids
Machairodus and Promegantereon at the fossil site
of Batallones-1 has provided for the first time an
opportunity to study in detail the early stages in the
evolution of this group, revealing a clear case of
mosaic evolution, with some features such as the
derived upper canine morphology evolving first
within the context of a relatively generalised, feline-
like cranio-mandibular complex.
In terms of their ecology and inferred behav-
iour, proposals concerning possible social behav-
iour and group hunting in sabre-tooths remain
purely hypothetical at present. The presence of
Smilodon bones with healed injuries is considered
by some as evidence of some type of social struc-
ture in that species, but other specialists see it as
compatible with solitary behaviour. Probably the
best way to infer the presence of social behaviour
in fossil carnivores is to learn more about the bio-
logical and ecological constraints of predation,
something that requires more data from alarming-
ly shrinking wild populations of modern large car-
nivores. Current knowledge suggests that group
living and hunting may become advantageous for
all large predators that hunt large prey in relative-
ly open environments, while it may be the only
way to catch large prey for carnivores (like canids
and hyaenids) that lack powerful, muscular
forepaws for subduing prey. Such reasoning points
towards homotherins, rather than smilodontins, as
the more likely candidates for group living among
machairodontine cats.
The mosaic nature of the evolution of sabre-tooth
adaptations points towards evolutionary plasticity,
which is against the concept of rigid “ecomorphs”
that would comprise whole complexes of anatomi-
cal features of the cranial and postcranial skeleton.
In fact, the discovery of Xenosmilus, a homotheriin
with an extremely robust skeleton, confirms that the
idea of two contrasting and clear-cut ecomorphs
among sabre-tooths is too rigid to fit the diversity of
this group.
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 273
e390-11 Turner.qxd 30/1/12 14:19 Página 273
We may hope that the machairodontine cats will
continue to excite the interest of palaeontologists
and the wider public, as befits a group that exempli-
fies better than most several core concepts of evolu-
tionary biology, such as mosaic evolution, conver-
gence and the opposition between adaptation and
phylogenetic constraints. In this process of rethink-
ing the evolution of sabre-toothed felids, the contri-
bution of the Batallones fossil sites has been cru-
cial, and will continue to provide valuable insights.
We can do no better than finish with a quotation
from Leonard Ginsburg (1961, p. 1):
“Les carnivores . . . ne dépendent en principe que
de l’abondance et de la facilité de capture des
proies et se sont peu à peu adaptés, au cours des
temps géologiques, à des régimes alimentaires var-
iés, réalisés dans les circonstances très différentes.”
ACKNOWLEDGEMENTS
Thanks are due Dr. Martin Pickford for the manuscript revision.
This study is part of the research projects CGL2008-00034 and
CGL2008-05813-C02-01 (Dirección General de Investigación,
Ministerio de Ciencia e Innovación, Spain), and PICS-CNRS
4737, and the Research Group UCM-BSCH-910607. M. J. Salesa
is a contracted researcher within the “Ramón y Cajal” program
(Ministerio de Ciencia e Innovación, reference RYC2007-00128).
References
Agustí, J.; Cabrera, L.; Garcés, M. & Llenas, M. (1999).
Mammal turnover and Global climate change in the
late Miocene terrestrial record of the Vallès-Penedès
Basin (NE Spain). 390-397. In: Hominoid evolution
and climatic change in Europe, Vol. 1. (Agustí, J.,
Rook, L. & Andrews, P., eds.). Cambridge University
Press, Cambridge, 528 pp.
Akersten, W.A. (1985). Canine function in Smilodon
(Mammalia, Felidae, Machairodontinae). Los Angeles
County Museum Contributions in Science, 356: 1-22.
Alderton, D. (1998). Wild Cats of the World. London,
Blandford.
Antón, M. & Galobart, A. (1999). Neck function and pre-
datory behaviour in the scimitar toothed cat Homothe-
rium latidens (Owen). Journal of Vertebrate Paleonto-
logy, 19: 771-784.doi:10.1080/02724634.1999.
10011190
Antón, M. & Morales, J. (2000). Inferencias paleoecoló-
gicas de la asociación de carnívoros del yacimiento de
Cerro Batallones. In: Patrimonio Paleontológico de la
Comunidad de Madrid (Morales, J., Nieto, M., Ame-
zua, L., Fraile, S., Gómez, E., Herráez, E., Peláez-
Campomanes, P., Salesa, M.J., Sánchez, I.M. & Soria,
D., eds). Servicio de Publicaciones de la Comunidad
de Madrid, Madrid, 190-201.
Antón, M.; Galobart, A. & Turner, A. (2005). Co-existen-
ce of scimitar-toothed cats, lions and hominins in the
European Pleistocene. Implications of the post-cranial
anatomy of Homotherium latidens (Owen) for compa-
rative palaeoecology. Quaternary Science Reviews, 24:
1287-1301.doi:10.1016/j.quascirev.2004.09.008
Antón, M.; Garcia-Perea, R. & Turner, A. (1998). Recons-
tructed facial appearance of the sabretoothed felid Smi-
lodon. Zoological Journal of the Linnean Society, 124:
369-386. doi:10.1111/j.1096-3642.1998.tb00582.x.
Antón, M.; Salesa, M.J.; Galobart, Á.; Pastor, J.F. & Turner,
A. (2009). Soft tissue reconstruction of Homotherium
latidens (Mammalia, Carnivora, Felidae). Implications for
the possibility of representation in Palaeolithic art. Geo-
bios, 42: 541-551. doi:10.1016/j.geobios.2009.02.003
Antón, M.; Salesa, M.J.; Morales, J. & Turner, A. (2004).
First known complete skulls of the scimitar-toothed cat
Machairodus aphanistus (Felidae, Carnivora) from the
Spanish Late Miocene site of Cerro Batallones-1. Jour-
nal of Vertebrate Paleontology, 24: 957-969. doi:
10.1671/02724634(2004)024[0957:FKCSOT]2.0.CO;2
Anyonge, W. (1996). Locomotor behaviour in Plio-Pleis-
tocene sabre-tooth cats: a biomechanical analysis.
Journal of Zoology, 238: 395-413. doi:10.1111/j.1469-
7998.1996.tb05402.x
Bailey, T.N. (1993). The African Leopard: Ecology and
Behaviour of a Solitary Felid. Columbia University
Press, New York.
Bakker, R.T. (1998). Brontosaur killers: late Jurassic allo-
saurids as sabre-tooth cat analogues. Gaia, 15: 145-158.
Beaumont, G. de (1975). Recherches sur les Félidés
(Mammifères, Carnivores) du Pliocène inférieur des
sables à Dinotherium des environs d’Eppelsheim
(Rheinhessen). Archives des Sciences Physiques et
Naturelles, Genève, 28: 369-405.
Biknevicius, A.R. & Van Valkenburgh, B. (1996).
Design for killing: craniodental adaptations of preda-
tors. In: Carnivore Behaviour, Ecology and Evolution,
Vol. 2 (Gittleman, J.L., ed.). Cornell University Press,
London, 393-428.
Bohlin, B. (1940). Food habit of the machairodonts, with
special regard to Smilodon. Bulletin of the Geological
Institute of Upsala, 28: 157-174.
Bohlin, B. (1947). The sabre-toothed tigers once more.
Bulletin of the Geological Institute of Upsala, 32: 11-20.
Bothma, J & Walker, C. (1999). Large Carnivores of the
African Savannas. Springer-Verlag, Berlin.
Bravard, A. (1828). Monographie de la Montagne de
Perrier, près d’Issoire (Puy-de-Dôme) et de deux espè-
ces fossiles du genre Felis découvertes dans l’une de
ses couches d’alluvions. Clermont-Ferrand, 145 pp.
Bryant, H.N. (1991). Phylogenetic relationships and sys-
tematics of the Nimravidae (Carnivora). Journal of
Mammalogy, 72: 56-78. doi:10.2307/1381980
Bryant, H.N. (1996). Force generation by the jaw adduc-
tor musculature at different gapes in the Pleistocene
sabretoothed felid Smilodon. In: Palaeoecology and
Palaeoenvironments of Late Cenozoic Mammals (Ste-
wart, K.M. & Seymour, K.L., eds.). Toronto: Univer-
sity of Toronto Press, Toronto, 283-299.
274 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
e390-11 Turner.qxd 30/1/12 14:19 Página 274
Carbone, C.; Maddox, T.; Funston, P.J.; Mills, M.G.L.;
Grether, G.F. & Van Valkenburg, B. (2009). Parallels
between playbacks and Pleistocene tar seeps suggest
sociality in an extinct sabretooth cat, Smilodon. Royal
Society Biology Letters, 5: 81-85.
Chang, H. (1957). On new material of some machairo-
donts of Pontian age from Shansi. Vertebrata Palasia-
tica, 1:193-200.
Cuvier, G. (1824). Recherches sur les ossements fossiles,
où l’on rétablit les caractères de plusieurs animaux
dont les révolutions du globe ont détruit les espèces,
Vol 5. Edmund d’Ocagne, Paris, 547 pp.
Daniel, J.C. (1996). The Leopard in India. A Natural
History. Natraj Publishers, Allahabad.
Dawson, M.R.; Stucky, R.K.; Krishtalka, L. & Black,
C.C. (1986). Machaeroides simpsoni, new species,
oldest known sabertooth creodont (Mammalia), of Lost
Cabin Eocene. Contributions to Geology, University of
Wyoming, Special Paper, 3: 177-182.
Durant, S.M. (2000). Predator avoidance, breeding expe-
rience and reproductive success in endangered chee-
tahs, Acinonyx jubatus. Animal Behaviour, 60: 121-
130. doi:10.1006/anbe.2000.1433
Fortelius, M.; Eronen, J.; Jernvall, J.; Liu, L.; Pushinka,
D.; Rinne, J.; Tesakov, A.; Vislobokova, I.; Zhang, Z.
& Zhou, L. (2002). Fossil mammals resolve regional
patterns of Eurasian climate change over 20 million
years. Evolutionary Ecology Research, 4: 1005-1016.
Ginsburg. L. (1961). Plantigradie et digitigradie chez les
carnivores fissipedes. Mammalia, 25 (1): 1-21.
doi:10.1515/mamm.1961.25.1.1
Ginsburg, L.; Morales, J. & Soria, D. (1981). Nuevos
datos sobres los carnivoros de Los Valles de Fuenti-
dueña, Segovia. Estudios Geologicos, 37: 383-415.
Gittleman, J.J. & Van Valkenburgh, B. (1997). Sexual
dimorphism in the canines and skulls of carnivores:
effects of size, phylogeny, and behavioural ecology.
Journal of Zoology, 242: 97-117. doi:10.1111/j.1469-
7998.1997.tb02932.x
Hanby, J.P. & Bygott, J.D. (1979). Population changes in
lions and other predators. In: Serengeti, Dynamics of an
Ecosystem (Sinclair, A.R.E. & Norton-Griffiths, M.,
eds.). University of Chicago Press, Chicago, 248-262.
Heald, F. (1989). Injuries and diseases in Smilodon cali-
fornicus. Journal of Vertebrate Paleontology, 9: 24A.
Hunt, R.M. (1987). Evolution of the aeluroid Carnivora:
significance of the auditory structure in the nimravid
cat, Dinictis. American Museum Novitates, 2886: 1-74.
Guggisberg, C.A.W. (1975). Wild Cats of the World.
David and Charles, London.
Kurtén, B. (1968). Pleistocene Mammals of Europe.
Weidenfeld and Nicolson, London.
Kurtén, B. & Anderson, E. (1980). Pleistocene Mammals
of North America. Columbia University Press, New
York.
Larson, S.E. (1997). Taxonomic re-evaluation of the jaguar.
Zoo Biology, 16: 107-120. doi:10.1002/(SICI)1098-
2361(1997)16:2<107::AID-ZOO2>3.0.CO;2-E
MacCall, S.; Naples, V. & Martin L. (2003). Assessing
Behavior in Extinct Animals: Was Smilodon Social?
Brain Behavior and Evolution, 61: 159-164.
doi:10.1159/000069752
Macdonald, D.W. (Ed.) (1984). The Encyclopedia of Mam-
mals. New York: Facts on File Publications. 895 pp.
Marean, C.W. (1989). Sabertooth cats and their relevan-
ce for early hominid diet and evolution. Journal of
Human Evolution, 18: 559-582. doi:10.1016/0047-
2484(89)90018-3
Martin. L.D. (1989). Fossil history of the terrestrial Car-
nivora. In: Carnivore Behaviour, Ecology and Evolu-
tion (Gittleman, J.L., ed.). Chapman and Hall, London,
535-568. doi:10.1007/978-1-4613-0855-3_20
Martin. L.D.; Babiarz, J.P.; Naples, V.L. & Hearst, J.
(2000). Three Ways to be a Sabertoothed Cat. Natur-
wissenschaften, 87: 41-44. doi:10.1007/s001140050007
McHenry, C.R.; Wroe, S.; Clausen, P.D.; Moreno, K. &
Cunningham, E. (2007). Supermodeled sabercat, pre-
datory behaviour in Smilodon fatalis revealed by high-
resolution 3D computer simulation. Proceedings of the
National Academy of Sciences, 104 (41): 16010-16015.
doi:10.1073/pnas.0706086104
Merriam, J.C. & Stock, C. (1932). The Felidae of Ran-
cho La Brea. Carnegie Institute of Washington Publi-
cations, 442: 1-231.
Miller, G.J. (1969). A new hypothesis to explain the met-
hod of food ingestion used by Smilodon californicus
Bovard. Tebiwa, 12: 9-19.
Morales, J.; Salesa, M.J.; Pickford, M. & Soria, D.
(2001). A new tribe, new genus and two new species of
Barbourofelinae (Felidae, Carnivora, Mammalia) from
the Early Miocene of East Africa and Spain. Transac-
tions of the Royal Society of Edinburgh: Earth Scien-
ces, 92: 97-102. doi:10.1017/S0263593300000067
Morlo, M.; Peigné, S. & Nagel, D. (2004). A new species
of Prosansanosmilus: implications for the systematic
relationships of the family Barbourofelidae new rank
(Carnivora, Mammalia). Zoological Journal of the Lin-
nean Society, 140: 43-61. doi:10.1111/j.1096-
3642.2004.00087.x
Morse, D.H. (1974). Niche breadth as a function of
social dominance. American Naturalist, 108: 808-813.
doi:10.1086/282957
Nuñez, R.; Miller, B. & Lindzey, F. (2000). Food habits
of jaguars and pumas in Jalisco, Mexico. Journal of
Zoology, 282: 373-379.
Packer, C. (1986). The ecology of sociability in felids.
In: Ecological Aspects of social Evolution: Birds and
Mammals (Rubenstein D.I. & Wrangham R.V., eds.).
Princeton university Press, Princeton, 429-451.
Packer, C.; Scheel, D. & Pusey, A. (1990). Why lions
form groups: food is not enough. American Naturalist,
136: 1-19. doi:10.1086/285079
Rabinowitz, A.R. & Nottingham, B.G. (1986). Ecology
and behaviour of the jaguar (Panthera onca) in Belize,
Central America. Journal of Zoology, 210: 149-159.
doi:10.1111/j.1469-7998.1986.tb03627.x
Riabinin, A. (1929). Faune de mammifères de Taraklia.
Carnivore vera, Rodentia, Subungulata. Travaux du
Musée de Géologie de l’Académie des Sciences
d’URSS, 5: 75-134.
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
Changing ideas about the evolution and functional morphology of Machairodontine felids 275
e390-11 Turner.qxd 30/1/12 14:19 Página 275
Riviere, H.L. & Wheeler, H.T. (2005). Cementum on
Smilodon sabers. The Anatomical Record, 285A: 634-
642. doi:10.1002/ar.a.20199
Salesa, M.J.; Antón, M.; Turner, A. & Morales, J.
(2005). 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. Zoological Journal of the Linnean Society, 144:
363-377. doi:10.1111/j.1096-3642.2005.00174.x
Salesa, M.J.; Antón, M.; Turner, A. & Morales, J.
(2006). Inferred behaviour and ecology of the primi-
tive sabre-toothed cat Paramachairodus ogygia
(Felidae, Machairodontinae) from the Late Miocene
of Spain. Journal of Zoology, 268: 243-254.
doi:10.1111/j.1469-7998.2005.00032.x
Salesa, M.J.; Antón, M.; Turner, A.; Alcalá, L.; Mon-
toya, P.; Morales, J. (2010a) Systematic revision of
the Late Miocene sabre-toothed felid Paramachae-
rodus in Spain. Palaeontology, 53 (6): 1369-1391.
doi:10.1111/j.1475-4983.2010.01013.x
Salesa, M. J.; Antón, M.; Turner, A. & Morales, J. (2010b).
Functional anatomy of the forelimb in the primitive felid
Promegantereon ogygia (Machairodontinae, Smilodonti-
ni) from the Late Miocene of Spain and the origins of the
saber-toothed felid model. Journal of Anatomy, 216:
381-396. doi:10.1111/j.14697580.2009.01178.x
Sankhala, K. (1978). Tiger!. Collins, London.
Schaller, G.B. (1972). The Serengeti Lion. A Study of
Predator-Prey Relations. University of Chicago Press,
Chicago.
Schmidt-Kittler, N. (1976). Raubteiere aus dem Junter-
tiär Kleinasiens. Palaeontographica, 155: 1-131.
Scott, W.B, & Jepsen, G.L. (1936). The mammalian
fauna of the White river Oligocene. Part I-Insectivora
and Carnivora. Transactions of the American Philo-
sophical Society, new series, 28: 1-153.
Seidensticker, J. (1976). On the ecological separation
between tigers and leopards. Biotropica, 8: 225-234.
doi:10.2307/2989714
Simpson, G.G. (1941). The function of sabre-like canines
in carnivorous mammals. American Museum Novita-
tes, 1130: 1-12.
Sotnikova, M. (1992). A new species of Machairodus
from the late Miocene Kalmakpai locality in eastern
Kazakhstan (USSR). Annales Zoologici Fennici, 28:
361-369.
Sunquist M.E. & Sunquist F.C. (1989). Ecological cons-
trains on predation by large felids. In: Carnivore Beha-
vior, Ecology and Evolution (Gittleman J. L., ed.).
Chapman & Hall, London, 220-245. doi:10.1007/978-
1-4613-0855-3_11
Turnbull-Kemp, P. (1967). The Leopard. Howard Tim-
mins, Cape Town
Turner, A. (1984). Dental sex dimorphism in European
lions (Panthera leo L) of the Upper Pleistocene: palae-
oecological and palaeoethological implications. Anna-
les Zoologici Fennici, 21: 1-8.
Turner, A. (1993). New fossil carnivore remains. In:
Swartkrans: a Cave’s Chronicle of Early Man (Brain,
C.K., ed.). Transvaal Museum Monograph No. 8, Pre-
toria, 151-165.
Turner, A. & Antón, M. (1999). Climate and evolution:
implications of some extinction patterns in African and
European machairodontine cats of the Plio-Pleistocene.
Estudios Geologicos, 54: 209-230.
Turner, A. & Antón, M. (2004). Evolving Eden: An Illus-
trated Guide to the Evolution of the African Large
Mammal Fauna. Columbia University Press, New York.
Van Valkenburgh, B. & Sacco, T. (2002). Sexual
dimorphism, social behavior, and intrasexual
competition in large Pleistocene carnivorans.
Journal of Vertebrate Paleontology, 22: 164-
169. doi: 10.1671/02724634(2002)022[0164:
SDSBAI]2.0.CO;2
Wroe, S., Lowry, M.B. & Antón, M. (2008). How to
build a mammalian super-predator. Zoology, 111: 196-
203. doi:10.1016/j.zool.2007.07.008
Recibido el 16 de febrero de 2011
Aceptado el 29 de agosto de 2011
276 A. Turner, M. Antón, M.J. Salesa, J. Morales
Estudios Geológicos, 67(2), 255-276, julio-diciembre 2011. ISSN: 0367-0449. doi:10.3989/egeol.40590.188
e390-11 Turner.qxd 30/1/12 14:19 Página 276