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Inferred behaviour and ecology of the primitive sabre-toothed cat Paramachairodus ogygia (Felidae,Machairodontinae) from the Late Miocene of Spain
M. J. Salesa1, M. Antón2, A. Turner1 & J. Morales2
1 School of Biological and Earth Sciences, Liverpool John Moores University, Liverpool, UK
2 Departamento de Paleobiologı́a, Museo Nacional de Ciencias Naturales-CSIC, Madrid, Spain
Keywords
behaviour; ecology; Felidae; Miocene;
Paramachairodus.
Correspondence
Manuel J. Salesa, School of Biological and
Earth Sciences, Byrom Street, Liverpool
John Moores University, Liverpool L3 3AF,
UK.
Email: [email protected]
Received 25 January 2005; accepted 17 May
2005
doi:10.1111/j.1469-7998.2005.00032.x
Abstract
The Late Miocene (Late Vallesian, MN 10, about 9Mya) carnivore trap of
Batallones-1 (Madrid, Spain) has yielded a large sample of two species of sabre-
toothed cats: the puma-sized Paramachairodus ogygia and the tiger-sized
Machairodus aphanistus. This has allowed, for the first time, complete studies of
the biomechanics and comparative anatomy of these animals. Focusing our study
on the small species, Par. ogygia, the most richly represented and best known
carnivore from Batallones-1, we attempt to infer some aspects of the behaviour
and ecology of this early sabre-toothed cat, such as breeding behaviour, the degree
of social interaction between individuals, sexual dimorphism, preferred habitat
and prey size. Our results suggest that Par. ogygia was a solitary felid with a low
sexual dimorphism index, which in turn indicates low competition between males
for access to females, and some degree of tolerance between adults, so that young
adults were allowed to share the territory of their mothers for some time
after maturity. The machairodont adaptations of Par. ogygia indicate that
this species was able to subdue and kill prey in less time than pantherines do,
thus minimizing the risk of injury and the energetic costs of this action. In a
wider context, the carnivore guild of Batallones-1 and the overall mammal
community indicate that the landscape around the trap was a wooded habitat.
Batallones-1 is thus establishing itself as one of the most important European Late
Miocene fossil localities, not only for the study of the anatomy and biomechanics
of the early sabre-toothed cats but also for our understanding of the intra- and
inter-specific ecological relationships of the first members of this specialized sub-
family of felids.
Introduction
Inferences about the palaeobiology of fossil carnivores can
be made based on field studies of extant species. However,
because this group of mammals is not usually well repre-
sented in fossil sites, it is rare that these studies can include
inferences about population structure, sexual dimorphism
or age group representation. The Late Miocene (Late
Vallesian, MN 10) carnivore trap of Batallones-1 (Madrid,
Spain) has yielded a large sample of several species of
carnivorans, and is now one of the most important Eur-
opean localities for investigation of the mammalian com-
munities of that epoch. The site was formed as an irregular
cavity in sepiolite levels, later filled with greenish clay. It
acted as a natural trap for many animals, attracting mainly
Carnivora (98% of the total macromammal sample in
number of bones) that were probably trapped while at-
tempting to scavenge (Fig. 1). Among them, abundant
remains of two species of sabre-toothed cats have been
found: Paramachairodus ogygia (Kaup, 1832) and Machair-
odus aphanistus (Kaup, 1832). We focus our study on the
former, which is the most richly represented carnivoran of
the Batallones-1 sample. This species was previously one of
the most poorly known Late Miocene machairodontines,
but thanks to the large amount of available skeletal ele-
ments, it is now possible to infer many aspects of its
biomechanics (Salesa, 2002; Salesa et al., 2005) and palaeoe-
cology.
The walls of sepiolite of the trap made escape very
difficult, because when this mineral is wet its surface
becomes slippery, and under these conditions, even big cats
were not able to climb out. Because the cavity was being
filled with clay, the bottom of the trap would have been
covered with wet mud, which would have hindered the
movement of animals and probably induced hypothermia,
contributing to their more or less rapid death (Morales
et al., 2000, 2004; Salesa, 2002; Antón et al., 2003). At least
seven additional and contemporaneous cavities have been
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London 243
Journal of Zoology. Print ISSN 0952-8369
identified in the Batallones area, and although only Batal-
lones-1 has been thoroughly excavated all of them fit with a
general geological process of piping, which in this case
consisted of the erosion of sepiolite levels by water along
fractures, causing collapses and the development of karst-
like (‘pseudokarst’) topography, already described in other
areas by Halliday (1960). This is the major project respon-
sible for the formation of the Batallones fossil site complex
(Antón et al., 2003; Morales et al., 2004; Pozo et al., 2004),
providing one of the most complete samples of Late Mio-
cene sabre-toothed cats.
Materials and methods
All the skeletal remains of the mammals of Batallones-1,
including the sample of Par. ogygia analysed in this study,
are held in the collections of the Museo Nacional de
Ciencias Naturales-CSIC (Madrid, Spain). Measurements
were taken using a digital calliper. Data on the minimum
number of individuals (MNI) of each species of carnivoran
were taken from Antón & Morales (2000). The sexual
dimorphism index of Par. ogygia was calculated following
the ‘average method’ of Van Valkenburgh & Sacco (2002),
which is based on four measurements of skull and dentition;
this method, which divides the sample into two sub-samples,
‘males’ and ‘females’, offers a good indication of the size
divergence between the sexes.
The body weight of Par. ogygia was estimated by Salesa
(2002) as 28–65 kg, which is within the range of an
extant puma. There were no previous estimates of the body
weight of M. aphanistus, so we used the regression formula
of Van Valkenburgh (1990) for Felidae to estimate it on the
base of the skull basal length of six individuals from
Batallones-1 (Table 1). The results, between 100 and
240 kg, placed M. aphanistus within the range of extant
tigers and lions.
The mammal sample fromBatallones-1
The faunal association of Batallones-1 is one of the richest
of the Late Miocene of Eurasia, and includes fishes, amphi-
bians, reptiles, birds and mammals (Morales et al., 2000,
2004). Nevertheless, the majority of the sample (98% of the
total bone sample) is of Carnivora. This is unusual in fossil
localities, because with carnivorans totalling about 11% of
the total mammal biomass in extant ecosystems (White
et al., 1984), the presence of this group in the fossil samples
usually totals around 7% of individuals (White et al., 1984;
Antón & Morales, 2000). The existence of such a large
proportion of carnivorans in Batallones-1 is explained as a
consequence of the presence of carcasses of animals that had
died within the trap (Antón &Morales, 2000; Morales et al.,
2000; Salesa, 2002). The absence of significant water flow
Figure 1 Reconstruction of the Batallones-1
natural trap. Within the trap, two adult
Machairodus aphanistus fight over a carcass
of the rhinoceros Aceratherium incisivum, in
the presence of a juvenile. Outside the trap,
on the left, a small feline cat pursues a lago-
morph of the genus Prolagus. In the centre, an
individual of Paramachairodus ogygia looks at
the trap from a branch, whereas on the right
side three individuals of the hyaenid Protic-
titherium crassum remain in the distance.
Above, a group of vultures await their chance
(art by I. M. Sánchez).
Table 1 Estimated body weight of Machairodus aphanistus from
Batallones-1: BL (skull), basal length of the skull, measured from the
anterior border of incisors to the anterior margin of foramen magnum
Number BL (Skull) Body weight (kg)
B-4272 257.0 130.28
B-1523 237.0 101.27
B-4711 310.0 233.42
B-5445 313.0 240.52
B-4151(1) 264.0 141.64
B-6046 246.0 113.71
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London244
Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.
after the accumulation of the sample prevented the total
disarticulation of the skeletons, allowing excellent preserva-
tion of the fossils and the presence of practically complete
skeletons (Morales et al., 2000, 2004).
The most abundant components of the mammal fauna of
Batallones-1, around 29% of the total (Fig. 2), are the sabre-
toothed cats, with two species represented: the puma-sized
Par. ogygia, with at least 18 individuals recorded (16% of
the mammal palaeocommunity) (Figs 2 and 3), and the
tiger-sized M. aphanistus, with 14 individuals (13% of the
mammal palaeocommunity) (Figs 2 and 3; Table 2) (Antón
& Morales, 2000). There are two species of primitive felines,
one of Felis-size and other of Lynx-size; they represent only
4% of the sample (Figs 2 and 4). The bear-dog Amphicyon
sp. aff. A. castellanus Ginsburg, Morales & Soria (1981) is
relatively abundant, with at least 12 individuals (11% of the
mammal sample) (Figs 2 and 5). The primitive hyaenid
Figure 2 Relative abundance of the different
groups of mammals present in the
Batallones-1 sample.
Figure 3 Fossil Carnivora from Batallones-1: (a) B-4778, skull and
mandible of Paramachairodus ogygia in lateral view; (b) B-5445, skull
and mandible of Machairodus aphanistus in lateral view.
Table 2 Minimum number of individuals (MNI) for the main mammal
groups represented in the Batallones-1 palaeocommunity
Species MNI (A) MNI (J) MNI (T)
Insectivora 8 1 9
Rodentia indet. 7 0 7
Castoridae 1 0 1
Prolagus crusafonti 16 0 16
Simocyon batalleri 2 0 2
Martes sp. 2 0 2
Proputorius sp. 1 0 1
Sabadellictis sp. 2 0 2
Mustelidae indet. 1 0 1
Amphicyon sp. aff. A. castellanus 6 6 12
Protictitherium crassum 9 0 9
Felinae indet. sp. 1 1 0 1
Felinae indet. sp. 2 2 1 3
Paramachairodus ogygia 17 1 18
Machairodus aphanistus 12 2 14
Tetralophodon longirostris 1 0 1
Hipparion sp. 4 0 4
Aceratherium incisivum 3 0 3
Microstonyx sp. 0 1 1
Cervidae indet. 1 0 1
Hispanomeryx sp. 2 0 2
MNI (A), minimal number of adult individuals; MNI (J), minimal
number of juvenile individuals; MNI (T), minimal number of total
individuals.
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London 245
Behaviour and ecology of Paramachairodus ogygiaM. J. Salesa et al.
Protictitherium crassum (Depéret, 1892), with nine indivi-
duals (8%), is the fourth most abundant Carnivora (Figs 2
and 3), whereas the ailurid Simocyon batalleri (Viret, 1929)
(Fig. 5) is one of the less represented, with only two
individuals (2%) (Peigné et al., 2005). Mustelids total 6%
of the sample, being represented by four species, the marten
Martes sp., two skunks (Sabadellictis sp. and Proputorius
sp.) and one undetermined species. It is noticeable that the
fossil pika (Lagomorpha) Prolagus crusafonti (López
Martı́nez, 1975) (in López Martı́nez & Thaler, 1975) is
almost as abundant as Par. ogygia, with 16 individuals and
15% of the total mammal community. The micro-mammal
fauna of Batallones-1 also includes insectivores (8% of the
sample), such as the moonrat Galerix sp. and two other
undetermined species, and rodents (7%), such as the squirrel
Spermophilinus sp., the beaver Steneofiber sp., the mouse
Progonomys hispanicus Michaux, 1971 and two species of
undetermined cricetid (hamsters) and zapodid (jumping
mice). The presence of the mouse Prog. hispanicus dates this
locality to the early part of the Late Miocene, Neogene
European Land Mammal Zone 10 (MN 10) of Mein (1975),
about 9 million years ago (Morales et al., 2000).
The mammal association also includes a small number of
ungulate taxa; these are the mastodont Tetralophodon long-
irostris Kaup, 1832 (representing only 1% of the total
sample), the hornless rhinoceros Aceratherium incisivum
Kaup, 1832 (3%), the tridactyl equid Hipparion sp. (4%),
the hornless ruminantHispanomeryx sp. (2%), the giant pig
Microstonyx sp. (only 1%) and two species of undetermined
cervids and bovids (1%) (Morales et al., 2000, 2004).
Discussion
Habitat preference in big cats
The three-dimensional structure of the habitat, which can be
highly variable, clearly determines several aspects of mam-
malian behaviour (Eisenberg & Lockhart, 1972; Geist,
1974). Among large cats, some species such as jaguar
Panthera onca, clouded leopard Neofelis nebulosa and tiger
Panthera tigris are mainly found in highly structured habi-
tats, typically dense forest (Mazák, 1981; Seymour, 1989;
Turner & Antón, 1997; Alderton, 1998). However, the tiger
can also be found in the ecotone between forest and grass-
land, or even in mountain valleys of pine woods in Man-
churia and near the Amur river (Mazák, 1981), and jaguars
have been reported in low-structured habitats such as
deserts and prairies (Seymour, 1989), while leopards
Panthera pardus and pumas Puma concolor can occupy a
range of very different habitats, from arid savannas to dense
tropical forests (Currier, 1983; Nowak & Paradiso, 1983;
Johnson et al., 1993; Alderton, 1998; Bothma & Walker,
1999). Lions Panthera leo and cheetahs Acinonyx jubatus are
found in low-structured habitats, such as savannas or grass-
lands with some shrub coverage (Nowak & Paradiso, 1983;
Alderton, 1998; Bothma &Walker, 1999). The snow leopard
Uncia uncia also occupies low-structured habitats, such as
rocky areas in Asia between 1400 and 3200m of altitude,
occasionally reaching 4300m (Hemmer, 1972; Gonyea,
1976a; Nowak & Paradiso, 1983; Alderton, 1998).
Figure 4 Fossil Carnivora from Batallones-1: (a) B-2800 skull and
mandible of Protictitherium crassum in lateral view; (b) B-2075, skull
and mandible of Martes sp. in lateral view; (c) B-5446, skull and
mandible of a juvenile individual of Felinae indet. in lateral view.
Figure 5 Fossil Carnivora from Batallones-1: (a) B-3620 skull of
Simocyon batalleri in ventral view; (b) B-4071, skull of Amphicyon
sp. aff. A. castellanus in ventral view.
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London246
Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.
Although the habitat preference of some species of felids
may be variable, they can probably be considered to derive
from closed habitat dwellers (Turner & Antón, 1997). In
general, felids have not derived too much from the primitive
body plan of the Early Miocene forms (Helbing, 1928;
Beaumont, 1961; Turner & Antón, 1997), such as Proailurus
lemanensis (Filhol, 1879) and although there are some
cursorial forms, such as Aci. jubatus or to a lesser extent,
U. uncia (Turner & Antón, 1997), felids lack the adaptations
to sustained terrestrial locomotion in open environments
seen in some other Carnivora, such as canids or hyaenids.
Inferences on the habitat of Batallones-1
The fact that sabre-toothed felids are the most abundant
Carnivora of the Batallones-1 sample (Table 2) has ecologi-
cal implications, because classical studies of vertebrate
ecology have shown that intra- and inter-specific compe-
tition for resources produce different patterns of habitat use
(Lack, 1945; MacArthur, 1958; Lanciani, 1970; Laerm,
1974; Gonyea & Ashworth, 1975; Rabinowitz & Nottingham,
1986; Bothma & Walker, 1999; Palomares & Caro, 1999).
According to this, when different species of extant felids live in
sympatry a marked segregation exists between them, with the
small-sized species constantly avoiding encounters with the
large ones, which can be very violent. It is known that lions
and leopards kill adults and cubs of other felids, and that
leopards 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 cats occurs in habitats with
some tree cover, which allows the smaller species to take
refuge in the trees from the attack of the larger one and so
avoid having its prey stolen or being killed (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 open
environments, sympatry is possible because cheetahs con-
stantly 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 continent
(Nuñez, Miller & Lindzey, 2000), but this is only possible
when resources are rich enough to allow the maintenance of
both species, which develop a marked ecological segregation
between them mainly based on the avoidance of adult
encounters (Rabinowitz & Nottingham, 1986; Nuñez et al.,
2000).
In summary, the sympatry of two large cat 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 facilitated
by the fact that leopards preferably occupy wooded sections
of the habitat, less favourable for lions (Bailey, 1993). The
body proportions of Par. ogygia andM. aphanistus are very
similar to those of the extant pantherine cats (Salesa, 2002;
Antón et al., 2003), probably reflecting similar habitat
preferences, that is, wooded environments. The predomi-
nance of Par. 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). Preliminary observations of the
post-cranial remains of the two species of small feline cats
from Batallones-1 show them to be relatively gracile and
thus comparable with extant species such as Felis sylvestris,
Felis lybica and Lynx pardinus. These extant species occupy
a wide range of habitats (Kitchener, 1991; Antón & Mor-
ales, 2000), so the presence of these felines in Batallones-1
does not allow precise ecological interpretations. Never-
theless, the high diversity of felids in this locality implies a
segregation of niches between the different species, much
more probable in a wooded environment.
Among the Mustelidae, the extant species of the genus
Martes are associated with forested habitats (Nowak &
Paradiso, 1983) and, although some species can occupy
rocky areas, prairies and riversides, they always avoid
treeless environments (Powell, 1981; Clark et al., 1987).
Thus, the presence of marten in Batallones-1 supports the
notion of a wooded habitat for this locality. Extant skunks
occupy a wide range of habitats (Nowak & Paradiso, 1983;
Antón & Morales, 2000), so that the presence of Sabadellic-
tis and Proputorius in Batallones-1 gives little information
about the palaeohabitat of the trap surroundings.
The only extant Ailuridae is the red panda, Ailurus
fulgens, which inhabits the forests of China, Nepal and
Burma (Nowak & Paradiso, 1983; Roberts & Gittleman,
1984). Its diet consists mainly of bamboo, but it also
includes insects, small mammals, eggs, fruits and leaves
(Nowak & Paradiso, 1983; Roberts & Gittleman, 1984).
Nevertheless, although S. batalleri is thought to be related to
Ai. fulgens (Wang, 1997), it has a very different dentition
that seems to be adapted to a diet based on flesh and carrion
(Baskin, 1998; Antón & Morales, 2000; Salesa & Fraile,
2000) and probably included small vertebrates (Peigné et al.,
2005). This animal does not show any cursorial adaptations
in its appendicular skeleton, so it is probable that it
inhabited at least moderately wooded areas.
The population of Amphicyon sp. aff. A. castellanus from
Batallones-1 is one of the richest samples of bear-dogs
known in the European fossil record (Morales et al., 2000).
Amphicyonids were powerfully built carnivorans, from the
size of a wolf to that of a brown bear, which inhabited North
America and Eurasia during the Oligocene and Miocene.
Their dentitions show adaptations to a carnivorous diet, but
also have strong post-carnassial teeth, probably reflecting
their abilities as both scavengers and hunters. Nevertheless,
the dentition of the Batallones-1 Amphicyon is more hyper-
carnivorous than that of previous species of this
genus, probably reflecting a late adaptation of this species
to more active hunting (Morales et al., 2000; Salesa & Fraile,
2000).
Protictitherium crassum is an early and primitive member
of the family Hyaenidae (Werdelin & Solounias, 1991), with
the approximate size and proportions of the extant African
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London 247
Behaviour and ecology of Paramachairodus ogygiaM. J. Salesa et al.
civet, Civettictis civetta (Antón & Morales, 2000). The latter
inhabits both forested and more or less open environments,
but always with enough vegetational cover to find refuge
(Nowak & Paradiso, 1983; Ray, 1995). The dentition of
Prot. crassum does not show the adaptations to bone
cracking seen in the later hyaenids, and it probably would
have been an opportunistic carnivoran, with a diet and
behaviour more similar to that of a jackal than to that of
an extant hyaenid.
The herbivore sample of Batallones-1 is scarce (12% of
the total sample), although the presence of some taxa with
low cheek teeth, such as cervids, mastodonts, Hispanomer-
yx, and Aceratherium, suggest the presence of a wooded
habitat. It is also noticeable that the most probable grazers
or at least mixed-feeders, Hipparion and the bovids, are
really rare in the sample.
In summary, the faunal association of Batallones-1 sug-
gests a wooded habitat for this locality, probably a more or
less dense woodland, with enough cover to allow the
sympatry of two species of large felids, the presence of
several species of small carnivorans (which need some cover
to protect them from the attack of the large predators) and
the feeding of large browsers such as mastodonts or rhinos.
Other factors, such as the presence of bovids and hippar-
ionine horses, indicate the presence of more open, grassy
patches in the vicinity of the site.
Sociability and sexual dimorphism in Felidae
Social behaviour in felids
Most of the extant felines lead solitary lives, and only in the
breeding season do they form pairs that last only a few
weeks (Nowak & Paradiso, 1983; Alderton, 1998; Bothma &
Walker, 1999). Only lions have the kind of behaviour that
can be considered as social (Leyhausen, 1979; Caro, 1989,
1994), although it has been observed that tigers inhabiting
open environments can form groups, and male cheetahs
often form coalitions (Alderton, 1998; Bothma & Walker,
1999). Nevertheless, none of the species live in complete
isolation, because they use several types of marks to keep in
contact with other individuals. These may be scent (territor-
ial marking with urine), visual (scratching on trees) or vocal,
used singly or in combination (Nowak & Paradiso, 1983;
Bailey, 1993; Daniel, 1996; Alderton, 1998).
Felids are highly territorial animals, that is, they occupy
very well-delimitated areas (home ranges or territories) that
are defended against other adults of the same species. Each
individual marks the limits of its range in order to show that
the area is occupied (Bailey, 1993; Turner & Antón, 1997;
Alderton, 1998). In most of the species, male territories
include several, smaller female territories (Rabinowitz &
Nottingham, 1986; Bailey, 1993). There are some excep-
tions, such as lions, in which groups of two to five related
males defend a huge range occupied by a pride of related
females (Nowak & Paradiso, 1983; Alderton, 1998; Bothma
&Walker, 1999). Cheetah male coalitions may include non-
related individuals (Nowell & Jackson, 1996), and can
occupy territories of between 12 and 150 km2 that include
the smaller female territories. There are also solitary cheetah
individuals that do not defend territories, moving through
huge areas (Nowak & Paradiso, 1983; Nowell & Jackson,
1996), but in other cases groups of 14 individuals have been
reported in areas in which lions and hyaenas have been
exterminated (Nowell & Jackson, 1996).
Territory size in large cats is variable, because it depends
on the sex and age of the owner, and available prey biomass
(Currier, 1983; Bailey, 1993). Thus, the territory of a male
leopard can vary between 16.4 and 96.1 km2, and that of a
female between 5.6 and 29.9 km2 (Bailey, 1993). A pride of
lions can occupy a territory as large as 470 km2 (Bothma &
Walker, 1999), whereas the territories of male tigers vary
between 380 km2 in the case of Indian individuals and the
1000 km2 of those from central Asia (Mazák, 1981). Male
jaguars have territories of between 28 and 40 km2, whereas
those of females tend to be around 10 km2 (Rabinowitz &
Nottingham, 1986; Seymour, 1989). Male pumas tend to
have larger territories than females, but in both cases they
are highly variable, between 96 and 243 km2 (Currier, 1983).
Sexual dimorphism in felids
Sexual dimorphism in mammals has been associated with a
high level of competition between males for access to
females (Short & Balaban, 1994; Weckerly, 1998). Among
the Carnivora, sexual dimorphism is more marked in canine
size than in other dental features or skull size, and these
differences can be related to the breeding system. Species in
which a male defends a group of females tend to be more
dimorphic than those with monogamous pairs or groups of
males and females (Gittleman & Van Valkenburgh, 1997;
Weckerly, 1998; Van Valkenburgh & Sacco, 2002). Felids
are dimorphic animals, but mainly in reference to body size,
with the mane of male lions being a unique example of
morphological variation between sexes among the family.
Table 3 shows the sexual dimorphism index for several
species of extant Felinae and the sabre-toothed cats
Smilodon fatalis, Par. ogygia and M. aphanistus. The most
dimorphic species are Pan. pardus and Pan. leo, which is
very interesting in view of the different breeding system of
these two felids. Lions have a very competitive system, with
males defending a large group of females (Alderton, 1998;
Bothma & Walker, 1999), which would explain the high
sexual dimorphism index (Bertram, 1979; Van Valkenburgh
& Sacco, 2002). On the other hand, leopards are basically
solitary animals, probably more so than any other panther-
ine (Bailey, 1993), which suggests that there is no clear
relationship between the sexual dimorphism index and the
presence of social systems in Felidae.
The development of sociability in felids has been seen as
associated with the habitat and prey biomass rather than the
breeding system (Turner & Antón, 1997; Alderton, 1998;
Funston et al., 1998). Thus, the social behaviour of lions has
been explained as a consequence of their special habitat,
much more low-structured than that of other felids; for a
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London248
Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.
hunter of this size, the formation of groups would be an
advantage to hunt large prey in high-visibility environments
(Turner & Antón, 1997; Alderton, 1998), and to defend
territory and cubs (Bothma & Walker, 1999). For Hemmer
(1978), the difference in the habitat occupied by lions and
tigers, much more closed in the latter, would explain why
tigers do not develop social behaviour, as the brains of both
species are very similar in weight and internal structure.
In leopards, female territories are included into larger
territories, defended by one male, and the territories of two
neighbour males never overlap, male encounters being very
aggressive (Rabinowitz & Nottingham, 1986; Bailey, 1993).
This implies that, in theory, a female only breeds with the
resident male in a breeding system with a high level of
competition between males. In jaguars, as in leopards,
females occupy territories included in those of males, but
neighbouring male territories usually overlap, although
aggressive encounters are very rare (Rabinowitz & Notting-
ham, 1986; Seymour, 1989). Thus, jaguar males show a
higher level of tolerance than male leopards, and this could
explain the lower sexual dimorphism index of jaguars.
Pumas have the same sexual dimorphism index as jaguars
and also similar territorial behaviour: males defend huge
areas and they do not tend to have any contact with other
males (Currier, 1983), although the home ranges do overlap
(Nowak & Paradiso, 1983). Females are highly tolerant of
the presence of other individuals, except when they have
cubs, and their ranges widely overlap with those of the
neighbour adults (Nowak & Paradiso, 1983).
Cheetahs exhibit a higher degree of sociability, with males
usually forming groups of three that can include non-related
individuals (Nowell & Jackson, 1996). There is no competi-
tion between males for access to females, and males simply
breed with those females that enter their area (Nowell &
Jackson, 1996). There is no active defence of territory, and,
although they mark the limits by urine and scratching, each
group of males tries not to come into contact with others
(Nowak & Paradiso, 1983). Finally, the least dimorphic
felids of the modern sample studied, Caracal caracal and
Leptailurus serval, are both supposed to be solitary, with
male ranges including those of the females (Nowell &
Jackson, 1996). Nevertheless, groups of caracals composed
of juveniles and adults have been reported (Nowak &
Paradiso, 1983; Nowell & Jackson, 1996; Alderton, 1998).
Among the fossil Felidae, the Pleistocene tiger-sized
sabre-toothed cat Sm. fatalis has a low sexual dimorphism
index, identical to that of the jaguar. For this species a social
model has been inferred that would be completely different
from any other seen in extant felids: monogamous couples
within larger groups, similar to that of wolves (Van Valk-
enburgh & Sacco, 2002). The latter authors suggest that the
huge sample of Sm. fatalis from the carnivore-trap locality
of Rancho La Brea, at least 2400 individuals (Miller, 1968),
and the presence of individuals with severe but healed
pathologies makes it improbable that this felid was solitary.
In this locality, the ratio between Sm. fatalis and the other
sympatric large cat, the American lion Panthera atrox is 30:1
(Merriam & Stock, 1932), which could be reflecting the
predictable difference between social and solitary felids.
But if that is the case then the American lion would be
solitary, just the opposite of its extant close relative, Pan.
leo. In our view, this proportion could also mean some kind
of ecological segregation between Sm. fatalis and Pan. atrox
in the use of resources, which would produce a marked
difference in the pattern of trapping, and thus in the
representation of each species. In any event, inferences
about the presence or lack of social grouping in fossil felids
probably need to take more account of the relationship
between body size, prey size and density, and the defence of
cubs and territory in relatively open environments, which
are thought to be the major factors involved in the origin of
grouping in modern lions (Packer, 1986; Turner & Antón,
1997; Bothma & Walker, 1999; Yamaguchi et al., 2004).
Across other families of Carnivora, it is these factors also
that influence the presence of social groupings, rather than
the type of breeding system (Van Valkenburgh, Sacco &
Wang, 2003). From this point of view, the forest affinities of
the Batallones-1 mammalian fauna do not especially favour
the notion of social groupings in its larger carnivores.
Table 3 also shows that the sexual dimorphism index of
Par. ogygia is similar to that of cheetahs and jaguars. This
would reflect a low level of competition between males, just
as in some extant large cats. In the Batallones-1 sample,
there is only one pathologic individual, with the four left
metatarsals broken and healed when the animal was alive
(Fig. 6). Nevertheless, they fused incorrectly and the animal
was probably unable to run or hunt by itself for some
Table 3 Sexual dimorphism index for several species of extant and
fossil Felidae
Species
BL
(Skull)
MIL
(upper C)
BB
(upper C)
MIL
(M1) Average
Caracal caracal 1.08 1.06 1.03 1.08 1.06
Leptailurus serval 1.08 1.10 1.14 0.97 1.07
Smilodon fatalis 1.06 1.09 1.12 1.07 1.09
Panthera onca 1.06 1.12 1.11 1.06 1.09
Puma concolor 1.08 1.14 1.09 1.04 1.09
Acinonyx jubatus 1.10 1.15 1.11 1.09 1.10
Paramachairodus ogygia 1.09 1.11 1.11 1.09 1.10
Lynx rufus 1.10 1.16 1.11 1.06 1.11
Felis sylvestris 1.10 1.15 1.13 1.08 1.12
Felis chaus 1.07 1.16 1.15 1.10 1.12
Panthera tigris 1.16 1.16 1.08 1.12 1.13
Machairodus aphanistus 1.24 1.22 1.16 1.10 1.18
Panthera leo 1.12 1.25 1.23 1.13 1.18
Panthera pardus 1.13 1.24 1.26 1.12 1.19
Four measurements are used to calculate this index: BL (Skull), basal
length of the skull, measured from the anterior border of incisors to
the anterior margin of foramen magnum; ML (upper C), mesiodistal
length of upper canines; BB (upper C), bucolingual breadth of upper
canines; ML (M1), mesiodistal length of M1. An average index
between these four measurements is also provided. Data were taken
from Salesa (2002) (for Par. ogygia), Antón et al. (2004) (for
M. aphanistus) and Van Valkenburgh & Sacco (2002) (for the remain-
ing species).
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London 249
Behaviour and ecology of Paramachairodus ogygiaM. J. Salesa et al.
considerable time after the injury. The presence of this
individual in the sample poses some interesting questions
about the territoriality of Par. ogygia. It is clear that this
individual fed after its accident, so it survived until it was
trapped in Batallones-1. It is known that temporarily ill
leopards feed on carrion, and even healthy individuals do so
(Houston, 1979; Bailey, 1993; Daniel, 1996; Bothma &
Walker, 1999) but chronically ill individuals die before
healing, whereas lions in similar circumstances often survive
thanks to their social system (Bailey, 1993). It is highly
probable that Par. ogygia included carrion in its diet, and its
presence in the Batallones-1 trap strongly supports this, but
it is also hard to believe that an injured individual could
survive only with carrion. This resource is not so abundant
and constant as prey, and the amphicyonids alone would
have been a serious competitor for a crippled individual of
Par. ogygia. We suggest that Par. ogygia developed some
degree of tolerance between adults, as jaguars do, and that an
injured individual could therefore feed on the carcasses left
by the territory owner. Based on the antero-posterior length
of the proximal epiphysis of metatarsal III, this individual is
included in the sub-sample of ‘females’. So if this individual
was a young female it could have been tolerated by its
mother, remaining in her territory and thus feeding on the
remains left by her, as occurs with leopards (Bailey, 1993).
In summary, we suggest that the probable territorial
behaviour for Par. ogygia would be very similar to that of
jaguars, in which males defend large, overlapping territories
that include smaller territories of several females (Rabino-
witz & Nottingham, 1986; Seymour, 1989). This model is
similar to that of the leopard, but in this species male
territories never overlap (Bailey, 1993), which could explain
the different sexual dimorphism index of this species with
respect to Par. ogygia and jaguar.
Demographic structure of the population ofPar. ogygia from Batallones-1
If Par. ogygia were a social felid, as lions are, it would be
expected that the sample from Batallones-1 had juveniles,
which would have followed the adults and been trapped as
well. Nevertheless, although the sample of Par. ogygia from
Batallones-1 is composed of at least 18 individuals, all are
young adults (with permanent but unworn dentition) with
the exception of only one sub-adult (Salesa, 2002). This
virtual absence of young supports the idea of a solitary
lifestyle for Par. ogygia, like most of the big cats, in which
females leave the cubs hidden when hunting (Antón &
Morales, 2000). It is interesting that in the fieldwork of
Bailey (1993), which consisted of the use of traps to capture
and place transmitters on leopards, he observed that indivi-
duals less than one year old and females with cubs were
never caught. The most frequently trapped individuals were
adult males, and the best trapping period was the dry season
(Bailey, 1993). So, if Par. ogygia behaved more like jaguars
and leopards than lions, the presence of juveniles in the trap
would be highly improbable, as is the case. But in addition
to the scarcity of juveniles, the sample from Batallones-1 has
another interesting feature: it is mostly composed of young
adults, that is, individuals with the complete permanent
dentition, but without any trace of wear. These animals,
which would have recently become independent of their
mothers, would not as yet have had any territory, moving
instead through the ranges of other adults and being more
easily attracted by an easy meal, such as carrion. This age
distribution therefore suggests that the sample of Par.
ogygia trapped in Batallones-1 corresponds to that fraction
of non-resident young individuals, both males and females,
which were in a phase of dispersion. In the case of leopards,
such individuals are more daring – or less cautious – than
adults, and they have been seen crossing rivers in spate,
whereas resident adults only cross at times of lower water
(Bailey, 1993). It has also been noticed that among these
individuals, males are even more inclined to make these
incursions than females, which remain longer with the
mother, especially if there is good availability of food
(Bailey, 1993). If this pattern of dispersion behaviour applied
to the young adults of Par. ogygia, it is likely that they were
trapped in Batallones-1 more often than the resident adults.
Prey size of Par. ogygia
The extremely strong forelimbs of some derived sabre-
toothed cats, such as Smilodon have been interpreted as an
adaptation to cope with larger prey than pantherines (Go-
nyea, 1976b; Emerson & Radinsky, 1980; Akersten, 1985;
Rawn-Schatzinger, 1992; Turner & Antón, 1997). However,
these strong forelimbs are already present in Par. ogygia,
which also shows some primitive morphology in other
Figure 6 Left metatarsals of two individual of Paramachairodus ogygia
from Batallones-1: (a) B-5447, an individual showing a severe pathol-
ogy. The fracture and abnormal healing of the four metatarsals led to
their fusing, which would have hindered this animal in hunting or even
walking normally. (b) B-1318, healthy individual.
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London250
Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.
characters and a moderate body size (Salesa, 2002; Salesa
et al., 2005). We recently proposed an alternative hypothesis
to explain the appearance of these early macairodont
adaptations (Salesa et al., 2005), suggesting that they were
developed to subdue prey quickly, thus minimizing the risk
of canine breakage and decreasing the energy used in the
hunt. Thus, the earlier species of machairodonts would have
been able to kill prey faster than sympatric Carnivora of
comparable size and prey preference, and this advantage
would have helped the sabre-toothed cats become the
dominant predators in the faunas of Late Miocene.
Extant felines of size similar to Par. ogygia (up to 68 kg)
prey upon animals of very different sizes: leopards hunt
animals from 20 to 100 kg (Seidensticker, 1976; Johnson
et al., 1993) whereas pumas and jaguars usually hunt smaller
animals, between 1 and 30 kg (Rabinowitz & Nottingham,
1986; Nuñez et al., 2000). Jaguars in rain forests take
mammal prey species in proportion to their occurrence
(Rabinowitz & Nottingham, 1986; Emmons, 1987), so the
relative abundance of small prey in their diet may reflect a
lack of available large prey rather than real preference. The
herbivorous fauna from Batallones-1 included the masto-
dont Tetralophodon longirostris, the three-toed equid Hip-
parion sp., the hornless rhinoceros Aceratherium incisivum,
the large pig Microstonyx sp., the primitive small ruminant
Hispanomeryx sp., and several species of undetermined
bovid and cervid (Morales et al., 2000). In view of the size
of Par. ogygia, it is probable that the most likely prey were
juvenile individuals of Hipparion and Microstonyx, and
perhaps the adults of cervids and bovids. Mastodonts,
rhinos and the adult individuals of equids and pigs would
be too large to be a target for this sabre-toothed cat, whereas
Hispanomeryx would be too small. The equid from Batal-
lones-1 is close to the size of extant zebra, so probably only
juveniles and sub-adults would be within the prey range of
Par. ogygia. These equids are considered to have been open
country dwellers (Alberdi & Bonadonna, 1990; Bernor et al.,
1990; Forsten, 1991), and with Batallones-1 being probably
a wooded area the relative abundance of Hipparion in the
vicinity would have been low and encounters with Par.
ogygia rare. The weight of the large pig Microstonyx has
been estimated at 300kg (Alcalá, 1994). Like the extant
Suinae, it would probably live in small groups that moved
through the woodlands, with the young being actively de-
fended against any predator (Nowak& Paradiso, 1983). Thus,
in view of the size of an adultMicrostonyx, the risk of trying to
snatch a piglet would usually be too high for Par. ogygia.
The weigh of Cervidae and Bovidae from Batallones-1
cannot be estimated, because there is not enough material
for determination even to the genus level. The weight range
of extant cervids is between 7 (genus Pudu) and 825 kg (Alces
alces) (Nowak & Paradiso, 1983), but the more common
cervids present in the Vallesian faunas of the Iberian
Peninsula were Amphiprox anocerus and Euprox dicrano-
cerus (Azanza, 1989; Azanza et al., 1997), about the size of
an extant fallow deer Dama dama or between 40 and 100 kg
(Nowak & Paradiso, 1983). For the bovids, four species are
known from that period in the Iberian Peninsula: Protrago-
cerus chantrei, Austroportax latifrons,Miotragocerus panno-
nie and Tragoportax gaudryi (Alcalá, Morales & Soria,
1990). All these species fall in about the same size range,
with weight estimates varying between 46 and 72 kg (Alcalá,
1994). At these sizes, the cervids and bovids of Batallones-1
would be natural prey for Par. ogygia.
The body size ofHispanomeryxwould be within the lower
part of the range of the extant hornless ruminant Moschus,
which weighs between 7 and 17 kg (Nowak & Paradiso,
1983), although given the special adaptations of Par. ogygia
for the canine shear-bite (Salesa et al., 2005), it is probable
that Par. ogygia ignored such small prey. Extant felids kill
small animals by biting on the nape or directly on the skull,
using their rounded-section canines (Gonyea, 1976b; Aker-
sten, 1985; Turner & Antón, 1997), but if any sabre-toothed
cat tried to do this they would have risked breaking the
laterally flattened upper canines. For this reason, it is more
probable that they developed some behavioural mechanism
to minimize that risk, such as ignoring prey below a given
size. It is likely that machairodontines developed this etho-
logical trait early in their evolution, and so narrowed their
prey size range in comparison with that of felines, which
hunt both large and small animals. This high specialization
has been pointed out as one of the possible reasons for the
gradual decline and final extinction of the sabre-toothed cats
in the Pleistocene (Turner & Antón, 1997, 1999; Turner,
1999). For this reason, Par. ogygia probably hunted animals
within the upper part of the prey range of a similar-sized
pantherine, but the kill is likely to have been achieved in a
faster and safer way than in the latter, making the hunt more
efficient. The development of this strategy was probably the
key reason for the sabre-tooted cats becoming the dominant
predators in the land mammal faunas from the Late Mio-
cene to Late Pleistocene.
Conclusions
The coexistence of two species of large cats in the fossil
sample of Batallones-1, Par. ogygia and M. aphanistus, is
used to infer a wooded habitat for this Late Vallesian fossil
locality from Spain. There are other factors that support this
interpretation, such as the high diversity of felids, with four
species, or the presence in the fauna of the genus Martes,
whose extant species are associated with forested environ-
ments, and a large community of browsing herbivores.
The structure of the population of Par. ogygia found in
Batallones-1, and the inferred sexual dimorphism of this
species, suggest a solitary pattern of behaviour with a high
level of tolerance between the resident adult males, resembling
extant pantherines such as jaguars or pumas and differing
from leopards, which exhibit a lower level of tolerance
between males. The sample of Par. ogygia trapped in Batal-
lones-1 clearly corresponds to that fraction of young adults
that are looking for a territory, a stage when they would be
more easily attracted to carrion than would resident adults.
The absence of cubs indicates that the hunting behaviour of
Par. ogygia was very similar to extant solitary pantherines
such as jaguars or leopards, in which cubs and young remain
Journal of Zoology 268 (2006) 243–254 c� 2006 The Zoological Society of London 251
Behaviour and ecology of Paramachairodus ogygiaM. J. Salesa et al.
hidden while the mother hunts. If Par. ogygia had developed
any kind of social system, cubs and adults would have
remained together most of the time, and thus there would be
a greater number of cubs trapped in Batallones-1.
This primitive sabre-toothed cat developed strong fore-
limbs and a huge pollex, which would have led to reducing
the time of prey subduing and the risk of injury during the
hunt rather than enabling it to kill significantly larger prey
than extant pantherines of similar body size (Salesa et al.,
2005). Thus, the habitual prey of Par. ogygia would have
been within the size range of that taken by an extant
pantherine, such as cervids and bovids, present also in the
Batallones-1 sample. Nevertheless, the elongated and later-
ally flattened upper canines of Par. ogygia were probably
associated with a behavioural avoidance of smaller prey,
hunting of which would have enhanced the risk of bone
contact and the consequent breakage of the upper canines.
This specialization, absent in felines, would have led to a
narrower prey range and could have been one of the main
causes of the eventual extinctions of the sabre-toothed cats.
Acknowledgements
We thank Stéphane Peigné and Lars Werdelin for their
useful comments in the manuscript. This study is part of
the research project BTE2002-00410 (Dirección General de
Investigación-MCYT) and EX2003-0243 (Secretarı́a de Es-
tado de Educación y Universidades and European Social
Funding). We thank the Comunidad Autónoma de Madrid
(Dirección General de Patrimonio Histórico) for the con-
tinuous funding support and research permissions, and
A. T. thanks the British Council for travel funding. Addi-
tional support was provided by the National Geographic
Society (Grant 6964-01).
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Inferred behaviour and ecology of the primitive sabre-toothed cat Paramachairodus ogygia (Felidae, Machairodontinae) from the Late Miocene of Spain学霸图书馆link:学霸图书馆