Inferred behaviour and ecology of the primitive sabre-toothed cat...

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.


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.



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



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



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).



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.



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



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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