Journal of Zoology. Print ISSN 0952-8369 Inferred behaviour and ecology of the primitive sabre- toothed cat Paramachairodus ogygia (, ) from the Late of Spain M. J. Salesa1, M. Anton´ 2, A. Turner1 & J. Morales2

1 School of Biological and Earth Sciences, Liverpool John Moores University, Liverpool, UK 2 Departamento de Paleobiolog´ıa, Museo Nacional de Ciencias Naturales-CSIC, Madrid, Spain

Keywords Abstract behaviour; ecology; Felidae; Miocene; Paramachairodus. The Late Miocene (Late Vallesian, MN 10, about 9 Mya) carnivore trap of Batallones-1 (Madrid, Spain) has yielded a large sample of two species of sabre- Correspondence toothed cats: the puma-sized Paramachairodus ogygia and the tiger-sized Manuel J. Salesa, School of Biological and aphanistus. This has allowed, for the first time, complete studies of Earth Sciences, Byrom Street, Liverpool the biomechanics and comparative anatomy of these . Focusing our study John Moores University, Liverpool L3 3AF, on the small species, Par. ogygia, the most richly represented and best known UK. carnivore from Batallones-1, we attempt to infer some aspects of the behaviour Email: [email protected] and ecology of this early sabre-toothed cat, such as breeding behaviour, the degree of social interaction between individuals, sexual dimorphism, preferred habitat Received 25 January 2005; accepted 17 May and prey size. Our results suggest that Par. ogygia was a solitary felid with a low 2005 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 doi:10.1111/j.1469-7998.2005.00032.x 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 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 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 found: Paramachairodus ogygia (Kaup, 1832) and Machair- odus aphanistus (Kaup, 1832). We focus our study on the Inferences about the palaeobiology of fossil carnivores can former, which is the most richly represented carnivoran of be made based on field studies of extant species. However, the Batallones-1 sample. This species was previously one of because this group of is not usually well repre- the most poorly known Late Miocene machairodontines, sented in fossil sites, it is rare that these studies can include but thanks to the large amount of available skeletal ele- inferences about population structure, sexual dimorphism ments, it is now possible to infer many aspects of its or age group representation. The Late Miocene (Late biomechanics (Salesa, 2002; Salesa et al., 2005) and palaeoe- Vallesian, MN 10) carnivore trap of Batallones-1 (Madrid, cology. Spain) has yielded a large sample of several species of The walls of sepiolite of the trap made escape very carnivorans, and is now one of the most important Eur- difficult, because when this mineral is wet its surface opean localities for investigation of the mammalian com- becomes slippery, and under these conditions, even big cats munities of that epoch. The site was formed as an irregular were not able to climb out. Because the cavity was being cavity in sepiolite levels, later filled with greenish clay. It filled with clay, the bottom of the trap would have been acted as a natural trap for many animals, attracting mainly covered with wet mud, which would have hindered the (98% of the total macromammal sample in movement of animals and probably induced hypothermia, number of bones) that were probably trapped while at- contributing to their more or less rapid death (Morales tempting to scavenge (Fig. 1). Among them, abundant et al., 2000, 2004; Salesa, 2002; Anton´ et al., 2003). At least remains of two species of sabre-toothed cats have been seven additional and contemporaneous cavities have been

Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London 243 Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.

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 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. Sanchez).´

identified in the Batallones area, and although only Batal- Table 1 Estimated body weight of Machairodus aphanistus from lones-1 has been thoroughly excavated all of them fit with a Batallones-1: BL (skull), basal length of the skull, measured from the general geological process of piping, which in this case anterior border of incisors to the anterior margin of foramen magnum consisted of the erosion of sepiolite levels by water along Number BL (Skull) Body weight (kg) fractures, causing collapses and the development of karst- B-4272 257.0 130.28 like (‘pseudokarst’) topography, already described in other B-1523 237.0 101.27 areas by Halliday (1960). This is the major project respon- B-4711 310.0 233.42 sible for the formation of the Batallones fossil site complex B-5445 313.0 240.52 (Anton´ et al., 2003; Morales et al., 2004; Pozo et al., 2004), B-4151(1) 264.0 141.64 providing one of the most complete samples of Late Mio- B-6046 246.0 113.71 cene sabre-toothed cats.

Materials and methods Batallones-1 (Table 1). The results, between 100 and 240 kg, placed M. aphanistus within the range of extant All the skeletal remains of the mammals of Batallones-1, tigers and lions. including the sample of Par. ogygia analysed in this study, are held in the collections of the Museo Nacional de The mammal sample from Ciencias Naturales-CSIC (Madrid, Spain). Measurements Batallones-1 were taken using a digital calliper. Data on the minimum number of individuals (MNI) of each species of carnivoran The faunal association of Batallones-1 is one of the richest were taken from Anton´ & Morales (2000). The sexual of the Late Miocene of Eurasia, and includes fishes, amphi- dimorphism index of Par. ogygia was calculated following bians, reptiles, birds and mammals (Morales et al., 2000, the ‘average method’ of Van Valkenburgh & Sacco (2002), 2004). Nevertheless, the majority of the sample (98% of the which is based on four measurements of skull and dentition; total bone sample) is of Carnivora. This is unusual in fossil this method, which divides the sample into two sub-samples, localities, because with carnivorans totalling about 11% of ‘males’ and ‘females’, offers a good indication of the size the total mammal biomass in extant ecosystems (White divergence between the sexes. et al., 1984), the presence of this group in the fossil samples The body weight of Par. ogygia was estimated by Salesa usually totals around 7% of individuals (White et al., 1984; (2002) as 28–65 kg, which is within the range of an Anton´ & Morales, 2000). The existence of such a large extant puma. There were no previous estimates of the body proportion of carnivorans in Batallones-1 is explained as a weight of M. aphanistus, so we used the regression formula consequence of the presence of carcasses of animals that had of Van Valkenburgh (1990) for Felidae to estimate it on the died within the trap (Anton´ & Morales, 2000; Morales et al., base of the skull basal length of six individuals from 2000; Salesa, 2002). The absence of significant water flow

244 Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London M. J. Salesa et al. Behaviour and ecology of Paramachairodus ogygia

Figure 2 Relative abundance of the different groups of mammals present in the Batallones-1 sample.

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 20 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 66 12 Protictitherium crassum 90 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 10 1 Hipparion sp. 4 0 4 Aceratherium incisivum 30 3 Microstonyx sp. 0 1 1 Cervidae indet. 1 0 1 Hispanomeryx sp. 2 0 2 Figure 3 Fossil Carnivora from Batallones-1: (a) B-4778, skull and mandible of Paramachairodus ogygia in lateral view; (b) B-5445, skull MNI (A), minimal number of adult individuals; MNI (J), minimal and mandible of Machairodus aphanistus in lateral view. number of juvenile individuals; MNI (T), minimal number of total individuals. after the accumulation of the sample prevented the total disarticulation of the skeletons, allowing excellent preserva- tiger-sized M. aphanistus, with 14 individuals (13% of the tion of the and the presence of practically complete mammal palaeocommunity) (Figs 2 and 3; Table 2) (Anton´ skeletons (Morales et al., 2000, 2004). & Morales, 2000). There are two species of primitive felines, The most abundant components of the mammal fauna of one of Felis-size and other of Lynx-size; they represent only Batallones-1, around 29% of the total (Fig. 2), are the sabre- 4% of the sample (Figs 2 and 4). The bear-dog Amphicyon toothed cats, with two species represented: the puma-sized sp. aff. A. castellanus Ginsburg, Morales & Soria (1981) is Par. ogygia, with at least 18 individuals recorded (16% of relatively abundant, with at least 12 individuals (11% of the the mammal palaeocommunity) (Figs 2 and 3), and the mammal sample) (Figs 2 and 5). The primitive hyaenid

Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London 245 Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.

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.

Kaup, 1832 (3%), the tridactyl equid Hipparion sp. (4%), the hornless ruminant Hispanomeryx sp. (2%), the giant pig Microstonyx sp. (only 1%) and two species of undetermined Figure 4 Fossil Carnivora from Batallones-1: (a) B-2800 skull and cervids and bovids (1%) (Morales et al., 2000, 2004). mandible of Protictitherium crassum in lateral view; (b) B-2075, skull and mandible of Martes sp. in lateral view; (c) B-5446, skull and Discussion mandible of a juvenile individual of Felinae indet. in lateral view. Habitat preference in big cats Protictitherium crassum (Deperet,´ 1892), with nine indivi- duals (8%), is the fourth most abundant Carnivora (Figs 2 The three-dimensional structure of the habitat, which can be and 3), whereas the ailurid Simocyon batalleri (Viret, 1929) highly variable, clearly determines several aspects of mam- (Fig. 5) is one of the less represented, with only two malian behaviour (Eisenberg & Lockhart, 1972; Geist, individuals (2%) (Peigne´et al., 2005). Mustelids total 6% 1974). Among large cats, some species such as jaguar of the sample, being represented by four species, the marten Panthera onca, clouded Neofelis nebulosa and tiger Martes sp., two skunks (Sabadellictis sp. and Proputorius Panthera tigris are mainly found in highly structured habi- sp.) and one undetermined species. It is noticeable that the tats, typically dense forest (Mazak,´ 1981; Seymour, 1989; fossil pika (Lagomorpha) Prolagus crusafonti (Lopez´ Turner & Anton,´ 1997; Alderton, 1998). However, the tiger Martınez,´ 1975) (in Lopez´ Martınez´ & Thaler, 1975) is can also be found in the ecotone between forest and grass- almost as abundant as Par. ogygia, with 16 individuals and land, or even in mountain valleys of pine woods in Man- 15% of the total mammal community. The micro-mammal churia and near the Amur river (Mazak,´ 1981), and jaguars fauna of Batallones-1 also includes insectivores (8% of the have been reported in low-structured habitats such as sample), such as the moonrat Galerix sp. and two other deserts and prairies (Seymour, 1989), while undetermined species, and rodents (7%), such as the squirrel Panthera pardus and pumas Puma concolor can occupy a Spermophilinus sp., the beaver Steneofiber sp., the mouse range of very different habitats, from arid savannas to dense Progonomys hispanicus Michaux, 1971 and two species of tropical forests (Currier, 1983; Nowak & Paradiso, 1983; undetermined cricetid (hamsters) and zapodid (jumping Johnson et al., 1993; Alderton, 1998; Bothma & Walker, mice). The presence of the mouse Prog. hispanicus dates this 1999). Lions Panthera leo and cheetahs Acinonyx jubatus are locality to the early part of the Late Miocene, Neogene found in low-structured habitats, such as savannas or grass- European Land Mammal Zone 10 (MN 10) of Mein (1975), lands with some shrub coverage (Nowak & Paradiso, 1983; about 9 million years ago (Morales et al., 2000). Alderton, 1998; Bothma & Walker, 1999). The snow leopard The mammal association also includes a small number of Uncia uncia also occupies low-structured habitats, such as ungulate taxa; these are the mastodont Tetralophodon long- rocky areas in Asia between 1400 and 3200 m of altitude, irostris Kaup, 1832 (representing only 1% of the total occasionally reaching 4300 m (Hemmer, 1972; Gonyea, sample), the hornless rhinoceros Aceratherium incisivum 1976a; Nowak & Paradiso, 1983; Alderton, 1998).

246 Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London M. J. Salesa et al. Behaviour and ecology of Paramachairodus ogygia

Although the habitat preference of some species of felids Anton´ et al., 2003), probably reflecting similar habitat may be variable, they can probably be considered to derive preferences, that is, wooded environments. The predomi- from closed habitat dwellers (Turner & Anton,´ 1997). In nance of Par. ogygia in Batallones-1 could imply that the general, felids have not derived too much from the primitive trap was in a wooded area with at least enough cover to body plan of the Early Miocene forms (Helbing, 1928; allow this species to coexist with the larger M. aphanistus Beaumont, 1961; Turner & Anton,´ 1997), such as Proailurus (Anton´ & Morales, 2000). Preliminary observations of the lemanensis (Filhol, 1879) and although there are some post-cranial remains of the two species of small feline cats cursorial forms, such as Aci. jubatus or to a lesser extent, from Batallones-1 show them to be relatively gracile and U. uncia (Turner & Anton,´ 1997), felids lack the adaptations thus comparable with extant species such as Felis sylvestris, to sustained terrestrial locomotion in open environments Felis lybica and Lynx pardinus. These extant species occupy seen in some other Carnivora, such as canids or hyaenids. a wide range of habitats (Kitchener, 1991; Anton´ & Mor- ales, 2000), so the presence of these felines in Batallones-1 does not allow precise ecological interpretations. Never- Inferences on the habitat of Batallones-1 theless, the high diversity of felids in this locality implies a segregation of niches between the different species, much The fact that sabre-toothed felids are the most abundant more probable in a wooded environment. Carnivora of the Batallones-1 sample (Table 2) has ecologi- Among the Mustelidae, the extant species of the genus cal implications, because classical studies of vertebrate Martes are associated with forested habitats (Nowak & ecology have shown that intra- and inter-specific compe- Paradiso, 1983) and, although some species can occupy tition for resources produce different patterns of habitat use rocky areas, prairies and riversides, they always avoid (Lack, 1945; MacArthur, 1958; Lanciani, 1970; Laerm, treeless environments (Powell, 1981; Clark et al., 1987). 1974; Gonyea & Ashworth, 1975; Rabinowitz & Nottingham, Thus, the presence of marten in Batallones-1 supports the 1986; Bothma & Walker, 1999; Palomares & Caro, 1999). notion of a wooded habitat for this locality. Extant skunks According to this, when different species of extant felids live in occupy a wide range of habitats (Nowak & Paradiso, 1983; sympatry a marked segregation exists between them, with the Anton´ & Morales, 2000), so that the presence of Sabadellic- small-sized species constantly avoiding encounters with the tis and Proputorius in Batallones-1 gives little information large ones, which can be very violent. It is known that lions about the palaeohabitat of the trap surroundings. and leopards kill adults and cubs of other felids, and that The only extant Ailuridae is the red panda, Ailurus leopards are killed by lions and tigers (Turnbull-Kemp, 1967; fulgens, which inhabits the forests of China, Nepal and Schaller, 1972; Bailey, 1993; Daniel, 1996; Alderton, 1998; Burma (Nowak & Paradiso, 1983; Roberts & Gittleman, Bothma & Walker, 1999). Thus, in modern ecosystems, the 1984). Its diet consists mainly of bamboo, but it also coexistence of two species of large cats occurs in habitats with includes insects, small mammals, eggs, fruits and leaves some tree cover, which allows the smaller species to take (Nowak & Paradiso, 1983; Roberts & Gittleman, 1984). refuge in the trees from the attack of the larger one and so Nevertheless, although S. batalleri is thought to be related to avoid having its prey stolen or being killed (Morse, 1974). This Ai. fulgens (Wang, 1997), it has a very different dentition is the case for lions and leopards in Africa (Bailey, 1993) and that seems to be adapted to a diet based on flesh and carrion tigers and leopards in Asia (Seidensticker, 1976). In the case of (Baskin, 1998; Anton´ & Morales, 2000; Salesa & Fraile, cheetahs and lions, both of which can be found in open 2000) and probably included small vertebrates (Peigne´et al., environments, sympatry is possible because cheetahs con- 2005). This does not show any cursorial adaptations stantly avoid encounters with lions, hunting during the hours in its appendicular skeleton, so it is probable that it of maximum heat when lions and hyaenas tend to be inactive inhabited at least moderately wooded areas. and resting in the shade (Hanby & Bygott, 1979; Durant, The population of Amphicyon sp. aff. A. castellanus from 2000). There is also sympatry among felids of similar size, such Batallones-1 is one of the richest samples of bear-dogs as pumas and jaguars in most of the American continent known in the European fossil record (Morales et al., 2000). (Nunez,˜ Miller & Lindzey, 2000), but this is only possible Amphicyonids were powerfully built carnivorans, from the when resources are rich enough to allow the maintenance of size of a wolf to that of a brown bear, which inhabited North both species, which develop a marked ecological segregation America and Eurasia during the Oligocene and Miocene. between them mainly based on the avoidance of adult Their dentitions show adaptations to a carnivorous diet, but encounters (Rabinowitz & Nottingham, 1986; Nunez˜ et al., also have strong post-carnassial teeth, probably reflecting 2000). their abilities as both scavengers and hunters. Nevertheless, In summary, the sympatry of two large cat species seems the dentition of the Batallones-1 Amphicyon is more hyper- to be determined not only by the presence of enough tree carnivorous than that of previous species of this cover, but also by high prey biomass (Seidensticker, 1976). genus, probably reflecting a late adaptation of this species In the case of lions and leopards, this sympatry is facilitated to more active hunting (Morales et al., 2000; Salesa & Fraile, by the fact that leopards preferably occupy wooded sections 2000). of the habitat, less favourable for lions (Bailey, 1993). The Protictitherium crassum is an early and primitive member body proportions of Par. ogygia and M. aphanistus are very of the family Hyaenidae (Werdelin & Solounias, 1991), with similar to those of the extant pantherine cats (Salesa, 2002; 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 ogygia M. J. Salesa et al. civet, Civettictis civetta (Anton´ & Morales, 2000). The latter occupy territories of between 12 and 150 km2 that include inhabits both forested and more or less open environments, the smaller female territories. There are also solitary cheetah but always with enough vegetational cover to find refuge individuals that do not defend territories, moving through (Nowak & Paradiso, 1983; Ray, 1995). The dentition of huge areas (Nowak & Paradiso, 1983; Nowell & Jackson, Prot. crassum does not show the adaptations to bone 1996), but in other cases groups of 14 individuals have been cracking seen in the later hyaenids, and it probably would reported in areas in which lions and hyaenas have been have been an opportunistic carnivoran, with a diet and exterminated (Nowell & Jackson, 1996). behaviour more similar to that of a jackal than to that of Territory size in large cats is variable, because it depends an extant hyaenid. on the sex and age of the owner, and available prey biomass The herbivore sample of Batallones-1 is scarce (12% of (Currier, 1983; Bailey, 1993). Thus, the territory of a male the total sample), although the presence of some taxa with leopard can vary between 16.4 and 96.1 km2, and that of a low cheek teeth, such as cervids, mastodonts, Hispanomer- female between 5.6 and 29.9 km2 (Bailey, 1993). A pride of yx, and Aceratherium, suggest the presence of a wooded lions can occupy a territory as large as 470 km2 (Bothma & habitat. It is also noticeable that the most probable grazers Walker, 1999), whereas the territories of male tigers vary or at least mixed-feeders, Hipparion and the bovids, are between 380 km2 in the case of Indian individuals and the really rare in the sample. 1000 km2 of those from central Asia (Mazak,´ 1981). Male In summary, the faunal association of Batallones-1 sug- jaguars have territories of between 28 and 40 km2, whereas gests a wooded habitat for this locality, probably a more or those of females tend to be around 10 km2 (Rabinowitz & less dense woodland, with enough cover to allow the Nottingham, 1986; Seymour, 1989). Male pumas tend to sympatry of two species of large felids, the presence of have larger territories than females, but in both cases they several species of small carnivorans (which need some cover are highly variable, between 96 and 243 km2 (Currier, 1983). 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- Sexual dimorphism in felids ionine horses, indicate the presence of more open, grassy patches in the vicinity of the site. Sexual dimorphism in mammals has been associated with a high level of competition between males for access to Sociability and sexual dimorphism in Felidae 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 Social behaviour in felids differences can be related to the breeding system. Species in Most of the extant felines lead solitary lives, and only in the which a male defends a group of females tend to be more breeding season do they form pairs that last only a few dimorphic than those with monogamous pairs or groups of weeks (Nowak & Paradiso, 1983; Alderton, 1998; Bothma & males and females (Gittleman & Van Valkenburgh, 1997; Walker, 1999). Only lions have the kind of behaviour that Weckerly, 1998; Van Valkenburgh & Sacco, 2002). Felids can be considered as social (Leyhausen, 1979; Caro, 1989, are dimorphic animals, but mainly in reference to body size, 1994), although it has been observed that tigers inhabiting with the mane of male lions being a unique example of open environments can form groups, and male cheetahs morphological variation between sexes among the family. often form coalitions (Alderton, 1998; Bothma & Walker, Table 3 shows the sexual dimorphism index for several 1999). Nevertheless, none of the species live in complete species of extant Felinae and the sabre-toothed cats isolation, because they use several types of marks to keep in fatalis, Par. ogygia and M. aphanistus. The most contact with other individuals. These may be scent (territor- dimorphic species are Pan. pardus and Pan. leo, which is ial marking with urine), visual (scratching on trees) or vocal, very interesting in view of the different breeding system of used singly or in combination (Nowak & Paradiso, 1983; these two felids. Lions have a very competitive system, with Bailey, 1993; Daniel, 1996; Alderton, 1998). males defending a large group of females (Alderton, 1998; Felids are highly territorial animals, that is, they occupy Bothma & Walker, 1999), which would explain the high very well-delimitated areas (home ranges or territories) that sexual dimorphism index (Bertram, 1979; Van Valkenburgh are defended against other adults of the same species. Each & Sacco, 2002). On the other hand, leopards are basically individual marks the limits of its range in order to show that solitary animals, probably more so than any other panther- the area is occupied (Bailey, 1993; Turner & Anton,´ 1997; ine (Bailey, 1993), which suggests that there is no clear Alderton, 1998). In most of the species, male territories relationship between the sexual dimorphism index and the include several, smaller female territories (Rabinowitz & presence of social systems in Felidae. Nottingham, 1986; Bailey, 1993). There are some excep- The development of sociability in felids has been seen as tions, such as lions, in which groups of two to five related associated with the habitat and prey biomass rather than the males defend a huge range occupied by a pride of related breeding system (Turner & Anton,´ 1997; Alderton, 1998; females (Nowak & Paradiso, 1983; Alderton, 1998; Bothma Funston et al., 1998). Thus, the social behaviour of lions has & Walker, 1999). Cheetah male coalitions may include non- been explained as a consequence of their special habitat, related individuals (Nowell & Jackson, 1996), and can much more low-structured than that of other felids; for a

248 Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London M. J. Salesa et al. Behaviour and ecology of Paramachairodus ogygia

Table 3 Sexual dimorphism index for several species of extant and Cheetahs exhibit a higher degree of sociability, with males fossil Felidae usually forming groups of three that can include non-related individuals (Nowell & Jackson, 1996). There is no competi- BL MIL BB MIL tion between males for access to females, and males simply Species (Skull) (upper C) (upper C) (M1) Average breed with those females that enter their area (Nowell & Caracal caracal 1.08 1.06 1.03 1.08 1.06 Jackson, 1996). There is no active defence of territory, and, Leptailurus serval 1.08 1.10 1.14 0.97 1.07 although they mark the limits by urine and scratching, each Smilodon fatalis 1.06 1.09 1.12 1.07 1.09 Panthera onca 1.06 1.12 1.11 1.06 1.09 group of males tries not to come into contact with others Puma concolor 1.08 1.14 1.09 1.04 1.09 (Nowak & Paradiso, 1983). Finally, the least dimorphic Acinonyx jubatus 1.10 1.15 1.11 1.09 1.10 felids of the modern sample studied, Caracal caracal and Paramachairodus ogygia 1.09 1.11 1.11 1.09 1.10 Leptailurus serval, are both supposed to be solitary, with Lynx rufus 1.10 1.16 1.11 1.06 1.11 male ranges including those of the females (Nowell & Felis sylvestris 1.10 1.15 1.13 1.08 1.12 Jackson, 1996). Nevertheless, groups of caracals composed Felis chaus 1.07 1.16 1.15 1.10 1.12 of juveniles and adults have been reported (Nowak & Panthera tigris 1.16 1.16 1.08 1.12 1.13 Paradiso, 1983; Nowell & Jackson, 1996; Alderton, 1998). Machairodus aphanistus 1.24 1.22 1.16 1.10 1.18 Among the fossil Felidae, the Pleistocene tiger-sized Panthera leo 1.12 1.25 1.23 1.13 1.18 sabre-toothed cat Sm. fatalis has a low sexual dimorphism Panthera pardus 1.13 1.24 1.26 1.12 1.19 index, identical to that of the jaguar. For this species a social model has been inferred that would be completely different Four measurements are used to calculate this index: BL (Skull), basal from any other seen in extant felids: monogamous couples length of the skull, measured from the anterior border of incisors to the anterior margin of foramen magnum; ML (upper C), mesiodistal within larger groups, similar to that of wolves (Van Valk- length of upper canines; BB (upper C), bucolingual breadth of upper enburgh & Sacco, 2002). The latter authors suggest that the huge sample of Sm. fatalis from the carnivore-trap locality canines; ML (M1), mesiodistal length of M1. An average index between these four measurements is also provided. Data were taken of Rancho La Brea, at least 2400 individuals (Miller, 1968), from Salesa (2002) (for Par. ogygia), Anton´ et al. (2004) (for and the presence of individuals with severe but healed M. aphanistus) and Van Valkenburgh & Sacco (2002) (for the remain- pathologies makes it improbable that this felid was solitary. ing species). 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 hunter of this size, the formation of groups would be an predictable difference between social and solitary felids. advantage to hunt large prey in high-visibility environments But if that is the case then the American lion would be (Turner & Anton,´ 1997; Alderton, 1998), and to defend solitary, just the opposite of its extant close relative, Pan. territory and cubs (Bothma & Walker, 1999). For Hemmer leo. In our view, this proportion could also mean some kind (1978), the difference in the habitat occupied by lions and of ecological segregation between Sm. fatalis and Pan. atrox tigers, much more closed in the latter, would explain why in the use of resources, which would produce a marked tigers do not develop social behaviour, as the brains of both difference in the pattern of trapping, and thus in the species are very similar in weight and internal structure. representation of each species. In any event, inferences In leopards, female territories are included into larger about the presence or lack of social grouping in fossil felids territories, defended by one male, and the territories of two probably need to take more account of the relationship neighbour males never overlap, male encounters being very between body size, prey size and density, and the defence of aggressive (Rabinowitz & Nottingham, 1986; Bailey, 1993). cubs and territory in relatively open environments, which This implies that, in theory, a female only breeds with the are thought to be the major factors involved in the origin of resident male in a breeding system with a high level of grouping in modern lions (Packer, 1986; Turner & Anton,´ competition between males. In jaguars, as in leopards, 1997; Bothma & Walker, 1999; Yamaguchi et al., 2004). females occupy territories included in those of males, but Across other families of Carnivora, it is these factors also neighbouring male territories usually overlap, although that influence the presence of social groupings, rather than aggressive encounters are very rare (Rabinowitz & Notting- the type of breeding system (Van Valkenburgh, Sacco & ham, 1986; Seymour, 1989). Thus, jaguar males show a Wang, 2003). From this point of view, the forest affinities of higher level of tolerance than male leopards, and this could the Batallones-1 mammalian fauna do not especially favour explain the lower sexual dimorphism index of jaguars. the notion of social groupings in its larger carnivores. Pumas have the same sexual dimorphism index as jaguars Table 3 also shows that the sexual dimorphism index of and also similar territorial behaviour: males defend huge Par. ogygia is similar to that of cheetahs and jaguars. This areas and they do not tend to have any contact with other would reflect a low level of competition between males, just males (Currier, 1983), although the home ranges do overlap as in some extant large cats. In the Batallones-1 sample, (Nowak & Paradiso, 1983). Females are highly tolerant of there is only one pathologic individual, with the four left the presence of other individuals, except when they have metatarsals broken and healed when the animal was alive cubs, and their ranges widely overlap with those of the (Fig. 6). Nevertheless, they fused incorrectly and the animal neighbour adults (Nowak & Paradiso, 1983). was probably unable to run or hunt by itself for some

Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London 249 Behaviour and ecology of Paramachairodus ogygia M. J. Salesa et al.

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 of Par. 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 (Anton´ & 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 Figure 6 Left metatarsals of two individual of Paramachairodus ogygia never caught. The most frequently trapped individuals were from Batallones-1: (a) B-5447, an individual showing a severe pathol- adult males, and the best trapping period was the dry season ogy. The fracture and abnormal healing of the four metatarsals led to (Bailey, 1993). So, if Par. ogygia behaved more like jaguars their fusing, which would have hindered this animal in hunting or even walking normally. (b) B-1318, healthy individual. 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 considerable time after the injury. The presence of this another interesting feature: it is mostly composed of young individual in the sample poses some interesting questions adults, that is, individuals with the complete permanent about the territoriality of Par. ogygia. It is clear that this dentition, but without any trace of wear. These animals, individual fed after its accident, so it survived until it was which would have recently become independent of their trapped in Batallones-1. It is known that temporarily ill mothers, would not as yet have had any territory, moving leopards feed on carrion, and even healthy individuals do so instead through the ranges of other adults and being more (Houston, 1979; Bailey, 1993; Daniel, 1996; Bothma & easily attracted by an easy meal, such as carrion. This age Walker, 1999) but chronically ill individuals die before distribution therefore suggests that the sample of Par. healing, whereas lions in similar circumstances often survive ogygia trapped in Batallones-1 corresponds to that fraction thanks to their social system (Bailey, 1993). It is highly of non-resident young individuals, both males and females, probable that Par. ogygia included carrion in its diet, and its which were in a phase of dispersion. In the case of leopards, presence in the Batallones-1 trap strongly supports this, but such individuals are more daring – or less cautious – than it is also hard to believe that an injured individual could adults, and they have been seen crossing rivers in spate, survive only with carrion. This resource is not so abundant whereas resident adults only cross at times of lower water and constant as prey, and the amphicyonids alone would (Bailey, 1993). It has also been noticed that among these have been a serious competitor for a crippled individual of individuals, males are even more inclined to make these Par. ogygia. We suggest that Par. ogygia developed some incursions than females, which remain longer with the degree of tolerance between adults, as jaguars do, and that an mother, especially if there is good availability of food injured individual could therefore feed on the carcasses left (Bailey, 1993). If this pattern of dispersion behaviour applied by the territory owner. Based on the antero-posterior length to the young adults of Par. ogygia, it is likely that they were of the proximal epiphysis of metatarsal III, this individual is trapped in Batallones-1 more often than the resident adults. included in the sub-sample of ‘females’. So if this individual was a young female it could have been tolerated by its Prey size of Par. ogygia mother, remaining in her territory and thus feeding on the remains left by her, as occurs with leopards (Bailey, 1993). The extremely strong forelimbs of some derived sabre- In summary, we suggest that the probable territorial toothed cats, such as Smilodon have been interpreted as an behaviour for Par. ogygia would be very similar to that of adaptation to cope with larger prey than pantherines (Go- jaguars, in which males defend large, overlapping territories nyea, 1976b; Emerson & Radinsky, 1980; Akersten, 1985; that include smaller territories of several females (Rabino- Rawn-Schatzinger, 1992; Turner & Anton,´ 1997). However, witz & Nottingham, 1986; Seymour, 1989). This model is these strong forelimbs are already present in Par. ogygia, similar to that of the leopard, but in this species male which also shows some primitive morphology in other

250 Journal of Zoology 268 (2006) 243–254 c 2006 The Zoological Society of London M. J. Salesa et al. Behaviour and ecology of Paramachairodus ogygia characters and a moderate body size (Salesa, 2002; Salesa cerus chantrei, Austroportax latifrons, Miotragocerus panno- et al., 2005). We recently proposed an alternative hypothesis nie and Tragoportax gaudryi (Alcala,´ Morales & Soria, to explain the appearance of these early macairodont 1990). All these species fall in about the same size range, adaptations (Salesa et al., 2005), suggesting that they were with weight estimates varying between 46 and 72 kg (Alcala,´ developed to subdue prey quickly, thus minimizing the risk 1994). At these sizes, the cervids and bovids of Batallones-1 of canine breakage and decreasing the energy used in the would be natural prey for Par. ogygia. hunt. Thus, the earlier species of machairodonts would have The body size of Hispanomeryx would be within the lower been able to kill prey faster than sympatric Carnivora of part of the range of the extant hornless ruminant Moschus, comparable size and prey preference, and this advantage which weighs between 7 and 17 kg (Nowak & Paradiso, would have helped the sabre-toothed cats become the 1983), although given the special adaptations of Par. ogygia dominant predators in the faunas of Late Miocene. for the canine shear-bite (Salesa et al., 2005), it is probable Extant felines of size similar to Par. ogygia (up to 68 kg) that Par. ogygia ignored such small prey. Extant felids kill prey upon animals of very different sizes: leopards hunt small animals by biting on the nape or directly on the skull, animals from 20 to 100 kg (Seidensticker, 1976; Johnson using their rounded-section canines (Gonyea, 1976b; Aker- et al., 1993) whereas pumas and jaguars usually hunt smaller sten, 1985; Turner & Anton,´ 1997), but if any sabre-toothed animals, between 1 and 30 kg (Rabinowitz & Nottingham, cat tried to do this they would have risked breaking the 1986; Nunez˜ et al., 2000). Jaguars in rain forests take laterally flattened upper canines. For this reason, it is more mammal prey species in proportion to their occurrence probable that they developed some behavioural mechanism (Rabinowitz & Nottingham, 1986; Emmons, 1987), so the to minimize that risk, such as ignoring prey below a given relative abundance of small prey in their diet may reflect a size. It is likely that machairodontines developed this etho- lack of available large prey rather than real preference. The logical trait early in their evolution, and so narrowed their herbivorous fauna from Batallones-1 included the masto- prey size range in comparison with that of felines, which dont Tetralophodon longirostris, the three-toed equid Hip- hunt both large and small animals. This high specialization parion sp., the hornless rhinoceros Aceratherium incisivum, has been pointed out as one of the possible reasons for the the large pig Microstonyx sp., the primitive small ruminant gradual decline and final of the sabre-toothed cats Hispanomeryx sp., and several species of undetermined in the Pleistocene (Turner & Anton,´ 1997, 1999; Turner, bovid and cervid (Morales et al., 2000). In view of the size 1999). For this reason, Par. ogygia probably hunted animals of Par. ogygia, it is probable that the most likely prey were within the upper part of the prey range of a similar-sized juvenile individuals of Hipparion and Microstonyx, and pantherine, but the kill is likely to have been achieved in a perhaps the adults of cervids and bovids. Mastodonts, faster and safer way than in the latter, making the hunt more rhinos and the adult individuals of equids and pigs would efficient. The development of this strategy was probably the be too large to be a target for this sabre-toothed cat, whereas key reason for the sabre-tooted cats becoming the dominant Hispanomeryx would be too small. The equid from Batal- predators in the land mammal faunas from the Late Mio- lones-1 is close to the size of extant zebra, so probably only cene to Late Pleistocene. juveniles and sub-adults would be within the prey range of Par. ogygia. These equids are considered to have been open Conclusions country dwellers (Alberdi & Bonadonna, 1990; Bernor et al., 1990; Forsten, 1991), and with Batallones-1 being probably The coexistence of two species of large cats in the fossil a wooded area the relative abundance of Hipparion in the sample of Batallones-1, Par. ogygia and M. aphanistus,is vicinity would have been low and encounters with Par. used to infer a wooded habitat for this Late Vallesian fossil ogygia rare. The weight of the large pig Microstonyx has locality from Spain. There are other factors that support this been estimated at 300 kg (Alcala,´ 1994). Like the extant interpretation, such as the high diversity of felids, with four Suinae, it would probably live in small groups that moved species, or the presence in the fauna of the genus Martes, through the woodlands, with the young being actively de- whose extant species are associated with forested environ- fended against any predator (Nowak & Paradiso, 1983). Thus, ments, and a large community of browsing herbivores. in view of the size of an adult Microstonyx, the risk of trying to The structure of the population of Par. ogygia found in snatch a piglet would usually be too high for Par. ogygia. Batallones-1, and the inferred sexual dimorphism of this The weigh of Cervidae and Bovidae from Batallones-1 species, suggest a solitary pattern of behaviour with a high cannot be estimated, because there is not enough material level of tolerance between the resident adult males, resembling for determination even to the genus level. The weight range extant pantherines such as jaguars or pumas and differing of extant cervids is between 7 (genus Pudu) and 825 kg (Alces from leopards, which exhibit a lower level of tolerance alces) (Nowak & Paradiso, 1983), but the more common between males. The sample of Par. ogygia trapped in Batal- cervids present in the Vallesian faunas of the Iberian lones-1 clearly corresponds to that fraction of young adults Peninsula were Amphiprox anocerus and Euprox dicrano- that are looking for a territory, a stage when they would be cerus (Azanza, 1989; Azanza et al., 1997), about the size of more easily attracted to carrion than would resident adults. an extant fallow deer Dama dama or between 40 and 100 kg The absence of cubs indicates that the hunting behaviour of (Nowak & Paradiso, 1983). For the bovids, four species are Par. ogygia was very similar to extant solitary pantherines known from that period in the Iberian Peninsula: Protrago- 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 ogygia M. J. Salesa et al. hidden while the mother hunts. If Par. ogygia had developed P., Salesa, M.J., Sanchez,´ I.M. & Soria, D. (Eds). Madrid: any kind of social system, cubs and adults would have Servicio de Publicaciones de la Comunidad de Madrid. remained together most of the time, and thus there would be Anton,´ M., Salesa, M.J., Morales, J., Peigne,´ S., Pelaez-´ a greater number of cubs trapped in Batallones-1. Campomanes, P. & Fraile, S. (2003). Early radiation of This primitive sabre-toothed cat developed strong fore- felid sabertooths documented in carnivore-trap fossil site in limbs and a huge pollex, which would have led to reducing the Late Miocene of Spain. J. Vertebr. Paleontol. 23 (Suppl. the time of prey subduing and the risk of injury during the 3), 32A. hunt rather than enabling it to kill significantly larger prey Anton,´ M., Salesa, M.J., Morales, J. & Turner, A. (2004). than extant pantherines of similar body size (Salesa et al., First known complete skulls of the scimitar-toothed cat 2005). Thus, the habitual prey of Par. ogygia would have Machairodus aphanistus (Felidae, Carnivora) from the been within the size range of that taken by an extant Spanish late Miocene site of Batallones-1. J. Vertebr. pantherine, such as cervids and bovids, present also in the Paleontol. 24, 957–969. Batallones-1 sample. Nevertheless, the elongated and later- Azanza, B. (1989). Los Cervidae (Artiodactyla, Mammalia) ally flattened upper canines of Par. ogygia were probably del Mioceno de las cuencas del Duero, Tajo, Calatayud- associated with a behavioural avoidance of smaller prey, Teruel y Levante. PhD thesis. A´rea de Paleontologıa,´ hunting of which would have enhanced the risk of bone Departamento de Ciencias de la Tierra, Universidad de contact and the consequent breakage of the upper canines. This specialization, absent in felines, would have led to a Zaragoza. narrower prey range and could have been one of the main Azanza, B., Nieto, M., Soria, D. & Morales, J. (1997). El causes of the eventual of the sabre-toothed cats. registro neogeno´ de los Cervoidea (Artiodactyla, Mamma- lia) de Espana.˜ In Avances en el conocimiento del terciario iberico.´ Comunicaciones del iii congreso del grupo espanol˜ Acknowledgements del terciario: 41–44. Calvo, J.P. & Morales, J. (Eds). Spain: Cuenca. We thank Stephane´ Peigne´ and Lars Werdelin for their Bailey, T.N. (1993). The African leopard: ecology and behavior useful comments in the manuscript. This study is part of of a solitary felid. Biology and resource management in the the research project BTE2002-00410 (Direccion´ General de tropics series. 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