Co-existence of scimitar-toothed cats, lions and hominins in the European Pleistocene. Implications of the post-cranial anatomy of Homotherium latidens (Owen) for comparative palaeoecology
Introduction
Whatever the antiquity of human occupation of Europe, it is clear that meat was most probably an important food source (Roebroeks, 2001). That interest in meat was shared by a guild of large Carnivora, and any understanding of earliest human presence must take account of the structure and activities of that guild (Turner, 1992). An obvious enigma among the guild members is the lion-sized sabre-toothed cat Homotherium latidens, which was widespread as perhaps the dominant predator in a variety of Eurasian and African environments from the Pliocene until at least the Middle Pleistocene. It certainly coexisted with several species of hominins across its spatial and temporal range, from African Pliocene sites with Australopithecus species to later levels of Zhoukoudian cave, home to Asian Homo erectus, and the upper levels of Gran Dolina at Atapuerca with Homo heidelbergensis. In Europe, Homotherium latidens coexisted with the lion, Panthera leo, for an interval of at least 200 kyr after the arrival of the latter species on the continent some time during the Middle Pleistocene, a coexistence that raises interesting palaeoecological problems (Turner, 1995a; Turner and Antón, 1999). The recent discover of a mandible of Homotherium latidens dated to around 28,000 yr BP in the North Sea (Reumer et al., 2003) even suggests that either the animal survived in Eurasia until the last glaciation, thus lengthening considerably the period of co-existence with lions, or that it re-entered the continent from North America (see discussion below on extinctions in Section 6.4). In either event it would have co-existed with Neanderthals and fully modern humans.
One assumption has been that Homotherium, like other large machairodont cats, would tend to leave a greater amount of scavengeable food at a kill (Turner, 1992). Assessing the ecological significance of Homotherium requires an understanding of its palaeobiology, and thus of its functional anatomy, but remains are usually rare and fragmentary with postcrania mostly known from a single semi-complete skeleton from the Pliocene locality of Senèze in France (Ballesio, 1963). That specimen confirmed the anatomical distinctiveness of Homotherium as a gracile sabre-tooth with a skeleton differing completely from the typical, hyper-robust sabre-tooths such as the well-known American genus Smilodon, or its likely ancestor Megantereon, as recognised on the basis of partial remains from Hundsheim in Austria by Schaub (1925). Kurtén (1952) coined the terms “scimitar-toothed cats” (such as Homotherium) and “dirk-toothed cats” (such as Smilodon and Megantereon) for the two contrasting types of felid sabre-tooths defined on the basis of the shape of their upper canines and also set apart by their differing postcranial anatomy. Martin, 1980, Martin, 1989 defined the scimitar-tooths and the dirk-tooths as “ecomorphs”, meaning that both the type of upper canines and the body proportions of each type were part of a set of adaptations to a particular lifestyle and predatory strategy.
Although the morphological distinctiveness of Homotherium is thus well established, the implications for its locomotory and predatory behaviour are more difficult to define, especially since the hunting and killing techniques of sabre-tooths as a whole are only now becoming clear (Turner and Antón, 1997, Turner and Antón, 1999; Antón and Galobart, 1999). Among earlier authors, Martin (1980) suggested that dirk-tooths were typical ambush hunters, while scimitar-tooths were more like pursuit predators, an interpretation elaborated on by Rawn-Schatzinger (1992), who used a large sample of the Late Pleistocene species Homotherium serum from Friesenhahn Cave (Texas) to conclude that it would have been a sprint runner like the modern cheetah. This agrees with the ideas of Martin (1989, p. 544) who thought that H. latidens had cheetah-like skeletal proportions. More recent studies by Anyonge (1996) and Lewis (1997) confirm the presence of cursorial adaptations in Homotherium, although neither considers the implications of such adaptations in terms of prey procurement and handling.
In contrast, Ballesio (1963, pp. 118–119) had earlier concluded after studying the Senèze specimen that Homotherium latidens would be less capable of jumping and sprinting than modern pantherine cats, arguing that although the elongated limb-bones of Homotherium suggest a similarity with the modern cheetah, the body proportions of these two cats were extremely different (1963, p. 112). Such contradictory interpretations do not seem to stem from real differences between the American and Old-World species, but rather from different authors focusing their studies on different aspects of anatomy. A comprehensive overview that unifies these disparate observations is required in order to obtain a more complete picture of Homotherium as a living predator.
Since the publication of Ballesio's monograph in 1963, virtually no new studies have considered the post-cranial anatomy of H. latidens in detail, although numerous remains have been recovered. Moreover, some elements important for functional interpretations, such as the ungual phalanges, are virtually absent in Senèze (only one claw was found, and the digit to which it corresponded is not known) and a single individual gives little idea of the range of morphological variation within a species. Fortunately, a rich assemblage from the Early Pleistocene Spanish site of Incarcal offers an exceptional contribution to our knowledge of the post-cranial anatomy of this taxon since there are complete and well-preserved elements of the trunk and limbs of several individuals (Fig. 1), including a substantial sample of ungual phalanges that allow us to assess the morphology and relative size of the claws in H. latidens for the first time (Galobart, 1996; Antón and Galobart, 1999).
The aims of this paper are therefore to describe the Incarcal sample in comparison with other published material of H. latidens, and then to broaden our comparisons to other species of felid sabertooths and the modern larger felids, with a special emphasis on the lion. From these comparisons and a detailed functional interpretation of the observed morphology we hope that a more comprehensive model of the predatory behaviour and ecology of H. latidens will emerge, which will allow us to address broader ecological implications. We thus hope to provide answers to a series of intriguing questions posed by the coexistence of Homotherium, the large pantherines, other large Carnivora and hominins in the European fossil record: Would there, for example, be a direct competition between Homotherium and the lion in the places where they coexisted? How would such a competition be affected by environmental factors? What can we learn from other examples of coexistence of competing large Carnivora in the fossil record, in modern environments or in historical times? Would the presence of hominins and their entrance to the large predator guild impinge upon Homotherium? To what extent did Homotherium consume and defend its kills, and how important would the remains of those kills be as a resource for scavengers, including hominins? Would lions, hyaenids and hominins exert pressure on, or even become kleptoparasites of, Homotherium? And, last but not least, what combination of ecological factors could bring about the extinction of Homotherium?
Section snippets
Materials and methods
We examined a sample of post-cranial bones of Homotherium latidens from the Spanish site of Incarcal comparing their morphology with that of modern pantherine species including skeletons of lion (Panthera leo), tiger (Panthera tigris), leopard (Panthera pardus), jaguar (Panthera onca), and cheetah (Acinonyx jubatus) in the Museu de Zoologia de Barcelona and one lion skeleton from the Museo Nacional de Ciencias Naturales of Madrid (Spain). We also used for reference published descriptions of
The Incarcal site
The Incarcal site complex is located in the lacustrine basin of Banyoles-Besalú (Northeastern Spain). A total of nine karst cavities filled with fossiliferous sediments in Pliocene limestones are currently known (Ros et al., 2003). Three of these fillings (Incarcal I, II, and V) have yielded the majority of the faunal remains, while the others have a much lower fossiliferous richness. The faunal association of the site is typical for the lower Biharian (Lower Pleistocene) of Western Europe (
Thoracic and lumbar vertebrae
The thoracic vertebrae of the Incarcal Homotherium display no remarkable differences from those of pantherine cats, but the centra of the lumbars are relatively shorter (Fig. 2). The anterozygapophises in anterior view are more “enveloping” than in modern cheetah and lion, but less so than in jaguar. The shape of the transverse processes, with a wide insertion in the vertebral body extending laterally in the first half and with only moderate ventral inclination, resembles the jaguar more than
Trunk
Homotherium has short lumbars with laterally projecting transverse processes, and thus departs from the primitive felid model seen in early machairodontines such as Nimravides (MacDonald, 1948) and in all living felines, where lumbar centra are long and transverse processes extend in more marked anterio-inferior direction. Similar changes are seen in bears and hyenas; and of course in a more pronounced manner in ungulates, and make the back of an animal more rigid and strong (Hildebrand, 1989).
European dispersion of Homotherium, and the Villafranchian large carnivore guild
Initial dispersion of Homotherium in Europe is probably linked with changes in the environment recorded at around 3.2 Ma, when the climate became cooler and drier and vegetational cover decreased. There was an increase in seasonality and the Mediterranean pattern of summer drought began at that time (Agustí and Antón, 2002), culminating in the well-established 2.4 Ma event that saw the beginning of northern hemisphere glaciations. The dominant large cat of the European early Pliocene had been the
Machairodonts and hominins in the European Middle Pleistocene
The importance of machairodontines as providers of resources for such scavengers as hyaenids and hominins has been a matter of long debate. The idea that machairodonts were unable to clean the bones of meat because of the shape of their teeth was largely falsified by the study of Marean and Ehrhardt (1995) of a Homotherium den in Friesenhahn Cave, Texas, where tooth marks on elephant bones showed that homotheres were able to use their protracted incisor battery, as could anyway be inferred from
Conclusion
The comparison of elements of the post-cranial skeleton of Homotherium latidens from Incarcal with the same elements in modern big cats and in other sabre-toothed taxa reveals the presence of moderate cursorial adaptations. Homotherium latidens had shortened lumbar vertebrae; a slender humerus with an elevated greater tuberosity, a narrow distal end and a vertical and deep olecranon fossa; a straight radius with a narrow distal end; a shortened robust pisiform; small claws on digits II–V with
Acknowledgements
We thank the curators of the Museu Arqueològic Comarcal de Banyoles, Josep Tarrús, and the Museu de Zoologia de Barcelona, Eulàlia Garcia, for access to their collections and facilities for study. This work has been supported by project BOS2001-1004 of the Ministerio de Ciencia y Tecnologia of Spain.
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