The lion (Panthera leo) can rightly claim to be the most oft-invoked animal in all of human culture. Whether praising someone as leonine or lion-hearted, or throwing them to the lions, the second largest of felines has the ability to evoke emotions that the tiger (Panthera tigris), leopard (Panthera pardus) and jaguar (Panthera onca) simply do not. This entwined history stretches at least as far back as the late Pleistocene (100,000 to 10,000 years ago) and possibly as far back as the late Pliocene (about 3.5mya), when the lion lineage first split from the other pantherine cats.
We tend to think of the lion as a quintessentially African animal and, indeed, this is where the vast majority of lions survive today. However, the tiny enclave holding around 400 lions, in the Gir forest reserve of India, hints at the expanses previously ranged by this majestic cat. If you were to travel back in time to 50,000 years ago, you would find lions in all of Africa (north and south of the Sahara), the Middle East, Europe, the Indian subcontinent (including Sri Lanka), Siberia, Alaska and North America as far south as Mexico. From the Cape of Good Hope to the isthmus of Darien, lions occupied a range greater than any other terrestrial mammal, except man (Fig. 1). It seems incredible to modern eyes, but the lion was an integral part of the European ecosystem right up until the Holocene (10,000 years ago to the present).
How did it get here? What did it look like? What did it eat? Why did it disappear? For all these questions, we are moving towards answers – answers that paint a fascinating picture of a vanished animal.
What do we know about the evolution of the lion? Quite a lot, thanks to the fact that the fossil record for this large carnivore is pretty good. The modern lion is the sister species to the leopard and jaguar (Fig. 2), which together make up the subgenus Panthera (the tiger is sufficiently different that it has its own subgenus – Tigris). Despite the obvious differences in adult pelage and morphology, the cubs of the three Panthera species are remarkably similar, all possessing rosettes, which are only lost in the lion on reaching maturity (and sometimes even then still faintly visible on the legs).
We know from molecular studies that this group split off from other pantherines around 2 to 3mya (Johnson et al., 2006). The best fossil representative we have for the base of this triumvirate is P palaeosinensis, from the Pliocene of northern China, a unique skull that blends features of all the Panthera cats (Mazak, 2010). After this, the first appearance of fossils that appear lion-like is at Laetoli, around 3.5mya, although whether these actually represent ancestral P leo, P pardus or some other offshoot is difficult to say (Turner and Antón, 1997).
It is not until the appearance of P leo fossilis in Europe around 500,000 years ago that we can be certain that the fossils are absolutely leonine in form. P leo fossilis, or the ancestral cave lion, was an enormous cat. Found at sites such as Bisnik cave in Poland (Marciszak and Stefaniak, 2010), Sierra de Atapuerca, Spain (Garcia et al., 1997) and Mauer in Germany (Wagner et al., 2010; and see Fig. 3), the ancestral cave lion was perhaps up to a quarter larger than the largest modern day lions. During the late Pleistocene, fossilis actually became slightly smaller, producing the true cave lion, P leo spelaea, which has been found in abundance in Europe, Siberia and Alaska – showing what an incredible range the species had. At some stage, fossilis even penetrated the Americas, crossing the Bering land bridge and becoming P leo atrox, the American lion (Barnett et al. 2009).
The ancestral cave lion must have been an imposing sight – in Europe, its only challenger to the title of apex predator would have been the sabretooth cat (Homotherium sp.). We know that sabretooths and the ancestral cave lion made it to Britain, as remains of both have been found in middle Pleistocene deposits in East Anglia (Lewis et al., 2010), which, at that time represented the north-westernmost peninsula of mainland Europe. The true cave lion was equally at home in southern England during the late Pleistocene. Remains of P spelaea have been found in many of the classic sites dating to this era (Fig. 3), including Kent’s cavern, Kirkdale and Wookey Hole (Dawkins et al., 1866). Incredibly, even underneath the giant lions that guard Trafalgar Square in London, remains of cave lions dating to the last interglacial have been found (Franks, 1960) – a rare case of nature imitating art.
Lions and humans
Lions are still often represented in human art. The ‘lions rampant’ and ‘lions passant’, familiar from heraldry, are far from the most ancient attempts at capturing the essence of the leonine. It is under-appreciated that the very oldest known example of figurative art (that is, art not depicting something found in the real world) is of a lion-headed human from the late Pleistocene site of Hohlenstein-Stadel in Germany (Fig. 4). This therianthrope is carved from mammoth ivory and has been radiocarbon dated to around 30,000 years BP (Vanhaeren and d’Errico, 2006). And it is not a one-off piece. Other lion-people (or “Löwenmensch”) have been unearthed from other sites in Germany (Conard, 2003), testifying to some important ritualistic importance for this were-animal in Palaeolithic European societies. What the cave lion meant to these people is now lost in time, but it clearly meant something important. Other groups even used the massive canine of the cave lion as a pendant in a necklace (Vanhaeren and d’Errico, 2006).
Palaeolithic people were also great observers of the natural world and this is shown vividly in the parietal art they have left behind. The magnificent site of Chauvet Cave in the Pont du Arc showcases the largest collection of cave lion images known (Chauvet et al., 2001); and Fig. 5). Interestingly, we can get a very good idea of how the cave lion appeared in life, and even some clues to its behaviour, from these images. The first thing to note is that male cave lions did not have manes. No image from any Pleistocene art shows a lion with more than the hint of a ruff on the neck. The possibility that early Europeans only depicted lionesses has been suggested and discarded as lions from Chauvet are anatomically correct down to the prominent scrotal sac in the maneless male (Packer and Clotte, 2000).
The cave lion seems to have operated in prides, as do modern lions, and the walls of Chauvet frequently show lions in groups of three, four or more. This suggests that the ancestor of all lion groups was a pride hunter, which passed this form of sociality to all its descendants (including P leo fossilis and P atrox) when it spread over the Old and New Worlds (Yamaguchi et al., 2004). Conversely, the impressive manes, so evocative of what we think of today as ‘lions’, are probably a recent evolutionary innovation of the African leo lineage, acquired after the split from other lion groups.
What sharp teeth you have!
A pride of lions is a formidable hunting machine. The lions of Chobe in Botswana are famously known to tackle even the largest of modern mammals, the adult African elephant (Loxodonta africana), and the cave lion, at around 25% bigger than an African lion, would without doubt have been just as capable. We have both direct and indirect evidence for the prey choices of cave lions, thanks to a combination of well-preserved fossils and recent innovations in palaeontological science. One of the most amazing examples of direct evidence for cave lion predation was found at the easternmost edge of the cave lions range in Alaska, which was during the late Pleistocene, a habitat of productive ‘mammoth steppe’, which is now mostly permafrost (that is, soil saturated with water that remains frozen all year round).
In 1979 at Pearl creek, Fairbanks in Alaska, some miners were removing the overburden of Pleistocene permafrost ‘muck’ to get at the gold-bearing gravel underneath, when they discovered something unprecedented. Washing out of the sediment was the mummified remains of a Steppe bison (Bison priscus). They contacted Dale Guthrie of the University of Alaska, who carefully rescued this unique carcass for further study. Christened “Blue Babe”, this preserved animal was a treasure trove of information about the epoch in which it lived (Guthrie, 1990; and see box, “Blue Babe” – the frozen baby bison). Amazingly, the bison retained evidence of being fed upon by large carnivores. A comparison of the bite marks left in the bison’s skin to the suite of predators available in the area (for example, the wolf, Canis lupus; sabretooth, Homotherium serum; short-faced bear, Arctodus simus; brown bear, Ursus arctos; and cave lion, Panthera leo spelaea) seemed to match the lion’s range of tooth measurements. They were also present on the Bison’s rump, the preferred site of attack for lions chasing down Cape buffalo (Syncerus caffer) in their modern range. In contrast, wolves tend to go for the stomach and sabretooths probably went for the throat or stomach. Incredibly, when Blue Babe was being prepared for taxidermy, a sliver of tooth enamel was found actually embedded in the skin. The enamel coatings of carnivore teeth are diagnostic and this sliver, again, matched the cave lion. It seems that when Blue Babe was already well-frozen, some itinerant lions had tried to take advantage of a free meal and earned a toothache.
“Blue Babe” – the frozen baby bison
Blue Babe is a treasure of the ice age. Named for the brilliant blue covering of the mineral vivianite that encrusts it skin due to reaction between phosphate in the corpse and iron in the surrounding soil, it is on display at the University of Alaska Museum in Fairbanks. The discovery, research and taxidermy of Blue Babe is recounted in the book Frozen Fauna of the Mammoth Steppe by Dale Guthrie (Guthrie, 1990).
The permafrost has preserved many mummies from the Pleistocene (for example, Dima the baby mammoth), beloved of creationists who claim that they were flash-frozen in the Noachian flood. This could not be further from the truth. Each permafrost mummy is unique, but most were present above ground for a period of time before eventual burial – evidence of predation in Blue Babe and others shows that mummification was not instant.
More macabre evidence is found at a site called Sima de los Huesos (“the pit of bones”) in Atapuerca. There, palaeontologists found a mass of human bones that looked like they had been brought in by lions, who had left characteristic gnaw marks on the vertebrae (Andrews and Fernandez Jalvo, 1997). Whether the human bodies had been scavenged or hunted is impossible to say. Other fossils show that sometimes the tables were turned, and cut marks on ribs show that Panthera leo fossilis was occasionally the hunted rather than the hunter (Blasco et al., 2010).
Indirect evidence of cave lion diet comes from research into stable isotopes (see box, Radiocarbon dating ancient food webs).
Radiocarbon dating ancient food webs
Most people are familiar with the use of isotopes in archaeology and palaeontology through the idea of radiocarbon dating. The radioactive decay of Carbon-14 allows the absolute date of organic material to be gauged. However, other isotopes that are not prone to radioactive decay (‘stable isotopes’) can be used to follow ancient food webs. The isotopes Carbon-13 and Nitrogen-15 can be used to follow trophic interactions due to a number of unique features. Carbon-13 is differentially incorporated into plant tissues depending on whether they use a terrestrial or marine source of carbon dioxide. Terrestrial plants can be further subdivided depending on which of a number of photosynthetic pathways they use. This allows for separation between strict grazers and strict browsers in the fossil record as grasses and trees use different metabolic pathways. Mixed feeders will have unique, identifiable signatures based on what proportion of each Carbon-13 source they eat. Carnivores get their Carbon-13 from herbivores and, therefore, the mix of browsing and grazing prey can be identified from the Carbon-13 signature of the carnivore.
Similarly, Nitrogen-15 is enriched in the tissues of carnivorous mammals compared to the herbivores they prey on, due to the processing of dietary protein and excretion of urea. Therefore, from these data, it is possible to reconstruct the dietary preferences of extinct animals.
The studies show that European and Beringian cave lions had hugely varied diets. In Beringia, they seem to have preyed on caribou (that is reindeer – Rangifer tarandus), horse (Equus caballus), bison (Bison bison) and perhaps moose (Alces alces) (Fox-Dobbs et al., 2008). In Europe, cave lions appear to have been partial to reindeer (R tarandus) and the cave bear (Ursus spelaeus) (Bocherens et al., 2011). The cave bear (see box, Cave bears), a huge relative of the brown bear (Ursus arctos), appears to have been predominantly herbivorous and, while hibernating in caves over winter, provided a much needed food source for cave lions and cave hyaenas (Crocuta crocuta spelaea) (Diedrich, 2011). Although the majority of Pleistocene cave lion, cave hyaena, and cave bear remains have been found in the karstic systems of Europe (hence their common names), it would perhaps be better to refer to a steppe lion. Only U spelaeus and C crocuta appears to have sought out caves as places of refuge and hibernation; the other lion remains found there were due to accumulation by hyaenas (Diedrich, 2009), or the animals accidentally falling into the cave and becoming trapped while hunting. The animosity between hyaena and lion, clearly observable in modern-day Africa, has also been inferred from the characteristically hyaena-chewed lion bones found in Pleistocene dens. Even the type-site for P leo spelaea (Zoolithen cave, where the cave lion was first described from fossil remains) appears to have been a hyaena den, with accumulations of hunted and scavenged lion bones (Diedrich, 2008).
The cave bear (Ursus spelaeus) is the quintessential Pleistocene European fossil mammal. Bones by the hundreds of thousands have been found in the caves of the Old World, allowing an unparalleled insight into their life and death. Much larger than the modern brown bear (Ursus arctos) and exhibiting a strangely bulbous forehead, the cave bear was probably analogous to the giant panda (Ailuropoda melanoleuca) in its strict herbivory, as shown by dental and stable isotope analyses. Originally thought to be confined to Europe (in the broadest sense), recent finds have been made as far east as Arctic Siberia, showing it to have been very wide-ranging indeed. The cave bear has been at the vanguard of ancient DNA testing (due to material abundance, as much as anything else) and was the first fossil mammal to have its complete genome sequenced.
Perhaps the most obvious fact about cave lions is that they are no longer around. Why is this? Their disappearance, along with mammoths, sabretooths and the rest of the Pleistocene menagerie, constitutes perhaps the biggest mystery in palaeontology. With the advent of radiocarbon dating and, more recently, the analysis of ancient DNA, we are starting to get close to an answer. The powerful combination of absolute dating and ancient DNA datasets has allowed palaeogeneticists to model demographic changes in extinct mammals before their extinction and in extant mammals that are no longer as common as they were during the Pleistocene. So far, this has been done on bison (Shapiro et al., 2004), mammoths (Barnes et al., 2007), cave bears (Stiller et al., 2010), muskox (Campos et al., 2010) and saiga (Campos et al., 2010), as well as cave lions (Barnett et al. 2009).
Interestingly, while those species that survived the Pleistocene extinction (bison, muskox and saiga) appear to go through population fluctuations related to climatic changes, the species that go extinct either go extinct abruptly (mammoth) or appear to go through a bottleneck event close to when modern humans first enter their habitat but not particularly tied with any known climatic events (cave bears and cave lions). Could humans have been responsible for the extinction of the cave lion? Certainly, modern lions are known to have been persecuted severely wherever their range has overlapped with humans, even in the pre-industrial era. Written accounts and artistic depictions show the killing of lions in Mesopotamia, Greece, Egypt and other ancient societies to have been widespread and sustained.
Perhaps, the reason lions are not to be found outside Africa and India today is simply due to competition for resources with humans. It is a sobering thought and one to bear in mind, as the African lion creeps closer to “endangered” status.
Andrews, P. & Fernandez Jalvo, Y. Surface modification of the Sima de los Huesos fossil humans. Journal of Human Evolution 33, 191-217 (1997).
Barnes, I. et al. Genetic Structure and Extinction of the Woolly Mammoth, Mammuthus primigenius. Current Biology 17, 1-4 (2007).
Barnett, R. et al. Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and late Pleistocene reduction in genetic diversity. Molecular Ecology 18, 1668-1677 (2009).
Blasco, R., Rosell, J., Arsuaga, J. L., Bermudez de Castro, J. M. & Carbonell, E. The hunted hunter: the capture of a lion (Panthera leo fossilis) at the Gran Dolina site, Sierra de Atapuerca, Spain. Journal of Archaeological Science 37, 2051-2060 (2010).
Bocherens, H. et al. Isotopic evidence for dietary ecology of cave lion (Panthera spelaea) in North-Western Europe: prey choice, competition and implications for extinction. Quaternary International in press (2011).
Campos, P. F. et al. Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics. Proceedings Of The National Academy Of Sciences Of The United States Of America 107, 5675-5680 (2010).
Campos, P. F. et al. Ancient DNA sequences point to a large loss of mitochondrial genetic diversity in the saiga antelope (Saiga tatarica) since the Pleistocene. Molecular Ecology 19, 4863-4875 (2010).
Chauvet, J., Deschamps, E. B., Hillaire, C., Clotte, J. & Bahn, P. G. Chauvet Cave: The Discovery of the World’s Oldest Paintings (Thames and Hudson, 2001).
Conard, N. J. Palaeolithic ivory sculptures from southwestern Germany and the origins of figurative art. Nature 426, 830-832 (2003).
Dawkins, W. B., Sanford, W. A. & Reynolds, S. H. A monograph of the British Pleistocene mammalia (Palaeontographical Society, London, 1866).
Diedrich, C. G. The holotype of the upper Pleistocene Crocuta crocuta spelaea (Goldfuss, 1823: Hyaenidae) and Panthera leo spelaea (Goldfuss, 1810: Felidae) of the Zoolithen Cave hyena den (South Germany) and their palaeo-ecological interpretation. Zoological Journal of the Linnean Society 154, 822-831 (2008).
Diedrich, C. G. Steppe lion remains imported by Ice Age spotted hyenas in the the Late Pleistocene Perick Caves hyena den in northern Germany. Quaternary Research 71, 361-374 (2009).
Diedrich, C. G. The largest European lion Panthera leo spelaea (Goldfuss) population from the Zoolithen Cave, Germany: specialised cave bear predators. Historical Biology (2011).
Fox-Dobbs, K., Leonard, J. A. & Koch, P. L. Pleistocene megafauna from eastern Beringia: Paleoecological and paleoenvironmental interpretations of stable carbon and nitrogen isotope and radiocarbon records. Palaeogeography, Palaeoclimatology, Palaeoecology 261, 30-46 (2008).
Franks, J. W. Interglacial deposits at Trafalgar Square, London. The New Phytologist 59, 145-150 (1960).
Garcia, N., Arsuaga, J. L. & Torres, T. The carnivore remains from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain). Journal of Human Evolution 33, 155-174 (1997).
Guthrie, R. D. Frozen Fauna of the Mammoth Steppe: The Story of Blue Babe (The University of Chicago Press, London, 1990).
Johnson, W. E. et al. The Late Miocene radiation of modern Felidae: A genetic assessment. Science 311, 73-77 (2006).
Lewis, M. E., Pacher, M. & Turner, A. The larger Carnivora of the West Runton Freshwater Bed. Quaternary International (2010).
Marciszak, A. & Stefaniak, K. Two forms of cave lion: Middle Pleistocene Panthera spelaea fossilis Reichenau, 1906 and Upper Pleistocene Panthera spelaea spelaea Goldfuss, 1810 from the Bisnik Cave, Poland. Neues Jahrbuch Für Geologie und Paläontologie Abhandlungen 258, 339-351 (2010).
Mazak, J. H. What is Panthera palaeosinensis? Mammal Review 40, 90-102 (2010).
Packer, C. & Clotte, J. When Lions Ruled France. Natural History 109, 52-57 (2000).
Shapiro, B. et al. Rise and Fall of the Beringian Steppe Bison. Science 306, 1561-1565 (2004).
Stiller, M. et al. Withering away-25,000 years of genetic decline preceded cave bear extinction. Molecular Biology and Evolution 27, 975-978 (2010).
Turner, A. & Antón, M. The Big Cats and their fossil relatives (Columbia University Press, New York, 1997).
Vanhaeren, M. & d’Errico, F. Aurignacian ethno-linguistic geography of Europe revealed by personal ornaments. Journal of Archaeological Science (2006).
Wagner, G. A., Maul, L. C., Löscher, M. & Schreiber, H. D. Mauer- the type site of Homo heidelbergensis: palaeoenvironment and age. Quaternary Science Reviews in press (2010).
Yamaguchi, N., Cooper, A., Werdelin, L. & MacDonald, D. W. Evolution of the mane and group-living in the lion (Panthera leo): a review. Journal of Zoology 263, 329-342 (2004).