Longevity and life history of cave bears – a review and novel data from tooth cementum and relative emergence of permanent dentition

Abstract

Longevity and other life history variables are key to understanding evolutionary processes and the biology of extinct animals. For the past 20 years, the lifespan of cave bears received an increased interest. Studies focusing on incremental lines of tooth cementum resulted in detailed mortality patterns from different localities. In this review, we summarise literature on age estimation as well as mortality of different European cave bear localities and present novel data on longevity from 94 teeth originating from 20 European localities. Additionally, the relative tooth emergence pattern of the permanent dentition is investigated under the Schultz’s rule framework of possible life history implications. For this, the known sequences of extant bear species are compared with the one of cave bears. Our results suggest that the typical duration of the life of cave bears was 19 years but data from literature show that in rare cases ages of up to 30–32 years were achieved. Additionally, we present the oldest known age for the Middle Pleistocene cave bear Ursus deningeri, 29 years. The tooth eruption pattern of cave bears exhibits a heterochronic shift that implies, under the assumption of Schulz’ rule, a slightly faster life history than closely related species.     

广西一些第四纪洞穴堆积中化石的氨基酸地质年龄

利用化石中氨基酸的外消旋程度随化石年龄增加而增大的原理,本文分别用“校正法”和“高温法”测定了广西柳州早更新世巨猿洞、中更新世笔架山洞、晚更新世一全新世白莲洞、大龙潭及桂林Chen皮岩的一此处第四纪洞穴堆积物中牙化石、骨化石或贝壳化石的氨基酸年龄,测年结果与其它地质证据或^14C年龄基本一致。     

Limb bone proportions and body mass of the cave bear (Ursus spelaeus)

The European cave bear evolved during the Middle Pleistocene and adapted to mountain environments. Earlier workers have described the cave bear as a robust bear. In this study the cave bears limb bone morphology is compared to the limb bone morphology of extant bears. Body mass estimates for the cave bear are made both based on different limb bone characters and based on dental and cranial characters. The shafts are wider in the cave bear limb bones than in the extant bear limb bones, and consequently the shaft widths give higher weight estimates to the cave bear than the other dimensions. The widened shafts are suggested to be a special adaptation (of presently unknown significance) rather than an indicator of an increased body mass.     

The largest European lion Panthera leo spelaea (Goldfuss 1810) population from the Zoolithen Cave,Germany: specialised cave bear predators of Europe

Remains of 13 individuals with 3/1 male/female ratio of the extinct Upper Pleistocene lion Panthera leo spelaea (Goldfuss, 1810) from the Zoolithen Cave near Burggeilenreuth (Bavaria, Germany) include the holotype skull and all paratype material. The highest mortality rate for the Zoolithen Cave lions is in their reproductive adult ages. Bite marks on lion bones or skulls are results of hyena activities, or rare cannibalism of lions under stress situations. Lions were possibly also killed in battles with cave bears during predation on hibernating bears in winter times. This cave bear hunt specialisation in caves overlaps with the ecological behaviour of cave bear feeding by Ice Age-spotted hyenas. Both largest Ice Age predators, lions and hyenas, had to specialise on feeding herbivorous cave bears in boreal forest mountainous cave rich regions, where the mammoth steppe megafauna prey was absent. This cave bear hunt by felids, and scavenging by hyenas and other large carnivores such as leopards and wolves explains why cave bears hibernated deep in to the European caves, for protection reasons against predators. Within such lion–cave bear and even lion–hyena conflicts in the caves lions must have been killed sometimes, explaining mainly the skeleton occurrences in different European caves.     

Hominid exploitation of the environment and cave bear populations. The case of Ursus spelaeus Rosenmüller-Heinroth in Amutxate cave (Aralar, Navarra-Spain)

Cave bears (Ursus deningeri and U. spelaeus) and hominids (Homo heidelbergensis, H. neanderthalensis, and H. sapiens) were potential competitors for environmental resources (subterranean and open air). Here, we examined the age at death of cave bear (Ursus spelaeus Rosenmüller-Heinroth) specimens from Amutxate cave in order to shed light on the effect of resource sharing between cave bears and hominids. After studying dental wear of the deciduous and permanent dentitions, the ontogenetic development of mandibles, and incremental layers of cement (annuli), we defined five age groups differentiated by marked development and size gaps. Our findings indicate that after hibernating, bears abandoned the den, thereby leaving the subterranean environment (caves) free for temporary hominid occupation-this would explain the subtle traces of hominid presence in many dens. However, a simple calculation based on age at death of subadult and adult cave bear specimens in Amutxate cave, extrapolated to the whole cave area, showed that the area surrounding this cave hosted bears for at least 9,000 years. This length of habitation, quite similar to the time-span derived from amino acid racemization and electron spin resonance, indicates that bear populations in the Amutxate cave constituted a serious constraint for hominid exploitation of the environment.     

Ancient DNA analysis reveals divergence of the cave bear, Ursus spelaeus, and brown bear, Ursus arctos, lineages

The cave bear, Ursus spelaeus, represents one of the most frequently found paleontological remains from the Pleistocene in Europe. The species has always been confined to Europe and was contemporary with the brown bear, Ursus arctos. Relationships between the cave bear and the two lineages of brown bears defined in Europe, as well as the origins of the two species, remain controversial, mainly due to the wide morphological diversity of the fossil remains, which makes interpretation difficult [1, 2]. Sequence analysis of ancient DNA is a useful tool for resolving such problems because it provides an independent source of data [3]. We previously amplified a short DNA fragment of the mitochondrial DNA control region (mt control region) of a 40,000-year-old Ursus spelaeus sample [4]. In this paper, we describe the DNA analysis of two mtDNA regions, the control region and the cytochrome b gene. Control region sequences were obtained from ten samples of cave bears ranging from 130,000 to 20,000 years BP, and one particularly well-conserved sample gave a complete cyt b sequence. Our data demonstrate that cave bears split largely before the lineages of brown bears around 1.2 million years ago. Given its abundance, its wide distribution in space and time, and its large morphological diversity, the cave bear is a promising model for direct observation of the evolution of sequences throughout time, extinction periods, and the differentiation of populations shaped by climatic fluctuations during the Pleistocene.     

Stable isotopes and the metabolism of the European cave bear

Isotopic analyses of fossil bones of the extinct European cave bear indicate that this animal was a hibernator with the same unusual metabolic processes as some modern bear species. This finding provides useful biological and archaeological information on an extinct species, and the methods themselves may prove generally useful in studies of the metabolisms of modern bears, other hibernators, and perhaps of starving animals. Received: 6 October 1997 / Accepted: 31 March 1998     

铀子系法测定骨化石年龄的可靠性研究及华北地区主要旧石器地点的铀子系年代序列

本文报告测定骨化石~(231)Pa/~(235)U比值的实验方法,并根据骨化石样品的铀子系法年龄与~(14)C年龄的对比,讨论了铀子系法测定哺乳动物骨化石年龄的可靠性。作者实际测定了华北地区周口店、丁村等十个重要旧石器地点的年代,尝试提出华北地区旧石器文化年表。     

广西柳江土博甘前洞的铀系年代

本文报道晚期智人化石地点广西柳江博甘前洞新生碳酸盐岩和骨化石样的铀系测年结果。该地点表层钙板在约94Ka前开始形成,含化石粘土堆积叠压的钙板年代为约20ka,人牙化石应位于二者之间。二个动物化石样的二种铀系法年代范围为85－139ka,表明该地点与含化石堆积与表层钙板间无地层倒序现象,支持人牙化石大于100ka的结论。邻近的柳江晚期智人化石地点和柳州白莲洞人类遗址铀系测年的结果与本文一致。具现代解剖特征智人在中国南方出现的时间,很可能不晚于西非和非洲。在现代人类起源方面,中国不应是远离中心、滞后和被取代的地区。     

Upper Pleistocene Panthera leo spelaea (Goldfuss, 1810) remains from the Bilstein Caves (Sauerland Karst) and contribution to the steppe lion taphonomy,palaeobiology and sexual dimorphism

Remains of the steppe lion Panthera leo spelaea (Goldfuss) from historical digs in the Bilstein Caves of Warstein (Sauerland, NW Germany) are described. Their age seems to be from the Early Weichselian periods (Upper Pleistocene). Whereas the Bilstein cave was inhabited by cave bears at that time only a few hyena prey remains, were most likely imported into the cave entrance by hyenas. Bite and crush marks on a few bones of Bison priscus, Bos primigenius, Cervus elaphus, a rhinoceros Coelodonta antiquitatis vertebra and even several chewed cave bear bones prove the hyena presence which is similar to other caves in the Sauerland hyena den cave rich region. Additionally some larger wolves subspecies Canis lupusspelaeus bones were found, but only few Crocuta crocuta spelaea remains are present. After taphonomic comparisons to six other hyena and cave bear den caves of northern Germany, this cave can be classified as a cave bear den, which was briefly used by hyenas only for food storage or commuting or cave bear predation site in one part of the Cave. The lion material refers at least to one young adult lioness, one more adult female and two male lions; therefore, at minimum, the remains of four adult individuals are represented. The absence of juvenile lion material, in contrast to cave bear cub remains in the Bilstein Caves, proves that P. leo spelaea did not use this and all other caves in the region to raise their cubs. The bone material from the Bilstein Caves would prove the same hyena-lion antagonism conflict being recently proven for the Perick Caves, Balve Cave or Martins Cave well. Other situations in caves such as the Keppler Cave and the Bilstein Cave initially show the more complex taphonomic situation of lion remains in European caves, especially in cave bear dens, where they seem to have hunted periodically cave bears, such as it is already proven for hyenas in the Sauerland Karst and other caves of Europe.     

华南若干旧石器时代地点的铀系年代

本文用铀系法测定了我国华南地区的建德乌龟洞、大冶石龙头、长阳龙洞、马坝狮子山、柳江通天岩、柳州白莲洞、桐梓岩灰洞、黔西观音洞、水城硝灰洞、桐梓马鞍山和呈贡龙潭山3号洞等11个旧石器时代地点的年代,根据测定结果,汇同我们发表的华北地区旧石器年代数据排列了它们的年代序列。     

周口店北京猿人洞骨化石铀系年龄数据——混合模式

铀系混合模式得出北京猿人在第一地点生活的年代是距今50万年到23万年。通过周口店猿人洞堆积物骨化石中 Th~(230)/U~(234)和 U~(234)/U~(232)的测定,建立铀系混合模式,给出下列年龄值:第1—3层距今23万年,6—7层距今35万年,8—9层大于40万年,12层距今50万年前或更早。一些中间层位的Th~(230)/U~(234)比值测定年龄偏低,可能是近20万年以来铀发生迁移造成的。     

Recent history of the brown bear in the Maghreb

Bones of the brown bear (Ursus arctos, mammalia, Carnivora) found in a cave of the Akouker massif (Djurdjura, Algeria) have been dated according to the 14C method as belonging to the historical times (420-600 A.D.). The bone and teeth measurements correspond to a small-sized animal, the smallest ever found in the Maghreb. A review of fossil bears in the Quaternary faunas of North Africa clearly shows that the area of distribution, which was initially wide, shrank at the end of the Upper Pleistocene. The bears had temporarily taken to mountainous areas difficult to access. The bone remains discovered up to now prove that the brown bear was represented by individuals or populations showing a large diversity of size.     

Phylogeographic and Demographic Analysis of the Asian Black Bear (Ursus thibetanus) Based on Mitochondrial DNA

The Asian black bear Ursus thibetanus is widely distributed in Asia and is adapted to broad-leaved deciduous forests, playing an important ecological role in the natural environment. Several subspecies of U. thibetanus have been recognized, one of which, the Japanese black bear, is distributed in the Japanese archipelago. Recent molecular phylogeographic studies clarified that this subspecies is genetically distantly related to continental subspecies, suggesting an earlier origin. However, the evolutionary relationship between the Japanese and continental subspecies remained unclear. To understand the evolution of the Asian black bear in relation to geological events such as climatic and transgression-regression cycles, a reliable time estimation is also essential. To address these issues, we determined and analyzed the mt-genome of the Japanese subspecies. This indicates that the Japanese subspecies initially diverged from other Asian black bears in around 1.46Ma. The Northern continental population (northeast China, Russia, Korean peninsula) subsequently evolved, relatively recently, from the Southern continental population (southern China and Southeast Asia). While the Japanese black bear has an early origin, the tMRCAs and the dynamics of population sizes suggest that it dispersed relatively recently in the main Japanese islands: during the late Middle and Late Pleistocene, probably during or soon after the extinction of the brown bear in Honshu in the same period. Our estimation that the population size of the Japanese subspecies increased rapidly during the Late Pleistocene is the first evidential signal of a niche exchange between brown bears and black bears in the Japanese main islands.This interpretation seems plausible but was not corroborated by paleontological evidence that fossil record of the Japanese subspecies limited after the Late Pleistocene. We also report here a new fossil record of the oldest Japanese black bear from the Middle Pleistocene, and it supports our new evolutionary hypothesis of the Japanese black bear.     

Ancient DNA analyses reveal high mitochondrial DNA sequence diversity and parallel morphological evolution of late pleistocene cave bears

Cave bears (Ursus spelaeus) existed in Europe and western Asiauntil the end of the last glaciation some 10,000 years ago.To investigate the genetic diversity, population history, andrelationship among different cave bear populations, we havedetermined mitochondrial DNA sequences from 12 cave bears thatrange in age from about 26,500 to at least 49,000 years andoriginate from nine caves. The samples include one individualfrom the type specimen population, as well as two small-sizedhigh-Alpine bears. The results show that about 49,000 yearsago, the mtDNA diversity among cave bears was about 1.8-foldlower than the current species-wide diversity of brown bears(Ursus arctos). However, the current brown bear mtDNA gene poolconsists of three clades, and cave bear mtDNA diversity is similarto the diversity observed within each of these clades. The resultsalso show that geographically separated populations of the high-Alpinecave bear form were polyphyletic with respect to their mtDNA.This suggests that small size may have been an ancestral traitin cave bears and that large size evolved at least twice independently.     

First DNA sequences from Asian cave bear fossils reveal deep divergences and complex phylogeographic patterns

Until recently, cave bears were believed to have only inhabited Europe. However, recent morphological evidence suggests that cave bears' geographic range extended as far east as Transbaikalia, Eastern Siberia. These Asian cave bears were morphologically distinct from European cave bears. However, how they related to European lineages remains unclear, stressing the need to assess the phylogenetic and phylogeographic relationship between Asian cave bears and their European relatives. In this work, we address this issue using a 227 base-pair fragment of the mitochondrial control region obtained from nine fossil bone samples from eight sites from the Urals, Caucasus, Altai Mountains, Ukraine and Yana River region in Eastern Siberia. Results of the phylogenetic analyses indicate that (i) the cave bear from the Yana River is most closely related to cave bears from the Caucasus region; (ii) the Caucasus/Yana group of bears is genetically very distinct from both European cave bears and brown bears, suggesting that these bears could represent an independent species; and (iii) the Western European cave bear lineage reached at least temporarily to the Altai Mountains, 7000 km east of their known centre of distribution. These results suggest that the diversity of cave bears was greater than previously believed, and that they could survive in a much wider range of ecological conditions than previously assumed. They also agree with recent studies on other extinct and extant species, such as wolves, hyenas and steppe bison, which have also revealed higher genetic and ecological diversity in Pleistocene populations than previously known.     

Was the European cave bear an occasional scavenger?

Rabal‐Garcés, R., Cuenca‐Bescós, G., Canudo, J.I. & de Torres, T. 2011: Was the European cave bear an occasional scavenger? Lethaia, Vol. 45, pp. 96–108. The cave bear Ursus spelaeus fossils remains are quite abundant in the Late Pleistocene site of Coro Tracito (Huesca, Spain). The site constitutes the highest mountain record of cave bears in the Iberian Peninsula. Being a monospecific locality, it permits the study of the biology and dietary habits of this species. The study of the limb bones established first, the mortality pattern of this population of Ursus spelaeus and, second, the alteration pattern due to carnivore tooth‐marks. Some authors have performed similar analyses in the same kind of skeletal elements in other cave bear localities all over Europe and, therefore it has been possible to compare our results with those from other sites. The tooth‐marks found in the bones of cave bears, especially in monospecific sites, have been attributed to a scavenging behaviour. In agreement with the authors, our analysis presented here supports the hypothesis of scavenging behaviour for cave bears. □Behaviour, Late Pleistocene, Spain, taphonomy, tooth‐marks, Ursus spelaeus.     

U-series dating and taphonomy of Quaternary vertebrates from Brazilian caves

The geochronology and taphonomy of internationally important fossil bearing cave deposits were studied, both in the semi-arid Northern Bahia area and the subtropical southeastern Lagoa Santa area of Brazil. Taphonomic analysis suggests that the processes responsible for bone accumulation in the Brazilian caves vary between sites, and taphonomic bias can therefore be significant in causing differences in faunal composition. In the Toca da Boa Vista caves the presence of single articulated skeletons, and the entrance-related distribution indicate that random penetration of animals is the main mechanism of fossil accumulation, a process that biases the assemblage to smaller species, and takes place over extended time periods. In nearby Toca dos Ossos cave transport by runoff in the cave river is predominant, and biases the fauna remains to larger more robust bones and species. Deposition probably also occurred only at times of enhanced runoff giving a more contemporaneous assemblage. Similar processes were responsible for emplacement of the copious fossil remains in the more humid Lagoa Santa area, where terrigenous fossil deposits are found intercalated by massive speleothem calcite layers. In this area runoff under a drier climate probably accounts for the sediment emplacement inside caves. In both areas the mode of emplacement implies bias in the fossil record, resulting in fossil assemblages that do not mirror surface faunas, limiting palaeoenvironmental reconstruction.

Mass spectrometric U-series analysis of speleothem calcite overlaying fossil remains gives minimum ages for fossil deposition. These ages confirm the previous view that many of the deposits derive from the late glacial, but also show that much older material (some > 350,000 yr) is also present. The habitat requirements of critical fossil species such as bats and monkeys strongly suggest that they derive from much wetter periods when forest cover was present in the currently semi-arid Northern Bahia area. Taphonomy exerts a major control on the diversity and mode of emplacement of cave fossil deposits in eastern Brazil and thus detailed sedimentological and hydrological studies coupled with a sound geochronological approach are essential in quantifying the relative importance of each taphonomic processes before faunal and palaeoecological interpretations can be attempted.     

Rapid radiation events in the family Ursidae indicated by likelihood phylogenetic estimation from multiple fragments of mtDNA.

The bear family (Ursidae) presents a number of phylogenetic ambiguities as the evolutionary relationships of the six youngest members (ursine bears) are largely unresolved. Recent mitochondrial DNA analyses have produced conflicting results with respect to the phylogeny of ursine bears. In an attempt to resolve these issues, we obtained 1916 nucleotides of mitochondrial DNA sequence data from six gene segments for all eight bear species and conducted maximum likelihood and maximum parsimony analyses on all fragments separately and combined. All six single-region gene trees gave different phylogenetic estimates; however, only for control region data was this significantly incongruent with the results from the combined data. The optimal phylogeny for the combined data set suggests that the giant panda is most basal followed by the spectacled bear. The sloth bear is the basal ursine bear, and there is weak support for a sister taxon relationship of the American and Asiatic black bears. The sun bear is sister taxon to the youngest clade containing brown bears and polar bears. Statistical analyses of alternate hypotheses revealed a lack of strong support for many of the relationships. We suggest that the difficulties surrounding the resolution of the evolutionary relationships of the Ursidae are linked to the existence of sequential rapid radiation events in bear evolution. Thus, unresolved branching orders during these time periods may represent an accurate representation of the evolutionary history of bear species.     

Isotopic insights on cave bear palaeodiet

Abstract

More than 300 cave bear bones from all over Europe have carbon and nitrogen isotopic composition that match overwhelmingly a diet based on plants, except for samples from two caves in Romania, for which high nitrogen-15 amounts have been interpreted as reflecting an omnivorous diet. This paper aims at deciphering the various factors influencing the carbon and nitrogen isotopic composition of a potential omnivorous species like cave bear, those linked to trophic levels and variations among plants and those caused by physiological factors. The comparison of European cave bears with coeval Late Pleistocene large mammals with different diets clearly shows that all the cave bear populations, including those from Romania, present isotopic values overlapping with herbivores, not with carnivores. Therefore omnivory is very unlikely for cave bears. Consumption of plants with high δ¹⁵N values, such as graminoids, forbs and possibly fungi, could explain in part the observed isotopic pattern. In addition, the variations in δ¹⁵N values through ontogeny support the hypothesis of a different hibernation pattern for the Romanian cave bears with high δ¹⁵N values. Future investigations using new isotopic approaches, especially nitrogen isotopic composition of collagen amino acids, should contribute to decipher the paleoecology of these Romanian cave bears.