Determination of the evolutionary mode of Austrian alpine cave bears by uranium series dating

Middle and Late Pleistocene sediments in many caves in Central and South Europe contain large numbers of bones and teeth of the cave bear (Ursus spelaeus). The cave bear differs in many characteristics from the recent brown bear and shows a rapid evolution especially in the changes of the teeth due to adaptation to pure herbivorous nutrition. The shifts of the morphotype frequencies of the fourth premolar from the upper jaw were used as a measure of the evolution. The uranium series method is the only suitable tool for the absolute age determination of the fossil bones with ages beyond the time range accessible to the radiocarbon method. By applying this method to the Herdengel cave profile the evolutionary rate of the cave bears was determined. Uranium series data from the fossil bones were partly verified by an independent carbonate speleothem age. For both, bone layers and carbonate formation found in stratigraphic relation, the determined ages correspond to a normal time sequence. According to the relatively fine time scale obtained by absolute dating, the evolutionary mode of the cave bears was determined as gradual. The main novelty of this study is the dating of the successive layers of the Herdengel cave and the determination of evolutionary stages of the cave bear in them.     

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.     

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.     

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.     

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.     

Variability of the upper incisors in the cave bears (Carnivora,Ursidae) from the Caucasus and Urals

Morphometric and morphotypic variability of the cave bear upper incisors from two different geographic regions (Caucasus and Urals), different stratigraphic periods (middle and late Pleistocene), and bearing different mitochondrial haplogroups (kudarensis and ingressus) was studied. The specific diet of the cave bears, i.e. hard vegetables, led to noticeable differences between their incisors and the incisors of the brown bear (Ursus arctos). It was found that the upper incisors of the Caucasian cave bears from different stratigraphic periods demonstrate consistent development of their morphology. The late Pleistocene cave bears from the Urals show a greater similarity to the Caucasian cave bears from earlier periods than with the cave bears from later periods. Our results suggest that the incisor morphology has evolved independently in the Caucasian and Ural cave bears as they belong to different phylogenetic lineages and display different ways of adaptation to local environmental conditions.     

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.     

Ecomorphological correlates of craniodental variation in bears and paleobiological implications for extinct taxa: an approach based on geometric morphometrics

Relative warp analyses of landmarks describing cranial and mandibular shape are used for investigating patterns of morphological variation among extant bears (Mammalia, Carnivora, Ursidae) indicative of diet and feeding behavior. These patterns are used for deriving inferences about the autecology of two extinct species previously assumed to have had different dietary preferences, the North American giant, short-faced bear Arctodus simus and the Eurasian cave bear Ursus spelaeus . Results reveal a set of shared craniodental traits among the herbivorous bears, including short and vaulted skulls with well-developed zygomatic arches, lateralized orbits and small canines, concave jaws with a highly positioned condyle, large moment arms for the temporalis and masseter muscles, and long cheek teeth. In contrast, those bears that consume animal resources have long skulls with small zygomatic arches, frontalized orbits and well-developed canines, and long jaws with a deep mandibular symphysis, low muscle leverages, a condyle situated at the level of the tooth row and reduced cheek teeth. The craniodental morphology of omnivorous bears is intermediate between those of faunivores and herbivores. This is also the case of the short-faced bear and the cave bear, which suggests that previous reconstructions of the feeding ecology of these extinct species (highly carnivorous for A. simus and herbivorous for U. spelaeus ) should be revised.     

Body mass in large extant and extinct carnivores

Body mass in six species of Plio-Pleistocene carnivores was estimated based on the relationship between mass and cross-sectional geometric properties, distal articular surface area, lengths and circumferences of proximal limb bones (femur and humerus) in 28 species of extant carnivores. All measures, except lengths, were found to give congruent body mass estimates. Two of the extinct carnivores ( Smilodon fatalis and Panthera atrox ) are estimated to be as much as one and a half times heavier than previously thought. Based on these results inferences are made concerning possible prey species.     

Hibernating bears as a model for preventing disuse osteoporosis

The hibernating bear is an excellent model for disuse osteoporosis in humans because it is a naturally occurring large animal model. Furthermore, bears and humans have similar lower limb skeletal morphology, and bears walk plantigrade like humans. Black bears (Ursus americanus) may not develop disuse osteoporosis during long periods of disuse (i.e. hibernation) because they maintain osteoblastic bone formation during hibernation. As a consequence, bone volume, mineral content, porosity, and strength are not adversely affected by annual periods of disuse. In fact, cortical bone bending strength has been shown to increase with age in hibernating black bears without a significant change in porosity. Other animals require remobilization periods 2-3 times longer than the immobilization period to recover the bone lost during disuse. Our findings support the hypothesis that black bears, which hibernate for as long as 5-7 months annually, have evolved biological mechanisms to mitigate the adverse effects of disuse on bone porosity and strength.     

泥河湾发现的板齿犀肢骨化石(英文)

板齿犀属(Elasmotherium)由Fischer(1808)根据在西伯利亚发现的材料建立,模式种为西伯利亚板齿犀(E.sibiricum)。板齿犀是一种很特别的犀牛,以其巨大的体型和强壮的额角为特征。目前板齿犀有两个有效种,即E.sibiricum和高加索板齿犀(E.caucasicum)。板齿犀的地理分布范围包括俄罗斯、阿塞拜疆、乌兹别克斯坦、蒙古和中国,时代为更新世。在中国,德日进等曾报道了在泥河湾发现的板齿犀的一块牙齿碎片和几件肢骨,但未进行详细的描述和深入的讨论(TeilharddeChardinandPiveteau,1930)。后来周明镇(1958)又根据山西的零星材料建立了板齿犀的两个新种。不过,中国的这些板齿犀材料最近都被Antoine(2002,2003)归入到E.caucasicum中。在俄罗斯的西伯利亚南部曾发现过相当丰富的E.sibiricum的化石材料,其中包括不少完整的头骨(Fischer,1808,1809)。另一方面,最早发现于亚速海南岸地区的E.caucasicum材料不多,主要是一些孤立的牙齿和齿列,肢骨特别少(Borissiak,1914)。在天津自然博物馆收藏的泥河湾化石标本中有一些桑志华采集的板齿犀的肢骨材料,以远端肢骨为主。此前在中国的板齿犀类方面只有对通古尔的西班牙犀(Hispanotherium)部分肢骨的研究发表(Cerdeo,1996)。本文描述和讨论了泥河湾的板齿犀肢骨材料,包括1件桡尺骨(THP20355)、3件腕舟骨(THP20325,20326,20336)、2件月骨(THP20328,20337)、1件三角骨(THP20338)、2件小多角骨(THP20330,20341)、4件钩骨(THP20333,20327,20329,20339)、3件第三掌骨(THP20342,20343,20332)、2件第四掌骨(THP20318,20319)、3件距骨(THP20303,20308,20310)、1件跟骨(THP20311)、2件跗舟骨(THP20305,20322)、2件骰骨(THP20304,20306)、2件第二骨(THP20316,20317)。早更新世早期的泥河湾动物群中已知包括云簇犀(Dicerorhinusyunchuensis)、泥河湾披毛犀(Coelodontanihowanensis)和E.caucasicum三种犀牛,但前两种犀牛的体型远小于板齿犀,所以仅从肢骨的尺寸上就可以很好地区别它们。泥河湾的这批材料增加了我们对E.caucasicum的了解,它与E.sibiricum在肢骨方面有很多相似性状,如桡骨上容纳腕伸肌的沟宽深,第三掌骨前视可见对头状骨关节面,第四掌骨的近端关节面呈三角形,第五掌骨退化,掌骨上附着腕伸肌的止端显著,距骨对腓骨的关节面倾斜、距骨颈低到中等、滑车与远端关节面的夹角轻度倾斜、对蜗突关节面具长大的舌状延伸、对载距突关节面与对跟骨的外下关节面分离,跟骨对胫骨关节面存在、跟结节粗大、附着腓长肌的止端平滑,肢骨细长,掌骨和骨的中央直嵴低平、骨干上附着骨间肌的止端长但无远端后侧结节。另一方面,这两种板齿犀也存在一些差别,如E.caucasicum的尺骨远端没有对桡骨的第二关节面,而E.sibiricum有;E.caucasicum的钩骨未显示有第五掌骨与其关节,而E.sibiricum钩骨上对第五掌骨的关节面还与对三角骨的关节面联合;E.caucasicum距骨上对腓骨的关节面凹陷,而E.sibiricum平坦。对比已知的少量E.caucasicum肢骨,泥河湾标本在性状和尺寸上与其完全一致,进一步证明将这些标本归入E.caucasicum是可信的。从泥河湾材料我们还了解到板齿犀属的一些未知性状,如骰骨近端呈三角形、跗舟骨顶视呈矩形、距骨的宽/高比达1.21、厚/高比达0.74、对骰骨关节面具后侧突起等。此前的支序分析表明Elasmotherium是板齿犀类中最进步的一个属,泥河湾标本所显示的大多数性状确实是进步的,但仍然有一些原始性状。在板齿犀的两个种中,E.caucasicum可能比E.sibiricum更进步,不过这两个种实际上相当接近。板齿犀类不是一个丰富的犀科类群,然而特别的是在中国有较多的发现,包括几个大型的属,如Elasmotherium、中华板齿犀(Sinotherium)、副板齿犀(Parelasmotherium)、宁夏犀(Ningxiatherium)和伊朗犀(Iranotherium),但都很少有肢骨化石发现。将泥河湾的材料与已知的少量Parelasmotherium和Iranotherium的肢骨相比,显示后两个属不比Elasmotherium进步,这与对它们系统关系的分析结果吻合。E.caucasicum细长的远端肢骨与其高冠和釉质褶皱丰富的颊齿相一致,指示它是干旷草原的硬草取食者。     

A three-dimensional analysis of tooth-root morphology in living bears and implications for feeding behaviour in the extinct cave bear

ABSTRACT

The morphology of both crowns and tooth-roots reflects dietary specialisation in mammalian carnivores. In this article, we analyse the tooth-root morphology of maxillary teeth from CT scans of living bears (Ursus arctos, Ursus americanus, Ursus maritimus, Ursus thibetanus, Melursus ursinus, Helarctos malayanus, Tremarctos ornatus and Ailuropoda melanoleuca) in order to make inferences about the diet and feeding behaviour of the extinct cave bear (Ursus spelaeus sensu lato). Specifically, we investigate two major mitochondrial clades of extinct cave bears recognized by previous authors: Ursus ingressus and Ursus spelaeus (U. spelaeus spelaeus, U. spelaeus ladinicus, U. spelaeus eremus). Our results indicate a close association between tooth-root surface area and feeding behaviour in all living bear species. Tooth-root surface area values of cave bears suggest that they relied more on vegetative matter than living brown bears (Ursus arctos) but subtle differences between these species/subspecies could also indicate different feeding strategies among the members of cave bear complex.     

From a molecules’ perspective – contributions of ancient DNA research to understanding cave bear biology

Abstract

Few members of the Pleistocene megafauna have been as extensively studied as cave bears. Multidisciplinary research into cave bears has provided insights into their morphology, ecology, and evolution. Genetic studies have profited from the availability of large numbers of well-preserved remains. As a result, ‘ancient DNA (aDNA)’ from cave bears has provided significant insights into cave bear ecology, phylogeography and even potential causes of their extinction. Here I review the contributions that genetic research has made to our understanding of cave bear biology and evaluate the potential that new, genomic tools provide to shed further light onto how these iconic representatives of the Pleistocene megafauna lived and died.     

An Overview of the Ichnological and Ethological Studies in the Cave Bear Den in Urşilor Cave (Western Carpathians,Romania)

This paper presents a preliminary investigation of late Pleistocene cave bear traces from Ur?ilor Cave in the western Carpathians, Romania. The bears left thousands of traces on the walls, plateaus, and slopes of the cave interior. Some areas in the cave have been heavily trampled, leaving more than 140 hibernation beds as well as fur impressions. The footprints of cave bears are assigned to Ursichnus europaeus nov. ichnogen. and nov. ichnosp. and the cave bear-beds to Ursalveolus carpathicus nov. ichnogen. and nov. ichnosp. as behavioral traces. Tens of thousands of scratch marks on the slopes and top of a clay plateau are the result of bears moving from the hibernation area down to a stream and back. These traces reveal that the cave bears had short claws, similar to those of modern, primarily herbivorous black bears. Deep within the cave, three weathered, articulated cave bear skeletons still lie in their hibernation beds on the clay plateaus or a natural cave corner. One of these bears was a one-year-old male cub that did not survive its first hibernation; a second skeleton close was an adult female. The third, a young male, was found close to the end of the cave system. The bears of Ur?ilor Cave would have felt well protected against carnivores during their hibernation because their sleeping places were so deep within the cave. Their strategy may well have been to avoid any conflict with hyenas and lions during hibernation.     

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.     

Evidence for reproductive isolation between cave bear populations

The European cave bear (Ursus spelaeus), which became extinct around 15,000 years ago, had several morphologically different forms. Most conspicuous of these were small Alpine cave bears found at elevations of 1,600 to 2,800 m. Whereas some paleontologists have considered these bears a distinct form, or even a distinct species, others have disputed this. By a combination of morphological and genetic methods, we have analyzed a population of small cave bears from Ramesch Cave (2,000 m altitude) and one of larger cave bears from Gamssulzen Cave (1,300 m), situated approximately 10 km apart in the Austrian Alps (Figure 1A). We find no evidence of mitochondrial gene flow between these caves during the 15,000 years when they were both occupied by cave bears, although mitochondrial DNA sequences identical to those from Gamssulzen Cave could be recovered from a site located about 200 km to the south in Croatia. We also find no evidence that the morphology of the bears in the two caves changed to become more similar over time. We suggest that the two cave bear forms may have represented two reproductively isolated subspecies or species.     

Proportions and function of the limbs of glyptodonts

Vizcaíno, S.F., Blanco, R.E., Bender, J.B. & Milne, N. 2010: Proportions and function of the limbs of glyptodonts. Lethaia, Vol. 44, pp. 93–101. This study examines the limb bone proportions and strength of glyptodonts (Xenarthra, Cingulata). Two methods are used to estimate the body mass and location of the centre of gravity of the articulated specimens. These estimates, together with measurements of the femur and humerus, are used to calculate strength indicators (SI). The other long bones of the limbs are used to calculate limb proportion indices that give an indication of digging ability, speed, and limb dominance in armadillos, the glyptodonts’ living closest relatives. The results show that regardless of how the body mass and centre of gravity are calculated, the majority of the glyptodont’s weight is borne by the hindlimbs. The SI calculations show that femora are sturdy enough to bear these loads. The fact that the femora have higher SI than the humerii indicates that sometimes the hindlimbs are required to bear an even greater proportion of the body weight, possibly when rising to a bipedal posture or pivoting on their hindlimbs to deliver a blow with their armoured tail. The analysis of limb proportions indicates that both the hindlimb and the forelimb have proportions that correlate strongly with body mass. This outcome supports the other results, but also shows that forelimbs must be also involved in manoeuvring the glyptodont body. □Glyptodonts, Mammalia, Xenarthra, limbs, strength indicators.     

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