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.     

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.     

Diet reconstruction in cave bears from craniodental morphology: past evidences,new results and future directions

ABSTRACT

The diet of the cave bear (Ursus spelaeus) is a controversial topic, as different paleobiological approaches (e.g. dental wear, isotopic biochemistry, skull morphometrics) result in different dietary inferences for the cave bear, ranging from carnivory to pure herbivory. Here, we review the main results obtained from these approaches, with special emphasis on those obtained from the morphometric analyses of the cave bear craniodental skeleton. Then, we compute a between-group Principal Components Analysis from a set of 3D-landmarks digitized on 103 mandibles of living bears and extinct cave bears and using a phylomorphospace approach. Moreover, we also reconstructed the evolutionary trajectory of the cave bear mandible from the hypothetical shape of its inferred ancestor. Our results indicate that the mandible of the cave bear possess specific traits indicative of a highly-herbivorous diet or, at least, more herbivorous than their closest living relative, the brown bear (Ursus arctos). Moreover, we also propose new directions for future research to obtain more detailed inferences on the potential food resources consumed by the cave bear being crucial to understand the ‘life and death’ of this vanished animal.     

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.     

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.     

Sequencing mtDNA of the cave bearUrsus spelaeus from the Bavarian Alps is feasible by nested and touchdown PCR

Ancient DNA from bones of the extinctUrsus spelaeus Rosamueller et Hainroth, 1794 found in the Bavarian Alps has been amplified by PCR. Two out of five samples yielded a distinct band of 135 bp originating from the mtDNA control region. A combination of nested and touchdown PCR supported the amplification. Analysis of the nucleotide sequences revealed four transitions compared to the French cave bear sequence, the only cave bear data known so far (Genbank database X80259, AF121779). The consensus distant matrix tree clustered the two cave bears next to the brown bearUrsus arctos Linnaeus, 1758.     

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.     

The story continues: recent advances on the life and death of the Pleistocene cave bear

ABSTRACT

In this issue, we cover an exceptional topic in Vertebrate Paleobiology that has been an enjoyable challenge for scientists and the popular media alike: the life and death of the Pleistocene cave bear (Ursus spelaeus). As an icon of the ice-age, the cave bear inhabited the glacial ecosystems of Eurasia, and it was the inspiration of a popular book written in 1976 by Björn Kurtén, entitled The cave bear story: life and death of a vanished animal. Although ‘The life and death’ was a summary of the knowledge acquired on cave bear biology at that time, four decades later, many aspects of its palaeoecology, extinction and evolution are still a matter of debate. With this volume, we aim to bring together the most recent research on cave bear biology in order to provide an update on the palaeoecology, biogeography, systematics, and phylogeny of this recently extinct ursine bear. We thus organised a symposium on the 1st of August 2017 as part of the three-day Annual Meeting of the European Association of Vertebrate Palaeontologists (EAVP) in Munich, Germany, that was an additional opportunity to announce the volume and to discuss this exciting subject face-to-face among specialists.     

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.     

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.     

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.     

Palaeoecology of cave bears as evidenced by dental wear analysis: a review of methods and recent findings

Abstract

The study of dental wear was first used years ago to infer the palaeoecology of fossil mammals and in particular their diet. Results depend predominantly on the scale of the analysis used. Analyses of dental macrowear, mesowear or microwear do not provide the same type of dietary information, be it about the seasonal, annual or lifetime diet. This contribution focuses on emblematic species, cave bears (Ursidae), in particular Ursus spelaeus spelaeus. Methods used by previous researchers to infer their dietary preferences and thus their palaeoecology are reviewed and compared. This review is complemented by an analysis of several specimens of cave bears from the Goyet cave in Belgium, using dental microwear texture analysis (DMTA), a methodology widely applied for reconstructing palaeodiets. Three main conclusions are drawn here: (1) DMTA is the method that provides the most precise palaeobiological inferences; (2) during the pre-dormancy period, cave bears show dietary flexibility; (3) dental wear alone might be not sufficient to provide a complete reconstruction of the cave bear palaeodiet.     

Sex-ratio et analyse des mélanges d'Ursus spelaeus (Carnivora,Ursidae) du gisement pléistocène supérieur de Fate (Ligurie,Italie). Implications paléobiologiques

Determination of the sex-ratio of a fossil population is essential for understanding the palaeoethology of a taxon, and this is especially true for the cave bear (Ursus spelaeus). Classical methods for determining sex-ratios such as analyses using uni and bivariate plots are based on an arbitrary fixing of the limit between the sexes. Therefore, a more robust statistical method termed mixture analysis has been applied in this study to test all the postcranial remains of cave bear (essentially carpals, tarsals and metapodials) derived from the Upper Pleistocene site of Fate (Liguria, Italy).Results give a sex-ratio of about 35% female individuals and show a clear predominance of males. Mixture analysis appears to be a reliable method for sex-ratio determination in U. spelaeus. In this study, few dimensions have been excluded because of a significant error in sex classification. The numerous measurements identified as good predictors of sexual dimorphism in the cave bear are probably linked to the marked sexual differences in the body mass of the animal. Palaeobiological interpretations suggest that there are no available hypotheses to explain the high variability of sex-ratios documented for the cave bear in Palaeolithic sites. The individual animal behaviour appears to be the only criteria in determining their choice of a winter den. But trophic and social regulations on living populations may have influenced this choice.The association between mortality profiles and sex-ratios appears to be related to the general function of a den. The thanatocenosis of cave bears in the Fate assemblage indicates the presence of a high number of juveniles and male individuals, such that the site may have served either as a nursery or and as a male den.     

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.     

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.     

Chronological and Isotopic data support a revision for the timing of cave bear extinction in Mediterranean Europe

Abstract

The Cave Bear, Ursus spelaeus (sensu lato), was one of many megafaunal species that became extinct during the Late Pleistocene in Europe. With new data we revisit the debate about the extinction and paleoecology of this species by presenting new chronometric, isotopic and taphonomic evidence from two Palaeolithic cave bear sites in northeastern Italy: Paina Cave and Trene Cave. Two direct radiocarbon dates on well-preserved collagen have yielded ages around 24,200–23,500 cal yr BP, which make them the latest known representatives of the species in Europe. The carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopic values of bone collagen exhibit values similar to those of older cave bears from Swabian Jura and France, suggesting that the feedings preferences of cave bears remained unchanged until the disappearance of this species in Europe. Several bear remains preserved traces of human modification such as cut marks, which enables a reconstruction of the main steps of fur recovery and the butchering process. The broad range of plant types available and the favorable location of Berici Hills may have played an important role in the range expansion of cave bears and their interaction with the Paleolithic hunters settled the same area.     

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.     

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.