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.     

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.     

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.     

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.     

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.     

The cave bear’s hibernation: reconstructing the physiology and behaviour of an extinct animal

Abstract

When studying an extinct species such as the cave bear (Ursus spelaeus ROSENMÜLLER 1794), it is possible to apply a variety of molecular biology techniques such as the study of stable isotopes or mitochondrial DNA (mDNA) to infer patterns of behaviour or physiology that would otherwise remain concealed. Throughout Europe and along time, differences in the isotopic values (δ¹³C and δ¹⁵N) of cave bears arise from environmental differences and the Pleistocene climatic evolution. The climate determines the hibernation length, during which the cave bears undergo a particular physiology that can be related to an increase in δ¹⁵N during climate cooling. In order to verify whether hibernation affected the isotopic values, we compared cave bears in different ontogenetic stages. The results show that perinatal values reflect the values for mothers during hibernation, while juveniles show differences in maternal investment. A previous study in the literature based on complete mitochondrial DNA sequences of several individuals collected from closely situated caves showed that each cave housed, almost exclusively, a single lineage of haplotypes. This pattern suggests extreme fidelity to the birth site, or homing behaviour, and that cave bears formed stable maternal social groups, at least for the purpose of hibernation. Studies of this type offer unexpected data on the palaeobiology of this extinct animal.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Stable isotopes data (delta13C, delta15N) from the cave bear (Ursus spelaeus): a new approach to its palaeoenvironment and dormancy

Palaeoclimatic data that can be extracted from the isotopic signatures of delta13C and delta15N, which are found in fossil bone collagen, should be analysed according to the specific metabolism of each species. Although Ursus spelaeus is an extinct species, its metabolism is assimilated to current, closely related species of bear. In this study, bone collagen isotopic signatures (delta13C and delta15N) of cave bears from Late Pleistocene Alpine sites were compared to those that have already been documented. The delta13C signature did not seem to follow a systematic trend according to climatic conditions, probably as a consequence of the high variability present in the values of C3 plants, which were the basis of feeding. On the contrary, the delta15N signature displayed higher values in sites corresponding to colder periods in which the delta15N signature appeared to be dominated by the physiology of dormancy. Then, due to the reuse of urea in synthesizing amino acids, the delta15N signature systematically increased along with dormancy duration. This was related to the length of winter and, in turn, depended on climate.     

Cranial and mandibular morphology of Middle Pleistocene cave bears (Ursus deningeri): implications for diet and evolution

ABSTRACT

Deninger’s bears (Ursus deningeri) have been studied less frequently than Ursus spelaeus s.l. Our objective is to present, for the first time, an analysis of the skull shape of U. deningeri.

Bear crania and mandibles were digitised with a Microscribe or CT-scanned and the surface models subsequently landmarked. The landmarks were chosen based on a compromise between functional morphology and sample size.

Results show that U. deningeri and U. spelaeus mandibles display very similar morphologies and allometric trajectories, both to each other and to Ailuropoda melanoleuca. It is inferred that masticatory adaptations to a herbivorous diet were already present in the Middle Pleistocene. U. deningeri displays a cranial morphology that is similar to that of U. spelaeus when comparing all species, but U. deningeri has a relatively narrower and dorsoventrally lower zygomatic arch than U. spelaeus, although the masticatory signal is less strong in the skull.

We observe intraspecific differences between different populations of U. deningeri, which could parallel the genetic diversity found in U. spelaeus. The intraspecific differences found within U. deningeri may be temporal and/or geographical in nature and could be related to the evolution of the Late Pleistocene cave bear, but this hypothesis remains to be tested.     

Ancient DNA reveals differences in behaviour and sociality between brown bears and extinct cave bears

Ancient DNA studies have revolutionized the study of extinct species and populations, providing insights on phylogeny, phylogeography, admixture and demographic history. However, inferences on behaviour and sociality have been far less frequent. Here, we investigate the complete mitochondrial genomes of extinct Late Pleistocene cave bears and middle Holocene brown bears that each inhabited multiple geographically proximate caves in northern Spain. In cave bears, we find that, although most caves were occupied simultaneously, each cave almost exclusively contains a unique lineage of closely related haplotypes. This remarkable pattern suggests extreme fidelity to their birth site in cave bears, best described as homing behaviour, and that cave bears formed stable maternal social groups at least for hibernation. In contrast, brown bears do not show any strong association of mitochondrial lineage and cave, suggesting that these two closely related species differed in aspects of their behaviour and sociality. This difference is likely to have contributed to cave bear extinction, which occurred at a time in which competition for caves between bears and humans was likely intense and the ability to rapidly colonize new hibernation sites would have been crucial for the survival of a species so dependent on caves for hibernation as cave bears. Our study demonstrates the potential of ancient DNA to uncover patterns of behaviour and sociality in ancient species and populations, even those that went extinct many tens of thousands of years ago.     

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.     

Natural-trap ursid mortality and the Kurtén Response

Ursid mortality data have long been used to evaluate associations between cave-bear remains (Ursus deningeri and U. spelaeus) and hominin (Homo sp.) remains. Typically, such ursid assemblages produce mortality patterns that indicate that juvenile and old bears died during hibernation, a pattern that is used to suggest that humans and bears occupied the same caves at different times. However, a different kind of mortality pattern can also be used to suggest human influence on cave bears, particularly under circumstances when bears and humans compete for habitat. In particular, data from Lawson Cave and Jerry Long Cave, Missouri indicate that young-adult North American black bears (Ursus americanus) are prone to capture in natural-trap caves. Similar faunal data from Sima de los Huesos in Spain, where cave-bear and hominin remains are found in the same deposit, might also suggest that the bears died from falling into a natural trap. It is concluded that mortality analysis of ursid remains from caves is a useful tool with which to evaluate accumulation histories of cave deposits and relations between humans, artifacts, and cave-bear remains. In particular, ursid mortality data are relevant to the Kurtén Response, a hypothesis reiterated in the recent literature that implicates human encroachment on ursid habitat (e.g., cave den sites) as a potential cause in cave-bear extinction.     

Bear-hybrids: behaviour and phenotype

The behaviour of a female and a male bear hybrid (brown bear Ursus arctos x polar bear Ursus maritimus) was studied. Behavioural and morphological comparisons between the hybrids and the two parent-species were made.The observation period covered July to November 2007. Different objects were offered to the bears to evoke new patterns of behaviour. While manipulating the offered objects, both bears showed elements of behaviour also found in polar bears, though the male performed those to a larger extend. Not only in the way of manipulating objects but also in the male's type of stereotype parallels to polar bears can be drawn. Phenotypically both bears possess features of both species, brown bear and polar bear. Concerning it lighter colour of fur and the structure of hair the female hybrid resembles more a polar bear than the male. Summarising, the female appears phenotypically more like a polar bear, the male with respect to the behaviour.