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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Efficacy of Bear Deterrent Spray in Alaska

Abstract: We present a comprehensive look at a sample of bear spray incidents that occurred in Alaska, USA, from 1985 to 2006. We analyzed 83 bear spray incidents involving brown bears (Ursus arctos; 61 cases, 74%), black bears (Ursus americanus; 20 cases, 24%), and polar bears (Ursus maritimus; 2 cases, 2%). Of the 72 cases where persons sprayed bears to defend themselves, 50 (69%) involved brown bears, 20 (28%) black bears, and 2 (3%) polar bears. Red pepper spray stopped bears' undesirable behavior 92% of the time when used on brown bears, 90% for black bears, and 100% for polar bears. Of all persons carrying sprays, 98% were uninjured by bears in close-range encounters. All bear—inflicted injuries (n = 3) associated with defensive spraying involved brown bears and were relatively minor (i.e., no hospitalization required). In 7% (5 of 71) of bear spray incidents, wind was reported to have interfered with spray accuracy, although it reached the bear in all cases. In 14% (10 of 71) of bear spray incidents, users reported the spray having had negative side effects upon themselves, ranging from minor irritation (11%, 8 of 71) to near incapacitation (3%, 2 of 71). Bear spray represents an effective alternative to lethal force and should be considered as an option for personal safety for those recreating and working in bear country. (JOURNAL OF WILDLIFE MANAGEMENT 72(3):640–645; 2008)     

The diverse dietary profiles of MIS 3 cave bears from the Romanian Carpathians: insights from stable isotope (δ13C and δ15N) analysis

Late Pleistocene European cave bears (Ursus spelaeus ) have been considered to be largely vegetarian, although stable isotope data (δ¹³C and δ¹⁵N values) from the Romanian Carpathians has suggested considerable dietary variation. Here we evaluate previous and additional adult cave bear isotopic data from four Marine Isotope Stage 3 (MIS 3) sites in the Carpathians. Pe?tera Ur?ilor (N  =  35), Pe?tera Cioclovina (N  =  32), Pe?tera Muierilor (N  =  8), and Pe?tera cu Oase (N  =  72) provide both a dichotomy between samples suggesting vegetarian diets (from Cioclovina and Muierilor) and more omnivorous diets (from Ur?ilor and Oase), and considerable isotopic variation within samples from each site. While an inference of a strictly vegetarian diet may apply to groups that lived in ecosystems which restricted the available animal protein for these large ursids, the within and between sample isotopic variation among the Carpathian cave bears indicates considerable flexibility in their sources of protein and hence in their dietary regimes. In addition, developmental assessment of Cioclovina isotopic profiles (neonates, juveniles, sub‐adults and adults) provides patterns of transfer of stable isotope signatures throughout immature life for both δ¹³C and δ¹⁵N (increase and decrease, respectively), whereas those from Ur?ilor show little developmental shift.     

Efficacy of firearms for bear deterrence in Alaska

We compiled, summarized, and reviewed 269 incidents of bear–human conflict involving firearms that occurred in Alaska during 1883–2009. Encounters involving brown bears (Ursus arctos; 218 incidents, 81%), black bears (Ursus americanus; 30 incidents, 11%), polar bears (Ursus maritimus; 6 incidents, 2%), and 15 (6%) unidentified species provided insight into firearms success and failure. A total of 444 people and at least 367 bears were involved in these incidents. We found no significant difference in success rates (i.e., success being when the bear was stopped in its aggressive behavior) associated with long guns (76%) and handguns (84%). Moreover, firearm bearers suffered the same injury rates in close encounters with bears whether they used their firearms or not. Bears were killed in 61% (n = 162) of bear–firearms incidents. Additionally, we identified multiple reasons for firearms failing to stop an aggressive bear. Using logistic regression, the best model for predicting a successful outcome for firearm users included species and cohort of bear, human activity at time of encounter, whether or not the bear charged, and if fish or game meat was present. Firearm variables (e.g., type of gun, number of shots) were not useful in predicting outcomes in bear–firearms incidents. Although firearms have failed to protect some users, they are the only deterrent that can lethally stop an aggressive bear. Where firearms have failed to protect people, we identified contributing causes. Our findings suggest that only those proficient in firearms use should rely on them for protection in bear country. © 2012 The Wildlife Society.     

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.     

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.     

Environmental enrichment for zoo bears

The high incidence of stereotypic behaviors in zoo bears (van Keulen-Kromhout: International Zoo Yearbook 18:177–186, 1978) suggests that the environment of these animals lacks essential stimuli for guiding normal behavior. Three experiments investigated ways in which bear husbandry procedures can be altered to promote normal behavior. In experiments 1 and 2, honey-filled logs were given to a sloth (Melursus ursinus), American black (Ursus americanus), and brown bear (Ursus arctos) to determine 1) the role of food in stimulating investigatory behavior, 2) the rate of habituation to manipulable objects introduced into the exhibit, and 3) effects on locomotory behaviors. Results show specific and general habituation to the introduced objects that can be counteracted by refilling the logs with honey and by providing multiple logs in the exhibit. Investigatory activity directed toward honey-logs replaces pacing and walking in the sloth bear and is most effective in doing so when the log is novel. Experiment 3 examined the behavioral effects of feeding an American black bear in three different ways: 1) once daily in the den, 2) once daily with supplemental food from a mechanical feeder, and 3) once daily with food hidden in the exhibit in manipulatable objects. The latter method reduced stereotypic pacing from a median of 150 min/day to 20 min/day; the mechanical feeder method had no such effect. The results of a survey of 67 zoos concerning the diet and manner of feeding these three species of bears, as well as Asian black bears (Ursus thibetanus) are presented. Results are discussed with respect to the ways in which husbandry procedures can be improved to stimulate functional foraging and feeding behavior in confined bears.