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Behavioural ecology of Late Pleistocene bears (Ursus spelaeus, Ursusingressus): Insight from stable isotopes (C, N, O) and tooth microwear

Susanne C. Münzel a,*, Florent Rivals b,c, Martina Pacher d, Doris Döppes e,Gernot Rabeder d, Nicholas J. Conard a, Hervé Bocherens f

aCenter for Archaeological Science, Archaeozoology, University of Tübingen, Germanyb Institut Català de Paleoecologia Humana i Evolució Social (IPHES), C. Marcel.lí Domingo s/n, Campus Sescelades URV (Edifici W3), 43007 Tarragona, Spainc ICREA, Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spaind Institute of Palaeontology, University of Vienna & Station Lunz am See, AustriaeReiss-Engelhorn Museen, Mannheim, Germanyf Fachbereich Geowissenschaften, Forschungsbereich Paläobiologie e Biogeologie, Universität Tübingen, Germany

a r t i c l e i n f o

Article history:Available online 12 November 2013

a b s t r a c t

Several types of bears lived in Europe during the Late Pleistocene. Some of them, such as cave bears(Ursus s. spelaeus and Ursus ingressus), did not survive after about 25,000 years ago, while others are stillextant, such as brown bear (Ursus arctos). Our article aims at a better understanding of the palaeoecologyof these large “carnivores” and focuses on two regions, the Ach valley in the Swabian Jura (SW-Germany)with Geißenklösterle and Hohle Fels, and the Totes Gebirge (Austria) with Ramesch and Gamssulzencaves. Both regions revealed two genetically distinct cave bear lineages, and previous studies suggestbehavioural differences for the respective bears in these two regions.

In the Ach valley, irrespective of the cave site, U. s. spelaeus was replaced by U. ingressus around 28 kauncal BP with limited chronological overlap without recognizable dietary changes as documented by theisotopic composition (13C, 15N) of the bones. Furthermore, the present study shows that the dentalmicrowear pattern was similar for all bears in both caves, however with a larger variability in Gei-ßenklösterle than in Hohle Fels.

In contrast, the two Austrian caves, Gamssulzen (U. ingressus) and Ramesch (Ursus s. eremus), showconsiderable differences in both palaeodietary indicators, i.e., stable isotopes, and dental microwear, overat least 15,000 years. The oxygen and carbon analysis of the tooth enamel combined with the dentalmicrowear of the same molars provide an extremely diversified picture of the feeding behaviour of thesefossil bears. The already known differences between these two study areas are confirmed and refinedusing the new approaches. Moreover, the differences between the two cave bear lineages in the TotesGebirge became even larger. Some niche partitioning between both types of cave bears was supported bythe present study but it does not seem to be triggered by climate. This multi-disciplinary approach givesnew insights into the palaeobiology of extinct bears.

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1. Introduction

The most straightforward palaeontological approach to gainmore knowledge about the paleoecology of fossil species is to usemetrical morphology. Using this classical method, Sacco and VanValkenburgh (2004) studied the cranio-dental morphology of

different extant bear species in order to classify typical diet andfeeding behaviour groups. They classified the feeding behaviour ofextant bears a priori as carnivorous, herbivorous or omnivorous(Sacco and Van Valkenburgh, 2004, Tab. 1). For some food spe-cialists amongst bears, such as polar bear feeding on meat or pandabears feeding on bamboo, just to mention the extreme feeders, it iseasy to predict the diet, but extant brown and black bears can covera broad spectrum of nutritional specialisations depending on theenvironment and coeval competing species. As the diet of thesebears is highly variable, it would have been necessary to combinethe morphometric analysis with a multi-disciplinary approachwhich track phenotypic features acquired by the individual animals

* Corresponding author.E-mail addresses: susanne.muenzel@uni-tuebingen.de (S.C. Münzel), frivals@

iphes.cat (F. Rivals), martina.pacher@univie.ac.at (M. Pacher), Doris.Doeppes@mannheim.de (D. Döppes), gernot.rabeder@univie.ac.at (G. Rabeder), nicholas.conard@uni-tuebingen.de (N.J. Conard), herve.bocherens@uni-tuebingen.de (H. Bocherens).

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during their life-time, such as stable isotope analysis of carbon andnitrogen as well as tooth microwear of the respective individuals.

Over the past two decades, progress wasmade in the knowledgeon cave bear paleoecology, thanks to applications of new methods,such as palaeogenetic and isotopic palaeoecologial tracking. Thehigh morphological variability of cave bears was and still is dis-cussed by many researchers regarding phylogenetic, geographicand intra-population variability (e.g. Ehrenberg,1922,1929; Kurtén,1976; Rabeder et al., 2000; Grandal d’Anglade and López-González,2005; Baryshnikov, 2006). This variability was supported by a highdiversity of ancient DNA during the last decade of research (Leonardet al., 2000; Loreille et al., 2001; Hofreiter, 2002; Hofreiter et al.,2002, 2004, 2007; Orlando et al., 2002; Knapp et al., 2009; Stilleret al., 2010). Palaeogenetic research revealed six different hap-logroups in Europe and Asia including numerous haplotypes (Stilleret al., 2014). This genetic diversity raised the question of ecologicaland behavioural differences amongst these cave bear lineages. Forthese questions stable isotope research comes into play.

Cave bear was the first Pleistocene extinct species for whichcarbon and nitrogen isotopic composition was used to investigateits palaeodiet (Bocherens et al., 1990, 1994), and it is probably theLate Pleistocene large mammal species with the largest isotopicdataset published so far (e.g. Bocherens, 2002, 2004; Bocherenset al., 2004, 2011a; Grandal d’Anglade et al., 2011; Münzel et al.,2011; Pacher et al., 2012; Robu et al., 2013). From almost all stud-ied cave bears in Europe, ranging from Spain to Romania, aconsistent patternwith nitrogen isotopic composition of adult bonecollagen as low or even lower than those of coeval herbivoresemerged, indicating negligible if any consumption of animal foodresources for the studied individuals, and therefore an essentiallyvegetarian diet (e.g. Bocherens et al., 1997, 2006, 2011a; Nelsonet al., 1998; Vila Taboada et al., 1999; Bocherens, 2004; Blantet al., 2010; Münzel et al., 2011; Horacek et al., 2012; Pacheret al., 2012). One possible exception to this pattern has beenobserved in cave bears from Romanian caves, where some speci-mens exhibit higher nitrogen isotopic composition than coevalungulates (Richards et al., 2008; Robu et al., 2013; Trinkaus andRichards, 2013). This led the authors to suggest omnivory or

carnivory for these cave bears, but the observed isotopic pattern isnot similar to the case of real carnivores or omnivorous brownbears, and could be related instead to a different kind of plant foodand/or to an impact of climate and length of hibernation ratherthan to carnivory (Grandal d’Anglade et al., 2011; Bocherens, comm.pers.). Therefore there is evidence of some amount of dietaryvariation within the distribution range of cave bears and under-standing the extent and the causes of such variation is important toprovide hypotheses about the possible causes of their extinction.

The analysis of tooth wear, in contrast, is a relatively newapproach for fossil mammals. It gives insights into the dietarybehaviour of individuals, provides insights into niche partitioningof entire populations and seasonal fluctuations in diet of ungulates(Merceron and Madelaine, 2006; Rivals et al., 2009; Rivals andSemprebon, 2011), and last but not least it also provides a snap-shot of the environmental condition at that time (Rivals andSemprebon, 2011). Tooth microwear features reflect the texture ofthe diet during the last days or weeks before the death of the in-dividual (last supper effect). In this respect it ideally complementsthe results gained by stable isotope analysis in bone or toothenamel, which reflect the time of the formation or development ofthe tissue several months or years ago (Fig. 1).

For ungulates, the tooth microwear patterns are usually classi-fied into dietary groups of browsers, grazers, mixed feeders andfruit browsers (Solounias and Semprebon, 2002). For bears as anomnivorous species we have to extend to groups including animalfood in their diet. The majority of the studies performed on un-gulates were aiming to test for example dietary plasticity of fossilspecies compared to their modern relatives, such as American andextinct bison (Rivals et al., 2007; Rivals and Semprebon, 2011). Thisstudy revealed a larger plasticity for these ungulates during LatePleistocene compared to extant bison and shows that data on theecology of modern relatives do not always reflect the ecology ofextinct species (Rivals and Semprebon, 2011). Besides direct in-ferences about the food, tooth microwear (pits in particular) mayreflect some also interesting non-dietary traits. For example,through tooth microwear analysis it is possible to identify the in-fluence of dust and grit, which is ingested if the animals feed close

Fig. 1. Summary of the periods of life recorded by the isotopic composition of different skeletal tissues and the tooth microwear in cave bears. A longevity of around 25 years waschosen in accordance with evaluations based on tooth cementochronology (Djebeljak, 2007).

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to the ground or on leaves in dry environments (Semprebon andRivals, 2007, 2010).

The approach of dental microwear is especially interesting forbears, as their multi-cusp dentition is characteristic for omnivorespecies and the enlargement of their molars is an important pre-requisite to digest vegetation (e.g. Ward and Kynaston, 1999). Todate there are very few studies of dental microwear on carnivores(Van Valkenburgh et al., 1990; Goillot et al., 2009; Schubert et al.,2010; Stynder et al., 2012) and especially on bears (Peigné et al.,2009; Pinto-Llona, 2006, 2013). When working with extinct spe-cies of unknown diet and unknown environment, one of the majordifficulties is to find the appropriate references. Peigné et al. (2009)studied the microwear of cave bears from Goyet (Belgium) andcame to the conclusion that these cave bears were omnivorous. Thisdeduction was based on a comparison with a set of modern car-nivores. The chosen reference extant bears belonged to specieswith very specialized diets, such as giant panda (Ailuropoda mela-noleuca) feeding on bamboo or spectacled bear (Tremarctos ornatus)consumingmainly tropical fruits. These two species of bears belongto lineages that separated early from ursine bears, to which cavebears belong (Krause et al., 2008). Moreover, the study by Peignéet al. (2009) was lacking analysis on ursine bears from temperateand boreal ecosystems, such as brown bears and American blackbears, which consume a large variety of food, such as grass, nuts,berries or tubers a diet, which was more likely available to cavebears (Bocherens, 2009). The difficulty with these omnivorousbears is that each individual may have a different diet (e.g. Jacobyet al., 1999; Beckmann and Berger, 2003; Bojarska and Selva,2011). To evaluate individual diet, we chose to use carbon and ni-trogen isotopic composition of bone collagen as a proxy for indi-vidual diet in modern, ancient, and fossil brown bears (Bocherenset al., 2004; Münzel et al., 2011).

Only one previous study compared cave bear to brown bearmicrowear, and found considerable differences between themicrowear pattern of the two bear species, even if they lived in thesame region (Pinto-Llona, 2006, 2013). However, this study con-siders brown bears with ‘known diet’ which were not coeval withthe cave bears, and the diets are deduced and not measured directlyon the same individuals. Without direct information about the po-sition of the individual bear in a food web, it is not possible to drawconclusions about the diets of either brown bears or cave bears.

The approach used in the present study is slightly different fromthat used in other studies, since we combine dental microwear ofextant and fossil bears with stable isotope analysis on the samespecimens. We used the carbon and nitrogen of bone collagen forthe isotopic composition to evaluate the diet of modern and ancientbrown bears used as reference, and we measured the carbon andoxygen isotopic composition of tooth enamel carbonate for cavebears in the same teeth as the ones investigated for microwearpatterns, allowing us to combine palaeodietary and palaeo-climatological information on the same specimens. The presentstudy is also the first one to our knowledge comparing differentassemblages of cave bears in Europe using these same approaches.

2. Background on the investigated cave bear assemblages

Among some of themost intensively investigated cave bear sitesare those from the Swabian Jura and the Totes Gebirge. The loca-tions under study come from two topographically very differentareas. The Swabian Jura in SW-Germany is a middle range moun-tainous areawith elevations up to 600m a.s.l., cut by valleys formedby former tributaries of the Danube. In this area we focus on theAch valley on Geißenklösterle cave near Blaubeuren and on HohleFels cave near Schelklingen, which are not more than 3 km apart(Fig. 2).

Archaeological research in the Ach valley began in the 19thcentury. In the years 1870/71 Oscar Fraas (1872) and TheodorHartmann started their work in Hohle Fels cave. Fraas’ researchquestion at his time was whether extinct Diluvial mammals co-existed with humans. During the excavation of the main hall ofHohle Fels large quantities of cave bear remains were recovered,but many faunal remains were lost during World War II.

Modern excavations in Hohle Fels and Geißenklösterle started inthe 1970s by Joachim Hahn (1977, 2000). His research wascontinued by Nicholas Conard from 1997 until today (Conard andMalina, 2012). The stratigraphical sequences of these two cavesites are well dated (Richter et al., 2000; Conard and Bolus, 2003,2008; Higham et al., 2012). Hohle Fels and Geißenklösterle arewell known for their earliest musical instruments (Hahn andMünzel, 1995; Conard et al., 2004, 2009) and their figurative art(Hahn,1986; Floss, 2007), with the earliest female figurine found inthe deepest Aurignacian layer of Hohle Fels (Conard, 2009). Thefaunal research has been completed for Geißenklösterle (Münzeland Conard, 2004a) and is still in progress for Hohle Fels (Münzeland Conard, 2004b; Conard et al., 2013). An important faunal findwas made in 2001. A cave bear vertebra was found with a projectilepoint still sticking in the transversal process (Münzel et al., 2001).This find, together with numerous cut marks on cave bear remains,initiated a new discussion on cave bear hunting, its demise andfinal extinction (Münzel et al., 2011; Bocherens et al., 2014).

The other area is Totes Gebirge in the Austrian High Alps,focusing on Ramesch-Knochenhöhle and Gamssulzen cave.Ramesch-Knochenhöhle is situated on the northern side of theWarscheneck at 1960 m a.s.l. and Gamssulzen cave in the easternpart of the Warscheneck at 1300 m a.s.l. Both caves are not morethan about 10 km apart (Fig. 2). In the more remote Totes Gebirgesystematic research started later than in the Swabian Jura.Palaeontological excavations in Ramesch started in 1979 andcontinued until 1984. The excavations revealed a rich faunalassemblage dominated by cave bear remains. Only one artefactwas found, ascribed to a Mousterian tradition (Hille and Rabeder,1986), but documenting presence of human hunters in these highelevations. Several radiocarbon dates place the cave bear remainsinto a time span from 49,500 to 30,000 uncal BP (Pacher andStuart, 2008).

Excavations in Gamssulzen cave started in 1988 and werecontinued until 1991. This large cave was excavated in threedifferent areas consisting two levels, which are both dominated bycave bear bones. However, evidence of a Late Glacial humanoccupation was documented at the cave entrance (Rabeder, 1995;Rabeder et al., 2008). Radiometric dates place the cave bear re-mains into a time span from 47 ka to 32 ka uncal BP (Pacher andStuart, 2008). Based on genetic and morphometric analysis,Ramesch and Gamssulzen caves were each visited by two distinctcave bear lineages, by Ursus s. eremus and Ursus ingressus respec-tively (Rabeder et al., 2004). Furthermore the datings suggest acoeval occupation of the two caves during a time span of circa15,000 years. These two distinct cave bear lineages U. s. eremus andU. ingressus living sympatric in the same area during the same timespan led to the question of a possible different adaptation to themountainous environment.

3. Previous paleobiological studies in both regions

In Totes Gebirge, two cave bear lineages, U. s. eremus in Rameschand U. ingressus in Gamssulzen, lived sympatrically for 15000 years(Hofreiter, 2002; Hofreiter et al., 2004). Although the carbon andnitrogen isotopic values of the bone collagen indicated that bothbears were herbivorous, the isotopic values are significantlydifferent and point to the consumption of different food resources

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(Bocherens et al., 2011a). Furthermore, the oxygen isotope values ofthe bone apatite were significantly different for the two caves,suggesting an occupation of the caves under different climatic re-gimes by the respective bear lineages (Bocherens et al., 2011a).These results led to the interpretation of genetic stability in eithercave (Hofreiter et al., 2004) and niche partitioning of the respectivebears (Bocherens et al., 2011a). It is, however, not yet clear whichplant resources were specifically used by both types of cave bears.

In the Ach valley the situation is quite different. The two cavebear lineages were not sympatric, since a genetic replacement ofU. s. spelaeus by U. ingressus in both caves, Geißenklösterle andHohle Fels, took place around 31,500 years ago (calibrated age)(Hofreiter, 2002; Hofreiter et al., 2007), with an overlap of the twotaxa of not more than 4000 years (Münzel et al., 2011). In this re-gion the genetic change was not linked to a change in diet due tothe stability of the stable isotope values of the bone collagen (13C,15N) (Münzel et al., 2011). However, preliminary oxygen isotopevalues of the bone apatite from metapodials exhibited a differentpattern between the two caves in the Ach valley (Bocherens et al.,2011b). The Hohle Fels samples had on average lower oxygen iso-topic values than the Geißenklösterle samples (Bocherens et al.,2011b). This difference might be due to the shape of these sitesused as hibernation caves by the cave bears. While Hohle Fels offersa large hall with stable summer/winter temperatures, which pro-vide ideal conditions for hibernating cave bears, Geißenklösterlehas more the character of a rockshelter. Therefore, a possibleinterpretation is that Geißenklösterle was used during warmerphases (interstadials) by hibernating cave bears and Hohle Felsduring colder phases (stadials). If this was the case, we could test ifthe dietary pattern, either in terms of items consumed or their

diversity, could be different between cave bears from both caves ifoccupations took place under different climatic conditions.

To try to answer these open questions, we chose to use thefollowing methods, namely tooth microwear and stable isotopes(13C, 18O) of tooth enamel in the same teeth, for the followingreasons:

(1) Tooth microwear directly reflects the texture of the individ-ual diet and provides a snapshot of the environment andvegetation. The formation of the microwear on the toothenamel represents the diet of the last days (last supper ef-fect) before the death of the individual.

(2) Carbon and oxygen isotopes in tooth enamel provide directinformation on diet and climatic context for the same indi-vidual than the one on which tooth wear was analyzed.However, we have to keep in mind that it corresponds to adifferent time interval in life history compared to microwear,it provides a snapshot of early life, when the tooth wasformed, instead of the last weeks of life for microwear(Fig. 1). Some variability between teeth is expected due todifferent timing in enamel formation. Therefore, we chose toanalyze always the same tooth for isotopic analysis (lowerm1) in order to provide consistent results.

4. Material and methods

4.1. Material

To study the nutritional biases of extinct cave bears referencematerial is needed with known diet gained from stable isotope

Fig. 2. Map of the regions and locations.

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Table 1Microwear results and stable isotope values on bone collagen (15N, 13C) for reference bears.

Reference bears Tooth microwear Stable isotopes on bone collagen

Species Collection Inventory# Origin/chronostratigraphy(all dates are uncalibrated)

Teeth NP DP NS DS LP Npp XS SWS Isotopesample#

d13C d15N Diet

Ursus maritimus(Polar bear)

NWA Bä-E10 Banks Island, NWT,Canada, 1970 AD

m1 inf 8.5 53.1 25.0 156.3 0 0 1 1 n.a. n.a. n.a. Carnivore e marine

Ursus maritimus NWA UR 3 Banks Island, NWT,Canada, 1970 AD

m1 inf 9.0 56.3 27.0 168.8 0 0 1 0 TUB-92 �16.0 21.3 Carnivore e marine

Ursus maritimus SZ Mamm 372 Arktis, 1878 AD m1 inf 8.0 50.0 26.5 165.6 0 0 1 0 n.a. n.a. n.a. Carnivore e marineUrsus maritimus SZ Mamm 606 Arktis m1 inf 9.0 56.3 27.5 171.9 0 0 1 1 n.a. n.a. n.a. Carnivore e marineUrsus arctos

(Brown bear)GemeindeAlland

AT1 Allander Tropfsteinhöhle,8920 � 80 BPb

m1 inf 9.0 56.3 27.0 168.8 0 0 1 1 AT1a �19.6 5.1 Herbivore

Ursus arctos horribilis(Brown bear, Grizzly)

NWA UR 7 Central Alaska, 1984 AD m1 inf 29.0 181.3 12.5 78.1 0 0 1 1 TUB-94 �20.1 2.8 Herbivore

Ursus arctos NWA UR 1 Dangstetten, Romancamp, 15e9 BC

m1 inf 27.0 168.8 9.0 56.3 0 0 1 1 DNG-20 �20.5 3.0 Herbivore

Ursus arctos SMNS Nr. 4815.1 Schussenquelle (SW-Germany),hunting camp, 12 ka BP

m1 inf 7.5 46.9 18.5 115.6 0 0 1 1 SCH-8 �20.6 3.3 Herbivore

Ursus arctos NHMW H83-47-1 Bärenkammer, 1466 � 22 BP m1 inf 10.5 65.6 18.5 115.6 0 0 1 0 UAA-27 �20.6 3.7 HerbivoreUrsus arctos NHMW H86-178-1 Bärenloch, 1985 � 35 BP m1 infa 14.8 92.2 23.5 146.9 0 0 1 1 UAA-21 �20.9 3.4 HerbivoreUrsus arctos NHMW H77-18-2 Brunnenschacht, 2877 � 23 BP m1 inf 14.5 90.6 25.0 156.3 0 0 1 2 UAA-26 �20.0 2.9 HerbivoreUrsus arctos NHMW H76-20-1 Wildes Loch, Grebenzen,

1210 � 30 BPbm1 inf 7.0 43.8 30.5 190.6 0 0 1 1 UAA-4a �20.1 2.6 Herbivore

Ursus arctos NHMW H89-27-1 Schoberbergschacht, 821 � 21 BP m2 inf 21.0 131.3 22.5 140.6 0 0 1 1 UAA-23 �21.2 0.3 HerbivoreUrsus arctos SZ Mamm 1837 Pailgam, Kaschmir, 1904 AD m1 inf 28.0 175.0 13.0 81.3 0 0 1 1 n.a. n.a. n.a. ?Ursus arctos SZ Mamm 192 Europa, Nordasien m1 inf 27.0 168.8 12.0 75.0 0 0 1 1 n.a. n.a. n.a. ?Ursus americanus

(American Black bear)SZ Mamm 200 Nordamerika m1 inf 10.5 65.6 16.0 100.0 0 0 0 2 n.a. n.a. n.a. ?

Ursus americanus SZ Mamm 604 Nordamerika, 1899 AD m1 inf 8.5 53.1 18.5 115.6 0 0 0 2 n.a. n.a. n.a. ?Ursus americanus SZ Mamm 607 Labrador, 1855 AD m1 inf 10.5 65.6 17.5 109.4 0 0 0 1 n.a. n.a. n.a. ?Ailuropoda melanoleuca

(Giant panda)SMNS Nr. 2298 Tibet, Sezchuan, 1900 AD m1 inf 12.0 75.0 25.0 156.3 0 0 1 0 SEA-17 �23.3 0.6 Herbivore

Ursus arctos e pre-LGMUrsus arctos NHMW P�redmostí P�redmostí, Moravia,

Tschechien, 27e25 ka BPm1em2 inf 7.5 46.9 30.5 190.6 0 0 1 0 n.a. n.a. n.a. Carnivorec

Ursus arctos NWA HF 69/1588 Hohle Fels (Swabian Jura),40e35 ka BP

M1 sup 12.0 75.0 26.5 165.6 0 0 0 1 n.a. n.a. n.a. Carnivorec

Ursus arctos NWA HF 55/1400 Hohle Fels (Swabian Jura),40e35 ka BP

m1 inf 10.5 65.6 27.5 171.9 1 0 1 1 n.a. n.a. n.a. Carnivorec

NHMW ¼ Natural History Museum Vienna (n ¼ 7).NWA ¼ Reference collection of the Institute of the Archaeological Sciences at the University of Tübingen (n ¼ 6).SMNS ¼ Natural History Museum in Stuttgart (n ¼ 2).SZ ¼ Reference collection of the Institute of Zoology at the University of Tübingen (n ¼ 7, without isotopes).NP ¼ raw number of pits.DP ¼ density of pits.NS ¼ raw number of scratches.DS ¼ density of scratches.LP ¼ presence/absence of large pits.Npp ¼ number of puncture pits.XS ¼ presence/absence of cross scratches.SWS ¼ scratch width score: 0 ¼ fine only; 1 ¼ mix of fine and coarse; 2 ¼ coarse only.

a Mean of left and right 1st molar.b Döppes et al., 2008, Stalactite 58.c The diet was determined indirectly (see details in the text).

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values in bone collagen (15N, 13C). In addition, dental microwearwas studied for these bears.

The reference bears for this study come from four collections.Two are at the University of Tübingen, the reference collection ofthe Archaeozoology at the Department of Archaeological Sciences(NWA) with six specimens and the reference collection of theZoology (SZ) with seven. Two specimens come from the NaturalHistory Museum in Stuttgart (SMNS) and another seven from theNatural History Museum in Vienna (NHMW) (Table 1). The diet ofthe bears used as reference for tooth microwear investigations wasevaluated either from their taxonomy for species with uniform andpredictable diet, such as polar bears and giant pandas, or individ-ually using carbon and nitrogen isotopic tracking on bone collagen,for species with flexible diet, such as brown bear and Americanblack bears.

All four polar bears (Ursus maritimus) were wild animals,coming from Banks Island, NWT, Canada and from unknownarctic environments. Stable isotopes are available only from onespecimen and, as expected for a top carnivore feeding on marineresources, it delivered a very high nitrogen isotopic value. Thuswe categorized the group of polar bears as carnivorous. The groupof brown bears is the most interesting reference group for ourstudy, since brown bears have by far the largest distributionacross northern Eurasia and North America and are able to copewith a large variety of different food sources (e.g. Jacoby et al.,1999; Beckmann and Berger, 2003; Bojarska and Selva, 2011).This group includes a grizzly bear from Alaska and several Ho-locene brown bears from Austria. In addition to recent brownbears, we included specimens from archaeological sites, such asDangstetten, a Roman camp site (Roth-Rubi, 2006), and Schus-senquelle, a Magdalenian reindeer hunting camp (Schuler, 1994).Furthermore we also included a few brown bears from pre-LGMtimes, two from Hohle Fels and one from P�redmosti, in order tocover the aspect of carnivorous/omnivorous brown bears. Stableisotopes (15N, 13C) were not directly measured on the P�redmostímandibular, but thanks to earlier research on stable isotopes (15N,13C) of the bone collagen from cave bear metapodials of the Achvalley and of the Totes Gebirge, it appears that the pre-LGMbrown bears are carnivorous as long as cave bears occupied theherbivore niche, and they shifted to an omnivorous diet after theextinction of the cave bears in post-LGM times (Münzel et al.,2011; Bocherens et al., 2011a). Therefore we can categorize thepre-LGM brown bears as carnivorous and use the dental micro-wear as a reference for such a diet. A giant panda (A. melanoleuca)was included as a reference, since it is one of the extreme her-bivorous food specialists. For three specimens of American blackbear, we have microwear analysis only, and no stable isotopevalues (15N, 13C) of the bone collagen. The number of referencebears with information on stable isotopes as well as on micro-wear is not very large, but they provide important landmarks offood specialisation amongst omnivorous ursine bears, which waslacking until now.

For the cave bear, we focused on only one type of tooth, thelower first molar (m1). This is important for the isotopic analysisof carbonate in tooth enamel, as the formation time of toothenamel depends on the formation time and seasonal fluctuationscould have an influence on the isotopic results. Nevertheless, forthe microwear analysis we had to include some upper M1 andlower m2 resp. m3 to see whether there are differences betweenthe respective molars. However, this was not the case, since thedental microwear pattern on the tooth crown was not differentfor different types of molar. This test was necessary for reasons ofcomparison with the pre-LGM reference brown bear teeth, sincethey are scarce and it was not always possible to analyse a lowerfirst molar.

4.2. Methods

4.2.1. Tooth microwear analysisMicrowear features of dental enamel were examined using a

stereomicroscope on high-resolution epoxy casts of teeth followingthe cleansing, molding, casting, and examination protocol devel-oped by Solounias and Semprebon (2002) and Semprebon et al.(2004).

The occlusal surface of each specimen was cleaned usingacetone and then 96% alcohol. The surface was molded using high-resolution silicone (vinylpolysiloxane) and casts were created usingtransparent epoxy resin. All specimens molded were carefullyscreened under the stereomicroscope. Those with badly preservedenamel or taphonomic defects (features with unusual morphologyand size, or fresh features made during the collecting process orduring storage) were removed from the analysis following Kinget al. (1999).

Casts were observed with a Zeiss Stemi 2000C stereomicroscopeat 35� magnification, using the refractive properties of the trans-parent cast to reveal microfeatures on the enamel. Photomicro-graphs were taken at 35 times magnification using a digital cameraInvenio 5SII and the DeltaPix InSight software in extended focusmode. In carnivores, microwear scars (i.e., elongated scratches androunded pits) are usually observed on the slicing or the grindingfacets (Goillot et al., 2009). However, in our study we decided tofocus our analyses on the unworn surfaces of enamel to get samplesizes as large as possible (Fig. 3). The microwear present on theunworn surfaces is not as directly related to slicing or grinding as onthe wear facets, but it is commonly used on primates and was re-ported to have significant implications for the study of feedingtraits (Ungar and Teaford, 1996). Primates and bears have multi-cusped premolars and molars and tooth morphology and belongto the omnivorous class. In this sense it is adequate to also useunworn surfaces without facets resp. unworn surfaces of the toothin the case of bears.

We observed and quantifiedmicrowear features in a square areaof 0.16 mm2 using an ocular reticule. We used the classification offeatures defined by Solounias and Semprebon (2002) andSemprebon et al. (2004) as follows:

(1) Pits are microwear scars that are circular or sub-circular inoutline and thus have approximately similar widths andlengths, while scratches are elongated microfeatures whichare not merely longer than they are wide, but they havestraight, parallel sides. Scratches and pits were quantified intwo areas near the protoconid of the m1 (Fig. 3), averaged,and converted to densities, i.e., number of features per mm2

(density of pits ‘DP’, and density of scratches ‘DS’, see Tables 1and 2).

Fig. 3. Lower 1st molar of a cave bear showing ‘worn’ and ‘unworn surfaces’. Toothmicrowear was analysed at 35� on both facets.

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(2) Large pits are deeper, less refractive (always dark), generallyat least about twice the diameter of small pits, and often haveless regular outlines than do small pits.

(3) Cross scratches are oriented somewhat at 90� to the majorityof scratches observed on tooth enamel.

(4) Scratch textures were assessed as being either fine (i.e.,narrow scratches that appear relatively shallow and have lowrefractivity) or coarse (i.e., wide scratches that are alsorelatively deep but have high refractivity (relatively shiny)),or a mixture per tooth surface. The scratch width score (SWS)is obtained by giving a score of ‘0’ to teeth with predomi-nantly fine scratches per tooth surface, ‘1’ to those with amixture of fine and coarse types of textures, and ‘2’ to thosewith predominantly coarse scratches. Individual scores for asample are then averaged to get the scratch width score.Fig. 4 gives an example of the microwear features and theirclassification on a bison tooth.

4.2.2. Isotopic analysis: collagen preparation and isotopic analysisSmall bone fragments sawn from the bones of referencemodern

and ancient bears were ultrasonicated in acetone and water, withan additional step in chloroform/methanol (2:1) for modern bones(Dufour et al., 1999), and rinsed with distilled water, dried andcrushed to a powder of 0.7mm grain size. The collagenwas purifiedaccording to a well established protocol (Bocherens et al., 1997).The elemental and isotopic measurements were performed at theGeochemical unit of the Geoscience Faculty at the University ofTübingen (Germany), using an elemental analyser NC 2500 con-nected to a Thermo Quest Delta þ XL mass spectrometer. Thereliability of the isotopic signatures of the collagen extracts ofancient bears was addressed using their chemical composition (%C,%N, and C/N ratios). These values must be similar to those ofcollagen extracted from fresh bone to be considered reliable forisotopic measurements and radiocarbon dating. Several studieshave shown that collagen with atomic C/N ratios lower than 2.9 orhigher than 3.6 is altered or contaminated, and should be dis-carded, as well as extracts with %N <5% (DeNiro, 1985; Ambrose,1990).

The d13C and d18O measurements of the carbonate fraction oftooth enamel were performed at the Department of Geosciences(University Tübingen, Germany). Around 10 mg of tooth enamelfrom lower first molars were sampled using a diamond-tipped drill

bit and a Dremmel� rotating tool. Prior to these analyses, powderswere chemically pre-treated with 2% NaOCl solution, followed by a0.1 M Ca-acetate acetic acid buffer solution (Bocherens et al., 1996).Samples were analyzed at 70 �C using a ThermoFinnigan GasbenchII on a Finnigan Delta Plus XL CFIRMS at the University of Tübingenfor d13C and d18O values of the carbonate fraction of bioapatite.

The isotopic ratios are expressed using the “d” (delta) value inparts per mil (&) as follows: dEX ¼ (Rsample/Rreference � 1) � 1000&where X is C, N or O, E is the atomic number 13,15 or 18, and R is theisotopic ratios 13C/12C, 15N/14N and 18O/16O, respectively. Deltavalues are reported relative to international reference standards: aVienna Pee Dee Belemnite (V-PDB) for carbon, atmospheric nitro-gen (AIR) for nitrogen and Vienna Standard Mean Ocean Water (V-SMOW) for O. Measurements were normalized to d13C values ofUSGS24 (d13C ¼ �16.00&) and to d15N values of IAEA 305A(d15N ¼ 39.80&). Analytical error was estimated to be �0.1& ford13C values, �0.2& for d15N values, and �0.15& for d18OCO3

valuesbased on replicate within-run analyses of lab standards.

5. Results

5.1. Tooth microwear of reference dataset on bears with known diet

The tooth microwear patterns of the reference bears are veryvariable due to their different feeding behaviour. In Fig. 5, thedensity of pits (DP) is plotted against the density of scratches (DS)for the reference dataset. The differences of texture and plasticity ofthe food are reflected in this plot. The distribution of the DP and DSseems to follow a co-variation trend, with samples having eitherhigh DP (�150) coeval with low DS (�90), or low DP (�100) coevalwith high DS (�100), with only one sample in between but stillintermediate for both parameters (Fig. 5). Interestingly, herbivo-rous brown bears show the whole range of diversity in relation ofpits to scratches, namely high number of pits combined with a lownumber of scratches and vice versa. In contrast to herbivorousbears, the carnivorous ones, such as polar bear and the pre-LGMbrown bears, are grouped closely together with high DS and rela-tively low DP. However, high scratch density is also found inextreme plant-feeders such as giant panda feeding on bamboo,which is situated quite close to the carnivorous bears, as well as twoother herbivorous ancient brown bears from Wildes Loch andAllander Tropfsteinhöhle (Döppes and Pacher, 2008). Both brownbears provided low d15N values, lower than coeval herbivores suchas red deer (Döppes et al., 2008), meaning that they belonged to the

Fig. 4. Photomicrograph of a bison (B. bison) tooth enamel at 35 times magnificationshowing the different types of microwear features. Scale bar ¼ 0.2 mm.

Fig. 5. Microwear traces for lower m1 of reference bears: density of pits (DP) plottedagainst density of scratches (DS).

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herbivore guild, but probably fed on abrasive food as do grazerssuch as giant panda.

To conclude, high density in scratches means either carnivores,such as polar bear (Fig. 6A) or pre-LGM carnivorous brown bears, orgrazers, such as giant panda or some herbivorous brown bears.High density in pits and low in scratches seems to be occupied onlyby herbivorous bears, as documented by their low d15N values. Thisshows that the dental microwear alone is not sufficient to make anunambiguous interpretation of the diet, especially for bears. Dentalmicrowear needs to be combined with an isotopic approach toseparate herbivorous from carnivorous bears, but it providesvaluable information on the quality of ingested food. The micro-wear pattern with high density of pits but low density of scratcheswas found only in herbivorous bears (Fig. 6B), and it seems that atleast this pattern can be interpreted in dietary terms.

5.2. Tooth microwear of Ramesch and Gamssulzen cave bears

The microwear features of the cave bears from the two caves ofRamesch and Gamssulzen separate very clearly as two distinctgroups (Fig. 7a), Ramesch yielded a large variability in the density ofpits in contrast to Gamssulzen, which is more variable in scratches(Fig. 8A and B).

Comparing the DP/DS values of the cave bears from Rameschand Gamssulzen with the reference bears (see landmarks for thegrizzly and the polar bear included in Fig. 7a), both groups, U. s.eremus and U. ingressus are clearly beyond the carnivorous/grazergroup of the reference bears with the Gamssulzen bears being

closer to it. To support the significance of the difference betweenthe latermentioned groups, we ran aWilcoxon/KruskaleWallis testcomparing the Gamssulzen bears (n ¼ 9) with the reference groupof carnivorous/grazer bears (Table 1) including the four polar bears,the pre-LGM brown bears (n¼ 3) and the grazing bears, namely thepanda bear and two brown bears (Allander cave and Wildes Loch).The difference between these two groups is obvious on the plot-box graphs (not shown here) for both DP and DS. The p-value is0.0003, much lower than the statistically significant threshold ofp ¼ 0.001 supporting the conclusion that these cave bears bothlived on vegetation with little contribution of grass. Within thisherbivorous niche, there is a wide range of feeding specialisationspossible and this is also visible for the reference bears (Fig. 5) aswell as for the cave bears (Fig. 7a,b).

5.3. Tooth microwear of Hohle Fels and Geißenklösterle cave bears

The tooth microwear results of the Ach valley caves (Fig. 7b andFig. 8C and D) differ considerably from the Totes Gebirge, as themicrowear data from both caves overlap greatly. However, even ifno groups based on microwear were visible, we recognized a dif-ference in the variability of the microwear features between thetwo cave sites (Fig. 7b). For Hohle Fels, the density of pits (m ¼ 135;sd ¼ 20.5) and scratches (m ¼ 82.9; sd ¼ 13.8) was less variable,while Geißenklösterle cave bears showed a larger range and vari-ability for both variables (DP: m ¼ 137; sd ¼ 25.7; DS: m ¼ 80.5;sd ¼ 24.2). As observed for the cave bears of the Totes Gebirge, themicrowear pattern of pits and scratches of the Swabian Jura

Fig. 6. Photomicrographs of extant bear tooth enamel at 35 times magnification. A ¼ Grizzly, Ursus arctos from Alaska (NWA UR7); B ¼ Polar bear, Ursus maritimus (NWA UR3).Scale bars ¼ 0.2 mm.

Fig. 7. aþb: Microwear traces for lower m1 of cave bears: density of pits (DP) plotted against density of scratches (DS) with reference points for Grizzly and Polar bear, a) Ramesch(RK) and Gamssulzen (GS) caves (Totes Gebirge), b) Hohle Fels (HF) and Geißenklösterle (GK) (Swabian Jura).

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samples is beyond the carnivore/grazer pattern of the referencebears, showing that the cave bears from the Ach valley belonged toherbivorous bears with negligible grass consumption (see ‘land-marks’ for the grizzly and the polar bear included in Fig. 7b).

5.4. Oxygen and carbon isotopy of the cave bear teeth

Before attempting palaeobiological interpretations, we must besure about the reliability of the measured isotopic values. Even iftooth enamel is recognized as extremely stable and typically retainsits isotopic signature formillions of years (e.g. Lee-Thorp andvanderMerwe,1991; Bocherenset al.,1996;Kochet al.,1997; Bocherens andDrucker, 2014), we cannot completely rule out diagenetic alterationin some cases. Therefore, the reliability of the d13C and d18O values oftooth enamel was evaluated using carbonate content (2.9e4.1%carbonate for 189 modern tooth enamel samples measured in thesame conditions), comparing it to the values measured in modernenamel and testing for possible co-variations between isotopicvalues and carbonate content that could indicate contamination oralteration. In the present case, possible diagenetic alteration wasdetected in some samples with lower than usual carbonate content(2.1e2.5% carbonate, Table 2), since they exhibited anomalous d13Cor d18O values compared to the samples with carbonate contentwithin the range of enamel from fresh teeth (Table 2). Therefore, weconservatively discarded from further discussion six enamel sam-ples (two from Hohle Fels and four from Geissenklösterle) thatyielded carbonate contents lower than 2.5%. Another two samplesfrom Hohle Fels did not deliver values.

In Fig. 9 the d18O values are plotted against the d13C values to seewhether a climatic signal could be recognized. For the Ach valleycaves (Fig. 9b) a difference in oxygen isotopes, but not in carbon

isotopes was observed between the two caves. The Geißenklösterlesamples revealed less negative oxygen isotopic values than theHohle Fels samples, meaning that the Geißenklösterle cave bearsfaced warmer climatic conditions than bears hibernating in HohleFels. Interestingly, the two clusters of d18O values do overlap tosome extent. There is just one sample from Geißenklösterle with ad18O value close to �9& in contrast to the pattern observed inHohle Fels, where about half of the samples have d18O values lowerthan �9&. The samples from Hohle Fels exhibit a larger range ofvariation for the d18O values and therefore, there are several sam-ples of Hohle Fels in the Geißenklösterle cluster.

For the Totes Gebirge, no obvious distinction of the oxygenvalues of tooth enamel related to the cave sites is visible (Fig. 9a).Samples from both caves cover the same d18O values, but a segre-gation in d13C values is visible, pointing towards nutritional dif-ferences. If this is the case, then we have to look for a possible co-variation with microwear features.

5.5. Microwear and carbon resp. Oxygen isotopy of teeth

In Fig. 10b the density of pits is plotted against the d13C values.For the Ach valley there is a larger diversity in the density of pits inGeißenklösterle than for Hohle Fels, a pattern that repeats the re-sults of Fig. 7b. This was also tested using the density of scratches,but there seems to be no difference in diet. Hohle Fels and Gei-ßenklösterle cover the same d13C values independently if plottedagainst the density of pits or scratches.

In the Totes Gebirge, the situation is different (Fig. 10a). Thegroup of the Ramesch samples can be subdivided in two subgroups,one with a high density of pits (DP), and one with low density ofpits. This contrasts with the samples from the Gamssulzen cave

Fig. 8. Photomicrographs of fossil bear tooth enamel at 35 times magnification. A ¼ Ursus spelaeus eremus from Ramesch cave (199e1); B ¼ Ursus ingressus from Gamssulzen cave(GS 685e1); C ¼ Ursus spelaeus from Hohle Fels (HF 29e1690); D ¼ Ursus spelaeus from Geißenklösterle (GK 79e457). Scale bars ¼ 0.2 mm.

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Table 2Microwear results and stable isotope values of tooth enamel (13C, 18O) for cave bears from Hohle Fels and Geißenklösterle (Swabian Jura) and Ramesch and Gamssulzen caves (Totes Gebirge).

Tooth microwear Stable isotopes

Site Square Find# Geol.horizon

Archaeol.horizon

Technocomplex Tooth Side NP DP NS DS LP Npp XS SWS %CaCO3 d13C d18OPDB d18OSMOW

Hohle Fels (HF), Ursus spelaeus (sensu lato)HF (n ¼ 24) 29 1485 PV Unstratified m1 inf dex 15.5 96.9 13.0 81.3 0 0 1 1 2.37 Not includedHF 57 637 3b IIb Gravettian m1 inf dex 26.0 162.5 11.5 71.9 0 0 1 1 2.75 �16.70 �10.30 20.24HF 79 2153 3d/5c IIc Gravettian m1 inf dex 24.5 153.1 16.5 103.1 0 0 1 1 2.78 �16.70 �9.02 21.57HF 66 812 3c IIc Gravettian m1 inf dex 22.5 140.6 10.5 65.6 0 0 1 0 2.52 �16.76 �8.41 22.20HF 79 2400 6 III Aurignacian m1 inf dex 22.0 137.5 17.0 106.3 1 0 1 1 2.76 �17.24 �9.62 20.95HF 78 2276 6a IIIa Aurignacian m1 inf dex 23.0 143.8 16.0 100.0 0 0 1 1 3.30 �16.65 �8.82 21.77HF 69 1717 6 IV Aurignacian m1 inf dex 21.0 131.3 15.0 93.8 1 0 1 1 3.53 �16.78 �7.88 22.74HF 24 1051 7 III? Aurignacian m1 inf dex 24.5 153.1 15.5 96.9 0 0 1 1 No valuesHF 87 334 3b IIb Gravettian m1 inf sin 18.0 112.5 13.0 81.3 0 0 1 1 2.86 �16.12 �8.74 21.85HF 66 399 3bl IIb Gravettian m1 inf dex 24.0 150.0 10.0 62.5 0 0 1 1 2.97 �16.92 �9.51 21.05HF 65 532 3bl IIb Gravettian m1 inf dex 17.0 106.3 11.0 68.8 0 0 1 1 No valuesHF 88 339 3b IIb Gravettian m1 inf dex 24.5 153.1 15.0 93.8 0 0 1 1 3.67 �16.47 �8.57 22.02HF 79 2505 3c IIc Gravettian m1 inf dex 24.0 150.0 13.0 81.3 0 0 1 0 3.33 �16.70 �9.46 21.11HF 68 1231 3c IIc Gravettian m1 inf dex 25.0 156.3 13.5 84.4 0 0 1 1 2.78 �17.06 �9.09 21.49HF 30 333 3C IIC Gravettian m1 inf dex 16.5 103.1 14.5 90.6 0 0 1 1 3.09 �16.75 �9.20 21.38HF 68 1881 3c IIc Gravettian m1 inf dex 14.0 87.5 14.5 90.6 0 0 1 1 2.46 Not includedHF 66 2874 3cf IIc Gravettian m1 inf dex 21.5 134.4 13.0 81.3 0 0 1 1 2.58 �17.17 �9.19 21.38HF 78 1677 3cf IIc Gravettian m1 inf dex 22.0 137.5 14.5 90.6 0 0 1 1 2.78 �17.11 �8.96 21.62HF 65 1370 6a IIIa Aurignacian m1 inf dex 22.5 140.6 13.0 81.3 0 0 1 1 3.27 �16.94 �7.49 23.14HF 29 1690 7 IV Aurignacian m1 inf dex 23.5 146.9 16.0 100.0 0 0 1 0 3.31 �16.86 �7.96 22.66HF 98 1362 7 IV Aurignacian m1 inf dex 25.0 156.3 11.5 71.9 0 0 1 1 2.98 �17.21 �7.48 23.15HF 79 2900 9 VI Middle Pal m1 inf dex 21.0 131.3 10.5 65.6 0 0 1 1 2.62 �17.16 �7.57 23.06HF 87 1770 9 VI Middle Pal m1 inf dex 19.5 121.9 9.5 59.4 0 0 1 0 3.14 �17.46 �8.12 22.49HF 78 2690 10 VII Middle Pal m1 inf dex 21.5 134.4 11.0 68.8 0 0 1 1 3.04 �17.29 �7.34 23.29

M 21.6 135.0 13.3 82.9 M L16.90 L8.64 21.96SD/CV 3.3/0.2 20.5/0.2 2.2/0.2 13.8/0.2 SD 0.32 0.83 0.86

Geißenklösterle (GK), Ursus spelaeus (sensu lato)GK (n ¼ 26) 100 105 4 Ir Holocene/Magdalenian m1 inf dex 18.5 115.6 14.5 90.6 1 0 1 1 2.49 Not includedGK 59 145 11 IIn upper Aurignacian m1 inf dex 21.5 134.4 14.0 87.5 0 0 1 0 4.03 �16.62 �7.51 23.12GK 110 419 12 IIa upper Aurignacian m1 inf sin 19.5 121.9 12.5 78.1 0 0 0 1 3.30 �17.32 �7.13 23.51GK 47 306 15 III lower Aurignacian m1 inf dex 28.5 178.1 9.5 59.4 1 0 1 0 2.63 �17.16 �8.43 22.17GK 46 851 18 IV Middle Pal m1 inf dex 19.0 118.8 8.5 53.1 1 0 1 1 2.68 �17.42 �8.55 22.04GK 78 1510 18b IV Middle Pal m1 inf dex 25.0 156.3 18.0 112.5 0 0 1 0 2.89 �16.82 �6.99 23.66GK 56 1429 19 V Middle Pal m1 inf dex 19.0 118.8 16.5 103.1 0 0 1 1 3.70 �17.20 �7.88 22.74GK 56 1656 22 8 Middle Pal m1 inf dex 22.0 137.5 13.5 84.4 0 0 1 1 2.37 Not includedGK 110 139 5a Is Gravettian m1 inf sin 16.5 103.1 8.0 50.0 0 0 1 0 2.76 �16.64 �7.28 23.35GK 89 145 6 Is Gravettian m1 inf dex 22.0 137.5 11.5 71.9 0 0 1 0 3.53 �17.10 �7.28 23.35GK 98 149 6 Is Gravettian m1 inf sin 23.5 146.9 18.5 115.6 0 0 1 1 2.92 �16.26 �8.93 21.65GK 79 457 7 It Gravettian m1 inf sin 15.5 96.9 12.0 75.0 0 0 1 1 3.12 �16.36 �7.21 23.42GK 33 38 8 Ia Gravettian m1 inf sin 25.0 156.3 11.0 68.8 0 0 1 1 2.94 �17.26 �7.85 22.77GK 98 274 8 Ia Gravettian m1 inf sin 20.5 128.1 22.0 137.5 0 0 1 1 2.34 Not includedGK 73 118 D8-12 Ia Gravettian m1 inf dex 19.0 118.8 12.0 75.0 1 0 1 1 2.12 Not includedGK 68 1009 15 III lower Aurignacian m1 inf dex 28.5 178.1 5.5 34.4 0 0 1 1 3.42 �17.68 �8.30 22.30GK 66 825 15 III lower Aurignacian m1 inf dex 20.0 125.0 13.5 84.4 0 0 1 1 3.35 �17.56 �7.76 22.86GK 78 1310 15 III lower Aurignacian m1 inf dex 18.0 112.5 6.0 37.5 0 0 1 1 2.60 �17.79 �7.64 22.98GK 36 528 15 III lower Aurignacian m1 inf sin 22.5 140.6 17.5 109.4 0 0 1 1 2.89 �16.49 �7.53 23.10GK 120 784 15 III lower Aurignacian m1 inf sin 25.5 159.4 12.5 78.1 0 0 1 1 3.05 �16.79 �7.56 23.07GK 36 552 16 III lower Aurignacian m1 inf sin 21.5 134.4 15.0 93.8 0 0 1 1 3.07 �16.67 �7.32 23.31

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Table 2 (continued )

Tooth microwear Stable isotopes

Site Square Find# Geol.horizon

Archaeol.horizon

Technocomplex Tooth Side NP DP NS DS LP Npp XS SWS %CaCO3 d13C d18OPDB d18OSMOW

GK 46 827 17 IIIc lower Aurignacian/Middle Pal m1 inf dex 26.5 165.6 13.5 84.4 0 0 1 0 2.70 �17.14 �8.00 22.61GK 68 871 17 IIIc lower Aurignacian/Middle Pal m1 inf dex 23.5 146.9 16.5 103.1 0 0 1 1 2.80 �17.56 �8.43 22.17GK 56 1405 18a IV Middle Pal m1 inf dex 18.5 115.6 12.0 75.0 0 0 1 1 2.83 �16.74 �7.01 23.63GK 67 2534 20 VI Middle Pal m1 inf dex 16.5 103.1 11.0 68.8 1 0 1 1 3.85 �16.64 �6.48 24.18GK 56 1585 21 VII Middle Pal m1 inf dex 32.0 200.0 10.0 62.5 0 0 1 1 3.39 �16.46 �7.00 23.65

M 21.8 136.5 12.9 80.5 M L16.99 L7.64 22.98SD/CV 4.1/0.2 25.7/0.2 3.9/0.3 24.2/0.3 SD 0.45 0.61 0.63

Tooth microwear Stable isotopes

Site Square Inv.# Find# Exc. area Depth (cm) Tooth Side NP DP NS DS LP Npp XS SWS %CaCO3 d13C d18OPDB d18OSMOW

Ramesch-Knochenhöhle (RK), Ursus s. eremusRK D6 252 1 190e200 m1 inf dex 12.5 78.1 10.0 62.5 0 0 1 1 3.63 �18.20 �7.69 22.94RK D7 98 1 grey layer m1 inf sin 39.5 246.9 5.5 34.4 1 1 1 1 3.83 �17.04 �8.17 22.44RK D4 124 1 30e40 m1 inf dex 10.5 65.6 9.0 56.3 0 0 1 1 2.75 �17.11 �8.62 21.97RK D3 83 2 30e40 m1 inf dex 42.0 262.5 7.0 43.8 1 0 1 1 2.61 �16.65 �8.55 22.05RK Z11 276 1 80e90 m1 inf 17.0 106.3 7.5 46.9 0 0 1 1 2.90 �17.16 �9.72 20.84RK U17 264 1 200e210 m1 inf dex 16.0 100.0 6.0 37.5 0 0 1 1 2.90 �17.57 �9.19 21.39RK B1 116 1 30e40 m1 inf dex 35.5 221.9 11.5 71.9 0 0 1 1 3.24 �17.44 �7.81 22.81RK Z11 199 1 30e40 m1 inf dex 31.0 193.8 5.0 31.3 0 0 1 1 3.50 �17.70 �6.87 23.78RK U16 596 2 280e290 m1 inf sin 14.5 90.6 9.5 59.4 0 0 1 1 3.40 �18.14 �7.13 23.51RK D4 123 1 50e60 m1 inf dex 23.0 143.8 7.0 43.8 0 0 0 1 3.51 �17.94 �6.43 24.23

M 24.2 150.9 7.8 48.8 M L17.50 L8.02 22.60SD 11.9 74.1 2.1 13.3 SD 0.51 1.04 1.07CV 0.5 0.5 0.3 0.3

Gamssulzen (GS), Ursus ingressusGS Cleaning surface 455 4 3 Surface-30 m1 inf sin 21.5 134.4 13.5 84.4 0 0 1 1 3.41 �16.15 �7.35 23.28GS Q1 57 2 2 150e160 m1 inf 23.0 143.8 15.0 93.8 0 0 1 1 2.75 �16.20 �8.61 21.98GS surface 26 5 2 m1 inf dex 21.5 134.4 19.5 121.9 0 0 1 1 3.11 �16.65 �9.19 21.39GS F5 603 1 1 150e155 m1 inf sin 23.0 143.8 16.0 100.0 1 4 1 2 2.96 �15.83 �8.09 22.52GS E6 685 1 1 180e185 m1 inf dex 22.0 137.5 21.5 134.4 0 0 1 1 3.00 �16.64 �7.29 23.34GS F8 131 5 1 150e160 m1 inf dex 26.5 165.6 19.0 118.8 0 0 1 1 2.81 �16.64 �8.34 22.26GS surface, below detritus 7 2 2 m1 inf sin No values 3.18 �16.65 �9.96 20.60GS surface, below detritus 7 3 2 m1 inf dex 22.5 140.6 17.5 109.4 0 0 1 1 2.71 �17.18 �8.02 22.60GS E6 708 e 1 205e232 m1 inf 25.5 159.4 15.5 96.9 0 0 1 1 3.21 �15.55 �8.79 21.80GS E6 708 4 1 205e232 m1 inf sin 22.5 140.6 14.0 87.5 0 0 1 1 3.12 �16.00 �8.46 22.14

M 23.1 144.4 16.8 105.2 M L16.35 L8.41 22.19SD 1.7 10.9 2.7 17.0 SD 0.49 0.80 0.83CV 0.1 0.1 0.2 0.2

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where all samples more or less have the same density of pits (DP).In the following graph (Fig. 11a) these subgroups of high and lowDPs in Ramesch were plotted against d18O and surprisingly, thesamples from each group have a linear correlation among eachother and both correlations are following parallel slopes (Fig. 11b).This segregation within the same environment and feeding groundcould be due to gender, but this idea needs further support by alarger sample size and by sexing of the molars. To test this hy-pothesis, we plotted length and width of the sampled lower 1stmolars on the background of all measured 1st molars fromRamesch and Gamssulzen. However, the variability in morphologyand size of themolars is quite large and does not provide any sexualdimorphic pattern. Unfortunately, the cave bear materials from theAch valley and from the Totes Gebirge do not provide mandibleswith canines and carnassials to sex the specimens as Baryshnikovet al. (2003) did. Nevertheless, sexual segregation of the feedingground still is an option to explain these pairwise subgroups inRamesch and Gamssulzen respectively.

Fig.12a shows a combination of density of scratches (DS) plottedagainst d13C. For the Ach valley, there is a difference in variability ofDS between Hohle Fels and Geißenklösterle. For the cave bearsfrom Totes Gebirge, an interesting pattern occurs. The plot showstwo groups of differences in scratches (DS) for Gamssulzen cave,which are correlatedwith different diet due to different d13C values.The two subgroups do not overlap, either in DS or in carbon isotopevalues. This is in contrast to Ramesch, where the two subgroups ofDP do not co-variate with d13C. Plotting these two subgroups of DSin Gamssulzen according to their oxygen and carbon isotope valuesdoes not show any difference in oxygen isotopes, suggesting thatthese groups do not correlate with temperature changes, but ratherthat they had different diets (Fig. 12b).

6. Discussion

At the beginning of this article we raised the question, if geneticdifferences in the cave bear species were related to behavioraldifferences, and if climatic factors may have influenced the feedingand hibernating behavior of cave bears from the Ach valley. Toanswer these questions, we combined in the present studydifferent approaches, namely tooth microwear and stable isotopeson the same specimens, which results were combined to the pre-vious palaeogenetic and isotopic results obtained on the same cavebear assemblages.

Morphological differences between the cave bears of theneighboring caves Ramesch (small bears ‘Hochalpine Kleinform’)and Gamssulzen (large bears) were discussed since they werediscovered (Ehrenberg, 1929; Rabeder, 1995; Rabeder andHofreiter, 2004; Rabeder et al., 2004). This morphological di-versity was recently supported by genetic diversity. Especially forthese two caves, the genetic distance of the two haplogroups andtheir stability in the same cave (Hofreiter et al., 2004), made themsuggesting a species status. In the caves of the Totes Gebirge, notonly the genetic distinction but also the results on stable isotopesof carbon and nitrogen are very different (Bocherens et al., 2011a),supporting the idea of distinct lifeways of the two bears in thearea where they roaming and where they fed. In the presentstudy, it was found that the microwear features of the cave bearsfrom the two caves Ramesch and Gamssulzen separate veryclearly as two distinct groups (Fig. 7a), thus supporting furtherthis ecological separation of the two cave bear lineages in the twoseparate caves. This is quite remarkable, as these molars arecompletely independent samples from the bone samples analyzedfor bone collagen isotopic composition, and a different approach

Fig. 9. aþb: Oxygen isotope values (d18O) plotted against carbon isotope values (d13C) for a) Totes Gebirge and b) Swabian Jura.

Fig. 10. aþb: Density of pits (DP) plotted against carbon isotope values (d13C) for a) Totes Gebirge and b) Swabian Jura.

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was used with a different time resolution during the individualslife-history.

In contrast with a previous study performed on metapodials,which suggested a niche partitioning of the two bears in Rameschand Gamssulzen depending on climatic differences (Bocherenset al., 2011a), the results on the molars obtained in the presentstudy do not confirm such a climatic difference, since the d18Ovalues of all lower first molars do not exhibit any difference be-tween both caves. In this last case, the carbonate isotopic mea-surements were performed on bones and, although the stage ofpreservation looked good enough, we cannot rule out a smallimpact of diagenetic alteration that may have changed the oxygenisotopic compositions in different ways in each cave, and led thecarbonate d18O values of bone to look slightly different.

In Totes Gebirge, differences in stable isotopes in bone collagen(Bocherens et al., 2011a), as well as in tooth enamel and dentalmicrowear investigated in the current study, do support the notionthat there was a clear niche partitioning between these two typesof herbivorous cave bears, and therefore the idea of two differentbear species with no interbreeding and different ecological habits.

In the Ach valley, the situation is different in several aspects. Asin Totes Gebirge, there are two distinct cave bear lineages. Thegenetic distance of these two haplogroups is more or less the same(Hofreiter, 2002), but in contrast toTotes Gebirge they do no exhibitrecognizable morphological differences (Münzel and Athen, 2009;Münzel et al., 2010). In the Ach valley the two cave bears did notlive sympatrically, but one lineage U. ingressus replaced the oldertaxon U. s. spelaeus around 31.5 ka cal BP with a limited co-occurrence in time (Münzel et al., 2011). According to the stableisotope results obtained on bone collagen U. ingressus also replacedU. s. spelaeus in its ecological niche (Münzel et al., 2011). Seeminglythe consumed dietary items remained the same. The carbon

isotopic results of tooth enamel of the present study support theearlier isotopic results obtained on bone collagen, as it does notshow any difference between the cave bears from both caves. Inaddition, the overlapping microwear results from the two cavesalso speaks in favor of an ecological continuity during the studiedperiod, including the genetic replacement. However, in contrast toTotes Gebirge, it is not possible in the Ach valley to evaluate if thegenetic groups had slightly different diets, as the replacement ofthe two lineages happened in both caves around 31.5 ka cal BP(Hofreiter et al., 2007) and because the morphology of the molars isnot distinct enough to separate the haplogroups when both bearsare mixed in the same layer (Münzel and Athen, 2009; Münzelet al., 2010). Only a direct palaeogenetic determination on eachanalyzed tooth would allow this genetic sorting.

However, we confirm in the present study a difference that wasfound previously in the Ach valley cave bears, which was observedin the oxygen isotopic values of bone apatite onmetapodials, whichdiffered for the two caves in the Ach valley (Bocherens et al., 2011b;Münzel et al., 2012). The Hohle Fels samples showed lower oxygenisotopic values than the Geißenklösterle samples. The presentstudy confirmed this trend with the d18O values of the enamel ofthe first lower molars: the d18O values of the Geißenklösterlesamples are clustered among the less negative values found in bothcaves, while the d18O values of the Hohle Fels samples seem morevariable and many of them are more negative than the valuesmeasured in Geißenklösterle. If we transfer this observation interms of climatically related behavior of the cave bears, it istempting to relate this phenomenon to the different shapes of thecaves. Geißenklösterle as a rockshelter was more likely visitedduring warmer phases (interstadials) by hibernating bears andHohle Fels during colder phases (stadials). Hohle Fels provides alarge cave hall with little fluctuations in temperatures, ideal for the

Fig. 12. aþb: a) shows a combination of density of scratches (DS) plotted against d13C, b) dietary subgroups in the Totes Gebirge (RK: Ramesch; GS: Gamssulzen).

Fig. 11. aþb: a) high and low DPs in Ramesch are plotted against d18O, b) with regression line.

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winter and for hibernating cave bears. Furthermore we recognizedanother interesting difference between the two regions concerningenvironment and climatic related factors. In the Ach valley thetooth microwear variability was different for the two caves. InGeißenklösterle, the variability of microwear features was largerand more diverse (Fig. 7b), it was less variable for the Hohle Felsbears. This divergence in tooth microwear features is not related todiet but to differences triggered by climate (Fig. 9b). The d13C valueswere the same for Geißenklösterle and Hohle Fels, indicatingsimilar diets, but the d18O values of Geißenklösterle were higherthan for Hohle Fels, indicating warmer conditions when cave bearshibernated in Geißenklösterle. This smaller variability in themicrowear pattern observed in the teeth of cave bears hibernatingin Hohle Fels, during colder episodes, could indicate that the di-versity of food items available before entering hibernation was notas large as during the warmer intervals. Therefore, cold spells wereprobably more stressful for cave bears in the Ach valley. They didnot change their diet, but had access to less diversity of plant food.

For the Totes Gebirge we could not recognize a co-variation oftooth microwear and climate. Nevertheless, the dietary groups aremore diversified including microwear then we assumed earlierfrom stable isotopes. In both caves, Ramesch and Gamssulzen, wedocument two groups with different dietary behavior obviously notrelated to climatic changes (Figs. 11a,b and 12b). This differentfeeding behavior could be due to gender resp. sexual segregation.Unfortunately the variability of the metrics of lower 1st molars forRamesch and Gamssulzen is too large to see any sexual dimorphismin a scatterplot. Nevertheless, the explanation of different feedingbehavior for the two sexes is very likely.

The very high density of pits (DP) for the Ramesch bears mightdepend on a larger intake of sand and grain due to their life inhigher altitudes with a lower vegetation cover. However, the twosubgroups of pit density among the Ramesch bears are peculiar.Fig. 12 shows that independently of the different temperaturesthere are two different feeding groups using different vegetationtypes. It could be related to chronology that the two feeding be-haviors are not coeval or it could be a gender related behavior.Chronological differences are difficult to demonstrate, becausethese molars are not directly dated and most of the Ramesch-stratigraphy is beyond the radiocarbon dating limits. When wechecked the depth of the finds, which also is an indirect indicator ofage, therewas no correlationwith oxygen or carbon isotopic values.Thus gender related differences in feeding behavior might be aplausible explanation for this phenomenon. Sexual dimorphism isrelatively large in bears and especially large for cave bears (Koby,1949) with differences in the extent of sexual dimorphism invarious populations (Pacher et al., 2011; Pacher and Quiles, 2013).Van Valkenburgh and Sacco (2002) relate the extent of the sexualdimorphism to the breeding system of extant carnivores.

The different density groups in scratches are also peculiar for theGamssulzen bears. Comparable to the subgroups in pits forRamesch, the subgroups for scratches do not correlate with oxygenisotopes. This distinct feeding behavior is independent of climate. Itdoes not correlate with the depth of the finds, which reflect thestratigraphy, so we might also suggest a gender dependent feedingbehavior of the Gamssulzen bears.

To conclude, the differences in the Totes Gebirge correspond todifferent adaptations to environment and feeding behavior in thishigh relief mountainous area. The feeding behavior is considerablymore diversified than in middle ranged mountains such as theSwabian Jura. The fact that two types of cave bears that aregenetically distinct but not always different morphologically andecologically raises the possibility of a case of ecological characterdisplacement. Indeed, “Character displacement is the situation inwhich, when two species of animals overlap geographically, the

differences between them are accentuated in the zone of sympatryand weakened or lost entirely in the parts of their ranges outsidethis zone” (Brown and Wilson, 1956). In the Ach valley, the twotypes of cave bears exhibited very limited morphological differ-ences and no clear ecological difference, even if they seem to havechanged their behavior according to climatic fluctuations, forinstance in the choice of cave for hibernation depending on coldintensity. In contrast, the situation in the Totes Gebirge where bothtypes of cave bears coexisted led to an ecological and morpholog-ical differentiation between these cave bears, which exploiteddifferent parts of the available resources, in other words a nichepartitioning.

7. Conclusion

The combined analysis of stable isotopes and tooth microwearon different cave bear lineages provided different palaeoecology inthe case of the Totes Gebirge, but not in case of the Swabian Jura.The present study showed that adopting different diet and differentbehavior is a matter of different adaptations to the environmentand not related to genetic groups. None of these cave bear pop-ulations, despite their differences in genetic background,morphology, chronology, climate, and life environment, providedany evidence for carnivory, but there is some variation in theirecology in response to climate fluctuations and probably tocompetition between cave bear types. This confirms the funda-mentally herbivorous adaptation of cave bears, but shows thatwithin this limitation, there was still some ecological flexibilitywhich probably made it possible for cave bears to survive throughseveral climatic fluctuations during the Late Pleistocene but morelimited than for brown bears, perhaps one of the causes of theirfinal demise.

Acknowledgements

We want to thank the colleagues from Staatliches Museum fürNaturkunde, Stuttgart, especially Dr. Doris Mörike, Thomas Rath-geber, and Dr. Reinhard Ziegler, for access to reference bear mate-rial. Martin Cotte, Bernd Steinhilber and Heinrich Taubald providedtechnical support. F. Rivals received the financial support of theresearch grant from the Ministerio de Economía y Competitividad(HAR2010-19957) and the sponsorship from the Alexander vonHumboldt Foundation.

References

Ambrose, S.H., 1990. Preparation and characterization of bone and tooth collagenfor isotopic analysis. Journal of Archaeological Science 17, 431e451.

Baryshnikov, G., 2006. Morphometric Variability of Cheek Teeth in Cave Bears, vol.98. Scientific Annals, School of Geology, pp. 81e102.

Baryshnikov, G., Germonpré, M., Sablin, M., 2003. Sexual dimorphism andmorphometric variability of cheek teeth of the cave bear (Ursus spelaeus).Belgian Journal of Zoology 133, 111e119.

Beckmann, J.P., Berger, J., 2003. Rapid ecological and behavioural changes in car-nivores: the responses of black bears (Ursus americanus) to altered food. Journalof Zoology London 261, 207e212.

Blant, M., Bocherens, H., Bochud, M., Braillard, L., Constandache, M., Jutzet, J.-M.,2010. Le gisement à faune Würmienne du Bärenloch (Préalpes fribourgeoises).Bulletin Société Fribourg, Science Naturelle, SFSN 99, 1e22.

Bocherens, H., 2002. Alimentation des ours et signatures isotopiques. In: Tillet, Th.,Binford, L. (Eds.), L’ours et l’homme, vol. 100. ERAUL, Liège, pp. 41e49.

Bocherens, H., 2004. Cave Bear Paleoecology and Stable Isotopes: Checking theRules of the Game. Cahiers scientifiques, Départ. du Rhone e Museum, Lyon,pp. 183e188. Hors série no. 2.

Bocherens, H., 2009. Dental microwear of cave bears: the missing temperate/borealvegetarian “carnivore”. Proceedings of the National Academy of Sciences U S A106, E133.

Bocherens, H., Drucker, D.G., 2013. Terrestrial teeth and bones. In: Elias, S.A. (Ed.),Encyclopedia of Quaternary Sciences, vol. 1. Elsevier, Amsterdam, pp. 304e314.

S.C. Münzel et al. / Quaternary International 339-340 (2014) 148e163 161

Author's personal copy

Bocherens, H., Argant, A., Argant, J., Billiou, D., Crégut-Bonnoure, E., Donat-Ayache, B., Philippe, M., Thinon, M., 2004. Diet reconstruction of ancient brownbears (Ursus arctos) from Mont Ventoux (France) using bone collagen stableisotope biogeochemistry (13C, 15N). Canadian Journal Zoology 82, 576e586.

Bocherens, H., Billiou, D., Patou-Mathis, M., Bonjean, D., Otte, M., Mariotti, A., 1997.Paleobiological implications of the isotopic signatures (13C, 15N) of fossilmammal collagen in Scladina Cave (Sclayn, Belgium). Quaternary Research 48,370e380.

Bocherens, H., Bonjean, D., Germonpré, M., Münzel, S., Pacher, M., Wissing, C.,2011b. Tracking climatic context of cave occupations in hibernation caves usingoxygen stable isotopic ratios (d18O) on bone phosphate. In: 17th InternationalCave Bear Symposium, Einhornhöhle, pp. 9e10.

Bocherens, H., Bridault, A., Drucker, D.G., Hofreiter, M., Münzel, S.C., Stiller, M., vander Plicht, J., 2014. The last of its kind? Radiocarbon, ancient DNA and stableisotope evidence from a late cave bear from Rochedane (France). QuaternaryInternational 339-340, 179e188.

Bocherens, H., Drucker, D., Billiou, D., Geneste, J.-M., van der Plicht, J., 2006. Bearsand humans in Chauvet Cave (Vallon-Pont-d’Arc, Ardèche, France): insightsfrom stable isotopes and radiocarbon dating of bone collagen. Journal of HumanEvolution 50, 370e376.

Bocherens, H., Fizet, M., Mariotti, A., 1990. Mise en évidence du régime alimentairevégétarien de l’ours des cavernes (Ursus spelaeus) par la biogéochimie iso-topique (13C, 15N) du collagène fossile. Comptes Rendus de l’Académie desSciences, Série II, Paris 311, 1279e1284.

Bocherens, H., Fizet, M., Mariotti, A., 1994. Diet, physiology and ecology of fossilmammals as inferred by stable carbon and nitrogen isotopes biogeochemistry:implications for Pleistocene bears. Palaeogeography, Palaeoclimatology, Palae-oecology 107, 213e225.

Bocherens, H., Koch, P.L., Mariotti, A., Geraads, D., Jaeger, J.-J., 1996. Isotopicbiogeochemistry (13C, 18O) of mammal enamel from African Pleistocene hom-inid sites: implications for the preservation of paleoclimatic isotopic signals.Palaios 11, 306e318.

Bocherens, H., Stiller, M., Hobson, K.A., Pacher, M., Rabeder, G., Burns, J.A., Tütken, T.,Hofreiter, M., 2011a. Niche partitioning between two sympatric geneticallydistinct cave bears (Ursus spelaeus and Ursus ingressus) and brown bear (Ursusarctos) from Austria: isotopic evidence from fossil bones. Quaternary Interna-tional 245, 238e248.

Bojarska, K., Selva, N., 2011. Spatial patterns in brown bear Ursus arctos diet: the roleof geographical and environmental factors. Mammal Review 42, 120e143.

Brown,W.L.,Wilson, E.O.,1956. Characterdisplacement. Systematic Zoology5, 49e65.Conard, N.J., 2009. A female figurine from the basal Aurignacian of Hohle Fels Cave

in southwestern Germany. Nature 459, 248e252.Conard, N.J., Bolus, M., 2003. Radiocarbon dating the appearance of modern

humans and timing of cultural innovations in Europe: new results and newchallenges. Journal of Human Evolution 44, 331e371.

Conard, N.J., Bolus, M., 2008. Radiocarbon dating the late Middle Paleolithic and theAurignacian of the Swabian Jura. Journal of Human Evolution 55, 886e897.

Conard, N.J., Krönneck, P., Kitagawa, K., Böhme, M., Münzel, S.C., 2013. The impor-tance of fish, fowl and small mammals in the Paleolithic diet of the SwabianJura, Southwestern Germany. In: Clark, J.M., Speth, J.D. (Eds.), Zooarchaeologyand Modern Human Origins: Human Hunting Behavior During the LaterPleistocene. Springer.

Conard, N.J., Malina, M., 2012. Neue Forschung in den Magdalénien-Schichten desHohle Fels bei Schelklingen. Archäologische Ausgrabungen Baden-Württem-berg 2011, 56e60.

Conard, N.J., Malina, M., Münzel, S.C., Seeberger, F., 2004. Eine Mammutelfenbein-flöte aus dem Aurignacien des Geißenklösterle. Neue Belege für eine musika-lische Tradition im frühen Jungpaläolithikum auf der Schwäbischen Alb.Archäologisches Korrespondenzblatt 34, 447e462.

Conard, N.J., Malina, M., Münzel, S.C., 2009. New flutes document the earliestmusical tradition in southwestern Germany. Nature 460, 737e740.

DeNiro, M.J., 1985. Postmortem preservation and alteration of in-vivo bone collagenisotope ratios in relation to palaeodietary reconstruction. Nature 317, 806e809.

Djebeljak, I., 2007. Fossil population structure and mortality of the cave bear fromthe Mokrica Cave (North Slovenia). Acta Carsologica 36 (3), 475e484.

Döppes, D., Pacher, M., 2008. Früholozäne Braunbären (Ursus arctos L.) aus nie-derösterreichischen Höhlen. Speldok 18, 43e48.

Döppes, D., Rosendahl, W., Pacher, M., Imhof, W., Dalmeri, G., Bocherens, H., 2008.Stabile Isotopenuntersuchungen an spätglazialen und holozänen Braunbär-funden aus Höhlen im Alpenraum. Stalactite 58 (2), 64e66.

Dufour, E., Bocherens, H., Mariotti, A., 1999. Palaeodietary implications of isotopicvariability in Eurasian lacustrine fish. Journal of Archaeological Science 26,627e637.

Ehrenberg, K., 1922. Über die ontogenetische Entwicklung des Höhlenbären (Diefrühen Entwicklungsstadien und Fortpflanzungsverhältnisse). Palae-ontologische Zeitschrift 5 (3), 239e245.

Ehrenberg, K., 1929. Die Ergebnisse der Ausgrabungen in der Schreiberwandhöhleam Dachstein. Palaeontologische Zeitschrift 11, 261e268.

Floss, H., 2007. L’art mobilier Aurignacien du Jura souabe et sa place dans l’artpaléolithique. Die Kleinkust des Aurignacien auf der Schwäbischen Alb und ihreStellung in der paläolithischen Kunst. In: Floss, H., Rouquerol, N. (Eds.), Leschemins de l’art Aurignacien en Europe. Colloque International, Aurignac, 16e18 Septembre 2005. Éditions Musée-forum Aurignac, France, pp. 295e316.

Fraas, O., 1872. Beiträge zur Culturgeschichte aus schwäbischen Höhlen entnom-men. Der Hohle Fels im Achthal. Archiv für Anthropologie 5, 173e213.

Goillot, C., Blondel, C., Peigné, S., 2009. Relationships between dental microwearand diet in Carnivora (Mammalia) d implications for the reconstruction of thediet of extinct taxa. Palaeogeography, Palaeoclimatology, Palaeoecology 271,13e23.

Grandal-d’Anglade, A., López-González, F., 2005. On factors that influence themorphology of the cave bear dentition and a study of the geographical variationin the Lower Carnassial. Mitteilungen der Kommission für Quartärforschungder Österreichischen Akademie der Wissenschaften 14, 41e52.

Grandal-d’Anglade, A., Pérez-Rama, M., Fernández-Mosquera, D., 2011. Diet, phys-iology and environment of the cave bear: a biogeochemical study. In:To�skan, Borut (Ed.), Fragments of Ice Age Environments. Proceedings in Honourof Ivan Turk’s Jubilee, Opera Instituti Archaeologici Sloveniae, vol. 21, pp. 111e125 (Ljubljana 2011).

Hahn, J., 1977. Nachgrabungen im Hohlen Felsen bei Schelklingen, Alb-Donau-Kreis.Archäologisches Korrespondenzblatt 7, 241e248.

Hahn, J., 1986. Kraft und Aggression. Die Botschaft der Eiszeitkunst im AurignacienSüddeutschlands? Archaeologica Venatoria 7. Institut für Urgeschichte derUniversität Tübingen.

Hahn, J., 2000. The Gravettian in Southwest Germany e environment and economy.In: Roebroeks, W., Mussi, M., Svoboda, J., Fennema, K. (Eds.), Hunters of theGolden Age. University Leiden, Netherlands, pp. 249e256.

Hahn, J., Münzel, S., 1995. Knochenflöten des Aurignacien im Geißenklösterle. In:Fundberichte aus Baden-Württemberg, vol. 20, pp. 1e12.

Higham, Th., Basell, L., Jacobi, R., Wood, R., Ramsey, Ch. B., Conard, N.J., 2012. Testingmodels for the beginnings of the Aurignacian and the advent of figurative artand music: the radiocarbon chronology of Geißenklösterle. Journal of HumanEvolution 62, 664e676.

Hille, P., Rabeder, G. (Eds.), 1986. Die Ramesch-Knochenhöhle im Toten Gebirge.Mitteilungen der Kommission für Quartärforschung der Österreichischen Aka-demie der Wissenschaften, vol. 6, pp. 1e66.

Hofreiter, M., 2002. Genetic Analyses of Late Pleistocene Cave Bear (Ursus spelaeus).Dissertation. Universität Leipzig.

Hofreiter, M., Capelli, Ch., Krings, M., Waits, L., Conard, N., Münzel, S., Rabeder, G.,Nagel, D., Paunovi�c, M., Jambresic, G., Meyer, S., Weiss, G., Pääbo, S., 2002.Ancient DNA analyses reveal high Mitochondrial DNA sequences diversity andparallel morphological evolution of late Pleistocene cave bears. MolecularBiology and Evolution 19 (8), 1244e1250.

Hofreiter, M., Münzel, S., Conard, N., Pollack, J., Slatkin, M., Weiss, G., Pääbo, S., 2007.Sudden replacement of cave bear mitochondrial DNA in the Late Pleistocene.Current Biology 17 (4), R1eR3.

Hofreiter, M., Rabeder, G., Jaenicke-Després, V., Withalm, G., Nagel, D., Paunovic, M.,Jambre�sic, G., Pääbo, S., 2004. Evidence for reproductive isolation between cavebear populations. Current Biology 14 (1), 40e43.

Horacek, M., Frischauf, Ch., Pacher, M., Rabeder, G., 2012. Stable isotopic analyses ofcave bear bones from the Conturines cave (2800 m, South Tyrol, Italy).Braunschweiger Naturkundliche Schriften 11, 47e52.

Jacoby, M.E., Hilderbrand, G.V., Servheen, C., Schwartz, C.C., Arthur, S.M.,Hanley, T.A., Robbins, C.T., Michener, R., 1999. Trophic relations of brown andblack bears in several western North American ecosystems. The Journal ofWildlife Management 63, 921e929.

King, T., Andrews, P., Boz, B., 1999. Effect of taphonomic processes on dentalmicrowear. American Journal of Physical Anthropology 108, 359e373.

Knapp, M., Rohland, N., Weinstock, J., Baryshnikov, G., Sher, A., Nagel, D.,Rabeder, G., Pinhasi, R., Schmidt, H.A., Hofreiter, M., 2009. First DNA sequencesfrom Asian cave bear fossils reveal deep divergences and complex phylogeo-graphic patterns. Molecular Ecology 18, 1225e1238.

Koby, F.-Ed., 1949. Le dimorphisme sexuel des canines d’Ursus arctos et d’U. spelaeus.Revue Suisse de Zoologie 56 (36), 675e687.

Koch, P.L., Tuross, N., Fogel, M.L., 1997. The effects of sample treatment anddiagenesis on the isotopic integrity of carbonate in biogenic hydroxalapatite.Journal of Archaeological Science 24, 417e429.

Krause, J., Unger, T., Noçon, A., Malaspinas, A.-S., Kolokotronis, S.-O., Stiller, M.,Soibelzon, L., Spriggs, H., Dear, P.H., Briggs, A.W., Bray, S.C.E., O’Brien, S.J.,Rabeder, G., Matheus, P., Cooper, A., Slatkin, M., Pääbo, S., Hofreiter, M., 2008.Mitochondrial genomes reveal an explosive radiation of extinct and extantbears near the MioceneePliocene boundary. BMC Evolutionary Biology 8, 220.

Kurtén, B., 1976. The Cave Bear Story. Life and Death of a Vanished Animal. ColumbiaUniversity Press, New York, p. 1995.

Lee-Thorp, J.A., van der Merwe, N.J., 1991. Aspects of the chemistry of modern andfossil biological apatites. Journal of Archaeological Science 18, 343e354.

Leonard, J.A., Wayne, R.K., Cooper, A., 2000. Population genetics of Ice Age brownbears. Early Edition 1999: 1e4. Proceedings of the National Academy of SciencesU S A 97, 1651e1654.

Loreille, O., Orlando, L., Patou-Mathis, M., Philippe, M., Taberlet, P., Hänni, C., 2001.Ancient DNA analysis reveals divergence of the cave bear, Ursus spelaeus, andbrown bear, Ursus arctos, lineages. Current Biology 11, 200e203.

Merceron, G., Madelaine, S., 2006. Molar microwear pattern and palaeoecology ofungulates from La Berbie (Dordogne, France): environment of Neanderthals andmodern human populations of the Middle/Upper Palaeolithic. Boreas 35, 272e278.

Münzel, S.C., Athen, K., 2009. Correlating genetic results with biometric analysis onmetapodial bones. Slovenský Kras, Acta Carsologica Slovaca 47 (Suppl.1), 47e56.

Münzel, S.C., Conard, N.J., 2004a. Change and continuity in Subsistence during themiddle and upper Paleolithic in the Ach valley of Swabia (SW-Germany). In-ternational Journal of Osteoarchaeology 14, 1e15.

S.C. Münzel et al. / Quaternary International 339-340 (2014) 148e163162

Author's personal copy

Münzel, S.C., Conard, N.J., 2004b. Cave bear hunting in the Hohle Fels, a cave site inthe Ach valley, Swabian Jura. Revue de Paléobiologie 23 (2), 877e885 (Genève2004).

Münzel, S., Langguth, K., Conard, N., Uerpmann, H.P., 2001. Höhlenbärenjagd auf derSchwäbischen Alb vor 30.000 Jahren. Archäologisches Korrespondenzblatt 31(3), 317e328.

Münzel, S.C., Rivals, F., Pacher, M., Rabeder, G., Conard, N., Bocherens, H., 2012.Behavioural ecology of Late Pleistocene bears (Ursus spelaeus and U. arctos):insight from stable isotopes and tooth microwear. In: The 18th InternationalCave Bear Symposium, Baile Herculane, Romania, 20e22 September 2012,Program e Abstracts e Field Trip, 30-31.

Münzel, S.C., Stiller, M., Hofreiter, M., Mittnik, A., Conard, N.J., Bocherens, H., 2011.Pleistocene bears in the Swabian Jura (Germany): genetic replacement,ecological displacement, extinctions and survival. In: Bocherens, H., Pacher, M.(Eds.), Late Quaternary Mammal Ecology: Insight from New Approaches. Qua-ternary International vol. 245, 225e237.

Münzel, S.C., Stiller, M., Pacher, M., Athen, K., 2010. Genetic results versusmorphological and biometrical analysis e the case of Ursus spelaeus (sensulato). In: Poster at the ICAZ Conference in Paris. SEssion 5e3 by Eva-mariaGeigl: Methodological Possibilities and Limits Used in Archaeozoology andPalaeogenetics and Their Mutual Impact on the Interpretation of the ResultsObtained by Collaborative Studies. Online published: http://alexandriaarchive.org/bonecommons/items/show/1415.

Nelson, D.E., Angerbjörn, A., Liden, K., Turk, I., 1998. Stable isotopes and themetabolism of the European cave bear. Oecologia 116, 177e181.

Orlando, L., Bonjean, D., Bocherens, H., Thenot, A., Argant, A., Otte, M., Hänni, C.,2002. Ancient DNA and the population genetics of cave bears (Ursus spelaeus)through space and time. Molecular Biology and Evolution 19 (11), 1920e1933.

Pacher, M., Quiles, J., 2013. Cave bear paleontology and paleobiology at Pestera cuOase: fossil population structure and size variability. In: Trinkaus, E.,Constantin, S., Zilhao, J. (Eds.), Life and Death at the Pestera cu Oase: a Settingfor Modern Human Emergence in Europe. Oxford Univ. Press, New York,pp. 127e146.

Pacher, M., Stuart, A.J., 2008. Extinction chronology and paleoecology of the cavebear Ursus spelaeus. Boreas 38 (2), 189e206.

Pacher, M., Bocherens, H., Döppes, D., Frischauf, C., Rabeder, G., 2012. First results ofstable isotopes from Drachenloch and Wildenmannlisloch, Swiss Alps. Braun-schweiger Naturkundliche Schriften 11, 101e110.

Pacher, M., Pohar, V., Rabeder, G. (Eds.), 2011. Ajdovska Jama. Palaeontology, Zoologyand Archaeology of Ajdovska jama near Krsko in Slovenia. Mitteilungen derKommission für Quartärforschung der Österreichischen Akademie der Wis-senschaften, vol. 20, pp. 1e112.

Peigné, St., Goillot, C., Germonpré, M., Blondel, C., Bignon, O., Merceron, G., 2009.Predormancy omnivory in European cave bears evidenced by dental microwearanalysis of Ursus spelaeus from Goyet, Belgium. Proceedings of the NationalAcademy of Sciences U S A, 1e4. Early Edition.

Pinto Llona, Ana C., 2006. Comparative Dental Microwear Analysis of Cave BearUrsus spelaeus Rosenmüller, 1794 and Brown Bear Ursus arctos Linnaeus, 1758,vol. 98. Scientific Annals, School of Geology Aristotle University of Thessaloniki(AUTH), pp. 103e108.

Pinto Llona, Ana C., 2013. Macrowear and occlusal microwear on teeth of cave bearsUrsus spelaeus and brown bears Ursus arctos: inferences concerning diet.Palaeogeography, Palaeoclimatology, Palaeoecology 370, 41e50.

Rabeder, G. (Ed.), 1995. Die Gamssulzenhöhle im Toten Gebirge. Mitteilungen derKommission für Quartärforschung der Österreichischen Akademie der Wis-senschaften, vol. 9, pp. 1e133. Wien.

Rabeder, G., Hofreiter, M., 2004. Der neue Stammbaum der Höhlenbären. Die Höhle55 (1e4), 58e77. Wien.

Rabeder, G., Debeljak, I., Hofreiter, M., Withalm, G., 2008. Morphological response ofcave bears (Ursus spelaeus group) to high-alpine habitats. Die Höhle 59 (1e4),59e70. Wien.

Rabeder, G., Hofreiter, M., Nagel, D., Withalm, G., 2004. New Taxa of Alpine CaveBears (Ursidae, Carnivora). Cahiers scientif./Dép. Rhône - Mus, Lyon, pp. 49e67.Hors série n� 2.

Rabeder, G., Nagel, D., Pacher,M., 2000. DerHöhlenbär. In: Thorbecke: SPECIES, vol. 4.Richards, M.P., Pacher, M., Stiller, M., Quilès, J., Hofreiter, M., Constantin, S., Zilhão, J.,

Trinkaus, E., 2008. Isotopic evidence for omnivory among European cave bears:Late Pleistocene Ursus spelaeus from the Pestera cu Oase. Romania Proceedingsof the National Academy of Sciences U S A 105 (2), 600e604.

Richter, D., Waiblinger, J., Rink, W.J., Wagner, G.A., 2000. Thermoluminescence,electron spin resonance and 14C-dating of the late Middle and Early Upper

Palaeolithic Site of Geissenklösterle cave in Southern Germany. Journal ofArchaeological Science 27, 71e89.

Rivals, F., Moncel, M.-H., Patou-Mathis, M., 2009. Seasonality and intra-site variationof Neanderthal occupations in the Middle Palaeolithic locality of Payre (Ardè-che, France) using dental wear analyses. Journal of Archaeological Science 36,1070e1078.

Rivals, F., Semprebon, G.M., 2011. Dietary plasticity in ungulates: insight from toothmicrowear analysis. In: Bocherens, H., Pacher, M. (Eds.), Late QuaternaryMammal Ecology: Insight from New Approaches. Quaternary International 245,279e284.

Rivals, F., Solounias, N., Mihlbachler, M.C., 2007. Evidence for geographic variation inthe diets of late Pleistocene and early Holocene Bison in North America, anddifferences from the diets of recent Bison. Quaternary Research 68, 338e346.

Robu, M., Fortin, J.K., Richards, M.P., Schwartz, Ch.C., Wynn, J.G., Robbins, Ch.T.,Trinkaus, E., 2013. Isotopic evidence for dietary flexibility among European LatePleistocene cave bears (Ursus spelaeus). Canadian Journal of Zoology 91 (4),227e234. http://dx.doi.org/10.1139/cjz-2012-0222.

Roth-Rubi, K., 2006. Dangstetten III: Das Tafelgeschirr aus dem Militärlager vonDangstetten. Konrad Theiss Verlag GmbH & Co, p. 230.

Sacco, T., Van Valkenburgh, B., 2004. Ecomorphological indicators of feedingbehavior in the bears (Carnivora: Ursidae). Journal of Zoology London 263, 41e54.

Schubert, B.W., Ungar, P.S., DeSantis, L.R.G., 2010. Carnassial microwear and dietarybehaviour in large carnivorans. Journal of Zoology London 280 (3), 257e263.

Schuler, A., 1994. Die Schussenquelle e Eine Freilandstation des Magdalénien inOberschwaben. In: Materialhefte zur Archäologie in Baden-Württemberg, vol.27. Theiss, Stuttgart.

Semprebon, G.M., Godfrey, L.R., Solounias, N., Sutherland, M.R., Jungers, W.L., 2004.Can low-magnification stereomicroscopy reveal diet? Journal of Human Evo-lution 47, 115e144.

Semprebon, G.M., Rivals, F., 2007. Was grass more prevalent in the pronghorn past?An assessment of the dietary adaptations of Miocene to recent Antilocapridae(Mammalia: Artiodactyla). Palaeogeography, Palaeoclimatology, Palaeoecology253, 332e347.

Semprebon, G.M., Rivals, F., 2010. Trends in the paleodietary habits of fossil camelsfrom the Tertiary and Quaternary of North America. Palaeogeography, Palae-oclimatology, Palaeoecology 295, 131e145.

Solounias, N., Semprebon, G., 2002. Advances in the reconstruction of ungulateecomorphology with application to early fossil equids. American MuseumNovitates 3366, 1e49.

Stiller, M., Baryshnikov, G., Bocherens, H., Grandal d’Anglade, A., Hilpert, B.,Münzel, S.C., Pinhasi, R., Rabeder, G., Rosendahl, W., Trinkaus, E., Hofreiter, M.,Knapp, M., 2010. Withering away e 25,000 years of genetic decline precededcave bear extinction. Molecular Biology and Evolution 27 (5), 975e978. http://dx.doi.org/10.1093/molbev/msq083.

Stiller, M., Molak, M., Prost, St., Rohland, N., Pacher, M., Rabeder, G., Baryshnikov, G.,Rosendahl, W., Münzel, S., Bocherens, H., Grandal-d’Anglade, A., Hilpert, B.,Germonpre, M., Stasyk, O., Pinhasi, R., Tintori, A., Ho, S.Y.W., Hofreiter, M.,Knapp, M., 2014. Mitochondrial DNA diversity and evolution of the Pleistocenecave bear complex. Quaternary International 339-340, 224e231.

Stynder, D.D., Ungar, P.S., Scott, J.R., Schubert, B.W., 2012. A dental microweartexture analysis of the MioePliocene hyaenids from Langebaanweg, South Af-rica. Acta Palaeontologica Polonica 57 (3), 485e496.

Trinkaus, E., Richards, M.P., 2013. Stable isotopes and dietary patterns of the faunalspecies from the Pestera cu Oase. In: Trinkaus, E., Constantin, S., Zilhao, J. (Eds.),Life and Death at the Pestera cu Oase: a Setting for Modern Human Emergencein Europe. Oxford Univ. Press, New York, pp. 211e226.

Ungar, P.S., Teaford, M.F., 1996. Preliminary examination of non-occlusal dentalmicrowear in anthropoids: implications for the study of fossil primates.American Journal of Physical Anthropology 100, 101e113.

Van Valkenburgh, B., Sacco, T., 2002. Sexual dimorphism, social behavior, andintrasexual competition in large Pleistocene carnivorans. Journal of VertebratePaleontology 22 (1), 164e169.

Van Valkenburgh, B., Teaford, M.F., Walker, A., 1990. Molar microwear and diet inlarge carnivores: inferences concerning diet in the sabertooth cat, Smilodonfatalis. Journal of Zoology London 222, 319e340.

Vila Taboada, M., Fernández Mosquera, D., López González, F., Grandal d’Anglade, A.,Vidal Romaní, J.R., 1999. Paleoecological Implications Inferred from Stable Iso-topic Signatures (d13C, d15N) in Bone Collagen of Ursus spelaeus ROS.-HEIN. In:Cadernos Lab. Xeolóxico de Laxe Coruña, vol. 24, pp. 73e87.

Ward, P., Kynaston, S., 1999. Bears of the World. Blandford, London UK, p. 191.

S.C. Münzel et al. / Quaternary International 339-340 (2014) 148e163 163