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Quaternary International 339-340 (2014) 209e216

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Quaternary International

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Functional morphology of the cave bear (Ursus spelaeus) cranium: athree-dimensional geometric morphometric analysis

Anneke H. van Heteren a,*, Ann MacLarnon a, Christophe Soligo b, Todd C. Rae a

aCentre for Research in Evolutionary and Environmental Anthropology, Department of Life Sciences, University of Roehampton, Holybourne Avenue, LondonSW15 4JD, United KingdombDepartment of Anthropology, University College London, Gower Street, London WC1E 6BT, United Kingdom

a r t i c l e i n f o

Article history:Available online 28 November 2013

* Corresponding author. Present address: BereicInstitut, Universität Bonn, Nußallee 8, 53115 Bonn, Ge

E-mail addresses: a.vanheteren@roehampton.ac.ubonn.de (A.H. van Heteren), a.maclarnon@roehampsoligo@ucl.ac.uk (C. Soligo), t.rae@roehampton.ac.uk (

1040-6182/$ e see front matter � 2013 Elsevier Ltd ahttp://dx.doi.org/10.1016/j.quaint.2013.10.056

a b s t r a c t

The diet of the fossil bear Ursus spelaeus has been debated extensively. U. spelaeus is thought to have beenherbivorous, but the exact composition of its diet remains unclear. To test this, the cranial morphology ofU. spelaeus was analysed using 3D geometric morphometrics and compared to that of extant Ursidae. Anapproach including the Ursus species with a varied diet (brown, and American and Asiatic black bears)allows for a more precise focus on food items that are directly relevant to the question of the diet ofU. spelaeus.

Landmarks for 3D digitisation of the cranium were chosen to reflect functional morphology relatingto the attachment of the musculus temporalis and m. masseter and general shape of the cranium.Extant Ursidae and the extinct U. spelaeus were digitised with a Microscribe G2. Generalised Pro-crustes superimposition was performed on the coordinates and allometry corrected for using pooledregression analysis. Principal Component Analysis (PCA) was conducted and interpreted with respectto diet.

PCA differentiates between genera in Ursidae and known dietary composition in extant Ursus onprincipal components 1 and 2. The position of U. spelaeus in morphospace suggests more foliage intake,relative to the extant brown bear Ursus arctos. These results suggest that the diet of U. spelaeus likelyconsisted mostly of foliage. Two cave bear specimens from Moravský Kras and Merkensteinhöhle areseparate from the others on PC2; this may be due to dietary differentiation, but the exact interpretationremains elusive, because precise geographical and temporal data are missing for the specimen fromMoravský Kras.

� 2013 Elsevier Ltd and INQUA. All rights reserved.

1. Introduction and previous research

There are eight living species of Ursidae in the world today,spread over five genera: Ursus, Helarctos, Melursus, Tremarctos andAiluropoda. In the Pleistocene of Europe, however, the now extinctcave bear (Ursus spelaeus) was also present. Its closest living rela-tives are all members of the genus Ursus and most have a mixeddiet (Table 1). Cave bears were generally confined to Europe andwestern Asia between 38� and 51� N latitude and evolved fromUrsus deningeri around the Middle-Late Pleistocene transition(Knapp et al., 2009). The distribution of U. spelaeus extended from

h Paläontologie, Steinmannrmany.k, Anneke.vanHeteren@uni-ton.ac.uk (A. MacLarnon), c.T.C. Rae).

nd INQUA. All rights reserved.

northwest Spain to the Urals and the Altai, and from Belgium andthe Harz region of Germany to Italy and Greece, and to the Crimea(Grandal d’Anglade and Vidal Romaní, 1997; Enloe et al., 2000;Baryshnikov, 2007; Kosintsev, 2007). In the large area occupiedby U. spelaeus, biotopes and vegetation likely varied widely. Therewould have been an east-west gradient from continental to coastalclimates, which is associated with flowering time of plants(Lewandowska-Sabat et al., 2012) and types of plants (Löffler,2003). There would also have been a north-south gradient, whichis associated with temperature and seasonality (Legates andWillmott, 1990) and plant response to climatic changes (Peñuelaset al., 2004). Additionally, there would have been an altitudinalgradient. As climatic conditions generally become harsher withincreasing altitude, vegetation becomes more restricted to speciesthat are resistant to these conditions (Larcher, 2003). Additionally,at high altitudes there is less biomass and primary productivity islower than at low altitudes (Garkoti and Singh, 1995; Larcher,

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2003). As a consequence, it makes sense for a large mammal, suchas a bear, to adapt its diet to the local circumstances governed bylongitude, latitude, and altitude. Research on extant bears hasshown that diet varies according to habitat (Graber and White,1983; Clevenger et al., 1992; Mattson, 1998).

Table 1Sample sizes and dietary preferences of bear species of the genus Ursus (in % volume), based on scats. Values do not sum exactly to 100% across rows, because (rounded off)values for each type of diet item are averaged over individual studies (Mattson, 1998).

Species Age Sample size (n) Foliage Roots Soft mast Hard mast Invertebrates Vertebrates

U. americanus Holocene 4 20 0 55 11 5 4U. arctos Holocene 16 27 7 42 6 6 11U. maritimus Holocene 0 1 0 1 0 0 98U. spelaeus Pleistocene 7 ? ? ? ? ? ?U. thibetanus Holocene 5 15 0 35 43 5 2

Cave bears were robust and comparable in size to the largestextant ursids (Christiansen, 1999; Stiner, 1999; Withalm, 2001;Quilès, 2002; Baryshnikov, 2007). Cave bears were sexuallydimorphic and males attained roughly twice the body mass of fe-males (Stirling and Derocher,1990; Christiansen,1999; Stiner, 1999;Tsoukala et al., 2001; Grandal d’Anglade and López-González,2005; Santi et al., 2005). In common with the extant brown bear(U. arctos), the extinct cave bear (U. spelaeus) shows high intra-specific variability, and sizes vary greatly between sexes and pop-ulations, both geographically and temporally (Grandal d’Anglade,1993; Rossi and Santi, 2001; Carlis et al., 2005; Rabeder et al.,2008; Baryshnikov and Puzachenko, 2011).

Several haplogroups have been identified (Hofreiter et al., 2002;Orlando et al., 2002, 2008; Rabeder, 2004a; Hofreiter, 2005;Rabeder et al., 2008) and it has been suggested that there are atleast four different lineages within U. spelaeus sensu lato (Rabederet al., 2004a). The first of these, U. s. ingressus, occurs in theeastern parts of the Alpine region, as well as Slovenia and Croatia(Rabeder et al., 2004b; Nagel et al., 2005), but also in the UralMountains in Russia (e.g., Knapp et al., 2009), Germany (Münzelet al., 2011), Poland (Baca et al., 2012) and the Ukraine (Nagelet al., 2005). The three other morphological forms were namedU. spelaeus ladinicus, U. spelaeus eremus, and U. spelaeus spelaeus(Rabeder and Hofreiter, 2004).U. s. ladinicuswas described from theDolomites and U. s. eremus from the Totes Gebirge. Body size in U. s.eremus and U. s. ladinicus is correlated with the altitude of thehabitat, whereas in U. s. ingressus there is a positive correlationbetween the tooth indices (e.g., P4/4 index, which indicates thecomplexity of the tooth) and the altitude of the habitat (Rabederet al., 2008). Some regional differences in cranial morphology inaddition to size and dental variation have been suggested byBaryshnikov and Puzachenko (2011).

A marked difference between cave bears and brown bears is theloss of the three anterior most premolars in the former, leaving onlyP4/4. This makes the dental formula of U. spelaeus: 3.1.1.2/3.1.1.3,although there is variation (Nagel et al., 2005). The loss of thepremolars results in a diastema, which is also observed in manyherbivores. The bite force of U. spelaeus has been calculated to besimilar to Ailuropoda melanoleuca, which has a herbivorous diet(Grandal d’Anglade, 2010). In fact, U. spelaeus is generally thoughtto have been primarily herbivorous based on the morphology of itsdentition (Kurten, 1971), limb proportions (Athen, 2006; Athen,2007) and isotopic analyses (Bocherens et al., 1994; Bocherenset al., 1997), contrary to its congeners.

This interpretation is not supported universally (Hilderbrandet al., 1996; Richards et al., 2008; Figueirido et al., 2009; Peignéet al., 2009). Microwear analyses have indicated a much largerproportion of pits on cave bear teeth than on brown bear teeth,

which has been interpreted as indicating a much more omnivorousdiet, at least in the pre-dormancy period (Pinto Llona, 2013),although the presence of pits may also indicate feeding on plants(Taylor and Hannam, 1987). Another study claiming pre-dormancyomnivory shows that the microwear of cave bears is most similar to

worm and larvae eating carnivores, which is attributed to grubbingfor roots and grit or soil ingestion (Peigné et al., 2009).

Additionally, isotopic evidence from Rumania, in the form ofhigh d15N, has been put forward to demonstrate that cave bearswere omnivorous or even carnivorous (Richards et al., 2008). Highd15N may, however, also be a consequence of urea recycling duringhibernation (Fernández Mosquera et al., 2001; Grandal d’Angladeand Fernández Mosquera, 2008). Furthermore, puncture marksfound on cave bear bones have been shown to be made by othercave bears, which may point to carnivory or bone gnawing formicronutrients (D’Errico et al., 1998). Signs of cannibalism inPestera cu Oase may also indicate either a more omnivorous dietthan is usually ascribed to cave bears or bone processing for traceelements (Quilès et al., 2006).

Analysis of cave bear morphology, stable isotopes, and toothmicrowear has, thus, not led to agreement on the precise diet ofcave bears or the possibility of intraspecific differences in diet.Previous morphological and morphometrical studies, however,have shown a strong correlation between feeding ecology andcraniodental morphology for the extant members of the familyUrsidae (Leney and Foley, 1999; Sacco and Van Valkenburgh, 2004;Christiansen, 2008). This paper builds on the two dimensionalgeometric morphometric approach of Figueirido et al. (2009) byapplying this methodology in three dimensions, following recentwork on ursid mandibulae (van Heteren et al., 2009), which willprovide an additional line of evidence regarding cave bear dietcomplementary to other lines of research. The cranium is not onlypart of the masticatory system, but is also involved with perceptionof the environment and respiration. As such, its shape is expectedto hold information about diet, but may also provide additionalinformation.

2. Materials and methods

To test between the proposed alternative diets for U. spelaeus,crania of bear species belonging to the genus Ursus with a mixeddiet (U. arctos, Ursus thibetanus and Ursus americanus) wereexamined. Bears of other generawere excluded, as well as the polarbear (Ursus maritimus), which has a diet consisting of close to 100%meat and close to 0% of anything else, making it unsuitable forlinear regression (as more than 100% or less than 0% is impossible,any relationship between variables, otherwise approximatinglinearity, will cease to be linear close to these values). Specimenswere studied in the museums listed in the appendix, which are thesame collections used by van Heteren et al. (2009). The extantmaterial consists of associated crania and mandibulae, but thefossils do not. The fossil specimens are all from older excavationsand exact stratigraphic information is limited or nonexistent.

Fig. 1. Positions of the landmarks on cranium 1912-103 belonging to Ursus arctos stored at the laboratoire d’Anatomie comparée du Muséum National d’Histoire Naturelle, Paris,France. The landmarks are described in Table 2. Top: lateral view; bottom left: ventral (left) and dorsal (right) views; bottom right: caudal view. Line drawing of cranium after Palesand Garcia (1981).

A.H. van Heteren et al. / Quaternary International 339-340 (2014) 209e216 211

One cave bear specimen comes from Merkensteinhöhle, whichis a cave locality in Austria at 16�080 E and 47�590 N and lies 441 mabove sea level. The cave bear remains come from OIS 3 (Döppesand Rabeder, 1997). Merkensteinhöhle cave bears display an in-termediate evolutionary development of the dentition, similar tothat seen in Frauenloch or Nixloch, falling midway between spec-imens with a more primitive dentition, such as those from Repo-lusthöhle or Hunas, and those with a more derived dentition, suchas the Lieglloch individuals (Rabeder, 1989; Döppes and Rabeder,1997). Pieces of Linearbandkeramik (Neolithic) have been found,but these overlie the cave bear fossils and are younger (Döppes andRabeder, 1997). There is no environmental information on thedeeper layers, which contain the cave bear fossils. The subspeciesattribution of the cave bear remains of Merkensteinhöhle has notbeen determined.

Three fossil specimens come from Drachenhöhle bei Mixnitz,which is a cave locality in Austria (47�1903300 N; 15�2205500 E; 949 mabove sea level). The older cave sediments have not been dated, butthe younger sediments contain charcoal remains, which have beendated to 25 thousand years ago (ka) (Fladerer, 1997). The culturethat produced the charcoal remains has been determined to be

Aurignacien (Fladerer, 1997). The sediments that contain cave bearremains aremost likely reworked, making it impossible to interpretthe climate and environment experienced by the bears (Fladerer,1997). The specimens display a derived, complex dentition(Fladerer, 1997) and are ascribed to U. s. ingressus (Rabeder andHofreiter, 2004; Rabeder et al., 2008).

Two specimens come from Sloup cave, which lies in thenorthern part of Moravský Kras, the Moravian Karst (Czech Re-public), and is situated in Devonian limestones at 49�2404200 N,16�44019 00E, 465 m above sea level (Diedrich, 2012). The cave sys-tem goes up to 70m deep, whereas its length exceeds 6 km (Kadlecet al., 2001). Cave sediments range in age between the Pliocene andthe Holocene (Kadlec et al., 2001). Unfortunately, most fossils werecollected and excavated without mapping (Diedrich, 2012). Mor-avský Kras itself occupies an area of approximately 85 km2 (Kadlecet al., 2001) and for one additional specimen this is themost preciseindication of locality available.

Diets of the members of the genus Ursus are given in Table 1.Values for U. arctos were calculated from Mattson (1998) as theaverage of the European, continental and Pacific coastal percent-ages weighted by the number of studies in each category.

A.H. van Heteren et al. / Quaternary International 339-340 (2014) 209e216212

Crania of adult Ursidae were digitised with a Microscribe G2desktop digitising system (Immersion Corporation, San Jose, CA).Landmarks for 3D digitisation were chosen to reflect functionalaspects of the cranium (Fig. 1 and Table 2). The maturity of eachspecimen was judged on the basis of full eruption of second upperand third lower molars, and upper and lower canines. Whereavailable, closure of the spheno-occipital suture and epiphyses wasalso used. Juveniles were not digitised and, wherever possible,equal numbers of extant adult males and females were included.When both sides of the cranium were present, the more completewas chosen for digitisation.

Table 2Landmarks used for describing cranial shape. Landmark types determined according to Bookstein (1991).

Landmark Type Description Reflects

1. 2 Opisthion: posterior edge of foramen magnum in the middle of the rim Position and size of foramen magnum2. 2 Basion: the point where the anterior margin of the foramen magnum

is intersected by the mid-sagital plane on the inner border directly opposite of opisthionPosition and size of foramen magnum

3. 2 Mastoidale: point at the inferior tip of the mastoid process Attachment area of the brachiocephalic muscle4. 1 Ventral end temporozygomatic suture: most posterior point on the ventral surface of the jugal Attachment area of the masseter5. 1 Ventral end zygomaticomaxillary suture: most anterior point on ventral surface of the jugal Attachment area of the masseter6. 2 Caudal edge of the canine socket on the palatal-facial border Position of canine7. 2 Dorsal point on the facial border of the infraorbital canal General shape of cranium and face and size

of infraorbital canal8. 1 Supraorbital process Size of temporal and size and shape of eyes9. 2 Maxillofrontal: maxilla-frontal suture on the bony margin of the orbit Size and shape of eyes10. 2 Dorsal end temporozygomatic suture: most anterior point on dorsal surface of the jugal Attachment area of the masseter11. 1 External occipital protuberance Extent of temporal and digastrics

attachment areas12. 1 Premaxillaemaxilla suture, on the palate Shape of oral cavity13. 1 Maxilla-palatine suture Shape of oral cavity

Using MorphoJ 1.05f (Klingenberg, 2008), raw 3D coordinateswere scaled, rotated and translated by Procrustes superimposition;the resulting Procrustes coordinates represent shape. To removethe effects of allometry including the allometric part of sexualdimorphism, a pooled regression analysis within species of theProcrustes coordinates onto log centroid size (LCS) was performed(Bookstein, 1991; van Heteren et al., 2009). This analysis assumesthat the allometry of the different species has the same slope, butdifferent intercepts; it has previously been shown to give goodresults (Stiner et al., 1998; Tseng and Binder, 2010). PrincipalComponent Analyses (PCA) was then conducted on the regressionresiduals.

After a Levene’s test for homogeneity of variances and a Kol-mogoroveSmirnov (KeS) test to determine normality, stepwiselinear regression was carried out in PASW Statistics 20.0.0 (SPSSInc., 2009) with the PC scores of extant members of the genusUrsus as dependent and the percentages of varying food items inthe diet (Table 1) as independent variables. The stepping methodcriterion was set to use the probability of F with entry of the vari-able at p ¼ 0.009999 and removal at p ¼ 0.010000. An independentsamples t-tests was performed on one occasion in PASW Statistics20.0.0 (SPSS Inc., 2009) to show intraspecific differences based onthe principal component scores.

3. Results

3.1. Principal Components Analysis

PCAwas performed on the regression residuals of the regressiononto LCS pooled per species for the extant specimens (n¼ 25) aloneand together with the seven U. spelaeus. Pearson’s correlation co-efficient (r) for the extant specimens of both datasets (with andwithout U. spelaeus) is 0.9688 for PC1 and highly significant(p < 0.001). This indicates that the addition of the fossils does notsubstantially alter the first dimension of shape-space.

In the PCA including fossils, PC1 explains 58.1% of the totalvariance. PC1 separates U. spelaeus from the extant bear species byvirtue of its relatively high PC1 scores (Fig. 2).

PC2 explains 9.9% of the total variance (68.0% cumulatively withPC1). U. spelaeus has PC2 scores that are comparable to other bears.There are two U. spelaeus that have visibly lower PC2 scores thanthe other five. These two come from Merkensteinhöhle and Mor-avský Kras and they are significantly different from the otherU. spelaeus on both PCs (t(5) ¼ �2.623, p ¼ 0.047 for PC1 andt(5) ¼ 11.567, p < 0.001 for PC2). It seems unlikely that the craniumfrom Moravský Kras came from Sloup; there are two other crania

from Sloup included in the analysis and both plot with the majorityof cave bears (Fig. 2).

3.2. Regression analysis

KeS tests failed to reject the null hypothesis that the data arenormally distributed for each species and a Levene’s test failed toreject the null hypothesis that all variances are homogeneous,indicating the data are likely suitable for a regression analysis. Togive an indication of what may have been the composition of thediet of U. spelaeus, a regression analysis was conducted with thePC1 scores as dependent variables, and the percentages of variousfood items as independent variables.

PC1 is highly significantly determined by the percentage of fo-liage in the diet (ANOVA, F(1,26) ¼ 44.858, p < 0.001). Substitutingthe mean PC1 score for cave bears (¼0.0755) for PC1 in theregression derived formula FOL¼(PC1þ0.182942)/0.007381 gives afoliage (FOL) content of 35%. Taking into account the 95% confi-dence intervals of the constant (standard error ¼ 0.0262) and thefactor (standard error ¼ 0.0011) gives a range between 21 and 61%.The regression analysis returned no significant food item for PC2.

3.3. Shapes

The shape of the cranium of U. spelaeus is generally most similarto U. arctos (Fig. 2) and, therefore, is compared with this species inFig. 3. U. spelaeus (green in Fig. 3) has a slightly deeper craniumdorsoventrally than U. arctos (violet in Fig. 3). Its zygomatic arch isdeeper as well. The zygomatic arches are approximately equallywide for both U. arctos and U. spelaeus. The upper part of the face ofU. spelaeus is positioned relatively caudally, whereas the canines arepositioned relatively rostrally, thereby increasing the relative lengthof the rostrum compared toU. arctos. The cave bears fromMoravskýKras and Merkensteinhöhle have a substantially different shape tothe other cave bears in the present study (Fig. 4). Most importantly,

Fig. 2. PCs 1 and 2 of the PCA on the regression residuals of the regression analysis of the Procrustes coordinates of U. arctos, U. americanus, U. thibetanus and U. spelaeus onto logcentroid size. The pie charts show the dietary composition for U. thibetanus, U. americanus and U. arctos (left to right) in percentages.

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the cranium as a whole is quite narrow and high. They also have aslightly longer maxilla (landmark 5) and the jugal bone (landmarks3, 4 and 9) is slightly less deep dorsoventrally.

3. Discussion

Within the genus Ursus, most species have a mixed diet con-sisting primarily of soft mast, hard mast and foliage (Table 1). PC1shows a gradient of increasing foliage intake with increasing PC1scores and with U. spelaeus scoring the highest values. These resultsare in line with previous analyses of cave bear mandibles (vanHeteren et al., 2009), which also indicate that U. spelaeus was notprimarily carnivorous and mostly ate foliage. The wear patterns onthe teeth confirm this, suggesting a very abrasive diet (Capasso andCaramiello, 1999). The foliage consumed by U. spelaeus could havebeen grass or other plants that grow close to the ground.

Thebrownbear is the onlyextant species that has roots in its diet,though only 7%. As such, it is not possible to obtain meaningful re-sults from a regression analysis regarding this food, because of thelimits of the comparative sample (i.e., two out of three values arezero and the third is very close to it). It is, however, possible torationalize that roots and tubers may have required similar adap-tations to foliage, as they are both fibrous. Consequently, morphol-ogies associated with larger percentages of roots in the diet than

Fig. 3. Average shapes of the crania of the seven U. spelaeus (dark green) and theirclosest living relative U. arctos (violet) from lateral (upper left), dorsal (lower left), andfrontal (right) views (compare Fig. 1). The landmarks are described in Table 2. (Forinterpretation of the references to colour in this figure legend, the reader is referred tothe web version of this article.)

brown bears may not be discernible from those associated with afoliage-rich diet. The fact that the extantmember of the genusUrsuswithmost foliage in its diet (i.e.,U. arctos) is also theonly species thatconsumes roots and tubers may suggest that U. spelaeus, which isexpected to have eaten a large amount of foliage, also included sig-nificant amounts of subterraneous plant matter in its diet, possiblyeven more than extant U. arctos. Exact percentages cannot becalculated, but the results strongly suggest thatU. spelaeushad a dietconsisting, for the most part, of fibrous vegetative matter.

Ingestion of these fibrous plants (or roots and tubers) possiblyinvolvedmasticationof grit aswell,whichmaybe responsible for thehigh degree ofwear seen in these bears (Stiner et al.,1998). However,the consumption of roots and underground tubers contaminatedwith grit has been associated with cusp-tip loss through breakageand the presence of microscopic enamel chips on the molars ofsouthern European brown bears (Pinto Llona and Andrews, 2001).The absenceof such features fromthewearpattern seen incavebearsfrom the same region has, conversely, been interpreted as evidenceagainst the consumption of grit on roots and underground tubers asthe cause of the extreme dental wear observed in many cave bears(Pinto Llona and Andrews, 2001). Recent experimental evidencepoints to crystalline quartz dust or grit as the most potent vector forenamel wear (Lucas et al., 2013), making it difficult to conceive of analternative cause for wear that involves the removal of substantial

Fig. 4. Average shapes of the crania of the two U. spelaeus from Merkensteinhöhle andMoravský Kras (light green) and the five other U. spelaeus (pink) from lateral (upperleft), dorsal (lower left), and frontal (right) views (compare Fig. 1). The landmarks aredescribed in Table 2. (For interpretation of the references to colour in this figurelegend, the reader is referred to the web version of this article.)

A.H. van Heteren et al. / Quaternary International 339-340 (2014) 209e216214

amounts of enamel. In contrast, silicates in the form of phytolithstend to acton the enamel surface bydisplacing, rather than removingmaterial (Lucas et al., 2013). It is conceivable, therefore, that theextreme dental wear in cave bears is due to the consumption of griton contaminated roots andunderground tubers in thefirst place, andthat the absence of the visible breakage patterns and microscopicenamel chips that would be expected from comparative data (PintoLlona and Andrews, 2001) is due to their masking and removalthrough the consumption of relatively large amounts of grass andtheir constituent phytoliths. A similarmechanismhasbeenproposedto explain the contradictory evidence for dietary adaptation seen insome fossil hominins (Lucas et al., 2013).

Hard mast, soft mast, and grasses have different distributionpatterns through time and space. Hard mast is more abundant inbroad-leaf forests, soft mast is relatively more abundant in conif-erous forests and roots are relatively more abundant in non-forestareas (Mattson, 1998). Similarly, it has been shown that Asiatic andAmerican black bears that live at higher elevations rely more on fo-liage, whereas those that live at lower elevations rely more on (soft)mast (Graber andWhite, 1983; Huygens et al., 2003). As the climatein the Late Pleistocene was considerably cooler than currently(Barron and Pollard, 2002), and temperature also decreases withincreasing altitude, the climatic conditions that currently prevail athigh altitudes were present at lower altitudes during the LatePleistocene. As such, it is not surprising that U. spelaeus, which livedon the mammoth steppe, included much foliage in its diet.

The cave bears from Moravský Kras and Merkensteinhöhle havea relatively long maxilla and the cranium as awhole is quite narrow.This general slenderness of the cranium could be an adaptation toselective feeding, as a slender cranium and rostrumwould be able tofeed more precisely than a broad rostrum, or eating more subter-raneous matter, such as roots and tubers, as a slender craniumwould more easily gain access to dug holes or between the roots oftrees than a broad cranium. For the aberrant Moravský Kras craniumin Fig. 2 the exact locality within the Moravský Kras is unknown,which makes it very difficult to determine what the possible causeof the difference between the bears from Moravský Kras/Merken-steinhöhle and other bears may be. It has previously been estab-lished that the mandibulae of the bears from Merkensteinhöhlehave greater mechanical advantage in their masseter-relatedmandibular morphology (van Heteren et al., 2012), although noneof these were associated with the cranium in this study. The man-dibles fromMerkensteinhöhle also have a large attachment area forthe masseter (van Heteren et al., 2012); this indicates that themasseter was a very important muscle for these bears, possibly forgrinding. Alternatively, it can also be noted that the variability of thecave bear sample excluding the Moravský Kras/Merkensteinhöhlespecimens is small compared to those of the extant species (Fig. 2)and the apparent separation of those two specimens from the rest ofthe sample may conceivably be a sampling artifact.

The results of the present and previous studies (Bocherens et al.,1994; Bocherens et al., 1997; Athen, 2006; Athen, 2007; van Heterenet al., 2009; Peigné et al., 2009; Grandal d’Anglade, 2010) haveindicated that U. spelaeus was most likely a large herbivorous bear.U. spelaeuswent extinct in theAlpine region around 27,800 cal yrs BP(Pacher and Stuart, 2008), which is probably representative of therest of Europe. The reasons behind their extinction are still unclear. Ithas been claimed that they went extinct due to masticatory malad-aptation to foliage (Capasso and Caramiello, 1999). This is based onthe fact that the most frequent pathologies are diseases of the teethand jaws. Others have, however, demonstrated that cave bears weregenerallyhealthyandcould reacholdages, oldenough tobe sufferingfrom arthrosis (Withalm, 2004). Climatic cooling and inferreddecreased vegetational productivity were possibly responsible forthe disappearance of U. spelaeus (Lascu and Puscas, 2002; Orlando

et al., 2002; Pacher and Stuart, 2008). Alternatively, human hunt-ing has also been put forward as a possible cause of extinction(Maroto et al., 2001; Johnson, 2002). A combination of climatechange and human hunting (McLellan and Reiner, 1994; Stiller et al.,2010) has also been proposed.

The results presented here demonstrate that the cranium waswell adapted to the consumption of foliage. Similar results havebeen obtained for the mandible (van Heteren et al., 2009). Thismakes it very unlikely that maladaptation to a foliage based dietcaused the extinction of U. spelaeus. Instead, the dental pathologiesshould be viewed as an indication that U. spelaeus could attainsufficient age to wear down their teeth almost completely and losesome of them without resulting in death, as indicated by alveolarresorption (Toledano et al., 2010).

4. Conclusion

The analyses presented herein indicate that U. spelaeus probablyate relatively large amounts of tough fibrous plant matter, such asfoliage and perhaps roots and tubers. As U. spelaeuswas present in avery large area with many different environmental circumstances,they show regional adaptations to the local habitats, as indicated,for example, by the bears from Moravský Kras and Merken-steinhöhle. In general, U. spelaeus appears very well adapted tomasticating tough fibrous plant matter in terms of cranial (herein)and mandibular (van Heteren et al., 2009) morphology.

Acknowledgements

The authors are grateful to S. Constantin and colleagues fororganising the symposium that generated this article. The authorsthank P. Agnelli of the Museum of Zoology and Natural History “LaSpecola”, Firenze, Italy; L. Tomsett and A. Currant of the NaturalHistory Museum, London, UK; O. Wiig of the Natural HistoryMuseum, University of Oslo, Oslo, Norway; K. Rauscher of theUniversität Wien, Vienna, Austria; U. Göhlich of the Naturhistor-isches Museum Wien, Vienna, Austria; Martina Laznickova-Galetova of the Moravian Museum, Brno, Czech Republic; and JanWagner of the Národni Museum Praha, Prague, Czech Republic forallowing access to specimens. Additionally, the authors are gratefulto two insightful anonymous reviewers for improving the quality ofthe manuscript. This research was partly funded by internal grant37913 from the University of Roehampton.

Appendix

List of specimens used in the analyses of the general shape of thecrania with twelve landmarks and their locality or location. Ursusspelaeus specimens are fossils. Abbreviations under ID:MZUF¼Museumof ZoologyandNaturalHistory “La Specola”, Firenze,Italy; BM(NH) ¼ Natural History Museum, London, UK;ZMUO ¼ Natural History Museum, University of Oslo, Oslo, Norway;UWIEN ¼ Universität Wien, Vienna, Austria;NMW ¼ Naturhistorisches Museum Wien, Vienna, Austria;MMAI ¼ Anthropos Institute, Moravian Museum, Brno, Czech Re-public; NMP ¼ Národní Museum Praha, Prague, Czech Republic. Ab-breviations under sex: f ¼ female; m ¼ male; u ¼ unsexed.CS¼ centroid size; LCS¼ log centroid size; PC¼ principal component.Footnotes indicate stratigraphical informationasgivenonthemuseumlabels. Superscript indicates the geographical classification ofMattson(1998). The first letter distinguishes between vegetation types:b¼broadleaf forest; c¼ coniferous forest; a¼ arctic/alpine.Thesecondletterdistinguished location:e¼European;c¼ continental;p¼Pacificcoastal.

ID Species Sex Locality/area of origin (altitude inmeters above sealevel)

CS LCS PC1 PC2

NMW 8275 U. americanus f Southern Alaska 275.26 5.6177 �.0363 �.0078NMW 8269 U. americanus f Arctic 265.91 5.5832 .0046 .0313NMW 63555 U. americanus u Alaskan Peninsula 259.90 5.5603 �.0244 �.0056NMW 64947 U. americanus u Glacier Mountain, Alaska 291.86 5.6763 �.0071 .0052BM(NH) 31.6.1.1 U. arctos f Caucasusbe 320.50 5.7699 �.0134 .0243BM(NH) 1010g U. arctos m Syriabc 344.58 5.8423 .0144 .0112BM(NH) 52.3.2.2 U. arctos u Syriabc 305.50 5.7220 .0191 .0267BM(NH) 87.5.5.3 U. arctos f Kashmirbc 312.96 5.7461 �.0084 �.0322BM(NH) 56.9.22.21 U. arctos m Kashmirbc 357.74 5.8798 .0288 .0141BM(NH) 87.5.15.2 U. arctos m Kashmirbc 327.75 5.7923 .0016 .0322BM(NH) 29.5.24.1 U. arctos f Lake Ladoga, Russiacc 335.69 5.8162 �.0049 .0253BM(NH) 88.2.20.18 U. arctos f Kamtschatka, Russiaap 331.18 5.8026 .0033 �.0075BM(NH) 90.8.1.3 U. arctos f Quikjock, Swedence 289.87 5.6694 �.0097 .0151BM(NH) 19.7.7.3609 U. arctos m Lake Ladoga, Russiacc 357.77 5.8799 .0001 .0058MZUF 11884 U. arctos f Abruzzo, Italybe 288.12 5.6634 .0026 .0061ZMUO 129-58 U. arctos m Ljørdalen, Norwayce 332.53 5.8067 �.0012 .0257ZMUO 3427 U. arctos m Stöa, Trysil, Norwayce 353.14 5.8669 .0072 .0266ZMUO 11847 U. arctos m Elverum, Norwayce 355.38 5.8732 .0794 �.0374MZUF 11883 U. arctos m Lombardia, Italyce 367.13 5.9057 .0659 �.0086MZUF 3584 U. arctos u Abruzzo, Italybe 350.58 5.8596 .0810 .0001NMW MS63 U. spelaeus u Merkensteinhöhle (441) 535.20 6.2826 .0649 .0017UWIEN 7 U. spelaeus u Mixnitz (949) 539.92 6.2914 .0961 �.0400UWIEN 43a U. spelaeus u Mixnitz (949) 456.97 6.1246 .0701 �.0014UWIEN 44b U. spelaeus u Mixnitz (949) 452.53 6.1149 .0713 �.0044MMAI OK4 U. spelaeus u Moravsky Kras (�490e600) 460.97 6.1333 �.0708 �.0224NMP 576B U. spelaeus u Sloup (465) 548.86 6.3078 �.0908 �.0163NMW A5545 U. spelaeus u Sloup (465) 522.57 6.2588 �.0656 �.0217BM(NH) 30.5.21.1 U. thibetanus f Monsmoo, Kashmir 268.26 5.5920 �.0740 .0016BM(NH) 31.9.21.2 U. thibetanus f Pir Panjal, Kashmir 286.84 5.6589 �.0792 �.0155BM(NH) 95.2.21.6 U. thibetanus f Amur Land, Russia 330.93 5.8019 �.0363 �.0078BM(NH) 31.9.21.4 U. thibetanus m Pir Panjal, Kashmir 322.12 5.7749 .0046 .0313BM(NH) 95.2.21.5 U. thibetanus m Amur Land, Russia 352.31 5.8645 �.0244 �.0056

a Zone 28: I. Stufe (zone 28: first layer).b 5 m von der Nordwand, 1.40 m tief (5 m from the north wall, 1.40 m deep).

A.H. van Heteren et al. / Quaternary International 339-340 (2014) 209e216 215

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