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Dietary habits of the cave bear from the Late Pleistocene in the northeast of the Iberian Peninsula
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Dietary habits of the cave bear from the Late Pleistocene in the northeast of the Iberian Peninsula Iván Ramírez-Pedrazaa,b,∗, Spyridoula Pappac,d, Ruth Blascoe, Maite Arillaa,b, Jordi Rosella,b, Ferran Millánf, Julià Marotof, Joaquim Solerf, Narcís Solerf, Florent Rivalsa,b,g a
Institut Català de Paleoecologia Humana i Evolució Social (IPHES), Campus Sescelades URV (Edifici W3), 43007, Tarragona, Spain Universitat Rovira i Virgili (URV), Àrea de Prehistoria, Avinguda de Catalunya 35, 43002, Tarragona, Spain c Department of Earth Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, United Kingdom d Department of Geography, Royal Holloway University of London, Egham, Surrey, TW20 0EX, United Kingdom e Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca 3, 09002, Burgos, Spain f Institut de Recerca Històrica, Universitat de Girona, Pl. Ferrater Mora 1, 17071, Girona, Spain g ICREA, Pg. Lluís Companys 23, 08010, Barcelona, Spain b
A R T I C LE I N FO
A B S T R A C T
Keywords: Dental microwear U. spelaeus Omnivore diet Variability
The aim of this study is to understand the feeding habits of the cave bear, Ursus spelaeus by investigating the dental microwear patterns of 106 molars from six Late Pleistocene caves in Catalonia (Spain): Ermitons Cave, Arbreda Cave, Mollet Cave, Llenes Cave, Toll Cave, and Teixoneres Cave. Dental microwear patterns of U. spelaeus were compared with a reference collection of extant ursid species. The results show an omnivorous and carnivorous diet in all sites analyzed with both intra- and inter-site pattern variability. Unlike previous studies, here dental microwear identified more carnivorous habits for the herbivorous cave bear during the days/weeks before death. More varied and higher energy items would help to cope with the hibernation period. The variability between the samples could be due to the characteristic climatic shifts of the Late Pleistocene and to the corresponding differences in the availability of resources.
1. Introduction The climatic history of the Middle and Late Pleistocene in the Iberian Peninsula is characterized by times of abrupt climatic shifts, in particular from cold to warm periods, such as deglaciations and glacial millennial-scale variations (Heinrich, 1988; Dansgaard et al., 1993; Fletcher et al., 2010). These climatic shifts had a strong influence on the distribution of ecosystems depending both on altitude and latitude and on the distribution of mammals (Stewart, 2005; Hofreiter and Stewart, 2009; Kjellström et al., 2010; Stuart and Lister, 2012). The Northeast of the Iberian Peninsula (Catalonia) is a territory of contrasts with complex orography. It is characterized by several mountain ranges of different altitudes such as the Catalan Central Depression, Catalan Transversal Range, Catalan Pre-Coastal Range, Pyrenees, and Pre-Pyrenees. The complex orography and geology of this area maintain a mosaic of landscapes that support very diverse habitats (Sánchez Goñi and D'Errico, 2005; Burjachs et al., 2012). Such an environment was also ideal for cave bears, which explains the plethora of fossil remains in this area.
∗
Despite being one of the most studied species of the Pleistocene, certain issues related to this extinct animal are still under investigation. One such issue involves feeding behaviour. Most studies employ stable isotopes. The results show homogeneity in nitrogen values among different localities similar or lower to those of contemporary strict herbivores from the same stratigraphic units. The lack of difference in the isotopic nitrogen signatures among populations in Europe suggests that the differences between soils were probably not very significant and the contribution of protein to cave bear diet was minimal in all sampled populations (Ramírez-Pedraza et al., 2019). The low nitrogen values of cave bear bone collagen show lower positions in the trophic chain similar or lower to those of values measured in pure herbivores. These values are related to a preferentially vegetarian diet (Bocherens et al., 1990, 1994; 1997, 2004; 2006, 2014; Fernández-Mosquera, 1998; Fernández-Mosquera et al., 2001; Vila Taboada et al., 2001; Bocherens, 2003, 2004; 2015, 2019; Grandal-d’Anglade et al., 2011, 2019; Münzel et al., 2011; Pérez-Rama et al., 2011; Pacher et al., 2012; Krajcarz et al., 2016; Naito et al., 2016; Martin et al., 2017; Ramírez-Pedraza et al., 2019). Conversely, samples of Ursus spelaeus from Peştera cu Oase
Corresponding author. Institut Català de Paleoecologia Humana i Evolució Social (IPHES), Campus Sescelades URV (Edifici W3), 43007, Tarragona, Spain. E-mail address: [email protected] (I. Ramírez-Pedraza).
https://doi.org/10.1016/j.quaint.2019.09.043 Received 23 July 2019; Received in revised form 20 September 2019; Accepted 24 September 2019 1040-6182/ © 2019 Elsevier Ltd and INQUA. All rights reserved.
Please cite this article as: Iván Ramírez-Pedraza, et al., Quaternary International, https://doi.org/10.1016/j.quaint.2019.09.043
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archaeological levels have been excavated, the first two correspond to Holocene levels and the third and fourth to Pleistocene levels (Fernández-García, 2014). The cave bear dental remains included in this work are from Level 4, dated to > 49,000 14C BP (Ramírez-Pedraza et al., 2019). Arbreda and Mollet Caves are located in the Palaeolithic complex known as Reclau Caves, a clustered formation located in a small talus on a somewhat karstic travertine cascade above the Serinyadell Stream at 206 m a.s.l. We analyzed the teeth of U. spelaeus belonging to Mousterian Levels I (c. 40 ka) (Bischoff et al., 1989; Maroto et al., 2012b; Wood et al., 2014) and J (71,000 ± 4,000 BP) from Arbreda Cave (Ajaja, 1994). We also analyzed one cave bear tooth from Mollet, Layer 5, dated to ca. 215 ka (Maroto et al., 2012a). Ermitons Cave is located inland of a calcareous massif in the Alta Garrotxa, belonging to the easternmost sectors of the Pre-Pyrenees at 400 m a.s.l. This location is different from the Reclau Caves; the surrounding relief is extremely rugged due to its lithology (mainly of massive limestone) and to its intensely folded and broken structure. Stratum IV, where the U. spelaeus samples analyzed come from, is dated to > 45,000 14C BP (Maroto et al., 2012b). Samples of Ursus arctos belonging to an early Neolithic level were also included in this study (Maroto, 1993). Llenes Cave is located in a Cretaceous limestone karstic complex at 750 m a.s.l. (Fig. 1). The cave is located in a vertical cliff on the right margin of the Erinyà Canyon, at 80 m above the Flamisell River. A first investigation of the cave was performed by J. Maluquer de Motes (1951) who discovered remains from the Bronze Age, Neolithic and, in the lowest level, the cave was used mainly by cave bears (U. spelaeus) and hyenas (Crocuta crocuta spelaea).
(Romania) show values of δ15N that place it at the same level as contemporary carnivores, suggesting a more carnivore diet for this bear population (Richards et al., 2008; Robu et al., 2013, 2017). Another technique that has been used to reconstruct the diet of the cave bear is dental wear analysis (Pinto Llona and Andrews, 2001; Pinto Llona, 2006; Peigné et al., 2009; Donohue et al., 2013; Pinto-Llona, 2013; Münzel et al., 2014; Jones and DeSantis, 2016; Pappa et al., 2019; Peigné and Merceron, 2019; Ramírez-Pedraza et al., 2019). This technique allows us to identify the animal's diet during the last days/ weeks before its death, thus providing a different temporal perspective. Isotopic analyses (carbon and nitrogen) on bone bulk collagen do not record the short-term diet and it is not possible to know the seasonal changes in the feeding habits of U. spelaeus from this proxy only. In the Ursidae, dental microwear began to be used relatively recently and the conclusions about the diet of cave bear are less uniform than those from stable isotopes, suggesting a more varied and less specialized diet for this ursid during the period before hibernation. The results indicate dietary plasticity that implies the capacity to adapt to the availability of resources due to factors such as seasonal changes (Peigné et al., 2009; Peigné and Merceron, 2019; Ramírez-Pedraza et al., 2019). The aim of this work is to evaluate the interpopulation variability of feeding habits of Middle and Late Pleistocene U. spelaeus populations from sites in Catalonia (Ermitons Cave, Arbreda Cave, Mollet Cave, Llenes Cave, Toll Cave, and Teixoneres Cave) by utilizing the method of dental microwear. 2. Description of the sites Teixoneres Cave and Toll Cave are located at an elevation of 760 m a.s.l. (Fig. 1). The stratigraphy of Teixoneres Cave is composed of ten archaeo-paleontological levels (Rosell et al., 2017; Rufà et al., 2016). The samples analyzed belong to Unit III that was radiocarbon dated > 51,000 14C yr BP to 44,210 cal. BP (Talamo et al., 2016). Toll Cave is located 50 m from Teixoneres Cave. In Toll cave, four
Fig. 1. Map of Catalonia showing the location of the sites involved in this study. 2
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Table 1 Dental microwear results from analyzed samples (N = number of specimens). Average data of: NFS = number of fine scratches; NCS = number of coarse scratches; NTS = total number of scratches; SWS = scratch width score; NLP = number of large pits; NSP = number of small pits; NTP = total number of pits. Taxa
Sites
N
NFS
NCS
NTS
SWS
LP
SP
NTP
U. spelaeus
Toll Teixoneres Arbreda Mollet Llenes Ermitons Ermitons
12 6 76 1 2 6 3
20.04 12.00 8.90 8.00 11.25 9.58 1.50
6.58 2.91 7.15 2.00 2.75 4.33 11.83
26.63 14.91 16.05 10.00 14.00 13.92 13.33
1.00 1.00 1.03 1.00 1.00 1.00 1.67
4.83 1.33 2.22 1.00 1.00 2.92 3.83
20.67 18.75 19.45 22.00 18.25 19.92 17.00
25.50 20.08 21.67 23.00 19.25 22.84 20.83
U. arctos
3. Materials and methods
3.15 (Hammer et al., 2001). The correspondence analysis was performed using the package ca (v. 0.70) in R (R Core Team, 2017). The script was adapted from the STHDA-statistical tools for high-throughput data analysis using fossil samples as supplementary observation (sthda. com).
3.1. Sample selection A total of 106 lower and upper first molars and upper fourth premolars with occlusal surface wear indicative of prime adults (Stiner, 1998) were selected for this work, according to Pappa et al. (2019). All specimens moulded were carefully screened under the stereomicroscope and 13 samples were discarded due to bad preservation or other taphonomical defects (King et al., 1999).
4. Results Dental microwear analysis (DMA) performed on the cave bear samples from all sites shows an average number of pits (more small pits than large pits) higher than the average number of scratches, except for in U. spelaeus from the Toll Cave, which have more scratches than pits. The general pattern shows a higher number of fine scratches than coarse scratches for all sites. Considering the scratch width score (SWS), all sites show a mixture of fine and coarse scratches (Table 1). In the case of Arbreda Cave, the individuals from the levels I and J were grouped in a single sample because three of the microwear variables do not show significant differences between the two levels; large pits (F = 0.2213; p = 0.64), small pits (F = 2.119; p = 0.1514), coarse scratches (F = 0.0103; p = 0.9167). In comparison to the extant ursid species (from the database of Pappa et al., 2019), U. spelaeus from Toll Cave has the highest number of scratches. U. spelaeus from Arbreda has the highest number of coarse scratches, similar to those of the U. arctos from Greece. However, the average number of pits from all sites fits in the range of the extant species, except for the number of pits of A. melanoleuca, which are higher compared to both extinct and extant ursids (F = 164.1; p < 0.0001). In Fig. 2, the numbers of pits and scratches for the extant ursid species with the values of the cave bear samples are compared. The extant herbivore species (A. melanoleuca) is located at the top with a higher number of pits, and the insectivore (M. ursinus), omnivore (U. thibetanus, H. malayanus, U. americanus and U. arctos), and hypercarnivore (U. maritimus) species are located in the middle. U. maritimus is furthest away from A. melanoleuca. The U. spelaeus samples are located mainly near those of U. maritimus except for the Toll Cave samples, which are located near the omnivorous ursids. In comparison with the extant bears and the other cave bears, U. arctos from Ermitons presents the highest number of coarse scratches and the lowest number of fine scratches. This ursid falls near the values of U. maritimus (Fig. 2). A Correspondence Analysis (CA) was performed to compare all the microwear variables (small pits, large pits, fine scratches, coarse scratches, and scratch width score) of the extant species and U. spelaeus from the different sites (Fig. 3). The results for the first two dimensions (Dim. 1 & 2) were used and plotted as these have a higher percentage of variance (Table 2). The CA indicates that A. melanoleuca is distant from the other species because it does not have any coarse and hypercoarse scratches and is characterized by a high number of small pits. U. arctos from Greece is in the lower right because it is the only species with a higher average of large pits than small pits and because it has the highest percentage of coarse scratches. The specimens of U. spelaeus are plotted far from the herbivorous species A. melanoleuca. U. maritimus is located in the middle on the right because it has the highest number of hypercoarse scratches. The fossil specimens from Ermitons, Teixoneres,
3.2. Microwear Enamel microwear features were observed via standard light stereomicroscopy (Zeiss Stemi 2000C) at x35 magnification on high-resolution epoxy casts of teeth, following the cleaning, molding, casting, and examination protocol developed by Solounias and Semprebon (2002) and Semprebon et al. (2004). The surface of each specimen was cleaned using acetone and then 96% ethanol. The surface was moulded using high-resolution silicone (vinylpolysiloxane) and casts were created using transparent epoxy resin. Photomicrographs were taken using a digital camera Invenio 5SII and the DeltaPix InSight software in extended focus mode that merges images acquired at various focal planes to produce a single image with a greater depth of field. A standard 0.16 mm2 ocular reticle was employed to quantify a series of microfeatures: number of small and large pits (round scars), fine and coarse scratches (elongated scars with parallel sides), and the scratch width score (a score of zero (0) was given when only fine scratches were present, one (1) when there was a mixture of fine and coarse scratches on the surface, two (2) when predominantly coarse scratches were present, and three (3) when the surface also had hypercoarse scratches). We took into account puncture pits when performing the analysis, but did not scored on any of the specimens. For our study, we focused on non-faceted and grinding enamel surfaces because they reveal the ecospace of each bear species better than other parts of the tooth surface (Ungar and Teaford, 1996; Münzel et al., 2014; Pappa, 2016; Pappa et al., 2019:Fig. 3B; Ramírez-Pedraza et al., 2019). As recommended by Solounias and Semprebon (2002) we did two reads per tooth and the two numbers were averaged to obtain a mean per individual. All specimens were analyzed by a single observer (IRP) to avoid inter-observer error. The results were compared with the reference dataset on extant bears established by Pappa et al. (2019) including the following species, plus brown bear specimens from different geographical latitudes: U. arctos (Brown bear) from Greece, central and northern Europe, N. America and Russia, Ursus maritimus (Polar bear), Ursus americanus (Black bear), Ailuropoda melanoleuca (Giant panda), Ursus thibetanus (Asian black bear), Helarctos malayanus (Sun bear), Melursus ursinus (Sloth bear) and Tremarctos ornatus (Spectacled bear). 3.3. Statistics Bivariate graphs and the ANOVA were made with the software Past 3
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Fig. 2. Bivariate plot of average number of pits of all sizes versus scratches of all sizes for bears from Catalonian sites in comparison with the extant bear database (Pappa et al., 2019). Error bars represent the standard deviation of pits and scratches.
Fig. 3. Correspondence Analysis (CA) based on five microwear variables (red triangles/NFS = number of fine scratches; NCS = number of coarse scratches; SWS = scratches width score; NSP = number of small pits; NLP = number of large pits) showing comparative distribution of microwear features of extant ursid species and the cave bears individuals from the Ermitons Cave (Er-sp) (also U. arctos – Er-ar), Arbreda Cave (A), Mollet Cave (Mo), Llenes Cave (Lle), Toll Cave (T), and Teixoneres Cave (Tx). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) 4
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short period of time near an animalʼs death that is not easily teased out of the averaged isotopic signal. Our dental microwear results make sense if we take into account the studies carried out on extant ursids (U.arctos and U. americanus) where a period of hyperphagia prior to hibernation has been documented (Christiansen, 1999; Bull et al., 2001; Rode et al., 2001). We assume that cave bear remains usually accumulate in caves as a result of deaths during hibernation (Andrews and Turner, 1992; Stiner, 1998; PintoLlona et al., 2005; Wojtal, 2007; Peigné et al., 2009; Grandal-d’Anglade et al., 2019). Dental microwear allows us to compare the diets of different individuals of U. spelaeus belonging to different archaeological sites at the same time of the year. Working with these temporal resolutions makes the comparison interesting in terms of seasonal changes. The fact that U. spelaeus from Arbreda Cave shows a more carnivorous diet than, for example, those from Toll Cave, is an example of dietary variability among populations of U. spelaeus in areas that are not very far from each other. Even so, we did not observe any relationship between the location of the different sites and the dental microwear patterns (i.e. Toll and Teixoneres caves are located in closer proximity to each other than to other sites, such as Ermitons and Arbreda). It is known that this area of the Mediterranean Basin does not have homogeneous characteristics, but is made up of a mosaic of landscapes and habitats (Sánchez Goñi and D'Errico, 2005; Burjachs et al., 2012). Consequently, the variability in dental microwear might be due to differences in the availability of resources in areas that are relatively close to each other. This variability might also be linked to paleoclimatical contexts. Despite having been found at virtually contemporary stratigraphical levels, the samples belong to a period in which abrupt climatic changes occurred in short time intervals. It is possible that cave bear populations that lived across diverse climatic conditions, and therefore had variable access to resources, were compared in this study. Therefore, they would have had a variable access to resources. Regardless, the results presented in this study are indicative of the great plasticity of this extinct species and its ability to adapt to different spaces and resources.
Table 2 Summary of Correspondence Analysis (CA). Eigenvalues, variance percentages of each dimension (Dim.).
Eigenvalues % of variance Cumulative % of variance
Dim.1
Dim.2
Dim.3
Dim.4
0.077 53.800 54.522
0.036 21.900 79.605
0.02 16.369 93.974
0.009 7.931 100
Arbreda, Mollet, and Llenes are located in the same zone, near U. maritimus, but the Toll samples appear of the extant omnivore species (U. arctos, U. thibetanus, H. malayanus and U. americanus). U. arctos from Ermitons are plotting together and do not fit into extant species, but like some samples from Arbreda they follow a trend similar to that of U. arctos from Greece and U. maritimus (Fig. 3).
5. Discussion In comparison with the extant bear database, our results show an omnivorous and carnivorous diet for the cave bears from all the sites analyzed (Toll, Teixoneres, Mollet, Llenes, Arbreda, and Ermitons). The dental microwear of Mollet and Llenes show the same pattern as the other sites, suggesting an omnivorous diet, but we cannot take them into account for the discussion due to the small sample size. Intra-population variability between specimens of the same site is observed and at the same time, an inter-population variability has also been detected. In spite of this variability and relative dispersion of the samples, the dental microwear results from U. spelaeus show a strong general pattern in relation to those of the extant ursid species. None of the fossil samples were found in the area corresponding to the extant herbivore species A. melanoleuca or in the range corresponding to the insectivore M. ursinus, U. arctos from Greece, U. arctos from northern Europe and T. ornatus. The Teixoneres and Ermitons samples are located near to the space of the omnivorous species and the hypercarnivore U. maritimus. The U. arctos from Ermitons does not fit into any of the extant species, yet it has a microwear pattern defined by many coarse scratches and very few fine scratches that are characteristic of carnivorous species (Pappa et al., 2019). The pattern of the Toll and Arbreda samples is more evident. The Toll specimens are clearly located in the ecospace of the omnivore species and the majority of the Arbreda specimens occupy the upper right part of the CA, in or around the ecospace of the hypercarnivore species U. maritimus. The analysis of dental microwear suggests that the diet of U. spelaeus in the Northeast of the Iberian Peninsula from the Late Pleistocene was omnivorous and carnivorous at least during the last days of their lives. These results contrast with the isotopic carbon and nitrogen values of these ursids analyzed in Europe (Bocherens et al., 1990, 1994; 1997, 2004; 2006, 2014; FernándezMosquera, 1998; Fernández-Mosquera et al., 2001; Vila Taboada et al., 2001; Bocherens, 2003, 2004; 2015, 2019; Grandal-d’Anglade et al., 2011, 2019; Münzel et al., 2011; Pérez-Rama et al., 2011; Pacher et al., 2012; Krajcarz et al., 2016; Naito et al., 2016; Martin et al., 2017; Ramírez-Pedraza et al., 2019). The analysis of the bone collagen of these fossils places them, with some exceptions (Hilderbrand et al., 1996; Richards et al., 2008; Robu et al., 2013, 2017), as animals with a vegetarian diet, including U. spelaeus of the Toll Cave (Ramírez-Pedraza et al., 2019). Recently, studies rejecting the presence of animal proteins in the diet of cave bear have also been developed using δ15N values of individual collagen amino acids (Naito et al., 2016). However, dental microwear does not contradict isotopic results, but provides complementary information, thus opening up the possibility of knowing an individual's diet at a specific time of their life. Dental microwear provides information on short-term diet during the life of the cave bear and this event is not necessarily reflected in the bone collagen. Thus, isotopes reflect a longer term and averaged dietary signal, whereas microwear captures a
6. Conclusion All the cave bear populations analyzed show an omnivorous-carnivorous diet at short-term scale, but there is no doubt, considering previous isotopic studies, that these ursids adopted a herbivorous diet. It is clear from this study that both short term dietary proxies like microwear as well as longer term proxies like isotopes are necessary to sufficiently address the dietary dynamics of cave bears. For future research, it would be interesting to combine different techniques to reconstruct the feeding habits of fossil bears (i.e. stable isotopes in bone and teeth, especially the nitrogen values of the collagen amino acids) emphasizing the use of complementary proxies on the same specimens. This should help solve the paradox of the diet of cave bears and also better our understanding how this large mammal survived important climatic changes until its disappearance towards the end of the Late Pleistocene. Acknowledgements This work was supported by the research grants from the Ministerio de Ciencia, Innovación y Universidades MICINN (grants HAR201676760-C3-1-P and HAR2016-76760-C3-3-P), MICINN/FEDER grants CGL2015-65387-C3-1-P and CGL2015-68604-P, and the Agència de Gestió d'Ajuts Universitaris i de Recerca (AGAUR 2017-SGR-836). The excavations are supported by the Generalitat de Catalunya projects CLT009/18/00055 at Toll and Teixoneres caves and CLT009/18/00092 at Serinyà caves. The research of J. Rosell and F. Rivals is funded by “CERCA Programme/Generalitat de Catalunya”. M. Arilla is the beneficiary of a research fellowship (FI) from AGAUR (2017FI-B-00096). We are grateful to Gina Semprebon and to an anonymous reviewer for 5
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constructive comments to improve the original manuscript.
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Sci. 106, 15390–15393. https://doi.org/10.1073/pnas.0907373106. Peigné, S., Merceron, G., 2019. Palaeoecology of cave bears as evidenced by dental wear analysis: a review of methods and recent findings. Hist. Biol. 31, 448–460. https:// doi.org/10.1080/08912963.2017.1351441. Pérez-Rama, M., Fernández-Mosquera, D., Grandal-d’Anglade, A., 2011. Recognizing growth patterns and maternal strategies in extinct species using stable isotopes: the case of the cave bear Ursus spelaeus ROSENMÜLLER. Quat. Int. 245, 302–306. https://doi.org/10.1016/j.quaint.2010.09.009. Pinto Llona, A.C., 2006. In: Comparative Dental Microwear Analysis of Cave Bears Ursus Spelaeus Rosenmüller, 1794 and Brown Bears Ursus Arctos Linnaeus, 1758, vol 98. Scientific Annals, School of Geology Aristotle University of Thessaloniki (AUTH), pp. 103–108. https://doi.org/10.13140/2.1.3064.6404. Pinto Llona, A.C., Andrews, P.J., 2001. Dental wear and grit ingestion in extant and extinct bears from Northern Spain. Cuad. do Lab. 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Dietary habits of the cave bear from the Late Pleistocene in the northeast of the Iberian Peninsula Iván Ramírez-Pedrazaa,b,∗, Spyridoula Pappac,d, Ruth Blascoe, Maite Arillaa,b, Jordi Rosella,b, Ferran Millánf, Julià Marotof, Joaquim Solerf, Narcís Solerf, Florent Rivalsa,b,g a
Institut Català de Paleoecologia Humana i Evolució Social (IPHES), Campus Sescelades URV (Edifici W3), 43007, Tarragona, Spain Universitat Rovira i Virgili (URV), Àrea de Prehistoria, Avinguda de Catalunya 35, 43002, Tarragona, Spain c Department of Earth Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, United Kingdom d Department of Geography, Royal Holloway University of London, Egham, Surrey, TW20 0EX, United Kingdom e Centro Nacional de Investigación sobre la Evolución Humana (CENIEH), Paseo Sierra de Atapuerca 3, 09002, Burgos, Spain f Institut de Recerca Històrica, Universitat de Girona, Pl. Ferrater Mora 1, 17071, Girona, Spain g ICREA, Pg. Lluís Companys 23, 08010, Barcelona, Spain b
A R T I C LE I N FO
A B S T R A C T
Keywords: Dental microwear U. spelaeus Omnivore diet Variability
The aim of this study is to understand the feeding habits of the cave bear, Ursus spelaeus by investigating the dental microwear patterns of 106 molars from six Late Pleistocene caves in Catalonia (Spain): Ermitons Cave, Arbreda Cave, Mollet Cave, Llenes Cave, Toll Cave, and Teixoneres Cave. Dental microwear patterns of U. spelaeus were compared with a reference collection of extant ursid species. The results show an omnivorous and carnivorous diet in all sites analyzed with both intra- and inter-site pattern variability. Unlike previous studies, here dental microwear identified more carnivorous habits for the herbivorous cave bear during the days/weeks before death. More varied and higher energy items would help to cope with the hibernation period. The variability between the samples could be due to the characteristic climatic shifts of the Late Pleistocene and to the corresponding differences in the availability of resources.
1. Introduction The climatic history of the Middle and Late Pleistocene in the Iberian Peninsula is characterized by times of abrupt climatic shifts, in particular from cold to warm periods, such as deglaciations and glacial millennial-scale variations (Heinrich, 1988; Dansgaard et al., 1993; Fletcher et al., 2010). These climatic shifts had a strong influence on the distribution of ecosystems depending both on altitude and latitude and on the distribution of mammals (Stewart, 2005; Hofreiter and Stewart, 2009; Kjellström et al., 2010; Stuart and Lister, 2012). The Northeast of the Iberian Peninsula (Catalonia) is a territory of contrasts with complex orography. It is characterized by several mountain ranges of different altitudes such as the Catalan Central Depression, Catalan Transversal Range, Catalan Pre-Coastal Range, Pyrenees, and Pre-Pyrenees. The complex orography and geology of this area maintain a mosaic of landscapes that support very diverse habitats (Sánchez Goñi and D'Errico, 2005; Burjachs et al., 2012). Such an environment was also ideal for cave bears, which explains the plethora of fossil remains in this area.
∗
Despite being one of the most studied species of the Pleistocene, certain issues related to this extinct animal are still under investigation. One such issue involves feeding behaviour. Most studies employ stable isotopes. The results show homogeneity in nitrogen values among different localities similar or lower to those of contemporary strict herbivores from the same stratigraphic units. The lack of difference in the isotopic nitrogen signatures among populations in Europe suggests that the differences between soils were probably not very significant and the contribution of protein to cave bear diet was minimal in all sampled populations (Ramírez-Pedraza et al., 2019). The low nitrogen values of cave bear bone collagen show lower positions in the trophic chain similar or lower to those of values measured in pure herbivores. These values are related to a preferentially vegetarian diet (Bocherens et al., 1990, 1994; 1997, 2004; 2006, 2014; Fernández-Mosquera, 1998; Fernández-Mosquera et al., 2001; Vila Taboada et al., 2001; Bocherens, 2003, 2004; 2015, 2019; Grandal-d’Anglade et al., 2011, 2019; Münzel et al., 2011; Pérez-Rama et al., 2011; Pacher et al., 2012; Krajcarz et al., 2016; Naito et al., 2016; Martin et al., 2017; Ramírez-Pedraza et al., 2019). Conversely, samples of Ursus spelaeus from Peştera cu Oase
Corresponding author. Institut Català de Paleoecologia Humana i Evolució Social (IPHES), Campus Sescelades URV (Edifici W3), 43007, Tarragona, Spain. E-mail address: [email protected] (I. Ramírez-Pedraza).
https://doi.org/10.1016/j.quaint.2019.09.043 Received 23 July 2019; Received in revised form 20 September 2019; Accepted 24 September 2019 1040-6182/ © 2019 Elsevier Ltd and INQUA. All rights reserved.
Please cite this article as: Iván Ramírez-Pedraza, et al., Quaternary International, https://doi.org/10.1016/j.quaint.2019.09.043
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archaeological levels have been excavated, the first two correspond to Holocene levels and the third and fourth to Pleistocene levels (Fernández-García, 2014). The cave bear dental remains included in this work are from Level 4, dated to > 49,000 14C BP (Ramírez-Pedraza et al., 2019). Arbreda and Mollet Caves are located in the Palaeolithic complex known as Reclau Caves, a clustered formation located in a small talus on a somewhat karstic travertine cascade above the Serinyadell Stream at 206 m a.s.l. We analyzed the teeth of U. spelaeus belonging to Mousterian Levels I (c. 40 ka) (Bischoff et al., 1989; Maroto et al., 2012b; Wood et al., 2014) and J (71,000 ± 4,000 BP) from Arbreda Cave (Ajaja, 1994). We also analyzed one cave bear tooth from Mollet, Layer 5, dated to ca. 215 ka (Maroto et al., 2012a). Ermitons Cave is located inland of a calcareous massif in the Alta Garrotxa, belonging to the easternmost sectors of the Pre-Pyrenees at 400 m a.s.l. This location is different from the Reclau Caves; the surrounding relief is extremely rugged due to its lithology (mainly of massive limestone) and to its intensely folded and broken structure. Stratum IV, where the U. spelaeus samples analyzed come from, is dated to > 45,000 14C BP (Maroto et al., 2012b). Samples of Ursus arctos belonging to an early Neolithic level were also included in this study (Maroto, 1993). Llenes Cave is located in a Cretaceous limestone karstic complex at 750 m a.s.l. (Fig. 1). The cave is located in a vertical cliff on the right margin of the Erinyà Canyon, at 80 m above the Flamisell River. A first investigation of the cave was performed by J. Maluquer de Motes (1951) who discovered remains from the Bronze Age, Neolithic and, in the lowest level, the cave was used mainly by cave bears (U. spelaeus) and hyenas (Crocuta crocuta spelaea).
(Romania) show values of δ15N that place it at the same level as contemporary carnivores, suggesting a more carnivore diet for this bear population (Richards et al., 2008; Robu et al., 2013, 2017). Another technique that has been used to reconstruct the diet of the cave bear is dental wear analysis (Pinto Llona and Andrews, 2001; Pinto Llona, 2006; Peigné et al., 2009; Donohue et al., 2013; Pinto-Llona, 2013; Münzel et al., 2014; Jones and DeSantis, 2016; Pappa et al., 2019; Peigné and Merceron, 2019; Ramírez-Pedraza et al., 2019). This technique allows us to identify the animal's diet during the last days/ weeks before its death, thus providing a different temporal perspective. Isotopic analyses (carbon and nitrogen) on bone bulk collagen do not record the short-term diet and it is not possible to know the seasonal changes in the feeding habits of U. spelaeus from this proxy only. In the Ursidae, dental microwear began to be used relatively recently and the conclusions about the diet of cave bear are less uniform than those from stable isotopes, suggesting a more varied and less specialized diet for this ursid during the period before hibernation. The results indicate dietary plasticity that implies the capacity to adapt to the availability of resources due to factors such as seasonal changes (Peigné et al., 2009; Peigné and Merceron, 2019; Ramírez-Pedraza et al., 2019). The aim of this work is to evaluate the interpopulation variability of feeding habits of Middle and Late Pleistocene U. spelaeus populations from sites in Catalonia (Ermitons Cave, Arbreda Cave, Mollet Cave, Llenes Cave, Toll Cave, and Teixoneres Cave) by utilizing the method of dental microwear. 2. Description of the sites Teixoneres Cave and Toll Cave are located at an elevation of 760 m a.s.l. (Fig. 1). The stratigraphy of Teixoneres Cave is composed of ten archaeo-paleontological levels (Rosell et al., 2017; Rufà et al., 2016). The samples analyzed belong to Unit III that was radiocarbon dated > 51,000 14C yr BP to 44,210 cal. BP (Talamo et al., 2016). Toll Cave is located 50 m from Teixoneres Cave. In Toll cave, four
Fig. 1. Map of Catalonia showing the location of the sites involved in this study. 2
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Table 1 Dental microwear results from analyzed samples (N = number of specimens). Average data of: NFS = number of fine scratches; NCS = number of coarse scratches; NTS = total number of scratches; SWS = scratch width score; NLP = number of large pits; NSP = number of small pits; NTP = total number of pits. Taxa
Sites
N
NFS
NCS
NTS
SWS
LP
SP
NTP
U. spelaeus
Toll Teixoneres Arbreda Mollet Llenes Ermitons Ermitons
12 6 76 1 2 6 3
20.04 12.00 8.90 8.00 11.25 9.58 1.50
6.58 2.91 7.15 2.00 2.75 4.33 11.83
26.63 14.91 16.05 10.00 14.00 13.92 13.33
1.00 1.00 1.03 1.00 1.00 1.00 1.67
4.83 1.33 2.22 1.00 1.00 2.92 3.83
20.67 18.75 19.45 22.00 18.25 19.92 17.00
25.50 20.08 21.67 23.00 19.25 22.84 20.83
U. arctos
3. Materials and methods
3.15 (Hammer et al., 2001). The correspondence analysis was performed using the package ca (v. 0.70) in R (R Core Team, 2017). The script was adapted from the STHDA-statistical tools for high-throughput data analysis using fossil samples as supplementary observation (sthda. com).
3.1. Sample selection A total of 106 lower and upper first molars and upper fourth premolars with occlusal surface wear indicative of prime adults (Stiner, 1998) were selected for this work, according to Pappa et al. (2019). All specimens moulded were carefully screened under the stereomicroscope and 13 samples were discarded due to bad preservation or other taphonomical defects (King et al., 1999).
4. Results Dental microwear analysis (DMA) performed on the cave bear samples from all sites shows an average number of pits (more small pits than large pits) higher than the average number of scratches, except for in U. spelaeus from the Toll Cave, which have more scratches than pits. The general pattern shows a higher number of fine scratches than coarse scratches for all sites. Considering the scratch width score (SWS), all sites show a mixture of fine and coarse scratches (Table 1). In the case of Arbreda Cave, the individuals from the levels I and J were grouped in a single sample because three of the microwear variables do not show significant differences between the two levels; large pits (F = 0.2213; p = 0.64), small pits (F = 2.119; p = 0.1514), coarse scratches (F = 0.0103; p = 0.9167). In comparison to the extant ursid species (from the database of Pappa et al., 2019), U. spelaeus from Toll Cave has the highest number of scratches. U. spelaeus from Arbreda has the highest number of coarse scratches, similar to those of the U. arctos from Greece. However, the average number of pits from all sites fits in the range of the extant species, except for the number of pits of A. melanoleuca, which are higher compared to both extinct and extant ursids (F = 164.1; p < 0.0001). In Fig. 2, the numbers of pits and scratches for the extant ursid species with the values of the cave bear samples are compared. The extant herbivore species (A. melanoleuca) is located at the top with a higher number of pits, and the insectivore (M. ursinus), omnivore (U. thibetanus, H. malayanus, U. americanus and U. arctos), and hypercarnivore (U. maritimus) species are located in the middle. U. maritimus is furthest away from A. melanoleuca. The U. spelaeus samples are located mainly near those of U. maritimus except for the Toll Cave samples, which are located near the omnivorous ursids. In comparison with the extant bears and the other cave bears, U. arctos from Ermitons presents the highest number of coarse scratches and the lowest number of fine scratches. This ursid falls near the values of U. maritimus (Fig. 2). A Correspondence Analysis (CA) was performed to compare all the microwear variables (small pits, large pits, fine scratches, coarse scratches, and scratch width score) of the extant species and U. spelaeus from the different sites (Fig. 3). The results for the first two dimensions (Dim. 1 & 2) were used and plotted as these have a higher percentage of variance (Table 2). The CA indicates that A. melanoleuca is distant from the other species because it does not have any coarse and hypercoarse scratches and is characterized by a high number of small pits. U. arctos from Greece is in the lower right because it is the only species with a higher average of large pits than small pits and because it has the highest percentage of coarse scratches. The specimens of U. spelaeus are plotted far from the herbivorous species A. melanoleuca. U. maritimus is located in the middle on the right because it has the highest number of hypercoarse scratches. The fossil specimens from Ermitons, Teixoneres,
3.2. Microwear Enamel microwear features were observed via standard light stereomicroscopy (Zeiss Stemi 2000C) at x35 magnification on high-resolution epoxy casts of teeth, following the cleaning, molding, casting, and examination protocol developed by Solounias and Semprebon (2002) and Semprebon et al. (2004). The surface of each specimen was cleaned using acetone and then 96% ethanol. The surface was moulded using high-resolution silicone (vinylpolysiloxane) and casts were created using transparent epoxy resin. Photomicrographs were taken using a digital camera Invenio 5SII and the DeltaPix InSight software in extended focus mode that merges images acquired at various focal planes to produce a single image with a greater depth of field. A standard 0.16 mm2 ocular reticle was employed to quantify a series of microfeatures: number of small and large pits (round scars), fine and coarse scratches (elongated scars with parallel sides), and the scratch width score (a score of zero (0) was given when only fine scratches were present, one (1) when there was a mixture of fine and coarse scratches on the surface, two (2) when predominantly coarse scratches were present, and three (3) when the surface also had hypercoarse scratches). We took into account puncture pits when performing the analysis, but did not scored on any of the specimens. For our study, we focused on non-faceted and grinding enamel surfaces because they reveal the ecospace of each bear species better than other parts of the tooth surface (Ungar and Teaford, 1996; Münzel et al., 2014; Pappa, 2016; Pappa et al., 2019:Fig. 3B; Ramírez-Pedraza et al., 2019). As recommended by Solounias and Semprebon (2002) we did two reads per tooth and the two numbers were averaged to obtain a mean per individual. All specimens were analyzed by a single observer (IRP) to avoid inter-observer error. The results were compared with the reference dataset on extant bears established by Pappa et al. (2019) including the following species, plus brown bear specimens from different geographical latitudes: U. arctos (Brown bear) from Greece, central and northern Europe, N. America and Russia, Ursus maritimus (Polar bear), Ursus americanus (Black bear), Ailuropoda melanoleuca (Giant panda), Ursus thibetanus (Asian black bear), Helarctos malayanus (Sun bear), Melursus ursinus (Sloth bear) and Tremarctos ornatus (Spectacled bear). 3.3. Statistics Bivariate graphs and the ANOVA were made with the software Past 3
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Fig. 2. Bivariate plot of average number of pits of all sizes versus scratches of all sizes for bears from Catalonian sites in comparison with the extant bear database (Pappa et al., 2019). Error bars represent the standard deviation of pits and scratches.
Fig. 3. Correspondence Analysis (CA) based on five microwear variables (red triangles/NFS = number of fine scratches; NCS = number of coarse scratches; SWS = scratches width score; NSP = number of small pits; NLP = number of large pits) showing comparative distribution of microwear features of extant ursid species and the cave bears individuals from the Ermitons Cave (Er-sp) (also U. arctos – Er-ar), Arbreda Cave (A), Mollet Cave (Mo), Llenes Cave (Lle), Toll Cave (T), and Teixoneres Cave (Tx). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) 4
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short period of time near an animalʼs death that is not easily teased out of the averaged isotopic signal. Our dental microwear results make sense if we take into account the studies carried out on extant ursids (U.arctos and U. americanus) where a period of hyperphagia prior to hibernation has been documented (Christiansen, 1999; Bull et al., 2001; Rode et al., 2001). We assume that cave bear remains usually accumulate in caves as a result of deaths during hibernation (Andrews and Turner, 1992; Stiner, 1998; PintoLlona et al., 2005; Wojtal, 2007; Peigné et al., 2009; Grandal-d’Anglade et al., 2019). Dental microwear allows us to compare the diets of different individuals of U. spelaeus belonging to different archaeological sites at the same time of the year. Working with these temporal resolutions makes the comparison interesting in terms of seasonal changes. The fact that U. spelaeus from Arbreda Cave shows a more carnivorous diet than, for example, those from Toll Cave, is an example of dietary variability among populations of U. spelaeus in areas that are not very far from each other. Even so, we did not observe any relationship between the location of the different sites and the dental microwear patterns (i.e. Toll and Teixoneres caves are located in closer proximity to each other than to other sites, such as Ermitons and Arbreda). It is known that this area of the Mediterranean Basin does not have homogeneous characteristics, but is made up of a mosaic of landscapes and habitats (Sánchez Goñi and D'Errico, 2005; Burjachs et al., 2012). Consequently, the variability in dental microwear might be due to differences in the availability of resources in areas that are relatively close to each other. This variability might also be linked to paleoclimatical contexts. Despite having been found at virtually contemporary stratigraphical levels, the samples belong to a period in which abrupt climatic changes occurred in short time intervals. It is possible that cave bear populations that lived across diverse climatic conditions, and therefore had variable access to resources, were compared in this study. Therefore, they would have had a variable access to resources. Regardless, the results presented in this study are indicative of the great plasticity of this extinct species and its ability to adapt to different spaces and resources.
Table 2 Summary of Correspondence Analysis (CA). Eigenvalues, variance percentages of each dimension (Dim.).
Eigenvalues % of variance Cumulative % of variance
Dim.1
Dim.2
Dim.3
Dim.4
0.077 53.800 54.522
0.036 21.900 79.605
0.02 16.369 93.974
0.009 7.931 100
Arbreda, Mollet, and Llenes are located in the same zone, near U. maritimus, but the Toll samples appear of the extant omnivore species (U. arctos, U. thibetanus, H. malayanus and U. americanus). U. arctos from Ermitons are plotting together and do not fit into extant species, but like some samples from Arbreda they follow a trend similar to that of U. arctos from Greece and U. maritimus (Fig. 3).
5. Discussion In comparison with the extant bear database, our results show an omnivorous and carnivorous diet for the cave bears from all the sites analyzed (Toll, Teixoneres, Mollet, Llenes, Arbreda, and Ermitons). The dental microwear of Mollet and Llenes show the same pattern as the other sites, suggesting an omnivorous diet, but we cannot take them into account for the discussion due to the small sample size. Intra-population variability between specimens of the same site is observed and at the same time, an inter-population variability has also been detected. In spite of this variability and relative dispersion of the samples, the dental microwear results from U. spelaeus show a strong general pattern in relation to those of the extant ursid species. None of the fossil samples were found in the area corresponding to the extant herbivore species A. melanoleuca or in the range corresponding to the insectivore M. ursinus, U. arctos from Greece, U. arctos from northern Europe and T. ornatus. The Teixoneres and Ermitons samples are located near to the space of the omnivorous species and the hypercarnivore U. maritimus. The U. arctos from Ermitons does not fit into any of the extant species, yet it has a microwear pattern defined by many coarse scratches and very few fine scratches that are characteristic of carnivorous species (Pappa et al., 2019). The pattern of the Toll and Arbreda samples is more evident. The Toll specimens are clearly located in the ecospace of the omnivore species and the majority of the Arbreda specimens occupy the upper right part of the CA, in or around the ecospace of the hypercarnivore species U. maritimus. The analysis of dental microwear suggests that the diet of U. spelaeus in the Northeast of the Iberian Peninsula from the Late Pleistocene was omnivorous and carnivorous at least during the last days of their lives. These results contrast with the isotopic carbon and nitrogen values of these ursids analyzed in Europe (Bocherens et al., 1990, 1994; 1997, 2004; 2006, 2014; FernándezMosquera, 1998; Fernández-Mosquera et al., 2001; Vila Taboada et al., 2001; Bocherens, 2003, 2004; 2015, 2019; Grandal-d’Anglade et al., 2011, 2019; Münzel et al., 2011; Pérez-Rama et al., 2011; Pacher et al., 2012; Krajcarz et al., 2016; Naito et al., 2016; Martin et al., 2017; Ramírez-Pedraza et al., 2019). The analysis of the bone collagen of these fossils places them, with some exceptions (Hilderbrand et al., 1996; Richards et al., 2008; Robu et al., 2013, 2017), as animals with a vegetarian diet, including U. spelaeus of the Toll Cave (Ramírez-Pedraza et al., 2019). Recently, studies rejecting the presence of animal proteins in the diet of cave bear have also been developed using δ15N values of individual collagen amino acids (Naito et al., 2016). However, dental microwear does not contradict isotopic results, but provides complementary information, thus opening up the possibility of knowing an individual's diet at a specific time of their life. Dental microwear provides information on short-term diet during the life of the cave bear and this event is not necessarily reflected in the bone collagen. Thus, isotopes reflect a longer term and averaged dietary signal, whereas microwear captures a
6. Conclusion All the cave bear populations analyzed show an omnivorous-carnivorous diet at short-term scale, but there is no doubt, considering previous isotopic studies, that these ursids adopted a herbivorous diet. It is clear from this study that both short term dietary proxies like microwear as well as longer term proxies like isotopes are necessary to sufficiently address the dietary dynamics of cave bears. For future research, it would be interesting to combine different techniques to reconstruct the feeding habits of fossil bears (i.e. stable isotopes in bone and teeth, especially the nitrogen values of the collagen amino acids) emphasizing the use of complementary proxies on the same specimens. This should help solve the paradox of the diet of cave bears and also better our understanding how this large mammal survived important climatic changes until its disappearance towards the end of the Late Pleistocene. Acknowledgements This work was supported by the research grants from the Ministerio de Ciencia, Innovación y Universidades MICINN (grants HAR201676760-C3-1-P and HAR2016-76760-C3-3-P), MICINN/FEDER grants CGL2015-65387-C3-1-P and CGL2015-68604-P, and the Agència de Gestió d'Ajuts Universitaris i de Recerca (AGAUR 2017-SGR-836). The excavations are supported by the Generalitat de Catalunya projects CLT009/18/00055 at Toll and Teixoneres caves and CLT009/18/00092 at Serinyà caves. The research of J. Rosell and F. Rivals is funded by “CERCA Programme/Generalitat de Catalunya”. M. Arilla is the beneficiary of a research fellowship (FI) from AGAUR (2017FI-B-00096). We are grateful to Gina Semprebon and to an anonymous reviewer for 5
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constructive comments to improve the original manuscript.
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