Ursus spelaeus (Rosenmüller, 1794) during the MIS 3: new evidence from the Cioclovina Uscată Cave and radiocarbon age overview for the Carpathians*

ABSTRACT

Ursus spelaeus, the Late Pleistocene a cave bear is known from numerous accumulations found in the fossil sector of caves situated in the Carpathian and Apuseni Mountains. In this study, we present new radiocarbon data along a profile of the Cioclovina Uscată Cave, which is situated in the South Carpathians. The data suggest that, during the entire Marine Isotope Stage 3 (MIS 3) interval, the cave was serving as a shelter for U. spelaeus, with the oldest dated bone indicating an age of > 47,710 and the youngest one, an age of 31,820 ± 400 years cal BP. Histogram plots of 110 radiocarbon data from different caves of the Carpathian and Apuseni Mountains as Cioclovina Uscată, Peștera (Cave) cu Oase, Peștera Muierii, or Peștera Urșilor, respectively, show a maximum expansion of the cave bear population between 50,000 and 40,000, a decline between 40,000 and 35,000 and a partial recovery from 35,000–30,000 years cal BP. Radiocarbon data of Homo sapiens remains, younger than 35,000 years cal BP, support the fact that H. sapiens accessed the same caves where the cave bear persisted to hibernate. Besides general cool conditions and restricted food sources, the presence of H. sapiens constituted an additional stress factor driving the cave bear to extinction.

KEYWORDS:

• Mammalia
• Ursus spelaeus
• radiocarbon data
• population variation
• extinction
• Carpathian and Apuseni Mountains
• marine isotope stage 3 (MIS 3)
• quaternary

1. Introduction

The Cioclovina Uscată Cave is known for its large phosphate deposit, mined from 1912 to ca. 1988. The presence of a thick sedimentary pile, rich paleontological remains as well as mineral formation related to bone diagenesis, have motivated various teams to scientific investigations. In this context, sedimentological studies, including the history of phosphate exploitation and discoveries of bone remains, were done [1–4].

Further, mineralogical investigations were carried out [5–10] and studies on vertebrate remains, including hominids were performed [1,11–31].

According to Soficaru and Petrea [22], with a few exceptions, the impressive fossil accumulations found in this cave belong to Ursus spelaeus. Rădulescu and Samson [14] described extremely rare occurrences of Ursus arctos, Canis lupus, Panthera (Leo) spelaea and Capra ibex. Previous investigations regarding the time when the cave bear inhabited the cave, determined an interval between ca. 44,200 and 31,400 years cal BP [28], an interval belonging to the Marine Isotope Stage 3 (MIS 3).

The purpose of the present study is to date a profile along the Cioclovina Uscată Cave and to compare the age range with previously published radiocarbon data of cave bear remains. For the Carpathian and Apuseni Mountains we consider for comparison, besides the Cioclovina Uscată Cave, Peștera (Cave) cu Oase, Peștera Muierii and Peștera Urșilor, all of them characterized by impressive accumulations of cave bear remains. Three of these caves, namely Cioclovina Uscată, Peștera cu Oase and Peștera Muierii are known for radiocarbon-dated Homo sapiens bones. Up to now, the following data were published for (1) Cioclovina Uscată Cave: for U. spelaeus remains [19,28,31]; H. sapiens skull [16,19]; (2) Peștera cu Oase: for U. spelaeus [28,32]; for H. sapiens [33]; (3) Peștera Muierii: for U. spelaeus [17,20,34,35]; for H. sapiens [16,17]; (4) Peștera Urșilor: for U. spelaeus [28,35,36].

Based on newly acquired data along Cioclovina Uscată Cave, previously published radiocarbon ages and available environmental data, the goal of the present study is to establish: (1) the time range for the presence of cave bears; (2) the cave bear population fluctuation during MIS 3 for the Carpathians and comparison with other European locations; (3) the circumstances during which the cave bear population declined towards extinction.

2. Geological frame of cioclovina uscată cave

The Cioclovina Uscată Cave is situated in the Southern Carpathians, Sebeș Mountains (45°34'30.9″N 23°08'20,6″E) at an altitude of 750 m (Figure 1 a, b). The cave developed in Oxfordian – Tithonian (Jurassic) limestones belonging to the sedimentary cover of the Getic Nappe. The lithostratigraphy of the sedimentary cover is synthesized by Stilla [37], being similar to the entire area of the Hațeg Basin and surroundings [38,39]. The cave entrance is situated above the Wet Cioclovina Cave (Peștera Cioclovina cu Apă), the former representing the exsurgence of a creek. The cave system Ponorici–Cioclovina cu Apă sums to ca. 7.8 km [1,40,41]. The entrance in the Cioclovina Cave is situated at the base of a sharp escarpment of Jurassic limestones belonging to an anticlinal structure oriented NE–SW, which is cut towards the south by a NE–SW trending dextral normal fault. The cave traverses the Cioclovina fault and ends in the adjacent syncline. The major NW–SE trending brittle faults are visible in the development directions of the Cioclovina Uscată Cave [42] (Figure 1 b, c in this study).

Figure 1. Cioclovina Uscată, Peștera cu Oase, Muierilor, Urșilor, Poleva cave positions on (a) Geographical map of Romania and (b) a Geological map of the region (after Pop et al. [43]); (c) location of the map with the approximate position of the analysed cave bear remains (Simplified cave map after Tomuș [44]). AM – Apuseni Mountains, EC – Eastern Carpathians, SC – Southern Carpathians.

3. Material and methods

3.1. Sample collection and graphical display

Material for analysis was available from a historical sampling at various sites along the main gallery of the cave (Figure 1c). The new radiocarbon data are displayed in Table 1 and Figures 2 and 3.

Figure 2. Probability distribution of ¹⁴C ages. For details, see Table 1.

Figure 3. Isotope stages of MIS 3 with stadials and interstadials [46] plotted with the radiocarbon ages from the Cioclovina Uscată cave for U. spelaeus: this study (red), [19] (violet); [28] (green); [31] (blue); for H. sapiens: [16,19] (brown and dashed lines); ¹⁴C determined ages are displayed as ages cal BP).

Table 1. The radiocarbon dates measured for this study and calibrated using the IntCal20 calibration dataset [45].

Sample name and lab. code	Material	Preparation	Collagen yield (%)	Carbon content in collagen (%C)	Nitrogen content in collagen (%N)	C/N atomic ratio	Conventional ^14C age	Calibrated age (years cal BP)
OS-6 GdA – 7119	Limb bone	Modified Longin + UF	9.0	11.70	4.01	3.3	>49430	68.3% probability  … (68.3%) 50470BP 95.4% probability  … (95.4%) 47710BP
OS-7 GdA – 7120	Radius	Modified Longin + UF	9.4	12.02	3.93	3.2	33450 ± 475	68.3% probability 39060BP (68.3%) 37600BP 95.4% probability 39510BP (95.4%) 36960BP Median: 38270 ± 690
OS-9 GdA – 7121	Femur	Modified Longin + UF	11.9	20.86	7.32	3.3	32300 ± 410	68.3% probability 37090BP (68.3%) 36200BP 95.4% probability 38070BP (0.6%) 37950BP 37820BP (94.9%) 35680BP Median: 36700 ± 530
OS-11a GdA – 7122	Femur	Modified Longin + UF	7.4	2.15	0.37	3.0	31110 ± 370	68.3% probability 36010BP (68.3%) 35180BP 95.4% probability 36210BP (95.4%) 34700BP Median: 35510 ± 400
OS-12-1 GdA – 7124	Femur	Modified Longin + UF	7.9	8.23	2.38	3.2	27865 ± 255	68.3% probability 32110BP (68.3%) 31430BP 95.4% probability 32860BP (10.2%) 32430BP 32350BP (85.3%) 31220BP Median: 31820 ± 400
OS-12-2 GdA – 7125	Femur	Modified Longin + UF	9.9	4.46	1.09	3.0	39355 ± 970	68.3% probability 43820BP (7.7%) 43610BP 43440BP (60.6%) 42360BP 95.4% probability 44510BP (95.4%) 42130BP Median: 43070 ± 660
OS8-1 GdA – 7406	Maxilar	Modified Longin	27.4	4.62	1.60	3.4	29000 ± 290	68.3% probability 33945BP (68.3%) 33125BP 95.4% probability 34255BP (90.2%) 32760BP 32610BP (5.3%) 32275BP Median: 33490 ± 450
OS6-1 GdA – 7407	Canin	Modified Longin	19.5	5.63	1.95	3.4	41930 ± 1380	68.3% probability 45930BP (62.2%) 43740BP 43705BP (6.0%) 43405BP 95.4% probability 47960BP (95.4%) 42805BP Median: 44940 ± 1420
OS13 GdA – 7408	Ulna	Modified Longin	27.8	12.23	6.10	2.3	>46670	68.3% probability 52395BP (68.3%) 46870BP 95.4% probability  … (95.4%) 46165BP

For Figure 4, we recalibrated the already published radiocarbon ages using the most recent IntCal20 calibration curve [45]. The histograms are designed using the median ages, a total number of approx. 110 radiocarbon ages on cave bear remains were considered, including the new dated material.

Figure 4. Histograms with the measured radiocarbon ages cal BP. The frequencies of age occurrence are considered as indicating demographic changes of U. spaeleus over time. Approx. 110 radiocarbon ages (including these presented for the first time in this study) were considered from the first publication date. Radiocarbon ages are recalibrated with IntCal 20 [45]. The considered caves from the Carpathian realm are: (1) Cioclovina Uscată for U. spelaeus: this study, [19,28,31]; for H. sapiens: [16,19]; (2) Peștera cu Oase for U. spelaeus: [28,32]; for H. sapiens: [33]; (3) Peștera Muierii for U. spelaeus: [17,20,34,35]; for H. sapiens: [16,17]; (4) Peștera Urșilor for U. spelaeus: [28,35,36].

3.2. Radiocarbon dating

Ten samples of bones were prepared in two batches. The first one, consisting of 7 samples, was subjected to preparation that included mechanical abrasion of the bones, then cleaning in demineralized water in an ultrasonic bath and drying. The next step was grinding in a hand mortar to ∼1 mm particles. The gelatine extraction was performed according to the Longin method [47], modified by Piotrowska and Goslar [48], with the use of an alkali solution at room temperature. First, 0.5 M hydrochloric acid was used and replaced several times until the reaction was considered complete, the pH stabilized at < 1 and no bubbles were observed. The insoluble residues were then rinsed with demineralized water and treated with 0.1 M sodium hydroxide at room temperature for 30 min and rinsed to neutral pH. After the second acid bath and rinsing, the residues were subjected to gelatinization in acidified solution (pH = 3) for at least 12 h at 85 °C. Next, the gelatine samples were filtered through pre-cleaned 9 mL Ezee Filters^TM and ultrafiltered with the use of Millipore Amicon® Ultra-15 ultrafiltration tubes (Merck). The protocol of ultrafilters pre-cleaning and samples ultrafiltration was based on Bronk Ramsey et al. [49] and Brock et al. [50]; it was also described in a more detailed way in [51]. One of the samples (OS-11b) gave too low collagen yield showing a low C/N atomic ratio (C/N_at); therefore it was not further analysed. Another batch of three samples (OS8-1, OS6-1 and OS13) was treated similarly but excluding the ultrafiltration step. All of the gelatine samples were freeze-dried and were subjected to graphitization using an automated graphitization unit AGE-3 [52,53] with VarioMicroCube by Elementar elemental analyser. The analyser was calibrated with reference materials – aspartic acid and glutamic acid – to obtain the weight per cent of C and N. C/N_at were calculated taking into account the atomic masses of C and N. The ¹⁴C concentrations were measured using a MICADAS accelerator mass spectrometer [54], and the data reduction performed in BATS software [55], including fractionation correction based on AMS-derived δ¹³C. Chemical pretreatment and radiocarbon measurements were performed in the Radiocarbon and Mass Spectrometry Laboratory at SUT, Gliwice, Poland. The detection limit for collagen can be estimated based on the results provided by Pawełczyk et al. [51] to 45,000–48,000 ¹⁴C BP, and the ages reaching the limit were reported as ‘older than’ in Table 1, based on the background correction for a given batch of samples. The ¹⁴C dates were calibrated with OxCal software [56] using the IntCal20 calibration curve [45].

4. Results

The results of ¹⁴C dating are displayed in Table 1 and Figures 1 and 2. The nine radiocarbon ages (from a total of 10 samples prepared) range from 31,800 ± 400 cal BP to the ages reaching the IntCal20 calibration curve (>47,710 years cal BP) representing the most complete profile of ages, which have been measured for the Cioclovina Uscată (Figure 3). The results of the AMS ¹⁴C dating extend the range when the cave bears inhabited the site, between approx. 52,000 and 27,000 years cal BP.

The measured data were compared with the available measurements for the same cave as well as Peștera cu Oase, Peștera Muierii and Peștera Urșilor caves (Figure 4a), all the radiocarbon ages determined for the four caves being plotted in Figure 4b.

5. Discussion

In Figure 3, the ¹⁴C ages cal BP measured for this study are plotted on a time scale together with the δ¹⁸O values measured on the NGRIP ice core from Greenland [46], values matching the more recent WAIS Divide ice core record from West Antarctica [57]. For each Dansgaard–Oeschger (DO)/Greenland interstadial (GIS) event, a corresponding Antarctic Isotopic Maximum (AIM) event can be identified [58]. The successive phases of cooling and warming belonging to the MIS 3 (Figures 3 and 4) have numbers from 16 downward. According to the stratigraphic convention for glacial fluctuations the cooler stadials are counted with even numbers, and the warmer interstadials with uneven numbers (e.g. [59]).

Both Figure 3 and the histograms from Figure 4 support that after an expansion between 40,000–50,000 years cal BP, U. spelaeus shows a decline of the population between 40,000 and 35,000 years cal BP. In a speleotheme record from Poleva Cave (location shown in Figure 1 a), Constantin et al. [60] documented lower δ¹⁸O values (as in Figure 1 of the mentioned publication), values representing a regional cold episode, younger than 40,000 years cal BP. This episode, possibly corresponding to stadials 8 and/or 6, is situated at the level showing a decline of cave bear population, thus between 40,000–35,000 years cal BP (Figure 4, present study). In the stalagmite from Poleva Cave [60] the decreasing δ¹⁸O values are associated with increasing δ¹³C values, probably related to the shift from vegetation-dominated to limestone-dominated carbon isotope signal, thus cooling. Using mitochondrial genomes (mtDNA) combined with a mtDNA sequence approach, Gretzinger et al. [61] suggest also a drastic cave bear population decline starting 40,000 years BP, associating this decline rather with human activity than with cooling. We suggest that the main reason for not associating the decline of cave bears with cooling is the scarce archives available for this period. For the Carpathians, the cooling documented by Constantin et al. [60] for the interval 40,000–35,000 years cal BP is older than by radiocarbon ages showing the presence of H. sapiens in the same caves, ages younger than 35,000 years cal BP (Figure 4a). The extended low temperatures between 40,000–35,000 could induce restricted vegetation (suggested also by increasing δ¹³C values), more restricted vegetation implying lowering food sources of cave bears, considered predominantly vegetarian [27,31,62–66] or consuming sporadically meat [35].

Interestingly, for Cioclovina Uscată the radiocarbon ¹⁴C ages determined by Olariu et al. [16] and Soficaru et al. [19] for H. sapiens skull fragment, indicate that for some thousands of years, H. sapiens and U. spelaeus were visitors of the same cave. Moreover, as displayed in Figure 4a, some thousands of years after the presence of H. sapiens was documented in the cave by radiocarbon dating, U. spelaeus ceased to use it as a hibernation place and completely disappeared. Extended cool period and population decline documented between 40,000 and 35,000 years cal BP (Figure 4a, b), was followed by a partial recovery in the interval 35,000–30,000 years cal BP, synchronously with the oldest dated H. sapiens remains. From the previous radiocarbon data presented as histograms in Figure 4, only one data from Peștera Muierii is younger than 25,000 years cal BP and two are younger than 27,000 years cal BP. In Table 4 of Mirea et al. [34], the authors indicate that the three mentioned ages belong to questionable radiocarbon data (samples PM/T6 – XVII-XVIII, PM/T6 – XIII-XIV, PM/P6 – IV-V). For Cioclovina Uscată Cave, the youngest dated bone for this study gives an age of 31,800 ± 400 years cal BP (Table 1), which is slightly older than the proposed date for the extinction of U. spaeleus around 28,000–29,000 years cal BP [62,63,65]. For the Urșilor Cave, Duñò-Iglesias et al. [35] dated a bone with 27,100 ± 220 (2σ) years cal BP, younger than this measured by Bocherens et al. [65] for U. speleaus from Rochedane Cave situated near Montbeliard (French Jura), where the authors put in evidence an age of 28,730–28,500 (1σ) years cal BP. For comparison of age ranges between European sites, Pacher and Stuart [63] included the data available at that time from Peștera cu Oase for the Carpathian Mountains. As observed in Figure 4 from our present study, Peștera cu Oase offers only a relative old and restricted range of data for the U. speleaus remains, even additional data for Peștera cu Oase are available, since the publication by Pacher and Stuart [63].

Radiocarbon data from the Carpathian caves considered for the present study indicate that cave bears had covered a wide time span from ca. 50,000–31,000 years cal BP, thus the entire MIS 3, similar to the range for Austria [63]. The data from Figures 3 and 4 (this publication) support the fact that, after cooling and decreasing vegetation productivity, the cave bear population increased again but not to the previous 40,000 years cal BP level. The subsequently documented presence of H. sapiens accessing the same caves, constituted an additional stress factor, contributing to U. speleaus extinction.

Paleomagnetic studies by Panaiotu and Petrea [3] indicated that cave bear bones dated at 40,000, respectively, 32,000 years cal BP were found in much younger sediments (15,000–12,000 years cal BP). This fact was interpreted as re-deposition of a large part of the deposits and implicitly of human and cave bear bones. The re-deposition is probably connected to water inflow during abrupt climatic warming at the end of MIS 2, thus the Late Pleistocene. The new radiocarbon data extend the age of the Cioclovina Uscată Cave sediments and shift the fossil regime and the maximum age of sediments approximated at 40,000 [22] to at least 52,000 years cal BP.

6. Conclusions

The radiocarbon data measured for this study show that Cioclovina Uscată Cave was visited by U. spelaeus (Rosenmüller, 1794) during the entire MIS 3 interval, similar to the age range determined for Peștera Muierii and Peștera Urșilor Caves. In this context, Peștera cu Oase shows a much restricted and old range of ages for the dated bones. This study indicates that, for the Cioclovina Uscată Cave, the oldest remains are situated in an appendix of the main gallery, left of the entrance. The youngest dated bone shows an age of 31,800 ± 400 years cal BP, slightly older than the dated bone of Ursus spelaeus from Peștera Urșilor (Apuseni) and Rochedane Caves (French Jura).

Histogram distribution of radiocarbon ages represents a powerful tool in order to trace population fluctuation over a region. Histograms of the newly dated bones as well as previously published data, summing a total of 110 radiocarbon data, show a maximum expansion of the cave bear between 50,000 and 40,000, a decline between 40,000 and 35,000 and a partial recovery from 35,000 to 30,000 years cal BP. The decline was associated with a period where probably cooler conditions prevailed during stadials 8 and 6, as suggested by stable isotope values from a stalagmite from Poleva Cave. The various records in this interval are scarce for the region probably related to general cool conditions and sedimentation hiatuses younger than 40,000 years BP. As cave bears had mainly a vegetarian diet, the general cool conditions dramatically restricted their food sources. Below 35,000 years cal BP, radiocarbon data documented that H. sapiens accessed the same caves as the caves where bears persisted to hibernate. We propose that besides general cool conditions and restricted food sources, this constituted an additional stress factor driving the cave bear to extinction.

Acknowledgements

We thank two anonymous reviewers for their valuable comments and suggestions, which improved our manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).