August 10, 2021

The Preliminary Analysis of Cave Lion Cubs Panthera spelaea (Goldfuss, 1810) from the Permafrost of Siberia

Open AccessArticle

by 1,*, 2, 2, 3, 4, 5,6, 5,6,7, 2, 8 and 3

1

Diamond and Precious Metals Geology Institute, Siberian Branch of Russian Academy of Sciences, 39 Prospect Lenina, 677980 Yakutsk, Russia

2

Academy of Sciences of Sakha Republic, Lenin Avenue 33, 677007 Yakutsk, Russia

3

Zoological Institute, RAS, 1 Universitetskaya Embankment, 199034 Saint Petersburg, Russia

4

MMSH, LAMPEA UMR 7269 CNRS, Aix Marseille Université, 5 rue du Château de l’Horloge, BP 647, CEDEX 2, 13094 Aix-en-Provence, France

5

Centre for Palaeogenetics, Svante Arrhenius väg 20C, 10691 Stockholm, Sweden

6

Department of Bioinformatics and Genetics, Swedish Museum of Natural History, 11418 Stockholm, Sweden

7

School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK

8

Institute for High-Dimensional Medical Imaging, School of Medicine, Jikei University, Tokyo 105-8461, Japan

*

Author to whom correspondence should be addressed.

Academic Editor: Maria Rita Palombo

Quaternary 2021, 4(3), 24; https://doi.org/10.3390/quat4030024

Received: 5 February 2021 / Revised: 12 July 2021 / Accepted: 22 July 2021 / Published: 4 August 2021

(This article belongs to the Special Issue Advances in Quaternary Studies: The Contribution of Mammalian Fossil Record II)

A preliminary description is presented of the well-preserved frozen mummies of two cubs of the extinct cave lion Panthera spelaea (finds of 2017–2018, Semyuelyakh River, Yakutia, eastern Siberia, Russia). The fossil lion cubs were found in close proximity, but they do not belong to the same litter, since their radiocarbon ages differ: the female (named ‘Sparta’) was dated to 27,962 ± 109 uncal years BP, and the male (named ‘Boris’) was dated to 43,448 ± 389 uncal years BP. The lion cubs have similar individual ages, 1–2 months. The general tone of the colour of the fur coat of Sparta is greyish to light brown, whereas, in Boris, the fur is generally lighter, greyish yellowish. It is, therefore, possible that light colouration prevailed with age in cave lions and was adaptive for northern snow-covered landscapes. The article discusses the results of computed tomography of cubs of the cave lion, the possible reasons for their death, and the peculiarities of their existence in the Siberian Arctic.

Keywords: cave lion; Panthera spelaea; cubs; morphological description; radiocarbon dating; Siberia

1. Introduction

The Pleistocene Siberian Arctic zone was replete with large mammals and is astonishingly different from the Arctic zone of the present day. Along with mammoth (Mammuthus primigenius), woolly rhinoceros (Coelodonta antiquitatis), bison (Bison priscus), and saiga (Saiga tatarica), lived the cave lion (Panthera spelaea), a close relative of contemporary Afro-Asiatic lion P. leo L. It was on top of the trophic pyramid of the land polar ecosystem, being a part of the large Pleistocene carnivore guild alongside wolf Canis lupus L., wolverine Gulo gulo L. and brown bear Ursus arctos L. It is still unknown exactly how cave lions adapted to life in the harsh conditions of the high latitudes with their rapid season periodicity, strong winds, and cold and long winters with associated continuous nights.

Figure 1. The locations of the cave lion cubs finds: on the Uyandina River (indicated by a red triangle) and on the Semyuelyakh River (indicated by a red asterisk).

2. Place of the Find and Geological Age

3. Material and Methods

In November 2018, the frozen remains of Boris were delivered to Yakutsk and microbiologically tested in the sanitary-epidemiological station of Yakutsk for possible carriage of infectious diseases (including foot and mouth disease, anthrax, brucellosis, and rinderpest), all of which yielded negative results. The frozen remains of Sparta were delivered to Yakutsk in January 2019 and were also tested for infectious diseases; they also yielded negative results. The results of the present paper are based on the studies of the exterior morphology of the cave lion cubs’ mummies conducted in November 2018 and May 2019, as well as genetic-based sex determination.

4. Results

5. Discussion

If we assume that cave lions were similar to contemporary Panthera species (lion, tiger, leopard) in the way in which their cubs were brought up with male lions not participating in caring for the young, they would have been exposed to danger from other predators every time the mother went away to hunt. In the case of their mother’s death, the cubs would likely die from hunger. The harsh living conditions for large cats in high latitudes also have to be taken into account.

It is possible that cave lions were in a similar situation. We do not know when Sparta and Boris were born, but probably in summer (or autumn) time, and they most likely died when they were about 1 to 2 months old, in their den under the snow or the earth. This would explain why predators and scavengers did not find their bodies, and that is why we do not see any damage on the mummies that could have been inflicted by them. Maybe the cubs were buried under the ground following a landslide, and their bodies were deformed by the earth’s mass and permafrost features and froze quickly to become mummies.

6. Conclusions

The preliminary examination of the cubs’ mummies shows that the colour of the hair coat was changing from the juvenile yellowish-brown shade to a more ‘adult’ one, light grey to brown, at some point between 1–2 weeks and 1–2 months. Adult lions probably had light grey hair, well adapted to the Siberian Arctic, which is snow covered for two-thirds of the year.

We noted similarities between examined lion cubs P. spelaea and the contemporary lion cubs: their ears are light in the front but dark in the back, and they do not have a dark tuft on the end of their tail when they are born, but it is instead developed in their first few months. At the same time, cave lion cubs did not have vivid dark spots on their bodies and limbs, typical for P. leo cubs.

There is no sign of predators or scavengers damaging the fossil cave lions, but computed tomography showed skull damages, ribs dislocation, and other distortions in their skeletons that could be caused by the earth’s mass pressure due to the landslide and the following deformation due to the permafrost features.

Author Contributions

Organisation of research in Yakutsk, A.V.P.; preparing frozen mummies for research, I.S.P. and V.V.P.; external morphology studies, G.G.B., V.V.P., A.V.P., I.S.P. and A.N.T.; computed tomography studies, N.S. with the participation of V.V.P. and A.N.T.; genetic sex determination, L.D. and D.W.G.S.; discussion of images of cave lions in the caves of France, P.F.; writing—original draft preparation, G.G.B., V.V.P., G.F.B., P.F., D.W.G.S. and A.N.T.; discussion and writing—review and editing, all authors. All authors have read and agreed to the published version of the manuscript.

Funding

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors would like to express their gratitude to Anna A. Tikhonova, Saint-Petersburg, Russia, for the translation of the manuscript from Russian into English and to David W.G. Stanton for improving English language of the manuscript. Acknowledgements are addressed to the French Ministry of Culture and to the scientific team of Chauvet cave (Carole Fritz, Gilles Tosello).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Vereshchagin, N.K.; Tikhonov, A.N. Exterior of the mammoth. Cranium 1999, 1, 4–44. [Google Scholar]
  2. Lazarev, P.A. Large Mammals of the Antropogene of Yakutia; Nauka Publ.: Novosibirsk, Russia, 2008; pp. 1–160. (In Russian) [Google Scholar]
  3. Boeskorov, G.G. Le mammoth Laineux. Biologie et Adaptation aux Conditions Glaciaires. In Memoire de Mammoth; Cretin, C., Madelaine, S., Eds.; Musee National de Prehistoire Print: Les Eyzies-de-Tayac, France, 2018; pp. 19–30. [Google Scholar]
  4. Boeskorov, G.G.; Lazarev, P.A.; Sher, A.V.; Davydov, S.P.; Bakulina, N.T.; Shchelchkova, M.V.; Binladen, J.; Willerslev, E.; Buigues, B.; Tikhonov, A. Woolly rhino discovery in the lower Kolyma River. Quat. Sci. Rev. 2011, 30, 2262–2272. [Google Scholar] [CrossRef]
  5. Boeskorov, G.G.; Potapova, O.R.; Protopopov, A.V.; Plotnikov, V.V.; Maschenko, E.N.; Shchelchkova, M.V.; Petrova, E.A.; Kowalczyk, R.; van der Plicht, J.; Tikhonov, A.N. A study of a frozen mummy of a wild horse from the Holocene of Yakutia, East Siberia, Russia. Mammal. Res. 2018, 63, 307–314. [Google Scholar] [CrossRef]
  6. Boeskorov, G.G.; Potapova, O.R.; Protopopov, A.V.; Plotnikov, V.V.; Kirikov, K.S.; Agenbroadd, L.D.; Pavlov, I.S.; Shchelchkova, M.V.; Belolyubskii, I.N.; Tomshin, V.D.; et al. The Yukagir Bison: Analysis of a complete frozen mummy of the bison, Bison priscus from the early Holocene of Northern Eurasia. Quat. Int.2016, 406, 94–110. [Google Scholar] [CrossRef]
  7. Mashchenko, E.; Boeskorov, G.; Potapova, O.; Protopopov, A. Lions—From the Pleistocene to the present. What did the cubs of a lion from Yakutia tell us about? Nauka I Zhizn Sci. Life 2016, 6, 24–32. (In Russian) [Google Scholar]
  8. Protopopov, A.V.; Potapova, O.; Kharlamova, A.; Boeskorov, G.G.; Maschenko, E.N.; Shapiro, B.; Soares, A.; Pavlov, I.; Plotnikov, V.; Klimovskii, A. The Frozen Cave Lion ((Panthera spelaea(Goldfuss, 1810)) Newborn Cubs from Eastern Siberia, Russia: The first data on early ontogeny of the extinct species. PA J. Vertebr. Paleontol. 2016, 209. Available online: https://www.researchgate.net/publication/309910192 (accessed on 1 July 2021).
  9. Dussex, N.; Stanton, D.W.G.; Sigeman, H.; Ericson, P.G.; Gill, J.; Fisher, D.C.; Protopopov, A.V.; Herridge, V.L.; Plotnikov, V.; Hansson, B.; et al. Biomolecular analyses reveal the age, sex and species identity of a near-intact Pleistocene bird carcass. Commun. Biol. 2020, 3, 84. [Google Scholar] [CrossRef]
  10. Gromov, I.M.; Gureev, A.A.; Novikov, G.A.; Sokolov, I.I.; Strelkov, P.P.; Chapskii, K.K. Fauna SSSR. Mlekopitayushie. Opredelitel mlekopitaiushikh. Chast 2. (Kitoobraznye, Khishnye, Lastonogie, Neparnopalye, Parnopalye); Academy of Sciences of the USSR Publ. House: Moscow-Leningrad, Soviet Union, 1963; pp. 641–2000. (In Russian) [Google Scholar]
  11. Stanton, D.W.; Alberti, F.; Plotnikov, V.; Androsov, S.; Grigoriev, S.; Fedorov, S.; Kosintsev, P.; Nagel, D.; Vartanyan, S.; Barnes, I.; et al. Early Pleistocene origin and extensive intra-species diversity of the extinct cave lion. Sci. Rep. 2020, 10, 1–7. [Google Scholar] [CrossRef]
  12. Gilbert, M.T.P.; Tomsho, L.P.; Rendulic, S.; Packard, M.; Drautz, D.I.; Sher, A.; Tikhonov, A.; Dalén, L.; Kuznetsova, T.; Kosintsev, P.; et al. Whole-Genome Shotgun Sequencing of Mitochondria from Ancient Hair Shafts. Science 2007, 317, 1927–1930. [Google Scholar] [CrossRef]
  13. Yang, D.Y.; Eng, B.; Waye, J.S.; Dudar, J.C.; Saunders, S.R. Improved DNA Extraction from Ancient Bones Using Silica-Based Spin Columns. Am. J. Phys. Anthropol.1998, 105, 539–543. [Google Scholar] [CrossRef]
  14. Meyer, M.; Kircher, M. Illumina Sequencing Library Preparation for Highly Multiplexed Target Capture and Sequencing. Cold Spring Harb. Protoc. 2010, 5. [Google Scholar] [CrossRef]
  15. Palkopoulou, E.; Mallick, S.; Skoglund, P.; Enk, J.; Rohland, N.; Li, H.; Omrak, A.; Vartanyan, S.; Poinar, H.; Götherström, A.; et al. Complete Genomes Reveal Signatures of Demographic and Genetic Declines in the Woolly Mammoth. Curr. Biol. 2015, 25, 1395–1400. [Google Scholar] [CrossRef]
  16. Flynn, J.M.; Hubley, R.; Goubert, C.; Rosen, J.; Clark, A.G.; Feschotte, C.; Smit, A.F. RepeatModeler2 for Automated Genomic Discovery of Transposable Element Families. Proc. Natl. Acad. Sci. USA 2020, 117, 9451–9457. [Google Scholar] [CrossRef] [PubMed]
  17. Li, H.; Durbin, R. Fast and Accurate Short Read Alignment with Burrows-Wheeler Transform. Bioinformatics 2009, 25, 1754–1760. [Google Scholar] [CrossRef] [PubMed]
  18. Stuiver, M.; Polach, H.A. Discussion: Reporting of 14C data. Radiocarbon 1977, 19, 355–363. [Google Scholar] [CrossRef]
  19. Bronk Ramsey, C. Bayesian analysis of radiocarbon dates. Radiocarbon 2009, 51, 337–360. [Google Scholar] [CrossRef]
  20. Reimer, P.J.; Bard, E.; Bayliss, A.; Beck, J.W.; Blackwell, P.G.; Bronk Ramsey, C.; Buck, C.E.; Cheng, H.; Edwards, R.L.; Friedrich, M.; et al. IntCal13 and Marine13 Radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 2013, 55, 1869–1887. [Google Scholar] [CrossRef]
  21. Reimer, P.J.; Austin, W.E.N.; Bard, E.; Bayliss, A.; Blackwell, P.G.; Ramsey, C.B.; Butzin, M.; Cheng, H.; Edwards, R.L.; Friedrich, M.; et al. The IntCal20 Northern Hemisphere radiocarbon age calibration curve (0–55 cal kBP). Radiocarbon 2020, 62, 725–757. [Google Scholar] [CrossRef]
  22. Smuts, G.L.; Anderson, J.L.; Austin, J.C. Age determination of the African lion (Panthera leo). J. Zool. 1978, 185, 115–146. [Google Scholar] [CrossRef]
  23. Smuts, G.L.; Robinson, G.A.; Whyte, I.J. Comparative growth of wild male and female lions (Panthera leo). J. Zool. 1980, 190, 365–373. [Google Scholar] [CrossRef]
  24. Schaller, G. The Serengeti Lion: A Study of Predator-Prey Relations; University of Chicago Press: Chicago, IL, USA, 1972; pp. 1–504. [Google Scholar]
  25. Colahan, H.; Asa, C.; Azzarello-Dole, C.; Boutelle, S.; Briggs, M.; Cox, K.; Kellerman, E.; Murray, S.; New, E.; Pukazhenthi, B.; et al. AZA Lion Species Survival Plan. Lion Care Manual; Association of Zoos and Aquariums: Silver Spring, MD, USA, 2012; pp. 1–143. [Google Scholar]
  26. De Carvalho, C.T. Comparative growth rates of hand-reared big cats. Int. Zoo Yearb.1968, 8, 56–59. [Google Scholar] [CrossRef]
  27. Chernova, O.F.; Protopopov, A.V.; Boeskorov, G.G.; Pavlov, I.S.; Plotnikov, V.V.; Suzuki, N. First Description of the Fur of Two Cubs of Fossil Cave Lion Panthera spelaea (Goldfuss, 1810) Found in Yakutia in 2017 and 2018. Dokl. Biol. Sci. 2020, 492, 93–98. [Google Scholar] [CrossRef]
  28. Scott, J.; Scott, A. Big Cat Diary: Lion; Harper Collins Press: New York, NY, USA, 2002; pp. 1–45. [Google Scholar]
  29. Packer, C.; Pusey, A.E. Adaptations of female lions to infanticide by incoming males. Am. Nat. 1983, 121, 716–728. [Google Scholar] [CrossRef]
  30. Macdonald, D. The Encyclopedia of Mammals; Facts on File: New York, NY, USA, 1984; p. 31. [Google Scholar]
  31. Guthrie, R.D. Frozen Fauna of the Mammoth Steppe. The Story of Blue Babe; University of Chicago Press: Chicago, IL, USA, 1990; pp. 1–323. [Google Scholar]
  32. Yamaguchi, N.; Cooper, A.; Werdelin, L.; Macdonald, D.W. Evolution of the mane and group-living in the lion (Panthera leo): A review. J. Zool. 2004, 263, 329–342. [Google Scholar] [CrossRef]
  33. Turner, A. Dental sex dimorphism in European lions (Panthera leo L.) of the Upper Pleistocene: Palaeoecological and palaeoethological implications. Ann. Zool. Fenn. 1984, 21, 1–8. [Google Scholar]
  34. Boeskorov, G.G.; Baryshnikov, G.F. Late Quaternary Carnivorous Mammals of Yakutia; Nauka Publ. House: St. Petersburg, Russia, 2013; pp. 1–199. (In Russian) [Google Scholar]
  35. Yudin, I.G.; Yudina, E.V. Tiger of the Russian Far East; Dalnauka Publ.: Vladivostok, Russia, 2009; pp. 1–485. (In Russian) [Google Scholar]
  36. Heptner, V.G.; Naumov, N.P.; Yurgenson, P.B.; Sludsky, A.A.; Chirkova, A.F.; Bannikov, A.G. Mammals of the Soviet Union. Sea Cows and Carnivores; Vysshaya Shkola Publ.: Moscow, USSR, 1967; Volume II, pp. 136–140. (In Russian) [Google Scholar]
  37. Sokolov, V.E.; Rossolimo, O.L. Systematics and Variability. In The Wolf. History, Systematics, Morphology, Ecology; Bibikov, D.I., Ed.; Nauka Publ.: Moscow, USSR, 1985; pp. 22–50. (In Russian) [Google Scholar]
  38. Nougier, L.R.; Robert, R. Les félins dans l’art quaternaire. Préhistoire Spéléologie Ariégeoises 1965, 20, 17–62. [Google Scholar]
  39. Guthrie, R.D. The Nature of Paleolithic Art; University of Chicago Press: Chicago, IL, USA, 2006; pp. 1–520. [Google Scholar]
  40. Clottes, J.; Azéma, M. Les félins de la grotte Chauvet; Seuil Publ.: Paris, France, 2005; pp. 1–125. [Google Scholar]
  41. Fritz, C.; Fosse, P.; Tosello, G.; Sauvet, G.; Azéma, M. Ours et lion; réfléxion sur la place des carnivores dans l’art paléolithique. In Prédateurs dans tous leurs états: Évolution, Biodiversité, Interactions, Mythes, Symboles. XXXI Rencontres Internationales D’archéologie et D’histoire d’Antibes; Brugal, J.P., Gardeisen, A., Zucker, A., Eds.; Éditions APDCA: Antibes, France, 2011; pp. 299–323. [Google Scholar]
  42. Haas, S.K.; Hayssen, V.; Krausman, P.R. Panthera Leo. Mamm. Species 2005, 762, 1–11. [Google Scholar] [CrossRef]

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