Histological stability of the Malolyakhovsky mammoth tissues to permafrost conditions

Darima Garmaeva; Sardaana Efremova; Lena Grigoreva; Maksim Cheprasov; Radik Khayrullin; Igor Dugunov; Maria Kirillina; Woo Suk Hwang

doi:10.21638/spbu03.2023.408

Authors

Darima Garmaeva Medical Institute, North-Eastern Federal University, ul. Kulakovskogo, 34, Yakutsk, 677000, Russian Federation
Sardaana Efremova Institute of Natural Sciences, North-Eastern Federal University, ul. Kulakovskogo, 48, Yakutsk, 677000, Russian Federation https://orcid.org/0000-0003-1595-0263
Lena Grigoreva Institute of Applied Ecology of the North, North-Eastern Federal University, ul. Kulakovskogo, 48, Yakutsk, 677000, Russian Federation https://orcid.org/0000-0002-9804-6570
Maksim Cheprasov Lazarev Mammoth Museum, Institute of Applied Ecology of the North, North-Eastern Federal University, ul. Kulakovskogo, 48, Yakutsk, 677000, Russian Federation
Radik Khayrullin Department of Morphology and Pathology, Private University REAVIZ, ul. Kalinina, 8, Saint Petersburg, 198095, Russian Federation; Department of Clinical Anatomy and Operative Surgery, Pavlov First Saint Petersburg State Medical University, ul. L'va Tolstogo, 6–8, Saint Petersburg, 197022, Russian Federation; Department of Anatomy and Physiology of International Medical Faculty, Osh State University, Osh, 723500, Kyrgyz Republic https://orcid.org/0000-0002-2796-7508
Igor Dugunov Medical Institute, North-Eastern Federal University, ul. Kulakovskogo, 34, Yakutsk, 677000, Russian Federation
Maria Kirillina Medical Institute, North-Eastern Federal University, ul. Kulakovskogo, 34, Yakutsk, 677000, Russian Federation
Woo Suk Hwang Institute of Natural Sciences, North-Eastern Federal University, ul. Kulakovskogo, 48, Yakutsk, 677000, Russian Federation; UAE Biotech Research Center, U46, Al Wathbah, Abu Dhabi, 30310, United Arab Emirates

DOI:

https://doi.org/10.21638/spbu03.2023.408

Abstract

This work presents a histological analysis of adipose, muscle, cartilaginous tissue, walls of blood vessels and tendons of the Malolyakhovsky mammoth, found on the island of Maly Lyakhovsky of the New Siberian archipelago in 2012, for signs of preservation and stability of tissue structures to permafrost conditions. We have also performed a comparative analysis of the obtained histological data with the data from other woolly mammoths from the available literature. It was revealed that the tissues which were most preserved and resistant to permafrost conditions were the ones with a compact structure of connective tissue. The results of the work and the data obtained are of great importance for further research in the field of paleontology. In the future, they can be used in a comparative analysis with other representatives of woolly mammoths and mammals of the mammoth fauna.

Keywords:

Malolyakhovsky mammoth, soft tissues, histological analysis, comparative morphological analysis, adipose tissue, muscle tissue, circulatory tissue, cartilaginous tissue, tendons

Downloads

Download data is not yet available.

References

Boeskorov, G. G., Belolyubsky, I. N., Plotnikov, V. V., Protopopov, A. V., Nogovitsyn, P. R., Mashchenko, E. N., Stepanov, A. D., Shchelchkova, M. V., Solomonov, N. G., and van der Plicht J. 2016. New data on Mammoth fauna mammals in the central Lena River basin (Yakutia, Lenskie Stolby National Nature Park and adjacent areas). Doklady Akademii nauk 469(1):647–651. https://doi.org/10.7868/S0869565216200147 (In Russian)

Boeskorov, G. G., Belolyubskii, I. N., Tomshin, M. D., Protopopov, A. V., Plotnikov, V. V., Kolesov, S. D., Mashchenko, E. N., Potapova, O. R., Kuznetsova, T. V., Grigoryev, S. E., Shchelchkova, M. V., van der Plicht, I., and Tikhonov, A. N. 2013a. New findings of unique preserved fossil mammals in the permafrost of Yakutia. Doklady Akademii nauk 452(1):291–295. https://doi.org/10.7868/S0869565213290203 (In Russian)

Boeskorov, G. G., Protopopov, A. V., Mashchenko, E. N., Potapova, O. R., Tikhonov, A. N., Kuznetsova, T. V., Plotnikov, V. V., Fisher, D., Agenbroad, L., Grigoriev, S. E., Beloliubskiy, I. N., Tomshin, M. D., Shchelchkova, M. V., Shapiro, B., Kolesov, S. N., Sergeenko, A. I., and Buigues, B. 2012. Preliminary data of the unique findings of the Ice Age mammals on the Yana-Indigirka lowland. Vestnik SVFU 9(4):10–16. (In Russian)

Boeskorov, G. G., Potapova, O. R., Mashchenko, E. N., Protopopov, A. V., Kuznetsova, T. V., Agenbroad, L., and Tikhonov, A. N. 2013b. Preliminary analyses of the frozen mummies of mammoth (Mammuthus primigenius), bison (Bison priscus) and horse (Equus sp.) from the Yana-Indigirka Lowland, Yakutia, Russia. Integrative zoology, Special Issue: Paleontology and evolution. Part II 9(4):471–480. https://doi.org/10.1111/1749-4877.12079

Boeskorov, G. G., Tikhonov, A. N., and Suzuki, N. 2007. Yukagir mammoth. 251 pp. St. Petersburg University Press, St. Petersburg. (In Russian)

Fisher, D. C., Tikhonov, A. N., Kosintsev, P. A., Rountrey, A. N., Buigues, B., and van der Plicht, J. 2012. Anatomy, death, and preservation of a woolly mammoth (Mammuthus primigenius) calf, Yamal Peninsula, Northwest Siberia. Quaternary International 255:94–105. https://doi.org/10.1016/j.quaint.2011.05.040

Galanin, A. A., Dyachkovsky, A. P., Lytkin, V. M., Burnasheva, M. P., Shaposhnikov, G. I., and Kut A. A. 2015. The results of definition of absolute age of samples in radio-carbon laboratory of permafrost Research Institute of the Siberian Branch of the RAS. Nauka i obrazovanie 4:45–49. (In Russian)

Garmaeva, D. K., Buzinaeva, M. T., and Grigoriev, S. E. 2019. Histological analysis of the preservation of the tissue structures of the trunk of the Malolyakhovsky mammoth under conditions of natural cryopreservation by permafrost. Morphologiya 155(2):75–76. (In Russian)

Garmaeva, D., Buzinaeva, M., Savvinov, G., Grigoriev, S., Fedorov, S., Tikhonov, A., Novgorodov, G., and Cheprasov, M. 2014. Histological evaluation of tissue structure preservation in the Malolyakhovski mammoth. Abstract book of the 5^th International Conference on Mammoths and their Relatives S. A. S. G. 102:63.

Grigoriev, S. E., Cheprasov, M. Yu., Savvinov, G. N., Tikhonov, A. N., Novgorodov, G. P., Fedorov, S. E., Boeskorov, G. G., Protopopov, A. V., Plotnikov, V. V., Belolubsky, I. N., Protodiyakonov, K. E., and van der Plicht, J. 2017. Paleontological and archaeozoological researches in the Yana River Basin. Vestnik SVFU 1(57):20–35. (In Russian)

Grigoriev, S. E., Fisher, D. C., Obadă, T., Shirley, E. A., Rountrey, A. N., Savvinov, G. N., Garmaeva, D. K., Novgorodov, G. P., Cheprasov, M. Yu., Vasilev, S. E., Goncharov, A. E., Masharskiy, A., Egorova, V. E., Petrova, P. P., Egorova, E. E., Akhremenko, Y. A., van der Plicht, J., Galanin, A. A., Fedorov, S. E., Ivanov, E. V., and Tikhonov, A. N. 2017. A woolly mammoth (Mammuthus primigenius) carcass from Maly Lyakhovsky Island (New Siberian Islands, Russian Federation). Quaternary International 455:89–103. https://doi.org/10.1016/j.quaint.2017.01.007

Hattori, S., Kiriyama-Tanaka, T., Kusubata, M., Taga, Y., Ebihara, T., Kumazawa, Y., Imai, K., Miura, M., Mezaki, Y., Tikhonov, A., and Senoo, H. 2021. Preservation of collagen in the soft tissues of frozen mammoths. PLoS ONE 16(10):1–14. https://doi.org/10.1371/journal.pone.0258699

Kato, H., Anzai, M., Mitani, T., Morita, M., Nishiyama, Y., Nakao, A., Kondo, K., Lazarev, P. A., Ohtani, T., Shibata, Y., and Iritani, A. 2009. Recovery of cell nuclei from 15,000 years old mammoth tissues and its injection into mouse enucleated matured oocytes. Proceedings of the Japan Academy, Series B 85:240–247. https://doi.org/10.2183/pjab.85.240

Kharlamova, A. S., Saveliev, S. V., Protopopov, A. V., Maseko, B. C., Bhagwandin, A., and Manger, P. R. 2015. The mummified brain of a pleistocene woolly mammoth (Mammuthus primigenius) compared with the brain of the extant African elephant (Loxodonta africana). The Journal of Comparative Neurology 523(16):2326–2343. https://doi.org/10.1002/cne.23817

Kornienko, I. V., Faleeva, T. G., Oreshkova, N. V., Grigoriev, S. E., Grigoreva, L. V., Putintseva, Yu. A., and Krutovsky, K. V. 2019. Structural and functional organization of the control region of Woolly mammoth (Mammuthus primigenius) Mitochondrial DNA. Molekulyarnaya biologiya 53(4):627–637. https://doi.org/10.1134/S0026898419040062 (In Russian)

Kornienko, I. V., Faleeva, T. G., Oreshkova, N. V., Grigoriev, S. E., Grigoreva, L. V., Simonov, E. P., Kolesnikova, A. I., Putintseva, Y. A., and Krutovsky, K. V. 2018. Complete mitochondrial genome of a woolly mammoth (Mammuthus primigenius) from Maly Lyakhovsky Island (New Siberian Islands, Russia) and its phylogenetic assessment. Mitochondrial DNA Part B 3(2):596–598. https://doi.org/10.1080/23802359.2018.1473721

Lazarev, P. A. 2007. Tracing back mammoths: Expeditions, research and exhibitions of the Mammoth Museum. 84 pp. Izdatelstvo IPES AN RS(Ya) Publ., Yakutsk. (In Russian)

Lazarev, P. A. 2008. Large mammals of the anthropogene of Yakutia. 158 pp. Nauka Publ., Novosibirsk. (In Russian)

Lazarev, P. A., Boeskorov, G. G., Savvinov, D. D., Savvinov, G. N., Protopopov, A. V., Shumilov, Yu. V., Vasiliev, V. M., and Rodionov, G. N. 2004. Yakut phenomenon: The world of mammoths. 127 pp. Yakutia Publ., Yakutsk. (In Russian)

Lazarev, P. A., Boeskorov, G. G., Tomskaya, A. I., Garutt, N. V., Vasiliev, E. M., Kasparov, A. K., and Rodionov G. N. 1998. Anthropogenous mammals of Yakutia. 158 pp. YaNTs SO RAN Publ., Yakutsk. (In Russian)

Mashchenko, E. N. 2002. Individual development, biology and evolution of the woolly mammoth Mammuthus primigenius (Blumenbach, 1799). Cranium 19(1):4–12.

Mashchenko, E. N., Tikhonov, A. N., and MacPhee, R. D. E. 2005. Mammoth calf from Bolshoi Lyakhovskii Island (New Siberian Islands, Arctic Siberia). Russian Journal of Theriology 4(1):79–88. https://doi.org/10.15298/rusjtheriol.04.1.06

Papageorgopoulou, C., Link, K., and Rühli, F. J. 2015. Histology of a woolly mammoth (Mammuthus primigenius) preserved in permafrost, Yamal Peninsula, Northwest Siberia. The Anatomical Record 298:1059–1071. https://doi.org/10.1002/ar.23148

Peshkova, E. V. and Akulinin, E. I. 2012. Study of the structure and methods of studying animal and human tissues: methodology instructions. 24 pp. Izdatelstvo FGBOU VPO “TGTU” Publ., Tambov. (In Russian)

Plotnikov, V. V., Maschenko, E. N., Pavlov, I. S., Protopopov, A. V., Boeskorov, G. G., and Petrova E. A. 2015. New data on trunk morphology in the woolly mammoth, Mammutus primigenius (Blumenbach). Paleontologicheskii Zhurnal 2:87–88. https://doi.org/10.1134/S0031030115020070 (In Russian)

Repin, V. E., Taranov, O. S., Ryabchikova, E. I., Tikhonov, A. N., and Pugachev, V. G. 2004. Sebaceous glands of the woolly mammoth, Mammothus primigenius Blum.: Histological evidence. Doklady Biological Sciences 398:382–384. https://doi.org/10.1023/B:DOBS.0000046662.43270.66

Shilo, N. A., Lozhkin, A. V., Titov, E. E., and Shumilov, Yu. V. 1983. Kirgilyakhsky mammoth. 215 pp. Nauka, Moscow. (In Russian)

Tikhonov, A. N. 2005. Mammoth (Series “Variety of Animals”). 518 pp. Tovarishchestvo nauchnykh izdaniy KMK Publ., Mosсow, Saint Petersburg. (In Russian)

Vereshchagin, N. K. 1979. Why mammoths became extinct. 195 pp. Nauka Publ., Leningrad. (In Russian)

Vereshchagin, N. K. and Mikhel’son, V. M. 1981. Magadansky baby mammoth. 279 pp. Nauka, Leningrad. (In Russian)

Vereshchagin, N. K. and Tikhonov, A. N. 1990. Mammoth exterior. 44 pp. Institut merzlotovedeniya SO AN SSSR Publ., Yakutsk. (In Russian)

Yanin, V. L., Bondarenko, O. M., and Sazonova, N. A. 2015. Research methods in Cytology and Histology. 65 pp. Khanty-Mansiyskaya gosudarstvennaya meditsinskaya akademiya Publ., Khanty-Mansiysk. (In Russian)