Skip to main content
SpringerLink
Log in

Cold Hardiness of Mass Soil Invertebrate Animals of Northeastern Asia: 1. Cold Hardiness and the Mechanisms of Its Maintenance

  • Published:
Biology Bulletin Aims and scope Submit manuscript

Abstract

The cold hardiness of soil invertebrates (37 species of insects and 27 species of other taxa) was studied in the continental areas of Northeast Asia, a region with extreme winter temperatures. Insects overwinter mostly (34 species) in a supercooled state surviving within the temperature range of –12 to –35°C. Thirteen species of invertebrates (including insects, centipedes, slugs, earthworms, and amphipods) can withstand temperatures within the range of –5 to –45°C in a frozen state. The eggs of slugs, cocoons of earthworms, and larvae of some species of elaterids use cryoprotective dehydration, which allows them to survive at temperatures from –20 to –40°C, down to the record minimum of –196°C. Most of the organisms studied can tolerate temperatures of –25 to –30°C, which correspond to the average minimal temperatures in the upper soil horizons in most habitats of the continental regions of Northeast Asia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.

Similar content being viewed by others

REFERENCES

  1. Alfimov, A.V., The thermal regime of the upper layers of soil in the main ecosystems of the sparse forest belt of the Upper Kolyma basin, in Poyas redkolesii verkhovii Kolymy (raion stroitel’stva Kolymskoi GES) (The Sparse Forest Belt of the Upper Reaches of the Kolyma River (the Kolyma HPP Construction Area)), Vladivostok: Dal’nevost. Nauch. Tsentr Akad. Nauk SSSR, 1985, pp. 9–29.

  2. Alfimov, A.V., Thermal regime of mountain tundras, in Pochvennyi yarus ekosistem gornykh tundr khrebta Bol’shoi Annachag (verkhov’e Kolymy) (The Soil Layer of Mountain Tundra Ecosystems of the Bol’shoi Annachag Ridge), Vladivostok: Dal’nevost. Nauch. Tsentr Akad. Nauk SSSR, 1984, pp. 6–40.

    Google Scholar 

  3. Balashov, Yu.S., Iksodovye kleshchi – parazity i perenoschiki infektsii (Ixodid Mites—Parasites and Vectors of Diseases), St. Petersburg: Nauka, 1998.

    Google Scholar 

  4. Berman, D.I. and Leirikh, A.N., The ability of the earthworm Eisenia nordenskioldi (Eisen) (Lumbricidae, Oligochaeta) to endure subfreezing temperatures // Doklady Biological Sciences, Proceedings of the Academy of Sciences of the USSR. Biol. Sci. Sections, 1985, vol. 285, no. 1–6, pp. 845–848.

  5. Berman, D.I. and Leirikh, A.N., Factors affecting the population dynamics of Acridoidea (Orthoptera: Insecta) of North-East Asia, in Populyatsionnaya ekologiya zhivotnykh. Materialy Mezhdunar. konf. “Problemy populyatsionnoi ekologii zhivotnykh” (Population Ecology of Animals: Proc. Int. Conf. “The Problems of Population Ecology of Animals”), Tomsk: Tomsk. Gos. Univ., 2006, pp. 275–277.

  6. Berman, D.I., Budarin, A.M., and Kritskaya, I.G., The fauna and spatial distribution of orthopterans of the continental regions of the North-East of the USSR, in Biologicheskie problemy Severa. Tez. X Vsesoyuz. Simpoz. (Biological Problems of the North: Proc. X All-Union Symp.), Magadan, 1983, part 2, pp. 345–346.

  7. Berman, D.I., Zhigul’skaya, Z.A., and Leirikh, A.N., Biotopic distribution and cold hardiness of Formica exsecta (Formicidae) in the northeastern boundary of the range (upper reaches of the Kolyma River), Byull. Mosk. Obshch. Ispytat. Prirody, Otd. Biol., 1984, vol. 89, no. 3, pp. 47–63.

    Google Scholar 

  8. Berman, D.I., Leirikh, A.N., and Yakimchuk, N.V., Wintering and related biological characteristics of Tetrix fuliginosa (Orthoptera, Tetrigidae) in the Northeast of the USSR, Zool. Zh., 1989, vol. 68, no. 9, pp. 86–95.

    Google Scholar 

  9. Berman, D.I., Alfimov, A.V., and Leirikh, A.N., Wintering conditions and cold-resistance of the amphipod Traskorchestia ditmari on the coast of the Sea of Okhotsk // The Soviet Journal of Marine Biology, 1991, pp. 267–271.

  10. Berman, D.I., Meshcheryakova, E.N., Alfimov, A.V., and Leirikh, A.N., The distribution of the earthworm Dendrobaena octaedra (Lumbricidae: Oligochaeta) in the north of the Holarctic is limited by its insufficient frost hardiness, Zool. Zh., 2002, vol. 81, no. 10, pp. 1210–1221.

    Google Scholar 

  11. Berman, D.I., Alfimov, A.V., Zhigul’skaya, Z.A., and Leirikh, A.N., Overwintering and Cold-Hardiness of Ants in the Northeast of Asia, Sofia-Moscow: Pensoft, 2010.

    Google Scholar 

  12. Berman, D.I., Meshcheryakova, E.N., Leirikh, A.N., and Kurenshchikov, D.K., Geographic range and cold hardiness of the earthworm Drawida ghilarovi (Oligochaeta, Moniligastridae), Biol. Bull. (Moscow), 2010a, vol. 37, no. 9, pp. 895–904.

    Article  Google Scholar 

  13. Berman, D.I., Meshcheryakova, E.N., and Leirikh, A.N., Cold hardiness, adaptive strategies, and invasion of slugs of the genus Deroceras (Gastropoda, Pulmonata) in Northeastern Asia, Biol. Bull. (Moscow), 2011, vol. 38, no. 8, pp. 765–778.

    Article  Google Scholar 

  14. Berman, D.I., Leirikh, A.N., and Zhigul’skaya, Z.A., A common strategy of cold hardiness in ants of the genus Myrmica (Formicidae, Hymenoptera) in Northeast Asia // Entomological Review, 2012, vol. 92, no. 3, pp. 247–261.

    Article  Google Scholar 

  15. Berman, D.I., Leirikh, A.N., and Bessolitzina, E.P., Three strategies of cold tolerance in click beetles (Coleoptera, Elateridae), Dokl. Biol. Sci., 2013, vol. 450, pp. 168–172.

    Article  CAS  PubMed  Google Scholar 

  16. Berman, D.I., Meshcheryakova, E.N., and Mikhaljova, E.V., Cold hardiness and range of the myriapod Angarozonium amurense (Polyzoniidae, Diplopoda, Arthropoda) in permafrost environments, CryoLetters, 2015, vol. 36, no. 4, pp. 237–242.

    CAS  PubMed  Google Scholar 

  17. Canal, J., Delatre, J., and Gilard, M.L., Acquistisus nouvelles dans le dosage des lipids totaux de serum: description d’une methode nephelometruqui, Ann. Biol. Clin., 1972, vol. 30, no. 4, pp. 325–332.

    CAS  Google Scholar 

  18. Danks, H.V., Key themes in the study of seasonal adaptations in insects. I. Patterns of cold hardiness, Appl. Entomol. Zool., 2005, vol. 40, no. 2, pp. 199–211.

    Article  Google Scholar 

  19. Gornye tundry khrebta Bol’shoi Annachag (verkhov’e Kolymy) (Mountain Tundras of the Bol’shoi Annachag Ridge (Upper Reaches of the Kolyma River)), Vladivostok: Dal’nevost. Nauch. Tsentr Akad. Nauk SSSR, 1980.

  20. Hao, S.G. and Kang, L., Supercooling capacity and cold hardiness of the eggs of the grasshopper Chorthippus fallax (Orthoptera: Acrididae), Eur. J. Entomol., 2004, vol. 101, pp. 231–236.

    Article  Google Scholar 

  21. Hara, A. and Radin, N.S., Lipid extraction of tissues with a low toxicity solvent, Anal. Biochem., 1978, vol. 90, pp. 420–426.

    Article  CAS  PubMed  Google Scholar 

  22. Holmstrup, M., Polyol accumulation in earthworm cocoons induced by dehydration, Comp. Biochem. Physiol., 1995, vol. 111A, no. 2, pp. 251–255.

    Article  CAS  Google Scholar 

  23. Holmstrup, M. and Westh, P., Dehydration of earthworm cocoons exposed to cold: a novel cold hardiness mechanism, J. Comp. Physiol. B, 1994, vol. 164, pp. 312–315.

    Article  Google Scholar 

  24. Holmstrup, M. and Zachariassen, K.E., Physiology of cold hardiness in earthworms, Comp. Biochem. Physiol., 1996, vol. 115A, no. 2, pp. 91–101.

    Article  CAS  Google Scholar 

  25. Leirikh, A.N., Cold hardiness of the arctic ensign scale Arctorthezia cataphracta (Homoptera, Coccinea: Ortheziidae) in the Northeast of Asia, Entomological Review, 2015, vol. 95, no. 8, pp. 1061–1065.

    Article  Google Scholar 

  26. Leirikh, A.N. and Meshcheryakova, E.N., Methods for the study of cold hardiness of invertebrates, Zool. Zh., 2015, vol. 94, no. 8, pp. 972–984.

    Google Scholar 

  27. Leirikh, A.N., Meshcheryakova, E.N., and Berman, D.I., Mechanisms and ecological implications of cold hardiness in cocoons of the Earthworm Dendrobaena octaedra (Lumbricidae, Oligochaeta), Entomological Review, 2005, vol. 85, suppl. 2, pp. S220–S227.

    Google Scholar 

  28. Leirikh, A.N., Meshcheryakova, E.N., Kuz’minykh, G.V., and Kurenshchikov, D.K., Cold hardiness and development rate as elements of adaptive strategies of phalangiid harvestmen (Opiliones, Phalangiidae) in Northeastern Asia, Entomological Review, 2009, vol. 89, no. 3, pp. 323–331.

    Article  Google Scholar 

  29. Low Temperature Biology of Insects, Denlinger, D.L. and Lee, R.E., Eds., New York: Cambridge Univ. Press, 2010.

    Google Scholar 

  30. Meshcheryakova, E.N. and Berman, D.I., The cold hardiness and geographic distribution of earthworms (Oligochaeta, Lumbricidae, Moniligastridae), Entomological Review, 2014, vol 94, no. 4, pp. 486–497.

    Article  Google Scholar 

  31. Mikhaljova, E.V. and Marusik, Yu.M., New data on taxonomy and fauna of the millipedes (Diplopoda) from the Russian Far East, Siberia and Mongolia, Far East. Entomol., 2004, no. 133, pp. 1–12.

  32. Miller, K., Cold-hardiness strategies of some adult and immature insects overwintering in interior Alaska, Comp. Biochem. Physiol., 1982, vol. 73A, no. 4, pp. 595–604.

    Article  CAS  Google Scholar 

  33. Mosin, A.F. and Petrova, K.M., Some biochemical and hematological parameters in voles and lemmings in normal state and in starvation, in Ekologiya mlekopitayushchikh Severo-Vostochnoi Sibiri (Ecology of Mammals of Northeastern Siberia), Moscow: Nauka, 1980, pp. 90–97.

    Google Scholar 

  34. Poyas redkolesii verkhovii Kolymy (raion stroitel’stva Kolymskoi GES) (The Sparse Forest Belt of the Upper Reaches of the Kolyma River (the Kolyma HPP Construction Area)), Vladivostok: Dal’nevost. Nauch. Tsentr Akad. Nauk SSSR, 1985.

  35. Prozorova, L.A. and Kavun, K.V., New species of terrestrial malacofauna of Southeastern Siberia and the Far East, in Bioraznoobrazie ekosistem Vnutrennei Azii: Tezisy Vserossiiskoi konferentsii s mezhdunarodnym uchastiem Ulan-Ude (Rossiya), 5–10 sentyabrya 2006 g. (Biodiversity of Ecosystems of Inner Asia: Proc. All-Russia Conf. with Int. Particip. Ulan-Ude (Russia), September 5–10, 2006), Ulan-Ude: Buryat. Nauch. Tsentr Sib. Otd. Ross. Akad. Nauk, 2006, vol. 1, pp. 167–168.

  36. Pryce, Y.D., A simple, rapid method for determining glucose in blood of plasma, Analyst, 1967, vol. 92, no. 1092, p. 198.

    Article  CAS  Google Scholar 

  37. Shekhovtsov, S.V., Berman, D.I., and Pel’tek, S.E., Phylogeography of the earthworm Eisenia nordenskioldi nordenskioldi (Lumbricidae, Oligochaeta) in northeastern Eurasia, Dokl. Biol. Sci., 2015, vol. 461, no. 1, pp. 85–88.

    Article  CAS  PubMed  Google Scholar 

  38. Sinclair, B.J., Insect cold tolerance: how many kinds of frozen?, Eur. J. Entomol., 1999, vol. 96, no. 2, pp. 157–164.

    Google Scholar 

  39. Vaskovsky, V.E. and Isay, S.V., Quantitative determination of formaldehyde liberated with periodate oxidation, Anal. Biochem., 1969, vol. 30, pp. 25–31.

    Article  CAS  PubMed  Google Scholar 

  40. Zambin, I., The cold hardiness of the Asiatic locust eggs, Zashch. Rast., 1939, vol. 19, pp. 48–56.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors are grateful to their colleagues in the laboratory A.V. Alfimov, A.P. Bel’ger, Z.A. Zhigul’skaya, G.V. Kuz’minykh, E.N. Meshcheryakova, and A.A. Poploukhin for many years of fruitful cooperation. We are grateful to all specialists who assisted in determining the species and unselfishly shared knowledge on the biology of the objects studied: E.P. Bessolitzina, L.L. Budnikova, Т.S. Vsevolodova-Perel’, E.M. Dantzig, N.T. Zalesskaya, I.G. Kritskaya, L.A. Prozorova, and Ya.I. Starobogatov.

This study was supported by the Russian Foundation for Basic Research (project nos. 01-04-48921-а, 04-04-48187-а, 07-04-00362-а, 07-04-07028-d, 10-04-00425-а, 13-04-00156-а, and 16-04-00082-а).

Author information

Authors and Affiliations

  1. Institute of Biological Problems of the North, Far East Branch, Russian Academy of Sciences, 685000, Magadan, Russia

    D. I. Berman & A. N. Leirikh

Authors
  1. D. I. Berman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. N. Leirikh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. I. Berman.

Additional information

Translated by N. Smolina

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berman, D.I., Leirikh, A.N. Cold Hardiness of Mass Soil Invertebrate Animals of Northeastern Asia: 1. Cold Hardiness and the Mechanisms of Its Maintenance. Biol Bull Russ Acad Sci 45, 669–679 (2018). https://doi.org/10.1134/S1062359018070038

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062359018070038

Keywords:

Search

Navigation