Skip to main content
SpringerLink
Log in

Seasonal Changes in Body Mass and Activity of Digestive Enzymes in Eptesicus nilssonii (Mammalia: Chiroptera: Vespertilionidae) during Hibernation

  • Experimental Papers
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

Hibernation can be considered as a circannual cycle of feeding and fasting. During winter, the absence of dietary substrates in fat-storing hibernators leads to a reduction in the mass of fats and digestive organs. We examined the seasonal changes in body mass and activity of digestive enzymes in the pancreas and small intestine of the torpid Eptesicus nilssonii (Keyserling & Blasius, 1839). Adult females and males were captured in autumn (November, early hibernation), winter (February, mid-hibernation) and spring (March–April, late hibernation) in northwestern Russia (Republic of Karelia). Our findings indicated that male and female E. nilssonii reduced body mass during hibernation, but females exhibited a slower decline in body mass during hibernation period than males. No significant differences in the activity of digestive enzymes were found between males and females. Pancreatic protease activity was the highest in autumn, decreased in the mid-hibernation season, and remained low during hibernation of E. nilssonii. There was no difference in the activity of amylase and lipase in the pancreas among all periods of hibernation. However, the activity of protease, amylase and lipase in small intestine was higher before the emergence from hibernation in spring than during autumn. This study provides new information of the maintenance of intestinal hydrolytic enzyme activity after months of fasting. E. nilssonii, a fat-storing hibernator, appears to maintain a digestive function during the hibernation season, apparently to allow efficient absorption of nutrients that are ingested after terminal arousal in the spring.

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.

Similar content being viewed by others

REFERENCES

  1. Mohr SM, Bagriantsev SN, Gracheva EO (2020) Cellular, molecular, and physiological adaptations of hibernation: the solution to environmental challenges. Annual Review of Cell and Developmental Biology 36: 315–338. https://doi.org/10.1146/annurev-cellbio-012820-095945

    Article  CAS  PubMed  Google Scholar 

  2. Kurtz CC, Otis JP, Regan MD, Carey HV (2021) How the gut and liver hibernate. Comparative Biochemistry and Physiology—Part A: Molecular and Integrative Physiology 253: 110875. https://doi.org/10.1016/j.cbpa.2020.110875

    Article  CAS  PubMed  Google Scholar 

  3. Giroud S, Habold C, Nespolo RF, Mejías C, Terrien J, Logan SM, Henning RH, Storey KB (2021) The Torpid state: recent advances in metabolic adaptations and protective mechanisms. Frontiers in Physiology 11: 623665. https://doi.org/10.3389/fphys.2020.623665

    Article  PubMed  PubMed Central  Google Scholar 

  4. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiological Reviews 83(4): 1153–1181. https://doi.org/10.1152/physrev.00008.2003

    Article  CAS  PubMed  Google Scholar 

  5. Carey HV (1990) Seasonal changes in mucosal structure and function in ground squirrel intestine. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 259: 385–392. https://doi.org/10.1152/ajpregu.1990.259.2.R385

    Article  Google Scholar 

  6. Hume D, Beiglböck C, Ruf T, Frey-Roos F, Bruns U, Arnold W (2002) Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). Journal of Comparative Physiology B 172(3): 197–207. https://doi.org/10.1007/s00360-001-0240-1

    Article  CAS  Google Scholar 

  7. Balslev-Clausen A, McCarthy JM, Carey HV (2003) Hibernation reduces pancreatic amylase levels in ground squirrels. Comparative Biochemistry and Physiology – Part A 134: 573–578. https://doi.org/10.1016/s1095-6433(02)00363-x

    Article  Google Scholar 

  8. Maxinová E, Sustr V, Uhrin M (2017) Digestive enzymes in Rhinolophus euryale (Rhinolophidae, Chiroptera) are active also during hibernation. European Journal of Ecology 3(1): 91–96. https://doi.org/10.1515/eje-2017-0010

    Article  Google Scholar 

  9. Carey HV, Martin SL(1996) Preservation of intestinal gene expression during hibernation. American Journal of Physiology Gastrointestinal and Liver Physiology 271: G805–G813. https://doi.org/10.1152/ajpgi.1996.271.5.G805

    Article  CAS  Google Scholar 

  10. Buchholz R, Wells P, Conaway C (1958) Digestive enzymes of mole, bat and rat. Journal of Mammalogy 39(3): 452–454. https://doi.org/10.2307/1376175

    Article  Google Scholar 

  11. Belkin VV, Fyodorov FV, Ilyukha VA, Yakimova AE (2021) Characteristics of the bat (Chiroptera) population in protected areas in the northern and middle taiga subzones of European Russia. Nature Conservation Research 6: 17–31. https://doi.org/10.24189/ncr.2021.002

    Article  Google Scholar 

  12. Siivonen Y, Wermundsen T (2008) Characteristics of winter roosts of bat species in southern Finland. Mammalia 72: 50–56. https://doi.org/10.1515/MAMM.2008.003

    Article  Google Scholar 

  13. Belkin VV, Panchenko DV, Tirronen KF, Yakimova AE, Fedorov FV (2015) Ecological status of bats (Chiroptera) in winter roosts in Eastern Fennoscandia. Russian Journal of Ecology 46: 463–469. https://doi.org/10.1134/S1067413615050045

    Article  Google Scholar 

  14. Anufriev AI, Revin YV (2006) Bioenergetics of hibernating bats (Chiroptera, Vespertilionidae) in Yakutia. Plecotus et al 9: 8–17.

    Google Scholar 

  15. Blomberg AS, Vasko V, Meierhofer MB, Johnson JS, Eeva T, Lilley TM (2021) Winter activity of boreal bats. Mammalian Biology 101: 609–618. https://doi.org/10.1007/s42991-021-00111-8

    Article  Google Scholar 

  16. Jonasson KA, Willis CK (2011) Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PloS one 6(6): e21061. https://doi.org/10.1371/journal.pone.0021061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wang X, Magkos F, Mittendorfer B (2011) Sex differences in lipid and lipoprotein metabolism: it’s not just about sex hormones. The Journal of Clinical Endocrinology & Metabolism 96: 885–893. https://doi.org/10.1210/jc.2010-2061

    Article  CAS  Google Scholar 

  18. Ploskey GR, Sealander JA (1979) Lipid deposition and withdrawal before and during hibernation in Pipistrellus subflavus (Chiroptera: Vespertilionidae). The Southwestern Naturalist 24: 71–78. https://doi.org/10.2307/3670626

    Article  Google Scholar 

  19. Beer JR, Richards AG (1956) Hibernation of the big brown bat. Journal of Mammalogy 37: 31–41.

    Article  Google Scholar 

  20. Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in Mammalian hibernation: a cost-benefit approach. Physiological and Biochemical Zoology 76(2): 165–179. https://doi.org/10.1086/367950

    Article  PubMed  Google Scholar 

  21. Kunz TH, Wrazen JA, Burnett CD (1998) Changes in body mass and fat reserves in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5: 8–17. https://doi.org/10.1080/11956860.1998.11682443

    Article  Google Scholar 

  22. Racey PA, Swift SM (1981) Variations in gestation length in a colony of pipistrelle bats (Pipistrellus pipistrellus) from year to year. Journal of Reproduction and Fertility 61(1): 123–9. https://doi.org/10.1530/jrf.0.0610123

    Article  CAS  PubMed  Google Scholar 

  23. Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, Vodzak ME, Darling SR, Stihler CW, Hicks AC, Jacob R, Grieneisen LE, Brownlee SA, Muller LK, Blehert DS (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One 7(6): e38920. https://doi.org/10.1371/journal.pone.0038920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Turner JM, Warnecke L, Wilcox A, Baloun D, Bollinger TK, Misra V, Willis CK (2015) Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. Physiology & Behavior 140: 71–78. https://doi.org/10.1016/j.physbeh.2014.12.013

    Article  CAS  Google Scholar 

  25. Mayberry HW, McGuire LP, Willis CKR (2018) Body temperatures of hibernating little brown bats reveal pronounced behavioural activity during deep torpor and suggest a fever response during white-nose syndrome. Journal of Comparative Physiology B 188(2): 333–343. https://doi.org/10.1007/s00360-017-1119-0

    Article  CAS  Google Scholar 

  26. Bauman WA (1990) Seasonal changes in pancreatic insulin and glucagon in the little brown bat (Myotis lucifugus). Pancreas 5: 342–346. https://doi.org/10.1097/00006676-199005000-00015

    Article  CAS  PubMed  Google Scholar 

  27. Bauman WA, Meryn S, Florant GL (1987) Pancreatic hormones in the nonhibernating and hibernating golden mantled ground squirrel. Comparative Biochemistry and Physiology—Part A 86: 241–244. https://doi.org/10.1016/0300-9629(87)90324-0

    Article  CAS  Google Scholar 

  28. Macrae JC, Lobley GE, Lobley GE (2003) Protein turnover—what does it mean for animal production? Canadian Journal of Animal Science 83: 327–340. https://doi.org/10.4141/A03-019

    Article  Google Scholar 

  29. Malatesta M, Zancanaro C, Marcheggiani F, Cardinali A, Rocchi MBL, Capizzi D, Vogel P, Fakan S, Gazzanelli G (1998) Ultrastructural, morphometrical and immunocytochemical analyses of the exocrine pancreas in a hibernating dormouse. Cell and Tissue Research 292: 531–541. https://doi.org/10.1046/j.0021-8782.2002.00103.x

    Article  CAS  PubMed  Google Scholar 

  30. Buck MJ, Squire TL, Andrews MT (2002) Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiological Genomics 8: 5–13. https://doi.org/10.1152/physiolgenomics.00076.2001

    Article  CAS  PubMed  Google Scholar 

  31. Price ER, Brun A, Caviedes-Vidal E, Karasov WH (2015) Digestive adaptations of aerial lifestyles. Physiology (Bethesda) 30(1): 69–78. https://doi.org/10.1152/physiol.00020.2014

  32. Karasov WH, Caviedes-Vidal E (2021) Adaptation of intestinal epithelial hydrolysis and absorption of dietary carbohydrate and protein in mammals and birds. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 253: 110860. https://doi.org/10.1016/j.cbpa.2020.110860

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The authors express their gratitude to the associates of the Laboratory of ecological physiology of animals (IB FRC KRC), especially to A.V. Morozov, for his assistance in conducting the experiment.

Funding

The research was supported by the state orders (project no. FMEN-2022-0003).

Author information

Authors and Affiliations

  1. Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences, Petrozavodsk, Russia

    E. P. Antonova, V. V. Belkin, V. A. Ilyukha, E. A. Khizhkin & S. N. Kalinina

  2. Petrozavodsk State University, Petrozavodsk, Russia

    E. A. Khizhkin & S. N. Kalinina

Authors
  1. E. P. Antonova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. V. Belkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. A. Ilyukha
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. A. Khizhkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. N. Kalinina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. P. Antonova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

All applicable international, national and institutional principles of handling and using experimental animals for scientific purposes were observed. This study did not involve human subjects as research objects. This study protocol was approved by the Research and Ethical Committee of the Institute of Biology, Karelian Research Centre, RAS.

CONFLICT OF INTEREST

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Antonova, E.P., Belkin, V.V., Ilyukha, V.A. et al. Seasonal Changes in Body Mass and Activity of Digestive Enzymes in Eptesicus nilssonii (Mammalia: Chiroptera: Vespertilionidae) during Hibernation. J Evol Biochem Phys 58, 1055–1064 (2022). https://doi.org/10.1134/S002209302204010X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S002209302204010X

Keywords:

Search

Navigation