Digestive enzymes in Rhinolophus euryale (Rhinolophidae, Chiroptera) are active also during hibernation

Open access


During the winter, bats use hibernation as a means of surviving the period of low prey offer. However, the Mediterranean horseshoe bat (Rhinolophus euryale) arouses from torpor quite frequently. Based on the actual climatic conditions, it can profit from occasional foraging oportunities, when they occur. We analysed faeces collected on four nights during the period from November 2012 to February 2013 from the Domica-Baradla cave system (Slovakia and Hungary). In mid-November, the largest proportion of faecal contents were from Lepidoptera. Later on, the proportion of non-consumptive mass in the faeces increased and prey remnants disappeared. We analysed the activity of digestive enzymes (amylase, chitobiase, endochitinase and glukosaminidase) in faeces. The activity of these enzymes was detected in fresh faeces throughout the whole winter. The faecal activity of the chitinases was relatively stable during the monitored period, whilst the activity of amylase was highest during late November and December. Some level of active digestive enzymes during the winter could be an adaptation to occasional winter foraging.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Avery M.I. (1985) Winter activity of pipistrelle bats. Journal of Animal Ecology 54 721-738.

  • Balslev-Clausen A. McCarthy J.M. & Carey H.V. (2003) Hibernation reduces pancreatic amylase levels in ground squirrels. Comparative Biochemistry and Physiology-Part A: Molecular & Integrative Physiology 134(3) 573-578.

  • Bauman W.A. (1990) Seasonal changes in pancreatic insulin and glucagon in the little brown bat (Myotis lucifugus). Pancreas 5(3) 342-346.

  • Bauman W.A. Meryn S. & Florant G. (1987) Pancreatic hormones in the nonhibernating and hibernating golden mantled ground squirrel. Comparative Biochemistry and Physiology Part A: Physiology 86(2) 241-244.

  • Boot R.G. Blommaart E.F.C. Swart E. van der Vlugt K.G. Bijl N. Moe C. et al. (2001) Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. The Journal of Biological Chemistry 276 6770-6778.

  • Boot R.G. Bussink A.P. Verhoek M. De Boer P.A. Moorman A.F. & Aerts J.M. (2005) Marked differences in tissue-specific expression of chitinases in mouse and man. Journal of Histochemistry & Cytochemistry 53(10) 1283-1292.

  • Bradford M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72(1-2) 248-254.

  • van Breukelen F. & Martin S.L. (2001) Translational initiation is uncoupled from elongation at 18 °C during mammalian hibernation. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 281(5) R1374-R1379.

  • van Breukelen F. & Martin S.L. (2002) Reversible depression of transcription during hibernation. Journal of Comparative Physiology B 172(5) 355-361.

  • Brigham R.M. (1987) The significance of winter activity by the big brown bat (Eptesicus fuscus): the influence of energy reserves. Canadian Journal of Zoology 65(5) 1240-1242.

  • Buchholz R.H. (1958) Digestive enzymes of the mole bat and rat. Journal of Mammalogy 39 452-453.

  • Dunbar M.B. & Tomasi T.E. (2006) Arousal patterns metabolic rate and an energy budget of eastern red bats (Lasiurus borealis) in winter. Journal of Mammalogy 87(6) 1096-1102.

  • Encarnação J.A. & Dietz M. (2006) Estimation of food intake and ingested energy in Daubenton’s bats (Myotis daubentonii) during pregnancy and spermatogenesis. European Journal of Wildlife Research 52 221-227.

  • Eurich K. (2009) Potential role of chitinase 3-like-1 in inflammation-associated carcinogenic changes of epithelial cells. World Journal of Gastroenterology 15 5249-5249.

  • Gaál Ľ. & Gruber P. (eds.) (2014) Jaskynný systém Domica-Baradla. Jaskyňa ktorá nás spája [anglický preklad]. Správa Aggtelekského národného parku Jósvafő 512 pp.

  • Hope P.R. Bohmann K. Gilbert M.T.P. Zepeda-Mendoza M.L. Razgour O. & Jones G. (2014) Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera Vespertilionidae) in winter. Frontiers in Zoology 11(1) 39.

  • Chinery M. (1977) A field guide to the insects of Britain and northern Europe. London: Collins 402 pp.

  • Janeček Š. (1997) α-amylase family: molecular biology and evolution. Progress in Biophysics & Molecular Biology 67 67-97.

  • Jeuniaux C. (1961) Chitinase: an addition to the list of hydrolases in the digestive tract of vertebrates. Nature 192 135-136.

  • Jonasson K.A. & Willis C.K. (2012) Hibernation energetics of free-ranging little brown bats. Journal of Experimental Biology 215(12) 2141-2149.

  • Klite P.D. (1965) Intestinal bacterial flora and transit time of three neotropical bat species. Journal of Bacteriology 90(2) 375-379.

  • Malatesta M. Zancanaro C. Marcheggiani F. Cardinali A. Rocchi M.B. Capizzi D. et al. (1998) Ultrastructural morphometrical and immunocytochemical analyses of the exocrine pancreas in a hibernating dormouse. Cell and Tissue Research 292(3) 531-541.

  • Maxinová E. Arrizabalaga A. Arriolabengoa M. Aloria K. Zaldibar B. Boldogh S. et al. (2017) Faeces of Rhinolophus euryale (Chiroptera) from winter season contain inorganic matter. Hystrix Italian Journal of Mammalogy in press.

  • McAney C. Shiel C. Sullivan C. & Fairley J. (1991) The analysis of bat droppings [An occasional publication of the mammal society no. 14]. The Mammal Society London 48 pp.

  • Miková E. Varcholová K. Boldogh S. & Uhrin M. (2013) Winter diet analysis in Rhinolophus euryale (Chiroptera). Central European Journal of Biology 8(9) 848-853.

  • Park H. & Hall E.R. (1951) The gross anatomy of the tongues and stomachs of eight new world bats. Transactions of the Kansas Academy of Science 54 64-72.

  • Ransome R.D. (1968) The distribution of the greater horse‐shoe bat Rhinolophus ferrumequinum during hibernation in relation to environmental factors. Journal of Zoology 154(1) 77-112.

  • Ransome R.D. (1971) The effect of ambient temperature on the arousal frequency of the hibernating greater horseshoe bat Rhinolophus fermmequinum in relation to site selection and the hibernation state. Journal of Zoology 164(3) 353-371.

  • Roswag A. Becker N.I. & Encarnação J.A. (2012) Inter‐ and intraspecific comparisons of retention time in insectivorous bat species (Vespertilionidae). Journal of Zoology 288(2) 85-92.

  • Stevens C.E. (1988) Comparative physiology of the vertebrate digestive system. Cambridge: Cambridge University Press 405 pp.

  • Strobel S. Roswag A. Becker N.I. Trenczek T.E. & Encarnação J.A. (2013) Insectivorous bats digest chitin in the stomach using acidic mammalian chitinase. PloS One 8(9) e72770.

  • Sugita H. Kumazawa J. & Deguchi Y. (1996) Production of chitinase and beta-N-acetylglucosamindase by intestinal bacteria of Pinnipedian animals. Letters in Applied Microbiology 23 275-278.

  • Šimůnek J. Hodrová B. Bartoňová H. & Kopečný J. (2001) Chitinolytic bacteria of the mammal digestive tract. Folia Microbiologica 46 76-78.

  • Thomas D.W. & Cloutier D. (1992) Evaporative water loss by hibernating little brown bats Myotis lucifugus. Physiological Zoology 65(2) 443-456.

  • Thomas D.W. Dorais M. & Bergeron J.M. (1990) Winter energy budgets and cost of arousals for hibernating little brown bats Myotis lucifugus. Journal of Mammalogy 71(3) 475-479.

  • Thomas D.W. & Geiser F. (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved?. Functional Ecology 11(5) 585-591.

  • Uhrin M. Boldogh S. Bücs S. Paunović M. Miková E. Juhász M. et al. (2012) Revision of the occurrence of Rhinolophus euryale in the Carpathian region Central Europe. Vespertilio 16 289-328.

  • Webb J. Speakman R. & Racey P.A. (1993) Defecation apparent absorption efficiency and the importance of water obtained in the food for water balance in captive brown long-eared (Plecotus auritus) and Daubenton’s (Myotis daubentoni) bats. Journal of Zoology 230 619-628.

  • Whitaker J.O. Jr. Dannelly H.K. & Prentice D.A. (2004) Chitinase in insectivorous bats. Journal of Mammalogy 85 15-18.

  • Whitaker J.O.Jr. McCracken G.F. & Siemers B.M. (2009) Food habits analysis of insectivorous bats. Pp.: 567-592. In: Kunz T. H. & Parsons S. (eds): Ecological and behavioral methods for the study of bats. Baltimore: The Johns Hopkins University Press xvii & 901 pp.

  • Williams C. Salter L. & Jones G. (2010) The winter diet of the lesser horseshoe bat (Rhinolophus hipposideros) in Britain and Ireland. Hystrix Italian Journal of Mammalogy 22(1) 159-166.

  • Zahn A. & Kriner E. (2016) Winter foraging activity of Central European Vespertilionid bats. Mammalian Biology 81(1) 40-45.

Journal information
Impact Factor

CiteScore 2018: 0.84

Source Normalized Impact per Paper (SNIP) 2018: 0.365

Cited By
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 342 105 7
PDF Downloads 188 65 4