Where am I? > Home > Articles > Volume 45
Research article


Snacking during hibernation? Winter bat diet and prey availabilities, a case study from Iskar Gorge, Bulgaria

Nia Toshkova https://orcid.org/0000-0003-4217-5653; Katrin Dimitrova https://orcid.org/0000-0002-1166-7519; Mario Langourov https://orcid.org/0000-0001-6756-3420; Boyan Zlatkov https://orcid.org/0000-0002-5704-1634; Rostislav Bekchiev https://orcid.org/0000-0001-6143-0184; Toshko Ljubomirov https://orcid.org/0000-0002-3202-3309; Eberhard Zielke; Radost Angelova; Rossina Parvanova; Tzvetan Simeonov https://orcid.org/0000-0001-9007-7084; Nikolay Simov https://orcid.org/0000-0003-1626-2964

2 May 2023 · volume 45 · (issue 5) · pp. 125–142 · PDF [full text]

Abstract: Better empirical knowledge of how bat and insect phenology are influenced by seasonal environmental conditions and how this may affect fitness is essential in the face of changing climatic conditions. We examined the winter diet of the Schreibers’ bent-winged bat Miniopterus schreibersii (Kuhl, 1817) from Razhishkata Cave, Balkan Mountains, Bulgaria during four sampling periods in the winter of 2021 (end of January – end of March). We used a combination of DNA metabarcoding and a microscope-based morphological analyses of bats droppings. Additionally, we tracked prey availability in the studied area using insect flight interception traps (FIT). The species was actively feeding outside the cave and did not use the cave fauna. Our samples indicate a shift in the winter diet of the bats throughout the studied periods. Even though Diptera was the most abundant order of insects during two of the study periods, bats were preying predominantly on Lepidoptera and Hymenoptera. The metabarcoding also supported this with data for the presence of insects with diurnal activity in the samples. The temperature loggers showed a strong correlation between the outside temperature and the temperature in the cave where the colony was located, probably impacting the activity patterns of the bats. To our knowledge, this is the first study of winter bat activity and diet in Bulgaria. Our research can serve as a potential framework for studying winter bat activity and insect activity during this sensitive period.

Keywords: bat guano, DNA metabarcoding, insects, Miniopterus schreibersii, winter activity, winter diet

References [67]

Aitchison C.W. 2001 The effect of snow cover on small animals. In: Jones H.G., Pomeroy J., Walker D.A., Hoham R. (eds) Snow ecology. Cambridge University Press, pp. 229–265.
Avery M.I. 1986 Factors affecting the emergence times of Pipistrelle bats. Journal of Zoology 209 (2): 293–296. https://doi.org/10.1111/j.1469-7998.1986.tb03589.x
Badino G. 2004 Cave temperatures and global climatic change. International Journal of Speleology 33 (1): 103–113. https://doi.org/10.5038/1827-806x.33.1.10
Barbu P. 1958 Contributii la studiul monografic al lui Miniopterus schreibersi Kuhl. Nota I. Curbele de frecventă în biometria lui Miniopterus schreibersi Kuhl și cîteva observatii biologice. Studii şi cercetări de biologie. Seria “biologie animală” 10 (2): 145–161.
Barros P.A., Ribeiro C., Cabral J.A. 2017 Winter activity of bats in Mediterranean peri-urban deciduous forests. Acta Chiropterologica 19 (2): 367–377. https://doi.org/10.3161/15081109acc2017.19.2.013
Beron P. 2015 Cave fauna of Bulgaria. East-West Publishing, Sofia, 434 pp.
Bouchard Jr R.W., Ferrington Jr L.C. 2009 Winter Growth, Development, and Emergence of Diamesa mendotae (Diptera: Chironomidae) in Minnesota Streams. Environmental Entomology 38 (1): 250–259. https://doi.org/10.1603/022.038.0131
Boyles J.G., Dunbar M.B., Whitaker Jr J.O. 2006 Activity following arousal in winter in North American vespertilionid bats. Mammal Review 36 (4): 267–280. https://doi.org/10.1111/j.1365-2907.2006.00095.x
Buck C.L., Barnes B.M. 2000 Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 279 (1): 255–262. https://doi.org/10.1152/ajpregu.2000.279.1.R255
Danks H.V. 1971 Overwintering of some north temperate and Arctic Chironomidae: II. Chironomid biology. The Canadian Entomologist 103 (12): 1875–1910. https://doi.org/10.4039/ent1031875-12
Deleva S., Toshkova N., Kolev M., Tanalgo K.C. 2023 Important underground roosts for bats in Bulgaria: current state and priorities for conservation. Biodiversity Data Journal 11: e98734. https://doi.org/10.3897/bdj.11.e98734
Dietz Ch., von Helversen O., Nill D. 2009 Bats of Britain, Europe and Northwest Africa. A and C Black Publishers, London, 400 pp.
Gazaryan S., Bücs S., Çoraman E. 2020 Miniopterus schreibersii (errata version published in 2021). The IUCN Red List of Threatened Species 2020: eT81633057A195856522. https://doi.org/10.2305/iucn.uk.2020-2.rlts.t81633057a195856522.en
Geiser F. 2004 Metabolic rate and body temperature reduction during hibernation and daily torpor. Annual Review of Physiology 66: 239–274. https://doi.org/10.1146/annurev.physiol.66.032102.115105
Hausmann A., Godfray H.C.J., Huemer P., Mutanen M., Rougerie R., van Nieukerken E.J., Ratnasingham S., Hebert P.D.N. 2013 Genetic Patterns in European Geometrid Moths Revealed by the Barcode Index Number (BIN) System. PLoS ONE 8 (12): e84518. https://doi.org/10.1371/journal.pone.0084518
Hausmann A., Segerer A.H., Greifenstein T., Knubben J., Morinière J., Bozicevic V., Doczkal D., Günter A., Ulrich W., Habel J.C. 2020 Toward a standardized quantitative and qualitative insect monitoring scheme. Ecology and evolution 10 (9): 4009–4020. https://doi.org/10.1002/ece3.6166
Hays G.C., Speakman J.R., Webb P.I. 1992 Why do brown long-eared bats (Plecotus auritus) fly in winter? Physiological Zoology 65 (3): 554–567.
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 (39): 1–15. https://doi.org/10.1186/1742-9994-11-39
Humphries M.M., Speakman J.R., Thomas D.W., Zubaid A., McCracken G.F., Kunz T.H. 2006 Functional and evolutionary ecology of bats. Oxford University Press. 341 pp.
Hågvar S. 2001 Occurrence and migration on snow, and phenology of egg-laying in the winter-active insects Boreus sp. (Mecoptera). Norwegian Journal of Entomology 48: 51–60.
Hågvar S. 2007 Why do some Psylloidea and Heteroptera occur regularly on snow? Norwegian Journal of Entomology 54: 3–9.
Hågvar S. 2010 A review of Fennoscandian arthropods living on and in snow. European Journal of Entomology 107 (3): 281–298. https://doi.org/10.14411/eje.2010.037
Hågvar S., Aakra K. 2006 Spiders active on snow in Southern Norway. Norwegian Journal of Entomology 53: 71–82.
Hågvar S., Greeve L. 2003 Winter active flies (Diptera, Brachycera) recorded on snow – a long-term study in south Norway. Studia Dipterologica 10: 401–421.
Hågvar S., Krzeminska E. 2007 Contribution to the winter phenology of Trichoceridae (Diptera) in snow-covered southern Norway. Studia Dipterologica 14: 271–283.
Ivanova T. 2005 Important Bat Underground Habitats (IBUH) in Bulgaria. Acta zoologica bulgarica 57 (2): 197–206.
Jaskuła R., Soszyńska-Maj A. 2011 What do we know about winter active ground beetles (Coleoptera, Carabidae) in Central and Northern Europe? In: Kotze D.J., Assmann T., Noordijk J., Turin H., Vermeulen R. (eds) Carabid Beetles as Bioindicators: Biogeographical, Ecological and Environmental Studies. ZooKeys 100: 517–532. https://doi.org/10.3897/zookeys.100.1543
Jones G., Jacobs D.S., Kunz T.H., Willig M.R., Racey P.A. 2009 Carpe noctem: the importance of bats as bioindicators. Endangered Species Research 8 (1–2): 93–115. https://doi.org/10.3354/esr00182
Kanuch P., Janeckova K., Kristin A. 2005 Winter diet of the noctule bat Nyctalus noctula. Folia Zoologica 54: 53–60.
Kovtun M.F., Zhukova N.F. 1994 Feeding and digestion intensity in chiropterans of different trophic groups. Folia Zoologica 43 (4): 377–386.
Langourov M. 2004 Scuttle flies (Diptera: Phoridae) from Eastern Rhodopes (Bulgaria) with special consideration of winter-active species. In: Beron P., Popov A. (eds) Biodiversity of Bulgaria. 2. Biodiversity of Eastern Rhodopes (Bulgaria and Greece). Pensoft and National Museum of Natural History, Sofia, pp. 759–768.
Leray M., Yang J.Y., Meyer C.P., Mills S.C., Agudelo N., Ranwez V., Boehm J.T., Machida R.J. 2013 A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Frontiers in zoology 10 (1): 1–14. https://doi.org/10.1186/1742-9994-10-34
Lino A., Fonseca C., Goiti U., Pereira M.J.R. 2014 Prey selection by Rhinolophus hipposideros (Chiroptera, Rhinolophidae) in a modified forest in Southwest Europe. Acta Chiropterologica 16 (1): 75–83. https://doi.org/10.3161/150811014x683282
Malmqvist E., Jansson S., Zhu S., Li W., Svanberg K., Svanberg S., Rydell J., Song Z., Bood J., Brydegaard M., Åkesson S. 2018 The bat–bird–bug battle: daily flight activity of insects and their predators over a rice field revealed by high-resolution Scheimpflug Lidar. Royal Society Open Science 5: 172303. https://doi.org/10.1098/rsos.172303
Mas M., Flaquer C., Puig-Montserrat X., Porres X., Rebelo H., López-Baucells A. 2022 Winter bat activity: The role of wetlands as food and drinking reservoirs under climate change. Science of The Total Environment 828: 154403. https://doi.org/10.1016/j.scitotenv.2022.154403
Mata V.A., Rebelo H., Amorim F., McCracken G.F., Jarman S., Beja P. 2019 How much is enough? Effects of technical and biological replication on metabarcoding dietary analysis. Molecular Ecology 28 (2): 165–175. https://doi.org/10.1111/mec.14779
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. https://doi.org/10.2478/s11535-013-0199-9
Mikula P., Morelli F., Lučan R.K., Jones D.N., Tryjanowski P. 2016 Predation of bats by diurnal birds. Mammal Review 46: 160–174. https://doi.org/10.1111/mam.12060
Morinière J., Cancian de Araujo B., Lam A.W., Hausmann A., Balke M., Schmidt S., Hendrich L., Doczkal D., Fartmann B., Arvidsson S., Haszprunar G. 2016 Species identification in malaise trap samples by DNA barcoding based on NGS technologies and a scoring matrix. PLoS ONE 11 (5): e0155497. https://doi.org/10.1371/journal.pone.0155497
Muñoz-Sabater J., Dutra E., Agustí-Panareda A., Albergel C., Arduini G., Balsamo G., Boussetta S., Choulga M., Harrigan S., Hersbach H., Martens B., Miralles D.G., Piles M., Rodríguez-Fernández N.J., Zsoter E., Buontempo C., Thépaut J.-N. 2021 ERA5-Land: a state-of-the-art global reanalysis dataset for land applications. Earth System Science Data 13: 4349–4383. https://doi.org/10.5194/essd-13-4349-2021
Pandurska R.S. 1993 Distribution and species diversity of cave-dwelling bats in Bulgaria and some remarks on the microclimatic conditions of the hibernation. Travaux de l’Institut de Spéologie “Emil Racovitza” 32: 155–163.
Park K.J., Jones G., Ransome R.D. 1999 Winter activity of a population of greater horseshoe bats (Rhinolophus ferrumequinum). Journal of Zoology 248 (4): 419–427. https://doi.org/10.1111/j.1469-7998.1999.tb01041.x
Park K.J., Jones G., Ransome R.D. 2000 Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Functional ecology 14 (5): 580–588. https://doi.org/10.1046/j.1365-2435.2000.t01-1-00460.x
Pavlova A., Stojanova A. 2020 Winter Activity of Fungus Gnats (Diptera: Mycetophilidae) in Critically-endangered Mediterranean Habitats in Bulgaria. Acta zoologica bulgarica, Supplement 15: 129–140.
Popov V., Ivanova T. 2015 Schreiber’s bat, Miniopterus schreibersii (Bonaparte, 1837). In: Golemanski V., Peev D., Chipev N., Beron P., Biserkov V. (eds) Red Data Book of the Republic of Bulgaria. Volume 2. Animals. BAS and MoEW, Sofia, p. 231.
Preselnik P., Aulagnier S. 2013 The diet of Schreiber’s bent-winged bat, Miniopterus schreibersii (Chiroptera: Miniopteridae), in northeastern Slovenia (Central Europe). The Journal Mammalia 77 (3): 297–305. https://doi.org/10.1515/mammalia-2012-0033
Ramløy U.B. 2000 Aspects of natural cold tolerance in ectothermic animals. Human reproduction 15, Supplement 5: 26–46. https://doi.org/10.1093/humrep/15.suppl_5.26
Ratnasingham S., Hebert P.D. 2013 A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8 (7): e66213. https://doi.org/10.1371/journal.pone.0066213
Revilla-Martín N., Budinski I., Puig-Montserrat X., Flaquer C., López-Baucells A. 2021 Monitoring cave-dwelling bats using remote passive acoustic detectors: a new approach for cave monitoring. Bioacoustics 30 (5): 527–542. https://doi.org/10.1080/09524622.2020.1816492
Roué S., Némoz M. 2002 Mortalité exceptionnelle du Minioptère de Schreibers en France lors de l’année 2002: bilan national. Société Française pour l’Etude et la Protection des Mammifères, Paris, 28 pp.
Russo D., Maglio G., Rainho A., Meyer C.F.J., Palmeirim J.M. 2011 Out of the dark: Diurnal activity in the bat Hipposideros ruber on São Tomé island (West Africa). Mammalian Biology 76 (6): 701–708. https://doi.org/10.1016/j.mambio.2010.11.007
Sano A. 2006 Impact of predation by a cave-dwelling bat, Rhinolophus ferrumequinum, on the diapausing population of a troglophilic moth, Goniocraspidum preyeri. Ecological Research 21: 321–324. https://doi.org/10.1007/s11284-005-0122-1
Shiel C., Mcaney C., Sullivan C., Fairley J. 1997 Identification of Arthropod Fragments in Bat Droppings. An Occasional Publication of The Mammal Society 7: 1–56.
Soszyńska-Maj A. 2008 The significance of forest complexes for preservation of snow fauna species diversity of Lodz. In: Indykiewicz P., Jerzak L., Barczak T. (eds) FAUNA MIAST Ochronić różnorodność biotyczną w miastach. SAR “Pomorze”, Bydgoszcz, 78–82.
Soszynska-Maj A., Buszko J. 2011 Lepidoptera recorded on snow in Central Poland. Entomologica Fennica 22: 21–28.
Speakman J.R., Racey P.A. 1989 Hibernal ecology of the pipistrelle bat: energy expenditure, water requirements and mass loss, implications for survival and the function of winter emergence flights. The Journal of Animal Ecology 58 (3): 797–813. https://doi.org/10.2307/5125
Taylor L.R. 1963 Analysis of the effect of temperature on insects flight. Journal of Animal Ecology 32: 99–117.
Thomas D.W. 1995 Hibernating bats are sensitive to nontactile human disturbance. Journal of Mammalogy 76: 940–94.
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.
Vincent S., Nemoz M., Aulagnier S. 2011 Activity and foraging habitats of Miniopterus schreibersii (Chiroptera, Miniopteridae) in southern France: implications for its conservation. Hystrix, the Italian Journal of Mammaliology (n. s.) 22: 57–72. https://doi.org/10.4404/hystrix-22.1-4524
Thomas M.D. 2004 Physiological ecology and energetics of bats. In: Kunz T.H., Fenton M.B. (eds) Bat Biology, pp. 430–490.
Whitaker J.O., Castor L. 2009 Identification of insect parts found in bat guano. In: Kunz T.H., Parsons S. (eds) Ecological and Behavioural Methods for the Study of Bats, 2nd edition. John Hopkins University Press, Baltimore, Maryland, pp. 567–592.
Whitaker J.O., Mccracken G.F., Siemers B.M. 2009 Food habits analysis of insectivorous bats. In: Kunz T.H., Parsons S. (eds) Ecological and Behavioural Methods for the Study of Bats, 2nd edition. John Hopkins University Press, Baltimore, Maryland, pp. 171–189.
Wilkening A.J., Foltz J.L., Atkinson T.H., Connor M.D. 1981 An omnidirectional flight trap for ascending and descending insects. Canadian Entomologist 113: 453–455. https://doi.org/10.4039/ent113453-5
Willams C., Salter L., Jones G. 2011 The winter diet of the lesser horseshoe bat (Rhinolophus hipposideros) in Britain and Ireland. Hystrix, the Italian Journal of Mammalogy 22 (1): 159–166. https://doi.org/10.4404/hystrix-22.1-4498
Willis C.K., Brigham R.M. 2007 Social thermoregulation exerts more influence than microclimate on forest roost preferences by a cavity-dwelling bat. Behavioral Ecology and Sociobiology 62: 97–108. https://doi.org/10.1007/s00265-007-0442-y
Zahn A., Kriner E. 2016 Winter foraging activity of Central European Vespertilionid bats. Mammalian Biology 81: 40–45. https://doi.org/10.1016/j.mambio.2014.10.005

Supplementary materials [5]

Document title: Raw data collected during the microscope-based morphological analysis used in the study
Kind of document: Microsoft Excel (OpenXML)
MIME type: application/vnd.openxmlformats-officedocument.spreadsheetml.sheet
Document name: 000513000452023-01.xlsx

Document title: Validated and raw metabarcoding data used in the study
Kind of document: Microsoft Excel (OpenXML)
MIME type: application/vnd.openxmlformats-officedocument.spreadsheetml.sheet
Document name: 000513000452023-02.xlsx

Document title: Flight interception traps data (February-March) presenting all the invertebrate orders recorded in the study
Kind of document: Microsoft Excel (OpenXML)
MIME type: application/vnd.openxmlformats-officedocument.spreadsheetml.sheet
Document name: 000513000452023-03.xlsx

Document title: Flight interception traps data (February-March) listing the model groups recorded in the study
Kind of document: Microsoft Excel (OpenXML)
MIME type: application/vnd.openxmlformats-officedocument.spreadsheetml.sheet
Document name: 000513000452023-04.xlsx

Document title: Air temperature data from Razhishkata Cave recorded in the study and ERA5 temperature data for Lakatnik region
Kind of document: Microsoft Excel (OpenXML)
MIME type: application/vnd.openxmlformats-officedocument.spreadsheetml.sheet
Document name: 000513000452023-05.xlsx

— views: 686 (updated daily)

Cite as

Toshkova N., Dimitrova K., Langourov M., Zlatkov B., Bekchiev R., Ljubomirov T., Zielke E., Angelova R., Parvanova R., Simeonov Tz., Simov N. 2023 Snacking during hibernation? Winter bat diet and prey availabilities, a case study from Iskar Gorge, Bulgaria. Historia naturalis bulgarica 45: 125–142.

Export: BibTeX EndNote RefMan · JATS metadata

Open access
All journal content is available for free under the Creative Commons Attribution 4.0 International License (CC BY 4.0).