Acoustic study of urban bat diversity in Veliko Tarnovo, Bulgaria

Maksim Kolev; Ilya Acosta-Pankov; Nia Toshkova; Stanimira Deleva

Maksim Kolev https://orcid.org/0000-0003-4908-4375; Ilya Acosta-Pankov https://orcid.org/0000-0001-7275-0482; Nia Toshkova https://orcid.org/0000-0003-4217-5653; Stanimira Deleva https://orcid.org/0000-0002-2964-8607

1 October 2024 · volume 46 · (issue 10) · pp. 273–284 · PDF [full text]

Abstract: Urbanisation presents both challenges and opportunities for bat populations. Understanding the composition and distribution of urban bat species is the first step toward their effective conservation. However, comprehensive studies on urban bat diversity remain scarce in Bulgaria. To address this gap, we conducted a year-long acoustic survey on five different habitats in the urbanised territory of Veliko Tarnovo. Our study identified the presence of eight bat species and other distinct acoustic groups within the urban environment. Bats were found to utilise various habitats across the urban landscape. Although the activity was highest during May and September, bats remained active all year round, including the winter. Our study provides insights into synanthropic bats’ seasonal and microhabitat-dependent use of urban areas. These findings will establish a baseline for future research focusing on habitat preferences, population dynamics, and interactions with urbanisation. Such research is essential for the effective management and conservation of bat populations in urban environments.

Keywords: bats, Chiroptera, echolocation, urbanisation, Veliko Tarnovo, winter bat activity

References [80]

Andrews M., Hodnett A., Andrews P. 2021 Lesser horseshoe bat Rhinolophus hipposideros (Bechstein, 1800). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 217–238.

Audet D. 1990 Foraging behaviour and habitat use by a gleaning bat, Myotis myotis (Chiroptera, Vespertilionidae). Journal of Mammalogy 71 (3): 420–427. https://doi.org/10.2307/1381955

Barros P., 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

Benda P., Ivanova T., Horáček I., Hanák V., Červený J., Gaisler J., Gueorguieva A., Petrov B., Vohralík V. 2003 Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 3. Review of bat distribution in Bulgaria. Acta Societalis Zoologicae Bohemicae 67 (4): 245–357.

BFSp 2020 Database of Bulgarian Caves. Bulgarian Federation of Speleology. https://caves.speleo-bg.org/.

Catto C., Hutson A., Racey P., Stephenson P. 1996 Foraging behaviour and habitat use of the serotine bat (Eptesicus serotinus) in southern England. Journal of Zoology 238 (4): 623–633. https://doi.org/10.1111/j.1469-7998.1996.tb05419.x

Collins J., Jones G. 2009 Differences in bat activity in relation to bat detector height: implications for bat surveys at proposed wind farm sites. Acta Chiropterologica 11 (2): 343–350. https://doi.org/10.3161/150811009x485576

Cortes K.M., Gillam E.H. 2020 Assessing the use of rivers as migratory corridors for temperate bats. Journal of Mammalogy 101 (2): 448–454. https://doi.org/10.1093/jmammal/gyz211

Czech B., Krausman P.R., Devers P.K. 2000 Economic associations among causes of species endangerment in the United States: associations among causes of species endangerment in the United States reflect the integration of economic sectors, supporting the theory and evidence that economic growth proceeds at the competitive exclusion of nonhuman species in the aggregate. BioScience 50 (7): 593–601.

Deleva S., Pavlova A. 2022 Research and Conservation of Bats (Mammalia, Chiroptera) in the Plovdiv City Urban Area: Current State and Future Perspectives. https://www.researchgate.net/publication/366824566.

Dietz C., Kiefer A. 2015 Bats of Britain and Europe. Bloomsbury Publishing, London–New York, 404 pp.

Dnevnik 2017 Prilepi sa bili zazidani jivi pri saniraneto na blokove v Burgas. https://www.dnevnik.bg/zelen/2017/11/14/3078029_prilepi_sa_bili_zazidani_jivi_pri_saniraneto_na/. (In Bulgarian)

Entwistle A.C., Racey P.A., Speakman J.R. 1996 Habitat exploitation by a gleaning bat, Plecotus auritus. Philosophical Transactions of the Royal Society of London B 351: 921–931. https://doi.org/10.1098/rstb.1996.0085

Estók P., Lefevre A., Sijpe M. van de, Russ J. 2021 Greater noctule Nyctalus lasiopterus (Schreber, 1780). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 458–468.

Fick S.E., Hijmans R.J. 2017 WorldClim 2: new 1 km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37 (12): 4302–4315. https://doi.org/10.1002/joc.5086

Furmankiewicz J., Kucharska M. 2009 Migration of bats along a large river valley in southwestern Poland. Journal of Mammalogy 90 (6): 1310–1317. https://doi.org/10.1644/09-mamm-s-099r1.1

Georgiakakis P., Russo D., Ancillotto L. 2021 Savi’s pipistrelle Hypsugo savii (Bonaparte, 1837). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 626–632.

Görföl T., Huang J.C., Csorba G., Győrössy D., Estók P., Kingston T., Szabadi K.L., McArthur E., Senawi J., Furey N., Tu V.T., Thong V.D., Khan F.A.A., Jinggong E.R., Donnelly M., Kumaran J.V., Liu J., Chen S., Tuanmu M., Ho Y., Chang H., Elias N., Abdullah N., Lim L., Squire C.D., Zsebők S. 2022 ChiroVox: a public library of bat calls. PeerJ 10. https://doi.org/10.7717/peerj.12445

Grimm N.B., Faeth S.H., Golubiewski N.E., Redman C.L., Wu J., Bai X., Briggs J.M. 2008 Global change and the ecology of cities. Science 319 (5864): 756–760. https://doi.org/10.1126/science.1150195

Hill A.P., Prince P.G.K., Snaddon J.L., Doncaster C.P., Rogers A. 2019 Audiomoth: a low-cost acoustic device for monitoring biodiversity and the environment. HardwareX 6: e00073. https://doi.org/10.1016/j.ohx.2019.e00073

Jardine C. 2022 Urbanization. In: Stephen C. (ed.) Wildlife Population Health. Springer, Cham, 144–152. https://doi.org/10.1007/978-3-030-90510-1_12

Jones G., Jacobs D.S., Kunz T.H., Wilig 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

Kipson M., Gazaryan S., Horáček I. 2023 Savi’s Pipistrelle Hypsugo savii (Bonaparte, 1837). In: Russo D. (ed.) Chiroptera. Handbook of the Mammals of Europe. Springer Nature Switzerland, 95–112. https://doi.org/10.1007/978-3-030-44029-9

Kohyt J., Karczmarz J., Pereswiet-Soltan A., Pierzchała E. 2024 Spatiotemporal use of urban rivers by local bat populations in a large city (Cracow, southern Poland). Urban Ecosystems. https://doi.org/10.1007/s11252-024-01545-x

Krauel J.J., LeBuhn G. 2016 Patterns of bat distribution and foraging activity in a highly urbanized temperate environment. PLoS ONE 11 (12). https://doi.org/10.1371/journal.pone.0168927

Krauel J.J., McGuire L., Boyles J.G. 2017 Testing traditional assumptions about regional migration in bats. Mammal Research 63 (2): 115–123. https://doi.org/10.1007/s13364-017-0346-9

Li H., Crihfield C., Feng Y., Gaje G., Guzman E., Heckman T., Mellis A., Moore L., Bechara N.R., Sanchez S., Whittington S., Wolf J.G., Garshong R., Morales K., Petric R., Zarecky L.A., Schug, M.D. 2020 The weekend effect on urban bat activity suggests fine scale human-induced bat movements. Animals 10 (9): 1636. https://doi.org/10.3390/ani10091636

Marques J.T., Rainho A., Carapuço M., Oliveira P., Palmeirim J.M. 2004 Foraging behaviour and habitat use by the European free-tailed bat Tadarida teniotis. Acta Chiropterologica 6 (1): 99–110.

Martinoli A., Mazzamuto M.V., Spada M. 2023 Serotine Eptesicus serotinus (Schreber, 1774). In: Russo D. (ed.) Chiroptera. Springer Nature Switzerland, 77–93. https://doi.org/10.1007/978-3-030-44029-9

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

McKinney M.L. 2006 Urbanization as a major cause of biotic homogenization. Biological Conservation 127 (3): 247–260. https://doi.org/10.1016/j.biocon.2005.09.005

MOEW 2024 Information System for protected areas from the Natura 2000 network. https://natura2000.egov.bg/EsriBg.Natura.Public.Web.App/Home/Natura2000ProtectedSites.

MOEW 2024 Protected areas in Bulgaria. https://eea.government.bg/zpo/bg/index.jsp.

Mucedda M., Pidinchedda E. 2021 Mehely’s horseshoe bat Rhinolophus mehelyi (Matschie, 1901). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 270–276.

Murphy S.E., Greenaway F., Hill D.A. 2012 Patterns of habitat use by female brown long-eared bats presage negative impacts of woodland conservation management. Journal of Zoology 288 (3): 177–183. https://doi.org/10.1111/j.1469-7998.2012.00936.x

Obrist M.K., Rathey E., Bontadina F., Martinoli A., Conedera M., Christe P., Moretti M. 2011 Response of bat species to sylvo-pastoral abandonment. Forest Ecology and Management 261 (3): 789–798. https://doi.org/10.1016/j.foreco.2010.12.010

Pandurski I. 2004 Bats (Mammalia, Chiroptera) of the Burgas Wetlands, Bulgarian Black Sea Coast. Acta Zoologica Bulgarica 56 (3): 283–296.

Papadatou E., Georgiakakis P., Kafkaletou-Diez A. 2021 Mediterranean horseshoe bat Rhinolophus euryale (Blasius, 1853). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 262–269.

QGIS Development Team 2024 QGIS Geographic Information System. 3.36.2. Open Source Geospatial Foundation Project. http://www.qgis.org/.

R Core Team 2023 R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/.

Ransome R.D. 1971 The effect of ambient temperature on the arousal frequency of the hibernating greater horseshoe bat, Rhinolophus ferrumequinum, relating to site selection and the hibernation state. Journal of Zoology 164: 357–371.

Ransome R. 2023 Greater Horseshoe Bat Rhinolophus ferrumequinum (Schreber, 1774). In: Russo D. (ed.) Chiroptera. Handbook of the Mammals of Europe. Springer Nature Switzerland, 839–874. https://doi.org/10.1007/978-3-030-44029-9

Razgour O. 2023 Plecotus austriacus Species Complex (P. austriacus, P. kolombatovici, P. gaisleri, P. teneriffae). In: Russo D. (ed.) Chiroptera. Handbook of the Mammals of Europe. Springer Nature Switzerland, 635–652. https://doi.org/10.1007/978-3-030-44029-9

Rodewald A.D., Gehrt S.D. 2014 Wildlife population dynamics in urban landscapes. In: McCleery R., Moorman C., Peterson M. (eds) Urban Wildlife conservation. Springer, Boston, 117–147. https://doi.org/10.1007/978-1-4899-7500-3_8

Rodrigues L., Zahn A., Rainho A., Palmeirim J.M. 2003 Contrasting the roosting behaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67 (3): 321–335. https://doi.org/10.1515/mamm.2003.67.3.321

Rowse E.G., Lewanzik D., Stone E.L., Harris S., Jones G. 2015 Dark matters: The effects of artificial lighting on bats. Bats in the Anthropocene: Conservation of Bats in a Changing World, 187–213. https://doi.org/10.1007/978-3-319-25220-9_7

Rudolph B.U., Liegl A., von Helversen O. 2009 Habitat selection and activity patterns in the greater mouse-eared bat Myotis myotis. Acta Chiropterologica 11 (2): 351–361. https://doi.org/10.3161/150811009X485585

Russ J. 2021 Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 752 pp.

Russ J. 2021 Common pipistrelle Pipistrellus pipistrellus (Schreber, 1774). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 548–562.

Russ J. 2021 Nathusius’s pipistrelle Pipistrellus nathusii (Keyserling and Blasius, 1839). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 585–597.

Russ J., Teixeira S. 2021 Leisler’s bat Nyctalus leisleri (Kuhl, 1818). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 469–485.

Russo D. 2023 Chiroptera. Handbook of the Mammals of Europe. Springer Nature Switzerland, 963 pp. https://doi.org/10.1007/978-3-030-44029-9

Russo D., Cosentino F., Festa F., De Benedetta F., Pejic B., Cerretti P., Ancillotto L. 2019 Artificial illumination near rivers may alter bat-insect trophic interactions. Environmental Pollution 252: 1671–1677. https://doi.org/10.1016/j.envpol.2019.06.105

Rydell J. 1992 Exploitation of insects around streetlamps by bats in Sweden. Functional Ecology 6 (6): 744–750. https://doi.org/10.2307/2389972

Rydell J., Boonman A. 2021 Parti-coloured bat Vespertilio murinus (Linnaeus, 1758). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 537–547.

Rydell J., Racey P. 1995 Street lamps and the feeding ecology of insectivorous bats. Symposia of the Zoological Society of London. The Society, London 1960–1999.

Safi K. 2023 Parti-Colored Bat Vespertilio murinus (Linnaeus, 1758). In: Russo D. (ed.) Chiroptera. Springer Nature Switzerland, 695–705. https://doi.org/10.1007/978-3-030-44029-9

Salinas-Ramos V.B., Ancillotto L., Cistrone L., Nastasi C., Bosso L., Smeraldo S., Cordero V.S., Russo D. 2021 Artificial illumination influences niche segregation in bats. Environmental Pollution 284: 117187. https://doi.org/10.1016/j.envpol.2021.117187

Schofield H.W., McAney C.M. 2008 Lesser horseshoe bat. In: Harris S., Yaldon D.W. (eds) Mammals of the British Isles, Handbook, 4th edition. Mammal Society, London, 306–310.

Simon M., Hüttenbügel S., Smit-Viergutz J. 2004 Ecology and Conservation of Bats in Villages and Towns. Bundesamt für Naturschutz, Federal Agency for Nature Conservation, Bonn, 263 pp.

Sjoberg D. 2021 Ggsankey: Sankey, alluvial and sankey bump plots. R package version 0.0, 99999.

Stone E.L., Harris S., Jones G. 2015 Impacts of artificial lighting on bats: A review of challenges and solutions. Mammalian Biology 80 (3): 213–219. https://doi.org/10.1016/j.mambio.2015.02.004

Stone E.L., Jones G., Harris S. 2012 Conserving energy at a cost to biodiversity? Impacts of LED lighting on bats. Global Change Biology 18 (8): 2458–2465. https://doi.org/10.1111/j.1365-2486.2012.02705.x

Stoycheva S., Georgiev D., Pandourski I., Tilova E. 2009 Bat diversity in two large towns of the Upper Thrace, Bulgaria (Chiroptera). Lynx, n. s. (Praha) 40: 83–93.

Stoycheva S., Georgiev D., Velcheva I. 2008 Feeding activity of three bat species (Mammalia: Chiroptera) in urban habitats of Upper Thracian Valley (Bulgaria). In: Velcheva I., Tsekov A. (eds) Anniversary Scientific Conference of Ecology Proceedings, Plovdiv, 538–542.

Taylor L.R. 1963 Analysis of the Effect of Temperature on Insects in Flight. Journal of Animal Ecology 32 (1): 99–117. https://doi.org/10.2307/2520

Teixeira S., Russo D. 2021 Kuhl’s pipistrelle Pipistrellus kuhlii (Kuhl, 1817). In: Russ J. (ed.) Bat Calls of Britain and Europe – A Guide to Species Identification. Pelagic Publishing, Exeter, 598–608.

Tilova E., Stoycheva S., Kmetova E., Nedyalkov N., Georgiev D. 2008 Discovery of a big hibernacula of Noctule bats, Nyctalus noctula (Schreber, 1774) (Chiroptera: Vespertilionidae). Historia naturalis bulgarica 19: 129–136.

Torre I., López-Baucells A., Stefanescu C., Freixas L., Flaquer C., Bartrina C., Coronado A., López-Bosch D., Mas M., Míguez S., Muñoz J., Páramo F., Puig-Montserrat X., Tuneu-Corral C., Ubach A., Arrizabalaga A. 2021 Concurrent Butterfly, Bat and Small Mammal Monitoring Programmes Using Citizen Science in Catalonia (NE Spain): A Historical Review and Future Directions. Diversity 13 (9): 454. https://doi.org/10.3390/d13090454

Toshkova N., Dimitrova K., Langourov M., Zlatkov B., Bekchiev R., Ljubomirov T., Zielke E., Angelova R., Parvanova R., Simeonov T., Simov N. 2023 Snacking during hibernation? Winter bat diet and prey availabilities, a case study from Iskar Gorge, Bulgaria. Historia naturalis bulgarica 45 (5): 125–142. https://doi.org/10.48027/hnb.45.053

Tzankov N., Popgeorgiev G., Kornilev Y., Petrov B., Zidarova S., Stefanov T. 2015 Sofia. In: Kelcey J. (ed.) Vertebrates and Invertebrates of European Cities: Selected Non-Avian Fauna. Springer, New York, 179–206.

Veliko Tarnovo Municipality 2020 Parkove v grad Veliko Tarnovo. https://www.veliko-tarnovo.bg/bg/opazvane-na-okolnata-sreda/zelena-sistema/parkove-v-grad-veliko-trnovo/. (In Bulgarian)

Vitousek P.M., Mooney H.A., Lubchenco J., Melillo J.M. 1997 Human domination of earth’s ecosystems. Science 277 (5325): 494–499. https://doi.org/10.1126/science.277.5325.494

Voigt C.C., Scholl J.M., Bauer J., Teige T., Yovel Y., Kramer-Schadt S., Gras P. 2020 Movement responses of common noctule bats to the illuminated urban landscape. Landscape Ecology 35 (1): 189–201. https://doi.org/10.1007/s10980-019-00942-4

Voigt C.C., Azam C., Dekker J., Ferguson J., Fritze M., Gazaryan S., Hölker F., Jones G., Leader N., Lewanzik D., Limpens H.J.G.A., Mathews F., Rydell J., Schofield H., Spoelstra K., Zagmajster M. 2018 Guidelines for consideration of bats in lighting projects. EUROBATS Publication Series No. 8. UNEP/EUROBATS Secretariat, Bonn, 62 pp.

Wickham H. 2007 Reshaping Data with the reshape Package. Journal of Statistical Software 21 (12): 1–20. http://www.jstatsoft.org/v21/i12/.

Wickham H. 2016 ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York.

Wildlife Acoustics 2023 Kaleidoscope Pro Analysis Software 5.6.4. Maynard, USA. https://www.wildlifeacoustics.com/products/kaleidoscope-pro.

Williams C.B. 1961 Studies in the effect of weather conditions on the activity and abundance of insect populations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 244 (713): 331–378. https://doi.org/10.1098/rstb.1961.0011

Wolf J.M., Jeschke J.M., Voigt C.C., Itescu Y. 2022 Urban affinity and its associated traits: A global analysis of bats. Global Change Biology 28 (19): 5667–5682. https://doi.org/10.1111/gcb.16320

Supplementary materials [2]

01
Document title: The supplementary material represents merged tables from the Kaleidoscope pro software 5.6.4 after analysis of the recordings from all 240 nights of recording with information on dates, times of recording, locations, echolocation call characteristics, automatic and manual call identifications
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02
Document title: The table represents information on the 111 recordings uploaded to the ChiroVox bat sound library, which can be found on the following link: https://www.chirovox.org/contributor_map.php?q=%D0%9Caksim%20Kolev
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