Abstract
In Eastern Europe, wind energy production is currently promoted as an important source of renewable energy, yet in most cases without appropriate consideration of the negative impacts wind turbines (WT) may have on protected species such as bats. Here, we present first data on fatality rates, fatality factors and the likely origin of bats killed by WT in the Dobrogea region (Romania), located in a major migratory corridor for wildlife in Eastern Europe. Over a 4-year period, we found a total of 166 bat carcasses from 10 species, mostly representing migratory species such as Pipistrellus nathusii and Nyctalus noctula. Most fatalities at WT occurred in July and August. We documented 15 cases of barotrauma and 34 cases of blunt-force trauma in carcasses found below WT. After adjusting for carcass removals and variations in searcher efficiency, we estimated for the 4-year study period a total of 2394 bat casualties at the studied WT facility consisting of 20 units, resulting in a mean fatality rate of 30 bats/WT/year, or 14.2 bats/MW/year. By implementing a curtailment measure at wind speeds below 6.5 m/s, we reduced fatality rates by 78%. Isoscape origin models based on hydrogen stable isotope ratios in fur keratin revealed that the majority of N. noctula that were killed by WT or captured nearby in mist nets originated from distant areas in the North (Ukraine, Belarus, Russia). The estimated high fatalitjegangy rates of bats at WT in this area have far-reaching consequences, particularly for populations of migratory bats, if no appropriate mitigation schemes are practised.
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Amorim F, Rebelo H, Rodrigues L (2012) Factors influencing bat activity and mortality at a wind farm in the Meditterranean region. Acta Chiropterologica 14(2):439–457. https://doi.org/10.3161/150811012X661756
Arnett EB, Huso M, Schirmacher MR, Hayes JP (2011) Altering turbine speed reduces bat mortality at wind-energy facilities. Front Ecol Environ 9:209–214. https://doi.org/10.1890/100103
Arnett EB, Baerwald EF, Mathews F, Rodrigues L, Rodríguez-Durán A, Rydell J, Villegas-Patraca R, Voigt CC (2016) Impacts of wind energy development on bats: a global perspective. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: conservation of Bats in a changing world. Springer International Publishing, pp 295–323
Baerwald EF, Patterson WP, Barclay RMR (2014) Origins and migratory patterns of bats killed by wind turbines in southern Alberta: evidence from stable isotopes. Ecosphere 5:1–17. https://doi.org/10.1890/ES13-00380.1
Barclay, R.M.R., Baerwald, E.F., Rydell, J. (2017) Bats, Chapter 9 in Wildlife and wind farms: conflicts and solutions, volume 1 (M. Perrow, ed)
Barnes RS, Hill M, Peters K (2018) Wind energy and bat conservation – a review by the Canadian Wind Energy Association. Document No.: 10017086-HOU-R-01-F, pp 253
Behr O, Brinkmann R, Hochradel K, Mages J, Korner-Nievergelt F, Niermann I, Nagy M (2017) Mitigating bat mortality with turbine-specific curtailment algorithms: a model based approach. In: Köppel J (ed) Wind energy and wildlife interactions. Springer, Cham, pp 135–160. https://doi.org/10.1007/978-3-319-51272-3_8
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 Soc Zool Bohem 67:245–357
Benítez-López AAR, Verweij PA (2010) The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biol Conserv 143(6):1307–1316
Bernardino J, Bispo R, Costa H, Mascarenhas M (2013) Estimating bird and bat fatality at wind farms: a practical overview of estimators, their assumptions and limitations. New Zealand Journal of Zoology 40:63–74. https://doi.org/10.1080/03014223.2012.758155
Blohm T, Heise G (2008) Uckermärkische Mückenfledermäuse, Pipistrellus pygmaeus (Leach, 1825) teils Fernwanderer, teils standorttreu. Nyctalus 13:263–266
Bonn (1979) Convention on the conservation of migratory species of wild animals. UNEP/CMS Secretariat, Bonn
Bosso L, Ancillotto L, Smeraldo S, D’Arco S, Migliozzi A, Conti P, Russo D (2018) Loss of potential bat habitat following a severe wildfire: a model-based rapid assessment. Int J Wildland Fire 27(11):756–769. https://doi.org/10.1071/WF18072
Bowen GJ, Wassenaar LI, Hobson KA (2005) Global application of stable hydrogen and oxygen isotopes to wildlife forensics. Oecologia 143:337–348. https://doi.org/10.1007/s00442-004-1813-y
Brinkmann R, Behr O, Niermann I, Reich M (2011) Entwicklung von Methoden zur Untersuchung und Reduktion des Kollisionsrisikos von Fledermausen an onshore-Windenergieanlagen. Schriftenreihe Institut fur Umweltplanung. Cuvillier Verlag Gottingen, p 457
Burnham KP, Anderson DR (2002) Model selection and inference: a practical information-theoretic approach, vol 355. Springer, New York. https://doi.org/10.1007/978-1-4757-2917-7
Carmen G, Chachula OM (2013) Fauna monitoring studies and the development of wind farms in Romania. Studii și Comunicări, Muzeul Olteniei, Ştiinţele Naturii 29:97–203
Courtiol A, Rousset F, Rohwäder MS, Soto DX, Lehnert LS, Voigt CC, Hobson KA, Wassenaar LI, Kramer-Schadt S (2019) Isoscape computation and inference of spatial origins with mixed models using the R package IsoriX. In: Tracking animal migration with stable isotopes (pp 207–236). Academic Press
Croitoru EO, Zamfir AI (2014) Management challenges for sustainable development. Proceedings of the 8th International Management Conference, November 6-7th, Bucharest, Romania, pp. 627-634
Cryan PM, Barclay RMR (2009) Causes of bat fatalities at wind turbines: hypotheses and predictions. J Mammal 90:1330–1340
Cryan PM, Brown AC (2007) Migration of bats past a remote island offers clues toward the problem of bat fatalities at wind turbines. Biol Conserv 139:1–11. https://doi.org/10.1016/j.biocon.2007.05.019
Cryan PM, Bogan MA, Rye RO, Landis GP, Kester CL (2004) Stable hydrogen isotope analysis of bat hair as evidence for seasonal molt and long-distance migration. Journal of Mammology 85:995–1001. https://doi.org/10.1644/BRG-202
Dalthorp DH, Simonis J, Madsen L, Huso MM, Rabie P, Mintz JM, Wolpert R, Studyvin J, Korner-Nievergelt F (2018) Generalized estimator of mortality (GenEst) - R Package: U.S. Geological Survey Software Release. https://doi.org/10.5066/P9O9BATL
Dietz C, Helversen O (2004) Illustrated identification key to the bats of Europe. Electronic Publication V1.0, Germany, pp 35
Dietz C, Helversen O, Nill D (2009) Bats of Britain, Europe & Northwest Africa. English edition, London: A & C Black Publishers Ltd, pp 400
Dincer I (2000) Renewable energy and sustainable development: a crucial review. Renew Sust Energ Rev 4(2):157–175
Dodelin B (2002) Identification des Chiroptères de France á partir de restes osseux, Fédération Française de Spéléologie, pp 48
Erickson JL, West SD (2002) The influence of regional climate and nightly weather conditions on activity patterns of insectivorous bats. Acta Chiropterologica 4:17–24. https://doi.org/10.3161/001.004.0103
Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: an empirical review and synthesis. Ecol Soc 14(1)
Fraser EE, Longstaffe FJ, Fenton MB (2013) Moulting matters: the importance of understanding moulting cycles in bats when using fur for endogenous marker analysis. Can J Zool 91:533–544. https://doi.org/10.1139/cjz-2013-0072
Frick WF, Baerwald EF, Pollock JF, Barclay RMR, Szymanski JA, Weller TJ, Russell AL, Loeb SC, Medellin RA, McGuire LP (2017) Fatalities at wind turbines may threaten population viability of a migratory bat. Biol Conserv 209:172–177. https://doi.org/10.1016/j.biocon.2017.02.023
Gashchak S, Vlaschenko A, Eśtok P, Kravchenko K (2015) New long-distance recapture of a noctule (Nyctalus noctula) from eastern Europe. Hystrix, the Italian Journal of Mammalogy 26:59–60. https://doi.org/10.4404/hystrix-26.1-10624
Haarsma AJ (2008) Manual for assessment of reproductive status, age and health in European Vespertilionid bats, Hillegom, Holland, Electronic Publication Version 1, pp 62
Hanák V, Benda P, Ruedi M, Horáček I, Sofianidou ST (2001) Bats (Mammalia:Chiroptera) of the Eastern Mediterranean, Part 2, New records and review of distribution of bats in Greece, Česká zoologická společnost, pp 68
Hayes MA (2013) Bats killed in large numbers at United States wind energy facilities. BioScience 63:975–979. https://doi.org/10.1525/bio.2013.63.12.10
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326. https://doi.org/10.1007/s004420050865
Huso M, Dalthorp D (2014) Accounting for unsearched areas in estimating wind turbine-caused fatality. J Wildl Manag 78(2):347–358
Huso M, Nicholas S, Lew L (2012) Fatality estimator user’s guide (ver. 1.1, December 2015). U.S. Geological Survey Data Series 729, pp 22. https://doi.org/10.3133/ds729
Huso M, Dalthorp D, Miller TJ, Bruns D (2016) Wind energy development: methods to assess bird and bat fatality rates postconstruction. Human-Wildlife Interactions 10:62–70 https://pubs.er.usgs.gov/publication/70170980
Hutterer R, Ivanova T, Meyer-Cords C, Rodrigues L (2005) Bat migration in Europe, a review of banding data and literature. Landwirtschaftsvlg Münster, pp 162
Ilyin VY (1990) The seasonal shedding of Pipistrellus nathusii and Nyctalus noctula. In Ilyin YV, Strelkov PP, Rodionov VA (ed). Proceedings of the Fifth All-Union Bat Conference, Penza, Russia, Penza State Educational Institute, pp 86–89
Kunz TH, Parsons S (2009) Ecological and behavioral methods for the study of bats, 2nd edn. The Johns Hopkins University Press, Baltimore, p 901
Lehnert LS, Kramer-Schadt S, Schönborn S, Lindecke O, Niermann I, Voigt CC (2014) Wind farm facilities in Germany kill noctule bats from near and far. PLoS One 9:e103106. https://doi.org/10.1371/journal.pone.0103106
Lehnert LS, Kramer-Schadt S, Teige T, Hoffmeister U, Popa-Lisseanu A, Bontadina F, Ciechanowski M, Dechmann DKN, Kravchenko K, Presetnik P, Starrach M, Straube M, Zöphel U, Voigt CC (2018) Variability and repeatability of noctule bat migration in Central Europe: evidence for partial and differential migration. Proc R Soc B 285:20182174
Măntoiu DȘ, Chişamera GB, Chachula OM, Mărginean G, Pocora I, Pocora V, Hodor C, Stanciu CR, Popescu-Mirceni R, Telea A, Bălăşoiu D, Şandric IC (2015) A bat fatality risk model at wind farms in Dobrogea, Romania , using a GIS approach. 4Th Inernational Berlin Bat Meeting, 13-15th March, Berlin, Germany, pp 116
Martin CM, Arnett EB, Stevens RD, Wallace MC (2017) Reducing bat fatalities at wind facilities while improving the economic efficiency of operational mitigation. J Mammal 98:378–385. https://doi.org/10.1093/jmammal/gyx005
Nellemann C, Vistnes I, Jordhøy P, Strand O (2001) Winter distribution of wild reindeer in relation to power lines, roads and resorts. Bio Consevr 101(3):351–360
Nghiem A, Mbistrova A, Pineda I, Tardieu P (2017) Wind Europe, Wind in power. 2016 European Statistics, Brusseles, Blegium, pp 24
Moreau RE (1972) Palearctic African bird migration systems. Academic Press Inc, p 384
O’Shea TJ, Cryan PM, Hayman DTS, Plowright RK, Streicker DG (2016) Multiple mortality events in bats: a global review. Mammal Rev 46:175–190. https://doi.org/10.1111/mam.12064
Panutin KK (1980) Bats. In Kucheruk VV (ed) Results of mammals banding, Moscow, USSR, pp 23–46
Popa-Lisseanu AG, Sörgel K, Luckner A, Wassenaar LI, Ibáñez C, Kramer-Schadt S, Ciechanowski M, Tamás G, Niermann I, Beuneux G, Mysłajek RW, Juste J, Fonderflick J, Kelm DH, Voigt CC (2012) A triple-isotope approach to predict the breeding origins of European bats. PLoS One 7:e30388. https://doi.org/10.1371/journal.pone.0030388
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Rodrigues L et al. (2014), UNEP/EUROBATS Publication Series No. 6, Guidelines for consideration of bats in wind farm projects, revision 2014, ISBN 978-92-95058-30-9, pp 133
Rodrigues L et al. (2017) UNEP/EUROBATS IWG - Report of the Intersessional Working Group on wind turbines and bat population, Doc. EUROBATS AC 22.10 In 22th Meeting of the Advisory Committee, Belgrade, Serbia, 27–29 March 2017. http://bit.do/turbines2017
Rollins KE, Meyerholz DK, Johnson GD, Capparella AP, Loew SS (2012) A forensic investigation into the etiology of bat mortality at a wind farm : barotrauma or traumatic injury? Vet Pathol 49:362–371. https://doi.org/10.1177/0300985812436745
Rydell J, Bach L, Dubourg-Savage MJ, Green M, Rodrigues L, Hedenström A (2010) Bat mortality at wind turbines in northwestern Europe. Acta Chiropterologica 12:261–274. https://doi.org/10.3161/150811010X537846
Sánchez-Zapata JA, Clavero M, Carrete M, DeVault TL, Hermoso V, Losada MA, Polo MJ, Sánchez-Navarro S, Pérez-García JM, Botella F, Ibáñez C, Donázar JA (2016) Effects of renewable energy production and infrastructure on wildlife, Current Trends in Wildlife Research, Springer, Cham, 97–123
Santos H, Rodrigues L, Jones G, Rebelo H (2013) Using specis distribution modelling to predict bat fatality risk at wind farms. Biol Conserv 157:178–186
Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253. https://doi.org/10.1644/10-MAMM-F-355.1
Spellerberg IAN (1998) Ecological effects of roads and traffic: a literature review. Global Ecology & Biogeography Letters 7(5):317–333
Strelkov PP (1969) Migratory and stationary bats (Chiroptera) of the European part of the Soviet Union. Acta Zool Cracov 14:393–436
Strelkov PP (1997) Breeding area and its position in range of migratory bats species (Chiroptera, Vespertilionidae) in East Europe and adjacent territories. Communication 1. Zoologicheskii Zhurnal 76:1073–1082
Strelkov PP (1999) Correlation of sexes in adult individuals of migratory bat species (Chiroptera, Vespertilionidae) from Eastern Europe and adjacent territories. The Journal of Zoology 78:1441–1454
Strelkov PP (2000) Seasonal distribution of migratory bat speceis (Chiroptera, Vespertilionidae) in Eastern Europe and adjacent territories: nursing area. Myotis 37:7–25
Strelkov PP (2002) Material on wintering of migratory bat species (Chiroptera) on the territory of the former USSR and adjacent regions, part 2, Nyctalus noctula. Plecotus 5:35–56
Strelkov PP, Abramov AV (2001) Sexual and age proportion of males in different parts of the range in migratory bat species (Chiroptera, Vespertilionidae) from Eastern Europe and adjacent territories during nursing period. Russian Journal of Zoology 80:222–229
Sullivan AR, Bump JK, Kruger LA, Peterson RO (2012) Bat‐cave catchment areas: using stable isotopes (δD) to determine the probable origins of hibernating bats. Ecol Appl 22(5):1428–1434
US Fish and Wildlife Service (2011) US fish and wildlife service draft land-based wind energy guidelines. US fish and wildlife service, Washington, DC
Vlaschenko AS, Kravchenko K, Prylutska AS (2013) Prediction of the future fatalities : bats and wind energy in Ukraine. Conference on Wind Power and Enviromental Impacts, Stockholm, 5-7th February. pp 109–110
Vlaschenko AS, Kravchenko K, Prylutska AS, Ivancheva Em Sitnikova E, Mishin A (2016) Structure of summer bat assemblages in forests in European Russia. Turk J of Zool 40:1–18. https://doi.org/10.3906/zoo-1508-56
Voigt CC, Popa-Lisseanu AG, Niermann I, Kramer-Schadt S (2012) The catchment area of wind farms for European bats: a plea for international regulations. Biol Conserv 153:80–86. https://doi.org/10.1016/j.biocon.2012.04.027
Voigt CC, Lehnert LS, Popa-Lisseanu AG, Ciechanowski M, Estók P, Gloza-Rausch F, Görföl T, Göttsche M, Harrje C, Hötzel M, Teige T, Wohlgemuth R (2014) The trans-boundary importance of artificial bat hibernacula in managed European forests. Biodivers Conserv 23:617–631. https://doi.org/10.1007/s10531-014-0620-y
Voigt CC, Lehnert LS, Petersons G, Adorf F, Bach L (2015) Wildlife and renewable energy: German politics cross migratory bats. Eur J Wildl Res 61:213–219. https://doi.org/10.1007/s10344-015-0903-y
Zimmerling JR, Francis CM (2016) Bat mortality due to wind turbines in Canada. J Wildl Manag 80:1360–1369. https://doi.org/10.1002/jwmg.21128
Acknowledgements
We would like to thank the Babadag Wind Park managers for giving us full access to environmental data and for the long-term collaboration regarding conservation actions of bats in the region. We thank Doris Fichte and Yvonne Klaar for their help in the stable isotope laboratory. We thank Stephanie Kramer-Schadt for the help with statistical analysis. We thank Manuela Huso (United States Geological Survey) for help regarding the estimation of fatality rates. We acknowledge the work done by Marius Alexandru Ciocănău, at the Faculty of Veterinary and Agricultural Sciences, University of Bucharest, Romania, for identifying the cause of death for the bat carcasses. Other valuable field activities were conducted with the help of Liviu Bufnilă, Marcel Ţîbîrnac, Mihai Ventoniuc, Gabriel Chişamera and Alexandra Doba. We are grateful to the anonymous reviewers for their suggestions that improved the manuscript.
Funding
Oana Teodora Moldovan was supported by a grant of the Ministry of Research and Innovation, CNCS - UEFISCDI, project number PN-III-P4-ID-PCCF-2016-0016, within PNCDI III. Kseniia Kravchenko expresses gratitude to The German Federal Ministry of Education and Research (BMBF) for Green Talents Award 2015 which provided great opportunity of research stay at IZW. The field visit of Kseniia Kravchenko and Anton Vlaschenko to Romania were supported by EUROBATS project initiative in the frame of ‘Trans-border collaboration in bat migration research in Eastern Europe and the Black Sea region, 2014’ project.
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Appendix
The list of bat mortalities at the Babadag Wind Park, 2013–2016
Abbreviations: Bat species acronyms: ESER – Eptesicus serotinus; HSAV – Hypsugo savii; MYOSP – Myotis sp.; NLEI – Nyctalus leisleri; NNOC – Nyctalus noctula; PKUL – Pipistrellus kuhlii; PNAT – Pipistrellus nathusii, PPIP – Pipistrellus pipistrellus; PPYG – Pipistrellus pygmaeus, PIPSP – Pipistrellus sp.; VMUR – Vespertilio murinus. Structure of citation: date (mm/yy), species, no. individuals (in the case of isolated individuals, no numbers have been aded), sex (♀- female, ♂ - male), age (ad – adult, sad-sub adult, juv – juvenile). In case of missing data, the n/a (not available) symbol was used, for example: PNAT n/a – no information about sex and age, or PNAT ♂n/a – no information about age. Each sex-age-n/a group was divided by a coma. Species belonging to the same date were delimited by semicolons and different months were delimited by a point
4.13 – PNAT ♂n/a, ♀n/a, n/a; PPIP ♂n/a, n/a ad; PIPSP n/a; VMUR n/a ad; NNOC ♂n/a. 05.13 – PNAT 2n/a. 06.13 – PNAT 2n/a; PPIP n/a; PIPSP n/a. 07.13 – PKUL ♂ad; PIPSP n/a ad, 2n/a; VMUR 3n/a. 08.13 – PNAT 3♂ad, 2♀ad, n/a juv; PKUL 2♂ad, n/a ad; PPYG ♂ad, n/a ad; PIPSP ♂juv, n/a juv, n/a ad, 3 n/a; NNOC ♂ad, 3♀ad, 2n/a; VMUR ♂ad, 3n/a. 04.14 – PNAT 7♂ad, ♂n/a, 4♀ad. 05.14 – PNAT 3♂ad, ♀ad; PKUL 2♂ad; PIPSP ♂ad; MYOSP n/a ad, ♂ad. 06.14 – PNAT 2♂ad, 2♀ad; NNOC ♀ad; NLEI 2♀n/a. 07.14 – PNAT ♂ad, n/a; PIPSP ♀ad; ESER ♂ad; NNOC ♂ad, ♂n/a, n/a ad, 2n/a; NLEI ♂ad, ♀n/a, n/a ad. 08.14 – PNAT ♀ad, ♂juv, 2n/a ad; HSAV ♂n/a; NNOC 2♂ad, ♀ad, n/a ad, 2n/a. 09.14 – PNAT 2♂ad, 3♀ad; PPYG n/a ad; PIPSP n/a ad; NNOC ♂ad, ♀ad, 2n/a ad, n/a; HSAV n/a. 10.14 – PNAT ♂ad, ♂n/a, n/a ad; NNOC ♀ad, 2n/a ad, n/a. 11.14 – PNAT ♀ad. 04.15 – PNAT ♂ad; NNOC ♀ad. 05.15 – PNAT ♂ad, PIPSP 2n/a, VMUR n/a ad. 06.15 – NNOC n/a. 07.15 – PNAT ♂ad; PIPSP 3n/a. 08.15 – PNAT ♂ad, 2♀ad; NNOC 2♂ad, 2n/a ad. 09.15 – PIPSP 3n/a. 5.16 – PNAT ♂ad; PPYG ♂n/a, PIPSP 2n/a; NNOC ♀ad. 7.16 – PNAT ♂ad; NNOC ♀ad; NLEI ♂ad.; VMUR n/a. 8.16 – PNAT ♂n/a; PPIP ♂ad; PIPSP 3n/a; NNOC 3♂ad, ♀ad, 2n/a. 9.16 – PNAT ♂ad; PPYG ♀n/a; PIPSP n/a; NNOC 2♀ad, n/a.
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Măntoiu, D.Ş., Kravchenko, K., Lehnert, L.S. et al. Wildlife and infrastructure: impact of wind turbines on bats in the Black Sea coast region. Eur J Wildl Res 66, 44 (2020). https://doi.org/10.1007/s10344-020-01378-x
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DOI: https://doi.org/10.1007/s10344-020-01378-x