Bat population recoveries give insight into clustering strategies during hibernation

. 2020 ; 17 () : 26. [epub] 20200901

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32884575

BACKGROUND: Behaviour during hibernation contributes to energy conservation in winter. Hibernating bats select roosts with respect to physiological and environmental stressors, available local microclimate and species-specific requirements. RESULTS: We found that, in the period between 1977 and 2018, hibernating Myotis myotis and Rhinolophus hipposideros bats showed exponential population growth. The growth rates, corrected for local winter seasonal severity and winter duration, were equal to 10 and 13%, respectively. While R. hipposideros only utilised the thermally stable and, at survey time, warmer corridors in the hibernaculum, an increasing proportion of M. myotis roosted in the thermally stable corridors as their abundance increased. About 14% of all hibernating M. myotis displayed solitary roosting, irrespective of other covariates. Those bats that clustered together formed progressively larger clusters with increasing abundance, particularly in cold corridors. We found no statistically significant relationship for clustering behaviour or cluster size with winter severity or winter duration. CONCLUSIONS: Abundance of hibernating bats is increasing in Central Europe. As the number of M. myotis bats increases, thermally unstable corridors become saturated with large clusters and the animals begin to roost deeper underground.

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Ruf T, Geiser F. Daily torpor and hibernation in birds and mammals. Biol Rev. 2015;90:891–926. PubMed PMC

Boyles JG, Johnson JS, Blomberg A, Lilley TM. Optimal hibernation theory. Mamm Rev. 2020;50:91–100.

Williams CT, Barnes BM, Kenagy GJ, Buck CL. Phenology of hibernation and reproduction in ground squirrels: intergration of environmental cues with endogenous programming. J Zool. 2014;292:112–24.

Sheriff MJ, Kenagy GJ, Richter M, Lee T, Tøien O, Kohl F, Buck CL, Barnes BM. Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels. Proc Biol Sci. 2011;278:2369–75. PubMed PMC

Degn HJ, Andersen BB, Baagøe H. Automatic registration of bat activity through the year at Mønsted Limestone Mine, Denmark. Z für Säugetierkd. 1995;60:129–35.

Uhrin M, Sabolíková M, Naďo L, Maxinová E. Environmental variables do not explain the high size fluctuations in Rhinolophus euryale pre-hibernating aggregation. Biologia. 10.2478/s11756-020-00428-8.

Zukal J, Řehák Z, Kovařík M. Bats of the Sloupsko-šošuvské jeskyně cave (Moravian Karst, Central Moravia) Lynx n.s. (Praha) 2003;34:205–20.

Zukal J, Berková H, Madaraszová J. Flying or sleeping: flight activity of bats in natural cave with confirmed wns. Folia Zool. 2016;65:46–51.

Zukal J, Berková H, Banďouchová H, Kováčová V, Pikula J. In: 3. Karabulut S, (ed).Bats and caves: activity and ecology of bats wintering in caves. Rijeka: InTech; 2017, pp. 51–75.

Meyer GA, Senulis JA, Reinartz JA. Effects of temperature and availability of insect prey on bat emergence from hibernation in spring. J Mammal. 2016;97:1623–33.

Currie SE, Stawski C, Geiser F. Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at sub-zero temperatures. J Exp Biol. 2018;221(1):170894. PubMed

Boyles JG, Dunbar MB, Storm JJ, Brack V. Energy availability influences microclimate selection of hibernating bats. J Exp Biol. 2007;210:4345–50. PubMed

Turbill C, Geiser F. Hibernation by tree-roosting bats. J Comp Physiol B. 2008;178:597–605. PubMed

Martínková N, Pikula J, Zukal J, Kovacova V, Bandouchova H, Bartonička T, Botvinkin AD, Brichta J, Dundarova H, Kokurewicz T, Irwin NR, Linhart P, Orlov OL, Piacek V, Škrabánek P, Tiunov MP, Zahradníková Jr. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence. 2018;9:1734–50. PubMed PMC

Klüg-Baerwald BJ, Gower LE, Lausen CL, Brigham RM. Environmental correlates and energetics of winter flight by bats in southern Alberta, Canada. Can J Zool. 2016;94:829–36.

Boyles JG, Storm JJ, Brack Jr. Thermal benefits of clustering during hibernation: a field test of competing hypotheses on Myotis sodalis. Funct Ecol. 2008;22:632–6.

Boratyński JS, Willis CKR, Jefimow M, Wojciechowski MS. Huddling reduces evaporative water loss in torpid Natterer’s bats, Myotis nattereri. Comp Biochem Physiol A Mol Integr Physiol. 2015;179:125–32. PubMed

Boratyński JS, Rusiński M, Kokurewicz T, Bereszyńki A, Wojciechowski MS. Clustering behavior in wintering greater mouse-eared bats Myotis myotis– the effect of micro-environmental conditions. Acta Chiropterol. 2012;14:417–24.

Ryan CC, Burns LE, Broders HG. Changes in underground roosting patterns to optimize energy conservation in hibernating bats. Can J Zool. 2019;97:1064–70.

Stawski C, Willis CKR, Geiser F. The importance of temporal heterothermy in bats. Can J Zool. 2014;292:86–100.

Turner JM, Warnecke L, Wilcox A, Baloun D, Bollinger TK, Misra V, Willis CKR. Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. Physiol Behav. 2015;140:71–78. PubMed

Kunz TH, Parsons S, editors. Methods for assessing colony size, population size, and relative abundance of bats. Baltimore: The Johns Hopkins University Press; 2009.

Haysom K, Dekker J, Russ J, Van Der Meijn T, Van Strien A. Support for a Project on ‘Streamlining European Biodiversity Indicators (SEBI)’: Development of a Prototype Indicator of European Bat Population Trends. London: Bat Conservation Trust & European Environment Agency (EEA); 2011.

Daan S, Glas GH, Voute AM. Long term changes in bat populations in the Netherlands. Lutra. 1980;22:1–118.

Baar A, Mayer A, Wirth J. 150 Jahre Fledermausforschung in der Hermannshohle. Ann Naturhist Mus Wien, Serie B Bot Zool. 1986;88-89:223–23.

Fuszara E, Kowalski M, Lesinski G, Cygan JP. Hibernation of bats in underground shelters of central and northeastern Poland. Bonn Zool Beitr. 1996;46:349–58.

Lutsar L, Masing M, Poots L. Changes in the numbers of hibernating bats in the caves of Piusa (Estonia), 1949–1999. Folia Theriol Estonica. 2000;5:101–17.

Kervyn T, Lamotte S, Nyssen P, Verschuren J. Major decline of bat abundance and diversity during the last 50 years in southern Belgium. Belg J Zool. 2009;139:124–32.

Uhrin M, Benda P, Obuch J, Urban P. Changes in abundance of hibernating bats in central Slovakia (1992-2009) Biologia. 2010;65:349–361.

Lesińki G, Ignaczak M, Kowalski M. Increasing bat abundance in a major winter roost in central Poland over 30 years. Mammalia. 2011;75:163–7.

Nagy ZL, Postawa T. Seasonal and geographical distribution of cave-dwelling bats in Romania: implications for conservation. Anim Conserv. 2011;14:74–86. PubMed PMC

Bücs S, Jére C, Csösz I, Barti L, Szodoray-Parádi F. Distribution and conservation status of cave-dwelling bats in the Romanian Western Carpathians. Vespertilio. 2012;16:97–113.

Spitzenberger F, Engelberger S. Negative trend reversal after 16 years of constant growth: The case of Rhinolophus hipposideros in an Austrian mass hibernaculum (Chiroptera: Rhinolophidae) Lynx, n.s., (Praha) 2013;44:149–56.

Uhrin M, Andreas M, Bačkor P, Benda P, Bryndza P, Hapl E, Obuch J, Reiter A. Results of bat census in hibernacula iof the Muránska planina National Park, Slovakia, in 2002-2013 (Chiroptera) Lynx, n.s. (Praha) 2013;44:157–72.

Kerbiriou C, Julien JF, Monsarrat S, Lustrat P, Haquart A, Robert A. Information on population trends and biological constraints from bat counts in roost cavities: a 22-year case study of a pipistrelle bats (Pipistrellus pipistrellus Schreber) hibernaculum. Wildl Res. 2015;43:35–43.

Sniťko VP, Sniťko IV. Bats (Chiroptera, Vespertilionidae) from the Cis-Urals and South Urals (Republic of Bashkortostan) Zoologicheskii Zh. 2015;94:1436–56.

Bufka L, Červený J. Population increase of Rhinolophus hipposideros in the Šumava Mts. Region, SW Bohemia. Vespertilio. 2012;16:115–30.

Chytil J, Gaisler J. Development of the Rhinolophus hipposideros population in southern Moravia, Czech Republic. Vespertilio. 2012;16:131–7.

Řehák Z, Zukal J, Kovařík M. Long-term and short-term changes in the bat community of the Kateřinská cave (Moravian karst)– a fundamental assessment. Folia Zool. 1994;43:425–36.

Řehák Z, Gaisler J. Long-term changes in the number of bats in the largest man-made hibernaculum of the Czech Republic. Acta Chiropterologica. 1999;1:113–23.

Horáček I. Scítání netopýru v zimovištích CR: 1969- 2001 [Censusing bats in the underground hibernacula of the Czech Republic: 1969-2001]. Vespertilio; 5:1–330. In Czech.

Zima J, Kovařík M, Gaisler J, Ř̌ehák Z, Zukal J. Dynamics of the number of bats hibernating in the Moravian karst in 1983 to 1992. Folia Zool. 1994;43:109–19.

Bauerová Z, Zima J. Výzkum netopýrå v jeskyni Býčí skála v letech 1977-1986. [Bat research in the Býčí skála cave in 1977-1986] Čs. kras. 1988;39:51–59.

Zima J. Zimoviště netopýrå ve střední části Moravského krasu [Bat hibernacula in the central part of Moravian Karst] Vespertilio. 2001;5:311–20.

Martínková N, Bač̌kor P, Bartonička T, Blažková P, Č̌ervený J, Falteisek L, Gaisler J, Hanzal V, Horáček D, Hubálek Z, Jahelková H, Kolařík M, Korytár L, Kubátová A, Lehotska B, Lehotský R, Luč̌an RK, Májek I, Matějå J, Řehák Z, Šafář J, Tájek P, Tkadlec E, Uhrin M, Wagner J, Weinfurtová D, Zima J, Zukal J, Horáček I. Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE. 2010;5:13853. PubMed PMC

Rakuš̌an M. CO 2 in Caves of the Moravian Karst. Brno: Masaryk University; 2010.

Roer H. Zur Bestandssituation von Rhinolophus ferrumequinum (Schreber, 1774) und Rhinolophus hipposideros (Bechstein, 1800) (Chiroptera) im westlichen Mitteleuropa. Myotis. 1983;21-22:122–31.

Kokurewicz T. The decrease in abundance of the lesser horseshoe bat Rhinolophus hipposideros Bechstein, 1800 (Chiroptera: Rhinolophidae) in winter quarters in Poland. Myotis. 1990;28:109–17.

Weinreich JA, Oude Voshaar JH. Population trends of bats hibernating in marl caves in the Netherlands (1943-1987) Myotis. 1992;30:75–84.

Blažek J, Zukal J, Bandouchova H, Berková H, Kovacova V, Martínková N, Pikula J, Řehák Z, Škrabánek P, Bartonička T. Numerous cold arousals and rare arousal cascades as a hibernation strategy in european Myotis bats. J Therm Biol. 2019;82:150–6. PubMed

Czenze ZJ, Park AD, Willis CKR. Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation. J Comp Physiol B. 2013;183:859–66. PubMed

Zukal J, Bandouchova H, Brichta J, Čmoková A, Jaron KS, Kolarik M, Kovacova V, Kubátová A, Nováková A, Orlov O, Pikula J, Presetnik P, Šuba J, Zahradníková Jr. A, Martínková N. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep. 2016;6:19826. PubMed PMC

Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles DS, Coleman JTH, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. Bat white-nose syndrome: an emerging fungal pathogen? Science. 2009;323:227. PubMed

Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH. An emerging disease causes regional population collapse of a common North American bat species. Science. 2010;329:679–82. PubMed

Gore JA, Lazure L, Ludlow ME. Decline in the winter population of gray bats (Myotis grisescens) in Florida. Southeast Nat. 2012;11:89–98.

Thogmartin WE, King RA, McKann PC, Szymanski JA, Pruitt L. Population-level impact of white-nose syndrome on the endangered Indiana bat. J Mammal. 2012;93:1086–98.

Ingersoll TE, Sewall BJ, Amelon SK. Improved analysis of long-term monitoring data demonstrates marked regional declines of bat populations in the eastern United States. PLoS ONE. 2013;8:65907. PubMed PMC

Frick WF, Puechmaille SJ, Hoyt JR, Nickel BA, Langwig KE, Foster JT, Barlow KE, Bartonicka T, Feller D, Haarsma AJ, Herzog C, Horacek I, van der Kooij J, Mulkens B, Petrov B, Reynolds R, Rodrigues L, Stihler CW, Turner GG, Kilpatric AM. Disease alters macroecological patterns in North American bats. Glob Ecol Biogeogr. 2015;24:741–9.

Ingersoll TE, Sewall BJ, Amelon SK. Effects of white-nose syndrome on regional population pattern in 3 hibernating bat species. Conserv Biol. 2016;30:1048–59. PubMed

Drees KP, Lorch JM, Puechmaille SJ, Parise KL, Wibbelt G, Hoyt JR, Sun K, Jargalsaikhan A, Dalannast M, Palmer JM, Lindner DL, Marm Kilpatrick A, Pearson T, Keim PS, Blehert DS, Foster JT. Phylogenetics of a fungal invasion: Origins and widespread dispersal of white-nose syndrome. mBio. 2017;8:01941–17. PubMed PMC

Harazim M, Horáček I, Jakešová L, Luermann K, Moravec JC, Morgan S, Pikula J, Sosík P, Vavrušová Z, Zahradníková jr. A, Zukal J, Martínková N. Natural selection in bats with historical exposure to white-nose syndrome. BMC Zoology. 2018;3:8.

Pikula J, Amelon SK, Bandouchova H, Bartonička T, Berkova H, Brichta J, Hooper S, Kokurewicz T, Kolarik M, Köllner B, Kovacova V, Linhart P, Piacek V, Turner GG, Zukal J, Martínková N. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS ONE. 2017;12:01804351. PubMed PMC

Davy CM, Donaldson ME, Bandouchova H, Breit AM, Dorville NAS, Dzal YA, Kovacova V, Kunkel EL, Martínková N, Norquay KJO, Paterson JE, Zukal J, Pikula J, Willis CKR, Kyle CJ. Transcriptional host-pathogen responses of Pseudogymnoascus destructans and three species of bats with white-nose syndrome. Virulence. 2020;11:781–94. PubMed PMC

Bogdanowicz W, Urbanczyk Z. Some ecological aspects of bats hibernating in city of Poznań. Acta Theriologica. 1983;28:371–85.

Taylor P. Rhinolophus hipposideros. IUCN Red List of Threatened Species. 2016;2016:19518–21972794.

Kryštufek B. Bat hibernacula in a cave-rich landscape of the northern Dinaric karst, Slovenia. Hystrix - Ital J Mammal. 2007;18:195–204.

Dragu A. Species structure of the bat community hibernating in Muierilor cave (Southern Carpathians, Romania) N West J Zool. 2009;5:281–9.

Stloukal M. Anthropologische Funde aus der Býčí Skála-Höhle. Brno: Antropologie; 1981.

Parzinger H, Nekvasil J, Barth FE. Die Býčí Skála-Höhle, Ein Hallstattzeitlicher Höhleopferplatz in Mähren. Mainz am Rhein: Verlag Philipp von Zahern; 1995.

Mayes Boustead BE, Hilberg SD, Shulski MD, Hubbard KG. The accumulated winter season severity index (AWSSI) J Appl Meteorol Climatol. 2015;54:1693–712.

Menne MJ, Durre I, Korzeniewski B, McNeal S, Thomas K, Yin X, Anthony S, Ray R, Vose RS, E.Gleason B, Houston TG. Global historical climatology network - daily (ghcn-daily), version 3. NOAA national climatic data center, NOAA national climatic data center. [2019-09-18]. 2012. 10.7289/V5D21VHZ.

Menne MJ, Durre I, Vose RS, Gleason BE, Houston TG. An overview of the global historical climatology network-daily database. J Atmos Oceanic Technol. 2012;29:897–910.

R Core Team . R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2019.

van Buuren S, Groothuis-Oudshoorn K. mice: Multivariate imputation by chained equations in r. J Stat Softw. 2011;45(3):1–67.

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