Male long-distance migrant turned sedentary; The West European pond bat (Myotis dasycneme) alters their migration and hibernation behaviour


Autoři: Anne-Jifke Haarsma aff001;  Peter H. C. Lina aff002;  Aldo M. Voûte aff003;  Henk Siepel aff001
Působiště autorů: Animal Ecology and Physiology, Institute for Water and Wetland Research, Radboud University Nijmegen, The Netherlands aff001;  Naturalis Biodiversity Center, Leiden, The Netherlands aff002;  Independent Researcher, Soest, The Netherlands aff003;  Wageningen Environmental Science, Animal Ecology Group, Wageningen, The Netherlands aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0217810

Souhrn

During autumn in the temperate zone, insectivorous male bats face a profound energetic challenge, as in the same period they have to make energy choices related to hibernation, mating and migration. To investigate these energetic trade-offs, we compared the body mass of male and female pond bats (Myotis dasycneme) through the summer season, characterized the known hibernacula in terms of male or female bias, and subsequently compared their population trend during two study periods, between 1930–1980 and 1980–2015. Towards the end of summer, males began losing weight whilst females were simultaneously accumulating fat, suggesting that males were pre-occupied with mating. We also found evidence for a recent adaptation to this energetic trade-off, males have colonised winter roosts in formerly unoccupied areas, which has consequently led to a change in the migration patterns for the male population of this species. As male bats do not assist in raising offspring, males have ample time to restore their energy balance after hibernation. Our results suggest that choosing a hibernacula closer to the summer range not only decreases energy cost needed for migration, it also lengthens the mating season of the individual male. Our findings have important conservation implications, as male and female biased hibernation assemblages may differ critically in terms of microclimate preferences.

Klíčová slova:

Animal migration – Bats – Limestone – Netherlands – Ponds – Summer – Winter – Hibernation


Zdroje

1. Russo D, Bosso L, Ancillotto L. Novel perspectives on bat insectivory highlight the value of this ecosystem service in farmland: research frontiers and management implications. Agriculture, Ecosystems & Environment. 2018 Nov 1;266:31–8.

2. Charbonnier YM, Barbaro L, Barnagaud JY, Ampoorter E, Nezan J, Verheyen K, et al. Bat and bird diversity along independent gradients of latitude and tree composition in European forests. Oecologia. 2016 Oct 1;182(2):529–37. doi: 10.1007/s00442-016-3671-9 27312262

3. Encarnação JA, Kierdorf U, Holweg D, Jasnoch U, Wolters V. Sex‐related differences in roost‐site selection by Daubenton's bats Myotis daubentonii during the nursery period. Mammal Rev. 2005 Jul;35(3‐4):285–94.

4. Senior P, Butlin RK, Altringham JD. Sex and segregation in temperate bats. Proc R Soc Lond B Biol Sci. 2005; 272: 2467–2473.

5. Safi K, Koning B, Kerth G. Sex differences in population genetics, home range size and habitat use of the parti-colored bat (Vespertilio murinus, Linnaeus 1758) in Switzerland and their consequences for conservation. Biol Conserv. 2007; 137: 28–36.

6. Papadatou E, Butlin RK, Altringham JD. Seasonal roosting habits and population structure of the long-fingered bat Myotis capaccinii in Greece. J Mammal. 2008; 89(2): 503–512.

7. Levin E, Roll U, Dolev A, Yom-Tov Y, Kronfeld-Shcor N. Bats of a gender flock together: sexual segregation in a subtropical bat. PloS one. 2013; 8(2), e54987. doi: 10.1371/journal.pone.0054987 23441148

8. Angell RL, Butlin RK, Altringham JD. Sexual segregation and flexible mating patterns in temperate bats. PloS one. 2013 Jan 24;8(1):e54194. doi: 10.1371/journal.pone.0054194 23365652

9. Vintulis V, Šuba J. Autumn swarming of the pond bat Myotis dasycneme at hibernation sites in Latvia. Estonian J Ecol. 2010; 59(1): 70–80.

10. Šuba J, Petersons G, Rydell J. Fly-and-forage strategy in the bat Pipistrellus nathusii during autumn migration. Acta Chiropt. 2012; 14(2): 379–385.

11. Levey DJ, Stiles FG. Evolutionary precursors of long-distance migration: resource availability and movement patterns in Neotropical landbirds. Amer Nat. 1992; 140(3): 447–476.

12. Teitelbaum CS, Fagan WF, Fleming CH, Dressler G, Calabrese JM, Leimgruber P, et al. How far to go? Determinants of migration distance in land mammals. Ecol Lett. 2015; 18(6): 545–552. doi: 10.1111/ele.12435 25865946

13. Popa-Lisseanu AG, Voigt CC. Bats on the move. J Mammal. 2009; 90(6): 1283–1289.

14. Hutterer R, Ivanova T, Meyer-Cords C, Rodriques L. Bat migrations in Europe: a review of banding data and literature. Bonn: Federal Agency for Nature Conservation; 2005. 162 p.

15. Smeraldo S, Di Febbraro M, Bosso L, Flaquer C, Guixé D, Lisón F, et al. Ignoring seasonal changes in the ecological niche of non-migratory species may lead to biases in potential distribution models: lessons from bats. Biodiversity and conservation. 2018 Jul 1;27(9):2425–41.

16. Newton I. Incredible journeys. In: The Migration Ecology of Birds. Oxford: Academic Press; 2007. pp 139–161.

17. Hedenström A. Optimal migration strategies in bats. J Mammal. 2009; 90: 1298–1309.

18. Voigt CC, Sörgel K, Šuba J, Keišs O, Pētersons G. The insectivorous bat Pipistrellus nathusii uses a mixed-fuel strategy to power autumn migration. Proc R Soc Lond B Biol Sci. 2012; 279(1743): 3772–3778.

19. Dechmann DK, Wikelski M, Ellis-Soto D, Safi K, O'Mara MT. Determinants of spring migration departure decision in a bat. Biol lett. 2017;13(9): p. 20170395. doi: 10.1098/rsbl.2017.0395 28931730

20. Jonasson KA, Willis CK. Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PLoS one. 2011 Jun 22;6(6):e21061. doi: 10.1371/journal.pone.0021061 21731647

21. Boyles JG, Dunbar MB, Storm JJ, Brack V. Energy availability influences microclimate selection of hibernating bats. Journal of Experimental Biology. 2007 Dec 15;210(24):4345–50.

22. Wilkinson GS, South JM. Life history, ecology and longevity in bats. Aging cell. 2002 Dec;1(2):124–31. doi: 10.1046/j.1474-9728.2002.00020.x 12882342

23. Culina A, Linton DM, Pradel R, Bouwhuis S, Macdonald DW. Live fast, don't die young: Survival–reproduction trade‐offs in long‐lived income breeders. J Anim Ecol. 2019 Feb 8.

24. Petit E, Balloux F, Goudet J. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution. 2001; 55(3): 635–640. doi: 10.1554/0014-3820(2001)055[0635:sbdiam]2.0.co;2 11327171

25. Siemers BM, Stilz P, Schnitzler HU. The acoustic advantage of hunting at low heights above water: behavioural experiments on the European ‘trawling’bats Myotis capaccinii, M. dasycneme and M. daubentonii. J Exp Biol. 2001; 204(22): 3843–3854.

26. Haarsma AJ, Siepel H. Macro-evolutionary trade-offs as the basis for the distribution of European bats. Animal Biology. 2013 Jan 1;63(4):451–71.

27. Limpens HJGA, Lina PHC, Hutson AM. Action plan for the conservation of the pond bat in Europe (Myotis dasycneme). Convention on the Conservation of European Wildlife and Natural Habitats (Bern Convention). Strasbourg: Council of Europe, No.108; 2000.

28. Haarsma A.-J, Tuitert AH. Overview and evaluation of methodologies for locating summer roost of pond bats in the Netherlands. Lutra. 2009; 52(1): 47–64.

29. Fairon J. Vingt-cinq années de baguage des chiroptères en Belgique. Bull Inst Roy Sc nat Belg. 1967;43: 1–37.

30. Feldmann R. Das mitteleuropäische Areal der Teichfledermaus, Myotis dasycneme (Boie, 1825). Säugetierkundl. Mitt. 1963 May 1;11:68–72.

31. Gilson R. Notes sur le thermopreferendum et l'emplacement preferentiel du Vespertilion des marais (Myotis dasycneme, Boie 1825) pendant l'hibernation. Bull Centre Bag Rech Cheiropt Belg. 1978;5: 74–95.

32. Glas G. Aantalsontwikkelingen in zomerverblijfplaatsen van vleermuizen in kerken. Lutra. 1980;22: 84–94.

33. Limpens HJGA, Mostert K, Bongers W, editors. Atlas van de Nederlandse vleermuizen. Onderzoek naar verspreiding en ecologie. Utrecht: KNNV; 1997.

34. Roer H. Weitere Ergebnisse und Aufgaben der Fledermausberingung in Europa. Decheniana. 1971; 18: 121–144.

35. Libois R. Atlas provisoire des mammifères sauvages de Wallonie: distribution, ecologie, ethologie, conservation. Cah Ethol. 1982; 2(suppl. 1–2).

36. Haarsma A.-J. De meervleermuis in Nederland. Zoogdiervereniging VZZ, Nijmegen. 2012; Rapport nr. 2011.40; Electronic publication, available from: www.batweter.nl. Accessed May 2019.

37. Haarsma AJ, Van Duijnen B. Ruwe data meervleermuis (Myotis dasycneme). [internet]. Available from: www.vleermuizentellen.nl. Accessed May 2019.

38. Roer H. 60 years of bat banding in Europe—results and tasks for future research. Myotis. 1960; 32–33: 251–261.

39. Dense C, Taake K, Mäscher G. Sommer und Wintervorkommen von Teichfledermäusen (Myotis dasycneme) in Nordwestdeutschland. Myotis. 1996: 34: 71–79

40. Lindenschmidt M, Vierhaus H. Ergebnisse sechzehnjähriger Kontrollen in Fledermaus-Winterquartieren des Kreises Steinfurt. Abh Westf Mus. 1997; 59(3): 25–38.

41. Dietz M, Simon M (2003) Gutachten zur gesamthessischen Situation der Teichfledermaus Myotis dasycneme Verbreitung, Kenntnisstand, Gefährdung. Gießen: Hessisches Dienstleistungszentrum für Landwirtschaft, Gartenbau und Naturschutz; 2003.

42. Korn V. Besiedlung von winterquartieren der Teichfledermaus mit betrachtung des paarungs und sozialverhaltens. M. Sc. Thesis, Fachhochschule Osnabrück. 2008.

43. 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 (2): 124–132.

44. Verkem S, De Maeseneer J, Vandendriessche B, Verbeylen G, Yskout S. Zoogdieren in Vlaanderen. Ecologie en verspreiding van 1987 tot 2002. Mechelen & Gent: Natuupunt Studie & JNM-Zoogdierenwerkgroep; 2003.

45. Van de Sijpe M, Vandendriessche B, Voet P, Vandenberghe J, Duyck J, Naeyaert E, Manhaeve M, Martens E. Summer distribution of the Pond bat Myotis dasycneme (Chiroptera, Vespertilionidae) in the west of Flanders (Belgium) with regard to water quality. Mammalia. 2004; 68(4): 377–386.

46. Labes R. Reproduktion der Teichfledermaus, Myotis dasycneme (Boie, 1825), in Mecklenburg-Vorpommern. Nyctalus (N.F.). 1992; 4(4): 339–342.

47. Hemmer C. Wochenstube der Teichfledermaus (Myotis dasycneme) in Diethe, Landkreis Nienburg/Weser. Mitt AG Zoolog Heimatforschung. 1997; 3: 7–13.

48. Schikore T, Zimmerman M. Von der Flugstraße über den Wochenstubennachweis zum Quartier der Teichfledermaus (Myotis dasycneme) in der Wesermarscherster Fortpflanzungsnachweis dieser Art in Niedersachsen. Nyctalus (N.F.). 2000; 7(4): 383–395

49. Sluiter JW Van Heerdt PF. The results of bat banding in the Netherlands in 1952 and 1953. Natuurhist Maandbl. 1953; 42(11): 101–104.

50. Sluiter JW, Van Heerdt PF. The results of bat banding in the Netherlands in 1955. Natuurhist Maandbl. 1956; 45(5/6): 62–64.

51. Sluiter JW, Van Heerdt PF, Voûte AM. Contribution to the population biology of the pond bat, Myotis dascyneme (Boie, 1825). Decheniana. 1971; 18: 1–44.

52. Haarsma A-J, Van Schaik J, Bosch T, Janssen R (2012) Manual for assessment of reproductive status, age and health in European bats. Electronic publication. www.vleermuizenvangen.nl. Accessed April 2019.

53. McGuire LP, Kelly LA, Baloun DE, Boyle WA, Cheng TL, Clerc J, et al. Common condition indices are no more effective than body mass for estimating fat stores in insectivorous bats. Journal of Mammalogy. 2018 Sep 3;99(5):1065–71.

54. Reinink AW, Vermeulen JG. IJskelders koeltechnieken van weleer [ice cellars, former refrigerating engineering]. 1st ed. Mijdrecht: Uitgeverij Heuff Nieuwkoop; 1981.

55. Tzalmona R. Traces of the Atlantikwall or The Ruins that were Built to Last. Third Text. 2011; 25(6): 775–786.

56. Dijkstra V, Korsten E Handleiding wintertellen van vleermuizen [manual fort he survey of bat hibernacula].Zoogdiervereniging VZZ, Arhnem. 2005.

57. Willems W, Boers K, Vandendriesche B, Vanreusel W, Lefevre A. Monitoringhandleiding Natuurpunt Module F10, wintertelling vleermuizen. Electronic publication; 2009. Available from: www.natuurpunt.be. Accessed July 2018.

58. Masing M, Lutsar L. Hibernation temperatures in seven species of sedentary bats (Chiroptera) in northeastern Europe. Acta Zool Litu. 2007 Jan 1;17(1):47–55.

59. Punt A, Van Nieuwenhoven P. The use of radioactive bands in tracing hibernating bats. Cell Mol Life Sci. 1957; 13: 51–54.

60. Kugelschafter K. 25 Years of Bat Research at the Limestone Cave in Bad Segeberg. Bad Segeberg: presentation; 2014. Available from: www.zoogdiervereniging.nl. Accessed July 2018.

61. O'Shea TJ, Bogan MA, Ellison LE. Monitoring trends in bat populations of the United States and territories: status of the science and recommendations for the future. Digital commons University of Nebraska; 2003.

62. Hayes JP, Ober HK, Sherwin RE. Surveying and monitoring of bats. In: Kunz TH, Parsons S, editors. Ecological and Behavioral Methods for the Study of Bats. Baltimore: Johns Hopkins University Press; 2009. pp. 115–132.

63. Battersby J. Guidelines for Surveillance and Monitoring of European Bats. EUROBATS Publication Series. No. 5. UNEP/EUROBATS Secretariat, Bonn, Germany. ISBN 978–92–95058–27–9; 2010.

64. Pannekoek J, Van Strien A. TRIM 3 Manual (Trends & Indices for Monitoring data). Electronic publication Statistics Netherlands; 2005. Available from: www.cbs.nl. Accessed April 2018.

65. Czenze ZJ, Jonasson KA, Willis CK. Thrifty females, frisky males: winter energetics of hibernating bats from a cold climate. Physiological and Biochemical Zoology. 2017 Jul 1;90(4):502–11. doi: 10.1086/692623 28641050

66. O’Mara MT, Bauer K, Blank D, Baldwin JW, Dechmann DK. Common noctule bats are sexually dimorphic in migratory behaviour and body size but not wing shape. PloS one. 2016 Nov 23;11(11):e0167027. doi: 10.1371/journal.pone.0167027 27880791

67. Fleming TH, Eby P, Kunz TH, Fenton MB. Ecology of bat migration. Bat ecology. 2003;156:164–65.

68. McGuire LP, Jonasson KA, Guglielmo CG. Bats on a budget: torpor-assisted migration saves time and energy. PLoS One. 2014 Dec 31;9(12):e115724. doi: 10.1371/journal.pone.0115724 25551615

69. Jonasson KA, Guglielmo CG. Sex differences in spring migration timing and body composition of silver-haired bats Lasionycteris noctivagans. Journal of Mammalogy. 2016 Jul 25;97(6):1535–42.

70. Kerth G, Kiefer A, Trappmann C, Weishaar M. High gene diversity at swarming sites suggest hot spots for gene flow in the endangered Bechstein's bat. Conserv Genet. 2003 Jul 1;4(4):491–9.

71. Rivers NM, Butlin RK, Altringham JD. Autumn swarming behaviour of Natterer’s bats in the UK: population size, catchment area and dispersal. Biol cons. 2006 Jan 1;127(2):215–26.

72. Dekeukeleire D, Janssen R, Haarsma AJ, Bosch T, Van Schaik J. Swarming behaviour, catchment area and seasonal movement patterns of the Bechstein's bats: implications for conservation. Acta chiropterol. 2016 Dec 30;18(2):349–58.

73. Furmankiewicz J. Population size, catchment area, and sex-influenced differences in autumn and spring swarming of the brown long-eared bat (Plecotus auritus). Can J Zool. 2008 Feb 29;86(3):207–16.

74. Jahelková H, Horáček I. Mating system of a migratory bat, Nathusius' pipistrelle (Pipistrellus nathusii): different male strategies. Acta Chiropterologica. 2011 Jun 30;13(1):123–37.

75. Ruckstuhl KE, Kokko H. Modelling sexual segregation in ungulates: effects of group size, activity budgets and synchrony. Animal Behav. 2002 Dec 1;64(6):909–14.

76. Lidgard DC, Bowen WD, Boness DJ. Longitudinal changes and consistency in male physical and behavioural traits have implications for mating success in the grey seal (Halichoerus grypus). Can J Zool. 2012 Jun 22;90(7):849–60.

77. Burns LE, Broders HG. Who swarms with whom? Group dynamics of Myotis bats during autumn swarming. Behavioral ecology. 2015 Apr 3;26(3):866–76.

78. Toth CA, Parsons S. Is lek breeding rare in bats?. Journal of Zoology. 2013 Sep;291(1):3–11.

79. van Schaik J, Janssen R, Bosch T, Haarsma AJ, Dekker JJ, Kranstauber B. Bats swarm where they hibernate: compositional similarity between autumn swarming and winter hibernation assemblages at five underground sites. PLoS One. 2015 Jul 8;10(7):e0130850. doi: 10.1371/journal.pone.0130850 26153691

80. Veith M, Beer N, Kiefer A, Johannesen J, Seitz A. The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus). Heredity. 2004 Oct;93(4):342. doi: 10.1038/sj.hdy.6800509 15241447

81. Humphrey SR, Cope JB. Population ecology of the little brown bat, Myotis lucifugus, in Indiana and north-central Kentucky. Special Publication of the American Society of Mammalogists. 1976; 4:1–81.

82. Parsons KN, Jones G, Davidson-Watts I, Greenaway F. Swarming of bats at underground sites in Britain—implications for conservation. Biological Conservation. 2003 May 1;111(1):63–70.

83. Zahn A, Dippel B. Male roosting habits and mating behaviour of Myotis myotis. J. Zool. (Lond), 1997; 243(4): 659–674.

84. Heckel G, von Helversen O. Male tactics and reproductive success in the harem polygynous bat Saccopteryx bilineata. Behav Ecol. 2002 Nov 1;13(6):750–6.

85. Rossiter SJ, Jones G, Ransome RD Barratt EM. Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proc R Soc Lond, B Biol Sci. 2000; 267: 545–551.

86. Kerth G, van Schaik J. Causes and consequences of living in closed societies: lessons from a long‐term socio‐genetic study on Bechstein’s bats. Molecular ecology. 2012 Feb;21(3):633–46. doi: 10.1111/j.1365-294X.2011.05233.x 21883583


Článek vyšel v časopise

PLOS One


2019 Číslo 10