Winter activity of bats in Mediterranean peri-urban deciduous forests

• Autorzy: Barros P.A. , Ribeiro C. , Cabral J.A.
• Języki publikacji: EN

Abstrakty

EN

Although the Vespertilionid bats typically hibernate during the winter to minimize energy expenditure in the cold months, in the temperate regions torpor breaks can be rather frequent. The aim of our study was to conduct a preliminary characterisation of the winter bat activity patterns in Mediterranean peri-urban deciduous forests of North Portugal. Echolocation calls were recorded between November and February, and bat activity was regularly detected on warm evenings, with sun set temperatures above 4.6°C during the night sampling, mostly in November (89.9%), only rarely in December (3.7%) and February (6.4%) and without activity detected in January. The most commonly recorded species were Pipistrellus pygmaeus, P. pipistrellus, and P. kuhlii. Socialization activity was mostly concentrated in November (96.8%), only with rare records in February (3.2%) and absent in December and January. Regarding the best fitting average model, obtained by the Multi-Model Inference (MMI) method to explaining the variation of bat passes, the main positive influencing factors are related with the night period of the monitoring process and temperature, and the negative influence with the precipitation recorded in the last 48 hours before surveys. The MMI results for the variation of social calls revealed as significant positive influences the humidity, temperature and wind speed and as negative influence the precipitation recorded in the last 48 hours before surveys. We outline our study as a promising baseline to the studies of winter bat activity, demonstrating how the present and past weather conditions can play a major role in bat torpor breaks. Therefore, for conservation purposes, further winter acoustic research efforts should be consider mandatory for full understanding the bat activity patterns facing the potential impacts of global climatic changes expected to occur in the Mediterranean region.

• Wydawca: -
• Czasopismo: Acta Chiropterologica
• Rocznik: 2017
• Tom: 19
• Numer: 2
• Opis fizyczny: p.367-377,fig.,ref.

Twórcy

autor

Barros P.A.

• Laboratory of Applied Ecology, University of Tras-os-Montes and Alto Douro (UTAD), Vila Real, Portugal

autor

Ribeiro C.

• Laboratory of Applied Ecology, University of Tras-os-Montes and Alto Douro (UTAD), Vila Real, Portugal

autor

Cabral J.A.

• Laboratory of Applied Ecology, University of Tras-os-Montes and Alto Douro (UTAD), Vila Real, Portugal
• Centre for the Research and Technology of Agro-Environment and Biological Sciences (CITAB), University of Tras-os-Montes and Alto Douro (UTAD), Vila Re

Bibliografia

• 1. Adam, D. S., and S. R. McWilliams. 2016. Bat activity during autumn relates to atmospheric conditions: implications for coastal wind energy development. Journal of Mammalogy, 97: 1565–1577. Google Scholar
• 2. Ancillotto, L., L. Santini, N. Ranc, L. Maiorano, and D. Russo. 2016. Extraordinary range expansion in a common bat: the potential roles of climate change and urbanisation. The Science of Nature, 103: 1–8. Google Scholar
• 3. Araújo, M. B., F. Guilhaumon, R. D. Neto, O. I. Pozo, and G. R. Calmaestra. 2011. Impactos, vulnerabilidad y adaptación al cambio climático de la biodiversidad Española. 2. Fauna de vertebrados. Ministerio de Medio Ambiente y Medio Rural y Marino, Madrid, 640 pp. Google Scholar
• 4. Avery, M. I. 1985. Winter activity of pipistrelle bats. Journal of Animal Ecology, 54: 721–738. Google Scholar
• 5. Barataud, M. 2015. Acoustic ecology of European bats. Species identification, studies of their habitats and foraging behaviour. Collection Inventaires et Biodiversité. Biotope Editions, Mèze and Muséum National d'Histoire Naturelle, Paris, 340 pp. Google Scholar
• 6. Barlow, K. E., and G. Jones. 1997. Function of pipistrelle social calls: field data and a playback experiment. Animal Behaviour, 53: 991–999. Google Scholar
• 7. Bartoñ, K. 2016. Mumin: Multi-Model Inference. R package version 1.15.6. Available at https://CRAN.R-project.org/package=MuMIn. Google Scholar
• 8. Boyles, J. G., M. B. Dunbar, and J. O. Whitaker, Jr . 2006. Activity following arousal in winter in North American vespertilionid bats. Mammal Review, 36: 267–280. Google Scholar
• 9. Boyles, J. G., M. B. Dunbar, J. J. Storm, and V. Brack, Jr . 2007. Energy availability influences microclimate selection of hibernating bats. Journal of Experimental Biology, 210: 4345–4350. Google Scholar
• 10. Brigham, R. M. 1987. The significance of winter activity by the big brown bat (Eptesicus fuscus): the influence of energy reserves. Canadian Journal of Zoology, 65: 1240–1242. Google Scholar
• 11. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multi model inference: a practical information-theoretic approach. Springer, New York, 488 pp. Google Scholar
• 12. Choi, I. H., Y. Cho, Y. K. Oh, N. P. Jung, and H. C. Shin. 1998. Behavior and muscle performance in heterothermic bats. Physiological and Biochemical Zoology, 71: 257–266. Google Scholar
• 13. Clawson, R. L., R. K. Laval, M. L. Laval, and W. Caire. 1980. Clustering behavior of hibernating Myotis sodalis in Missouri. Journal of Mammalogy, 61: 245–253. Google Scholar
• 14. Correia, C. M., J. F. Coutinho, E. A. Bacelar, B. M. Gonçalves, L. O. Björn, and J. M. Pereira. 2012. Ultraviolet-B radiation and nitrogen affect nutrient concentrations and the amount of nutrients acquired by above-ground organs of maize. The Scientific World Journal, 1: 1–11. Google Scholar
• 15. Czenze, Z. J., and C. K. R. Willis. 2015. Warming up and shipping out: arousal and emergence timing in hibernating little brown bats (Myotis lucifugus). Journal of Comparative Physiology, 185B: 575–586. Google Scholar
• 16. Daan, S. 1973. Activity during natural hibernation in three species of vespertilionid bats. Netherlands Journal of Zoology, 23: 1–71. Google Scholar
• 17. Downs, N. C., and P. A. Racey. 2007. Temporal and spatial differences in the emission of calls by pipistrelle bats Pipistrellus pipistrellus and P. pygmaeus. Acta Theriologica, 52: 55–64. Google Scholar
• 18. Elith, J., C. H. Graham, R. P. Anderson, M. Ferrier, S. Dudík, A. Guisan, R. J. Hijmans, F. Huettmann, J. R. Leathwick, A. Lehmann , et al. 2006. Novel methods improve prediction of species' distributions from occurrence data. Ecography, 29: 129–151. Google Scholar
• 19. Erkert, H. G. 1982. Ecological aspects of bat activity rhythms. Pp. 201–242, in Ecology of bats ( T. H. Kunz, ed.). Plenum Press, New York, xviii + 425 pp. Google Scholar
• 20. Giorgi, F., and P. Lionello. 2008. Climate change projections for the Mediterranean region. Global and Planetary Change, 63: 90–104. Google Scholar
• 21. Halsall, A. L., J. G. Boyles, and J. O. Whitaker, Jr . 2012. Body temperature patterns of big brown bats during winter in a building hibernaculum. Journal of Mammalogy, 93: 497–503. Google Scholar
• 22. Hays, G. C., J. R. Speakman, and P. I. Webb. 1992. Why do brown longeared bats (Plecotus auritus) fly in winter? Physiological Zoology, 65: 554–567. Google Scholar
• 23. Hope, P. R., K. Bohmann, and M. T. P. Gilbert. 2014. Second generation sequencing and morphological faecal analysis reveal unexpected foraging behaviour by Myotis nattereri (Chiroptera, Vespertilionidae) in winter. Frontiers in Zoology, 11(1): 39. Google Scholar
• 24. Humphries, M. M., D. W. Thomas, and D. L. Kramer. 2003. The role of energy availability in mammalian hibernation: a cost benefit approach. Physiological and Biochemical Zoology, 76: 165–179. Google Scholar
• 25. Johnson, J. S., M. J. Lacki, S. C. Thomas, and J. F. Grider. 2012. Frequent arousals from winter torpor in Rafinesque's big-eared bat (Corynorhinus rafinesquii). PLoS ONE, 7: e49754. Google Scholar
• 26. Jonasson, K. A., and C. K. R. Willis. 2011. Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PLoS ONE, 6: e21061. Google Scholar
• 27. Jones, G., and H. Rebelo. 2013. Responses of bats to climate change: learning from the past and predicting the future. Pp. 457–478, in Bat evolution, ecology, and conservation ( R. A. Adams and S. C. Pedersen, eds.). Springer, New York, 640 pp. Google Scholar
• 28. Jones, G., P. L. Duvergé, and R. D. Ransome. 1995. Conservation biology of na endangered species: field studies of greater horseshoe bats. Symposia of the Zoological Society of London, 67: 309–324. Google Scholar
• 29. Kokurewicz, T. 2004. Sex and age related habitat selection and mass dynamics of Daubenton's bats Myotis daubentonii (Kuhl, 1817) hibernating in natural conditions, Acta Chiropterologica, 6: 121–144. Google Scholar
• 30. Luis, A. D., and O. J. Hudson. 2006. Hibernation patterns in mammals: a role for bacterial growth? Functional Ecology, 20: 471–477. Google Scholar
• 31. Lundy, M., I. Montgomery, and J. Russ. 2010. Climate changelinked range expansion of Nathusius' pipistrelle bat, Pipistrellus nathusii (Keyserling & Blasius, 1839). Journal of Biogeography, 37: 2232–2242. Google Scholar
• 32. Martin, Y., H. Van Dyck, N. Dendoncker, and N. Titeux. 2013. Testing instead of assuming the importance of landuse change scenarios to model species distributions under climate change. Global Ecology and Biogeography, 22: 1204–1216. Google Scholar
• 33. Mendes, E. S., M. J. Ramos Pereira, S. F. Marques, and C. Fonseca. 2014. A mosaic of opportunities? Spatio-temporal patterns of bat diversity and activity in a strongly humanized Mediterranean wetland. European Journal of Wildlife Research, 60: 651–664. Google Scholar
• 34. Meserve, P. L., H. Hernan Vásquez, D. A. Kelt, J. R Gutierrez, and W. B. Milstead. 2016. Patterns in arthropod abundance and biomass in the semiarid thorn scrub of Bosque Fray Jorge National Park, north-central Chile: a preliminary assessment. Journal of Arid Environments, 126: 68–75. Google Scholar
• 35. Miková, E., K. Varcholová, S. Boldogh, and M. Uhrin. 2013. Winter diet analysis in Rhinolophus euryale (Chiroptera). Central European Journal of Biology, 8: 848–853. Google Scholar
• 36. Nunes, L., S. T. Gower, S. D. Peckham, M. Magalhães, D. Lopes, and F. C. Rego. 2014. Estimation of productivity in pine and oak forests in the north of Portugal using Biome-BGC. Forestry, 88: 200–212. Google Scholar
• 37. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics, 37: 637–669. Google Scholar
• 38. R CORE TEAM. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/. Google Scholar
• 39. Racey, P. A. 1974. The temperature of a pipistrelle hibernaculum. Jounal of Zoology (London), 173: 260–262. Google Scholar
• 40. Rainho, A., P. Alves, F. Amorim, and J. T. Marques. 2013. Atlas dos morcegos de Portugal continental. Instituto da Conservação da Natureza e das Florestas, Lisboa, 76 pp + appendices. Google Scholar
• 41. Ransome, R. D. 1971. The effect of ambient temperature on the arousal frequency of the hibernating greater horseshoe bat, Rhinolophus ferrumequinum, in relation to site selection and the hibernation state. Journal of Zoology (London), 164: 353–371. Google Scholar
• 42. Rebelo, H., P. Tarroso, and G. Jones. 2010. Predicted impact of climate change on European bats in relation to their biogeographic patterns. Global Change Biology, 16: 561–576. Google Scholar
• 43. Rodrigues, L., L. Bach, M. J. Dubourg-Savage, J. Goodwin, and C. Harbusch. 2008. Guidelines for consideration of bats in wind farm projects. EUROBATS Publication Series No. 3 (English version), 51 pp. Google Scholar
• 44. Russo, D., and G. Jones. 2003. Use of foraging habitats by bats in a Mediterranean area determined by acoustic surveys: conservation implications. Ecography, 26: 197–209. Google Scholar
• 45. Schwab, N. A., and T. J. Mabee. 2014. Winter acoustic activity of bats in Montana. Northwestern Naturalist, 95: 13–27. Google Scholar
• 46. Sherwin, H. A., W. I. Montgomery, and M. G. Lundy. 2013. The impact and implications of climate change for bats. Mammal Review, 43: 171–182. Google Scholar
• 47. Shono, H. 2000. Efficiency of the finite correction of Akaike's information criteria. Fisheries Science, 66: 608–610. Google Scholar
• 48. Smith, A., M. C. Schoeman, M. Keith, B. F. M. Erasmus, A. Monadjem, A. Moilanen, and E. Minin. 2016. Synergistic effects of climate and land-use change on representation of African bats in priority conservation areas. Ecological Indicators, 69: 276–283. Google Scholar
• 49. Stawski, C., C. K. R. Willis, and F. Geiser. 2014. The importance of temporal heterothermy in bats. Journal of Zoology (London), 292: 86–100. Google Scholar
• 50. Taylor, L. R. 1963 Analysis of the effects of temperature on insects in flight. Journal of Animal Ecology, 32: 99–117. Google Scholar
• 51. Thomas, D. W., and F. Geiser. 1997. Periodic arousals in hibernating mammals: is evaporative water loss involved ? Functional Ecology, 11: 585–591. Google Scholar
• 52. Trachsel, L., D. M. Edgar, and H. C. Heller. 1991. Are ground-squirrels sleep-deprived during hibernation. American Journal of Physiology, 260: R1123–R1129. Google Scholar
• 53. Turbill, C. 2008. Winter activity of Australian tree-roosting bats: influence of temperature and climatic patterns. Journal of Zoology (London), 276: 285–290. Google Scholar
• 54. Turbill, C., and F. Geiser. 2008. Hibernation by tree-roosting bats. Journal of Comparative Physiology, 178B: 597–605. Google Scholar
• 55. Van Breukelen, F., and S. L. Martin. 2002. Reversible depression of transcription during hibernation. Journal of Comparative Physiology, 172B: 355–361. Google Scholar
• 56. Vaughan, N., G. Jones, and J. G. A. Limpens. 1997. Habitat use by bats (Chiroptera) assessed by means of a broad-band acoustic method. Applied Ecology, 34: 716–730. Google Scholar
• 57. Walther, G. R., E. Post, P. Convey, A. Menze, C. Parmesan, T. J. C. Beebee, J. M. Fromentin, O. Hoegh-Guldberg, and F. Bairlein. 2002. Ecological responses to recent climate change. Nature, 416: 389–395. Google Scholar
• 58. Weller, T. J., and J. A. Baldwin. 2012. Using echolocation monitoring to model bat occupancy and inform mitigations at wind energy facilities. Journal of Wildlife Management, 76: 619–631. Google Scholar
• 59. Wermundsen, T., and Y. Siivonen. 2010. Seasonal variation in use of winter roosts by five bat species in south-east Finland. Central European Journal of Biology, 5: 262–273. Google Scholar
• 60. White, J. A., B. R. Andersen, H. W. Otto, C. A. Lemen, and P. W. Freeman. 2014. Winter activity of bats in south eastern Nebraska: an acoustic study. Transactions of the Nebraska Academy of Sciences and Affiliated Societies, 34: 80–83. Google Scholar
• 61. Wisz, M., and A. Guisan. 2009. Do pseudo-absence selection strategies affect geographic predictions of species? A virtual species approach. BMC Ecology, 9: 8. Google Scholar
• 62. Zahn, A., and E. Kriner. 2016. Winter foraging activity of Central European vespertilionid bats. Mammalian Biology, 81: 40–45. Google Scholar
• 63. Zar, J. H., 2010. Biostatistical analysis, 5th edition. Pearson Prentice Hall, Upper Saddle River, N.J., 944 pp. Google Scholar
• 64. Zukal, J., H. Berková, and Z. Řehák. 2005. Activity and shelter selection by Myotis myotis in the Kateřinská cave (Czech Republic). Mammalian Biology, 70: 271–281. Google Scholar

Identyfikatory

DOI

10.3161/15081109ACC2017.19.2.013