Are torpid bats immune to anthropogenic noise?

Journal of Experimental Biology

Volumn 217, Issue 7, 2014, Pages 1072-1078

  Luo, Jinhong ^a,b   Clarin, B Markus ^a   Borissov, Ivailo M ^a   Siemers, Björn M ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b NORTHEAST NORMAL UNIVERSITY   (China)

Author keywords

Anthropogenic noise; Habituation; Myotis myotis; Roosting bat; Torpor; Traffic noise

Indexed keywords

ADAPTATION; ANIMAL; AUDITORY STIMULATION; BAT; BULGARIA; HABITUATION; NOISE; PHYSIOLOGY; PSYCHOLOGY; SKIN TEMPERATURE; TORPOR;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; BULGARIA; CHIROPTERA; HABITUATION, PSYCHOPHYSIOLOGIC; NOISE; SKIN TEMPERATURE; TORPOR;

EID: 84907487382     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.092890     Document Type: Article

References (61)

1. Abbott, I. M., Harrison, S. and Butler, F. (2012). Clutter-adaptation of bat species predicts their use of under-motorway passageways of contrasting sizes - a natural experiment. J. Zool. (Lond.) 287, 124-132.
2. Altringham, J. D. (2012). Bats: From Evolution to Conservation. New York, NY: Oxford University Press.
3. Audet, D. and Thomas, D. W. (1996). Evaluation of the accuracy of body temperature measurement using external radio transmitters. Can. J. Zool. 74, 1778-1781.
4. Barclay, R. M. R., Kalcounis, M. C., Crampton, L. H., Stefan, C., Vonhof, M. J., Wilkinson, L. and Brigham, R. M. (1996). Can external radiotransmitters be used to assess body temperature and torpor in bats? J. Mammal. 77, 1102-1106.
5. Bayne, E. M., Habib, L. and Boutin, S. (2008). Impacts of chronic anthropogenic noise from energy-sector activity on abundance of songbirds in the boreal forest. Conserv. Biol. 22, 1186-1193.
6. Bergmann, H. H., Helb, H. W. and Baumann, S. (2008). Die Stimmen der Vögel Europas: 474 Vogelporträts mit 914 Rufen und Gesängen auf 2200 Sonagrammen. Wiebelsheim: Aula.
7. Berthinussen, A. and Altringham, J. (2012). Do bat gantries and underpasses help bats cross roads safely? PLoS ONE 7, e38775.
8. Boyles, J. G., Cryan, P. M., McCracken, G. F. and Kunz, T. H. (2011). Conservation. Economic importance of bats in agriculture. Science 332, 41-42.
9. Brumm, H. (2010). Anthropogenic noise: implications for conservation. In Encyclopedia of Animal Behavior, Vol. 1 (ed. M. D. Breed and J. Moore), pp. 89-93. Oxford: Academic Press.
10. Brumm, H. and Slabbekoorn, H. (2005). Acoustic communication in noise. Adv. Stud. Behav. 35, 151-209.
11. Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach. New York, NY: Springer-Verlag.
12. Burnham, K., Anderson, D. and Huyvaert, K. (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav. Ecol. Sociobiol. 65, 23-35.
13. Carey, H. V., Andrews, M. T. and Martin, S. L. (2003). Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 83, 1153-1181.
14. Coats, A. C. (1965). Temperature effects on the peripheral auditory apparatus. Science 150, 1481-1483.
15. Dietz, C., Helversen, O. V. and Nill, D. (2009). Bats of Britain, Europe & Northwest Africa. London: A & C Black Publisher.
16. Foote, A. D., Osborne, R. W. and Hoelzel, A. R. (2004). Environment: whale-call response to masking boat noise. Nature 428, 910-910.
17. Forman, R. T. T. and Alexander, L. E. (1998). Roads and their major ecological effects. Annu. Rev. Ecol. Syst. 29, 207-231.
18. Francis, C. D., Paritsis, J., Ortega, C. and Cruz, A. (2011). Landscape patterns of avian habitat use and nest success are affected by chronic gas well compressor noise. Landscape Ecol. 26, 1269-1280.
19. Geiser, F. (2004). Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66, 239-274.
20. Haarsma, A.-J. and De Hullu, E. (2012). Keeping bats cool in the winter: hibernating bats and their exposure to 'hot' incandescent lamplight. Wildl. Biol. 18, 14-23.
21. Halfwerk, W., Holleman, L. J. M., Lessells, C. M. and Slabbekoorn, H. (2011a). Negative impact of traffic noise on avian reproductive success. J. Appl. Ecol. 48, 210-219.
22. Halfwerk, W., Bot, S., Buikx, J., Van Der Velde, M., Komdeur, J., Ten Cate, C. and Slabbekoorn, H. (2011b). Low-frequency songs lose their potency in noisy urban conditions. Proc. Natl. Acad. Sci. USA 108, 14549-14554.
23. Harrison, J. B. (1965). Temperature effects on responses in the auditory system of the little brown bat Myotis lucifugus. Physiol. Zool. 38, 34-48.
24. Hoffmann, S., Baier, L., Borina, F., Schuller, G., Wiegrebe, L. and Firzlaff, U. (2008). Psychophysical and neurophysiological hearing thresholds in the bat Phyllostomus discolor. J. Comp. Physiol. A 194, 39-47.
25. Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65-70.
26. Humphries, M. M., Thomas, D. W. and Speakman, J. R. (2002). Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418, 313-316.
27. Kerth, G. and Melber, M. (2009). Species-specific barrier effects of a motorway on the habitat use of two threatened forest-living bat species. Biol. Conserv. 142, 270-279.
28. Kiefer, A., Merz, H., Rackow, W., Roer, H. and Schlegel, D. (1995). Bats as traffic casualties in Germany. Myotis 32-33, 215-220.
29. Körtner, G. and Geiser, F. (2000). The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol. Int. 17, 103-128.
30. Kristoffersson, R. E. and Soivio, A. (1964). Hibernation in the Hedgehog (Erinaceus europaeus L.): Changes of Respiratory Pattern, Heart Rate and Body Temperature in Response to Gradually Decreasing or Increasing Ambient Temperature. Annales Academiae scientiarum Fennicae, Series A 4, Biologica, Vol. 82. Helsinki: Suomalainen tiedeakatemia.
31. Kunz, T. H., Braun De Torrez, E., Bauer, D., Lobova, T. and Fleming, T. H. (2011). Ecosystem services provided by bats. Ann. New York Acad. Sci. 1223, 1-38.
32. Leonard, M. L. and Horn, A. G. (2005). Ambient noise and the design of begging signals. Proc. Biol. Sci. 272, 651-656.
33. Lesinski, G., Sikora, A. and Olszewski, A. (2011). Bat casualties on a road crossing a mosaic landscape. Eur. J. Wildl. Res. 57, 217-223.
34. Lovegrove, B. G. (2009). Modification and miniaturization of Thermochron iButtons for surgical implantation into small animals. J. Comp. Physiol. B 179, 451-458.
35. Luther, D. and Baptista, L. (2010). Urban noise and the cultural evolution of bird songs. Proc. Biol. Sci. 277, 469-473.
36. Lyman, C. P., Willis, J., Malan, A. and Wang, L. C. H. (1982). Hibernation and Torpor in Mammals and Birds. New York, NY: Academic Press.
37. Neuweiler, G. (1990). Auditory adaptations for prey capture in echolocating bats. Physiol. Rev. 70, 615-641.
38. Neuweiler, G. (2000). The Biology of Bats. New York, NY: Oxford University Press.
39. Park, K. J., Jones, G. and Ransome, R. D. (2000). Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct. Ecol. 14, 580-588.
40. Parks, S. E., Johnson, M., Nowacek, D. and Tyack, P. L. (2011). Individual right whales call louder in increased environmental noise. Biol. Lett. 7, 33-35.
41. Pfalzer, G. and Kusch, J. (2003). Structure and variability of bat social calls: implications for specificity and individual recognition. J. Zool. (Lond.) 261, 21-33.
42. Rankin, C. H., Abrams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., Coppola, G., Geyer, M. A., Glanzman, D. L., Marsland, S. et al. (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol. Learn. Mem. 92, 135-138.
43. 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. J. Zool. 164, 353-371.
44. Reijnen, R. and Foppen, R. (2006). Impact of road traffic on breeding bird populations. In The Ecology of Transportation: Managing Mobility for the Environment, Vol. 10 (ed. J. Davenport and J. L. Davenport), pp. 255-274. Netherlands: Springer.
45. Rolland, R. M., Parks, S. E., Hunt, K. E., Castellote, M., Corkeron, P. J., Nowacek, D. P., Wasser, S. K. and Kraus, S. D. (2012) Evidence that ship noise increases stress in right whales. Proc. Biol. Sci. 279, 2363-2368.
46. Rossi, G. T. and Britt, R. H. (1984). Effects of hypothermia on the cat brainstem auditory evoked response. Electroencephalogr. Clin. Neurophysiol. 57, 143-155.
47. Rydell, J. (1992). Exploitation of insects around streetlamps by bats in Sweden. Funct. Ecol. 6, 744-750.
48. Schaub, A., Ostwald, J. and Siemers, B. M. (2008). Foraging bats avoid noise. J. Exp. Biol. 211, 3174-3180.
49. Schroeder, J., Nakagawa, S., Cleasby, I. R. and Burke, T. (2012). Passerine birds breeding under chronic noise experience reduced fitness. PLoS ONE 7, e39200.
50. Schwarz, B. (2007). Behavioural audiogram of greater mouse-eared bat (Myotis myotis): ears adapted for detecting rustling prey? Masters thesis, University of Tübingen, 64pp.
51. Siemers, B. M. and Schaub, A. (2011). Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators. Proc. Biol. Sci. 278, 1646-1652.
52. Speakman, J. R. and Thomas, D. W. (2003). Physiological ecology and energetics of bats. In Bat Ecology (ed. T. H. Kunz and M. B. Fenton), pp. 430-490. Chicago, IL: University of Chicago Press.
53. Speakman, J. R., Webb, P. I. and Racey, P. A. (1991). Effects of disturbance on the energy expenditure of hibernating bats. J. Appl. Ecol. 28, 1087-1104.
54. Stone, E. L., Jones, G. and Harris, S. (2009). Street lighting disturbs commuting bats. Curr. Biol. 19, 1123-1127.
55. Stone, E. L., Jones, G. and Harris, S. (2012). Conserving energy at a cost to biodiversity? Impacts of LED lighting on bats. Glob. Change Biol. 18, 2458-2465.
56. Thomas, D. W. (1995). Hibernating bats are sensitive to nontactile human disturbance. J. Mammal. 76, 940-946.
57. Thompson, R. F. (2009). Habituation: a history. Neurobiol. Learn. Mem. 92, 127-134.
58. Turbill, C., Körtner, G. and Geiser, F. (2008). Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of lesser long-eared bats. J. Exp. Biol. 211, 3871-3878.
59. Twente, J. W. and Twente, J. A. (1968). Progressive irritability of hibernating Citellus lateralis. Comp. Biochem. Physiol. 25, 467-474.
60. Willis, C. K. R. (2007). An energy-based body temperature threshold between torpor and normothermia for small mammals. Physiol. Biochem. Zool. 80, 643-651.
61. Withers, P. C. (1992). Comparative Animal Physiology. Philadelphia, PA: Saunders College Publishing.