Cave-dwelling bats do not avoid TMT and 2-PT - Components of predator odour that induce fear in other small mammals

Journal of Experimental Biology

Volumn 213, Issue 14, 2010, Pages 2453-2460

  Driessens, Tess ^a,b   Siemers, Björn M ^a  

^a MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

2 PT; Bats; Least weasel; Myotis myotis; Olfaction; Predator recognition; Scent; TMT

Indexed keywords

2,4,5 TRIMETHYLTHIAZOLINE; THIAZOLE DERIVATIVE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; AVOIDANCE BEHAVIOR; BAT; CHEMISTRY; ENVIRONMENT; FEAR; FEMALE; MAZE TEST; METABOLISM; ODOR; PHYSIOLOGY; PREDATION;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CHIROPTERA; ENVIRONMENT; FEAR; FEMALE; MAZE LEARNING; ODORS; PREDATORY BEHAVIOR; THIAZOLES;

ACRIDA; ANIMALIA; CAPRA HIRCUS; MAMMALIA; MUSTELA NIVALIS; MUSTELIDAE; MYOTIS; MYOTIS MYOTIS; OCIMUM; RODENTIA;

EID: 77954048656     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.044743     Document Type: Article

References (91)

1. Amo, L., Galvan, I., Tomas, G. and Sanz, J. J. (2008). Predator odour recognition and avoidance in a songbird. Funct. Ecol. 22, 289-293. (Pubitemid 351416625)
2. Antoniadis, E. A. and McDonald, R. J. (1999). Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav. Brain Res. 101, 113.
3. Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A. and McGregor, I. S. (2005). The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29, 1123-1144. (Pubitemid 41446891)
4. Arlettaz, R. (1996). Feeding behaviour and foraging strategy of free-living mouseeared bats, Myotis myotis and Myotis blythii. Anim. Behav. 51, 1-11. (Pubitemid 3017075)
5. Avanzi, V., Castilho, V. M., de Andrade, T. and Brandao, M. L. (1998). Regulation of contextual conditioning by the median raphe nucleus. Brain Res. 790, 178-184.
6. Barclay, R. M. R., Thomson, C. E. and Phelan, F. J. S. (1982). Screech owl, Otus asio, attempting to capture little brown bats, Myotis lucifugus, at a colony. Can. Field Nat. 96, 205-206.
7. Baxter, D. J. M., Psyllakis, J. M., Gillingham, M. P. and O'Brien, E. L. (2006). Behavioural response of bats to perceived predation risk while foraging. Ethology 112, 977-983.
8. Bekker, J. P. (1988). Daubenton's bat Myotis daubentoniias prey of beech marten Martes foina in subterranean marl pits. Lutra 31, 82-85.
9. Berger, J. (1999). Anthropogenic extinction of top carnivores and interspecific animal behaviour: implications of the rapid decoupling of a web involving wolves, bears, moose and ravens. Proc. R. Soc. Lond. B. Biol. Sci. 266, 2261-2267.
10. Bert on, F., Vogel, E. and Belzung, C. (1998). Modulation of mice anxiety in response to cat odor as a consequence of predators diet. Physiol. Behav. 65, 247-254.
11. Blanchard, D. C., Markham, C., Yang, M., Hubbard, D., Madarang, E. and Blanchard, R. J. (2003). Failure to produce conditioning with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav. Neurosci. 117, 360-368. (Pubitemid 36384254)
12. Bloss, J. (1999). Olfaction and the use of chemical signals in bats. Acta Chiropterol. 1, 31-45.
13. Bloss, J., Aeree, T. E., Bloss, J. M., Hood, W. R. and Kunz, T. H. (2002). Potential use of chemical cues for colony-mate recognition in the big brown bat, Eptesicus fuscus. J. Chem. Ecol. 28, 819-834. (Pubitemid 34498947)
14. Bolbroe, T., Jeppesen, L. L. and Leirs, H. (2000). Behavioural response of field voles under mustelid predation risk in the laboratory: more than neophobia. Ann. Zool. Fenn. 37, 169-178.
15. Borowski, Z. (2002). Individual and seasonal differences in antipredatory behaviour of root voles-a field experiment. Can. J. Zool. Rev. Can. Zool. 80, 1520-1525.
16. Bouchard, S. (2001). Sex discrimination and roostmate recognition by olfactory cues in the African bats, Mops condylurus and Chaerephon pumilus (Chiroptera: Molossidae). J. Zool. 254, 109-117.
17. Bouskila, A. and Blumstein, D. T. (1992). Rules of thumb for predation hazard assessment: predictions from a dynamic model. Am. Nat. 139, 161-176.
18. Boyles, J. G. and Storm, J. J. (2007). Avoidance of predator chemical cues by bats: an experimental assessment. Behaviour144, 1019-1032.
19. Burwash, M. D., Tobin, M. E., Woolhouse, A. D. and Sullivan, T. P. (1998). Field testing synthetic predator odors for roof rats (Rattus rattus) in Hawaiian macadamia nut orchards. J. Chem. Ecol. 24, 603-630.
20. Caro, T. (2005). Antipredator Defenses in Birds and Mammals. Chicago: The University of Chicago Press.
21. Caspers, B. A., Schroeder, F. C., Franke, S., Streich, W. J. and Voigt, C. C. (2009). Odour-based species recognition in two sympatric species of sac-winged bats (Saccopteryx bilineata, S. ieptura): combining chemical analyses, behavioural observations and odour preference tests. Behav. Ecol. Sociobioi. 63, 741-749.
22. Castilho, V. M. and Brandao, M. L. (2001). Conditioned antinociception and freezing using electrical stimulation of the dorsal periaqueductal gray or inferior colliculus as unconditioned stimulus are differentially regulated by 5-HT2A receptors in rats. Psychopharmacoiogy 155, 154-162.
23. Chivers, D. P. and Smith, R. J. F. (1994). The role of experience and chemical alarm signaling in predator recognition by fathead minnows, Pimephales prometas. J. Fish Biol. 44, 273-285.
24. Conover, M. R. and Perito, J. J. (1981). Response of starlings to distress calls and predator models holding conspecific prey. Z Tierpsychol./J. Comp. Ethol. 57, 163-172.
25. Defanis, E. and Jones, G. (1995). The role of odor in the discrimination of conspecifics by pipistrelle bats. Anim. Behav. 49, 835-839.
26. Dielenberg, R. A. and McGregor, I. S. (2001). Defensive behavior in rats towards predatory odors: a review. Neurosci. Biobehav. Rev. 25, 597-609.
27. Eisenberg, J. F. (1983). The Mammalian Radiations: an Analysis of Trends in Evolution, Adaptation, and Behavior. Chicago: University of Chicago Press.
28. Estok, P., Zsebok, S. and Siemers, B. M. (2010). Great tits search for, capture, kill and eat hibernating bats. Biol. Lett. 6, 59-62.
29. Fendt, M. and Endres, T. (2008). 2,3,5-Trimethyl-3-thiazoline (TMT), a component of fox odor-Just repugnant or really fear-inducing? Neurosci. Biobehav. Rev. 32, 1259-1266.
30. Fendt, M., Endres, T., Lowry, C. A., Apfelbach, R. and McGregor, I. S. (2005). TMT-induced autonomic and behavioral changes and the neural basis of its processing. Neurosci. Biobehav. Rev. 29, 1145-1156. (Pubitemid 41446892)
31. Fenton, M. B., Rautenbach, I. L., Smith, S. E., Swanepoel, C. M., Grosell, J. and Vanjaarsveld, J. (1994). Raptors and bats -threats and opportunities. Anim. Behav. 48, 9-18.
32. Ferrara, F. J. and Leberg, P. L. (2005). Characteristics of positions selected by dayroosting bats under bridges in Louisiana. J. Mammal. 86, 729-735.
33. Findley, J. S. and Wilson, D. E. (1974). Observations on neotropical disk-winged bat, Thyroptera tricolor Spix. J. Mammal. 55, 562-571.
34. Fuelling, O. and Halle, S. (2004). Breeding suppression in free-ranging grey-sided voles under the influence of predator odour. Oecologia 138, 151-159. (Pubitemid 38161947)
35. Goodpaster, W. and Hoffmeister, D. F. (1950). Bats as prey for mink in Kentucky cave. J. Mammal. 31, 457-457.
36. Griffin, A. S. (2004). Social learning about predators: a review and prospectus. Learn. Behav. 32, 131-140.
37. Gustin, M. K. and McCracken, G. F. (1987). Scent recognition between females and pups in the bat Tadarida brasiliensis mexicana. Anim. Behav. 35, 13-19.
38. Hanson, M. T. and Coss, R. G. (1997). Age differences in the response of California ground squirrels (Spermophilus beecheyi) to avian and mammalian predators. J. Comp. Psychol. 111, 174-184.
39. Heale, V. R. and Vanderwolf, C. H. (1994). Toluene and weasel (2-propylthietane) odors suppress feeding in the rat. J. Chem. Ecol. 20, 2953-2958.
40. Hutchinson, J. T. and Lacki, M. J. (2000). Selection of day roosts by red bats in mixed mesophytic forests. J. Wildl. Manage. 64, 87-94.
41. Jedrzejewski, W. and Jedrzejewska, B. (1990). Effect of a predator's visit on the spatial distribution of bank voles: experiments with weasels. Can. J. Zool./Rev. Can. Zool. 68, 660-666.
42. Jenkins, E. V., Laine, T., Morgan, S. E., Cole, K. R. and Speakman, J. R. (1998). Roost selection in the pipistrelle bat, Pipistrellus pipistrellus (Chiroptera: Vespertilionidae), in northeast Scotland. Anim. Behav. 56, 909-917. (Pubitemid 28494537)
43. Jones, G. and Rydell, J. (1994). Foraging strategy and predation risk as factors influencing emergence time in echolocating bats. Philos. Trans. R. Soc. B. Biol. Sci. 346, 445-455.
44. Kalcounis, M. C. and Brigham, R. M. (1994). Impact of predation risk on emergence by little brown bats, Myotis lucifugus (Chiroptera, Vespertilionidae), from a maternitiy colony. Ethology 98, 201-209.
45. Kats, L. B. and Dill, L. M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience5, 361-394.
46. Koivisto, E. and Pusenius, J. (2003). Effects of temporal variation in the risk of prédation by least weasel (Mustela nivalis) on feeding behavior of field vole (Microtus agrestis). Evol. Ecol. 17, 477-489. (Pubitemid 38047147)
47. Korpimaki, E., Koivunen, V. and Hakkarainen, H. (1996). Microhabitat use and behavior of voles under weasel and raptor predation risk: predator facilitation? Behav. Ecol. 7, 30-34. (Pubitemid 126624966)
48. Kramer, G. and Von St. Paul, U. (1951). Über angeborenes und erworbenes Feinderkennen beim Gimpel (Pyrrhula pyrrhula L.). Behaviour 3, 243-255.
49. Kunz, T. H. (1982). Ecology of Bats. Dordrecht: Springer.
50. Laska, M., Fendt, M., Wieser, A., Endres, T., Salazar, L. T. H. and Apfelbach, R. (2005). Detecting danger-or just another odorant? Olfactory sensitivity for the fox odor component 2,4,5-trimethylthiazoline in four species of mammals. Physiol. Behav. 84, 211-215.
51. Lewis, S. E. (1995). Roost fidelity of bats - a review. J. Mammal. 76, 481-496.
52. Luft, S., Curio, E. and Tacud, B. (2003). The use of olfaction in the foraging behaviour of the golden-mantled flying fox, Pteropus pumilus, and the greater musky fruit bat, Ptenochirus jagori (Megachiroptera: Pteropodidae). Naturwissenschaften 90, 84-87. (Pubitemid 36286906)
53. Mateo, J. M. and Holmes, W. G. (1997). Development of alarm-call responses in Belding's ground squirrels: the role of dams. Anim. Behav. 54, 509-524. (Pubitemid 27413933)
54. McGowan, K. J. and Woolfenden, G. E. (1989). A sentinel system in the Florida scrub jay. Anim. Behav. 37, 1000-1006.
55. McGregor, I. S., Schrama, L., Ambermoon, P. and Dielenberg, R. A. (2002). Not all 'predator odours' are equal: cat odour but not 2,4,5 trimethylthiazoline (TMT; fox odour) elicits specific defensive behaviours in rats. Behav. Brain Res. 129, 1-16. (Pubitemid 34059221)
56. Medway, L. and Marshall, A. G. (1972). Roosting associations of flat-headed bats, Tylonycteris spp. (Chiroptera - Vespertilionidae) in Malaysia. J. Zool. 168, 463-&.
57. Mistry, S. and McCracken, G. F. (1990). Behavioral response of the Mexican freetailed bat, Tadarida brasiliensis mexicana, to visible and infrared light. Anim. Behav. 39, 598-599.
58. Mumford, R. E. (1969). Long-tailed weasel preys on big brown bats. J. Mammal. 50, 360.
59. Neuweiler, G. (2000). The Biology of Bats. New York: Oxford University Press.
60. Petrzelkova, K. and Zukal, J. (2001). Emergence behaviour of the serotine bat (Eptesicus serotinus) under predation risk. Netherl. J. Zool. 51, 395-414.
61. Petrzelkova, K. J. and Zukal, J. (2003). Does a live barn owl (Tyto alba) affect emergence behavior of serotine bats (Eptesicus serotinus)? Acta Chiropterol. 5, 177-184.
62. Punzo, F. (2005). Chemosensory recognition by males of the desert pocket mouse, Chaetodipus pencillatus, to odors of various species of snakes. Ethol. Ecol. Evol. 17, 83-89.
63. Rieger, J. F. and Jakob, E. M. (1988). The use of olfaction in food location by frugivorous bats. Biotropica 20, 161-164.
64. Riskin, D. K. and Fenton, M. B. (2001). Sticking ability in Spix's disk-winged bat, Thyroptera tricolor (Microchiroptera: Thyropteridae). Can. J. Zool./Rev. Can. Zool. 79, 2261-2267.
65. Riskin, D. K. and Pybus, M. J. (1998). The use of exposed diurnal roosts in Alberta by the little brown bat, Myotis lucifugus. Can. J. Zool./Rev. Can. Zool. 76, 767-770.
66. Roth, T. C., Cox, J. G. and Lima, S. L. (2008). Can foraging birds assess predation risk by scent? Anim. Behav. 76, 2021-2027.
67. Ruczynski, I. and Bogdanowicz, W. (2005). Roost cavity selection by Nyctalus noctula and N. leisten (Vespertilionidae, Chiroptera) in Bialowieza Primeval Forest, eastern Poland. J. Mammal. 86, 921-930.
68. Ruprecht, A. L. (1979). Bats (Chiroptera) as constituents of the food of barn owls Tyto alba in Poland. Ibis 121, 489-494.
69. Russ, J. M., Racey, P. A. and Jones, G. (1998). Intraspecific responses to distress calls of the pipistrelle bat, Pipistrellus pipistrellus. Anim. Behav. 55, 705-713.
70. Rydell, J. and Speakman, J. R. (1995). Evolution of nocturnality in bats - potential competitors and predators during their early history. Biol. J. Linn. Soc. 54, 183-191.
71. Schmidley, D. J. (1991). The Bats of Texas. College Station, Texas: Texas A and M University Press.
72. Sih, A. and Kats, L. B. (1994). Age, experience, and the response of streamside salamander hatchlings to chemical cues from predatory sunfish. Ethology 96, 253-259.
73. Sparks, D. W., Roberts, K. J. and Jones, C. (2000). Vertebrate predators on bats in North America north of Mexico. In Reflections of a Naturalist: Papers Honoring Professor Eugene D. Fleharty, pp. 229-241. Hays: Fort Hays State University.
74. Speakman, J. R. (1995). Chiropteran nocturnality. In Ecology, Evolution and Behaviour of Bats(eds P. A. Racey and S. M. Swift), pp. 187-201. Oxford: Clarendon Press.
75. Speakman, J. R., Stone, R. E. and Kerslake, J. E. (1995). Temporal patterns in the emergence behavior of pipistrelle bats, Pipistrellus pipistrellus, from maternity colonies are consistent with an antipredator response. Anim. Behav. 50, 1147-1156.
76. Stoddart, D. M. (1980). Some responses of a free-living community of rodents to the odors of predators. In Chemical Signals: Vertebrates and Aquatic Invertebrates (ed. D. Muller-Schwarze and R. M. Silverstein). New York: Plenum Publishing.
77. Sullivan, T. P., Crump, D. R. and Sullivan, D. S. (1988a). Use of predator odors as repellents to reduce feeding damage by herbivores. III: Montane and meadow voles (Microtus montanus and Microtus pennsylvanicus). J. Chem. Ecol. 14, 363-378.
78. Sullivan, T. P., Crump, D. R. and Sullivan, D. S. (1988b). Use of predator odors as repellents to reduce feeding damage by herbivores. IV: Northern pocket gophers (Thomomys talpoides). J. Chem. Ecol. 14, 379-390.
79. Sullivan, T. P., Crump, D. R., Wieser, H. and Dixon, E. A. (1990). Response of pocket gophers (Thomomys talpoides) to an operational application of synthetic semiochemicals of stoat (Mustela erminea). J. Chem. Ecol. 16, 941-949.
80. Thomas, R. S., Glen, D. M. and Symondson, W. O. C. (2008). Prey detection through olfaction by the soil-dwelling larvae of the carabid predator Pterostichus meianarius. Soil Biol. Biochem. 40, 207-216.
81. Tryjanowski, P. (1997). Food of fire stone marten (Martes foina) in Nietoperek Bat Reserve. Z Saugetier./internat. J. Mammal. Biol. 62, 318-320.
82. VanDamme, R. and Castilla, A. M. (1996). Chemosensory predator recognition in the lizard Podareis hispanica: Effects of predation pressure relaxation. J. Chem. Ecol. 22, 13-22.
83. Vernetmaury, E., Polak, E. H. and Demael, A. (1984). Structure-activity relationship of stress-inducing odourants in the rat. J. Chem. Ecol. 10, 1007-1018.
84. Voigt, C. C. and von Helversen, O. (1999). Storage and display of odour by male Saccopteryx biiineata (Chiroptera, Emballonuridae). Behav. Ecol. Sociobioi. 47, 29-40.
85. von Helversen, O., Winkler, L. and Bestmann, H. J. (2000). Sulphur-containing 'perfumes' attract flower-visiting bats. J. Comp. Physiol. A 186, 143-153.
86. Vonhof, M. J. and Barclay, R. M. R. (1997). Use of tree stumps as roosts by the western long-eared bat. J. Wildl. Manage. 61, 674-684.
87. Wallace, K. J. and Rosen, J. B. (2000). Predator odor as an unconditioned fear stimulus in rats: elicitation of freezing by trimethylthiazoline, a component of fox feces. Behav. Neurosci. 114, 912-922.
88. Weldon, P. J. (1990). Responses by vertebrates to chemicals from predators. In Chemical Signals in Vertebrates 5, pp. 500-521. Oxford: Oxford University Press.
89. Woolhouse, A. D. and Morgan, D. R. (1995). An evaluation of repellents to suppress browsing by possums. J. Chem. Ecol. 21, 1571-1583.
90. Yancey, F. D., Roberts, K. J. and Jones, C. (1996). Prairie falcon predation on Brazilian free-tailed bats. Prairie Natural 28, 146-147.
91. Zar, J. H. (1999). Biostatistical Analysis. Upper Saddle River: Prentice Hall.