Bats and moths: What is there left to learn?

Physiological Entomology

Volumn 28, Issue 4, 2003, Pages 237-250

  Waters, Dean A ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Bat; Coevolution; Moth; Neuroethology; Temporal integration; Ultrasound

Indexed keywords

ADAPTATION; BAT; BIOACOUSTICS; COEVOLUTION; ECHOLOCATION; MOTH; PREDATOR-PREY INTERACTION;

LEPIDOPTERA; PROTEA;

EID: 0348196706     PISSN: 03076962     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3032.2003.00355.x     Document Type: Review

References (131)

1. Acharya, L. & Fenton, M.B. (1992) Echolocation behaviour of vespertillionid bats (Lasiurus cinereus and Lasiurus borealis) attacking airborne targets including arctiid moths. Canadian Journal of Zoology, 70, 1292-1298.
2. Acharya, L. & Fenton, M.B. (1999) Bat attacks and moth defensive behaviour around street lights. Canadian Journal of Zoology, 77, 27-33.
3. Adams, W.B. (1972) Mechanical tuning of the acoustic receptor of Prodenia eridania (Cramer) (Noctuidae). Journal of Experimental Biology, 57, 297-304.
4. Bailey, W.J. (1978) Resonant wing systems in the Australian whistling moth Hecatesia (Agaristidae, Lepidoptera). Nature, 272, 444-446.
5. Bates, D.L. & Fenton, M.B. (1990) Aposematism or startle? Predators learn their responses to the defences of prey. Canadian Journal of Zoology, 68, 49-52.
6. Belton, P. (1956) Responses to sound in pyralid moths. Nature, 196, 1198-1199.
7. Blest, A.D., Collett, T.S. & Pye, J.D. (1963) The generation of ultrasonic clicks by a new world arctiid moth. Proceedings of the Royal Society of London B, 158, 196-207.
8. Bogdanowicz, W., Fenton, M.B. & Daleszczyk, K. (1999) The relationships between echolocation calls, morphology and diet in insectivorous bats. Journal of Zoology, London, 247, 381-393.
9. Boyan, G.S. & Fullard, J.H. (1988) Information processing at a central synapse suggests a noise filter in the auditory pathway of a noctuid moth. Journal of Comparative Physiology A, 164, 251-258.
10. Conner, W.E. (1987) Ultrasound: its role in the courtship of arctiid moth, Cycnia tenera. Experientia, 43, 1029-1031.
11. Conner, W.E. (1999) 'Un chant d'appel amoureaux': acoustic communication in moths. Journal of Experimental Biology, 202, 1711-1723.
12. Cook, M.A. & Scoble, M.J. (1992) Tympanal organs of geometrid moths: review of their morphology, function and systematic importance. Systematic Entomology, 17, 219-232.
13. Coro, F. & Pérez, M. (1984) Intensity coding by auditory receptors in Empyreuma pugione (Lepidoptera, Ctenuchidae). Journal of Comparative Physiology A, 154, 287-295.
14. Coro, F., Pérez, M. & Machado, A. (1994) Effects of temperature on a moth auditory receptor. Journal of Comparative Physiology A, 174, 517-525.
15. Dooling, R. (1980) Behaviour and psychophysics of hearing in birds. Comparative Studies of Hearing in Vertebrates (ed. by A. Popper and R. Fay), pp. 261-288. Springer, Berlin.
16. Douglass, J.K., Wilkens, L., Pantazelou, E. & Moss, F. (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature, 365, 337-340.
17. Driver, P.M. & Humphries, D.A. (1988) Protean Behaviour: The Biology of Unpredictability. Oxford University Press, Oxford.
18. Dunning, D.C. (1968) Warning sounds of moths. Zeitschrift für Tierpsychology, 25, 129-138.
19. Dunning, D.C. & Roeder, K.D. (1965) Moth sounds and the insect catching behaviour of bats. Science, 147, 173-174.
20. Dunning, D.C., Acharya, L., Merriman, C.B. & Dal Ferro, L. (1992) Interactions between bats and arctiid moths. Canadian Journal of Zoology, 70, 2218-2223.
21. Eggers, F. (1911) Über das thoracale tympanale-organ der Noctuiden. Sitzungsberichte der Naturforscher-Gellenschaft bei der Universität Tartu (Dorpat), 30, 138-145.
22. Eggers, F. (1919) Das thoracale bitypanale organ einer gruppe der Lepidoptera Heterocera. Zoologische Jahrbuecher Abteilung für Anatomie und Ontogenie der Tiere, 41, 273-376.
23. Eggers, F. (1925) Versuche über das Gehör der Noctuiden. Zeitschrift für Vergleichende Physiologie, 2, 297-314.
24. Ewing, A.W. (1989) Arthropod Bioacoustics. Edinburgh University Press, Edinburgh.
25. Faure, P.A., Fullard, J.H. & Barclay, M.R. (1990) The response of tympanate moths to the echolocation calls of a substrate gleaning bat, Myotis evotis. Journal of Comparative Physiology A, 166, 843-849.
26. Faure, P.A., Fullard, J.H. & Dawson, J.W. (1993) The gleaning attacks of the northern long-eared bat, Myotis septentrionalis are relatively inaudible to moths. Journal of Experimetal Biology, 178, 173-189.
27. Fenton, M.B. & Fullard, J.H. (1979) The influence of moth hearing on at echolocation strategies. Journal of Comparative Physiology, 132, 77-86.
28. Forbes, W.T.M. (1916) On the tympanum of certain lepidoptera. Psyche, 23, 183-192.
29. Fullard, J.H. (1979) Behavioral analyses of auditory sensitivity in Cycnia tenera (Lepidoptera: Arctiidae). Journal of Comparative Physiology, 129, 79-83.
30. Fullard, J.H. (1982) Echolocation assemblages and their effects on moth auditory systems. Canadian Journal of Zoology, 60, 2572-2576.
31. Fullard, J.H. (1984a) Acoustic relationships between tympanate moths and the Hawaiian hoary bat (Lasiurus cinnereus semotus). Journal of Comparative Physiology A, 155, 795-801.
32. Fullard, J.H. (1984b) Listening for bats: pulse repetition rate as a cue for defensive behaviour in Cycnia tenera (Lepidoptera: Arctiidae). Journal of Comparative Physiology A, 154, 249-252.
33. Fullard, J.H. (1988) The tuning of moth ears. Experientia, 44, 423-428.
34. Fullard, J.H. (1992) The neuroethology of sound production in tiger moths (Lepidoptera, Arctiidae). I. Rhythmicity and central control. Journal of Comparative Physiology A, 170, 575-588.
35. Fullard, J.H. (1994) Auditory changes in noctuid moths endemic to a bat-free habitat. Journal of Evolutionary Biology, 7, 435-445.
36. Fullard, J.H. & Dawson, J.W. (1997) The echolocation calls of the spotted bat (Euderma maculatum) are relatively inaudible to moths. Journal of Experimental Biology, 200, 129-137.
37. Fullard, J.H. & Heller, B. (1990) Functional organization of the arctiid moth tymbal (Insecta, Lepidoptera). Journal of Morphology, 204, 57-65.
38. Fullard, J.H. & Napoleone, N. (2001) Diel flight periodicity and the evolution of auditory defences in the Macrolepidoptera. Animal Behaviour, 62, 349-368.
39. Fullard, J.H. & Thomas, D.W. (1981) Detection of certain African insectivorous bats by sympatric tympanate moths. Journal of Comparative Physiology, 143, 363-368.
40. Fullard, J.H., Fenton, M.B. & Simmons, J.A. (1979) Jamming bat echolocation: the clicks of arctiid moths. Canadian Journal of Zoology, 57, 647-649.
41. Fullard, J.H., Simmons, J.A. & Saillant, P.A. (1994) Jamming bat echolocation: the dogbane tiger moth Cycnia tenera times its clicks to the terminal attack calls of the big brown bat Eptesicus fuscus. Journal of Experimental Biology, 194, 285-298.
42. Fullard, J.H., Dawson, J.W., Otero, L.D. & Surlykke, A. (1997) Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae). Journal of Comparative Physiology A, 181, 477-483.
43. Fullard, J.H., Dawson, J.W. & Jacobs, D.S. (2003a) Auditory encoding during the last moments of a moth's life. Journal of Experimental Biology, 206, 281-294.
44. Fullard, J.H., Muma, K.E. & Dawson, J.W. (2003b) Quantifying an anti-bat flight response by eared moths. Canadian Journal of Zoology, 81, 395-399.
45. Futuyma, D.J. & Slatkin, M. (1983) Coevolution. Sinauer, Massachusetts.
46. Ghiradella, H. (1971) Fine structure of the noctuid moth ear I. The transducer area and connections to the tympanic membrane in Feltia subgothica. Journal of Morphology, 134, 21-46.
47. Greenfield, M.D. & Weber, T. (2000) Evolution of ultrasonic signaling in wax moths: discrimination of ultrasonic mating calls from bat echolocation signals and the exploitation of an anti-predator receiver bias by sexual advertisement. Ethology Ecology and Evolution, 12, 259-279.
48. Griffin, D.R. (1958) Listening in the Dark. Yale University Press, Comstock.
49. Griffin, D.R. (1971) The importance of atmospheric attenuation for the echolocation calls of bats. Animal Behaviour, 19, 55-61.
50. Griffin, D.R. & Galambos, R. (1941) The sensory basis of obstacle avoidance by flying bats. Journal of Experimental Zoology, 86, 481-506.
51. Hinton, H.E. (1955) Sound producing organs in the Lepidoptera. Proceedings of the Royal Entomological Society London, 20, 5-14.
52. Holloway, J.D., Brandly, J.D. & Carter, D.J. (1987) CIE Guides to Insects of Importance to Man I. Lepidoptera. CAB International Institute of Entomology, British Museum of Natural History.
53. Hoy, R.R. & Robert, D. (1996) Tympanal hearing in insects. Annual Revue of Entomology, 41, 433-450.
54. Janzen, D.H. (1980) When is it coevolution? Evolution, 34, 611-612.
55. Jones, G. (1992) Bats vs moths: studies on the diets of rhinolophid and hipposiderid bats support the allotonic frequency hypothesis. Prague Studies in Mammalogy (ed. by I. Horáček and V. Vohralik), pp. 87-92. Charles University Press, Prague.
56. Jones, G. & Waters, D.A. (2000) Moth hearing in response to bat echolocation calls manipulated independently in time and frequency. Proceedings of the Royal Society B, 267, 1627-1632.
57. Jones, G., Barabas, A., Elliott, W. & Parsons, S. (2001) Female greater wax moths reduce sexual display behaviour in relation to the potential risk of predation by echolocating bats. Behavioral Ecology, 13, 375-380.
58. Jordan, K. (1905) Note on a peculiar secondary sexual character found among Geometridae at the sensory organ situated at the base of the abdomen. Novitates Zoologicae, 12, 506-170.
59. Krasnoff, S.B. & Yager, D.D. (1988) Acoustic response to a pheromonal cue in the arctiid moth Pyrrharctia isabella. Physiological Entomology, 13, 433-440.
60. Lechtenberg, R. (1971) Acoustic responses in the B cell in noctuid moths. Journal of Insect Physiology, 17, 2395-2408.
61. Lewis, F. & Fullard, J.H. (1996) Neurometamorphosis of the ear in the gypsy moth, Lymantria dispar, and its homologue in the earless forest tent caterpillar moth, Malacoscoma disstria. Journal of Neurobiology, 31, 245-262.
62. Lewis, F., Fullard, J.H. & Morrill, S. (1993) Auditory influences on the flight behaviour of of moths at a nearctic siet. II. Flight times, heights and erracticism. Canadian Journal of Zoology, 71, 1562-1568.
63. Madsen, B.M. & Miller, L.A. (1987) Auditory input to motor neurons of the dorsal longitudinal flight muscles in a noctuid moth (Barathra brassicae L.). Journal of Comparative Physiology A, 160, 23-31.
64. McIndoo, N.B. (1929) Tropisms and sense organs of Lepidoptera. USNM Smithsonian Miscellaneous. Collections, 81, 1-59.
65. Miller, L.A. (1991) Arctiid moth clicks can degrade the accuracy of range difference discrimination in echolocating big brown bats, Eptesicus fuscus. Journal of Comparative Physiology A, 168, 571-579.
66. Minet, J. (1983) Etude morphologique et phylogénétigue des organes tympaniques des Pyraloidea. 1. Généralities et homologies. Annales de la Société Entomologique de France, 19, 175-207.
67. Morril, S.B. & Fullard, J.H. (1992) Auditory influences on the flight behaviour of moths in a Nearctic site I. Flight tendency. Canadian Journal of Zoology, 70, 1097-1101.
68. Norberg, U.M. & Rayner, J.M.V. (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London, 316, 335-427.
69. Norman, A.P. & Jones, G. (2000) Size, peripheral auditory tuning and target strength in noctuid moths. Physiological Entomology, 25, 346-353.
70. Nüesch, H. (1953) The morphology of the thorax of Telea polyphemus (Lepidoptera) I. Skeleton and muscles. Journal of Morphology, 93, 589-608.
71. Nüesch, H. (1957) Die morphologie des thorax von Telea polyphemus Cr. (Lepid.) II Nervensystem. Zoologische Jahrbuecher Abteilung für Anatomie und Ontogenie der Tiere, 75, 615-642.
72. Pérez, M. & Coro, F. (1984) Physiological characteristics of the tympanic organ in noctuid moths. I. responses to brief acoustic pulses. Journal of Comparative Physiology A, 154, 441-441.
73. Pérez, M. & Coro, F. (1985) Physiological characteristics of the tympanic organ in noctuid moths II. Responses to 45 ms and 5 s acoustic stimuli. Journal of Comparative Physiology A, 156, 689-696.
74. Plomp, R. & Bouman, M.A. (1959) Relation between hearing thresholds and duration for tone pulses. Journal of the Acoustic Society of America, 31, 749-758.
75. Richards, A.G. (1932) Comparative skeletal morphology of the noctuid tympanum. Entomologica Americana, 13, 1-43.
76. Roeder, K.D. (1962) The behaviour of free flying moths in the presence of artificial ultrasonic pulses. Animal Behaviour, 10, 300-304.
77. Roeder, K.D. (1967) Turning tendency of moths exposed to ultrasound while in stationary flight. Journal of Insect Physiology, 13, 873-888.
78. Roeder, K.D. (1969) Nerve Cells and Insect Behaviour. Harvard University Press, Cambridge.
79. Roeder, K.D. (1972) Acoustic and mechanicals sensitivity of the distal lobe of the pilifer; an ultrasonic receptor in choerocampine hawkmoths. Journal of Insect Physiology, 18, 1249-1264.
80. Roeder, K.D. (1975) Neural factors and evitability in insect behaviours. Journal of Experimental Zoology, 194, 75-88.
81. Roeder, K.D. & Treat, A.E. (1956) Electrical responses of the noctuid tympanum to ultrasonic stimulation. Proceedings of the 10th International Congress of Zoology, 2, 117-120.
82. Roeder, K.D. & Treat, A.E. (1957) Ultrasonic reception by the tympanic organ of noctuid moths. Journal of Experimental Zoology, 134, 127-157.
83. Rydell, J. & Arlettaz, R. (1994) Low-frequency echolocation enables the bat Tadarida teniotis to feed on tympanate insects. Proceedings of the Royal Society of London B, 257, 175-178.
84. Rydell, J., Jones, G. & Waters, D.A. (1995) Echolocating bats and hearing moths: who are the winners? Oikos, 73, 419-424.
85. Rydell, J., Roininen, H. & Philip, K.W. (2000) Persistence of bat defence reactions in high Arctic moths (Lepidoptera). Proceedings of the Royal Society of London B, 267, 553-557.
86. Rydell, J., Skals, N., Surlykke, A. & Svenson, M. (1997) Hearing and bat defence in geometrid winter moths. Proceedings of the Royal Society of London B, 254, 83-88.
87. Schaller, F. & Timm, C. (1949) Schallreaktionen bi Nachtfaltern. Experientia, 5, 162.
88. Schaller, F. & Timm, C. (1950) Das Hörvermögen der Nachtschmetterlinge. Zeitschrift für Vergleichende Physiologie, 32, 468-481.
89. Schiolten, P., Larsen, O.N. & Michelsen, A. (1981) Mechanical time resolution in some insect ears I. Impulse responses and time constants. Journal of Comparative Physiology, 143, 289-295.
90. Schnitzler, H.-U. (1968) Die ultraschall-ortungslante der hufeisenfledermause (Chiroptera: Rhinolophidae) in verscheiden orientierungssituationen. Zeitschrift für Vergleichende Physiologie, 57, 376-408.
91. Schnitzler, H.-U. (1987) Echoes of fluttering insects: information for echolocating bats. Recent Advances in the Study of Bats (ed. by M.B. Fenton, P. Racey and J.M.V. Rayner), pp. 226-243. Cambridge University Press, Cambridge.
92. Schnitzler, H.-U. & Kalko, E.K.V. (2001) Echolocation by insect-eating bats. Bioscience, 51, 557-569.
93. Scoble, M.J. (1995) The Lepidoptera: Form, Function and Diversity. Oxford University Press, Oxford.
94. Sharp, D. (1899) Cambridge Natural History: Volume 6. Insects. Macmillan, London.
95. Simmons, R.B. & Conner, W.E. (1996) Ultrasonic signals in the defense and courtship of Euchaetes egle Drury and E. bolteri Stretch (Lepidoptea: Arctiidae). Journal of Insect Behaviour, 9, 909-919.
96. Skals, N. & Surlykke, A. (2000) Hearing and evasive behaviour in the greater wax moth Galleria mellonella. Physiological Entomology, 25, 354-362.
97. Sneddon, W.A., Tosh, C.R. & Ritchie, M.G. (1994) The ultrasonic signal of the male lesser wax moth. Phsiological Entomology, 19, 367-372.
98. Snodgrass, R.E. (1926) The morphology of the insect sense organs and the sensory nervous system. USNM Miscellaneous Collections, 11, 1-80.
99. Spangler, H.G. (1988) Moth hearing, defense and communication. Annual Revue of Entomology, 33, 59-81.
100. Speakman, J.R. & Rydell, J. (2000) Avoidance behaviour of bats and moths: when is it predator defence? Oikos, 88, 221-223.
101. Surlykke, A. (1984) Hearing in Notodontid moths: a tympanic organ with a single auditory neurone. Journal of Experimental Biology, 113, 323-335.
102. Surlykke, A. (1986) Moth hearing on the Faeroe islands, an area without bats. Physiological Entomology, 11, 221-225.
103. Surlykke, A. & Fullard, J.H. (1989) Hearing of the Australian whistling moth, Hecatesia thyridion. Naturwissenschaften, 76, 132-134.
104. Surlykke, A. & Miller, L.A. (1982) Central branchings of three sensory axons from a moth ear (Agrotis segetum). Journal of Insect Physiology, 28, 357-364.
105. Surlykke, A., Larsen, O.N. & Michelsen, A. (1988) Temporal coding in the auditory receptor of the moth ear. Journal of Comparative Physiology A, 162, 367-374.
106. Surlykke, A., Filskov, M., Fullard, J.H. & Forrest, E. (1999) Auditory relationships to size in noctuid moths: bigger is better. Naturwissenschaften, 86, 238-241.
107. Svensson, M.G.E., Rydell, J. & Brown, R. (1999) Bat predation and flight timing of winter moths, Epirrita and Operophtera species (Lepidoptera, Geometridae). Oikos, 84, 193-198.
108. Svensson, G.P., Skals, N. & Löfstedt, C. (2003) Disruption of the odour-mediated mating behaviour of Plodia interpunctella using high frequency sound. Entomologica Experimentalis et Applicata, 106, 187-192.
109. Swinton (1877) On an organ of hearing in insects with special reference to Lepidoptera. Entomologists Monthly Magazine, 14, 121-126.
110. Thompson, J.N. (1994) The Coevolutionary Process. University of Chicago Press, Chicago.
111. Tougaard, J. (1996) Energy detection and temporal integration in the noctuid A1 auditory receptor. Journal of Comparative Physiology A, 178, 669-677.
112. Tougaard, J. (1998) Detection of short pure-tone stimuli in the noctuid ear: what are temporal integration and integration time all about? Journal of Comparative Physiology A, 183, 563-572.
113. Tougaard, J. (2000) Stochastic resonance and signal detection in an energy detector - implications for biological receptor systems. Biology Cybernetics, 83, 471-480.
114. Tougaard, J., Casseday, J.H. & Covey, E. (1998) Arctiid moths and bat echolocation: broad-band clicks interfere with neural responses to auditory stimuli in the buclei of the lateral lemniscus of the big brown bat. Journal of Comparative Physiology A, 182, 203-215.
115. Treat, A.E. (1955) The response to sound in certain Lepidoptera. Annals of the Entomological Society of America, 48, 272-284.
116. Treat, A.E. (1959) The metathoracic musculature of Crymodes devastator (Brace) (Noctuidae) with special reference to the tympanic organ. Studies in Invertebrate Morphology, pp. 262-270, Smithsonian Institution, Washington, DC.
117. Treat, A.E. & Roeder, K.D. (1959) A nervous element of unknown function in the tympanic organs of moths. Journal of Insect Physiology, 3, 262-270.
118. Vaughan, N. (1997) The diets of British bats. Mammal Revue, 27, 77-94.
119. Viemeister, N.F. & Wakefield, G.H. (1991) Temporal integration and multiple looks. Journal of the Acoustic Society of America, 90, 858-865.
120. von Kennel, J. (1912) Über tympanal-organe im abdomen der Spanner und Zünsler. Zoologischer Anzeiger, 39, 163-170.
121. von Kennel, J. & Eggers, F. (1933) Die abdominalen Tympanalorgane der Lepidopteren. Zoologishe Jahrbücher Abteilung für Anatomie und Ontogenie der Tiere, 57, 1-105.
122. Waters, D.A. (1996) The peripheral auditory characteristics of noctuid moths: information encoding and endogenous noise. Journal of Experimental Biology, 199, 857-868.
123. Waters, D.A. & Jones, G. (1994) Wingbeat generated ultrasound in noctuid moths increases the discharge rate of the bat-detecting A1 cell. Proceedings of the Royal Society B, 258, 41-46.
124. Waters, D.A. & Jones, G. (1995) Echolocation call structure and intensity in five species of insectivorous bats. Journal of Experimental Biology, 198, 475-489.
125. Waters, D.A. & Jones, G. (1996) The peripheral auditory characteristics of noctuid moths: responses to the search-phase echolocation calls of bats. Journal of Experimental Biology, 199, 857-868.
126. Waters, D.A., Rydell, J. & Jones, G. (1995) Echolocation call design and limits on prey size: a case study using the aerial-hawking bat Nyctalus leisleri. Behavioral Ecology and Sociobiology, 37, 321-328.
127. White, F.B. (1877) Untitled communication. Nature, 15, 293.
128. Yack, J.E. & Fullard, J.H. (1993) Proprioceptive activity of the wing-hinge stretch receptor in Manduca sexta and other atympanate moths: a study of the noctuoid moth ear B cell homologue. Journal of Comparative Physiology A, 173, 301-307.
129. Yack, J.E. & Fullard, J.H. (2000) Ultrasonic hearing in nocturnal butterflies. Nature, 403, 265-266.
130. Yack, J.E., Scudder, G.G.E. & Fullard, J.H. (1999) Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera. Zoomorphology, 119, 93-103.
131. Zwislocki, J.J. (1960) Theory of temporal auditory summation. Journal of the Acoustic Society of America, 32, 1046-1060.