It's not black or white-on the range of vision and echolocation in echolocating bats

Frontiers in Physiology

Volumn 4 SEP, Issue , 2013, Pages

  Boonman, Arjan ^a   Bar On, Yinon ^a   Cvikel, Noam ^a   Yovel, Yossi ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Eocene; Foxp2; Hearing gene; Oilbird; Pteropodidae; Swiftlet; Yangochiroptera; Yinpterochiroptera

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BAT; COMPARATIVE STUDY; DARK ADAPTATION; DEPTH PERCEPTION; ECHOLOCATION; EVOLUTION; FORAGING; LIGHT INTENSITY; NONHUMAN; PHOTOPIC VISION; PIPISTRELLUS KUHLII; PREY SELECTION; RHINOPOMA MICROPHYLLUM; THEORETICAL STUDY; VISION; VISUAL ACUITY; VISUAL ADAPTATION; VISUAL FIELD;

EID: 84884558211     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00248     Document Type: Article

References (79)

1. Altringham, J. D., and Fenton, B. M. (2005). "Sensory ecology and communication in Chiroptera," in Bat Ecology, eds T. H. Kunz and B. M. Fenton (London: University of Chicago Press), 90-118.
2. Anthony, E. L. P., and Kunz, T. H. (1977). Feeding strategies of the little brown bat, Myotis lucifugus, in Southern New Hampshire. Ecology 58, 775-786. doi: 10.2307/1936213
3. Armstrong, K. N., and Kerry, L. (2011). Modelling the prey detection performance of Rhinonicteris aurantia (Chiroptera: Hipposideridae) in different atmospheric conditions discounts the notional role of relative humidity in adaptive evolution. J. Theor. Biol. 278, 44-54. doi: 10.1016/j.jtbi.2011.02.026
4. Aytekin, M., Mao, B., and Moss, C. F. (2010). Spatial perception and adaptive sonar behavior. J. Acoust. Soc. Am. 128, 3788-3798. doi: 10.1121/1.3504707
5. Bates, M. E., Watanabe, Y., Furusawa, Y., Fujioka, E., Hiryu, S., Riquimaroux, H., et al. (2010). Echolocation behavior of pairs of flying Eptesicus fuscus recorded with a Telemike microphone. J. Acoust. Soc. Am. 127, 1971. doi: 10.1121/1.3385042
6. Beck, R. W., Beck, R. W., Maguire, M. G., Bressler, N. M., Glassman, A. R., Lindblad, A. S., et al. (2007). Visual acuity as an outcome measure in clinical trials of retinal diseases. Ophthalmology 114, 1804-1809. doi: 10.1016/j.ophtha.2007.06.047
7. Bell, G. P. (1985). The sensory basis of prey location by the California leaf-nosed bat Macrotus californicus (Chiroptera: Phyllostomidae). Behav. Ecol. Sociobiol. 16, 343-347. doi: 10.1007/BF00295547
8. Bell, G. P., and Fenton, M. B. (1986). Visual acuity, sensitivity and binocularity in a gleaning insectivorous bat, Macrotus californicus (Chiroptera, Phyllostomidae). Anim. Behav. 34, 409-414. doi: 10.1016/S0003-3472(86)80110-5
9. Bohmann, K., Monadjem, A., Noer, C. L., Rasmussen, M., Zeale, M., Clare, E., et al. (2011). Molecular diet analysis of two African free-tailed bats, (Molossidae) using high throughput sequencing. PLoS ONE 6:e21441. doi: 10.1371/journal.pone.0021441
10. Bradbury, J., and Nottebohm, F. (1969). The use of vision by the little brown bat, Myotis lucifugus, under controlled conditions. Anim. Behav. 17, 480-485. doi: 10.1016/0003-3472(69)90150-X
11. Brinkløv, S., Fenton, M. B., and Ratcliffe, J. M. (2013). Echolocation in Oilbirds and swiftlets. Front. Physiol. 4:123. doi: 10.3389/fphys.2013.00123
12. Chase, J. (1972). The Role of Vision in Echolocating Bats. Ph. D. thesis, Indiana University.
13. Chase, J. (1981).Visually guided escape responses of microchiropteran bats. Anim. Behav. 29, 708-713. doi: 10.1016/S0003-3472(81)80005-X
14. Chiu, C., Xian, W., and Moss, C. F. (2008). Flying in silence: echolocating bats cease vocalizing to avoid sonar jamming. Proc. Natl. Acad. Sci. U.S.A. 105, 13116-13121. doi: 10.1073/pnas.0804408105
15. Christensen-Dalsgaard, J. (2011). Vertebrate pressure-gradient receivers. Hear. Res. 273, 37-45. doi: 10.1016/j.heares.2010.08.007
16. Deneve, S., and Pouget, A. (2004). Bayesian multisensory integration and cross-modal spatial links. J. Physiol. (Paris) 98, 249-258. doi: 10.1016/j.jphysparis.2004.03.011
17. Denzinger, A., Kalko, E. K. V., and Jones, G. (2004). "Ecological and evolutionary aspects of echolocation in bats," in Echolocation in Bats and Dolphins, eds J. Thomas, C. F. Moss, and M. Vater (Chicago, IL: Chicago University Press), 311-326.
18. Dietz, C., von Helversen, O., and Nill, D. (2007). Die Fledermäuse Europas und Nordwestafrikas. Biologie, Kennzeichen, Gefährdung. Stuttgart: Kosmos Verlag.
19. Eklöf, J. (2003). Vision in Echolocating Bats. Doctoral Thesis, Zoology Department, Göteborg University.
20. Eklöf, J., Svensson, A. M., and Rydell, J. (2002). Northern bats, Eptesicus nilssonii, use vision but not flutter-detection when searching for prey in clutter. Oikos 99, 347-351. doi: 10.1034/j.1600-0706.2002.990216.x
21. Ellins, S. R., and Masterson, F. A. (1974). Brightness discrimination thresholds in the bat, Eptesicus fuscus. Brain Behav. Evol. 9, 248-263. doi: 10.1159/000123669
22. Fenton, M. B., Portfors, C. V., Rautenbach, I. L. 8: and Waterman, M. (1998). Compromises: sound frequencies used in echolocation by aerial-feeding bats. Can. J. Zool. 76, 1174-1182.
23. Goiti, U., Vecin, P., Garin, I., Salona, M., and Aihartza, J. R. (2003). Diet and prey selection in Kuhl's pipistrelle Pipistrellus kuhlii (Chiroptera: Vespertilionidae) in south-western Europe. Acta Theriol. 48, 457-468. doi: 10.1007/BF03192492
24. Gray, L. J. (1993). Response of insectivorous birds to emerging aquatic insects in riparian habitats of a tallgrass prairie stream. Am. Midl. Nat. 129, 288-300. doi: 10.2307/2426510
25. Griffin, D. R. (1958). Listening in the Dark: The Acoustic Orientation of Bats and Men. New Haven, CT: Yale University Press.
26. Griffin, D. R., and Thompson, D. (1982). Echolocation by cave swiftlets. Behav. Ecol. Sociobiol. 10, 119-123. doi: 10.1007/BF00300171
27. Griffin, D. R., and Suthers, R. A. (1970). Sensitivity of echolocation in cave swiftlets. Biol. Bull. 139, 495-501. doi: 10.2307/1540368
28. Griffin, D. R., Webster, F. A., and Michael, C. R. (1960). The echolocation of flying insects by bats. Anim. Behav. 8, 141-154. doi: 10.1016/0003-3472(60)90022-1
29. Hecht, S., and Mintz, E. U. (1939). The visibility of single lines at various illuminations and the terminal basis of visual resolution. J. Gen. Physiol. 22, 593-612. doi: 10.1085/jgp.22.5.593
30. Heffner, H. E., and Heffner, R. S. (1985). Hearing in two cricetid rodents: wood Rat (Neotoma floridana) and grasshopper mouse (Onychomys leucogaster). J. Comp. Psychol. 99, 275-288. doi: 10.1037/0735-7036.99.3.275
31. Heffner, H. E., and Heffner, R. S. (2008). "High-frequency hearing," in Handbook of the Senses: Audition, eds P. Dallos, D. Oertel, and R. Hoy (New York, NY: Elsevier), 55-60.
32. Heffner, H., Ravizza, R., and Masterton, B. (1969). Hearing in primitive mammals, III: tree shrew (Tupaia glis). J. Audit. Res. 9, 12-18.
33. Holderied, M. W., and Von Helversen, O. (2003). Echolocation range and wingbeat period match in aerial-hawking bats. Proc. Biol. Sci. 270, 2293-2299. doi: 10.1098/rspb.2003.2487
34. Holyoak, D. T. (2001). Nightjars and Their Allies: The Caprimulgiformes. Oxford: Oxford University Press.
35. Hope, G. M., and Bhatnagar, K. P. (1979). Effect on light adaptation on electrical responses on the retina of four species of bats. Experentia 35, 1191-1192. doi: 10.1007/BF01963280
36. Houston, R. D., Boonman, A. M., and Jones, G. (2004). "Do echolocation signal parameters restrict bats' choice of prey?" in Echolocation in Bats and Dolphins, eds J. Thomas, C. F. Moss, and M. Vater (Chicago, IL: Chicago University Press), 339-345.
37. Jackson, J. K., and Fisher, S. G. (1986). Secondary production, emergence, and export of aquatic insects of a Sonoran desert stream. Ecology 67, 629-638. doi: 10.2307/1937686
38. Jakobsen, L., Ratcliffe, J. M., and Surlykke, A. (2013). Convergent acoustic field of view in echolocating bats. Nature 493, 93-96. doi: 10.1038/nature11664
39. Jetz, W., Steffen, J., and Linsenmair, K. E. (2003). Effects of light and prey availability on nocturnal, lunar and seasonal activity of tropical nightjars. Oikos 103, 627-639. doi: 10.1034/j.1600-0706.2003.12856.x
40. Jones, G., and Rydell, J. (1994). Foraging strategy and predation risk as factors influencing emergence time in echolocating bats. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346B, 445-455. doi: 10.1098/rstb.1994.0161
41. Kalko, E. K. V., and Schnitzler, H. U. (1993). Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection. Behav. Ecol. Sociobiol. 33, 415-428. doi: 10.1007/BF00170257
42. Kick, S. (1982). Target-detection by the echolocating bat, Eptesicus fuscus. J. Comp. Physiol. A 145, 432-435. doi: 10.1007/BF00612808
43. King, R. S., and Wrubleski, D. A. (1998). Spatial and diel availability of flying insects as potential duckling food in prairie wetlands. Wetlands 18, 100-114. doi: 10.1007/BF03161448
44. Koay, G., Kearns, D., Heffner, H. E., and Heffner, R. S. (1998). Passive sound-localization ability of the big brown bat (Eptesicus fuscus). Hear. Res. 119, 37-48. doi: 10.1016/S0378-5955(98)00037-9
45. Kon, M. (1989). Swarming and mating behaviour of Chironomus flaviplumus (Diptera: Chironomidae), compared with a sympatric congeneric species, C. yoshimatsui. J. Ethol. 7, 125-131. doi: 10.1007/BF02350034
46. Krasheninnikov, A. B. (2012). Phenology of some chironomid species (Diptera, Chironomidae) of the Middle Urals. Fauna Norvegica 31, 55-63. doi: 10.5324/fn.v3ee0.1371
47. Levin, E., Yom-Tov, Y., and Barnea, A. (2009). Frequent summer nuptial flights of ants provide a primary food source for bats. Die Naturwissenschaften 96, 477-483. doi: 10.1007/s00114-008-0496-3
48. Lie, I. (1980). Visual detection and resolution as a function of retinal locus. Vision Res. 20, 967-974. doi: 10.1016/0042-6989(80)90079-6
49. Lynch, R. J., Bunn, S. E., and Catterall, C. P. (2002). Adult aquatic insects: potential contributors to riparian food webs in Australia's wet-dry tropics. Aust. Ecol. 27, 515-526.
50. Manley, G. (2012). Evolutionary paths to mammalian cochleae. J. Assoc. Res. Otolaryngol. 13, 733-743. doi: 10.1007/s10162-012-0349-9
51. Melcón, M. L., Yovel, Y., Denzinger, A., and Schnitzler, H. U. (2011). How greater mouse-eared bats deal with ambiguous echoic scenes. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 197, 505-514. doi: 10.1007/s00359-010-0563-z
52. Mistry, S. (1990). Characterisics of the visually guilded escape response of the Mexican free-tailed bat Tadarida brasiliensis mexicana. Anim. Behav. 39, 314-320. doi: 10.1016/S0003-3472(05)80876-0
53. Moss, C. F., and Schnitzler, H. U. (1995). "Behavioral studies of auditory information processing," in Hearing by Bats, eds A. N. Popper and R. R. Fay (New York, NY: Springer-Verlag), 87-145.
54. Müller, R., and Kuc, R. (2000). Foliage echoes: a probe into the ecological acoustics of bat echolocation. J. Acoust. Soc. Am. 108, 836-845. doi: 10.1121/1.429617
55. Necker, R. (2000). "The avian ear and hearing," in Sturkie's Avian Physiology, ed G. C. Whinow (New York, NY: Academic Press), 21-38.
56. Neuweiler, G., and Fenton, M. B. (1988). "Behavior and foraging ecology of echolocating bats," in Animal Sonar: Processes and Performance, eds P. E. Nachtigall and P. W. B. Moore (New York, NY: Plenum Press), 535-549.
57. Racey, P. A., and Swift, S. M. (1985). Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. I. Foraging behaviour. J. Anim. Ecol. 54, 205-215. doi: 10.2307/4631
58. Ramsier, M. A., Cunningham, A. J., Moritz, G. L., Finneran, J. J., Williams, C. V., Ong, P. S., et al. (2012). Primate communication in the pure ultrasound Primate communication in the pure ultrasound. Biol. Lett. 8, 508-511. doi: 10.1098/rsbl.2011.1149
59. Rydell, J., Entwistle, J., and Racey, P. (1996). Timing of foraging flights of three species of bats in relation to insect activity and predation risk. Oikos 76, 243-252. doi: 10.2307/3546196
60. Ryer, A. (1997). Light Measurement Handbook. Massachsetts, MA: International light Inc.
61. Schnitzler, H. U. (1970). Echoortung bei der Fledermaus, Chilonycteris rubiginosa. Z. Vergl. Physiol. 68, 25-38. doi: 10.1007/BF00297809
62. Simmons, N. B., and Geisler, J. H. (1998). Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx to extant bat lineages, with comments on the evolution of echolocation and foraging strategies in Microchiroptera. Bull. Am. Mus. Nat. Hist. 235, 4-182.
63. Simmons, N. B., Seymour, K. L., Habersetzer, J., and Gunnell, G. F. (2008). Primitive. Early Eocene bat from wyoming and the evolution of flight and echolocation. Nature 451, 818-821. doi: 10.1038/nature06549
64. Skolnik, M. I. (1970). Radar Handbook. Columbus, OH: McGraw-Hill.
65. Speakman, J. R. (2001). The evolution of flight and echolocation in bats: another leap in the dark. Mammal Rev. 31, 111-130. doi: 10.1046/j.1365-2907.2001.00082.x
66. Speakman, J. R., and Racey, P. A. (1991). No cost of echolocation for bats in flight. Nature 350, 421-423. doi: 10.1038/350421a0
67. Stilz, W.-P., and Schnitzler, H.-U. (2012). Estimation of the acoustic range of bat echolocation for extended targets. J. Acoust. Soc. Am. 132, 1765-1775. doi: 10.1121/1.4733537
68. Surlykke, A., and Kalko, E. K. V. (2008). Echolocating bats cry out loud to detect their prey. PLoS ONE 3:e2036. doi: 10.1371/journal.pone.0002036
69. Suthers, R. A. (1966). Optomotor responses by echolocating bats. Science 152, 1102-1104. doi: 10.1126/science.152.3725.1102
70. Suthers, R. A., and Wallis, N. E. (1970). Optics of the eyes of echolocating bats. J. Vision Res. 10, 1165-1173. doi: 10.1016/0042-6989(70)90034-9
71. Swift, S. M., Racey, P. A., and Avery, M. I. (1985). Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during pregnancy and lactation. II - Diet. J. Anim. Ecol. 54, 217-225. doi: 10.2307/4632
72. Taylor, P., and Jackson, H. D. (2003). A review of foraging and feeding behaviour, and associated anatomical adaptations in Afrotropical nightjars. Ostrich 74, 187-204. doi: 10.2989/00306520309485392
73. Thomas, R. J., Székely, T., Cuthill, I. C., Harper, D. G. C., Newson, S. E., Frayling, T. D., et al. (2002). Supplement - Eye size in birds and the timing of song at dawn. Proc. Biol. Sci. 269, 831-837. doi: 10.1098/rspb.2001.1941
74. Thomassen, H. A. (2005). Swift as Sound. Design and Evolution of the Echolocation System in Swiflets (Apodidae: Collocaliini). Leiden: Print Partners lpskamp B. V.
75. Ulanovsky, N., Fenton, M. B., Tsoar, A., and Korine, C. (2004). Dynamics of jamming avoidance in echolocating bats. Proc. Biol. Sci. 271, 1467-1475. doi: 10.1098/rspb.2004.2750
76. Vaughan, N. (1997). The diets of British bats (Chiroptera). Mammal Rev. 27, 77-94. doi: 10.1111/j.1365-2907.1997.tb00373.x
77. Waters, D. A., Rydell, J., and Jones, G. (1995). Echolocation call design and limits on prey size: a case study using the aerial-hawking bat Nyctalus leisleri. Behav. Ecol. Sociobiol. 37, 321-328. doi: 10.1007/BF00174136
78. Williams, T. C., and Williams, J. M. (1967). Radio tracking of homing bats. Science 155, 1435-1436. doi: 10.1126/science.155.3768.1435
79. Yela, J., and Herrera, C. M. (1993). Seasonality and life cycles of woody plant-feeding noctuid moths (Lepidoptera: Noctuidae) in Mediterranean habitats. Ecol. Entomol. 18, 259-269. doi: 10.1111/j.1365-2311.1993.tb01099.x