Research article: Acoustic gaze adjustments during active target selection in echolocating porpoises

Journal of Experimental Biology

Volumn 215, Issue 24, 2012, Pages 4358-4373

  Wisniewska, Danuta Maria ^a   Johnson, Mark ^b   Beedholm, Kristian ^a   Wahlberg, Magnus ^c   Madsen, Peter Teglberg ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Acoustic gaze control; Echolocation; Porpoise; Scanning; Toothed whale

Indexed keywords

ANIMALIA; CETACEA; ODONTOCETI; PHOCOENA; PHOCOENIDAE;

ACOUSTICS; ANIMAL; ARTICLE; ECHOLOCATION; PHYSIOLOGY; PORPOISE; SOUND; SWIMMING;

ACOUSTICS; ANIMALS; ECHOLOCATION; PHOCOENA; SOUND; SWIMMING;

EID: 84870044146     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.074013     Document Type: Article

References (72)

1. Aivar, M. P., Hayhoe, M. M., Chizk, C. L. and Mruczek, R. E. B. (2005). Spatial memory and saccadic targeting in a natural task. J. Vis. 5, 177-193. (Pubitemid 41522115)
2. Akamatsu, T., Wang, D., Wang, K. X. and Naito, Y. (2005). Biosonar behaviour of free-ranging porpoises. Proc. Biol. Sci. 272, 797-801. (Pubitemid 41411113)
3. Akamatsu, T., Teilmann, J., Miller, L. A., Tougaard, J., Dietz, R., Wang, D., Wang, K. X., Siebert, U. and Naito, Y. (2007). Comparison of echolocation behaviour between coastal and riverine porpoises. Deep Sea Res. Part II Top. Stud. Oceanogr. 54, 290-297. (Pubitemid 46428546)
4. Amundin, M., Starkhammar, J., Evander, M., Almqvist, M., Lindström, K. and Persson, H. W. (2008). An echolocation visualization and interface system for dolphin research. J. Acoust. Soc. Am. 123, 1188-1194. (Pubitemid 351208325)
5. Aroyan, J. L., Cranford, T. W., Kent, J. and Norris, K. S. (1992). Computer modeling of acoustic beam formation in Delphinus delphis. J. Acoust. Soc. Am. 92, 2539-2545.
6. Atem, A., Rasmussen, M. H., Wahlberg, M., Petersen, H. C. and Miller, L. (2009). Changes in click source levels with distance to targets: studies of free-ranging whitebeaked dolphins (Lagenorhynchus albirostris) and captive harbor porpoises (Phocoena phocoena). Bioacoustics 19, 49-65.
7. Au, W. W. L. (1993). The Sonar of Dolphins. New York: Springer-Verlag.
8. Au, W. W. L. and Benoit-Bird, K. J. (2003). Automatic gain control in the echolocation system of dolphins. Nature 423, 861-863. (Pubitemid 36781275)
9. Au, W. W. L., Penner, R. H. and Kadane, J. (1982). Acoustic behavior of echolocating Atlantic bottlenose dolphins. J. Acoust. Soc. Am. 71, 1269-1275.
10. Au, W. W. L., Kastelein, R. A., Rippe, T. and Schooneman, N. M. (1999). Transmission beam pattern and echolocation signals of a harbor porpoise (Phocoena phocoena). J. Acoust. Soc. Am. 106, 3699-3705. (Pubitemid 129520733)
11. Au, W. W. L., Branstetter, B. K., Benoit-Bird, K. J. and Kastelein, R. A. (2009). Acoustic basis for fish prey discrimination by echolocating dolphins and porpoises. J. Acoust. Soc. Am. 126, 460-467.
12. Barber, J. R., Razak, K. A. and Fuzessery, Z. M. (2003). Can two streams of auditory information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus. J. Comp. Physiol. A 189, 843-855. (Pubitemid 37519135)
13. Beedholm, K. and Miller, L. A. (2007). Automatic gain control in harbour porpoises (Phocoena phocoena)? Central versus peripheral mechanisms. Aquat. Mamm. 33, 69-75.
14. Bregman, A. S. (1990). Auditory Scene Analysis: The Perceptual Organization of Sound. Cambridge, MA: MIT Press.
15. De Pierrepont, J. F., Dubois, B., Desormonts, S., Santos, M. B. and Robin, J. P. (2005). Stomach contents of English Channel cetaceans stranded on the coast of Normandy. J. Mar. Biol. Assoc. U. K. 85, 1539-1546. (Pubitemid 41607468)
16. DeRuiter, S. L., Bahr, A., Blanchet, M. A., Hansen, S. F., Kristensen, J. H., Madsen, P. T., Tyack, P. L. and Wahlberg, M. (2009). Acoustic behaviour of echolocating porpoises during prey capture. J. Exp. Biol. 212, 3100-3107.
17. DeRuiter, S. L., Hansen, M., Koopman, H. N., Westgate, A. J., Tyack, P. L. and Madsen, P. T. (2010). Propagation of narrow-band-high-frequency clicks: measured and modeled transmission loss of porpoise-like clicks in porpoise habitats. J. Acoust. Soc. Am. 127, 560-567.
18. Eckmeier, D., Geurten, B. R. H., Kress, D., Mertes, M., Kern, R., Egelhaaf, M. and Bischof, H. J. (2008). Gaze strategy in the free flying zebra finch (Taeniopygia guttata). PLoS ONE 3, e3956.
19. Gellermann, L. W. (1933). Chance orders of alternating stimuli in visual discrimination experiments. Pedagog. Semin. J. Genet. Psychol. 42, 206-208.
20. Griffin, D. R. (1958). Listening in the Dark: The Acoustic Orientation of Bats and Men. New York: Cornell University Press.
21. Hartley, D. J. (1992). Stabilization of perceived echo amplitudes in echolocating bats. II. The acoustic behavior of the big brown bat, Eptesicus fuscus, when tracking moving prey. J. Acoust. Soc. Am. 91, 1133-1149.
22. Hayhoe, M. and Ballard, D. (2005). Eye movements in natural behavior. Trends Cogn. Sci. 9, 188-194. (Pubitemid 40543254)
23. Henson, O. W., Jr. (1965). The activity and function of the middle-ear muscles in echolocating bats. J. Physiol. 180, 871-887.
24. Jakobsen, L. and Surlykke, A. (2010). Vespertilionid bats control the width of their biosonar sound beam dynamically during prey pursuit. Proc. Natl. Acad. Sci. USA 107, 13930-13935.
25. Jensen, F. H., Bejder, L., Wahlberg, M. and Madsen, P. T. (2009). Biosonar adjustments to target range of echolocating bottlenose dolphins (Tursiops sp.) in the wild. J. Exp. Biol. 212, 1078-1086.
26. Johnson, M. P. and Tyack, P. L. (2003). A digital acoustic recording tag for measuring the response of wild marine mammals to sound. IEEE J. Oceanic Eng. 28, 3-12.
27. Johnson, M., Madsen, P. T., Zimmer, W. M. X., de Soto, N. A. and Tyack, P. L. (2004). Beaked whales echolocate on prey. Proc. R. Soc. Lond. B 271, S383-S386.
28. Johnson, M., Madsen, P. T., Zimmer, W. M. X., de Soto, N. A. and Tyack, P. L. (2006). Foraging Blainville's beaked whales (Mesoplodon densirostris) produce distinct click types matched to different phases of echolocation. J. Exp. Biol. 209, 5038-5050. (Pubitemid 46166731)
29. Johnson, M., Hickmott, L. S., Aguilar Soto, N. and Madsen, P. T. (2008). Echolocation behaviour adapted to prey in foraging Blainville's beaked whale (Mesoplodon densirostris). Proc. Biol. Sci. 275, 133-139. (Pubitemid 350174599)
30. Johnson, M., de Soto, N. A. and Madsen, P. T. (2009). Studying the behaviour and sensory ecology of marine mammals using acoustic recording tags: a review. Mar. Ecol. Prog. Ser. 395, 55-73.
31. Jones, B. A., Stanton, T. K., Lavery, A. C., Johnson, M. P., Madsen, P. T. and Tyack, P. L. (2008). Classification of broadband echoes from prey of a foraging Blainville's beaked whale. J. Acoust. Soc. Am. 123, 1753-1762. (Pubitemid 351379601)
32. Kadane, J. and Penner, R. H. (1983). Range ambiguity and pulse interval jitter in the bottlenose dolphin. J. Acoust. Soc. Am. 74, 1059-1061. (Pubitemid 14452893)
33. Kastelein, R. A., Verlaan, M. and Jennings, N. (2008). Number and duration of echolocation click trains produced by a harbor porpoise (Phocoena phocoena) in relation to target and performance. J. Acoust. Soc. Am. 124, 40-43. (Pubitemid 352019330)
34. Kellogg, W. N., Kohler, R. and Morris, H. N. (1953). Porpoise sounds as sonar signals. Science 117, 239-243.
35. Koblitz, J. C., Wahlberg, M., Stilz, P., Madsen, P. T., Beedholm, K. and Schnitzler, H. U. (2012). Asymmetry and dynamics of a narrow sonar beam in an echolocating harbor porpoise. J. Acoust. Soc. Am. 131, 2315-2324.
36. Kustov, A. A. and Robinson, D. L. (1996). Shared neural control of attentional shifts and eye movements. Nature 384, 74-77. (Pubitemid 26374590)
37. Land, M. F. and Hayhoe, M. (2001). In what ways do eye movements contribute to everyday activities? Vision Res. 41, 3559-3565. (Pubitemid 33096274)
38. Linnenschmidt, M., Kloepper, L. N., Wahlberg, M. and Nachtigall, P. E. (2012a). Stereotypical rapid source level regulation in the harbour porpoise biosonar. Naturwissenschaften 99, 767-771.
39. Linnenschmidt, M., Beedholm, K., Wahlberg, M., Højer-Kristensen, J. and Nachtigall, P. E. (2012b). Keeping returns optimal: gain control exerted through sensitivity adjustments in the harbour porpoise auditory system. Proc. Biol. Sci. 279, 2237-2245.
40. Liversedge, S. P. and Findlay, J. M. (2000). Saccadic eye movements and cognition. Trends Cogn. Sci. 4, 6-14. (Pubitemid 30066502)
41. Madsen, P. T. and Wahlberg, M. (2007). Recording and quantification of ultrasonic echolocation clicks from free-ranging toothed whales. Deep Sea Res. Part I Oceanogr. Res. Pap. 54, 1421-1444. (Pubitemid 47103259)
42. Madsen, P. T., Wahlberg, M. and Møhl, B. (2002). Male sperm whale (Physeter macrocephalus) acoustics in a high-latitude habitat: implications for echolocation and communication. Behav. Ecol. Sociobiol. 53, 31-41. (Pubitemid 36708044)
43. Madsen, P. T., Kerr, I. and Payne, R. (2004). Echolocation clicks of two free-ranging, oceanic delphinids with different food preferences: false killer whales Pseudorca crassidens and Risso's dolphins Grampus griseus. J. Exp. Biol. 207, 1811-1823. (Pubitemid 38826056)
44. Madsen, P. T., Johnson, M., de Soto, N. A., Zimmer, W. M. X. and Tyack, P. (2005). Biosonar performance of foraging beaked whales (Mesoplodon densirostris). J. Exp. Biol. 208, 181-194. (Pubitemid 40307223)
45. Møhl, B., Wahlberg, M., Madsen, P. T., Miller, L. A. and Surlykke, A. (2000). Sperm whale clicks: directionality and source level revisited. J. Acoust. Soc. Am. 107, 638-648. (Pubitemid 30039188)
46. Moore, P. W., Dankiewicz, L. A. and Houser, D. S. (2008). Beamwidth control and angular target detection in an echolocating bottlenose dolphin (Tursiops truncatus). J. Acoust. Soc. Am. 124, 3324-3332.
47. Morozov, V. P., Akopian, A. I., Burdin, V. I., Zatseva, K. A. and Sokovykh, I. A. (1972). Sequential frequency of location signals of dolphins as a function of distance from the target. Biofizika 17, 139-145.
48. Moss, C. F. and Surlykke, A. (2001). Auditory scene analysis by echolocation in bats. J. Acoust. Soc. Am. 110, 2207-2226. (Pubitemid 32959719)
49. Moss, C. F. and Surlykke, A. (2010). Probing the natural scene by echolocation in bats. Front. Behav. Neurosci. 5, 33.
50. Nachtigall, P. E. and Supin, A. Y. (2008). A false killer whale adjusts its hearing when it echolocates. J. Exp. Biol. 211, 1714-1718. (Pubitemid 351960078)
51. Nelson, M. E. and MacIver, M. A. (2006). Sensory acquisition in active sensing systems. J. Comp. Physiol. A 192, 573-586.
52. Norris, K. (1968). The evolution of acoustic mechanisms in odontocete cetaceans. In Evolution and Environment (ed. E. T. Drake), pp. 297-324. New Haven, CT: Yale University Press.
53. Norris, K. S., Prescott, J. H., Asa-Dorian, P. V. and Perkins, P. (1961). An experimental demonstration of echolocation behavior in the porpoise, Tursiops truncatus (Montagu). Biol. Bull. 120, 163-176.
54. Penner, R. (1988). Attention and detection in dolphin echolocation. In Animal Sonar: Process and Performance (ed. P. E. Nachtigall and P. W. Moore), pp. 707-713. New York: Plenum Press.
55. Ridgway, S. H. (2011). Neural time and movement time in choice of whistle or pulse burst responses to different auditory stimuli by dolphins. J. Acoust. Soc. Am. 129, 1073-1080.
56. Schevill, W. E. and Lawrence, B. (1956). Food-finding by a captive porpoise (Tursiops truncatus). Breviora 53, 1-15.
57. Schnitzler, H. U. (1973). Control of Doppler shift compensation in the greater horseshoe bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 82, 79-92.
58. Schnitzler, H. U., Moss, C. F. and Denzinger, A. (2003). From spatial orientation to food acquisition in echolocating bats. Trends Ecol. Evol. 18, 386-394. (Pubitemid 36933028)
59. Schusterman, R. J. (1980). Behavioral methodology in echolocation by marine mammals. In Animal Sonar Systems (ed. R. G. Busnel and J. F. Fish), pp. 11-41. New York: Plenum Press.
60. Snyder, J. B., Nelson, M. E., Burdick, J. W. and Maciver, M. A. (2007). Omnidirectional sensory and motor volumes in electric fish. PLoS Biol. 5, e301.
61. Supin, A. Y., Nachtigall, P. E., Au, W. W. L. and Breese, M. (2004). The interaction of outgoing echolocation pulses and echoes in the false killer whale's auditory system: evoked-potential study. J. Acoust. Soc. Am. 115, 3218-3225. (Pubitemid 38781253)
62. Supin, A. Y., Nachtigall, P. E. and Breese, M. (2008). Forward masking as a mechanism of automatic gain control in odontocete biosonar: a psychophysical study. J. Acoust. Soc. Am. 124, 648-656. (Pubitemid 352019351)
63. Surlykke, A., Ghose, K. and Moss, C. F. (2009). Acoustic scanning of natural scenes by echolocation in the big brown bat, Eptesicus fuscus. J. Exp. Biol. 212, 1011-1020.
64. Teilmann, J., Miller, L. A., Kirketerp, T., Kastelein, R. A., Madsen, P. T., Nielsen, B. K. and Au, W. W. L. (2002). Characteristics of echolocation signals used by a harbour porpoise (Phocoena phocoena) in a target detection experiment. Aquat. Mamm. 28, 275-284.
65. Teloni, V., Johnson, M. P., Miller, P. J. O. and Madsen, P. T. (2008). Shallow food for deep divers: dynamic foraging behavior of male sperm whales in a high latitude habitat. J. Exp. Mar. Biol. Ecol. 354, 119-131. (Pubitemid 50012863)
66. Urick, R. J. (1983). Principles of Underwater Sound. Los Altos, CA: Peninsula Publishing.
67. Verfuss, U. K., Miller, L. A. and Schnitzler, H. U. (2005). Spatial orientation in echolocating harbour porpoises (Phocoena phocoena). J. Exp. Biol. 208, 3385-3394. (Pubitemid 41399784)
68. Verfuss, U. K., Miller, L. A., Pilz, P. K. D. and Schnitzler, H. U. (2009). Echolocation by two foraging harbour porpoises (Phocoena phocoena). J. Exp. Biol. 212, 823-834.
69. Villadsgaard, A., Wahlberg, M. and Tougaard, J. (2007). Echolocation signals of wild harbour porpoises, Phocoena phocoena. J. Exp. Biol. 210, 56-64. (Pubitemid 46160831)
70. Wilson, M., Schack, H. B., Madsen, P. T., Surlykke, A. and Wahlberg, M. (2011). Directional escape behavior in allis shad (Alosa alosa) exposed to ultrasonic clicks mimicking an approaching toothed whale. J. Exp. Biol. 214, 22-29.
71. Yarbus, A. L. (1961). Eye movements during the examination of complicated objects. Biofizika 6, 52-56.
72. Yovel, Y., Falk, B., Moss, C. F. and Ulanovsky, N. (2010). Optimal localization by pointing off axis. Science 327, 701-704.