Sperm whale echolocation behaviour reveals a directed, prior-based search strategy informed by prey distribution

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• 作者：A. Fais (1) (6)
  N. Aguilar Soto (1)
  M. Johnson (2)
  C. P茅rez-Gonz谩lez (3)
  P. J. O. Miller (2)
  P. T. Madsen (4) (5)
  
  1. BIOECOMAC ; Department of Animal Biology ; La Laguna University ; Canary Islands ; Spain
  6. Institute for Terrestrial and Aquatic Wildlife Research ; University of Veterinary Medicine Hannover ; Hannover ; Germany
  2. Scottish Ocean Institute ; University of St. Andrews ; St. Andrews ; Scotland
  3. Department of Statistics ; Operating Research and Computation ; La Laguna University ; Canary Islands ; Spain
  4. Zoophysiology ; Department of Bioscience ; Aarhus University ; Aarhus ; Denmark
  5. MUCRU ; Centre for Fish ; Fisheries and Aquatic Ecosystems Research ; School of Veterinary and Life Sciences ; Murdoch University ; Perth ; Australia
  
• 关键词：Sperm whales ; Echolocation behaviour ; Directed search behaviour ; Prior information ; Multi ; target acoustic scene
• 刊名：Behavioral Ecology and Sociobiology
• 出版年：2015
• 出版时间：April 2015
• 年：2015
• 卷：69
• 期：4
• 页码：663-674
• 全文大小：959 KB
• 参考文献：1. Aguilar Soto, N, Johnson, MP, Madsen, PT, D铆az, F, Dom铆nguez, I, Brito, A, Tyack, P (2008) Cheetahs of the deep sea: deep foraging sprints in short-finned pilot whales off Tenerife (Canary Islands). J Anim Ecol 77: pp. 936-947 CrossRef
  2. Anderson, MJ, Braak, CJF (2003) Permutation test for multi-factorial analysis of variance. J Stat Comput Simul 73: pp. 85-113 CrossRef
  3. Angel, M, Boxshall, G (1990) Life in the benthic boundary layer: connections to the mid-water and sea floor [and Discussion]. Phil Trans R Soc A 331: pp. 15-28 CrossRef
  4. Arranz, P, Aguilar Soto, N, Madsen, PT, Brito, A, Bordes, F, Johnson, MP (2011) Following a foraging fish-finder: diel habitat use of Blainville鈥檚 beaked whales revealed by echolocation. PLoS ONE 6: pp. e28353 CrossRef
  5. Au, WWL (1993) The sonar of dolphins. Springer, New York CrossRef
  6. Au, WWL, Benoit-Bird, KJ (2003) Automatic gain control in the echolocation system of dolphins. Nature 423: pp. 861-863 CrossRef
  7. Bar-Shalom, Y, Li, XR, Kirubarajan, T (2004) Estimation with applications to tracking and navigation: theory algorithms and software. Wiley, New York
  8. Bell, WJ (1991) Searching behaviour鈥攖he behavioural ecology of finding resources. Chapman and Hall, London
  9. Berzin, AA (1972) The sperm whale. Israel Program for Scientific Translations, Jerusalem
  10. Blachowiak-Samolyk, K, Kwasniewski, S, Richardson, K, Dmoch, K, Hansen, E, Hop, H, Falk-Petersen, S, Mouritsen, LT (2006) Arctic zooplankton do not perform diel vertical migration (DVM) during periods of midnight sun. Mar Ecol Prog Ser 308: pp. 101-116 CrossRef
  11. Costa, DP, Gales, NJ (2003) Energetics of a benthic diver: seasonal foraging ecology of the Australian sea lion, Neophoca cinerea. Ecol Monogr 73: pp. 27-43 CrossRef
  12. Dall, SRX, Giraldeau, L, Olsson, O, McNamara, JM, Stephens, DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20: pp. 187-193 CrossRef
  13. Crocker DE, Gales NJ, Costa DP (2001) Swimming and foraging strategies of New Zealand sea lions ( / Phocarctos hookeri). J Zool 254:267鈥?77
  14. Dehnhardt, G, Mauck, B, Hanke, W, Bleckmann, H (2001) Hydrodynamic trail-following in harbor seals (Phoca vitulina). Science 293: pp. 102-104 CrossRef
  15. Fox, J (2002) An R and S-Plus companion to applied regression. Sage, CA
  16. Fristrup, KM, Harbison, GR (2002) How do sperm whales catch squids?. Mar Mamm Sci 18: pp. 42-54 CrossRef
  17. Gallon, SL, Sparling, CE, Georges, J-Y, Fedak, MA, Biuw, M, Thompson, D (2007) How fast does a seal swim? Variations in swimming behaviour under differing foraging conditions. J Exp Biol 210: pp. 3285-3294 CrossRef
  18. Johnson, MP, Tyack, PL (2003) A digital acoustic recording tag for measuring the response of wild marine mammals to sound. IEEE J Ocean Eng 28: pp. 3-12 CrossRef
  19. Johnson MP, Hickmott LS, Aguilar Soto N, Madsen PT (2008) Echolocation behaviour adapted to prey in foraging Blainville鈥檚 beaked whale ( / Mesoplodon densirostris). Proc R Soc Lond聽B 275:133鈥?39
  20. Kramer, DL (1988) The behavioral ecology of air breathing by aquatic animals. Can J Zool 66: pp. 89-94 CrossRef
  21. Kuhn, CE, Crocker, DE, Tremblay, Y, Costa, DP (2009) Time to eat: measurements of feeding behaviour in a large marine predator, the northern elephant seal Mirounga angustirostris. J Anim Ecol 78: pp. 513-523 CrossRef
  22. Lettevall, E, Richter, C, Jaquet, N, Slooten, E, Dawson, S, Whitehead, H, Christal, J, Howard, PM (2002) Social structure and residency in aggregations of male sperm whales. Can J Zool 80: pp. 1189-1196 CrossRef
  23. Lima, SL, Zollner, PA (1996) Towards a behavioural ecology of ecological landscape. Trends Ecol Evol 11: pp. 131-135 CrossRef
  24. Lou芒pre, P, Baaren, J, Pierre, JS, Alphen, JJM (2011) Information gleaned and former patch quality determine foraging behavior of parasitic wasps. Behav Ecol 22: pp. 1064-1069 CrossRef
  25. Madsen, PT, Surlykke, A (2013) Functional convergence in bat and toothed whale. Physiology 28: pp. 276-283 CrossRef
  26. Madsen, PT, Wahlberg, M, M酶hl, B (2002) Male sperm whale (Physeter macrocephalus) acoustics in a high-latitude habitat: implications for echolocation and communication. Behav Ecol Sociobiol 53: pp. 31-41 CrossRef
  27. Madsen, PT, Payne, R, Kristiansen, NU, Wahlberg, M, Kerr, I, M酶hl, B (2002) Sperm whale sound production studied with ultrasound time/depth-recording tags. J Exp Biol 205: pp. 1899-1906
  28. Madsen, PT, Johnson, M, Aguilar Soto, N, Zimmer, WMX, Tyack, P (2005) Biosonar performance of foraging beaked whales (Mesoplodon densirostris). J Exp Biol 208: pp. 181-194 CrossRef
  29. Madsen, PT, Wilson, M, Johnson, MP, Hanlon, RT, Bocconcelli, A, Aguilar Soto, N, Tyack, PL (2007) Clicking for calamari: toothed whales can echolocate squid Loligo pealeii. Aquat Biol 1: pp. 141-150 CrossRef
  30. Madsen PT, Aguilar Soto N, Arranz P, Johnson M (2013) Echolocation in Blainville鈥檚 beaked whales ( / Mesoplodon densirostris). J Comp Physiol A 1鈥?9
  31. Martin, AR, Clarke, MR (1986) The diet of sperm whales (Physeter macrocephalus) captured between Iceland and Greeenland. J Mar Biol Assoc UK 66: pp. 779-790 CrossRef
  32. McArthur, RH, Pianka, ER (1966) On the optimal use of a patchy environment. Am Nat 100: pp. 603-610 CrossRef
  33. McNamara, JM, Green, RF, Olsson, O (2006) Bayes鈥?theorem and its applications in animal behaviour. Oikos 112: pp. 243-251 CrossRef
  34. Miller, PJO, Johnson, M, Tyack, PL, Terray, EA (2004) Swimming gaits, passive drag and bouyancy of diving sperm whales Physeter macrocephalus. J Exp Biol 207: pp. 1953-1967 CrossRef
  35. Miller, PJO, Johnson, MP, Tyack, PL (2004) Sperm whale behaviour indicates the use of echolocation click buzzes 鈥榗reaks鈥?in prey capture. Proc R Soc Lond B 271: pp. 2239-2247 CrossRef
  36. M酶hl, B, Wahlberg, M, Madsen, PT, Heerfordt, A, Lucas, A (2003) The monopulsed nature of sperm whale clicks. J Acoust Soc Am 114: pp. 1143-1154 CrossRef
  37. Moss, CF, Surlykke, A (2001) Auditory scene analysis by echolocation in bats. J Acoust Soc Am 110: pp. 2207-2226 CrossRef
  38. Moss, CF, Surlykke, A (2010) Probing the natural scene by echolocating bats. Front Behav Neurosci 4: pp. 1-16
  39. Naito, Y, Costa, DP, Adachi, T, Robinson, PW, Fowler, M, Takahashi, A (2013) Unravelling the mysteries of a mesopelagic diet: a large apex predator specializes on small prey. Funct Ecol 27: pp. 710-717 CrossRef
  40. Nelson, ME, MacIver, MA (2006) Sensory acquisition in active sensing systems. J Comp Physiol A 192: pp. 573-586 CrossRef
  41. Oliveira, C, Wahlberg, M, Johnson, M, Miller, PJ, Madsen, PT (2013) The function of male sperm whale slow clicks in a high latitude habitat: communication, echolocation, or prey debilitation?. J Acoust Soc Am 133: pp. 3135-3144 CrossRef
  42. Penner, RH Attention and detection in dolphin echolocation. In: Nachtigall, PE, Moore, PWB eds. (1988) Animal sonar process and performance. Plenum Press, New York and London, pp. 707-713 CrossRef
  43. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
  44. Ropert-Coudert, Y, Kato, A, Baudat, J, Bost, C, Maho, Y, Naito, Y (2001) Time/depth usage of Ad茅lie penguins: an approach based on dive angles. Polar Biol 24: pp. 467-470 CrossRef
  45. Santos, M, Pierce, G, Boyle, P, Reid, R, Ross, H, Patterson, I, Kinze, C, Tougaard, S, Lick, R, Piatkowski, U (1999) Stomach contents of sperm whales Physeter macrocephalus stranded in the North Sea 1990-1996. Mar Ecol Prog Ser 183: pp. 281-294 CrossRef
  46. Sato, K, Charrassin, J, Bost, C, Naito, Y (2004) Why do macaroni penguins choose shallow body angles that result in longer descent and ascent durations?. J Exp Biol 207: pp. 4057-4065 CrossRef
  47. Schnitzler, H-U, Moss, CF, Denzinger, A (2003) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18: pp. 386-394 CrossRef
  48. Steele, JH (1989) The ocean 鈥榣andscape鈥? Landsc Ecol 3: pp. 185-192 CrossRef
  49. Teloni, V, Johnson, M, Miller, PJO, Tyack, PL (2008) Shallow food for deep divers: dynamic foraging behavior of male sperm whales in a high latitude habitat. J Exp Mar Biol Ecol 354: pp. 119-131 CrossRef
  50. Thode, A, Melling, DK, Stienessen, S, Martinez, A, Mullin, K (2002) Depth-dependent acoustic features of diving sperm whales (Physeter macrocephalus) in the Gulf of Mexico. J Acoust Soc Am 112: pp. 308-321 CrossRef
  51. Thompson, D, Fedak, M (2001) How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim Behav 61: pp. 287-296 CrossRef
  52. Vacqui茅-Garcia, J, Royer, F, Dragon, AC, Viviant, M, Bailleul, F, Guinet, C (2012) Foraging in the darkness of the southern ocean: influence of bioluminescence on a deep diving predator. PLoS ONE 7: pp. e43565 CrossRef
  53. Verfu尾, UK, Miller, LA, Schnitzler, H-U (2005) Spatial orientation in echolocating harbour porpoises (Phocoena phocoena). J Exp Biol 208: pp. 3385-3394 CrossRef
  54. Watwood, SL, Miller, PJO, Johnson, M, Madsen, PT, Tyack, PL (2006) Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus). J Anim Ecol 75: pp. 814-825 CrossRef
  55. Wilson RP (2003) Penguins predict their performance. Mar Ecol-Prog Ser 249:305鈥?10
  56. Wisniewska, DM, Johnson, M, Beedholm, K, Wahlberg, M, Madsen, PT (2012) Acoustic gaze adjustments during active target selection in echolocating porpoises. J Exp Biol 215: pp. 4358-4373 CrossRef
  57. Zimmer, WMX, Johnson, MP, D鈥橝mico, A, Tyack, PL (2003) Combining data from a multisensor tag and passive sonar to determine the diving behavior of a sperm whale (Physeter macrocephalus). IEEE J Ocean Eng 28: pp. 13-28 CrossRef
  58. Zimmer, WMX, Madsen, PT, Teloni, V, Johnson, M, Tyack, PL (2005) Off-axis effects on the multipulse structure of sperm whale usual clicks with implications for sound production. J Acoust Soc Am 118: pp. 3337-3345 CrossRef
  59. Zollner, PA, Lima, SL (1999) Search strategies for landscape-level interpatch movements. Ecol Soc Am 80: pp. 1019-1030
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Behavioural Sciences
  Zoology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0762

文摘

Predators make foraging decisions based upon sensory information about resource availability, but little is known about how large, air-breathing predators collect and use such information to maximize energy returns when foraging in the deep sea. Here, we used archival tags to study how echolocating sperm whales (Physeter macrocephalus) use their long-range sensory capabilities to guide foraging in a deep-water habitat consisting of multiple, depth-segregated prey layers. Sperm whales employ a directed search behaviour by modulating their overall sonar sampling with the intention to exploit a particular prey layer. They forage opportunistically during some descents while actively adjusting their acoustic gaze to sequentially track different prey layers. While foraging within patches, sperm whales adjust their clicking rate both to search new water volumes as they turn and to match the prey distribution. This strategy increases information flow and suggests that sperm whales can perform auditory stream segregation of multiple targets when echolocating. Such flexibility in sampling tactics in concert with long-range sensing capabilities apparently allow sperm whales to efficiently locate and access prey resources in vast, heterogeneous, deep water habitats.