Fear of Killer Whales Drives Extreme Synchrony in Deep Diving Beaked Whales.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
06 02 2020
06 02 2020
Historique:
received:
03
09
2019
accepted:
13
11
2019
entrez:
8
2
2020
pubmed:
8
2
2020
medline:
2
12
2020
Statut:
epublish
Résumé
Fear of predation can induce profound changes in the behaviour and physiology of prey species even if predator encounters are infrequent. For echolocating toothed whales, the use of sound to forage exposes them to detection by eavesdropping predators, but while some species exploit social defences or produce cryptic acoustic signals, deep-diving beaked whales, well known for mass-strandings induced by navy sonar, seem enigmatically defenceless against their main predator, killer whales. Here we test the hypothesis that the stereotyped group diving and vocal behaviour of beaked whales has benefits for abatement of predation risk and thus could have been driven by fear of predation over evolutionary time. Biologging data from 14 Blainville's and 12 Cuvier's beaked whales show that group members have an extreme synchronicity, overlapping vocal foraging time by 98% despite hunting individually, thereby reducing group temporal availability for acoustic detection by killer whales to <25%. Groups also perform a coordinated silent ascent in an unpredictable direction, covering a mean of 1 km horizontal distance from their last vocal position. This tactic sacrifices 35% of foraging time but reduces by an order of magnitude the risk of interception by killer whales. These predator abatement behaviours have likely served beaked whales over millions of years, but may become maladaptive by playing a role in mass strandings induced by man-made predator-like sonar sounds.
Identifiants
pubmed: 32029750
doi: 10.1038/s41598-019-55911-3
pii: 10.1038/s41598-019-55911-3
pmc: PMC7005263
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13Références
Fedak, M. A. & Thompson, D. Behavioural and physiological options in diving seals. Symposium Zoological Society of London 66, 349–368 (1993).
Tyack, P. L., Johnson, M., Aguilar de Soto, N., Sturlese, A. & Madsen, P. T. Extreme diving of beaked whales. J. Exp. Biol. 209, 4238–4253 (2006).
pubmed: 17050839
doi: 10.1242/jeb.02505
Arranz, P. et al. Following a foraging fish-finder: diel habitat use of Blainville’s beaked whales revealed by echolocation. PLoS One 6, e28353 (2011).
pubmed: 22163295
pmcid: 3233560
doi: 10.1371/journal.pone.0028353
Aguilar de Soto, N. et al. No shallow talk: Cryptic strategy in the vocal communication of Blainville’s beaked whales. Mar. Mammal Sci. 28, E75–E92 (2012).
doi: 10.1111/j.1748-7692.2011.00495.x
Madsen, P. T., Aguilar de Soto, N., Tyack, P. & Johnson, M. Beaked whales. Curr. Biol. 24, R2 (2014).
doi: 10.1016/j.cub.2014.06.041
Hooker, S. K. et al. Deadly diving? Physiological and behavioural management of decompression stress in diving mammals. Proc. R. Soc. B Biol. Sci. 279, 1041–1050 (2012).
doi: 10.1098/rspb.2011.2088
Velten, B. P., Dillaman, R. M., Kinsey, S. T., McLellan, W. A. & Pabst, D. A. Novel locomotor muscle design in extreme deep-diving whales. J. Exp. Biol 216, 1862–1871, https://doi.org/10.1242/jeb.081323 (2013).
doi: 10.1242/jeb.081323
pubmed: 23393275
Miller, P. J. O., Johnson, M. P., Tyack, P. L. & Terray, E. A. Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus. J. Exp. Biol. 207, 1953–1967 (2004).
pubmed: 15107448
doi: 10.1242/jeb.00993
Aguilar Soto, N. et al. Cheetahs of the deep sea: deep foraging sprints in short-finned pilot whales off Tenerife (Canary Islands). J. Anim. Ecol. 77, 936–947 (2008).
pubmed: 18444999
doi: 10.1111/j.1365-2656.2008.01393.x
Jensen, F., Marrero, J., Johnson, M., Aguilar de Soto, N. & Madsen, P. T. Calling under pressure: Short-finned pilot whales make social calls during deep foraging dives. Proc. R. Soc. B. 278(1721), 3017–3025 (2011).
pubmed: 21345867
doi: 10.1098/rspb.2010.2604
Marrero, J., Jensen, F., Rojano, L. & Aguilar de Soto, N. Different modes of acoustic communication in deep diving short‐finned pilot whales (Globicephala macrorhynchus). Mar. Mam. Sci. 33(1), 59 (2017).
doi: 10.1111/mms.12344
Visser, F. et al. Vocal foragers and silent crowds: context-dependent vocal variation in Northeast Atlantic long-finned pilot whales. Behavioral Ecology and Sociobiology 71, 170 (2017).
pubmed: 29167596
pmcid: 5674111
doi: 10.1007/s00265-017-2397-y
Oliveira, C. et al. Sperm whale codas may encode individuality as well as clan identity. J. Acoust. Soc. Am. 139(5), 2860 (2016).
pubmed: 27250178
doi: 10.1121/1.4949478
Baird, R. W., Webster, D. L., Schorr, G. S., McSweeney, D. J. & Barlow, J. Diel variation in beaked whale diving behavior. Mar. Mamm. Sci. 24, 630–642 (2008).
doi: 10.1111/j.1748-7692.2008.00211.x
Zanette, L., White, A., Allen, M. & Clinchy, M. Perceived predation risk reduces the number of offspring songbirds produce per year. Science. 334, 1398–1401 (2011).
pubmed: 22158817
doi: 10.1126/science.1210908
Creel, S. & Christianson, D. Relationships between direct predation and risk effects. Trends Ecol. Evol. 23, 194–201 (2008).
pubmed: 18308423
doi: 10.1016/j.tree.2007.12.004
Ford, J. & Reeves, R. Fight or flight: antipredator strategies of baleen whales. Mammal Rev. 38(1), 50–86 (2008).
doi: 10.1111/j.1365-2907.2008.00118.x
McSweeney, D. J., Baird, R. W. & Mahaffy, S. D. Site fidelity, associations and movements of Cuvier’s (Ziphius cavirostris) and Blainville’s (Mesoplodon densirostris) beaked whales off the island of Hawai’i. Marine Mammal Science 23, 666–687 (2007).
doi: 10.1111/j.1748-7692.2007.00135.x
Cañadas, A. pers.comm. Observations of striped dolphins harassing a Cuvier’s beaked whale in the Mediterranean.
Jefferson, T. A., Stacey, P. J. & Baird, R. W. A review of killer whale interactions with other marine mammals: predation to co-existence. Mammal Rev. 21, 151–180 (1991).
doi: 10.1111/j.1365-2907.1991.tb00291.x
Wellard, R. et al. Killer whale (Orcinus orca) predation on beaked whales (Mesoplodon spp.) in the Bremer Sub-Basin, Western Australia. PLoS One 11, e0166670 (2016).
pubmed: 27923044
pmcid: 5140045
doi: 10.1371/journal.pone.0166670
Gualtieri, D. & Pitman, R. L. Killer Whale (Orcinus orca) Predation on a Gervais’ Beaked Whale (Mesoplodon europaeus) in the Eastern Atlantic Ocean. Aquat. Mamm. 45(2), 244–245 (2019).
doi: 10.1578/AM.45.2.2019.244
Johnson, M., Madsen, P. T., Zimmer, W. M. X., Soto, N. Ade & Tyack, P. L. Beaked whales echolocate on prey. Proc. R. Soc. London. Ser. B Biol. Sci. 271, S383–S386 (2004).
Barrett-Lennard, L. G., Ford, J. K. B. & Heise, K. A. The mixed blessing of echolocation: differences in sonar use by fish-eating and mammal-eating killer whales. Anim. Behav. 51, 553–565 (1996).
doi: 10.1006/anbe.1996.0059
Williams, R. & Noren, D. P. Swimming speed, respiration rate, and estimated cost of transport in adult killer whales. Mar. Mammal Sci. 25, 327–350 (2009).
doi: 10.1111/j.1748-7692.2008.00255.x
Andersen, S. & Amundin, M. Possible predator-related adaption of sound production and hearing in the harbour porpoise (Phocoena phocoena). Aquat. Mamm (1976).
Morisaka, T. & Connor, R. C. Predation by killer whales (Orcinus orca) and the evolution of whistle loss and narrow-band high frequency clicks in odontocetes. J. Evol. Biol. 20, 1439–1458 (2007).
pubmed: 17584238
doi: 10.1111/j.1420-9101.2007.01336.x
De Stephanis, R. et al. Mobbing-like behavior by pilot whales towards killer whales: a response to resource competition or perceived predation risk? Acta Ethol, https://doi.org/10.1007/s10211-014-0189-1 (2014).
doi: 10.1007/s10211-014-0189-1
Curé, C. et al. Responses of male sperm whales (Physeter macrocephalus) to killer whale sounds: implications for anti-predator strategies. Sci. Rep. 3(1), 1579 (2013).
pubmed: 23545484
pmcid: 3613802
doi: 10.1038/srep01579
Marques, T. A., Thomas, L., Ward, J., DiMarzio, N. & Tyack, P. L. Estimating cetacean population density using fixed passive acoustic sensors: An example with Blainville’s beaked whales. J. Acoust. Soc. Am. 125, 1982–1994 (2009).
pubmed: 19354374
doi: 10.1121/1.3089590
Baird, R. W. Behavior and Ecology of Not-So-Social Odontocetes: Cuvier’s and Blainville’s Beaked Whales. In: Würsig (ed.), Ethology and Behavioral Ecology of Marine Mammals. Springer. ISSN: 2523–7500 (2019).
Tyack, P. L. et al. Beaked whales respond to simulated and actual navy sonar. PLoS One 6, e17009 (2011).
pubmed: 21423729
pmcid: 3056662
doi: 10.1371/journal.pone.0017009
Miller, P. J. O. et al. First indications that northern bottlenose whales are sensitive to behavioural disturbance from anthropogenic noise. R. Soc. Open Sci. 2, 140484 (2015).
pubmed: 26543576
pmcid: 4632540
doi: 10.1098/rsos.140484
Allen, A. N., Schanze, J. J., Solow, A. R. & Tyack, P. L. Analysis of a Blainville’s beaked whale’s movement response to playback of killer whale vocalizations. Mar. Mammal Sci. 30, 154–168 (2014).
doi: 10.1111/mms.12028
DeRuiter, S. L. et al. First direct measurements of behavioural responses by Cuvier’s beaked whales to mid-frequency active sonar. Biol. Lett. 9, 20130223 (2013).
pubmed: 23825085
pmcid: 3730631
doi: 10.1098/rsbl.2013.0223
Frantzis, A. Does acoustic testing strand whales? Nature 392, 29 (1998).
pubmed: 9510243
doi: 10.1038/32068
Jepson, P. D. et al. Gas-bubble lesions in stranded cetaceans. Nature 425, 575–576 (2003).
pubmed: 14534575
doi: 10.1038/425575a
pmcid: 14534575
Bernaldo de Quirós, Y. et al. Advances in research on the impacts of anti-submarine sonar on beaked whales. Proc. R. Soc. B 286, 20182533 (2019).
pubmed: 30963955
doi: 10.1098/rspb.2018.2533
D’Amico, A. et al. Beaked whale strandings and naval exercises. Aquat. Mamm. 35, 452–472 (2009).
doi: 10.1578/AM.35.4.2009.452
Johnson, M. P. & Tyack, P. L. A digital acoustic recording tag for measuring the response of wild marine mammals to sound. IEEE J. Ocean. Eng. 28, 3–12 (2003).
doi: 10.1109/JOE.2002.808212
Miller, P. J. O., Shapiro, A. D. & Deecke, V. B. The diving behaviour of mammal-eating killer whales (Orcinus orca): variations with ecological not physiological factors. Can. J. Zool. 88, 1103–1112 (2010).
doi: 10.1139/Z10-080
Towers, J. et al. Movements and dive behaviour of a toothfish-depredating killer and sperm whale. ICES J. Mar. Sci. 76(1), 298–311 (2019).
doi: 10.1093/icesjms/fsy118
Whitehead, H. Babysitting, dive synchrony, and indications of alloparental care in sperm whales. Behav Ecol Sociobiol 38, 237–244 (1996).
doi: 10.1007/s002650050238
Augusto, J. F., Frasier, T. R. & Whitehead, H. Characterizing alloparental care in the pilot whale (Globicephala melas) population that summers off Cape Breton, Nova Scotia, Canada. Mar. Mammal Sci (2016).
Tønnesen, P., Gero, S., Ladegaard, M., Johnson, M. & Madsen, P. T. First-year sperm whale calves echolocate and perform long, deep dives. Behav. Ecol. Soci. 72(10), https://doi.org/10.1007/s00265-018-2570-y (2018).
Gassmann, M., Wiggins, S. & Hildebrand, J. Three-dimensional tracking of Cuvier’s beaked whales’ echolocation sounds using nested hydrophone arrays. JASA 138, 2483 (2015).
doi: 10.1121/1.4927417
Clinchy, M., Sheriff, M. & Zanette, L. The ecology of stress. Predator-induced stress and the ecology of fear. Func. Ecol. 27, 56–65 (2013).
doi: 10.1111/1365-2435.12007
Martin Lopez, L. M., Miller, P. J. O., Aguilar de Soto, N. & Johnson, M. Gait switches in deep-diving beaked whales: biomechanical strategies for long-duration dives. J. Exp. Biol. 218, 1325–1338 (2015).
pubmed: 25954042
doi: 10.1242/jeb.106013
Berman, T., Walline, P., Schneller, A., Rothenberg, J. & Townsend, D. Secchi disk depth record: a claim for the Eastern Mediterranean. Limn. Oceano. 30, 447 (1985).
doi: 10.4319/lo.1985.30.2.0447
Baird, R. W. et al. Diving behaviour of Cuvier’s (Ziphius cavirostris) and Blainville’s (Mesoplodon densirostris) beaked whales in Hawai’i. Can. J. Zool. 84, 1120–1128 (2006).
doi: 10.1139/z06-095
Barclay, R. M. R. Interindividual use of echolocation calls: Eavesdropping by bats. Behav. Ecol. Sociobiol. 10, 271–275 (1982).
doi: 10.1007/BF00302816
Mead, J. G. Beaked whales, overview. In: Encyclopedia of Marine Mammals, 2nd edition. Perrin, W. F., Würsig, B. & Thewissen, J. G. M. (Eds.), Academic Press, San Diego, pp. 81–84 (2002).
Pitman, R., Balance, L., Mesnick, S. & Chivers, S. Killer whale predation on sperm whales: observations and implications. Mar. Mam. Sci. 17, 494–507 (2001).
doi: 10.1111/j.1748-7692.2001.tb01000.x
Laundré, J., Hernández, L. & Ripple, W. The landscape of fear: ecological implications of being afraid. Open Ecol. J. 3, 1–7 (2010).
doi: 10.2174/1874213001003030001
Blumstein, D. et al. The evolution of capture myopathy in hooved mammals: a model for human stress cardiomyopathy? Evolution, Medicine, and Public Health 2015(1), 195–203 (2015).
pubmed: 26198189
pmcid: 4538952
doi: 10.1093/emph/eov015
Fernández, A., Sierra, E., Martin, V. M. M. & Sacchini, S. Last ‘atypical’beaked whales mass stranding in the Canary Islands (July, 2004). Journal Marine Science Research and Develpment 2 (2012).