Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Editors' Suggestion
  • Open Access

Synchronization of bowhead whales

Evgeny A. Podolskiy1,*, Jonas Teilmann2, and Mads Peter Heide-Jørgensen3

  • *Contact author: e.podolskiy@arc.hokudai.ac.jp

Phys. Rev. Research 6, 033174 – Published 15 August, 2024

DOI: https://doi.org/10.1103/PhysRevResearch.6.033174

Abstract

Inferring animal behavior from irregular tracking data is a challenging area of research. It is particularly difficult to determine if whales, who intermittently explore different depths while staying in the same acoustic medium, synchronize their days with their prey and each other over kilometer-scale distances. Here, we aim to better understand the diving behavior of bowhead whales (Balaena mysticetus) in Disko Bay, West Greenland, using the largest high-frequency dive-depth dataset to date (144 days at 1 Hz from 12 different whales) and nonlinear dynamics, whereby we consider the whales to be chaotic (aperiodic) oscillators. We find that foraging whales dive deeper during the daytime in spring, with this diving behavior being in apparent synchrony with their vertically migrating prey. Furthermore, we demonstrate that bowhead whales can synchronize their behavior with each other for up to a week while staying within a range of up to ∼100km. This discovery agrees with the acoustic herd theory of long-range signaling in baleen whales. On the other hand, the synchrony might emerge when animals experience similar ecological conditions, which are, however, difficult to name because targeted depths and locations were separated for hundreds of meters and tens of kilometers, respectively. In this paper, we identify a framework for studying the sociality and behavior of such chaotically moving, unrestrained marine animals and call for more simultaneous tagging campaigns.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (50)

  1. J. C. George, J. Bada, J. Zeh, L. Scott, S. E. Brown, T. O'Hara, and R. Suydam, Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization, Can. J. Zool. 77, 571 (1999).
  2. B. Würsig and W. Koski, Natural and potentially disturbed behavior of bowhead whales, in The Bowhead Whale: Balaena Mysticetus: Biology and Human Interactions, edited by J. George and J. Thewissen (Academic Press/Elsevier, London, 2021), Chap. 23, pp. 339–363.
  3. M. S. Savoca, M. F. Czapanskiy, S. R. Kahane-Rapport, W. T. Gough, J. A. Fahlbusch, K. C. Bierlich, P. S. Segre, J. Di Clemente, G. S. Penry, D. N. Wiley et al., Baleen whale prey consumption based on high-resolution foraging measurements, Nature (London) 599, 85 (2021).
  4. L. Gilbert, T. Jeanniard-du Dot, M. Authier, T. Chouvelon, and J. Spitz, Composition of cetacean communities worldwide shapes their contribution to ocean nutrient cycling, Nat. Commun. 14, 5823 (2023).
  5. R. Suydam and J. George, Current indigenous whaling, in The Bowhead Whale. Balaena Mysticetus: Biology and Human Interactions, edited by J. George and J. Thewissen (Academic Press/Elsevier, London, 2021), Chap. 32, pp. 519–535.
  6. J. W. Higdon, Commercial and subsistence harvests of bowhead whales (Balaena mysticetus) in Eastern Canada and West Greenland, J. Cetacean Res. Manage. 11, 185 (2023).
  7. S. M. E. Fortune, S. H. Ferguson, A. W. Trites, J. M. Hudson, and M. F. Baumgartner, Bowhead whales use two foraging strategies in response to fine-scale differences in zooplankton vertical distribution, Sci. Rep. 10, 20249 (2020).
  8. C. J. D. Matthews, G. A. Breed, B. LeBlanc, and S. H. Ferguson, Killer whale presence drives bowhead whale selection for sea ice in arctic seascapes of fear, Proc. Natl. Acad. Sci. USA 117, 6590 (2020).
  9. S. M. E. Fortune, A. W. Trites, V. LeMay, M. F. Baumgartner, and S. H. Ferguson, Year-round foraging across large spatial scales suggest that bowhead whales have the potential to adapt to climate change, Front. Mar. Sci. 9, 853525 (2023).
  10. A. L. Willoughby, M. C. Ferguson, R. Stimmelmayr, J. T. Clarke, and A. A. Brower, Bowhead whale (Balaena mysticetus) and killer whale (Orcinus orca) co-occurrence in the U.S. Pacific Arctic, 2009–2018: Evidence from bowhead whale carcasses, Polar Biol. 43, 1669 (2020).
  11. The Bowhead Whale: Balaena Mysticetus: Biology and Human Interactions, edited by J. George and J. Thewissen (Academic Press/Elsevier, London, 2021).
  12. D. A. Croll, A. Acevedo-Gutiérrez, B. R. Tershy, and J. Urbán-Ramírez, The diving behavior of blue and fin whales: Is dive duration shorter than expected based on oxygen stores? Comp. Biochem. Physiol. A 129, 797 (2001).
  13. M. Simon, M. Johnson, P. Tyack, and P. T. Madsen, Behaviour and kinematics of continuous ram filtration in bowhead whales (Balaena mysticetus), Proc. R. Soc. B 276, 3819 (2009).
  14. M. P. Heide-Jørgensen, K. L. Laidre, N. H. Nielsen, R. G. Hansen, and A. Røstad, Winter and spring diving behavior of bowhead whales relative to prey, Anim. Biotelemetry 1, 15 (2013).
  15. E. A. Podolskiy and M. P. Heide-Jørgensen, Strange attractor of a narwhal (Monodon monoceros), PLoS Comput. Biol. 18, e1010432 (2022).
  16. A. Roy, S. Lanco Bertrand, and R. Fablet, Deep inference of seabird dives from GPS-only records: Performance and generalization properties, PLoS Comput. Biol. 18, e1009890 (2022).
  17. N. H. Packard, J. P. Crutchfield, J. D. Farmer, and R. S. Shaw, Geometry from a time series, Phys. Rev. Lett. 45, 712 (1980).
  18. F. Takens, Detecting strange attractors in turbulence, in Dynamical Systems and Turbulence, Warwick 1980, Lecture Notes in Mathematics Vol. 898, edited by D. Rand and L. Young (Springer, Berlin, 1981), Chap. 2, pp. 366–381.
  19. H. Kantz and T. Schreiber, Nonlinear Time Series Analysis (Cambridge University Press, Cambridge, 2003).
  20. R. A. York, A. Carreira-Rosario, L. M. Giocomo, and T. R. Clandinin, Flexible analysis of animal behavior via time-resolved manifold embedding, bioRxiv (2021), doi:10.1101/2020.09.30.321406.
  21. T. D. Pereira, J. W. Shaevitz, and M. Murthy, Quantifying behavior to understand the brain, Nat. Neurosci. 23, 1537 (2020).
  22. T. Ahamed, A. C. Costa, and G. J. Stephens, Capturing the continuous complexity of behaviour in Caenorhabditis elegans, Nat. Phys. 17, 275 (2021).
  23. S. Tajima, T. Mita, D. J. Bakkum, H. Takahashi, and T. Toyoizumi, Locally embedded presages of global network bursts, Proc. Natl. Acad. Sci. USA 114, 9517 (2017).
  24. S. R. Datta, D. J. Anderson, K. Branson, P. Perona, and A. Leifer, Computational neuroethology: A call to action, Neuron 104, 11 (2019).
  25. S. Strogatz, Nonlinear Dynamics and Chaos: with Applications to Physics, Biology, Chemistry, and Engineering (Westview Press, Boulder, 2015).
  26. R. Payne and D. Webb, Orientation by means of long range acoustic signaling in baleen whales, Ann. N.Y. Acad. Sci. 188, 110 (1971).
  27. S. Fortune, S. Ferguson, A. Trites, B. LeBlanc, V. LeMay, J. Hudson, and M. Baumgartner, Seasonal diving and foraging behaviour of Eastern Canada–West Greenland bowhead whales, Mar. Ecol. Prog. Ser. 643, 197 (2020).
  28. K. Laidre, M. Heide-Jørgensen, and T. Nielsen, Role of the bowhead whale as a predator in West Greenland, Mar. Ecol. Prog. Ser. 346, 285 (2007).
  29. J. Citta, J. Olnes, S. Okkonen, L. Quakenbush, J. George, W. Maslowski, R. Osinski, and M. Heide-Jørgensen, Influence of oceanography on bowhead whale (Balaena mysticetus) foraging in the Chukchi Sea as inferred from animal-borne instrumentation, Cont. Shelf Res. 224, 104434 (2021).
  30. P. Priou, A. Nikolopoulos, H. Flores, R. Gradinger, E. Kunisch, C. Katlein, G. Castellani, T. Linders, J. Berge, J. A. Fisher et al., Dense mesopelagic sound scattering layer and vertical segregation of pelagic organisms at the Arctic-Atlantic Gateway during the midnight sun, Prog. Oceanogr. 196, 102611 (2021).
  31. S. Gonzalez, J. K. Horne, and S. L. Danielson, Multi-scale temporal variability in biological-physical associations in the NE Chukchi Sea, Polar Biology 44, 837 (2021).
  32. P. G. H. Evans, Ecology and behaviour of the little auk Alle alle in West Greenland, Ibis 123, 1 (1981).
  33. K. M. Stafford, S. E. Moore, and C. G. Fox, Diel variation in blue whale calls recorded in the eastern tropical pacific, Anim. Behav. 69, 951 (2005).
  34. W. K. Oestreich, J. A. Fahlbusch, D. E. Cade, J. Calambokidis, T. Margolina, J. Joseph, A. S. Friedlaender, M. F. McKenna, A. K. Stimpert, B. L. Southall et al., Animal-borne metrics enable acoustic detection of blue whale migration, Curr. Biol. 30, 4773 (2020).
  35. C. P. H. Elemans, W. Jiang, M. H. Jensen, H. Pichler, B. R. Mussman, J. Nattestad, M. Wahlberg, X. Zheng, Q. Xue, and W. T. Fitch, Evolutionary novelties underlie sound production in baleen whales, Nature (London) 627, 123 (2024).
  36. A. Pikovsky, M. Rosenblum, and J. Kurths, Synchronization: A Universal Concept in Nonlinear Science (Cambridge University Press, Cambridge, 2001).
  37. S. Boccaletti, J. Kurths, G. Osipov, D. Valladares, and C. Zhou, The synchronization of chaotic systems, Phys. Rep. 366, 1 (2002).
  38. O. M. Tervo, M. F. Christoffersen, M. Simon, L. A. Miller, F. H. Jensen, S. E. Parks, and P. T. Madsen, High source levels and small active space of high-pitched song in bowhead whales (Balaena mysticetus), PLoS ONE 7, e52072 (2012).
  39. V. Senigaglia and H. Whitehead, Synchronous breathing by pilot whales, Mar. Mammal Sci. 28, 213 (2012).
  40. N. J. Quick, S. Isojunno, D. Sadykova, M. Bowers, D. P. Nowacek, and A. J. Read, Hidden Markov models reveal complexity in the diving behaviour of short-finned pilot whales, Sci. Rep. 7, 45765 (2017).
  41. B. Würsig and C. Clark, Behavior of bowhead whales, in The Bowhead Whale, edited by J. Burns, J. Montague, and C. Cowles (Allen Press, Lawrence, 1993), Chap. 5, pp. 157–199.
  42. C. Clark, W. Ellison, and K. Beeman, Acoustic tracking of migrating bowhead whales, in OCEANS '86 (IEEE, Washington, DC, USA, 1986), pp. 341–346.
  43. K. Stafford and C. Clark, Acoustic behaviour, in The Bowhead Whale: Balaena Mysticetus: Biology and Human Interactions, edited by J. George and J. Thewissen (Academic Press/Elsevier, London, 2021), Chap. 22, pp. 323–338.
  44. J. A. Fahlbusch, D. E. Cade, E. L. Hazen, M. L. Elliott, B. T. Saenz, J. A. Goldbogen, and J. Jahncke, Submesoscale coupling of krill and whales revealed by aggregative Lagrangian coherent structures, Proc. R. Soc. B 291, 20232461 (2024).
  45. H. M. Oliveira and L. V. Melo, Huygens synchronization of two clocks, Sci. Rep. 5, 11548 (2015).
  46. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevResearch.6.033174 for bowhead whale dive records from Disko Bay, West Greenland.
  47. M. Heide-Jørgensen, R. Hansen, and O. Shpak, Distribution, migrations, and ecology of the Atlantic and the Okhotsk Sea populations, in The Bowhead Whale: Balaena Mysticetus: Biology and Human Interactions, edited by J. George and J. Thewissen (Academic Press/Elsevier, London, 2021), Chap. 5, pp. 57–75.
  48. L. R. Nielsen, O. M. Tervo, S. B. Blackwell, M. P. Heide-Jørgensen, and S. Ditlevsen, Using quantile regression and relative entropy to assess the period of anomalous behavior of marine mammals following tagging, Ecol. Evol. 13, e9967 (2023).
  49. C. M. Albertsen, K. Whoriskey, D. Yurkowski, A. Nielsen, and J. M. Flemming, Fast fitting of non-Gaussian state-space models to animal movement data via template model builder, Ecology 96, 2598 (2015).
  50. E. Tan, S. Algar, D. Corrêa, M. Small, T. Stemler, and D. Walker, Selecting embedding delays: An overview of embedding techniques and a new method using persistent homology, Chaos 33, 032101 (2023).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation