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Discovery of a sensory organ that coordinates lunge feeding in rorqual whales

Abstract

Top ocean predators have evolved multiple solutions to the challenges of feeding in the water1,2,3. At the largest scale, rorqual whales (Balaenopteridae) engulf and filter prey-laden water by lunge feeding4, a strategy that is unique among vertebrates1. Lunge feeding is facilitated by several morphological specializations, including bilaterally separate jaws that loosely articulate with the skull5,6, hyper-expandable throat pleats, or ventral groove blubber7, and a rigid y-shaped fibrocartilage structure branching from the chin into the ventral groove blubber8. The linkages and functional coordination among these features, however, remain poorly understood. Here we report the discovery of a sensory organ embedded within the fibrous symphysis between the unfused jaws that is present in several rorqual species, at both fetal and adult stages. Vascular and nervous tissue derived from the ancestral, anterior-most tooth socket insert into this organ, which contains connective tissue and papillae suspended in a gel-like matrix. These papillae show the hallmarks of a mechanoreceptor, containing nerves and encapsulated nerve termini. Histological, anatomical and kinematic evidence indicate that this sensory organ responds to both the dynamic rotation of the jaws during mouth opening and closure, and ventral groove blubber7 expansion through direct mechanical linkage with the y-shaped fibrocartilage structure. Along with vibrissae on the chin9, providing tactile prey sensation, this organ provides the necessary input to the brain for coordinating the initiation, modulation and end stages of engulfment, a paradigm that is consistent with unsteady hydrodynamic models and tag data from lunge-feeding rorquals10,11,12,13. Despite the antiquity of unfused jaws in baleen whales since the late Oligocene14 (23–28 million years ago), this organ represents an evolutionary novelty for rorquals, based on its absence in all other lineages of extant baleen whales. This innovation has a fundamental role in one of the most extreme feeding methods in aquatic vertebrates, which facilitated the evolution of the largest vertebrates ever.

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Figure 1: Key jaw anatomy of a rorqual lunge, shown in a fin whale ( B. physalus).
Figure 2: Anatomy and histology of the rorqual mandibular symphysis, shown in fin whales ( B. physalus).
Figure 3: Digital imaging of the rorqual chin, shown in fin whales ( B. physalus).

References

  1. Sanderson, S. L. & Wassersug, R. in The Skull, Functional and Evolutionary Mechanisms Vol. 3 (eds Hanken, J. & Hall, B. K. ) 37–112 (Univ. Chicago Press, 1993)

    Google Scholar 

  2. Friedman, M. et al. 100-million-year dynasty of giant planktivorous bony fishes in the Mesozoic seas. Science 327, 990–993 (2010)

    Article  CAS  ADS  Google Scholar 

  3. Werth, A. J. in Feeding: Form, Function and Evolution in Tetrapod Vertebrates (ed. Schwenk, K. ) 475–514 (Academic, 2000)

    Google Scholar 

  4. Goldbogen, J. A. The ultimate mouthful: lunge feeding in rorqual whales. Am. Sci. 98, 124–131 (2010)

    Article  Google Scholar 

  5. Brodie, P. F. in Secondary Adaptation of Tetrapods to Life in Water (eds Mazin, J.-M. & de Buffrenil, V. ) 345–352 (Pfeil, 2001)

    Google Scholar 

  6. Lambertsen, R., Ulrich, N. & Straley, J. Frontomandibular stay of Balaenopteridae: a mechanism for momentum recapture during feeding. J. Mamm. 76, 877–899 (1995)

    Article  Google Scholar 

  7. Orton, L. S. & Brodie, P. F. Engulfing mechanics of fin whales. Can. J. Zool. 65, 2898–2907 (1987)

    Article  Google Scholar 

  8. Pivorunas, A. Fibrocartilage skeleton and related structures of the ventral pouch of balaenopterid whales. J. Morphol. 151, 299–313 (1977)

    Article  CAS  Google Scholar 

  9. Ling, J. K. in Functional Anatomy of Marine Mammals (ed. Harrison, R. J. ) 387–415 (Academic, 1977)

    Google Scholar 

  10. Potvin, J., Goldbogen, J. A. & Shadwick, R. E. Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whales. J. R. Soc. Interface 6, 1005–1025 (2009)

    Article  CAS  Google Scholar 

  11. Potvin, J., Goldbogen, J. A. & Shadwick, R. E. Scaling of lunge feeding in rorqual whales: an integrated model of engulfment duration. J. Theor. Biol. 267, 437–453 (2010)

    Article  CAS  MathSciNet  Google Scholar 

  12. Goldbogen, J. A. et al. Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density. J. Exp. Biol. 214, 131–146 (2011)

    Article  CAS  Google Scholar 

  13. Goldbogen, J. A. et al. Scaling of lunge feeding performance in rorqual whales: mass-specific energy expenditure increases with body size and progressively limits diving capacity. Funct. Ecol. 26, 216–226 (2012)

    Article  Google Scholar 

  14. Fitzgerald, E. M. G. Archaeocete-like jaws in a baleen whale. Biol. Lett. 8, 94–96 (2012)

    Article  Google Scholar 

  15. Deméré, T. A., McGowen, M. R., Berta, A. & Gatesy, J. Morphological and molecular evidence for a step-wise evolutionary transition from teeth to baleen in mysticete whales. Syst. Biol. 57, 15–37 (2008)

    Article  Google Scholar 

  16. Fitzgerald, E. M. G. The morphology and systematics of Mammalodon colliveri (Cetacea: Mysticeti), a toothed mysticete from the Oligocene of Australia. Zool. J. Linn. Soc. 158, 367–476 (2010)

    Article  Google Scholar 

  17. Goldbogen, J. A., Pyenson, N. D. & Shadwick, R. E. Big gulps require high drag for fin whale lunge-feeding. Mar. Ecol. Prog. Ser. 349, 289–301 (2007)

    Article  ADS  Google Scholar 

  18. Lambertsen, R. H. Internal mechanism of rorqual feeding. J. Mamm. 64, 76–88 (1983)

    Article  Google Scholar 

  19. Brodie, P. F. Noise generated by the jaw actions of feeding fin whales. Can. J. Zool. 71, 2546–2550 (1993)

    Article  Google Scholar 

  20. Currey, J. D. Bones: Structure and Mechanics (Princeton Univ. Press, 2002)

    Google Scholar 

  21. Best, R. C. The tusk of the narwhal (Monodon monoceros L.): interpretation of its function (Mammalia: Cetacea). Can. J. Zool. 59, 2386–2393 (1981)

    Article  Google Scholar 

  22. McKenna, M. F., Cranford, T. W., Berta, A. & Pyenson, N. D. Morphological diversity of the odontocete melon: implications for acoustic function. Mar. Mamm. Sci. (2011)

  23. Tershy, B. R. & Wiley, D. M. Asymmetrical pigmentation in the fin whale: a test of two feeding related hypotheses. Mar. Mamm. Sci. 8, 315–318 (1992)

    Article  Google Scholar 

  24. Canning, C. et al. Population-level lateralized feeding behaviour in North Atlantic humpback whales, Megaptera novaeangliae . Anim. Behav. 82, 901–909 (2011)

    Article  Google Scholar 

  25. Catania, K. C., Hare, J. F. & Campbell, K. L. Water shrews detect movement, shape, and smell to find prey underwater. Proc. Natl Acad. Sci. USA 105, 571–576 (2008)

    Article  CAS  ADS  Google Scholar 

  26. Czech-Damal, N. U. et al. Electroreception in the Guiana dolphin (Sotalia guianensis). Proc. R. Soc. Lond. B 279, 663–668 (2012)

    Article  Google Scholar 

  27. Thewissen, J. G. M. & Nummela, S. Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates. (Univ. California Press, 2008)

    Google Scholar 

  28. Scapino, R. Morphological investigation into functions of the jaw symphysis in carnivorans. J. Morphol. 167, 339–375 (1981)

    Article  CAS  Google Scholar 

  29. Johnston, C. et al. Observations on the musculoskeletal anatomy of the head of a neonate gray whale (Eschrichtius robustus). Mar. Mamm. Sci. 26, 186–194 (2010)

    Article  Google Scholar 

  30. Reeves, R. R. & Smith, T. D. in Whales, Whaling, and Ocean Ecosystems (eds Estes, J. A. et al.) 82–101 (Univ. California Press, 2006)

    Google Scholar 

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Acknowledgements

For logistical support, we thank K. Loftsson and the staff at Hvalur hf; D. Ólafsdóttir, S. D. Halldórsson and G. A. Víkingsson at the Marine Research Institute, Reykjavík; G. Bergmann and the staff at Hrefnuveiðimenn ehf; S. Raverty; P. F. Brodie; and A. Trites. For additional samples and data, we also thank P.-Y. Daoust, G. Williams, the Amarok Hunters and Trappers Organization of Iqaluit, Captain S. Awa and the Inuit whaling crew from Iqaluit, J. Higgins and the Cascadia Research Collective, M. R. Buono, A. van Helden and the Museum of New Zealand Te Papa Tongarewa, and R. E. Fordyce. We also thank T. S. Hunter for assistance with laboratory samples. Comments from D. J. Bohaska, M. T. Carrano, R. B. Irmis, J. G. Mead, J. F. Parham, C. W. Potter and J. Velez-Juarbe improved this manuscript. N.D.P. was supported by a postdoctoral research fellowship from the Natural Sciences and Engineering Research Council of Canada and by funding from the Smithsonian Institution and its Remington Kellogg Fund. J.A.G. was supported by a University Graduate Fellowship for Research from the University of British Columbia, a Scripps Postdoctoral Research Fellowship and NSERC funding to R.E.S.

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Authors

Contributions

N.D.P., J.A.G., A.W.V. and R.E.S. conducted field and laboratory investigations and wrote the paper. G.S. provided expertise with XRCT scanning and image reconstruction, and R.L.D. supervised the MRI reconstructions.

Corresponding author

Correspondence to Nicholas D. Pyenson.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text, Supplementary Table 1, Supplementary Figures 1- 9 and Supplementary References. (PDF 6605 kb)

Supplementary Movie 1

This movie shows a mandibular symphysis of an adult fin whale (B. physalus), rendered in 3D. (MOV 19914 kb)

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Pyenson, N., Goldbogen, J., Vogl, A. et al. Discovery of a sensory organ that coordinates lunge feeding in rorqual whales. Nature 485, 498–501 (2012). https://doi.org/10.1038/nature11135

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