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).

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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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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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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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