Slick, Stretchy Fascia Underlies the Sliding Tongue of Rorquals

The tongue of rorqual (balaenopterid) whales slides far down the throat into the expanded oral pouch as an enormous mouthful of water is engulfed during gulp feeding. As the tongue and adjacent oral floor expands and slides caudoventrally, it glides along a more superficial (outer) layer of ventral body wall musculature, just deep to the accordion‐like ventral throat pleats. We hypothesize that this sliding movement of adjacent musculature is facilitated by a slick, stretchy layer of loose areolar connective tissue that binds the muscle fibers and reduces friction: fascia. Gross anatomical examination of the gular region of adult minke, fin, and humpback whales confirms the presence of a discrete, three‐layered sublingual fascia interposed between adhering fasciae of the tongue and body wall. Histological analysis of this sublingual fascia reveals collagen and elastin fibers loosely organized in a random feltwork along with numerous fibroblasts in a watery extracellular matrix. Biomechanical testing of tissue samples in the field and laboratory, via machine‐controlled or manual stretching, demonstrates expansion of the sublingual fascia and its three layers up to 250% beyond resting dimensions, with slightly more extension observed in anteroposterior (rather than mediolateral or oblique) stretching, and with the most superficial of the fascia's three layers. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:735–744, 2019. © 2018 Wiley Periodicals, Inc.

[1]  R. Shadwick,et al.  Two Levels of Waviness Are Necessary to Package the Highly Extensible Nerves in Rorqual Whales , 2017, Current Biology.

[2]  A. Friedlaender,et al.  How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration. , 2017, Annual review of marine science.

[3]  A. Friedlaender,et al.  Kinematic Diversity in Rorqual Whale Feeding Mechanisms , 2016, Current Biology.

[4]  J. Potvin,et al.  Baleen Hydrodynamics and Morphology of Cross-Flow Filtration in Balaenid Whale Suspension Feeding , 2016, PloS one.

[5]  R. Shadwick,et al.  Stretchy nerves are an essential component of the extreme feeding mechanism of rorqual whales , 2015, Current Biology.

[6]  Sarah S. Kienle,et al.  Tongue and Hyoid Musculature and Functional Morphology of a Neonate Gray Whale (Cetacea, Mysticeti, Eschrichtius robustus) , 2015, Anatomical record.

[7]  Jean Potvin,et al.  Novel muscle and connective tissue design enables high extensibility and controls engulfment volume in lunge-feeding rorqual whales , 2013, Journal of Experimental Biology.

[8]  A. Werth Flow-dependent porosity and other biomechanical properties of mysticete baleen , 2013, Journal of Experimental Biology.

[9]  Peter T. Madsen,et al.  Keeping momentum with a mouthful of water: behavior and kinematics of humpback whale lunge feeding , 2012, Journal of Experimental Biology.

[10]  R. Shadwick,et al.  Discovery of a sensory organ that coordinates lunge feeding in rorqual whales , 2012, Nature.

[11]  J. Potvin,et al.  Mechanics, hydrodynamics and energetics of blue whale lunge feeding: efficiency dependence on krill density , 2011, Journal of Experimental Biology.

[12]  J. Goldbogen The Ultimate Mouthful: Lunge Feeding in Rorqual Whales , 2010 .

[13]  R. Shadwick,et al.  Skull and buccal cavity allometry increase mass-specific engulfment capacity in fin whales , 2010, Proceedings of the Royal Society B: Biological Sciences.

[14]  J A Goldbogen,et al.  Passive versus active engulfment: verdict from trajectory simulations of lunge-feeding fin whales Balaenoptera physalus , 2009, Journal of The Royal Society Interface.

[15]  A. Berta,et al.  Observations on the musculoskeletal anatomy of the head of a neonate gray whale (Eschrichtius robustus) , 2009 .

[16]  Robert E. Shadwick,et al.  Big gulps require high drag for fin whale lunge feeding , 2007 .

[17]  Alexander J Werth,et al.  Adaptations of the cetacean hyolingual apparatus for aquatic feeding and thermoregulation , 2007, The Anatomical Record.

[18]  John Calambokidis,et al.  Kinematics of foraging dives and lunge-feeding in fin whales , 2006, Journal of Experimental Biology.

[19]  P. Arnold,et al.  Gulping behaviour in rorqual whales: underwater observations and functional interpretation , 2005 .

[20]  R. Schleip,et al.  Active fascial contractility: Fascia may be able to contract in a smooth muscle-like manner and thereby influence musculoskeletal dynamics. , 2005, Medical hypotheses.

[21]  R. J. Hintz,et al.  MAXILLOMANDIBULAR CAM ARTICULATION DISCOVERED IN NORTH ATLANTIC MINKE WHALE , 2004 .

[22]  Alexander J. Werth,et al.  CHAPTER 16 – Feeding in Marine Mammals , 2000 .

[23]  Kurt Schwenk,et al.  Feeding : form, function, and evolution in tetrapod vertebrates , 2000 .

[24]  J. Dubbeldam,et al.  Histology of the grooved ventral pouch of the minke whale, Balaenoptera acutorostrata, with special reference to the occurrence of lamellated corpuscles , 1997 .

[25]  Janice M. Straley,et al.  Frontomandibular Stay of Balaenopteridae: A Mechanism for Momentum Recapture during Feeding , 1995 .

[26]  Lisa Schichtel Orton,et al.  Engulfing mechanics of fin whales , 1987 .

[27]  Richard H. Lambertsen,et al.  Internal Mechanism of Rorqual Feeding , 1983 .

[28]  W Hanafee,et al.  Computed tomography of the tongue and floor of the mouth. , 1982, Radiology.

[29]  A. Pivorunas,et al.  The fibrocartilage skeleton and related structures of the ventral pouch of Balaenopterid whales , 1977, Journal of morphology.

[30]  R. G. Ackman,et al.  Layering and tissue composition in the blubber of the northwest Atlantic sei whale (Balaenoptera borealis). , 1975, Canadian journal of zoology.

[31]  G. Doran Review of the evolution and phylogeny of the mammalian tongue. , 1975, Acta anatomica.

[32]  A. Solomon Anatomy: A Regional Study of Human Structure , 1960 .

[33]  Montgomery The occurrence of arteriovenous anastomoses in the tongue of the dog , 1938 .

[34]  M. E. Brown,et al.  The occurrence of arterio‐venous anastomoses in the tongue of the dog , 1937 .

[35]  F. Sonntag The Comparative Anatomy of the Tongues of the Mammalia.—VII. Cetaeea, Sirenia, and Ungulata. , 1922 .

[36]  Alexander Carte,et al.  VIII. On the anatomy of balænoptera rostrata , 1868, Philosophical Transactions of the Royal Society of London.