Way back in 2010, I published a series of articles on the various pouches, pockets and sacs (virtually all of which are laryngeal diverticula of one sort or another) that exist in the heads, necks and chests of mammals. I never finished that series.
Caption: screengrabs of parts I and II of the pouches, pockets and sacs series.
Here’s one of the articles from that series: the one on baleen whales. The original is here. I haven’t really updated it relative to the 2010 original, but if corrections are required I’ll add them when time allows.
Caption: cartoon from Desray Reeb's 1997 thesis, the bagpipe here being a clever reference to the potential role of the laryngeal sac as a vocal organ… on which read on.
Like the primates we looked at previously, mysticetes have enlarged laryngeal ventricles* that (mostly) meet along the ventral midline of the throat and form a single large laryngeal pouch or sac. The presence of a raphe along the sac's ventral midline seems to mark the line of fusion between the two ancestral, bilateral sacs. It's probably understandable that few of us are aware of the presence of inflatable laryngeal sacs in mysticetes, but people have known about the existence of these structures for a long time: pioneering scientist and surgeon John Hunter, for example, wrote about their presence in Northern/Common minke whales Balaenoptera acutorostrata in 1787, and they've frequently been remarked on in the cetacean anatomical literature.
* The laryngeal ventricles are normally bilateral recesses, located on either sides of the glottis (if you need help with the terminology, see the relevant section in the first article).
Caption: everything about whales is amazing. Here’s a minke whale skeleton, probably belonging to a Northern or Common minke. I should mention in passing that minke whales appear to be a species complex. Image: User BS Thurner Hof, CC BY-Sa 3.0 (original here).
The sac is surrounded by muscle and is very flexible: when it's contracted, a series of folds in the side walls provide additional surface area that facilitates expansion (Reidenberg & Laitman 2007a). Some authors have suggested that the sac can be filled with air when the whale surfaces, and that the sac can then be used as an oxygen store during diving (Negus 1962). The idea here is that the whales are able to push this stored gas from the laryngeal sac into the lungs and thereby 'take a breath' while submerged.
Caption: it should be obvious from this article where the laryngeal sac is located, but this dissection image of Fin whale anatomy (from Brodie & Påsche 2001, p. 357) helps. Here, you’re standing in the location of the lungs, looking towards the position of the tip of the snout. The trachea (t) is huge and wide (c 40 cm); the oesophagus (e) is above it. The laryngeal sac (s) is massive, heavily muscular, and beneath the trachea.
The problem with this idea is that it can't really work at depth, given that the lungs are thought to collapse at depths greater than 100 m, thereby making any gas exchange impossible (Reeb & Best 1999). Also possibly counting against the idea of an extra 'gas store' in mysticetes is that it seems inconsistent with the surprisingly low theoretical aerobic dive limits (TADLs) present in some species (namely the rorquals): I covered the topic of mysticete TADLs, and other neat aspects of their diving and feeding behaviour, here.
However, while respiratory exchange might not be possible at depth, it's still theoretically conceivable that the laryngeal sac might work as a gas store in shallow water... even though this would put the whales close to the surface and hence in relatively ready reach of the sea surface. Also possible is that the sac does indeed serve as a 'gas store', but that the role of this gas is not a respiratory one: maybe the whales move gases from the sac into other parts of the respiratory tract to prevent lung collapse, or ear damage, during diving (Reidenberg & Laitman 2010)
Caption: Blue whale exhaling at the surface, "the greatest respiratory action in history". Image: NOAA, public domain (original here).
A role in dynamic exhalation? Another really interesting possibility is that the sac doesn't function as a 'store' at all, but that it plays a crucial role in the dynamic exhalation practised by these animals: an event described by Brodie & Påsche (2001) as "the greatest respiratory action in history" (p. 353). What is it with cetaceans and superlatives? Brodie & Påsche (2001) proposed that – in its inflated condition – the laryngeal sac becomes forced up against the glottis when the whale is at depth, and thereby forces the arms of the paired arytenoid cartilages together to form a tight seal. The arms of the arytenoid cartilages seem to be similar in all mysticetes, and have often been referred to in the descriptive literature as 'lips' located at the opening of the laryngeal sac.
Increasing the pressure within the sac forces the arytenoid cartilage arms to push even closer together: they seem to act as a self-sealing valve. In another memorable quote, Brodie & Påsche (2001) said that "the remarkable size and robust nature of this entire tracheal/laryngeal mechanism appears more reminiscent of some man-made industrial device, than a component of the respiratory tract of a mammal" (p. 359).
It might be that, as pressure is relieved in the trachea (through the opening of the blowhole), the seal formed by the arytenoid cartilages relaxes, causing the laryngeal sac to deflate and fall away from its close contact with the trachea. This, in turn, allows the gases in the bronchi and lungs to be suddenly released; they then rush outwards at high speed, forming the characteristically explosive blow. Brodie & Påsche (2001) performed a number of experiments with the laryngeal sacs of fin and sei whales at an Icelandic whaling station, and found that the structures operated as hypothesised. Their proposal that the sac facilitates high velocity exhalation is a neat one... the problem is that it seems to contradict other possible functions, as we'll see.
A vocal role. Moving away from a role in exhalation, it's also been argued that the sac is used in vocalising. It's well known that mysticetes are able to generate low-frequency noises, and there's no doubt that these noises come from the lower and lateral parts of the throat (a contrast to odontocetes [toothed whales], where noises are mostly – but perhaps not entirely – generated by apparatus around and within the nasal region). Accordingly, it’s been suggested that the comparatively enormous mysticete larynx is the source of these sounds (e.g,, Quayle 1991, Reidenberg & Laitman 2007a). Recent spectral analyses of Humpback Megaptera novaeangliae songs seem to show that the noises are indeed generated here, with resonating air chambers probably contributing to sound production (Mercado et al. 2010).
Caption: diagram (from Reidenberg & Laitman 2007b) showing how the laryngeal sac (marked 's' in upper diagram) might partly function as an air store, receive air from the lungs, and have a role in the production of a bubble cloud.
How might the sac contribute to vocalisation? Perhaps it enables air to be 'recycled' between the larynx and lungs during vocalising. And perhaps it (also?) acts as a resonating chamber when inflated (some pinnipeds may use laryngeal diverticula in the same way: we'll be looking at pinnipeds, and other carnivorans, later on). The adjacent diagram (from Reidenberg & Laitman 2007b) shows a Humpback using the laryngeal sac in concert with its lungs and mouth during the release of a bubble cloud (the ability of humpback whales to release bubbles is itself a fascinating and complex operation).
The massive size of the mysticete larynx, the large size of the expandable laryngeal sac, and the large size of these animals in general seem, combined, to allow mysticetes to generate some of the loudest, longest and lowest sounds produced by any mammal. As Reidenberg & Laitman (2010) said, they are vocal athletes.
Caption: most of us know that humpbacks sing, and make a variety of other sounds too. But the idea that laryngeal structures have a possible resonating role isn’t well known outside of specialists on cetacean anatomy. Image: Christopher Michel, CC BY 2.0 (original here).
That contradiction I mentioned earlier. You might have noticed that the possible use of the laryngeal sac in seal-forming and dynamic exhalation (as proposed by Brodie & Påsche (2001)) is, apparently, at odds with the possible use of the sac in relieving pressure in the respiratory tract or ear region, as a gas store, or in vocalising. If the sac works in maintaining a tight seal at the arytenoid cartilages, it has to (I presume) remain inflated: if it becomes deflated, high pressure in the bronchi and lungs is lost, and the relaxation of the proposed laryngeal seal cannot be the 'trigger' responsible for dynamic exhalation. Yet, if the sac is used in vocalising or as a store allowing deeper and/or longer dives, gas simply must be passed back and forth between the sac and the trachea at least. It seems to me that the possible role of the laryngeal sac in vocalising is likely and backed by experimental support. Ergo, the presence of a permanently inflated sac that help form a seal against the glottis cannot be permitted. The proposals seem to contradict one another.
However... is it possible that the sac might still work in sealing the glottis at particular times (such as immediately prior to exhalation)? Maybe the sac can be used as a gas store and/or as a resonating chamber when the whale is at depth (albeit not at depths greater than 100 m, as discussed above), but can be pressurised and used to seal the throat when the whale approaches the surface for exhalation? If mysticetes can blow and vocalise at the same time, the 'glottal seal' hypothesis is dead. Probably.
Caperea: weird weird weird, like you didn't already know. While the laryngeal sacs of most mysticetes are located on the midline, that of the weird little Pygmy right whale Caperea marginata is positioned on the animal's right side (Reeb & Best 1999). The sac undergoes extensive expansion and contraction: possibly more than that of any other mysticete.
Caption: Caperea lungs and associated laryngeal sac (in the human hand).
It's possible that the unusual laryngeal sac anatomy of Caperea explains the unusually long thorax* and weird, partially overlapping, strangely flattened ribs of this whale: this long thorax, and the weird rib shape, might provide a lot more space for expansion of the laryngeal sac, and help to protect and maintain the sac's shape when fully inflated (Reeb & Best 1999). The ambiguity in this explanation – for which I apologise – results from the fact that the proposed correlation here is a vague, speculative and un-tested. It's also been said that the ribs of Caperea are rather loosely connected to the transverse processes of the vertebrae (Beddard 1901), perhaps implying that the ribcage is more flexible than is usual for a mysticete. Those weird ribs have always been the source of interesting speculation: there's the idea that they function as some sort of armour, and the peculiar notion that they perhaps help support the whale's weight when it lies on the sea floor... yeah, because whales are always lying down on the seafloor, right?
* The thoracic vertebrae make up about 39-45% the length of the vertebral column, whereas they make up less than 33% the length of the column in all other mysticetes (Reeb & Best 1999).
Caption: image from a Caperea dissection, showing the distinctive, partly overlapping ribs of this most unusual whale.
As every Caperea fan knows, the dissection of a juvenile that stranded in New Zealand in 2007 was live-blogged at Te Papa's Blog. A team of international experts, including Catherine Kemper, Ewan Fordyce, Joy Reidenberg and Sentiel Rommel, assisted in the dissection: the image above of the lungs and (juvenile!) laryngeal sac is borrowed from the event, as is the adjacent picture of the peculiar, overlapping ribs (the size of the laryngeal sac increases substantially during ontogeny: the adult sac is about five times bigger than that of the juvenile (Reeb & Best 1999)).
Caption: Caperea skeleton, photographed in New Zealand. Other images of the same skeleton appear in this Tet Zoo article from 2010. Image: Joy Riedenberg, used with permission.
We'll finish on cetaceans by noting that laryngeal sacs are not unique to mysticetes: they're also present in such odontocetes as the Sperm whale Physeter macrocephalus, Beluga Delphinapterus leucas and Risso's dolphin Grampus griseus.
For the previous article on pouches, pockets and sacs in mammal heads, necks and chests, see...
If you're interested in tracheae and their role in respiration, vocalising and such, or on any of the associated structures in the neck, check out...
Deer oh deer, this joke gets worse every time I use it, November 2007
Dissecting an emu, April 2009
Inside Nature's Giants part IV: the incredible anatomy of the giraffe, July 2009
Dissecting lions and tigers: Inside Nature's Giants series 2, part III, September 2010
And for more on mysticete anatomy, evolution and diversity, see...
A 6 ton model, and a baby that puts on 90 kg a day: rorquals part I, October 2006
From cigar to elongated, bloated tadpole: rorquals part II, October 2006
Lunging is expensive, jaws can be noisy, and what’s with the asymmetry? Rorquals part III, October 2006
Inside Nature's Giants part II: whale guts and hindlimbs ahoy, July 2009
When GREY WHALES - you know, from the PACIFIC OCEAN - crossed the Atlantic, May 2010
Did I mention that Caperea is really, really weird?, October 2010
Once more on little Caperea, October 2010
Caperea alive!, November 2010
Cetacean Heresies: How the Chromatic Truthometer Busts the Monochromatic Paradigm, April 2015 (but now lacking all images)
Whale Watching in the Bay of Biscay, August 2019
Beddard, F. E. 1901. Contribution towards a knowledge of the osteology of the pygmy whale (Neobalaena marginata). Transactions of the Zoological Society of London 16, 87-114.
Brodie, P. F. & Påsche, A. J. 2001. The mechanics of cetacean respiration: the significance of rapid gas exchanges in a selectively tuned system, with emphasis on the rorquals (Balaenoptera sp.). In Mazin, J.-M. & de Buffrénil, V. (eds) Secondary Adaptation of Tetrapods to Life in Water. Dr Friedrich Pfeil (München), pp. 353-362.
Ellis, R. 1982. The Book of Whales. Alfred Knopf, New York.
Mercado, E., Schneider, J. N., Pack, A. A. & Herman, L. M. 2010. Sound production by singing humpback whales. The Journal of the Acoustical Society of America 127 2678-2691.
Negus, V. E. 1962. The Comparative Anatomy and Physiology of the Larynx. New York, Hafner.
Quayle, C. J. 1991. A dissection of the larynx of a humpback whale calf with a review of its functional morphology. Memoirs of the Queensland Museum 30, 351-354.
Reeb, D. 1997. Comparative anatomy of the larynx of the minke whale, Balaenoptera acutorostrata and the pygmy right whale, Caperea marginata. MSc disertation, University of Pretoria, Pretoria.
Reeb, D. & Best, P. B. 1999. Anatomy of the laryngeal apparatus of the pygmy right whale, Caperea marginata (Gray 1846). Journal of Morphology 242, 67-81.
Reidenberg , J. S. & Laitman , J. T. 2007a. Discovery of a low frequency sound source in Mysticeti (baleen whales): anatomical establishment of a vocal fold homolog. Anatomical Record 290, 745-760.
Reidenberg , J. S. & Laitman , J. T. 2007b. Blowing bubbles: an aquatic adaptation that risks protection of the respiratory tract in Humpback whales (Megaptera novaeangliae). The Anatomical Record 290, 569-580.
Reidenberg , J. S. & Laitman , J. T. 2010. Generation of sound in marine mammals. In Brudzynski, S. M. (ed) Handbook of Mammalian Vocalization. Elsevier, pp. 451-466.
