Pouches, pockets and sacs in the heads, necks and chests of mammals, part III: baleen whales

Time to continue in the Tet Zoo series on laryngeal diverticula (and other pouches, pockets and sacs). This time, we look at baleen whales, or mysticetes. 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 [adjacent cartoon from Desray Reeb's 1997 thesis].

* The laryngeal ventricles are normally bilateral recesses, located on either sides of the glottis (if you need help with the terminology, remember to see the relevant section in the first article).

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 they 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 at depth (and 'at depth' should - based on what we know about dive depths of whales and on the distribution of possible prey - be well below 100 m). The problem with this idea is that it can't really work at depth at all, 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)

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 & PÃ¥sche (2001) as "the greatest respiratory action in history" (p. 353) [Blue whale blow shown here, from wikipedia]. What is it with cetaceans and superlatives? Brodie & PÃ¥sche (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 & PÃ¥sche (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 & PÃ¥sche (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 has 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).

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 [marked 's' in upper diagram] 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.

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 & PÃ¥sche (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. 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 [the image below of (part of) a Caperea skeleton comes from my 1997 BSc thesis: I copied it from the skeletal drawing in Ellis (1982)]. 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).

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)) [a juvenile Caperea skeleton is shown below; photographed at the University of Cambridge Museum of Zoology].

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.

A few ING-related announcements

Finally for now, the obvious link between the content of this article and Inside Nature's Giants (you might recall the ING series 1 rorqual episode) brings me to a few ING-related announcements. Firstly of all, please visit Channel 4's ING site: it has tons of neat stuff, including background information on the episodes, games, biographies and interviews. Secondly, those of you in the UK, and in the London area in particular, might be interested to know that the 75-minute giant squid episode of ING will be shown at the Clapham Picturehouse (on Venn Street) on the evening of Sunday 24th October. Even better, the showing will be followed by a Q&A session with members of the ING team (including Joy Reidenberg). Note that you have to book and pay online: you can't just turn up. I'll be there - I hope some of you will be too!

For the previous article on pouches, pockets and sacs in mammal heads, necks and chests, see...

• Pouches, pockets and sacs in the heads, necks and chests of mammals, part I: primates
• Pouches, pockets and sacs in the heads, necks and chests of mammals, part II: elephants have a pouch in the throat... or do they?

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
• Dissecting an emu
• Ridiculous super-elongate, coiled windpipes allow some birds to function like trombones - - or is it violins?
• Inside Nature's Giants part IV: the incredible anatomy of the giraffe
• Dissecting lions and tigers: Inside Nature's Giants series 2, part III

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
• From cigar to elongated, bloated tadpole: rorquals part II
• Lunging is expensive, jaws can be noisy, and what's with the asymmetry? Rorquals part III
• Inside Nature's Giants part II: whale guts and hindlimbs ahoy
• When GREY WHALES - you know, from the PACIFIC OCEAN - crossed the Atlantic

Refs - -

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 3rd, Schneider JN, Pack AA, & Herman LM (2010). Sound production by singing humpback whales. The Journal of the Acoustical Society of America, 127 (4), 2678-91 PMID: 20370048

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.

- . & 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.

- . & 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.

- . & Laitman , J. T. 2010. Generation of sound in marine mammals. In Brudzynski, S. M. (ed) Handbook of Mammalian Vocalization. Elsevier, pp. 451-466.