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I’ve mentioned laryngeal and tracheal anatomy a few times on Tet Zoo (see the links at the very bottom for more). Well, time to look at it again. It’s (relatively) little known that a long list of mammal species possess an assortment of ‘pouches’, pocket-like structures and pneumatic sacs and spaces within their throats, skulls, chests, and sometimes on their palates. Some of these are air-filled, epithelium-lined structures that originate as outgrowths of the throat or windpipe, and are hence known as diverticula (singular: diverticulum) [image below shows Siamang Symphalangus syndactylus (from wikipedia) with inflated throat pouch, and a diagrammatic great ape showing the extent of the laryngeal pouches (based on a diagram in Meldrum (2006)].
As someone interested in pneumaticity, the mechanics and anatomy of respiration and vocalising, and in sheer weirdness, I’ve been planning for ages to write some articles that summarise our knowledge of these structures. It’s a fairly big subject, so I ended up writing quite a lot: this article is part 1 of a series of several.
Before looking at the structures of interest, a brief (and very basic) anatomical primer (for this and the following articles you’ll need to be familiar with the following terms… skip the next few paragraphs if you already know the anatomy).
A brief anatomical primer
The pharynx is the name for the space between the back of the mouth (and nasal cavity) and the most anterior part of the trachea: the trachea is the tube (held open by cartilaginous rings) that connects the pharynx to the bronchi and eventually the lungs. The upper part of the trachea is occupied by a specialised vocal compartment (and some associated glands), the larynx. The larynx is complicated, consisting of various different cartilaginous components and membranes, and contains the vocal folds (or vocal cords). The vocal folds and the immediate surrounding space are known as the glottis [some of these structures are shown in the adjacent sagittal section, ultimately from Gray's Anatomy but borrowed here from wikipedia].
Within the pharynx, the epiglottis is a projecting cartilaginous process located close to the base of the tongue, and normally kept in contact with the soft palate or velum (humans are unusual [though probably not unique] in possessing an epiglottis that is located some distance down the throat, and a short velum: this combination means that there is no contact between the two structures). In between the tongue and epiglottis is a shallow recess termed the epiglottic valecula: this is the part of the mouth where chewed food is formed into a bolus for swallowing. The nasal cavity, larynx and trachea can all be referred to collectively as the upper respiratory tract.
Finally, note that I won’t be talking about the various sinuses that are located within the nasal region, forehead, middle ear and temporal region of mammals (some mammals do possess the same combination of sinuses that we do, others do not). I might, however, mention some of the sinuses in passing.
Ok, time to move on…
Among the huge variety of air-filled sacs and spaces present in mammals, perhaps the ones that are of most interest to people are those seen in other hominids [male orangutan shown here, from here. The pendulous pouch on the chest is mostly occupied by laryngeal pouches]. Orangutans, gorillas and chimpanzees possess paired, inflatable sacs – termed laryngeal pouches (and actually representing hypertrophied versions of the laryngeal ventricles*) – that run along the sides of the neck and upper part of the chest [image below - from Fitch (2000) - compares the respiratory tract anatomy of (a) orangutan, (b) chimp and (c) human. The tongue is in red, the larynx in yellow and the air sacs in blue**. The non-human MRIs were provided by Sugio Hayama and Kiyoshi Honda]. The larger gibbons (like the Siamong shown at top] also possess these laryngeal pouches, as do some guenons, baboons, macaques and howler monkeys (Hewitt et al. 2002).
* Laryngeal ventricles (sometimes called the ventricles of Morgagni) are bilateral folds, located on the inside walls (close to the glottis) of the larynx. They are present in all primates. Some primates possess additional ventricles on either the dorsal (some lemurs and spider monkeys) or ventral (some lemurs and various New World and Old World monkeys) inside surfaces of the larynx.
** Air sacs across Tetrapoda are consistently shown in blue, even though there’s no proper convention on this sort of thing.
Studies have shown that the pouches of primates are inflated during exhalation (yes, exhalation: not inhalation), and that the air they contain is removed during inhalation. They can be surprisingly large, with those of orangutans extending to 6000 cubic cm when inflated (and thus being the biggest of any primate). Primate air sacs can be prone to bacterial infection: numerous species kept in captivity have been treated for air sac disorders and there’s a large veterinary literature on the subject, particularly in apes. Believe it or don’t, the commonest disease affecting air sacs is known as airsacculitis (the same name is used for air sac infection in birds).
As is the case with most structures present in living animals, the function of these diverticula is tremendously under-studied, but it’s widely thought that they act as resonating chambers used during vocalising. Other proposed acoustic roles include that they function as impedance matchers, or that they suppress resonance. An acoustic function is supported by the fact that the calls of a monkey (a De Brazza’s monkey Cercopithecus neglectus) were shown in a 1971 experiment to be lower in intensity after the pouches were punctured. And – in monkeys at least – the pouches are larger in males than females, and it’s males who make the louder calls.
However, other possible functions have been proposed: perhaps they help prevent hyperventilation during long bouts of calling, or perhaps they somehow strengthen the ribcage during climbing (yeah, don’t ask me how that one’s supposed to work). In another experiment, air sacs were surgically removed from a macaque (a Rhesus macaque Macaca mulatta), and its calls after the operation were reportedly no different than they were before. These observations perhaps suggest that the air sacs of primates have different roles in different species.
A question that’s been asked many times concerns their distribution within hominids. If non-human hominids have them, did humans possess them ancestrally? It’s generally agreed that they were lost some time between the divergence of the human lineage from the chimpanzee one. The good news is that their presence can be inferred from the shape of the hyoid bone. In chimps and some other primates with laryngeal pouches, the anterior part of the hyoid is enlarged, anteriorly convex and forms a hollow bulla (these are, so far as we know, the only cases in mammals of tracheal diverticula invading the skeleton). It’s well known that this hyoid bulla is over-the-top developed in howler monkeys (Alouatta) where it’s enormous, particularly in males [howler monkey - labelled as A. seniculus, but used in the old, inclusive sense of the name - with hypertrophied hyoid bulla shown here; photographed at the Cambridge University Museum of Zoology].
One australopithecine specimen – the juvenile A. afarensis from Dikika in Ethiopia (sometimes called ‘Selam’: shown here, from wikipedia) – definitely has a bulla, so australopithecines do seem to have had air sacs (Alemseged et al. 2006)*. Other fossil hyoids show that, like modern humans, at least some fossil members of our genus (H. neanderthalensis and H. heidelbergensis) lacked bullae, and thus probably lacked air sacs as we do. However, we can’t be absolutely sure about that because Pongo – which very definitely does have air sacs – has a simple hyoid without the bulla shape.
* Because the Dikika specimen is a juvenile, it’s always possible that hyoid shape changed during ontogeny.
Nevertheless, for now it seems fairly sensible to assume that air sacs were present in early members of the human lineage, but lost somewhere between Australopithecus and the younger members of Homo. Why were air sacs lost in the human lineage? Several proposals have been made. Perhaps they were lost because humans switched to quieter forms of communication, or perhaps finer control over breathing patterns meant that humans no longer needed assistance from air sacs (Hewitt et al. 2002). However…
When humans have air sacs
We modern humans are not ordinarily supposed to have enlarged tracheal diverticula. In some people – as many as 15-30% of adults according to some studies – either one of the laryngeal ventricles is abnormally long, extending superiorly above the level of the thyroid cartilage at the top of the larynx (note that ‘abnormally long’ still means c. 5-15 mm). These enlarged ventricles are termed internal laryngocoeles: they’re internal because they don’t extend beyond the limits of the larynx. Because enlarged laryngeal ventricles are, as we’ve seen above, normal for other hominid species, it’s been suggested that big ventricles in humans might be atavistic.
Some long ventricles in some people reach – and even pierce – the thyrohyoid membrane right at the top of the larynx (normally only pierced by the internal laryngeal nerve and superior laryngeal artery), and thus become external laryngocoeles. Sometimes the laryngocoeles have a dumbbell shape and consist of both internal and external components; the ‘waisted’ portion in the middle being that part that squeezes through the thyrohyoid membrane (Giovanniello et al. 1970). The x-rays below show an external laryngocoele in a patient; from Giovanniello et al. (1970).
Enlarged laryngeal ventricles in humans might result from congenital deformity, but it’s more likely that they result from excessive build up of pressure in the glottis. Glass-blowers, people who play saxophones and other wind and brass instruments, and people who suffer from chronic coughing are therefore mostly the ones who develop these structures [diagram below showing internal and external laryngocoeles, from Giovanniello et al. (1970). When both internal and external laryngocoeles are present, the term 'mixed laryngocoele' is used... but this is redundant and unnecessary, given that external laryngocoeles only occur when internal ones are already present].
Due to their interference with the vocal cords, internal laryngocoeles produce chronic hoarseness, and can also create the impression of throat blockage and shortness of breath. External laryngocoeles, however, may not ordinarily cause any obvious negative effects other than creating an unsightly soft bulge on the side of the neck. This bulge can change size and shape as the owner performs the Valsalva manoeuvre (the process where you forcibly exhale without releasing the air from the mouth or nose). However, there are several cases of external laryngocoeles causing death following acute obstruction of the upper respiratory tract.
The really neat thing about laryngocoeles is that they demonstrate how diverticula can herniate surrounding structures and then sit in new positions, sometimes close to the skin and visible externally. If an animal that possessed these was provided with some sort of selective advantage (say, they assisted flotation, in enhancing the acoustics of calls, or were somehow attractive to mates or intimidating to rivals), you can imagine that they might become a fixed feature. Maybe this is how the inflatable nasal balloons of certain seals and other animals evolved.
Moving away from laryngocoeles for a moment, people have learnt that they can create pouch-like structures in their throats by keeping lead discs inside their pyriform sinuses, thereby enlarging the sinuses over time (the pyriform sinuses are yet another set of paired pockets, this time positioned on either side of the opening to the larynx). These resulting pouches – termed ganahs – were said by Guthrie (in Anon. 1927) to be used by Indian criminals “as a safe hiding place for coins or precious stones”.
Sasquatch and the Aquatic Ape Hypothesis
One last thing to say about primate air sacs. You might find it interesting that diverticula have been mentioned in a few ‘non-standard hypotheses’ on hominid diversity and evolution. As we’ll see in a later article, inflatable air sacs are present in some marine mammals, and probably play a buoyancy role in some pinnipeds. Unsurprisingly, proponents of the aquatic ape hypothesis (= AAH) have therefore suggested that air sacs might be something to do with the amphibious stage they imagine for hominids. As with other pieces of data used to support the AAH, the logic here doesn’t quite follow given that air sacs are biggest in primates that have nothing to do with water, nor is there any reason for thinking that the primates that have them use them on the (mostly rare) occasions when they wade or swim.
The possible presence of hypertrophied laryngeal pouches has also been discussed a few times in the literature on sasquatch (Krantz 1999, Meldrum 2006). If sasquatch is a non-human ape, the presence of enlarged air sacs would be expected. Furthermore, it’s been suggested that the loud vocalisations inferred by some to be created by sasquatches indicate the presence of giant, orangutan-like air sacs in this animal. Grover Krantz even considered the idea that the large, human-like breasts of ‘Patty’ – the subject of the 1967 Patterson-Gimlin film – might be partially inflated air sacs, but noted that this was more unlikely than the idea that they really are breasts (Krantz 1999) [Patty and her famous breasts shown in the adjacent image] [UPDATE: my comments inspired this article over on Cryptomundo].
And on that note… time to leave! Next: elephants with pouches.
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 apes and other primates, see…
- Bipedal orangs, gait of a dinosaur, and new-look Ichthyostega: exciting times in functional anatomy part I
- The Cultured Ape, and Attenborough on gorillas
- Zihlman’s ‘pygmy chimpanzee hypothesis’
- Encounters with gigantic orangutans
- The Yaounde Zoo mystery ape and the status of the Kooloo-Kamba
- Fame beckons at last for the Horton Plains slender loris
Refs – -
Alemseged, Z., Spoor, F., Kimbel, W. H., Bobe, R., Geraads, D., Reed, D. & Wynn. J. G. 2006. A juvenile early hominin skeleton from Dikika, Ethiopia. Nature 443, 296-301.
Anon. 1927. Pharyngeal and laryngeal pouches. The British Medical Journal Dec’ 3rd 1927, 1043.
Fitch, W. T. 2000. The evolution of speech: a comparative review. Trends in Cognitive Sciences 4, 258-267.
Giovanniello, J., Vincent Grieco, R. & Bartone, M. F. 1970. Laryncocele. American Journal of Roentgenology 108, 825-829.
Hewitt G, MacLarnon A, & Jones KE (2002). The functions of laryngeal air sacs in primates: a new hypothesis. Folia primatologica; international journal of primatology, 73 (2-3), 70-94 PMID: 12207055
Krantz, G. S. 1999. Bigfoot Sasquatch Evidence. Hancock House (Surrey, B.C. & Blaine, WA.)
Meldrum, J. 2006. Sasquatch: Legend Meets Science. Tom Doherty Associates (New York).
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) that aethiopicus-boisei belonged to Gorilla, and africanus-robustus to Pan, both lineages evolving in parallel (gracile>robust) when climates became cooler & drier c 2.2 Ma or so.” I don’t care, or mention, who came up with the idea first; Marc has been pushing it for years… since the mid-1990s at least.