Everybody knows that camels are weird. As you'll know if you've been keeping an eye on SV-POW! lately, we've recently been quite taken with their necks. But it's not just camel's necks that are weird. Here, we embark on another look at the sometimes bizarre pouches, pockets and sacs present in certain mammals, most of which are outgrowths of the respiratory system.
Relatively little known is that (some) camels possess an inflatable diverticulum on the palate, termed the dhula, dulaa, gulah, goola, qulla or pálu, and known technically as the vesica palatina or palatine diverticulum. It seems unique to the Dromedary Camelus dromedarius (where it's present in both adult males and females): people have looked for it in the Bactrian camel and Llama and have shown it to be absent [screen-captures above shows inflated dhula in an Australian dromedary, as seen in a memorable scene from BBC's Wild Down Under, © BBC].
As you might guess for such a weird-looking structure, the dhula is used in sexual display: it's inflated when the camel displays to conspecifics, hanging from the side of the mouth (usually the right side) for 25-35 cm. It looking like a grotesque, heavy bladder; Tecumseh Fitch (2006) described it as like a "large wet balloon". The exact mechanism behind its inflation is not well understood, but it's assumed that the camel forces air from the lungs into the dhula at will (Arnautovic & Abdul Magid 1974). Copious amounts of foamy saliva are produced during dhula inflation, and the animal may toss the head up and down, flopping the dhula about and throwing saliva all over the place.
Victorian authors who were unaware of the dhula's role in display speculated that it might help the camel to moisture its mouth with water or mucus, and hence "allay the feeling of thirst" (this quote comes from Richard Owen). The dhula is present in females, but is apparently never used.
The heavy cost of the dhula
In keeping with its role as an exaggerated organ that functions in display, the dhula can exact a heavy cost on its owner. Owning and using one can be dangerous, possibly fatal. While the dhula is normally retracted and folded up against the rest of the soft palate, it seems that its large size can interfere with airflow in the mouth: camels are ordinarily nose-breathers, but some male camels used in racing are sometimes observed to switch to mouth-breathing, and to then struggle to get enough air. Understandably, these camels perform relatively poorly in racing. In fact, it's said (Kuhad et al. 1998) that female camels are faster racers than males (20-30 seconds faster at 8 and 10-km distances), and it's been inferred that this is because their breathing doesn't ever become restricted.
In order to improve the racing efficiency of male camels, their dhulas are sometimes surgically removed in an operation termed a soft palatectomy. This isn't a difficult operation: the camel is restrained and tranquilised, the dhula is grasped with forceps and spread out to maximum extent. It's then cut away with surgical tools, and any large blood vessels (often present at the base of the dhula) are cauterised (Kuhad et al. 1998) [the photo below, from Kuhad et al. (1998), shows an excised dhula].
Because male camels often fight at about the same time as they are displaying the dhula, the organ is often damaged by the canine or other teeth of the opponent. I presume that severe damage might ruin it entirely, since a full puncture would prevent future inflation. These wounds can also become infected, leading to a swelling in the neck and resultant inability to swallow, laboured breathing and unusual neck posture (Kamal 2008). Catastrophic prolapse of the dhula has sometimes been reported, and the result is totally grotesque: imagine a foot-long, mangled, dangling organ, dripping with snot, mucus and blood and hanging heavily down well below the head, with a lumpy, red and purple viscous surface. Just such an image is included in Reese & Chawla (2001): I decided against using it here, but did plan to (email me if you want the pdf). Surgical removal of the dhula is recommended in such cases, and the animals soon recover.
Also on record are instances where camels have managed to swallow their own dhulas. Semieka (2010) described a case where a 6-year-old malnourished camel was not eating, was salivating excessively, and was holding the neck in an unusual extended position. Radiography revealed a rounded structure lodged in the throat that proved to be a paralysed and wounded dhula that was completely blocking the oesophagus. Again, this was surgically removed and the camel rapidly returned to health. Other dhula-related problems have also been described. I think I might have said this before, but there's a large and very rich literature on camel pathology... and on pathologies caused by camels. I'm finding the veterinary literature really very interesting these days.
Pharyngeal, tympanic and laryngeal pouches of the Mongolian gazelle
A superficially similar structure to the dhula - the palatinal pharyngeal pouch (PPP) - is present in the Mongolian gazelle or Zeren Procapra gutturosa [shown below, from here... though that lump in the throat is not the PPP: read on]. At rest, the pouch hangs down from the soft palate, lying between the root of the tongue and the epiglottis, between the two halves of the hyoid apparatus (Frey & Gebler 2003). Because much of Zeren courtship and mating behaviour occurs at night, observations are few, and it remains uncertain whether these gazelles extend their PPPs from out of their mouths. While a role in courtship looks likely, the precise role of the Mongolian gazelle's PPP remains undetermined.
The larynx is descended relative to that of other bovids, perhaps because it had to make space for the pharyngeal pouch. As we saw in the September article on lion and tiger anatomy, big cats, koalas, deer and some bats join humans in having a larynx that is set low within the throat compared to the normal mammalian condition.
However, the gazelle goes one better in also possessing paired, tympanic pharyngeal pouches. These thin-walled sacs are located on the dorsal wall of the pharynx, close to the tympanic bullae (ventrally convex bony structures that surround the inner ear). And it also possesses enlarged, paired laryngeal ventricles (if you need a reminder on the terminology, do go check the first article in the pouches, pockets and sacs series). The presence of enlarged ventricles is totally atypical for bovids. The gazelle's ventricles are also unusual in being two-chambered, and in that their connection to the rest of the larynx is lateral (rather than medial) to the top of the laryngeal cartilage (Frey & Gebler 2003). In their un-inflated state, each ventricle has a volume of 30 cubic cm. As with the palatinal pharyngeal pouch, a precise role for the enlarged ventricles has yet to be demonstrated, but it has been inferred that - like the enlarged ventricles of some primates - they act as resonating chambers used during vocalisation [image below - from Frey & Gebler (2003) - shows internal cranial anatomy of a male Mongolian gazelle. The bits we're interested in are Burs pal. phar. (palatinal pharyngeal pouch) and Burs. tymp. phar. (tympanic pharyngeal pouch). The laryngeal ventricles are adjacent to the fibroelastic pad of the vocal fold (fibrelast. pad)].
The complicated, enlarged larynx - which forms a prominent bulge in the male Mongolian gazelle's neck - is proportionally huge, weighing about 500-600 g (this, in an animal with a total weight of 31.5 kg). The structure is sexually dimorphic, being twice as big in males as it is in females (despite the fact that males are only 1.3 times as big as females in overall body size) (Frey & Riede 2003).
With a large palatinal pharyngeal pouch, paired tympanic pharyngeal pouches, paired, internally chambered, enlarged laryngeal ventricles, and a descended larynx, the Mongolian gazelle is - I think you'll agree - a pretty remarkable artiodactyl. In the next article in this series, we'll be looking at horses, tapirs and rhinos.
For the previous articles 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?
- Pouches, pockets and sacs in the heads, necks and chests of mammals, part III: baleen whales
- Pouches, pockets and sacs in the heads, necks and chests of mammals, part IV: reindeer and a whole slew of others
And for previous Tet Zoo articles on artiodactyls, see...
- Dammit, and I sooo loved the 'necks for sex' hypothesis
- Welcome.... to the world of sheep
- Return.... to the world of sheep
- Giant killer pigs from hell
- Stuffed megamammal week, day 1: Khama
- Stuffed megamammal week, day 2: Eland
- Stuffed megamammal week, day 3: Okapi
- A 'consensus cladogram' for artiodactyls
- Pronghorn, "designed by committee" (pronghorns part I)
- Release the fossil pronghorns!! (pronghorns part II)
Refs - -
ArnautoviÄ I, & Abdel Magid AM (1974). Anatomy and mechanism of distension of the dulaa of the one-humped camel. Acta anatomica, 88 (1), 115-24 PMID: 4838369
Fitch, W. T. 2006. Production of vocalizations in mammals. In Brown, K. (ed) Encyclopedia of Language and Linguistics. Brown (Oxford), pp. 115-121.
Frey, R. & Gebler, A. 2003. The highly specialized vocal tract of the male Mongolian gazelle (Procapra gutturosa Pallas, 1777 - Mammalia, Bovidae). Journal of Anatomy 203, 451-471.
- . & Riede, T. 2003. Sexual dimorphism of the larynx of the Mongolian gazelle (Procapra gutturosa Pallas, 1777) (Mammalia, Artiodactyla, Bovidae). Zoologischer Anzeiger - A Journal of Comparative Zoology 242, 33-62.
Kamal, A. M. 2008. Some biochemical, hematological and clinical studies of selected ruminal and blood constituents in camels affected by various diseases. Research Journal of Veterinary Sciences 1, 16-27.
Kuhad, K. S., Tinson, A. H., Rehman, A., Rajesh & Almasri, J. 1998. New technique for soft palatectomy in One-humped male racing camels. Proceedings of the Third Annual Meeting for Animal Production Under Arid Conditions 2, 145-153.
Reese, J. F. & Chawla, S. K. 2001. Prolapse of the soft palate in a male Arabian
camel (Camelus dromidarius [sic]). The Veterinary Record 149, 656-657.
Semieka, M. A. 2010. Radiography of unusual foreign body in ruminants. Veterinary World 3, 473-475.
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Has any hypothesis been offered for the (apparent) absence of this structure in the Bactrian camel? Climatic factors would seem like an insufficient explanation, given that a 'dhula' is also present in the Mongolian gazelle (which has a natural distribution and habitat preferences roughly similar to those of the wild Bactrian camel).
Yikes!
Doesn't look so much like a bladder to me, in that B&W pic. Something close but more superficial?
Isn't there evidence that Pelecimimus had a throat pouch as well? thus the name.
Doesn't look so much like a bladder to me, in that B&W pic.
bladder: a membranous sac or organ serving as a receptacle for a fluid or air.
Something close but more superficial?
???
Cameron, John is being rude and employing phallus-based humour :)
Crap! I've got to get a better radar for this sort of thing.
Dartian wrote:
Why should there be an explanation? If the thing's unique to the dromedary, it's likely an innovation in than particular lineage.
Nice Pictures
Such a strange structure to develop. There've gotta be easier ways to employ courtship display. Look at those goddamn humps, you idiot camels! LOL. And yes, the B&W picture makes it look like the camel has bitten off its rival's sexual organ. Or perhaps its own, accidentally.
It could also be a juvenile graboid.
.... or a Mongolian death worm (but, dammit, dromedaries don't live in Mongolia).
...or Arabian sandtrout (but sandworms don't come from Arabia either).
As gung-ho as I usually am about these things, I'm honestly quite glad you decided against using the dhula prolapse picture in the article.
Andreas:
I was asking Darren - who knows the relevant literature better than I do - if someone has suggested an explanation (and the dhula, like any costly structure, practically begs for an evolutionary explanation). The dromedary and the Bactrian camel are very closely related; why, then, does the other species possess a dhula when the other does not? Is there some crucial difference in the respective biology of the extant Camelus species?
Or, it could have been present in the LCA of the extant Camelus species and subsequently lost in the bactrianus lineage. Judging by the available data, that alternative scenario does not violate the principle of parsimony to the extent that it could be dismissed.
It's, of course, not impossible or even very implausible that it's been lost in bactrianus. Essentially we'd be locking at two "evolutionary events" rather than one.
Nevertheless, it seems to me odd to start looking for an explanation in the absence of any good reason to assume there's anything to explain in the first place.
If it's purely a signalling organ, functioning only in sexual selection, then there's no surprise about it being restricted to a single lineage.
I wonder if there is any indication of a dhula in the embryonic development in the Bactrian.
And might the dhula be an odd example of the Handicap principle?
Given my palaeontological bent, one of the first things I thought about when considering the dhula is whether it might have been present in various fossil camelids - after all, the thought of a scene where a group of Gigantocamelus are displaying their dhulas and flopping frothy saliva all over the place is quite exciting :) However, it is specifically stated in the literature that the structure is unique to the Dromedary and that there is no indication of its presence in the Bactrian camel: e.g., "It is not seen in any other mammal, even close relatives like the Bactrian camel or South American Llama" (Kuhad et al. (1998), "This structure is unique to Arabian camels" (Reece & Chawla 2001). This is perhaps surprising, since the two Camelus species are really similar - more similar than you might think, since the Dromedary actually has two humps, it's just that the anterior one is small (though I see that this has just been contested by Kinne et al. (2010)). But, as some commenters have said above, the presence of a weird sexually-selected display structure is consistent with its uniqueness to one species and absence in a sister-species.
But then I read this: it specifically refers to the presence of a dhula in Bactrian camels!
It's (so far) the only place I've seen this, and I'd like confirmation. There are quite a few papers on the soft-tissue cranial anatomy of the Bactrian camel (mostly on nervous supply and the anatomy of the nasal cavity and sinuses), but I've yet to see one that discusses the palate or its morphogenesis in detail. Even without the possible presence of a dhula, Bactrian camels already do weird displays: the males soak their long tails with urine and perform a distinctive tail-flapping display; they also squat and make roaring noises.
Refs - -
Kinne, J., Wani, N. A., Wernery, U., Peters, J. & Knospe, C. 2010. Is there a two-humped stage in the embryonic development of the Dromedary? Anatomia, Histologia, Embryologia 39, 479â480.
Kuhad, K. S., Tinson, A. H., Rehman, A., Rajesh & Almasri, J. 1998. New technique for soft palatectomy in One-humped male racing camels. Proceedings of the Third Annual Meeting for Animal Production Under Arid Conditions 2, 145-153.
Reese, J. F. & Chawla, S. K. 2001. Prolapse of the soft palate in a male Arabian camel (Camelus dromidarius [sic]). The Veterinary Record 149, 656-657.
AnJaCo:
Perhaps, but if sexual display is the dhula's only function one would expect its presence to be restricted just to the members of the other sex. The 'classic' version of the Handicap principle hypothesis alone doesn't quite explain why female dromedaries also possess a dhula.
Darren, thanks for the detailed response; much appreciated.
Fair enough. But then again, many similar claims that have been made in the literature have later turned out to be inaccurate (*cough* 'the giraffe can't swim' *cough*); thus, mild scepticism of that claim is not entirely unwarranted, IMO.
Interesting!
The dhula as a vestige of a split upper lip, involved in salivation, and secondarily as a male display device (advertizing ability to salivate thus eat very dry herbage) sounds correct. It and the external nasal air sac of some seals seem unrelated to a buoyancy function more common in animals with internal air sacs. Some fish produce sounds that are amplified in their gas sac, but I don't think anyone has suggested that 'vocalization' is the primary function of the gas sac. Looking forward to the tapir post!
Ah, I had missed this. Absent some sort of ineluctable developmental constraint (of the type that gives male mammals vestigial nipples, e.g.), a purely sexual-selection hypothesis would predict it to be expressed only in males.
An ineluctable developmental constraint, then?
The original function of that sac is to breathe air. It's the swim bladder, and swim bladders are derived lungs.
@ 21 Yes DM, originally a pocket from the gut tissue, but today in most bony fish it is primarily a buoyancy device.
I'm sorry, but the picture of a dissected dhula makes my stomach churn :(
BTW - any good overview of history of wild Dromedaries in their native range? They seem to be almost unknown, even more controversies than about wild horse and Aurochsen.