Back to the series on pouches, pockets and sacs (for previous articles see links below). The previous article finished by looking at the guttural pouches present in the Mongolian gazelle Procapra gutturosa. This links us nicely to the select group of mammals – perissodactyls, hyraxes, bats and rodents – that possess air-filled structures (called guttural pouches) located in the upper respiratory tract, pressed up close to the tympanic region at the back of the skull. In this article, I’m only going to deal with perissodactyls: the other groups can wait to later.
Guttural pouches are best known in the Horse Equus caballus where they contain 300-500 ml of air (accounting for up to 4% of the head’s entire volume) and consist of both lateral and medial compartments. The size and shape of the pouches changes as the animal contracts and relaxes surrounding musculature. The medial guttural pouch compartment is virtually wrapped around the internal carotid artery; this close proximity suggests that the pouches might play a role in selective brain-cooling. In other words, they might help to cool blood running from the hot body core, up the internal carotid and past the brain. Many mammals – including bovids, deer, dogs and cats – keep brain temperature low by virtue of a carotid rete (a heat-exchange network where carotid arterial blood is cooled by venous blood drained from the nasal region), but horses don’t have this [the diagram below, showing the guttural pouches and other details of horse cranial anatomy, is from the Forever Horses blog. The guttural pouches are the cream-coloured areas at the back of the skull].
In a brilliant case of logical deduction preceding discovery, Keith Baptise (and colleagues) suggested a cooling role for the guttural pouches of horses as early as 1993 (e.g., Baptiste et al. 1993), and were later able to demonstrate exactly this somewhat later (Baptise et al. 2000). However, other possible functions have been suggested over the years, including an immunological one and a role in swallowing. So far as I can tell, these are more speculative.
Having mentioned the comparatively large size of the pouches in the domestic horse, note that they’re rather smaller in Przewalski’s horse. In fact, domestic horses bred for racing or use as pack animals have the biggest pouches, suggesting that selective breeding has encouraged an increase in the size of the pouches concomitant with an increase in exercise and activity.
The literature reporting, describing and interpreting horse guttural pouches is fairly substantial. Donkeys definitely have them too, and their presence in tapirs was demonstrated during the 1850s. A result of this distribution is that it’s sometimes been assumed that they’re ubiquitous in perissodactyls, and hence also present in rhinos. However, Endo et al. (1998) showed that guttural pouches were absent in the white rhinos Ceratotherium and their absence was also later demonstrated in a juvenile Indian rhino Rhinoceros indicus (Endo et al. 2009). Some sources do state that they are present in other rhino species, however, and in these species we await modern study that confirms or refutes their possible presence.
There are a few other weird pockets and cavities present in the heads of perissodactyls. Horses have paired, cone-shaped, fur-lined, blind recesses – the false nostrils (properly called nasal diverticula) – that open dorsal to the true nostrils and extend posteriorly for a short distance on the upper surface of the snout [the extent of the false nostril is shown below, in a diagram from Witmer et al. (1999). dn = nasal diverticulum, in' = position of incisura nasoincisiva, pa' = plica alaris, with lamina of alar carilage dorsal to it, cac' = lateral ala of nostril overlying cornu of cartilago alaris].
It’s been thought that both tapirs and rhinos possess the same structures, and that these are particularly well developed in tapirs. However, the supposed ‘false nostrils’ of tapirs are completely different to those of horses: the tapir structures are not external, cutaneous pouches “but rather… intracapsular, mucocartilaginous tube[s] that maintain communication with the nasal cavity at both ends” (Witmer et al. 1999, p. 263). Exactly what’s going on with the rhino nostril cavity isn’t entirely clear, as detailed descriptions of rhino noses don’t seem to exist (though I confess that I haven’t seen Bordoloi & Kalita (1996)). Of incidental interest to this section of the article (but of relevance to this series of articles as a whole) is that all species of living rhino possess an epipharyngeal diverticulum (a pouch-like recess) on the dorsal wall of the pharynx (Cave 1973, 1974a, b). We’ll return to epipharyngeal diverticula in a later article.
But to return to false nostrils… no obvious function has ever been discovered for these structures. Because their floors flutter during exhalation, I wonder if they might play a role in amplifying or otherwise enhancing the loud snorting noises that horses use in communication.
Preorbital cavities in horses, rhinos and tapirs
I think – rightly or not – that false nostrils are weird. But they’re not the only weird, poorly understood ‘pockets’ known to be present in horse heads. A number of fossil horses – in particular members of the equine clade Hipparionini – possess a roughly oval bony recess on the side of the skull, located about half-way between the bony nostril and eye socket. It’s typically termed the dorsal preorbital fossa (maxillary fossa is also sometimes used) and is highly variable in size and shape [skull of Hipparion gracile with obvious preorbital fossa shown here; image by Ghedo, from wikipedia]. In some specimens of some taxa (Cormohipparion for one), its posterior part excavates parts of the nasal, lacrimal and maxillary bones. This structure superficially resembles the antorbital cavity you might recognise from the skulls of dinosaurs and other archosaurs, so here is obvious evidence that horses are not mammals, but actually archosaurs. I’m joking: regular readers will recognise one-character reclassifications of this sort as characteristic of the Mihalda School.
Preorbital fossae are not unique to horses among perissodactyls: they’re also present in various fossil rhinos, and in some living and fossil tapirs. As we’ll see, however, these various structures are highly distinct, non-homologous and probably associated with very different bits of soft-tissue biology.
Among rhinos, preorbital fossae are present in the amynodontids Rostriamynodon and Amynodon, and in Forstercooperia, Juxia and Paraceratherium. The last three taxa have often been grouped together in a small group termed Indricotheriinae, itself ‘traditionally’ contained within the more inclusive Hyracodontidae (e.g., Prothero et al. 1986, Prothero 1998); the presence of a preorbital fossa has been regarded as an indricotheriine synapomorphy. However, the preorbital fossae of these various ‘indricotheriines’ aren’t that similar after all. The structures in Juxia are shallow, positioned high up on the sides of the maxillae, and not all that different from the fossae seen in various tapiroids [the adjacent Juxia skull photo shown here is by Captmondo and is from wikipedia], those in Forstercooperia are larger and partially roofed by the nasals (an amnynodontid-like condition), while those in Paraceratherium [skull shown below: by Ryan Somma, from wikipedia] are very dorsal in position and located immediately posterior to the enormous narial incision.
Holbrook (1999, 2001) included data from these characters and many others and didn’t support indricotheriine monophyly, nor did he find these taxa to be within Hyracodontidae. Instead, Paraceratherium and Forstercooperia were successive sister-taxa to an amnyodontid + rhinocerotid + Uintaceras clade. While the preorbital fossae present in the taxa discussed here look rather distinct, the peculiar thing is that – under Holbrook’s (2001) topology – it looks most likely that fossae evolved once in rhinos (early on in the clade that includes amynodontids, Paraceratherium and rhinocerotids), but were then lost a few times independently.
A slightly different structure – a semi-circular depression present closer to the eye socket – is present in the tapiroids Helaletes, Colodon, Plesiocolopirus, Protapirus and Tapirus (Holbrook 1999, 2001) [in the Tapirus skull shown here, the structure we're interested in is the rounded concavity directly above the eye socket and at the back of the deep nasal cavity. The nasal bones ordinarily roof the whole of the nasal cavity, but are very obviously well retracted in tapirs]. However, while this concavity is sometimes called a preorbital fossa, it’s very different from the same-named structures of horses and rhinos and could well have a separate origin.
Facial glands? Elaborate facial muscles? What gives??
So what were, and are, these bony ‘pockets’ for? Did/do they house soft structures of some sort? Several roles for the fossae present in fossil horses have been suggested. One is that they housed inflatable diverticula that were used in somehow enhancing the volume or resonance of vocalisations (Gregory 1920, MacFadden 1984). Another is that they housed glands like the superficially similar preorbital pockets present in deer (Meladze 1967) [and, no, I don't think hippariorine horses had inflatable sacs on the sides of their faces - as shown below - but I wanted to know what a horse would look like with them].
Yet another hypothesis is that they were the attachment sites for lip and/or nasal muscles that allowed the lips and nasal region to be flared in a manner more elaborate than that seen in any living equids (MacFadden 1994). Possible links with feeding behaviour have been mentioned on occasion: quite how facial fossae relate to ecology has never been explained, but Zhegallo (1978) suggested that the fossae might be correlated with a complex lip and jaw musculature that was itself linked to complicated jaw movements used in browsing.
The structures termed preorbital fossae in tapirs house cartilaginous structures associated with the proboscis, and are better termed meatal diverticulum fossae (Witmer et al. 1999). Similar structures in some fossil tapirs almost certainly served the same role (Colbert 2005), but this doesn’t help us in interpreting the preorbital fossae of fossil horses and rhinos as these fossae – particularly those of horses – are in a very different location and don’t seem to be associated with nasal cartilages.
For now, the story behind the evolution of preorbital fossae in horses and other perissodactyls remains enigmatic, and we await a key discovery (perhaps a beautifully preserved fossil with some preserved soft tissue). Anyway… few (if any) previous sources have combined discussions of guttural pouches, false nostrils and preorbital fossae: I hope this review has been interesting, and perhaps that it proves useful in future.
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
- Pouches, pockets and sacs in the heads, necks and chests of mammals, part V: palatal (and other) pouches in camels and gazelles
For previous Tet Zoo articles on perissodactyls, see…
- War rhinos
- Tet Zoo picture of the day # 3 (on Elasmotherium)
- Multiple new species of large, living mammal (part I) (discusses alleged new dwarf Amazonian tapir)
- Chinese black rhinos and deinotheres, giant sengis, and yet more new lemurs
- How did the White rhino get its name? Not how you think (even if you’re very clever)
- Snow White and the six perissodactyls
- Thunder beasts in pictures
- Thunder beasts of New York
- Stuffed megamammal week, day 4: Sumatran rhino
- Because you can never have too many tapirs
- The biggest tapir
- A new species of modern-day rhinoceros
Refs – -
Baptiste, K. E., Grandage, J. & Johnson, K. 1993. Is the guttural pouch of the horse a brain-cooling device? Journal of Anatomy 183, 174.
Baptiste KE, Naylor JM, Bailey J, Barber EM, Post K, & Thornhill J (2000). A function for guttural pouches in the horse. Nature, 403 (6768), 382-3 PMID: 10667779
Bordoloi, C. C. & Kalita, H. C. 1996. Gross anatomical studies of nasal cavity of rhino calf (Rhinocerous unicornis). Indian Veterinary Journal 73, 470-472.
Cave, A. J. 1973. The bursa epipharyngea in the Sumatran rinoceros (Didermocerus sumatrensis). Mammalia 37, 654-657.
- . 1974a. The epipharyngeal bursa in the Rhinocerotidae. Journal of Zoology 172, 133-145.
- . 1974b. Bilocular epipharyngeal bursa in Diceros bicornis. Journal of Zoology 174, 159-169.
Colbert, M. W. 2005. The facial skeleton of the Early Oligocene Colodon (Perissodactyla, Tapiroidea). Palaeontologia Electronica 8 (1); 12A:27p; http://palaeo-electronica.org/paleo/2005_1/colbert12/issue1_05.htm
Endo, H., Manglai, Fujisawa, M., Kurohmaru, M. and Hayashi, Y. 1998. The guttural pouch is not present in the white rhinoceros (Ceratotherium simum); morphology of the Eustachian tube and nasopharynx. Anatomia, Histologia and Embryologia 27, 327-330.
- ., Taru, H., Hayashida, A., Kimura, J., Itou, T., Koie, H. & Sakai, T. 2009. Absence of the guttural pouch in a newborn Indian rhinoceros demonstrated by three-dimensional image observations. Mammal Study 34, 7-11.
Gregory, W. K. 1920. Studies in comparative myology and osteology, no. V: On the anatomy of the preorbital fossae of Equidae and other ungulates. Bulletin of the American Museum of Natural History 42, 265-284.
Holbrook, L. T. 1999. The phylogeny and classification of tapiromorph perissodactyls. Cladistics 15, 331-350.
- . 2001. Comparative osteology of early Tertiary tapiromorphs (Mammalia, Perissodactyla). Zoological Journal of the Linnean Society 132, 1-54.
MacFadden, B. J. 1984. Astrohippus and Dinohippus from the Yepómera Local Fauna (Hemphillian, Mexico) and implications for the phylogeny of one-toed horses. Journal of Vertebrate Paleontology 4, 273-283.
- . 1994. Fossil Horses: Systematics, Paleobiology, and Evolution of the Family Equidae. Cambridge University Press, Cambridge.
Meladze, G. K. 1967. Gipparionovaja fauna Arkneti I Bazaleti. Izdatel’stvo “Metsnierebl” 1-168.
Prothero, D. R. 1998. Hyracodontidae. In Janis, C. M., Scott, K. M. & Jacobs, L. L. (eds) Evolution of Tertiary Mammals of North America. Volume 1: Terrestrial Carnivores, Ungulates, and Ungulatelike Mammals. Cambridge University Press, pp. 589-594.
- ., Manning, E. & Hanson, C. B. 1986. The phylogeny of the Rhinoceratoidea (Mammalia, Perissodactyla). Zoological Journal of the Linnean Society 87, 341-366.
Witmer, L. M., Sampson, S. D. & Solounias, N. 1999. The proboscis of tapirs (Mammalia: Perissodactyla): a case study in novel narial anatomy. Journal of Zoology 249, 249-267.
Zhegallo, V. I. 1978. Gippariony Tsentral’noj Azii. Sovmestnaya Sovetsko-Mongol’skaya Paleontologicheskaya Ekspiditsiya, Trudy 7, 1-152.