Over the past
several months months and months I've been trying to complete a series of articles on the various sac- and pocket-like head and neck structures that have evolved in such diverse mammals as apes, horses, camels and baleen whales (links to the previous articles in the series are provided below). In an effort to get the series finished, here's the next part of the series. This time, we focus on rodents, rabbits and hyraxes. Yeah, just like it says above, in the title.
It's well known that pneumatisation of the skull bones is widespread in mammals: sinuses in the nasal region, frontal region and around the middle ear are widespread across phylogeny (though the same set of sinuses are not present in all groups, read on). I haven't been covering such sinuses in this series, as I've been more interested in the peculiar (often) inflatable structures that are altogether less familiar and rather weirder (check out the preceding articles if you haven't already). Nevertheless, while I'm here it's worth saying some
very brief things about cranial sinuses.
Frontal sinuses in bovids were recently reviewed in comprehensive depth by Farke (2010) (that's Andy Farke of The Open Source Paleontologist, ceratopsian worker extraordinaire). The structures range from small, isolated recesses present within each frontal bone to relatively enormous, ramifying structures that, in cases, invade the horncores and parietal bones all the way to the occiput [one of Andy's many beautiful figures - from Farke (2010) - is shown here]. However, the sinuses have been lost or substantially reduced within several lineages.
Interestingly, there's no direct correlation between elaboration or size of the frontal sinuses and a head-butting habit (to take one example: duikers, which butt heads, lack sinuses entirely). In a previous study on the role of the frontal sinuses in goat skulls, Farke (2008) showed that the sinuses didn't prove advantageous in absorbing stresses of the sort incurred during head-butting. Another beautiful hypothesis (= that enlarged frontal sinuses evolved under selection for use in shock absorption) slain by an ugly fact, as they say.
Maxillary sinuses: how mammals try their best to mimic archosaurs
Thanks in part to studies like this, the mere existence of frontal sinuses is relatively well known. But I don't think you can say the same for another structure - the maxillary sinus - despite the fact that it's widespread across Mammalia. Actually, when I think about it, that might not be true, since enough of us humans suffer maxillary sinus infections, blockages and so on that we often have to get our maxillary sinuses looked at or treated. Maxillary sinuses are, together with the sinuses in the frontal, ethmoid and sphenoid bones, part of the array of structures lumped together as the paranasal sinuses [adjacent x-ray of human skull, showing paranasal sinuses, by Mnolf, from wikipedia]. Ethmoidal sinuses are typically said to be unique to apes (including humans) (e.g., Reznik 1990). In fact, they're definitely present elsewhere (e.g., in muroid rodents: Phillips et al. (2009)).
As with some of the other structures we've looked at in this series (in particular the preorbital fossae of horses), mammalian maxillary sinuses are interesting if you're familiar with dinosaurs and other archosaurs, since they 'mimic' the antorbital fossae of archosaurs in approximate position and shape (unlike archosaur fossae, the sinuses are not, of course, visible from the outside of the skull). Check out this series of x-rays (from Koppe et al. 2000), showing growth of the maxillary sinus in domestic pigs (scale bars = 2 cm)...
Your maxillary sinus isn't all that different, but never becomes as large. We (mostly) keep the sinus retained within the maxilla, whereas pigs (and other artiodactyls) 'allow' the sinus to invade parts of the zygomatic region, the lacrimal and various other parts of the skull.
Actually, at least some apes - Sivapithecus is a classic example - developed enlarged maxillary sinuses too, with that of Sivapithecus invading much of the zygomatic arch (Ward & Brown 1986). As with so many pneumatic structures, any biological 'function' has yet to be conclusively determined for the maxillary sinus, and it might just be a void that develops in an area where skull bones fail to ossify (for whatever reason). These days Larry Witmer is (quite appropriately) credited for proposing that sinuses might be the functionless result of opportunistic pneumatisation that occurs, well, just because it can (Witmer 1997), but I see that the same hypothesis was mooted in the 1940s and 50s by the likes of Franz Weidenreich (1941) and Tilly Edinger (1950).
The enormous zygomatic chambers of the Paca
Having mentioned pneumatic invasion of the zygomatic region, a massively inflated zygoma is present in the Paca Cuniculus paca [adjacent Paca photo by Hans Hillewaert, from wikipedia]. Pacas are large, mostly South and Central American* caviomorph rodents, notable for large size (up to 10 kg), an inflated look to the head and a reddish coat with longitudinal rows of white spots. The Paca was formerly known as Agouti paca, a name that incites confusion with the agoutis, a group of caviomorphs grouped together in the genus Dasyprocta. However, Cuniculus Brisson, 1762 has priority over Agouti LacÃ©pÃ¨de, 1799.
* The species also occurs in southern Mexico, Cuba and the Lesser Antilles. It's sometimes called the Lowland paca in order to distinguish it from the Mountain paca Cuniculus taczanowskii. Marc van Roosmalen has claimed to have a third species but this is looking doubtful.
Anyway, the cheek region of the paca skull has a grotesquely swollen appearance, with both the jugal and maxilla enlarged outwards and downwards and housing two enlarged maxillary chambers (as in, two on each side of the skull) [adjacent Paca skull image from PÃ©rez (1992); see also the photo at very top]. Because the ventral part of the structure is narrow from side to side, the whole ensemble is sometimes called the zygomatic plate. Within the plate, the lingual chamber is connected via an aperture to the oral cavity and so has sometimes been called a 'cheek pouch' (Howell 1940). It clearly isn't homologous to the integumentary structures normally termed cheek pouches in rodents. The external texture of the zygomatic place is often gnarly and roughened and some sources describe the skull as "reptilian" or having an "armour-plated" appearance (e.g., Hanney 1975).
Is it known why pacas have such massive pneumatic chambers in the cheek region?
One suggestion is that the chambers amplify the noise of teeth being ground together. Another is that the animals push air into the lingual chamber and use it to make a 'rumbling' noise that's amplified by the more labial chamber (Hershkovitz 1955). Regardless of exactly what happens, it seems agreed that the chambers serve an acoustic role: like the air pouches and inflatable bony bullae of apes, howler monkeys and some other primates, they seem to amplify noises and therefore serve a sociosexual role.
In view of this, it seems logical that there are claims of sexual dimorphism; it's been said that male pacas have the biggest chambers. However, Nelson & Shump (1978) analysed growth changes in paca and didn't report any sexual variation in the skull. They did find, however, that the zygomatic region exhibited marked allometric increase in length and width, with the biggest-headed individuals having zygomatic plates that were proportionally much larger than those of smaller-headed individuals. The structures increase rapidly in size somewhere during sexual maturity.
Similar pneumatic skull chambers are said to be present in the peculiar African Maned rat or Crested rat Lophiomys imhausi (PÃ©rez 1992) and this species is also said to have a skull that looks "armour-plated" (Hanney 1975). Lophiomys is not a caviomorph of course, it's a muroid, so any similarities it has in skull morphology with the paca are very much convergent [adjacent photo by Kevin Deacon, from wikipedia]. Unfortunately there doesn't seem to be much information available on its skull anatomy. Harking back to the discussion above of paranasal sinuses, guinea-pigs (members of Caviomorpha of course) lack an ethmoidal sinus, in contrast to rats and mice (Phillips et al. 2009). I'm not sure whether guinea-pigs are unusual in lacking ethmoidal sinuses, or whether rats and mice are unusual in possessing them.
At least some lagomorphs also possess peculiar air-filled skull features. Rabbits have paranasal sinuses of the sort seen widely in mammals, but they also have an additional air-filled space within their nasal region: it's actually enclosed within the nasoturbinate (a dorsally located midline bone that occupies part of the nasal cavity: it arises from the nasal, and is located above the maxilloturbinates and ethmoturbinates) (Kelemen 1955, Reznik 1990).
Long-time readers who recall my article on the weirdness of rabbits (included as Chapter 31 of Tetrapod Zoology Book One: shown above) - in which I discussed several old ideas linking lagomorphs to marsupials - will be pleased to know that this structure is termed the marsupium. So, rabbits have a marsupium: FACT. So far as I can tell from the literature, this structure is unique to rabbits.
Bony jaw pockets in hyraxes
In a previous article in this series I mentioned hyraxes. These fascinating little Afro-Arabian herbivores exhibit a variety of pneumatic cranial structures [Heterohyrax brucei shown here, from wikipedia].
Guttural pouches (air-filled sacs located in the upper respiratory tract, close to the tympanic region at the back of the skull) are present in the living hyrax species and recall the similar structures seen elsewhere in horses. In horses, a role in cooling the internal carotid artery has been supported; maybe the guttural pouches of hyraxes do the same job, but (as yet) this hasn't been investigated (so far as I can tell: say if you know otherwise!).
In addition, many fossil hyraxes belonging to the extinct group Pliohyracidae possess a pneumatic chamber within the dentary bone of the lower jaw. Termed the internal mandibular fenestra (or IMF), this structure is absent in some taxa (like Saghatherium, Selenohyrax and Antilohyrax), sexually dimorphic in some (like Thyrohyrax and Pachyhyrax) (apparently being limited to males), but present in both sexes of others (like Bunohyrax and at least one species of Megalohyrax). In the Miocene Kenyan hyrax Parapliohyrax, the IMF is connected to an external mandibular fenestra on the labial (= outside) surface of the lower jaw, though whether this is sexually dimorphic as well is not yet known. By the way, I've been planning to cover fossil hyraxes properly for ages. Sigh, one day...
Anyway, is it possible to work out what these structures were for? As reviewed by De Blieux et al. (2006), several suggestions have been made: that the IMF housed part of Meckel's cartilage, that it anchored a muscle slip, that it contained an enlarged salivary gland, or that it housed an air sac which acted as a vocal resonator.
In extant hyraxes, some of the salivary glands are in about the right place for the IMF, but if the IMF really did house such a gland, we would expect to see some sort of distinctive texture on the bone (we don't). Furthermore, it seems pretty radical for a gland to be enclosed within bone, and just why would fossil hyraxes need such bizarrely modified salivary glands anyway? And why the sexual dimorphism in saliva production? (As Dr Vector once said on this exact same issue: "[T]here's no obvious reason why one sex would need a lot more saliva than the other. (Yeah, I know how that sounds. If I can leave it alone, so can you)"). The other proposals also don't withstand scrutiny.
The vocal resonator hypothesis is most likely for several reasons. Firstly, the evolution of air sacs involved in vocalisation have a clear precedent elsewhere in Mammalia (see the discussion of pacas given above, and the previous discussion of apes, howler monkeys and so on). Secondly, the anatomy of the hyrax IMF (in particular the smooth walls) is consistent with invasion by an air sac and not with the other hypothesized roles. Thirdly, extant hyraxes are vocal animals that produce loud, repetitive calls (especially during the breeding season). The evolution of structures that would allow elaborate and/or louder vocalisations would therefore seem theoretically 'acceptable' within fossil members of the group. And fourthly, the IMF is located close to the posteroventral 'corner' of the mandible and hence in close proximity to the original position of the larynx. As we've seen, the vocal sacs and other structures associated with loud vocalisations in mammals have most frequently evolved as outgrowths of the larynx. Ergo, identification of the IMF as an extension of the vocal apparatus looks pretty good.
My aim here was to finish the series. I failed... there is more to do. Anyway, for the previous parts in the 'pouches, pockets and sacs' series, please 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
- Pouches, pockets and sacs in the heads, necks and chests of mammals, part VI: guttural pouches, false nostrils and preorbital fossae in horses, tapirs and rhinos
And for more on various of the animals mentioned or discussed in this article, see...
- Multiple new species of large, living mammal (part II) (mentions pacas)
- Duiker, rhymes with biker
- Giant furry pets of the Incas (mentions pacas)
Refs - -
DE BLIEUX, D., BAUMRIND, M., SIMONS, E., CHATRATH, P., MEYER, G., & ATTIA, Y. (2006). SEXUAL DIMORPHISM OF THE INTERNAL MANDIBULAR CHAMBER IN FAYUM PLIOHYRACIDAE (MAMMALIA) Journal of Vertebrate Paleontology, 26 (1), 160-169 DOI: 10.1671/0272-4634(2006)26[160:SDOTIM]2.0.CO;2
Edinger T. 1950. Frontal sinus evolution (particularly in the Equidae). Bulletin of the Museum of Comparative Zoology at Harvard College 103, 411-496.
Farke, A. A. 2008. Frontal sinuses and head-butting in goats: a finite element analysis. Journal of Experimental Biology 211, 3085-3094.
- . 2010. Evolution and functional morphology of the frontal sinuses in Bovidae (Mammalia: Artiodactyla), and implications for the evolution of cranial pneumaticity. Zoological Journal of the Linnean Society 159, 988-1014.
Hanney, P. W. 1975. Rodents: Their Lives and Habits. David & Charles, Newton Abbot.
Hershkovitz, P. 1955. On the cheek pouches of the tropical American paca, Agouti paca (Linn., 1766). SÃ¤ugetierkundliche Mitteilungen 3, 67-70.
Howell, A. B. 1940. Cheek pouches of the paca. Journal of Mammalogy 21, 361.
Kelemen, G. 1955. The nasal and paranasal cavities of the rabbit in experimental work. Archives of Otolaryngology 61, 497-512.
Koppe, T., Klauke, T., Lee, S. & Schumacher, G.-H. 2000. Growth pattern of the maxillary sinus in the miniature pig (Sus scrofa). Cells Tissues Organs 167, 58-67.
Nelson, T. W. & Shump, K. A. 1978. Cranial variation and size allometry in Agouti paca from Ecuador. Journal of Mammalogy 59, 387-394.
PÃ©rez, E. M. 1992. Agouti paca. Mammalian Species 404, 1-7.
Phillips, J. E., Ji, L., Rivelli, M. A., Chapman, R. W. & Corboz, M. R. 2009. Three-dimensional analysis of rodent paranasal sinus cavities from X-ray computed tomography (CT) scans. The Canadian Journal of Veterinary Research 73, 205-211.
Reznik, G. K. 1990. Comparative anatomy, physiology, and function of the upper respiratory tract. Environmental Health Perspectives 85, 171-176.
Ward, S. C. & Brown, B. 1986. The facial skeleton of Sivapithecus indicus. In Swindler, D. R. & Erwin, J. (eds) Comparative Primate Biology. New York, Alan R. Liss, volume 1, pp. 413-452.
Weidenreich F. 1941. The brain and its role in the phylogenetic transformation of the human skull. Transactions of the American Philosophical Society 31, 320-442.
Witmer, L. M. 1997. The evolution of the antorbital cavity of archosaurs: a study in soft-tissue reconstruction in the fossil record with an analysis of the function of pneumaticity. Journal of Vertebrate Paleontology 17 (1, Supplement), 1-73.
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There is a structure which sometimes occurs in human mandibulae, which looks very similar to the internal mandibular fenestra, the so-called Stafne-cyst. On an x-ray image it looks like a cyst, but in fact it is only a pseudocyst without any pathological meaning, and yields often tissue of the Glandula submandibularis. However this structure is normally only unilaterlly present, and always below the Canalis mandibulae, and from the photo alone, I am not sure where the Nervus mentalis was in the mandibula of those fossil hyraxes. But possibly the internal mandibular fenestra was some kind of genetically fixed bilateral Stafne-Cyst.
The paca occurs in Cuba?!
I had no idea that the paca was also found on Cuba and the Lesser Antilles... its presence is due to human introduction, right? And same goes for most if not all of the island populations of agoutis on Cuba and Lesser Antilles. After all, these islands are supposed to be the haunt of the hutias.
(The IUCN Red List mentions the paca as being introduced to Cuba and... Algeria??! Maybe it got mixed up with the European rabbit Oryctolagus cuniculus)
Hi Darren, very interesting as always. Thanks for those paca skulls ... I've heard of that enlarged bone structure in the cheeks but these are the first good pictures I see of it.
I would LOVE an article about fossil hyraxes! I live in South Africa and see hyraxes a lot but I know very little about their evolutionary history.
The paca does occur in Cuba, though I'm not sure about it living in the Lesser Antilles.
That's right - pacas and agoutis are, of course, not native to Cuba. According to Borroto-PÃ¡ez (2009), they were introduced there from Mexico in the 1930ies; nowadays, they appear to be fairly well established at least in the western part of the island.
Borroto-PÃ¡ez, R. 2009. Invasive mammals in Cuba: an overview. Biological Invasions 11, 2279-2290.
I took the presence of the paca on the Lesser Antilles and Cuba from PÃ©rez (1992). To quote that author: "[Its] distribution includes Central America, the Lesser Antilles, Cuba (Varona, 1974), Colombia, Venezuela, Guianas, Ecuador, Peru, Bolivia, Paraguay and Argentina" (p. 2). This certainly implies that the animal is found on both Cuba and somewhere in the Lesser Antilles, though PÃ©rez doesn't say exactly where. It seems at the moment that people have moved pacas around quite a bit, presumably for their value as a food item.
Refs - -
PÃ©rez, E. M. 1992. Agouti paca. Mammalian Species 404, 1-7.
Varona, L. S. 1974. Catalogo de los mamiferos vivientes y extinguidos de las Antillas. Academia de Ciencias de Cuba.