Monday, 6 October 2014

Introduction to pterosaur skeletal pneumaticity

In my last post, I talked about the “lightweight” skeleton of birds, and a bit about the possible myth that birds evolved lightweight skeletons in order to fly. I discussed the fact that birds have light skeletons because of their respiratory system which invades and hollows out the bony tissue, filling many bones with air rather than marrow (especially the vertebral column, but also the appendicular skeleton in the wings).

As mentioned, this feature is unique to birds today, but was also found in their ancestral theropods, as well as in the necks of the large-bodied sauropods, and of course in pterosaurs. Pterosaur pneumaticity is something that has been discussed a fair bit in the literature as it is believed to be a key feature that allowed pterosaurs to reach their large sizes. While many animals of cranial pneumaticity (including humans – we have sinuses throughout our skulls that are full of air), the presence of pneumaticity in the postcranial skeleton is much more rare. For brevity, if I talk about pneumaticity here, I mean postcranial skeletal pneumaticity!

It appears that all pterosaurs had some aspect of postcranial skeletal pneumaticity, with evidence of it in the axial skeleton of the Triassic pterosaurs Raeticodactylus and Eudimorphodon [1]. This can be identified by the presence of pneumatic foramina, small holes that go into the bone cavity where the respiratory system would enter the bone through structures called diverticulae. To identify these as pneumatic features rather than nutrient foramina, we can look at modern bird bones and see how these features differ. In the earliest pterosaurs, only the axial skeleton can explicitly be described as pneumatic: several pneumatic foramina have been identified in the cervical vertebrae, ribs and dorsal vertebrae.
Pneumatic foramina (PF) in a modern swan humerus (A and B), and a goose cervical vertebra. From O'Connor [2]
Pneumatic openings in the dorsal vertebrae of Dimorphodon [1]

Pneumaticity seems to be found in all groups of pterosaurs. Thus far, no specimen unequivocally lacks pneumatisation, and those that are thought to lack it are more likely crushed or destroyed [1]. As we move further up into the derived pterosaurs, the pterodactyloids, pneumaticity becomes much more interesting in my opinion. While the early pterosaurs had only cranial and axial pneumaticity, most pterodactyloids have some degree of appendicular pneumaticity in their wings as well.

Scapulacoracoid of Montanazhdarcho showing
 a pneumatic foramen (pf). From McGowen et al. [3].
Many of the wing elements were pneumatic. The scapulacoracoid (the bone that articulates with the vertebral column and the humerus at the glenoid fossa) in many species is pneumatic (e.g. Montanazhdarcho, Anhanguera, Pteranodon). Pterodactyloid humeri and first wing phalanges (the biggest bone in the wing of a pterosaur) show the highest degree of pneumaticity. The number and location of pneumatic foramina can differentiate different groups, but in general, pterodactyloids have foramina on the proximal end of their humeri. For example, these have been found in Tapejara [4], Montanazhdarco [3], Pteranodon [5], Anhanguera [6], etc. The air sacs would enter the humerus proximally near the glenoid, and leave the humerus at the distal end where the humerus articulates with the radius and ulna.
Tapejara humerus showing pneumatic foramina on the proximal end. From Eck et al. [4]
Distal end of a Pteranodon humerus with pneumatic foramen. From Bennett [5]

While there isn’t as much documented evidence for pneumatisation in the radius and ulna, it has been reported in the ulna and radius of Pteranodon [5]. There is also significant pneumatisation of the carpals (the bones that articulate between the metacarpals and phalanges to make the pterosaur wrist). This is seen in the proximal carpals (e.g. Montanazhdarcho) and fused syncarpals and preaxial carpals of Pteranodon. Even small bones like the pteroid have pneumatic foramina in Pteranodon [5]. This pattern of extensive pneumatisation in the wings of Pteranodon continues, with nearly every element showing some kind of evidence of pneumatisation.
Pneumatic foramina in the proximal carpal of
Montanazhdarcho. From McGowen et al. [3]

Finally, the wing finger of pterodactyloid pterosaurs shows extensive pneumatisation, especially the first phalanx. In Pteranodon, the pneumatisation occurs all the way down to the 4th wing phalanx. The 1st wing phalanx is also pneumatic in Tapejara, Anhanguera and more.
PFO - Pneumatic foramen in the first wing phalanx of
Anhanguera. From Kellner and Tomida [6]
This should have shown you that there is evidence of skeletal pneumaticity throughout the axial skeleton and the wings of pterosaurs, meaning that air sacs existed all the way down the wing in at least pterodactyloid pterosaurs. This indicates that they had a very efficient respiratory system which allowed for respiration all the way down the wings. This is more than what is found in modern birds, which are primarily pneumatic only in the axial skeleton and a few elements in the wings. Very few birds have distal pneumatic elements [2].
Pneumatic openings in the wing phalanges of Pteranodon.From Bennett [5]
Pulmonary air sac system in Anhanguera: lungs (orange),
cervical (green), abdominal (blue), abdominal (grey) and
wing diverticular system (light blue). From Claessens et al. [7]
Detailed studies of the pneumatic system of pterosaurs has suggested that number of different pulmonary air sacs existed. It is thought that derived pterosaurs had lungs as well as cervical, abdominal, and thoracic air sacs. They also had an air sac or diverticular system that went into their wings. 

While we've been talking about pterosaurs that show pneumaticity, there are also some that have very little. Dsungaripterids, for example, are quite derived pterodactyloids, but they have virtually no post cranial skeletal pneumaticity. In fact, they have extremely thick-walled bones. This makes them a bit strange, but this is a topic for the future!

Pneumaticity can also be quantified using Air Space Proportion (ASP). Pterosaurs have varying degrees of pneumaticity within the bones with relation to the size of the air sacs, which I will talk about in the next post.  

[1] Butler et al. 2009. Postcranial skeletal pneumaticity and air-sacs in the earliest pterosaurs. Biology Letters 5: 557-560.
[2] O'connor 2004. Pulmonary pneumaticity in the postcranial skeleton of extant Aves: a case study examining Anseriformes. Journal of Morphology 261: 141-161.
[3] McGowen et al. 2002. Description of Montanazhdarcho minor, an azhdarchid pterosaur from the Two Medicine Formation (Campanian) of Montana. PaleoBios 22: 1-9.
[4] Eck et al. 2011. On the osteology of Tapejara wellnhoferi KELLNER 1989 and the first occurrence of a multiple specimen assemblage from the Santana Formation, Araripe Basin, NE-Brazil. Swiss Journal of Palaeontology 130: 277-296.
[5] Bennett 2001. The osteology and functional morphology of the Late Cretaceous pterosaur Pteranodon. Palaeontographica Abteilung A 260:1-112.
[6] Kellner and Tomida 2000. Description of a new species of Anhangueridae (Pterodactyloidea) with comments on the pterosaur fauna from the Santana Formation (Aptian-Albian), northeastern Brazil. National Science Museum Monographs 17: ix-137.