The evolution of the "lightweight" skeleton of birds

We often read in the literature, or hear it in popular science shows that birds are able to fly because of their lightweight skeleton, but is this really true?

There are several aspects surrounding this issue that I am going to try to discuss. I'll talk about where the idea of the lightweight skeleton comes from, whether or not it actually is the case, and whether this feature truly evolved to allow them to fly.

First of all, where does the idea of a lightweight skeleton in birds come from? This comes from the fact that many bird bones are hollow. Unlike mammal bones which have generally thick walled bones filled with marrow, bird bones are commonly filled with air. This is related to their breathing system and the intake of oxygen. In mammals, this is done primarily in the lungs, but also the trachea, bronchi, and diaphragm. Birds, however, have very different respiratory systems. They have air sacs in addition to lungs which is significantly more efficient than the typical mammalian system. These air sacs act in a manner similar to bellows which allow for air to be pushed through uni-directionally. This allows for consistent movement of the oxygenated air in one direction, which prevents the mixture of oxygenated and de-oxygenated air. Another unique feature related to the avian respiratory system is that the air sacs have diverticulae, finger-like projections that invade/hollow out the bones. This commonly occurs in the arm/wing bones of birds, and occurs at varying degrees of pneumatisation (air within the bones) throughout the wing [1].

From O'Connor [1]

O'Connor [1] found that the pneumaticity index (the number of elements pneumatised in the skeleton) varies throughout birds with heavier birds such as swans and geese having higher degrees of pneumaticity. If heavier flying birds have more pneumatic skeletons, then it stands to reason that they need pneumaticity to lighten the bones, right?

Well maybe... but there's much more to this topic than originally thought. A few studies have suggested that birds don't have that light of skeletons after all. First, Prange et al. [2] compared the dried skeletal mass of birds and mammals to their body mass and found that the relationships were remarkably similar in these phylogenetically distant groups. It was always assumed that the skeleton of birds was lighter than those of similarly sized mammals, but this seems to suggest that bird skeletons are just as heavy as mammal bones for a similar size.


Left (top), the body mass - skeletal mass relationship found in birds, compared to the same relationship in mammals (left bottom). The regression was found to be very similar in both. From Prange et al. [2]

Now I've spent a lot of time looking at this relationship and discussing it with people and I always thought there something a bit off with the conclusions, but never could fully put my finger on it. However, Matt Wedel (a sauropod palaeontologist and expert on pneumaticity) very correctly pointed out that by weighing the dry skeletal mass of the mammals, the authors had essentially artificially pneumatised the mammal bones. While the actual bone     itself may not be heavier in mammals, it most certainly would be in a living animal when the bone would be filled with marrow, unlike the hollow air-filled bird bones. This means that the relationship may not be that shocking after all when compared with mammals. Interestingly enough, when marrow is accounted for, small rodents appear to have similar soft tissue mass - skeletal mass proportions to birds, while bats have a heavier skeleton for a given amount of soft tissue [3].

The graph to the right shows soft tissue mass - skeletal mass relationships in passerine birds (black squares), and rodents (grey diamonds) and bats (white circles) which have had 15% of the dried skeletal mass added to it to account for marrow. From Dumont [3]. 

More interestingly, Dumont [3] found that the actual bone density in birds and bats was higher than those found in the similarly sized rodents. While the bony material is less, the density appears to be slightly higher.

But how do density and pneumaticity affect the bone? Here is where I believe this all comes together. Both density and pneumaticity have the same effect as both the pneumaticity and density increase, so does the bone's stiffness and strength. Bone density is proportional to stiffness and strength, and the shape affects stiffness. Hollow bones follow the same principles as a an I-beam. If you look at any construction site, you'll see that the beams used for major load bearing parts are I-shaped (that's why they're called I-beams). This is because bending results in high stress in the areas located furthest from the neutral axis. Material must be concentrated along these areas of high stress (the horizontal portions of the I), whereas less material is needed along the neutral axis (the central portion between the two horizontal axes). This is the same principle seen in hollow bones. The neutral axis is the central hollow shaft of the bone, where little stress occurs, whereas the bone is concentrated towards the outside, where the stresses occur. A perfectly circular hollow cylinder will be stiff in all directions, unlike an I-beam which is easier to bend one way than the other. However, the details of the direction of stiffness in bones is an entirely too complicated topic for now, and I will likely discuss later in a different post.


Right: image from Dumont [3] showing how density, and the shape of the bone relate to stiffness and strength.

For now, the important thing is this: birds have hollow bones which make them more stiff.

Now the title of this post is the evolution of the lightweight skeleton of birds, and I haven't talked at all about evolution yet. So where does evolution come in, you might ask? Well I think, and I'm not alone in thinking this, that the hollow pneumatic skeleton of birds (and in fact pterosaurs, the extinct flying reptiles I study) evolved not purely as a weight-decreasing method, but likely in a more complicated intertwined way of increasing strength, decreasing weight, and improving the respiratory system while flying. This is certainly not a novel idea, but it's about time this idea of the hollow bird skeleton evolving purely as a means to decrease mass be put to rest. I've seen it several times on "science" shows, and it's brought up constantly in the media. It's not all about mass reduction, but likely a complicated number of things that affect each other.

In the future, I'll talk a bit about the pneumaticity in pterosaurs, as that's part of my PhD so look forward to that!

References:
1. O'Connor, P. M. 2004. Pulmonary pneumaticity in the postcranial skeleton of extant Aves: a case study examining Anseriformes. Journal of Morphology 261: 141-161.
2. Prange, H. D., et al. 1979. Scaling of skeletal mass to body mass in birds and mammals. The American Naturalist 113: 103-122.
3. Dumont, E. R. 2010. Bone density and the lightweight skeleton of birds. Proceedings of the Royal Society B 277: 2193-2198.

North American Summer

As I mentioned previously, my summer was billed to be a pretty busy time, and indeed it was. I am now back in the UK, and back at work, but I'll talk a bit about my trip to North America looking at pterosaurs and digging for dinosaurs.

My trip to North America started out in Los Angeles, where I spent 4 days working at the LA County Museum of Natural History (LACM) with one of my supervisors, Mike Habib. I had a great week looking through material, mainly of Pteranodon, but also some casts of Pterodaustro, and a Nyctosaurus. The museum has a decent amount of material, including part of a very large skull which is on display, and also a few partial or nearly complete wings, which I really enjoyed. I also was fortunate to have arrived just after they had prepared a new specimen (I say new, but they actually received it in the '60s, but it was only recently opened up and prepared), which was very exciting. It was a really cool specimen, but I am not sure if I'm allowed to talk about it too much yet, so maybe later. We spent a lot of time looking at the wings for evidence of pneumaticity, which is one of my interests as you will know if you've read my previous posts. Unfortunately, as many of you may know, Pteranodon and Nyctosaurus are both almost completely flattened, which means that finding pneumatic foramina can be extremely difficult.

Pteranodon display at the LACM. Note the absolutely massive partial skull on the bottom right.

I also got to go to the Page Museum where the La Brea tar pits are, and got to go behind the barriers and see some material actually being excavated which was pretty cool. Probably my favourite part of that museum was looking at the birds, particularly the teratorns, that have come out of the tar pits. Standing there for some time while Mike pointed out features like pneumatic foramina, the tank-like nature of the teratorns, and other cool things was a big highlight for me.

Not a great picture, but here's a complete skeleton of a Teratornis at the Page Museum. I was amazed by the tank-like stature of it compared to more typical gracile birds.

The best part of the summer for me was spent doing 2 weeks of field work in Alberta, Canada, near Grande Prairie, where I got to work on a dig with Phil Currie's lab, in conjunction with the 'soon-to-be-open' Philip J. Currie Dinosaur Museum. We were working mainly at the Pipestone Creek bone bed, which is an almost completely monotaxic (one group of animals) Pachyrhinosaurus bone bed located near the town of Wembley. This site is 73 million years old, and may represent the most abundant bone bed from the Late Cretaceous (or one of the most fossiliferous bone beds anywhere!), with between 30-100 bones found per square metre! While only a small portion has been excavated to date, it's estimated that the bone bed takes up over two football (American football) fields in size. It's likely that over 1000 Pachyrhinosaurus (a ceratopsian dinosaur distantly related to Triceratops) died here, possibly in a flood. While over 99% of the bones found here are Pachyrhinosaurus, there are tyrannosaur teeth, and very rarely some theropod bones.

The area of the bone bed we exposed this summer was found underneath the tarp, which we laid down each night to keep it dry. You can see the massive hill behind that we had to climb with our buckets of matrix (dirt/rock) after uncovering the fossils.

Palaeontologists and volunteers hard at work uncovering Pachyrhinosaurus fossils.

The bones found here are all disarticulated and jumbled up, rather than nicely articulated, complete skeletons. This indicates that the skeletons were broken apart before buried and fossilised. The animals were likely scavenged by large and small predators alike as their bodies rotted and the carcasses lay exposed after dying after the flood. The large number of shed tyrannosaur teeth indicates this, as tyrannosaurs like Albertosaurus lost and replaced their teeth constantly, like modern sharks.

This site was initially excavated by the Royal Tyrrell Museum of Palaeontology in the 80s when Phil Currie was still working there after being told about the site in the 70s. After moving to the University of Alberta, he realised that the remains represented a new species of Pachyrhinosaurus, and named it Pachyrhinosaurus lakustai, after the science teacher (Al Lakusta) that found the site. Dr. Currie and the U of A team have continued to work at this site each summer. Now that a permanent palaeontology museum with palaeontologists like Matthew Vavrek has started up in the area, the U of A team will likely scaled down their work there and let the new museum take over. While it has been worked on for many years, there is still lots of new information coming out of the bone bed, and lots to be learned!

Some Pachyrhinosaurus fossils as they were being uncovered. The large top one near the feet is a fairly complete rib that continued to go underneath several other bones which can barely be made out.

The grid square - an important palaeontological tool. This allows for all bones found to be mapped so the orientation can be analysed later. This allows us to better understand patterns in orientation related to things like palaeo-river flow.

I was also able to spend some time at another bone bed that is found along the Wapiti River. This site is much smaller, and located on the side of a cliff/steep hill, which poses some interesting problems with access and specimen collection. The material found here is interesting though because while it is Pachyrhinosaurus, it's unclear exactly what species it is, since the material is found in extremely hard and difficult to prepare iron nodules. This makes it challenging to figure out exactly what is going on, as it may not represent the same time period as the Pipestone Creek bone bed.

The Wapiti River bone bed - what a wonderful view!

Another fun thing about being there when I was, was it was the official ribbon cutting ceremony of the Philip J. Currie Dinosaur Museum, named for my old supervisor that I was doing field work. This meant that we were host to a number of celebrities over the final week, including Dan Aykroyd and family, Fran Drescher, and the Canadian Tenors. We also got to go to the Dinosaur Ball, which is an annual event to raise money for the museum.

Some of us and Dan Aykroyd! I'm on the right