Monday, 19 January 2015

Quantifying pneumaticity

A few months ago I started talking about skeletal pneumaticity in pterosaurs and planned on following it up with this post on quantifying pneumaticity, but a few things got in the way, so here it is.

How do you quantify pneumaticity?

Most often in bones, and especially in the fossil record, pneumaticity is discussed on the basis of presence or absence, and documenting the location of pneumatic foramina. This is primarily done for taxonomic purposes, as the location of these foramina can be characteristic of the taxonomic group the pterosaur belongs in. Pat O'Connor started to look at quantifying pneumaticity in one way using what he called the Pneumaticity Index (PI), which was a way of comparing the number of pneumatic elements in different birds [1]. A PI of 1.00 indicates all potentially pneumatic elements of the bird's post cranial skeleton are pneumatised, and smaller numbers indicate fewer pneumatic elements. This allows for comparison of the number of pneumatised elements between taxa, but not the degree of pneumaticity between bones.

Air Space Proportion

Matt Wedel, a sauropod palaeontologist, does a lot of work on the pneumaticity in sauropod vertebrae and realised that there was no way of quantifying pneumaticity within a single bone. He proposed using the Air Space Proportion (ASP), a ratio of the cross-sectional area of the air-filled section compared to the total cross-sectional area [2]. From 0-1, an ASP closer to 1 indicates a bone that is mainly full of air, vs. closer to 0, which is mainly bone. He started doing this on sauropod vertebrae and comparing the ASP between different sauropods and different vertebrae. While Matt came up with the idea of ASP, several people in the past of used the K value (the ratio of the internal to outer diameter) to compare the bone thickness of different bird and pterosaur bones. In a tubular bone, ASP is roughly equal to K^2.

In 2012, Matt approached me after seeing a talk I gave on my MSc research on pterosaur bone mass and suggested that I look at ASP in pterosaurs using my CT scans. He had always been curious as to if it would change throughout the bone and if the cross-section of the bone would significantly change the ASP. I thought this was a good idea, and that it would also allow me to look at ASP in pterosaurs and see how it related to other animals.

Looking at CT scan slices at set intervals throughout several pterosaur bones, we found some interesting results. It turns out that ASP actually varies quite a lot throughout a bone, at least it does in pterosaur wing bones [3]. In fact, all pterosaur wing phalanges had high ASP values  at the ends of the bone (e.g. approximately 0.85 in NHMUK PV OR39411) and lower values in the shaft (e.g. approximately 0.71).
From Martin and Palmer [3]
This was not initially expected. Pterosaur bones are full of spongy trabecular bone in the ends, while the shafts are almost completely hollow with just cortical bone along the outsides, so at first glance you would expect less air in the ends. However, the ends are also expanded in diameter, the cortical thickness is extremely low and trabeculae are very small in thickness, while the shaft has higher cortical thickness, but a smaller diameter. The result of this is an increase in both air and bone at the ends, but proportionally more air. As most long bones in the fossil record are found broken in the shaft, it means that any estimates of pneumaticity of long bones using a shaft cross-section may be underestimating the values. It also means that single cross-sections of bones may not be accurately showing how pneumatic the bones are.

How do pterosaurs compare to other animals?

First of all, it's important to remember exactly what these numbers mean. If an ASP is 0.9, that means it 90% air, vs. an ASP of 0.1, or 10% air. Of the bones we looked at, they had average ASP values of 0.68-0.83, but the complete range was 0.56-0.88.
ASP values of pterosaur wing bones from Martin and Palmer [3]
This is significantly higher than the same bone and most others in a juvenile azhdarchid, similar to Pteranodon (calculated from K), and much higher than an unknown bone from a dsungaripteroid (from K). It's also higher than most birds, although these are all calculated from K values rather than ASPs. Finally, they are generally higher than sauropod vertebrae ASP, but there are some sauropods that have higher ASP values. This means that pterosaurs are among, if not THE, most pneumatic animals in the world.
ASP values of pterosaurs, birds, and sauropods from the literature in Martin and Palmer [2]
There is still a lot of work to be done on this. First of all, more bones need to be looked at as our study only included wing bones, and mostly wing phalanges. Next, more pterosaur taxa need to be studied. This is already underway and is showing some interesting results, so stay tuned! Finally, more groups need to be looked at, particularly birds. Do birds show the same patterns? Again, something that I am looking at! This work will be continued in my PhD in more detail, so more will come.

If you're interested, you can read more about this paper over at SVPOW where Matt Wedel summarised it. Also, the paper is published open access in Plos One, and can be read here.

Thanks to everyone who helped me along the way, especially Matt Wedel and Colin Palmer, and also Davide Foffa, Lorna Steel, Lauren Howard, Dave Martill, the staff at Muvis, Mike Habib, the Smithsonian staff, and Gareth Dyke. And of course to my other half Josh Silverstone :) 

References:
[1] O'connor 2004. Pulmonary pneumaticity in the postcranial skeleton of extant Aves: a case study examining Anseriformes. Journal of Morphology 261: 141-161.
[2] Wedel MJ (2005) Postcranial skeletal pneumaticity in sauropods and its implications for mass estimates. In: Curry Rogers K, Wilson J, editors. The sauropods: evolution and paleobiology. Berkeley: University of California Press. 201–228
[3] Martin EG, Palmer C (2014) Air space proportion in pterosaur limb bones using computed tomography and its implications for previous estimates for pneumaticity. Plos One 9: e97159.

Monday, 8 December 2014

2014 - The year of pterosaur bonebeds

This post is part of the Science Borealis Blog Carnival discussing the most important science news in our fields. As a pterosaur palaeontologist, I've chosen to talk about pterosaur bonebeds - enjoy!

Pterosaurs (extinct flying reptiles that lived alongside the dinosaurs) are rare in the fossil record. Most species are known from a few specimens, and rarely found with more than one individual in one place. This is primarily because pterosaur bones are extremely fragile due to the thin-walled hollow nature of the bones caused by the respiratory system and pneumaticity. This is why it is so rare to find them together and why this year has been so important for pterosaur-related news. There was not one, but two pterosaur bonebeds reported in 2014: one in China, and one in Brazil.

What is a bonebed?


Pachyrhinosaurus bonebed in Alberta. The left image shows just how many people
 can work in one area as there are so many bones. The right shows how many
bones are found in one section. This bonebed is one of the highest concentrated
bonebeds in the world.
The first thing to understand why this is so important in palaeontology is to learn what a bonebed is. A bonebed is a geological deposit with many bones found throughout it. They are important in palaeontology for many reasons. First of all, and probably fairly obviously, they provide us with many specimens to study. Large accumulations of bones can provide us with a lot of information that single skeletons can't. If the bonebed is full of several species, it can be caused by something like quick sand that many different animals can get trapped in. If there is only one species, that can tell us that the animals were living in some kind of group that died in some kind of catastrophic event. For example, ceratopsian (horned dinosaur) bonebeds are common in North America, including PachyrhinosaurusCentrosaurus, and Styracosaurus. These have commonly been interpreted as herds of ceratopsians that have been caught in something like a flooded river. In addition to understanding things like social behaviour, it can also help us understand ontogenetic (developmental/age-related) changes and sexual differences. As herds consist of males and females, as well as all ages, these herd-accumulated bonebeds can be very important in understanding the biology of these extinct animals. 


As mentioned above, accumulations like this are extremely rare in pterosaurs. Before this year, only one had been found. This was from the Lower Cretaceous of Argentina, at a locality referred to as "Loma del Pterodaustro", named for the hundreds of specimens of the bizarre filter-feeding pterosaur Pterodaustro [1]. This locality provided information for this pterosaur from egg to adult. Unfortunately, the majority of this material is two-dimensionally flattened. Until this year, that was the only major pterosaur accumulation known.


Hamipterus - The Chinese Bonebed 

Large block showing several Hamipterus bones including
3 partial skulls (labeled sk). Scale bar = 10cm. Image from
Wang et al. [2]
The first pterosaur bonebed of 2014 came out in June describing a new species, Hamipterus tianshanensis [2]. This find was exciting for many reasons: it included specimens of all ages, several 3D preserved eggs, and evidence of sexual dimorphism. It represents an Early Cretaceous (100-120 million years ago) stream or lake deposit potentially formed by a storm, catastrophically killing all the animals at once and preserving them together. About 40 individuals (meaning identifiable individuals, not just bone fragments) have been removed from the locality, but the authors suggest there may be hundreds, making this a massive deposit. 


Hamipterus was a pteranodontoid pterosaur with teeth, a bony crest on the pre maxilla (the front part of the rostrum), and a wingspan of about 3.5 m. This crest changes throughout ontogeny (over its lifetime) and appears to be sexually dimorphic. Throughout its ontogeny, the rostrum (snout) and premaxillary crest becoming more robust. Crests and features that have some kind of sexually selective function become more prominent as the animal reaches sexual maturity, which is why these features are generally larger and more robust in older individuals. In Hamipterus, the crest also appears to represent a sexually dimorphic feature, with two different crest morphologies present in similarly sized skulls. Skulls tentatively described as males were larger and thicker with more strongly curved anterior portions, while "female" skulls have shorter crests without an anteriorly curved portion. Several skulls of both morphs were found and sex was tentatively assigned, although more information is needed to confirm these assignments such as difference in pelvis shape or presence of medullary bone. Finally, the other exciting thing about this find is the presence of five eggs, which doubles the total number of pterosaur eggs found in the fossil record. Even more exciting is that these eggs, like the rest of the fossils, are preserved in three dimensions, unlike the previous pterosaur eggs that were flattened. The morphology of the eggs confirms previous studies that have suggested pterosaur eggs were soft-shelled eggs, more similar to some snakes and lizards than modern birds. 
Hamipterus skulls: A and E represent "females", while B, D, and F represent
"males". C shows the outline of both female (lighter grey with dark lines) and
male (darker with white lines curving forwards) premaxillary crests. Image
from Wang et al. [2]

The presence of so many individuals and eggs lead the authors to suggest this was a nesting ground and that Hamipterus may have been gregarious, living (or at least nesting) in large flocks, much like some modern birds. 

This study was covered significantly in the media including the Guardian, Reuters, and CBC.


Caiuajara - The Brazilian Counterpart

After the announcement of Hamipterus, pterosaur specialists and other palaeontologists were very excited. Imagine our excitement when just 2 months later, in August, the massive Caiuajara (pronounced Kai-u-a-har-a, I believe) bonebed from Brazil was described [3]. This bonebed from the Late Cretaceous was found in the southwest part of Brazil, where pterosaur fossils were previously unknown. While Brazil has a lot of wonderfully preserved pterosaurs, they all come from the northeastern region. While the Hamipterus bonebed was from a water-logged area, Caiuajara dobruskii was found in a desert-lake deposit, the first time a pterosaur has been found in this kind of environment. 47 individuals have so far been identified from hundreds of bones, and there may be as many as a few hundred individuals present.
Block showing hundreds of Caiuajara bones with at least 14 partial skulls. Image from Manzig et al. [3]
Caiuajara was a tapejarid pterosaur, with a full grown wingspan of approximately 2.4 m, and was characterised by a ventrally deflected (curved down) front portion of the upper jaw, toothless jaws, and another premaxillary crest starting at the front of the rostrum and continuing towards the back of the skull. Tapejarid pterosaurs are known for their toothless jaws, thought to be used to eat fruit, and their large dorsally directed cranial crests. In the Caiuajara bonebed, skulls are present from all sizes, showing the ontogenetic trend in crest growth. It shows that as the animal got larger and reached sexual maturity, the size and shape of the crest changed, much like that seen in Hamipterus, only the crest of Caiuajara is much larger. Furthermore, the entire skeleton is known, even if bones cannot be attributed to specific individuals. 

The images above show the ontogenetic variation in Caiuajara dobruskii. The left image shows various skulls from the youngest and smallest (top left) all the way to the largest, oldest individual (bottom right). The image on the right is a very nice schematic drawing showing how the skull changes from the younger individuals (white) up to the oldest (dark red). Images are from Manzig et al. [3].

Like the Hamipterus bonebed, most of these fossils were preserved in 3D, allowing the scientists to understand information such as the actual morphology of the bones, and potentially the internal structure. The geologic bed has additional interesting information. 3-4 different accumulations were found, thought to be formed by separate events. This large accumulation, and the fact that there are a few independent events further supports the thought that some pterosaurs may have had some kind of gregarious behaviour, living together in a colony-like manner around an internal lake in the desert, rather than a fluke one-time occurrence. Furthermore, most pterosaur fossils are found are found in marine deposits, with few from inland terrestrial deposits, let alone deserts (only one found previously). This find has increased our understanding of pterosaur behaviour by adding another piece of evidence to the diversity of pterosaurs. They aren't all big pterosaurs swimming over the oceans and catching fish like is often portrayed.

This find also had a significant amount of media coverage including CBC and National Geographic

These two bonebeds have provided us with a lot of new information about pterosaurs. First of all, it suggests that pterosaurs may have been gregarious, living and nesting in groups (flocks?), much like modern birds. Whether or not this is a behaviour that they exhibit all year round, or just when nesting or mating is still unknown. While other pterosaurs are known from several ages and sizes, such as Pteranodon, Pterodactylus and Rhamphorhynchus, the ages and species are frequently debated, so ontogenetic sequences can be difficult. However, Caiuajara and Hamipterus provide us with 2 examples of true growth series from different, distantly related pterosaurs, which shows how they grew and how their biology changed over time. Furthermore, these bonebeds are so concentrated that they will continue to unearth a wealth of information about these pterosaurs. The next few years is going to be exciting to see what we learn from both of these!

And another bonus? Both of these studies are open access, so anyone can read about them. Check out the links below.


References:
1. Chiappe LM, Rivarola D, Romero E, Davila S, Codorniu L (1998) Recent Advances in the Paleontology of the Lower Cretaceous Lagarcito Formation (Parque Nacional Sierra de Las Quijadas, San Luis, Argentina). In Lower and Middle Cretaceous Terrestrial Ecosystems, New Mexico: Museum of Natural History and Science Bulletin Lucas SG, Kirkland JI, Estep JW, editors. 14: 187–192.

2. Wang X, Kellner AWA, Jiang S, Wang Q, Ma Y, Paidoula Y, Cheng X, Rodrigues T, Meng X, Zhang J, Li N, Zhou Z (2014) Sexually dimorphic tridimensionally preserved pterosaurs and their eggs from China. Current Biology 24: 1323-1330. (open access)
3. Manzig PC, Kellner AWA, Weinschütz LC, Fragoso CE, Vega CS, Guimarães GB, Godoy LC, Liccardo A, Ricetti JHZ, de Moura CC (2014) Discovery of a rare pterosaur bone bed in a Cretaceous desert with insights on ontogeny and behavior of flying reptiles. PLoS ONE 9: e100005. (open access)

Thursday, 20 November 2014

Pterosaurs of Stuttgart and Munich

As part of my PhD, and with the help of the Geological Association of London, I've been fortunate enough to go on several research trips to some museums in Germany including Tübingen, Karlsruhe, Stuttgart, and Munich. Stuttgart and Munich in particular have excellent pterosaur collections, including many historically significant specimens.

Stuttgart

The Staatsliches Museum für Naturkunde in Stuttgart (SMNS) is a large museum that houses one of the state collections of Baden-Württemberg (the other one being in Karlsruhe). The museum has a significant collection of material from the area, as well as some excellent material on display, but I'm only going to talk about some interesting pterosaur material. 

Campylognathoides
Campylognathoides zitteli was first found in 1858, from the Early Jurassic deposits of Württemberg. In 1893, a new specimen was discovered from the Holzmaden shale, and was named as a new genus and species, "Campylognathus zitteli", based on the specimen found below. It was later discovered that the genus was already in use for an insect, and so a new genus, Campylognathoides, was named in 1928.  
Type specimen SMNS 9787 of Campylognathoides zitteli
Austriadactylus
The type specimen of Austridactylus cristatus was found in the Alps of Austria, dating back to the Late Triassic. This is one of the earliest pterosaurs known so far as Triassic pterosaurs are extremely rare. They are also very poorly preserved, and Austriadactylus is a perfect example of this. Like many pterosaurs, it is completely crushed and incomplete, but some features can be seen. It has many primitive pterosaurian features including a long flexible tail (which lacks the stiffening rods seen in later pterosaurs) and heterodont teeth. 
Type specimen of Austridactylus cristatus SMNS 56342 

Line drawing of Austriadactylus cristatus from Dalla Vecchia et al. [1]
Miscellaneous
Also in the SMNS collections is some miscellaneous pterosaur material that shows some interesting features. Specifically, there are some 3D, beautifully preserved pterodactyloid fossils that show the internal structure of pterosaur bones, the delicate trabecular structure that existed in the heads, and the trabeculae that occur in the shafts.
Close ups of the internal structure of two pterosaur bones in the shaft (above) and head (below)

Munich

The Munich palaeontology collections exist in the Bayerisches Staatssammlung für Paläontologie ind Geologie (BSP), and are quite extensive, as shown by the large number of researchers there after the Society of Vertebrate Paleontology meeting in Berlin. It is especially great for pterosaurs, including numerous historically significant specimens, including the first ever pterosaur known to sciences, Pterodactylus antiquus. Unfortunately, that specimen is so valuable that it is kept out of prying eyes and is only accessible under specific permission, so I wasn't able to see it. However, that aside, there were many other significant specimens for me to see. 

 Aerodactylus
BSP AS V 29, type specimen of A. scolopaciceps
This genus has a complicated history. In 1860, a new species, "Pterodactylus scolopaciceps" was named by Meyer after being found in the Bavarian Solnhofen limestone from the Jurassic. This was later synonomised in 1883 with "P. kochi" which was thought to be a smaller species of Pterodactylus. However, over the years it has generally been agreed that "P. kochi" is just an ontogenetic stage of P. antiquus, meaning that they are just smaller, younger individuals. The original type specimen of "P. scolopaciceps" was more recently re-described as a new genus, Aerodactylus [2]. While all specimens of A. scolopaciceps are considered to be juvenile, it has been suggested there is enough of a difference to be a different genus.  
Beautifully preserved specimen of Aerodactylus
Close up of some details of the wing of Aerodactylus. Note the long slender pteroid bone, which is unique to pterosaurs
Germanodactylus
Germanodactylus cristatus was first described as a specimen of "P. kochi" by Pleininger in 1901 after being discovered in the Solnhofen lagerstätt, another Late Jurassic German pterosaur. It was then described as a new species of Pterodactylus, "P. cristatus". In 1964, a new genus Germanodactylus was named, and BSP 1892 IV 1 was named the type specimen of G. cristatus. The precise position of Germanodactylus within the Pterosauria has been debated, but it is definitely a pterodactyloid pterosaur. 
Type specimen of Germanodactylus cristatus, BSP 1892 IV 1
The Zittel Wing
By far, the most historically interesting specimen and biggest surprise for me came when I opened up a drawer and found the "Zittel Wing", a nearly complete Rhamphorhynchus wing. This wing was described by Alfred von Zittel in 1882. It was a significant find then, and to this day still represents one of, if not the best preserved wing membrane of a pterosaur. Nearly all the wing bones are complete, and the membrane is preserved from the tip of the wing finger (the elongated 4th finger) to underneath the humerus. It showed the width of the wing, as well as the actinofibrils, which are the strengthening fibres that provided the pterosaur wing with strength when they are overlain in criss-crossing layers. This was the first sign at how pterosaur wing membranes were formed.
The Zittel Wing
 3D ornithocheird wing bones!
For me, a highlight was looking at the 3D preserved specimens from the Early Cretaceous of Brazil. These were large pterosaurs, with wingspans of 5 m or so, and were part of the pterosaur revival of the 1970s to 1990s after being described in detail by Peter Wellnhofer. These bones are all very well preserved and have mainly been prepared out of the rock, meaning that you can pick them up, move them around, and really start to understand them. These were definitely the highlight for me!
Beautifully 3D preserved Santanadactylus spixi radius, ulna, and wing carpals.
Wing metacarpal with 3 other metacarpals from Santanadactylus pricei. Note the small pneumatic foramen (see previous post on pneumaticity for details) underneath the small finger metacarpals.
Those are my highlights from the natural history museums in Stuttgart and Munich. There were many more interesting specimens, and I could go on for ages about it, but I think I'll stop here!

References:
[1] Dalla Vecchia FM et al. 2002. A crested rhamphorhynchoid pterosaur from the Late Triassic of Austria. Journal of Vertebrate Paleontology 22: 196-199.
[2] Vidovic SU and Martill DM. 2014. Pterodactylus scolopaciceps Meyer, 1860 (Pterosauria, Pterodactyloidea) from the Upper Jurassic of Bavaria, Germany: the problem of cryptic pterosaur taxa in early ontogeny. PLoS ONE 9: e110646.

Tuesday, 11 November 2014

Pterosaur bone mass

The last post here was on pterosaur skeletal pneumaticity, and while I said I was going to continue this discussion in the next post, I'm going to take a side-road for a bit and talk about my first research paper, which has just come out! It's still related though, and ties in with these questions nicely.

Estimating pterosaur bone mass using CT scans

Summary of Martin and Palmer 2014 [1]

At the beginning of my MSc, my supervisor (Colin Palmer) and I wanted to look at estimating pterosaur bone mass using CT scans. Total mass of pterosaurs is a controversial topic, with different methods and authors coming up with very different results, which you can read about in a previous post (and this one) if you are interested. It is essential to accurately estimate mass in pterosaurs as they were the largest animals to ever fly, an mass is extremely important in flight. The key thing to know here is that one method for estimating pterosaur body mass relied on the relationship between skeletal mass and total mass in birds [2], and applied this relationship to pterosaurs by estimating skeletal mass geometrically (i.e. a long bone is a hollow cylinder) [3]. Colin was interested in using computed tomography (CT) scans to estimate bone mass, to see how different (if any) the mass would be using this method. I agreed that it would be an interesting project, and started on my MSc at the University of Bristol.

The basic principle was that by calculating the cross-sectional area of bone in several slices throughout the bone (approximately every 5-10 mm), bone volume (as in the actual volume of bony material) could be calculated through integration. Then, mass can be estimated by applying a density and multiplying by the volume. This was done for a number of bones, but we only published on 3 first wing phalanges (the first big finger bone in the wing, herein referred to as WP1). We were then able to compare the results directly to the previous method used by Witton [3] thanks to him kindly sharing his dataset with us (thanks again Mark!).
CT scans through a pterosaur wing bone showing the shaft (A,B) and proximal head (C,D) cross-sections. Top images show unmodified CT scans, bottom images show reconstructed cortical bone and removed matrix used for area calculations. Image from Martin and Palmer [1]
What we found was quite different from what we had expected. We generally assumed that the mass would be somewhat similar to what Witton found. However, we found that all three bones were about twice as heavy using this method as previous estimates, which made us wonder what that means for the rest of the skeleton.
Table indicating measurements from 3 WP1s including mass estimates. Note the differences between mass estimates in our method and in the previous method. From Martin and Palmer [1]
While there are differences between our method and Witton's original study, he could only do what was available to him, which for many reasons, did not include CT scans. However, he did suggest in his original paper that using CT scans would be another way to do this study and likely would be more accurate, so credit to Mark for that! It was a pragmatic method at the time, and well done using the materials available to him at that point.

So why is the mass so much more using the CT method? There are several possible explanations for this. First of all, the original method did not account for trabeculae, which did add 10-15% of mass in our study. Another explanation is that the cortical thickness used by Witton (which was calculated using a regression model derived by someone else) was consistently lower than what we found in the CT scans (see the table above), which also would affect the mass. And finally, one point that is related to the last one is that the original method did not account for the variation within the cortical thickness throughout the bone.

And what does this all mean? While this information, as well as some additional new data suggests that the wings of pterosaurs were heavier than previously estimated. This isn't really a big surprise when noted that some previous estimates suggest that the pectoral muscles (the muscles around the shoulder) in pterosaurs account for 30-40% of the total body mass [4]. While these muscles are mainly used for flight, they would also be the main muscles for take off if pterosaurs did take-off using their forelimbs to launch as has been suggested [5].

This study made us wonder what the rest of the skeleton would look like if we calculated it using CT scans, which has lead to my PhD project at the University of Southampton. The amount of bone tissue in the wing bones is related to both mass and pneumaticity, which are both subjects I am interested in, as they all related to the biomechanics and flight capabilities of pterosaurs. If anyone would like to see the paper and does not have access, let me know!

Next up, I'll talk about quantifying and comparing the amount of air (pneumaticity) found within the skeletons of pterosaurs, looking at different bones, and different pterosaurs, another paper that Colin and I have published on the topic.

Acknowledgements
Just wanted to say thanks to everyone that helped me with CT scans and along with this project that I am so happy is finally out! This includes: first and foremost thanks to Colin Palmer for putting up with me the last 2 years, and to Mark Witton for sharing lots of things along the way, and also Davide Foffa, Lorna Steel, Lauren Howard, Dave Martill, the staff at Muvis, Mike Habib, Emily Rayfield, and many more! I'm so happy to finally have this paper out :)
EDIT: Also, this should seem obvious, but I'm going to add it anyways. Many thanks goes out to my wonderful partner in crime Josh Silverstone for helping through the last 7 years (and especially the last 3), and for helping me with figures of course!

References
[1] Martin, EG and Palmer, C (2014) A novel method of estimating pterosaur skeletal mass using computed tomography scans. Journal of Vertebrate Paleontology 34: 1466-1469.
[2] Prange, HD et al. (1979) Scaling of skeletal mass to body mass in birds and mammals. American Naturalist 113:103–122.
[3] Witton, MP (2008) A new approach to determining pterosaur body mass and its implications for pterosaur flight. Zitteliana, Reihe B 28:143–158.
[4] Strang, KA (2009) Efficient flapping flight of pterosaurs. Ph.D. disserta- tion, Stanford University, Stanford, California, 295 pp.
[5] Habib, MB (2008) Comparative evidence for quadrupedal launch in pterosaurs. Zitteliana, Reihe B 28:159–166.

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.  

References
[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.

Tuesday, 16 September 2014

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.

Tuesday, 9 September 2014

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